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Innate Immune Responses to Tuberculosis

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  • Authors: Jeffrey S. Schorey1, Larry S. Schlesinger2
  • Editors: William R. Jacobs Jr.3, Helen McShane4, Valerie Mizrahi5, Ian M. Orme6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biological Sciences, Eck Institute for Global Health, Center for Rare and Neglected Diseases, University of Notre Dame, Notre Dame, IN 46556; 2: Department of Microbial Infection and Immunity, Center for Microbial Interface Biology, The Ohio State University, Columbus, OH 43210; 3: Howard Hughes Medical Institute, Albert Einstein School of Medicine, Bronx, NY 10461; 4: University of Oxford, Oxford OX3 7DQ, United Kingdom; 5: University of Cape Town, Rondebosch 7701, South Africa; 6: Colorado State University, Fort Collins, CO 80523
  • Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0010-2016
  • Received 24 January 2016 Accepted 04 February 2016 Published 09 December 2016
  • Larry S. Schlesinger, larry.schlesinger@osumc.edu
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  • Abstract:

    Tuberculosis remains one of the greatest threats to human health. The causative bacterium, , is acquired by the respiratory route. It is exquisitely adapted to humans and is a prototypic intracellular pathogen of macrophages, with alveolar macrophages being the primary conduit of infection and disease. However, bacilli interact with and are affected by several soluble and cellular components of the innate immune system which dictate the outcome of primary infection, most commonly a latently infected healthy human host, in whom the bacteria are held in check by the host immune response within the confines of tissue granuloma, the host histopathologic hallmark. Such individuals can develop active TB later in life with impairment in the immune system. In contrast, in a minority of infected individuals, the early host immune response fails to control bacterial growth, and progressive granulomatous disease develops, facilitating spread of the bacilli via infectious aerosols. The molecular details of the -host innate immune system interaction continue to be elucidated, particularly those occurring within the lung. However, it is clear that a number of complex processes are involved at the different stages of infection that may benefit either the bacterium or the host. In this article, we describe a contemporary view of the molecular events underlying the interaction between and a variety of cellular and soluble components and processes of the innate immune system.

  • Citation: Schorey J, Schlesinger L. 2016. Innate Immune Responses to Tuberculosis. Microbiol Spectrum 4(6):TBTB2-0010-2016. doi:10.1128/microbiolspec.TBTB2-0010-2016.

Key Concept Ranking

Macrophage Inflammatory Protein 1 alpha
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References

1. WHO. 2015. Global tuberculosis report 2015, 20th ed. http://www.who.int/tb/publications/global_report/en/. [PubMed]
2. Hasenberg M, Stegemann-Koniszewski S, Gunzer M. 2013. Cellular immune reactions in the lung. Immunol Rev 251:189–214 http://dx.doi.org/10.1111/imr.12020. [PubMed]
3. Weibel ER. 2009. What makes a good lung? Swiss Med Wkly 139:375–386. [PubMed]
4. Burri PH. 2011. Development and growth of the human lung, p 1–46. In Reich M (ed), Comprehensive Physiology, Supplement 10. Handbook of Physiology: The Respiratory System, Circulation, and Nonrespiratory Functions, 10th ed. John Wiley and Sons Hoboken, NJ.
5. Hartung GH, Myhre LG, Nunneley SA. 1980. Physiological effects of cold air inhalation during exercise. Aviat Space Environ Med 51:591–594. [PubMed]
6. Ryu J-H, Kim C-H, Yoon J-H. 2010. Innate immune responses of the airway epithelium. Mol Cells 30:173–183 http://dx.doi.org/10.1007/s10059-010-0146-4. [PubMed]
7. Whitsett JA, Alenghat T. 2015. Respiratory epithelial cells orchestrate pulmonary innate immunity. Nat Immunol 16:27–35 http://dx.doi.org/10.1038/ni.3045. [PubMed]
8. Bastacky J, Goerke J. 1992. Pores of Kohn are filled in normal lungs: low-temperature scanning electron microscopy. J Appl Physiol (1985) 73:88–95. [PubMed]
9. Mason RJ. 2006. Biology of alveolar type II cells. Respirology 11(Suppl):S12–S15 http://dx.doi.org/10.1111/j.1440-1843.2006.00800.x.
10. Guillot L, Nathan N, Tabary O, Thouvenin G, Le Rouzic P, Corvol H, Amselem S, Clement A. 2013. Alveolar epithelial cells: master regulators of lung homeostasis. Int J Biochem Cell Biol 45:2568–2573 http://dx.doi.org/10.1016/j.biocel.2013.08.009. [PubMed]
11. Debbabi H, Ghosh S, Kamath AB, Alt J, Demello DE, Dunsmore S, Behar SM. 2005. Primary type II alveolar epithelial cells present microbial antigens to antigen-specific CD4+ T cells. Am J Physiol Lung Cell Mol Physiol 289:L274–L279 http://dx.doi.org/10.1152/ajplung.00004.2005.
12. Fels AO, Cohn ZA. 1986. The alveolar macrophage. J Appl Physiol (1985) 60:353–369. [PubMed]
13. Murphy J, Summer R, Wilson AA, Kotton DN, Fine A. 2008. The prolonged life-span of alveolar macrophages. Am J Respir Cell Mol Biol 38:380–385 http://dx.doi.org/10.1165/rcmb.2007-0224RC. [PubMed]
14. Hussell T, Bell TJ. 2014. Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol 14:81–93 http://dx.doi.org/10.1038/nri3600. [PubMed]
15. van oud Alblas AB, van Furth R. 1979. Origin, kinetics, and characteristics of pulmonary macrophages in the normal steady state. J Exp Med 149:1504–1518 http://dx.doi.org/10.1084/jem.149.6.1504. [PubMed]
16. Bitterman PB, Saltzman LE, Adelberg S, Ferrans VJ, Crystal RG. 1984. Alveolar macrophage replication. One mechanism for the expansion of the mononuclear phagocyte population in the chronically inflamed lung. J Clin Invest 74:460–469 http://dx.doi.org/10.1172/JCI111443.
17. Landsman L, Jung S. 2007. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J Immunol 179:3488–3494 http://dx.doi.org/10.4049/jimmunol.179.6.3488.
18. Kopf M, Schneider C, Nobs SP. 2015. The development and function of lung-resident macrophages and dendritic cells. Nat Immunol 16:36–44 http://dx.doi.org/10.1038/ni.3052. [PubMed]
19. Epelman S, Lavine KJ, Randolph GJ. 2014. Origin and functionsof tissue macrophages. Immunity 41:21–35 http://dx.doi.org/10.1016/j.immuni.2014.06.013. [PubMed]
20. Ginhoux F. 2014. Fate PPAR-titioning: PPAR-γ ‘instructs’ alveolar macrophage development. Nat Immunol 15:1005–1007 http://dx.doi.org/10.1038/ni.3011. [PubMed]
21. Lambrecht BN. 2006. Alveolar macrophage in the driver’s seat. Immunity 24:366–368 http://dx.doi.org/10.1016/j.immuni.2006.03.008. [PubMed]
22. Rajaram MVS, Ni B, Dodd CE, Schlesinger LS. 2014. Macrophage immunoregulatory pathways in tuberculosis. Semin Immunol 26:471–485 http://dx.doi.org/10.1016/j.smim.2014.09.010. [PubMed]
23. Rajaram MVS, Brooks MN, Morris JD, Torrelles JB, Azad AK, Schlesinger LS. 2010. Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor gamma linking mannose receptor recognition to regulation of immune responses. J Immunol 185:929–942 http://dx.doi.org/10.4049/jimmunol.1000866.
24. Schneider C, Nobs SP, Kurrer M, Rehrauer H, Thiele C, Kopf M. 2014. Induction of the nuclear receptor PPAR-γ by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat Immunol 15:1026–1037 http://dx.doi.org/10.1038/ni.3005.
25. Hoidal JR, Schmeling D, Peterson PK. 1981. Phagocytosis, bacterial killing, and metabolism by purified human lung phagocytes. J Infect Dis 144:61–71 http://dx.doi.org/10.1093/infdis/144.1.61.
26. Greening AP, Lowrie DB. 1983. Extracellular release of hydrogen peroxide by human alveolar macrophages: the relationship to cigarette smoking and lower respiratory tract infections. Clin Sci (Lond) 65:661–664 http://dx.doi.org/10.1042/cs0650661.
27. Lyons CR, Ball EJ, Toews GB, Weissler JC, Stastny P, Lipscomb MF. 1986. Inability of human alveolar macrophages to stimulate resting T cells correlates with decreased antigen-specific T cell-macrophage binding. J Immunol 137:1173–1180.
28. Holt PG, Oliver J, Bilyk N, McMenamin C, McMenamin PG, Kraal G, Thepen T. 1993. Downregulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. J Exp Med 177:397–407 http://dx.doi.org/10.1084/jem.177.2.397.
29. Roth MD, Golub SH. 1993. Human pulmonary macrophages utilize prostaglandins and transforming growth factor beta 1 to suppress lymphocyte activation. J Leukoc Biol 53:366–371. [PubMed]
30. Schneberger D, Aharonson-Raz K, Singh B. 2012. Pulmonary intravascular macrophages and lung health: what are we missing? Am J Physiol Lung Cell Mol Physiol 302:L498–L503 http://dx.doi.org/10.1152/ajplung.00322.2011. [PubMed][CrossRef]
31. Lohmann-Matthes M-L, Steinmüller C, Franke-Ullmann G. 1994. Pulmonary macrophages. Eur Respir J 7:1678–1689. [PubMed]
32. Cai Y, Sugimoto C, Arainga M, Alvarez X, Didier ES, Kuroda MJ. 2014. In vivo characterization of alveolar and interstitial lung macrophages in rhesus macaques: implications for understanding lung disease in humans. J Immunol 192:2821–2829 http://dx.doi.org/10.4049/jimmunol.1302269.
33. Schneberger D, Aharonson-Raz K, Singh B. 2011. Monocyte and macrophage heterogeneity and Toll-like receptors in the lung. Cell Tissue Res 343:97–106 http://dx.doi.org/10.1007/s00441-010-1032-2. [PubMed]
34. Guilliams M, Lambrecht BN, Hammad H. 2013. Division of labor between lung dendritic cells and macrophages in the defense against pulmonary infections. Mucosal Immunol 6:464–473 http://dx.doi.org/10.1038/mi.2013.14.
35. Thornton EE, Looney MR, Bose O, Sen D, Sheppard D, Locksley R, Huang X, Krummel MF. 2012. Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. J Exp Med 209:1183–1199 http://dx.doi.org/10.1084/jem.20112667. [PubMed]
36. Vermaelen KY, Carro-Muino I, Lambrecht BN, Pauwels RA. 2001. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J Exp Med 193:51–60 http://dx.doi.org/10.1084/jem.193.1.51.
37. Halle S, Dujardin HC, Bakocevic N, Fleige H, Danzer H, Willenzon S, Suezer Y, Hämmerling G, Garbi N, Sutter G, Worbs T, Förster R. 2009. Induced bronchus-associated lymphoid tissue serves as a general priming site for T cells and is maintained by dendritic cells. J Exp Med 206:2593–2601 http://dx.doi.org/10.1084/jem.20091472.
38. Randall TD. 2010. Pulmonary dendritic cells: thinking globally, acting locally. J Exp Med 207:451–454 http://dx.doi.org/10.1084/jem.20100059. [PubMed]
39. Gold MC, Napier RJ, Lewinsohn DM. 2015. MR1-restricted mucosal associated invariant T (MAIT) cells in the immune response to Mycobacterium tuberculosis. Immunol Rev 264:154–166 http://dx.doi.org/10.1111/imr.12271.
40. Gold MC, Cerri S, Smyk-Pearson S, Cansler ME, Vogt TM, Delepine J, Winata E, Swarbrick GM, Chua W-J, Yu YYL, Lantz O, Cook MS, Null MD, Jacoby DB, Harriff MJ, Lewinsohn DA, Hansen TH, Lewinsohn DM. 2010. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol 8:e1000407. doi:10.1371/journal.pbio.1000407 http://dx.doi.org/10.1371/journal.pbio.1000407.
41. Le Bourhis L, Martin E, Péguillet I, Guihot A, Froux N, Coré M, Lévy E, Dusseaux M, Meyssonnier V, Premel V, Ngo C, Riteau B, Duban L, Robert D, Huang S, Rottman M, Soudais C, Lantz O. 2010. Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 11:701–708 http://dx.doi.org/10.1038/ni.1890. (Erratum 11:969.)
42. Le Bourhis L, Dusseaux M, Bohineust A, Bessoles S, Martin E, Premel V, Coré M, Sleurs D, Serriari N-E, Treiner E, Hivroz C, Sansonetti P, Gougeon M-L, Soudais C, Lantz O. 2013. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog 9:e1003681. doi:10.1371/journal.ppat.1003681 http://dx.doi.org/10.1371/journal.ppat.1003681.
43. Chua W-J, Truscott SM, Eickhoff CS, Blazevic A, Hoft DF, Hansen TH. 2012. Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect Immun 80:3256–3267 http://dx.doi.org/10.1128/IAI.00279-12.
44. Craig A, Mai J, Cai S, Jeyaseelan S. 2009. Neutrophil recruitment to the lungs during bacterial pneumonia. Infect Immun 77:568–575 http://dx.doi.org/10.1128/IAI.00832-08. [PubMed]
45. Wright JR. 1997. Immunomodulatory functions of surfactant. Physiol Rev 77:931–962. [PubMed]
46. Wright JR. 2005. Immunoregulatory functions of surfactant proteins. Nat Rev Immunol 5:58–68 http://dx.doi.org/10.1038/nri1528.
47. Mason RJ, Voelker DR. 1998. Regulatory mechanisms of surfactant secretion. Biochim Biophys Acta 1408:226–240 http://dx.doi.org/10.1016/S0925-4439(98)00070-2. [PubMed]
48. Crouch E, Wright JR. 2001. Surfactant proteins a and d and pulmonary host defense. Annu Rev Physiol 63:521–554 http://dx.doi.org/10.1146/annurev.physiol.63.1.521. [PubMed]
49. Beharka AA, Gaynor CD, Kang BK, Voelker DR, McCormack FX, Schlesinger LS. 2002. Pulmonary surfactant protein A up-regulates activity of the mannose receptor, a pattern recognition receptor expressed on human macrophages. J Immunol 169:3565–3573 http://dx.doi.org/10.4049/jimmunol.169.7.3565.
50. Crowther JE, Kutala VK, Kuppusamy P, Ferguson JS, Beharka AA, Zweier JL, McCormack FX, Schlesinger LS. 2004. Pulmonary surfactant protein a inhibits macrophage reactive oxygen intermediate production in response to stimuli by reducing NADPH oxidase activity. J Immunol 172:6866–6874 http://dx.doi.org/10.4049/jimmunol.172.11.6866.
51. Nguyen HA, Rajaram MVS, Meyer DA, Schlesinger LS. 2012. Pulmonary surfactant protein A and surfactant lipids upregulate IRAK-M, a negative regulator of TLR-mediated inflammation in human macrophages. Am J Physiol Lung Cell Mol Physiol 303:L608–L616 http://dx.doi.org/10.1152/ajplung.00067.2012.
52. van Iwaarden F, Welmers B, Verhoef J, Haagsman HP, van Golde LM. 1990. Pulmonary surfactant protein A enhances the host-defense mechanism of rat alveolar macrophages. Am J Respir Cell Mol Biol 2:91–98 http://dx.doi.org/10.1165/ajrcmb/2.1.91. [PubMed]
53. Haagsman HP. 1998. Interactions of surfactant protein A with pathogens. Biochim Biophys Acta 1408:264–277 http://dx.doi.org/10.1016/S0925-4439(98)00072-6.
54. Carlson TK, Brooks MN, Rajaram MVS, Henning LN, Meyer DA, Schlesinger LS. 2010. Pulmonary innate immunity: soluble and cellular host defenses of the lung, p 167–211. In Marsh CB, Hunter, Tridandapani S, Piper MG (ed), Regulation of Innate Immune Function. Transworld Research Signpost, STM Books.
55. Gaynor CD, McCormack FX, Voelker DR, McGowan SE, Schlesinger LS. 1995. Pulmonary surfactant protein A mediates enhanced phagocytosis of Mycobacterium tuberculosis by a direct interaction with human macrophages. J Immunol 155:5343–5351. [PubMed]
56. Downing JF, Pasula R, Wright JR, Twigg HL III, Martin WJ II. 1995. Surfactant protein a promotes attachment of Mycobacterium tuberculosis to alveolar macrophages during infection with human immunodeficiency virus. Proc Natl Acad Sci USA 92:4848–4852 http://dx.doi.org/10.1073/pnas.92.11.4848.
57. Pasula R, Downing JF, Wright JR, Kachel DL, Davis TE Jr, Martin WJ II. 1997. Surfactant protein A (SP-A) mediates attachment of Mycobacterium tuberculosis to murine alveolar macrophages. Am J Respir Cell Mol Biol 17:209–217 http://dx.doi.org/10.1165/ajrcmb.17.2.2469. [PubMed]
58. Sidobre S, Nigou J, Puzo G, Rivière M. 2000. Lipoglycans are putative ligands for the human pulmonary surfactant protein A attachment to mycobacteria. Critical role of the lipids for lectin-carbohydrate recognition. J Biol Chem 275:2415–2422 http://dx.doi.org/10.1074/jbc.275.4.2415.
59. Ferguson JS, Voelker DR, McCormack FX, Schlesinger LS. 1999. Surfactant protein D binds to Mycobacterium tuberculosis bacilli and lipoarabinomannan via carbohydrate-lectin interactions resulting in reduced phagocytosis of the bacteria by macrophages. J Immunol 163:312–321. [PubMed]
60. Ferguson JS, Martin JL, Azad AK, McCarthy TR, Kang PB, Voelker DR, Crouch EC, Schlesinger LS. 2006. Surfactant protein D increases fusion of Mycobacterium tuberculosis-containing phagosomes with lysosomes in human macrophages. Infect Immun 74:7005–7009 http://dx.doi.org/10.1128/IAI.01402-06.
61. Ferguson JS, Voelker DR, Ufnar JA, Dawson AJ, Schlesinger LS. 2002. Surfactant protein D inhibition of human macrophage uptake of Mycobacterium tuberculosis is independent of bacterial agglutination. J Immunol 168:1309–1314 http://dx.doi.org/10.4049/jimmunol.168.3.1309.
62. Ferguson JS, Schlesinger LS. 2000. Pulmonary surfactant in innate immunity and the pathogenesis of tuberculosis. Tuber Lung Dis 80:173–184 http://dx.doi.org/10.1054/tuld.2000.0242.
63. Arcos J, Diangelo LE, Scordo JM, Sasindran SJ, Moliva JI, Turner J, Torrelles JB. 2015. Lung mucosa lining fluid modification of Mycobacterium tuberculosis to reprogram human neutrophil killing mechanisms. J Infect Dis 212:948–958 http://dx.doi.org/10.1093/infdis/jiv146.
64. Herzog EL, Brody AR, Colby TV, Mason R, Williams MC. 2008. Knowns and unknowns of the alveolus. Proc Am Thorac Soc 5:778–782 http://dx.doi.org/10.1513/pats.200803-028HR. [PubMed]
65. Strunk RC, Eidlen DM, Mason RJ. 1988. Pulmonary alveolar type II epithelial cells synthesize and secrete proteins of the classical and alternative complement pathways. J Clin Invest 81:1419–1426 http://dx.doi.org/10.1172/JCI113472.
66. Cole FS, Matthews WJ Jr, Rossing TH, Gash DJ, Lichtenberg NA, Pennington JE. 1983. Complement biosynthesis by human bronchoalveolar macrophages. Clin Immunol Immunopathol 27:153–159 http://dx.doi.org/10.1016/0090-1229(83)90065-X.
67. Schlesinger LS, Bellinger-Kawahara CG, Payne NR, Horwitz MA. 1990. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J Immunol 144:2771–2780. [PubMed]
68. Ferguson JS, Weis JJ, Martin JL, Schlesinger LS. 2004. Complement protein C3 binding to Mycobacterium tuberculosis is initiated by the classical pathway in human bronchoalveolar lavage fluid. Infect Immun 72:2564–2573 http://dx.doi.org/10.1128/IAI.72.5.2564-2573.2004.
69. Figueroa JE, Densen P. 1991. Infectious diseases associated with complement deficiencies. Clin Microbiol Rev 4:359–395. [PubMed]
70. Mold C. 1999. Role of complement in host defense against bacterial infection. Microbes Infect 1:633–638 http://dx.doi.org/10.1016/S1286-4579(99)80063-X.
71. Tedesco F. 2008. Inherited complement deficiencies and bacterial infections. Vaccine 26(Suppl 8):I3–I8 http://dx.doi.org/10.1016/j.vaccine.2008.11.010.
72. Moliva JI, Rajaram MVS, Sidiki S, Sasindran SJ, Guirado E, Pan XJ, Wang S-H, Ross P Jr, Lafuse WP, Schlesinger LS, Turner J, Torrelles JB. 2014. Molecular composition of the alveolar lining fluid inthe aging lung.Age (Dordr) 36:9633 http://dx.doi.org/10.1007/s11357-014-9633-4.
73. Arcos J, Sasindran SJ, Fujiwara N, Turner J, Schlesinger LS, Torrelles JB. 2011. Human lung hydrolases delineate Mycobacterium tuberculosis-macrophage interactions and the capacity to control infection. J Immunol 187:372–381 http://dx.doi.org/10.4049/jimmunol.1100823.
74. Stahl PD. 1990. The macrophage mannose receptor: current status. Am J Respir Cell Mol Biol 2:317–318 http://dx.doi.org/10.1165/ajrcmb/2.4.317.
75. Speert DP, Silverstein SC. 1985. Phagocytosis of unopsonized zymosan by human monocyte-derived macrophages: maturation and inhibition by mannan. J Leukoc Biol 38:655–658. [PubMed]
76. Wileman TE, Lennartz MR, Stahl PD. 1986. Identification of the macrophage mannose receptor as a 175-kDa membrane protein. Proc Natl Acad Sci USA 83:2501–2505 http://dx.doi.org/10.1073/pnas.83.8.2501. [PubMed]
77. McGreal EP, Miller JL, Gordon S. 2005. Ligand recognition by antigen-presenting cell C-type lectin receptors. Curr Opin Immunol 17:18–24 http://dx.doi.org/10.1016/j.coi.2004.12.001.
78. Stahl PD, Ezekowitz RA. 1998. The mannose receptor is a pattern recognition receptor involved in host defense. Curr Opin Immunol 10:50–55 http://dx.doi.org/10.1016/S0952-7915(98)80031-9.
79. Martinez-Pomares L, Linehan SA, Taylor PR, Gordon S. 2001. Binding properties of the mannose receptor. Immunobiology 204:527–535 http://dx.doi.org/10.1078/0171-2985-00089.
80. Lee SJ, Evers S, Roeder D, Parlow AF, Risteli J, Risteli L, Lee YC, Feizi T, Langen H, Nussenzweig MC. 2002. Mannose receptor-mediated regulation of serum glycoprotein homeostasis. Science 295:1898–1901 http://dx.doi.org/10.1126/science.1069540.
81. Medzhitov R, Janeway C Jr. 2000. Innate immunity. N Engl J Med 343:338–344 http://dx.doi.org/10.1056/NEJM200008033430506.
82. Schlesinger LS, Hull SR, Kaufman TM. 1994. Binding of the terminal mannosyl units of lipoarabinomannan from a virulent strain of Mycobacterium tuberculosis to human macrophages. J Immunol 152:4070–4079. [PubMed]
83. Torrelles JB, Schlesinger LS. 2010. Diversity in Mycobacterium tuberculosis mannosylated cell wall determinants impacts adaptation to the host. Tuberculosis (Edinb) 90:84–93 http://dx.doi.org/10.1016/j.tube.2010.02.003.
84. Torrelles JB, Azad AK, Schlesinger LS. 2006. Fine discrimination in the recognition of individual species of phosphatidyl-myo-inositol mannosides from Mycobacterium tuberculosis by C-type lectin pattern recognition receptors. J Immunol 177:1805–1816 http://dx.doi.org/10.4049/jimmunol.177.3.1805.
85. Schlesinger LS, Kaufman TM, Iyer S, Hull SR, Marchiando LK. 1996. Differences in mannose receptor-mediated uptake of lipoarabinomannan from virulent and attenuated strains of Mycobacterium tuberculosis by human macrophages. J Immunol 157:4568–4575. [PubMed]
86. Torrelles JB, Knaup R, Kolareth A, Slepushkina T, Kaufman TM, Kang P, Hill PJ, Brennan PJ, Chatterjee D, Belisle JT, Musser JM, Schlesinger LS. 2008. Identification of Mycobacterium tuberculosis clinical isolates with altered phagocytosis by human macrophages due to a truncated lipoarabinomannan. J Biol Chem 283:31417–31428 http://dx.doi.org/10.1074/jbc.M806350200.
87. Kang PB, Azad AK, Torrelles JB, Kaufman TM, Beharka A, Tibesar E, DesJardin LE, Schlesinger LS. 2005. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 202:987–999 http://dx.doi.org/10.1084/jem.20051239.
88. Aderem A, Underhill DM. 1999. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17:593–623 http://dx.doi.org/10.1146/annurev.immunol.17.1.593.
89. Singh CR, Moulton RA, Armitige LY, Bidani A, Snuggs M, Dhandayuthapani S, Hunter RL, Jagannath C. 2006. Processing and presentation of a mycobacterial antigen 85B epitope by murine macrophages is dependent on the phagosomal acquisition of vacuolar proton ATPase and in situ activation of cathepsin D. J Immunol 177:3250–3259 http://dx.doi.org/10.4049/jimmunol.177.5.3250.
90. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J, Russell DG. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678–681 http://dx.doi.org/10.1126/science.8303277.
91. Astarie-Dequeker C, N’Diaye EN, Le Cabec V, Rittig MG, Prandi J, Maridonneau-Parini I. 1999. The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages. Infect Immun 67:469–477. [PubMed]
92. Chieppa M, Bianchi G, Doni A, Del Prete A, Sironi M, Laskarin G, Monti P, Piemonti L, Biondi A, Mantovani A, Introna M, Allavena P. 2003. Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program. J Immunol 171:4552–4560 http://dx.doi.org/10.4049/jimmunol.171.9.4552.
93. Azad AK, Rajaram MVS, Schlesinger LS. 2014. Exploitation of the macrophage mannose receptor (CD206) in infectious disease diagnostics and therapeutics. J Cytol Mol Biol 1:1000003. doi:10.13188/2325-4653.1000003.
94. McNally AK, DeFife KM, Anderson JM. 1996. Interleukin-4-induced macrophage fusion is prevented by inhibitors of mannose receptor activity. Am J Pathol 149:975–985. [PubMed]
95. Gordon S, Martinez FO. 2010. Alternative activation of macrophages: mechanism and functions. Immunity 32:593–604 http://dx.doi.org/10.1016/j.immuni.2010.05.007. [PubMed]
96. Gordon S, Keshav S, Stein M. 1994. BCG-induced granuloma formation in murine tissues. Immunobiology 191:369–377 http://dx.doi.org/10.1016/S0171-2985(11)80442-0.
97. Bleijs DA, Geijtenbeek TB, Figdor CG, van Kooyk Y. 2001. DC-SIGN and LFA-1: a battle for ligand. Trends Immunol 22:457–463 http://dx.doi.org/10.1016/S1471-4906(01)01974-3. [PubMed]
98. Tailleux L, Pham-Thi N, Bergeron-Lafaurie A, Herrmann J-L, Charles P, Schwartz O, Scheinmann P, Lagrange PH, de Blic J, Tazi A, Gicquel B, Neyrolles O. 2005. DC-SIGN induction in alveolar macrophages defines privileged target host cells for mycobacteria in patients with tuberculosis. PLoS Med 2:e381. doi:10.1371/journal.pmed.0020381 http://dx.doi.org/10.1371/journal.pmed.0020381.
99. Puig-Kröger A, Serrano-Gómez D, Caparrós E, Domínguez-Soto A, Relloso M, Colmenares M, Martínez-Muñoz L, Longo N, Sánchez-Sánchez N, Rincon M, Rivas L, Sánchez-Mateos P, Fernández-Ruiz E, Corbí AL. 2004. Regulated expression of the pathogen receptor dendritic cell-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin in THP-1 human leukemic cells, monocytes, and macrophages. J Biol Chem 279:25680–25688 http://dx.doi.org/10.1074/jbc.M311516200.
100. Geijtenbeek TBH, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CMJE, Appelmelk B, Van Kooyk Y. 2003. Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197:7–17 http://dx.doi.org/10.1084/jem.20021229.
101. Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, Amara A, Legres L, Dreher D, Nicod LP, Gluckman JC, Lagrange PH, Gicquel B, Neyrolles O. 2003. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197:121–127 http://dx.doi.org/10.1084/jem.20021468.
102. Guirado E, Schlesinger LS, Kaplan G. 2013. Macrophages in tuberculosis: friend or foe. Semin Immunopathol 35:563–583 http://dx.doi.org/10.1007/s00281-013-0388-2.
103. Matsumoto M, Tanaka T, Kaisho T, Sanjo H, Copeland NG, Gilbert DJ, Jenkins NA, Akira S. 1999. A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J Immunol 163:5039–5048. [PubMed]
104. Yamasaki S, Matsumoto M, Takeuchi O, Matsuzawa T, Ishikawa E, Sakuma M, Tateno H, Uno J, Hirabayashi J, Mikami Y, Takeda K, Akira S, Saito T. 2009. C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc Natl Acad Sci USA 106:1897–1902 http://dx.doi.org/10.1073/pnas.0805177106.
105. Yamasaki S, Ishikawa E, Sakuma M, Hara H, Ogata K, Saito T. 2008. Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat Immunol 9:1179–1188 http://dx.doi.org/10.1038/ni.1651.
106. Ishikawa E, Ishikawa T, Morita YS, Toyonaga K, Yamada H, Takeuchi O, Kinoshita T, Akira S, Yoshikai Y, Yamasaki S. 2009. Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med 206:2879–2888 http://dx.doi.org/10.1084/jem.20091750.
107. Schoenen H, Bodendorfer B, Hitchens K, Manzanero S, Werninghaus K, Nimmerjahn F, Agger EM, Stenger S, Andersen P, Ruland J, Brown GD, Wells C, Lang R. 2010. Cutting edge: mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J Immunol 184:2756–2760 http://dx.doi.org/10.4049/jimmunol.0904013.
108. Heitmann L, Schoenen H, Ehlers S, Lang R, Hölscher C. 2013. Mincle is not essential for controlling Mycobacterium tuberculosis infection. Immunobiology 218:506–516 http://dx.doi.org/10.1016/j.imbio.2012.06.005.
109. Tsoni SV, Brown GD. 2008. beta-Glucans and dectin-1. Ann N Y Acad Sci 1143:45–60 http://dx.doi.org/10.1196/annals.1443.019.
110. Taylor PR, Brown GD, Reid DM, Willment JA, Martinez-Pomares L, Gordon S, Wong SY. 2002. The β-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J Immunol 169:3876–3882 http://dx.doi.org/10.4049/jimmunol.169.7.3876.
111. van de Veerdonk FL, Teirlinck AC, Kleinnijenhuis J, Kullberg BJ, van Crevel R, van der Meer JWM, Joosten LAB, Netea MG. 2010. Mycobacterium tuberculosis induces IL-17A responses through TLR4 and dectin-1 and is critically dependent on endogenous IL-1. J Leukoc Biol 88:227–232 http://dx.doi.org/10.1189/jlb.0809550.
112. Rothfuchs AG, Báfica A, Feng CG, Egen JG, Williams DL, Brown GD, Sher A. 2007. Dectin-1 interaction with Mycobacterium tuberculosis leads to enhanced IL-12p40 production by splenic dendritic cells. J Immunol 179:3463–3471 http://dx.doi.org/10.4049/jimmunol.179.6.3463.
113. Yadav M, Schorey JS. 2006. The beta-glucan receptor dectin-1 functions together with TLR2 to mediate macrophage activation by mycobacteria. Blood 108:3168–3175 http://dx.doi.org/10.1182/blood-2006-05-024406.
114. Betz BE, Azad AK, Morris JD, Rajaram MVS, Schlesinger LS. 2011. β-Glucans inhibit intracellular growth of Mycobacterium bovis BCG but not virulent Mycobacterium tuberculosis in human macrophages. Microb Pathog 51:233–242 http://dx.doi.org/10.1016/j.micpath.2011.06.006.
115. Taylor PR, Reid DM, Heinsbroek SEM, Brown GD, Gordon S, Wong SYC. 2005. Dectin-2 is predominantly myeloid restricted and exhibits unique activation-dependent expression on maturing inflammatory monocytes elicited in vivo. Eur J Immunol 35:2163–2174 http://dx.doi.org/10.1002/eji.200425785.
116. Yonekawa A, Saijo S, Hoshino Y, Miyake Y, Ishikawa E, Suzukawa M, Inoue H, Tanaka M, Yoneyama M, Oh-Hora M, Akashi K, Yamasaki S. 2014. Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria. Immunity 41:402–413 http://dx.doi.org/10.1016/j.immuni.2014.08.005.
117. Zhao X-Q, Zhu L-L, Chang Q, Jiang C, You Y, Luo T, Jia X-M, Lin X. 2014. C-type lectin receptor dectin-3 mediates trehalose 6,6′-dimycolate (TDM)-induced Mincle expression through CARD9/Bcl10/MALT1-dependent nuclear factor (NF)-κB activation. J Biol Chem 289:30052–30062 http://dx.doi.org/10.1074/jbc.M114.588574.
118. Miyake Y, Toyonaga K, Mori D, Kakuta S, Hoshino Y, Oyamada A, Yamada H, Ono K, Suyama M, Iwakura Y, Yoshikai Y, Yamasaki S. 2013. C-type lectin MCL is an FcRγ-coupled receptor that mediates the adjuvanticity of mycobacterial cord factor. Immunity 38:1050–1062 http://dx.doi.org/10.1016/j.immuni.2013.03.010.
119. Myones BL, Dalzell JG, Hogg N, Ross GD. 1988. Neutrophil and monocyte cell surface p150,95 has iC3b-receptor (CR4) activity resembling CR3. J Clin Invest 82:640–651 http://dx.doi.org/10.1172/JCI113643. [PubMed]
120. Arnaout MA. 1990. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75:1037–1050. [PubMed]
121. Schlesinger LS, Azad AK. 2008. Determinants of phagocytosis, phagosome biogenesis and autophagy for Mycobacterium tuberculosis, p 1–22. In Kaufmann SHE, Britton WJ (ed), Handbook of Tuberculosis: Immunology and Cell Biology. Wiley VCH Publishers, Weinheim, Germany.
122. Schlesinger LS. 1993. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J Immunol 150:2920–2930. [PubMed]
123. Cywes C, Hoppe HC, Daffé M, Ehlers MR. 1997. Nonopsonic binding of Mycobacterium tuberculosis to complement receptor type 3 is mediated by capsular polysaccharides and is strain dependent. Infect Immun 65:4258–4266. [PubMed]
124. Villeneuve C, Gilleron M, Maridonneau-Parini I, Daffé M, Astarie-Dequeker C, Etienne G. 2005. Mycobacteria use their surface-exposed glycolipids to infect human macrophages through a receptor-dependent process. J Lipid Res 46:475–483 http://dx.doi.org/10.1194/jlr.M400308-JLR200.
125. Armstrong JA, Hart PD. 1975. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival. J Exp Med 142:1–16 http://dx.doi.org/10.1084/jem.142.1.1.
126. Basu S, Fenton MJ. 2004. Toll-like receptors: function and roles in lung disease. Am J Physiol Lung Cell Mol Physiol 286:L887–L892 http://dx.doi.org/10.1152/ajplung.00323.2003.
127. Pandey S, Kawai T, Akira S. 2015. Microbial sensing by Toll-like receptors and intracellular nucleic acid sensors. Cold Spring Harb Perspect Biol 7:a016246. doi:10.1101/cshperspect.a016246. http://dx.doi.org/10.1101/cshperspect.a016246. [PubMed]
128. Kawasaki T, Kawai T. 2014. Toll-like receptor signaling pathways. Front Immunol 5:461 http://dx.doi.org/10.3389/fimmu.2014.00461.
129. Kawai T, Akira S. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34:637–650 http://dx.doi.org/10.1016/j.immuni.2011.05.006.
130. Cambi A, Koopman M, Figdor CG. 2005. How C-type lectins detect pathogens. Cell Microbiol 7:481–488 http://dx.doi.org/10.1111/j.1462-5822.2005.00506.x.
131. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085–2088 http://dx.doi.org/10.1126/science.282.5396.2085. [PubMed]
132. Malhotra R, Thiel S, Reid KB, Sim RB. 1990. Human leukocyte C1q receptor binds other soluble proteins with collagen domains. J Exp Med 172:955–959 http://dx.doi.org/10.1084/jem.172.3.955.
133. Akira S, Uematsu S, Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell 124:783–801 http://dx.doi.org/10.1016/j.cell.2006.02.015.
134. Yamamoto M, Takeda K, Akira S. 2004. TIR domain-containing adaptors define the specificity of TLR signaling. Mol Immunol 40:861–868 http://dx.doi.org/10.1016/j.molimm.2003.10.006. [PubMed]
135. Kobayashi K, Hernandez LD, Galán JE, Janeway CA Jr, Medzhitov R, Flavell RA. 2002. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110:191–202 http://dx.doi.org/10.1016/S0092-8674(02)00827-9.
136. Means TK, Lien E, Yoshimura A, Wang S, Golenbock DT, Fenton MJ. 1999. The CD14 ligands lipoarabinomannan and lipopolysaccharide differ in their requirement for Toll-like receptors. J Immunol 163:6748–6755.
137. Jones BW, Means TK, Heldwein KA, Keen MA, Hill PJ, Belisle JT, Fenton MJ. 2001. Different Toll-like receptor agonists induce distinct macrophage responses. J Leukoc Biol 69:1036–1044. [PubMed]
138. Kindrachuk J, Potter J, Wilson HL, Griebel P, Babiuk LA, Napper S. 2008. Activation and regulation of toll-like receptor 9: CpGs and beyond. Mini Rev Med Chem 8:590–600 http://dx.doi.org/10.2174/138955708784534481.
139. Báfica A, Scanga CA, Feng CG, Leifer C, Cheever A, Sher A. 2005. TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med 202:1715–1724 http://dx.doi.org/10.1084/jem.20051782.
140. Drennan MB, Nicolle D, Quesniaux VJF, Jacobs M, Allie N, Mpagi J, Frémond C, Wagner H, Kirschning C, Ryffel B. 2004. Toll-like receptor 2-deficient mice succumb to Mycobacterium tuberculosis infection. Am J Pathol 164:49–57 http://dx.doi.org/10.1016/S0002-9440(10)63095-7.
141. Abel B, Thieblemont N, Quesniaux VJF, Brown N, Mpagi J, Miyake K, Bihl F, Ryffel B. 2002. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice. J Immunol 169:3155–3162 http://dx.doi.org/10.4049/jimmunol.169.6.3155.
142. Reiling N, Hölscher C, Fehrenbach A, Kröger S, Kirschning CJ, Goyert S, Ehlers S. 2002. Cutting edge: toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J Immunol 169:3480–3484 http://dx.doi.org/10.4049/jimmunol.169.7.3480.
143. Hölscher C, Reiling N, Schaible UE, Hölscher A, Bathmann C, Korbel D, Lenz I, Sonntag T, Kröger S, Akira S, Mossmann H, Kirschning CJ, Wagner H, Freudenberg M, Ehlers S. 2008. Containment of aerogenic Mycobacterium tuberculosis infection in mice does not require MyD88 adaptor function for TLR2, -4 and -9. Eur J Immunol 38:680–694 http://dx.doi.org/10.1002/eji.200736458.
144. Fremond CM, Yeremeev V, Nicolle DM, Jacobs M, Quesniaux VF, Ryffel B. 2004. Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J Clin Invest 114:1790–1799 http://dx.doi.org/10.1172/JCI200421027.
145. Mayer-Barber KD, Barber DL, Shenderov K, White SD, Wilson MS, Cheever A, Kugler D, Hieny S, Caspar P, Núñez G, Schlueter D, Flavell RA, Sutterwala FS, Sher A. 2010. Caspase-1 independent IL-1beta production is critical for host resistance to Mycobacterium tuberculosis and does not require TLR signaling in vivo. J Immunol 184:3326–3330 http://dx.doi.org/10.4049/jimmunol.0904189.
146. Canton J, Neculai D, Grinstein S. 2013. Scavenger receptors in homeostasis and immunity. Nat Rev Immunol 13:621–634 http://dx.doi.org/10.1038/nri3515.
147. Doi T, Higashino K, Kuriharag Y, Wada Y, Miyazaki T, Nakamura H, Uesugi S, Imanishi T, Kawabe Y, Itakura H, Yazaki Y, Matsumoto A, Kodama T. 1993. Charged collagen structure mediates the recognition of negatively charged macromolecules by macrophage scavenger receptors. J Biol Chem 268:2126–2133. [PubMed]
148. Yamamoto K, Nishimura N, Doi T, Imanishi T, Kodama T, Suzuki K, Tanaka T. 1997. The lysine cluster in the collagen-like domain of the scavenger receptor provides for its ligand binding and ligand specificity. FEBS Lett 414:182–186 http://dx.doi.org/10.1016/S0014-5793(97)01006-5.
149. Arredouani MS, Palecanda A, Koziel H, Huang Y-C, Imrich A, Sulahian TH, Ning YY, Yang Z, Pikkarainen T, Sankala M, Vargas SO, Takeya M, Tryggvason K, Kobzik L. 2005. MARCO is the major binding receptor for unopsonized particles and bacteria on human alveolar macrophages. J Immunol 175:6058–6064 http://dx.doi.org/10.4049/jimmunol.175.9.6058.
150. Reddy RC. 2008. Immunomodulatory role of PPAR-gamma in alveolar macrophages. J Investig Med 56:522–527 http://dx.doi.org/10.2310/JIM.0b013e3181659972.
151. Zimmerli S, Edwards S, Ernst JD. 1996. Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages. Am J Respir Cell Mol Biol 15:760–770 http://dx.doi.org/10.1165/ajrcmb.15.6.8969271.
152. Bowdish DME, Sakamoto K, Kim M-J, Kroos M, Mukhopadhyay S, Leifer CA, Tryggvason K, Gordon S, Russell DG. 2009. MARCO, TLR2, and CD14 are required for macrophage cytokine responses to mycobacterial trehalose dimycolate and Mycobacterium tuberculosis. PLoS Pathog 5:e1000474. doi:10.1371/journal.ppat.1000474. http://dx.doi.org/10.1371/journal.ppat.1000474.
153. Mahajan S, Dkhar HK, Chandra V, Dave S, Nanduri R, Janmeja AK, Agrewala JN, Gupta P. 2012. Mycobacterium tuberculosis modulates macrophage lipid-sensing nuclear receptors PPARγ and TR4 for survival. J Immunol 188:5593–5603 http://dx.doi.org/10.4049/jimmunol.1103038.
154. Almeida PE, Roque NR, Magalhães KG, Mattos KA, Teixeira L, Maya-Monteiro C, Almeida CJ, Castro-Faria-Neto HC, Ryffel B, Quesniaux VFJ, Bozza PT. 2014. Differential TLR2 downstream signaling regulates lipid metabolism and cytokine production triggered by Mycobacterium bovis BCG infection. Biochim Biophys Acta 1841:97–107. [PubMed]
155. Asada K, Sasaki S, Suda T, Chida K, Nakamura H. 2004. Antiinflammatory roles of peroxisome proliferator-activated receptor γ in human alveolar macrophages. Am J Respir Crit Care Med 169:195–200 http://dx.doi.org/10.1164/rccm.200207-740OC.
156. Court N, Vasseur V, Vacher R, Frémond C, Shebzukhov Y, Yeremeev VV, Maillet I, Nedospasov SA, Gordon S, Fallon PG, Suzuki H, Ryffel B, Quesniaux VFJ. 2010. Partial redundancy of the pattern recognition receptors, scavenger receptors, and C-type lectins for the long-term control of Mycobacterium tuberculosis infection. J Immunol 184:7057–7070 http://dx.doi.org/10.4049/jimmunol.1000164.
157. Arredouani MS, Yang Z, Imrich A, Ning Y, Qin G, Kobzik L. 2006. The macrophage scavenger receptor SR-AI/II and lung defense against pneumococci and particles. Am J Respir Cell Mol Biol 35:474–478 http://dx.doi.org/10.1165/rcmb.2006-0128OC. [PubMed]
158. Hollifield M, Bou Ghanem E, de Villiers WJS, Garvy BA. 2007. Scavenger receptor A dampens induction of inflammation in response to the fungal pathogen Pneumocystis carinii. Infect Immun 75:3999–4005 http://dx.doi.org/10.1128/IAI.00393-07.
159. Arredouani M, Yang Z, Ning Y, Qin G, Soininen R, Tryggvason K, Kobzik L. 2004. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J Exp Med 200:267–272 http://dx.doi.org/10.1084/jem.20040731.
160. Hawkes M, Li X, Crockett M, Diassiti A, Finney C, Min-Oo G, Liles WC, Liu J, Kain KC. 2010. CD36 deficiency attenuates experimental mycobacterial infection. BMC Infect Dis 10:299 http://dx.doi.org/10.1186/1471-2334-10-299.
161. Flannagan RS, Jaumouillé V, Grinstein S. 2012. The cell biology of phagocytosis. Annu Rev Pathol 7:61–98 http://dx.doi.org/10.1146/annurev-pathol-011811-132445.
162. Russell DG. 2001. Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2:569–577 http://dx.doi.org/10.1038/35085034.
163. Reiner NE. 1994. Altered cell signaling and mononuclear phagocyte deactivation during intracellular infection. Immunol Today 15:374–381 http://dx.doi.org/10.1016/0167-5699(94)90176-7.
164. Deretic V, Singh S, Master S, Harris J, Roberts E, Kyei G, Davis A, de Haro S, Naylor J, Lee H-H, Vergne I. 2006. Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell Microbiol 8:719–727 http://dx.doi.org/10.1111/j.1462-5822.2006.00705.x.
165. Lugo-Villarino G, Neyrolles O. 2014. Manipulation of the mononuclear phagocyte system by Mycobacterium tuberculosis. Cold Spring Harb Perspect Med 4:a018549. doi:10.1101/cshperspect.a016246. http://dx.doi.org/10.1101/cshperspect.a018549. [PubMed]
166. Shukla S, Richardson ET, Athman JJ, Shi L, Wearsch PA, McDonald D, Banaei N, Boom WH, Jackson M, Harding CV. 2014. Mycobacterium tuberculosis lipoprotein LprG binds lipoarabinomannan and determines its cell envelope localization to control phagolysosomal fusion. PLoS Pathog 10:e1004471. doi:10.1371/journal.ppat.1004471. (Correction 10:e1004596.) http://dx.doi.org/10.1371/journal.ppat.1004471.
167. Gaur RL, Ren K, Blumenthal A, Bhamidi S, González-Nilo FD, Jackson M, Zare RN, Ehrt S, Ernst JD, Banaei N. 2014. LprG-mediated surface expression of lipoarabinomannan is essential for virulence of Mycobacterium tuberculosis. PLoS Pathog 10:e1004376. doi:10.1371/journal.ppat.1004376. (Errata 10:e1004489, 10:e1004494.) http://dx.doi.org/10.1371/journal.ppat.1004376. [PubMed]
168. Welin A, Lerm M. 2012. Inside or outside the phagosome? The controversy of the intracellular localization of Mycobacterium tuberculosis. Tuberculosis (Edinb) 92:113–120 http://dx.doi.org/10.1016/j.tube.2011.09.009.
169. Leake ES, Myrvik QN, Wright MJ. 1984. Phagosomal membranes of Mycobacterium bovis BCG-immune alveolar macrophages are resistant to disruption by Mycobacterium tuberculosis H37Rv. Infect Immun 45:443–446. [PubMed]
170. McDonough KA, Kress Y, Bloom BR. 1993. Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 61:2763–2773. [PubMed]
171. Myrvik QN, Leake ES, Wright MJ. 1984. Disruption of phagosomal membranes of normal alveolar macrophages by the H37Rv strain of Mycobacterium tuberculosis. A correlate of virulence. Am Rev Respir Dis 129:322–328. [PubMed]
172. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, Brosch R, Enninga J. 2012. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 8:e1002507. doi:10.1371/journal.ppat.1002507. http://dx.doi.org/10.1371/journal.ppat.1002507. [PubMed]
173. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ. 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129:1287–1298 http://dx.doi.org/10.1016/j.cell.2007.05.059.
174. Houben D, Demangel C, van Ingen J, Perez J, Baldeón L, Abdallah AM, Caleechurn L, Bottai D, van Zon M, de Punder K, van der Laan T, Kant A, Bossers-de Vries R, Willemsen P, Bitter W, van Soolingen D, Brosch R, van der Wel N, Peters PJ. 2012. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol 14:1287–1298 http://dx.doi.org/10.1111/j.1462-5822.2012.01799.x.
175. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS. 2012. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11:469–480 http://dx.doi.org/10.1016/j.chom.2012.03.007.
176. Watson RO, Manzanillo PS, Cox JS. 2012. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150:803–815 http://dx.doi.org/10.1016/j.cell.2012.06.040.
177. Shen H-M, Mizushima N. 2014. At the end of the autophagic road: an emerging understanding of lysosomal functions in autophagy. Trends Biochem Sci 39:61–71 http://dx.doi.org/10.1016/j.tibs.2013.12.001.
178. Mizushima N, Komatsu M. 2011. Autophagy: renovation of cells and tissues. Cell 147:728–741 http://dx.doi.org/10.1016/j.cell.2011.10.026.
179. Levine B, Mizushima N, Virgin HW. 2011. Autophagy in immunity and inflammation. Nature 469:323–335 http://dx.doi.org/10.1038/nature09782. [PubMed][CrossRef]
180. Deretic V. 2014. Autophagy in tuberculosis. Cold Spring Harb Perspect Med 4:a018481. doi:10.1101/cshperspect.a018481. http://dx.doi.org/10.1101/cshperspect.a018481.
181. Yang C-S, Kim J-J, Lee H-M, Jin HS, Lee S-H, Park J-H, Kim SJ, Kim J-M, Han Y-M, Lee M-S, Kweon GR, Shong M, Jo E-K. 2014. The AMPK-PPARGC1A pathway is required for antimicrobial host defense through activation of autophagy. Autophagy 10:785–802 http://dx.doi.org/10.4161/auto.28072.
182. Abnave P, Mottola G, Gimenez G, Boucherit N, Trouplin V, Torre C, Conti F, Ben Amara A, Lepolard C, Djian B, Hamaoui D, Mettouchi A, Kumar A, Pagnotta S, Bonatti S, Lepidi H, Salvetti A, Abi-Rached L, Lemichez E, Mege J-L, Ghigo E. 2014. Screening in planarians identifies MORN2 as a key component in LC3-associated phagocytosis and resistance to bacterial infection. Cell Host Microbe 16:338–350 http://dx.doi.org/10.1016/j.chom.2014.08.002.
183. Romagnoli A, Etna MP, Giacomini E, Pardini M, Remoli ME, Corazzari M, Falasca L, Goletti D, Gafa V, Simeone R, Delogu G, Piacentini M, Brosch R, Fimia GM, Coccia EM. 2012. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8:1357–1370 http://dx.doi.org/10.4161/auto.20881.
184. Shin D-M, Jeon B-Y, Lee H-M, Jin HS, Yuk J-M, Song C-H, Lee S-H, Lee Z-W, Cho S-N, Kim J-M, Friedman RL, Jo E-K. 2010. Mycobacterium tuberculosiseis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog 6:e1001230. doi:10.1371/journal.ppat.1001230. http://dx.doi.org/10.1371/journal.ppat.1001230.
185. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. 2004. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119:753–766 http://dx.doi.org/10.1016/j.cell.2004.11.038.
186. Fabri M, Stenger S, Shin D-M, Yuk J-M, Liu PT, Realegeno S, Lee H-M, Krutzik SR, Schenk M, Sieling PA, Teles R, Montoya D, Iyer SS, Bruns H, Lewinsohn DM, Hollis BW, Hewison M, Adams JS, Steinmeyer A, Zügel U, Cheng G, Jo E-K, Bloom BR, Modlin RL. 2011. Vitamin D is required for IFN-gamma-mediated antimicrobial activity of human macrophages. Sci Transl Med 3:104ra102. doi:10.1126/scitranslmed.3003045. http://dx.doi.org/10.1126/scitranslmed.3003045.
187. Castillo EF, Dekonenko A, Arko-Mensah J, Mandell MA, Dupont N, Jiang S, Delgado-Vargas M, Timmins GS, Bhattacharya D, Yang H, Hutt J, Lyons CR, Dobos KM, Deretic V. 2012. Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc Natl Acad Sci USA 109:E3168–E3176 http://dx.doi.org/10.1073/pnas.1210500109.
188. Kim J-J, Lee H-M, Shin D-M, Kim W, Yuk J-M, Jin HS, Lee S-H, Cha G-H, Kim J-M, Lee Z-W, Shin SJ, Yoo H, Park YK, Park JB, Chung J, Yoshimori T, Jo E-K. 2012. Host cell autophagy activated by antibiotics is required for their effective antimycobacterial drug action. Cell Host Microbe 11:457–468 http://dx.doi.org/10.1016/j.chom.2012.03.008.
189. Bento CF, Empadinhas N, Mendes V. 2015. Autophagy in the fight against tuberculosis. DNA Cell Biol 34:228–242 http://dx.doi.org/10.1089/dna.2014.2745.
190. Stanley SA, Barczak AK, Silvis MR, Luo SS, Sogi K, Vokes M, Bray M-A, Carpenter AE, Moore CB, Siddiqi N, Rubin EJ, Hung DT. 2014. Identification of host-targeted small molecules that restrict intracellular Mycobacterium tuberculosis growth. PLoS Pathog 10:e1003946. doi:10.1371/journal.ppat.1003946. http://dx.doi.org/10.1371/journal.ppat.1003946.
191. Hu D, Wu J, Zhang R, Chen L, Chen Z, Wang X, Xu L, Xiao J, Hu F, Wu C. 2014. Autophagy-targeted vaccine of LC3-LpqH DNA and its protective immunity in a murine model of tuberculosis. Vaccine 32:2308–2314 http://dx.doi.org/10.1016/j.vaccine.2014.02.069.
192. Olive AJ, Sassetti CM. 2014. New TB treatments hiding in plain sight. EMBO Mol Med 7:125–126 http://dx.doi.org/10.15252/emmm.201404815.
193. Ting JP-Y, Duncan JA, Lei Y. 2010. How the noninflammasome NLRs function in the innate immune system. Science 327:286–290 http://dx.doi.org/10.1126/science.1184004. [PubMed]
194. Franchi L, Eigenbrod T, Muñoz-Planillo R, Nuñez G. 2009. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 10:241–247 http://dx.doi.org/10.1038/ni.1703.
195. Werner JL, Steele C. 2014. Innate receptors and cellular defense against pulmonary infections. J Immunol 193:3842–3850 http://dx.doi.org/10.4049/jimmunol.1400978.
196. Killick KE, Ní Cheallaigh C, O’Farrelly C, Hokamp K, MacHugh DE, Harris J. 2013. Receptor-mediated recognition of mycobacterial pathogens. Cell Microbiol 15:1484–1495 http://dx.doi.org/10.1111/cmi.12161.
197. dos Santos G, Kutuzov MA, Ridge KM. 2012. The inflammasome in lung diseases. Am J Physiol Lung Cell Mol Physiol 303:L627–L633 http://dx.doi.org/10.1152/ajplung.00225.2012.
198. Hansen JM, Golchin SA, Veyrier FJ, Domenech P, Boneca IG, Azad AK, Rajaram MVS, Schlesinger LS, Divangahi M, Reed MB, Behr MA. 2014. N-glycolylated peptidoglycan contributes to the immunogenicity but not pathogenicity of Mycobacterium tuberculosis. J Infect Dis 209:1045–1054 http://dx.doi.org/10.1093/infdis/jit622.
199. Coulombe F, Divangahi M, Veyrier F, de Léséleuc L, Gleason JL, Yang Y, Kelliher MA, Pandey AK, Sassetti CM, Reed MB, Behr MA. 2009. Increased NOD2-mediated recognition of N-glycolyl muramyl dipeptide. J Exp Med 206:1709–1716 http://dx.doi.org/10.1084/jem.20081779.
200. Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, Crespo J, Fukase K, Inamura S, Kusumoto S, Hashimoto M, Foster SJ, Moran AP, Fernandez-Luna JL, Nuñez G. 2003. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn’s disease. J Biol Chem 278:5509–5512 http://dx.doi.org/10.1074/jbc.C200673200. [PubMed]
201. Brooks MN, Rajaram MVS, Azad AK, Amer AO, Valdivia-Arenas MA, Park J-H, Núñez G, Schlesinger LS. 2011. NOD2 controls the nature of the inflammatory response and subsequent fate of Mycobacterium tuberculosis and M. bovis BCG in human macrophages. Cell Microbiol 13:402–418 http://dx.doi.org/10.1111/j.1462-5822.2010.01544.x.
202. Divangahi M, Mostowy S, Coulombe F, Kozak R, Guillot L, Veyrier F, Kobayashi KS, Flavell RA, Gros P, Behr MA. 2008. NOD2-deficient mice have impaired resistance to Mycobacterium tuberculosis infection through defective innate and adaptive immunity. J Immunol 181:7157–7165 http://dx.doi.org/10.4049/jimmunol.181.10.7157.
203. Gandotra S, Jang S, Murray PJ, Salgame P, Ehrt S. 2007. Nucleotide-binding oligomerization domain protein 2-deficient mice control infection with Mycobacterium tuberculosis. Infect Immun 75:5127–5134 http://dx.doi.org/10.1128/IAI.00458-07.
204. Juárez E, Carranza C, Hernández-Sánchez F, León-Contreras JC, Hernández-Pando R, Escobedo D, Torres M, Sada E. 2012. NOD2 enhances the innate response of alveolar macrophages to Mycobacterium tuberculosis in humans. Eur J Immunol 42:880–889 http://dx.doi.org/10.1002/eji.201142105.
205. McElvania Tekippe E, Allen IC, Hulseberg PD, Sullivan JT, McCann JR, Sandor M, Braunstein M, Ting JP-Y. 2010. Granuloma formation and host defense in chronic Mycobacterium tuberculosis infection requires PYCARD/ASC but not NLRP3 or caspase-1. PLoS One 5:e12320. doi:10.1371/journal.pone.0012320. http://dx.doi.org/10.1371/journal.pone.0012320.
206. Shah S, Bohsali A, Ahlbrand SE, Srinivasan L, Rathinam VAK, Vogel SN, Fitzgerald KA, Sutterwala FS, Briken V. 2013. Cutting edge: Mycobacterium tuberculosis but not nonvirulent mycobacteria inhibits IFN-β and AIM2 inflammasome-dependent IL-1β production via its ESX-1 secretion system. J Immunol 191:3514–3518 http://dx.doi.org/10.4049/jimmunol.1301331.
207. Saiga H, Kitada S, Shimada Y, Kamiyama N, Okuyama M, Makino M, Yamamoto M, Takeda K. 2012. Critical role of AIM2 in Mycobacterium tuberculosis infection. Int Immunol 24:637–644 http://dx.doi.org/10.1093/intimm/dxs062.
208. Glass CK, Ogawa S. 2006. Combinatorial roles of nuclear receptors in inflammation and immunity. Nat Rev Immunol 6:44–55 http://dx.doi.org/10.1038/nri1748.
209. Ahmadian M, Suh JM, Hah N, Liddle C, Atkins AR, Downes M, Evans RM. 2013. PPARγ signaling and metabolism: the good, the bad and the future. Nat Med 19:557–566 http://dx.doi.org/10.1038/nm.3159.
210. Malur A, Mccoy AJ, Arce S, Barna BP, Kavuru MS, Malur AG, Thomassen MJ. 2009. Deletion of PPAR gamma in alveolar macrophages is associated with a Th-1 pulmonary inflammatory response. J Immunol 182:5816–5822 http://dx.doi.org/10.4049/jimmunol.0803504.
211. Almeida PE, Silva AR, Maya-Monteiro CM, Töröcsik D, D’Avila H, Dezsö B, Magalhães KG, Castro-Faria-Neto HC, Nagy L, Bozza PT. 2009. Mycobacterium bovis bacillus Calmette-Guérin infection induces TLR2-dependent peroxisome proliferator-activated receptor gamma expression and activation: functions in inflammation, lipid metabolism, and pathogenesis. J Immunol 183:1337–1345 http://dx.doi.org/10.4049/jimmunol.0900365.
212. Guo H, Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466:835–840 http://dx.doi.org/10.1038/nature09267.
213. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297 http://dx.doi.org/10.1016/S0092-8674(04)00045-5.
214. He L, Hannon GJ. 2004. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531 http://dx.doi.org/10.1038/nrg1379.
215. Foster PS, Plank M, Collison A, Tay HL, Kaiko GE, Li J, Johnston SL, Hansbro PM, Kumar RK, Yang M, Mattes J. 2013. The emerging role of microRNAs in regulating immune and inflammatory responses in the lung. Immunol Rev 253:198–215 http://dx.doi.org/10.1111/imr.12058. [PubMed][CrossRef]
216. Sittka A, Schmeck B. 2013. MicroRNAs in the lung. Adv Exp Med Biol 774:121–134 http://dx.doi.org/10.1007/978-94-007-5590-1_7.
217. Kumar M, Sahu SK, Kumar R, Subuddhi A, Maji RK, Jana K, Gupta P, Raffetseder J, Lerm M, Ghosh Z, van Loo G, Beyaert R, Gupta UD, Kundu M, Basu J. 2015. MicroRNA let-7 modulates the immune response to Mycobacterium tuberculosis infection via control of A20, an inhibitor of the NF-κB pathway. Cell Host Microbe 17:345–356 http://dx.doi.org/10.1016/j.chom.2015.01.007.
218. Kumar R, Sahu SK, Kumar M, Jana K, Gupta P, Gupta UD, Kundu M, Basu J. 2015. MicroRNA 17-5p regulates autophagy in Mycobacterium tuberculosis-infected macrophages by targeting Mcl-1 and STAT3. Cell Microbiol 18:679–691. [PubMed]
219. Ma C, Li Y, Li M, Deng G, Wu X, Zeng J, Hao X, Wang X, Liu J, Cho WCS, Liu X, Wang Y. 2014. MicroRNA-124 negatively regulates TLR signaling in alveolar macrophages in response to mycobacterial infection. Mol Immunol 62:150–158 http://dx.doi.org/10.1016/j.molimm.2014.06.014.
220. Ni B, Rajaram MVS, Lafuse WP, Landes MB, Schlesinger LS. 2014. Mycobacterium tuberculosis decreases human macrophage IFN-γ responsiveness through miR-132 and miR-26a. J Immunol 193:4537–4547 http://dx.doi.org/10.4049/jimmunol.1400124.
221. Dorhoi A, Iannaccone M, Farinacci M, Faé KC, Schreiber J, Moura-Alves P, Nouailles G, Mollenkopf H-J, Oberbeck-Müller D, Jörg S, Heinemann E, Hahnke K, Löwe D, Del Nonno F, Goletti D, Capparelli R, Kaufmann SH. 2013. MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment. J Clin Invest 123:4836–4848 http://dx.doi.org/10.1172/JCI67604.
222. Liu Y, Wang X, Jiang J, Cao Z, Yang B, Cheng X. 2011. Modulation of T cell cytokine production by miR-144* with elevated expression in patients with pulmonary tuberculosis. Mol Immunol 48:1084–1090 http://dx.doi.org/10.1016/j.molimm.2011.02.001.
223. Ma F, Xu S, Liu X, Zhang Q, Xu X, Liu M, Hua M, Li N, Yao H, Cao X. 2011. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-γ. Nat Immunol 12:861–869 http://dx.doi.org/10.1038/ni.2073.
224. Yi Z, Fu Y, Ji R, Li R, Guan Z. 2012. Altered microRNA signatures in sputum of patients with active pulmonary tuberculosis. PLoS One 7:e43184. doi:10.1371/journal.pone.0043184 http://dx.doi.org/10.1371/journal.pone.0043184.
225. Singh Y, Kaul V, Mehra A, Chatterjee S, Tousif S, Dwivedi VP, Suar M, Van Kaer L, Bishai WR, Das G. 2013. Mycobacterium tuberculosis controls microRNA-99b (miR-99b) expression in infected murine dendritic cells to modulate host immunity. J Biol Chem 288:5056–5061 http://dx.doi.org/10.1074/jbc.C112.439778.
226. Wang J, Yang K, Zhou L, Minhaowu, Wu Y, Zhu M, Lai X, Chen T, Feng L, Li M, Huang C, Zhong Q, Huang X. 2013. MicroRNA-155 promotes autophagy to eliminate intracellular mycobacteria by targeting Rheb. PLoS Pathog 9:e1003697. doi:10.1371/journal.ppat.1003697 http://dx.doi.org/10.1371/journal.ppat.1003697.
227. Rajaram MVS, Ni B, Morris JD, Brooks MN, Carlson TK, Bakthavachalu B, Schoenberg DR, Torrelles JB, Schlesinger LS. 2011. Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc Natl Acad Sci USA 108:17408–17413 http://dx.doi.org/10.1073/pnas.1112660108.
228. Busch S, Auth E, Scholl F, Huenecke S, Koehl U, Suess B, Steinhilber D. 2015. 5-lipoxygenase is a direct target of miR-19a-3p and miR-125b-5p. J Immunol 194:1646–1653 http://dx.doi.org/10.4049/jimmunol.1402163.
229. Iannaccone M, Dorhoi A, Kaufmann SHE. 2014. Host-directed therapy of tuberculosis: what is in it for microRNA? Expert Opin Ther Targets 18:491–494 http://dx.doi.org/10.1517/14728222.2014.897696. [PubMed]
230. Schorey JS, Cheng Y, Singh PP, Smith VL. 2015. Exosomes and other extracellular vesicles in host-pathogen interactions. EMBO Rep 16:24–43 http://dx.doi.org/10.15252/embr.201439363.
231. Bhatnagar S, Schorey JS. 2007. Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. J Biol Chem 282:25779–25789 http://dx.doi.org/10.1074/jbc.M702277200.
232. Giri PK, Kruh NA, Dobos KM, Schorey JS. 2010. Proteomic analysis identifies highly antigenic proteins in exosomes from M. tuberculosis-infected and culture filtrate protein-treated macrophages. Proteomics 10:3190–3202 http://dx.doi.org/10.1002/pmic.200900840.
233. Singh PP, Li L, Schorey JS. 2015. Exosomal RNA from Mycobacterium tuberculosis-infected cells is functional in recipient macrophages. Traffic 16:555–571 http://dx.doi.org/10.1111/tra.12278.
234. Cheng Y, Schorey JS. 2013. Exosomes carrying mycobacterial antigens can protect mice against Mycobacterium tuberculosis infection. Eur J Immunol 43:3279–3290 http://dx.doi.org/10.1002/eji.201343727.
235. Ramachandra L, Qu Y, Wang Y, Lewis CJ, Cobb BA, Takatsu K, Boom WH, Dubyak GR, Harding CV. 2010. Mycobacterium tuberculosis synergizes with ATP to induce release of microvesicles and exosomes containing major histocompatibility complex class II molecules capable of antigen presentation. Infect Immun 78:5116–5125 http://dx.doi.org/10.1128/IAI.01089-09.
236. Lamkanfi M, Dixit VM. 2010. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8:44–54 http://dx.doi.org/10.1016/j.chom.2010.06.007.
237. Duprez L, Wirawan E, Vanden Berghe T, Vandenabeele P. 2009. Major cell death pathways at a glance. Microbes Infect 11:1050–1062 http://dx.doi.org/10.1016/j.micinf.2009.08.013.
238. Golstein P, Kroemer G. 2007. Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32:37–43 http://dx.doi.org/10.1016/j.tibs.2006.11.001.
239. Bergsbaken T, Fink SL, Cookson BT. 2009. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7:99–109 http://dx.doi.org/10.1038/nrmicro2070.
240. Divangahi M, Behar SM, Remold H. 2013. Dying to live: how the death modality of the infected macrophage affects immunity to tuberculosis. Adv Exp Med Biol 783:103–120 http://dx.doi.org/10.1007/978-1-4614-6111-1_6.
241. Srinivasan L, Ahlbrand S, Briken V. 2014. Interaction of Mycobacterium tuberculosis with host cell death pathways. Cold Spring Harb Perspect Med 4:a022459. doi:10.1101/cshperspect.a022459 http://dx.doi.org/10.1101/cshperspect.a022459. [PubMed]
242. Behar SM, Martin CJ, Booty MG, Nishimura T, Zhao X, Gan H-X, Divangahi M, Remold HG. 2011. Apoptosis is an innate defense function of macrophages against Mycobacterium tuberculosis. Mucosal Immunol 4:279–287 http://dx.doi.org/10.1038/mi.2011.3.
243. Briken V. 2013. Mycobacterium tuberculosis genes involved in regulation of host cell death. Adv Exp Med Biol 783:93–102 http://dx.doi.org/10.1007/978-1-4614-6111-1_5.
244. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. 2000. Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 192:1213–1222 http://dx.doi.org/10.1084/jem.192.9.1213.
245. Tailleux L, Neyrolles O, Honoré-Bouakline S, Perret E, Sanchez F, Abastado J-P, Lagrange PH, Gluckman JC, Rosenzwajg M, Herrmann J-L. 2003. Constrained intracellular survival of Mycobacterium tuberculosis in human dendritic cells. J Immunol 170:1939–1948 http://dx.doi.org/10.4049/jimmunol.170.4.1939.
246. Buettner M, Meinken C, Bastian M, Bhat R, Stössel E, Faller G, Cianciolo G, Ficker J, Wagner M, Röllinghoff M, Stenger S. 2005. Inverse correlation of maturity and antibacterial activity in human dendritic cells. J Immunol 174:4203–4209 http://dx.doi.org/10.4049/jimmunol.174.7.4203.
247. Madan-Lala R, Sia JK, King R, Adekambi T, Monin L, Khader SA, Pulendran B, Rengarajan J. 2014. Mycobacterium tuberculosis impairs dendritic cell functions through the serine hydrolase Hip1. J Immunol 192:4263–4272 http://dx.doi.org/10.4049/jimmunol.1303185.
248. Kopf M, Schneider C, Nobs SP. 2015. The development and function of lung-resident macrophages and dendritic cells. Nat Immunol 16:36–44 http://dx.doi.org/10.1038/ni.3052.
249. Reljic R, Di Sano C, Crawford C, Dieli F, Challacombe S, Ivanyi J. 2005. Time course of mycobacterial infection of dendritic cells in the lungs of intranasally infected mice. Tuberculosis (Edinb) 85:81–88 http://dx.doi.org/10.1016/j.tube.2004.09.006.
250. Lagranderie M, Nahori M-A, Balazuc A-M, Kiefer-Biasizzo H, Lapa e Silva JR, Milon G, Marchal G, Vargaftig BB. 2003. Dendritic cells recruited to the lung shortly after intranasal delivery of Mycobacterium bovis BCG drive the primary immune response towards a type 1 cytokine production. Immunology 108:352–364 http://dx.doi.org/10.1046/j.1365-2567.2003.01609.x.
251. Henderson RA, Watkins SC, Flynn JL. 1997. Activation of human dendritic cells following infection with Mycobacterium tuberculosis. J Immunol 159:635–643. [PubMed]
252. Giacomini E, Iona E, Ferroni L, Miettinen M, Fattorini L, Orefici G, Julkunen I, Coccia EM. 2001. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J Immunol 166:7033–7041 http://dx.doi.org/10.4049/jimmunol.166.12.7033.
253. Cooper AM, Solache A, Khader SA. 2007. Interleukin-12 and tuberculosis: an old story revisited. Curr Opin Immunol 19:441–447 http://dx.doi.org/10.1016/j.coi.2007.07.004.
254. Hickman SP, Chan J, Salgame P. 2002. Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J Immunol 168:4636–4642 http://dx.doi.org/10.4049/jimmunol.168.9.4636.
255. Humphreys IR, Stewart GR, Turner DJ, Patel J, Karamanou D, Snelgrove RJ, Young DB. 2006. A role for dendritic cells in the dissemination of mycobacterial infection. Microbes Infect 8:1339–1346 http://dx.doi.org/10.1016/j.micinf.2005.12.023.
256. Khader SA, Partida-Sánchez S, Bell G, Jelley-Gibbs DM, Swain S, Pearl JE, Ghilardi N, Desauvage FJ, Lund FE, Cooper AM. 2006. Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J Exp Med 203:1805–1815 http://dx.doi.org/10.1084/jem.20052545.
257. Rodriguez A, Regnault A, Kleijmeer M, Ricciardi-Castagnoli P, Amigorena S. 1999. Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat Cell Biol 1:362–368 http://dx.doi.org/10.1038/14058.
258. Schaible UE, Winau F, Sieling PA, Fischer K, Collins HL, Hagens K, Modlin RL, Brinkmann V, Kaufmann SHE. 2003. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 9:1039–1046 http://dx.doi.org/10.1038/nm906.
259. Kaufmann SHE, Schaible UE. 2003. A dangerous liaison between two major killers: Mycobacterium tuberculosis and HIV target dendritic cells through DC-SIGN. J Exp Med 197:1–5 http://dx.doi.org/10.1084/jem.20021964.
260. van Kooyk Y, Appelmelk B, Geijtenbeek TBH. 2003. A fatal attraction: Mycobacterium tuberculosis and HIV-1 target DC-SIGN to escape immune surveillance. Trends Mol Med 9:153–159 http://dx.doi.org/10.1016/S1471-4914(03)00027-3.
261. Campbell KS, Hasegawa J. 2013. Natural killer cell biology: an update and future directions. J Allergy Clin Immunol 132:536–544 http://dx.doi.org/10.1016/j.jaci.2013.07.006. [PubMed]
262. Cooper MA, Fehniger TA, Caligiuri MA. 2001. The biology of human natural killer-cell subsets. Trends Immunol 22:633–640 http://dx.doi.org/10.1016/S1471-4906(01)02060-9.
263. Moretta L. 2010. Dissecting CD56dim human NK cells. Blood 116:3689–3691 http://dx.doi.org/10.1182/blood-2010-09-303057.
264. Kruse PH, Matta J, Ugolini S, Vivier E. 2014. Natural cytotoxicity receptors and their ligands. Immunol Cell Biol 92:221–229 http://dx.doi.org/10.1038/icb.2013.98. [PubMed]
265. Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S. 2013. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol 31:227–258 http://dx.doi.org/10.1146/annurev-immunol-020711-075005.
266. Adib-Conquy M, Scott-Algara D, Cavaillon J-M, Souza-Fonseca-Guimaraes F. 2014. TLR-mediated activation of NK cells and their role in bacterial/viral immune responses in mammals. Immunol Cell Biol 92:256–262 http://dx.doi.org/10.1038/icb.2013.99. [PubMed]
267. Souza-Fonseca-Guimaraes F, Adib-Conquy M, Cavaillon J-M. 2012. Natural killer (NK) cells in antibacterial innate immunity: angels or devils? Mol Med 18:270–285 http://dx.doi.org/10.2119/molmed.2011.00201.
268. Junqueira-Kipnis AP, Kipnis A, Jamieson A, Juarrero MG, Diefenbach A, Raulet DH, Turner J, Orme IM. 2003. NK cells respond to pulmonary infection with Mycobacterium tuberculosis, but play a minimal role in protection. J Immunol 171:6039–6045 http://dx.doi.org/10.4049/jimmunol.171.11.6039.
269. Feng CG, Kaviratne M, Rothfuchs AG, Cheever A, Hieny S, Young HA, Wynn TA, Sher A. 2006. NK cell-derived IFN-gamma differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis. J Immunol 177:7086–7093 http://dx.doi.org/10.4049/jimmunol.177.10.7086.
270. Vitale M, Della Chiesa M, Carlomagno S, Pende D, Aricò M, Moretta L, Moretta A. 2005. NK-dependent DC maturation is mediated by TNFα and IFNγ released upon engagement of the NKp30 triggering receptor. Blood 106:566–571 http://dx.doi.org/10.1182/blood-2004-10-4035.
271. Schierloh P, Yokobori N, Alemán M, Musella RM, Beigier-Bompadre M, Saab MA, Alves L, Abbate E, de la Barrera SS, Sasiain MC. 2005. Increased susceptibility to apoptosis of CD56dimCD16+ NK cells induces the enrichment of IFN-gamma-producing CD56bright cells in tuberculous pleurisy. J Immunol 175:6852–6860 http://dx.doi.org/10.4049/jimmunol.175.10.6852.
272. Wu YE, Zhang SW, Peng WG, Li KS, Li K, Jiang JK, Lin JH, Cai YM. 2009. Changes in lymphocyte subsets in the peripheral blood of patients with active pulmonary tuberculosis. J Int Med Res 37:1742–1749 http://dx.doi.org/10.1177/147323000903700610.
273. Ratcliffe LT, Lukey PT, MacKenzie CR, Ress SR. 1994. Reduced NK activity correlates with active disease in HIV- patients with multidrug-resistant pulmonary tuberculosis. Clin Exp Immunol 97:373–379 http://dx.doi.org/10.1111/j.1365-2249.1994.tb06097.x.
274. Ratcliffe LT, Mackenzie CR, Lukey PT, Ress SR. 1992. Reduced natural killer cell activity in multi-drug resistant pulmonary tuberculosis. Scand J Immunol Suppl 36(s1):167–170 http://dx.doi.org/10.1111/j.1365-3083.1992.tb01643.x.
275. Wang F, Hou H, Wu S, Tang Q, Huang M, Yin B, Huang J, Liu W, Mao L, Lu Y, Sun Z. 2015. Tim-3 pathway affects NK cell impairment in patients with active tuberculosis. Cytokine 76:270–279 http://dx.doi.org/10.1016/j.cyto.2015.05.012. [PubMed]
276. Zufferey C, Germano S, Dutta B, Ritz N, Curtis N. 2013. The contribution of non-conventional T cells and NK cells in the mycobacterial-specific IFNγ response in Bacille Calmette-Guérin (BCG)-immunized infants. PLoS One 8:e77334. doi:10.1371/journal.pone.0077334. http://dx.doi.org/10.1371/journal.pone.0077334.
277. Kleinnijenhuis J, Quintin J, Preijers F, Joosten LAB, Jacobs C, Xavier RJ, van der Meer JWM, van Crevel R, Netea MG. 2014. BCG-induced trained immunity in NK cells: role for non-specific protection to infection. Clin Immunol 155:213–219 http://dx.doi.org/10.1016/j.clim.2014.10.005.
278. Kemp K, Hviid L, Kharazmi A, Kemp M. 1997. Interferon-γ production by human T cells and natural killer cells in vitro in response to antigens from the two intracellular pathogens Mycobacterium tuberculosis and Leishmania major. Scand J Immunol 46:495–499 http://dx.doi.org/10.1046/j.1365-3083.1997.d01-154.x. [PubMed]
279. Dhiman R, Indramohan M, Barnes PF, Nayak RC, Paidipally P, Rao LVM, Vankayalapati R. 2009. IL-22 produced by human NK cells inhibits growth of Mycobacterium tuberculosis by enhancing phagolysosomal fusion. J Immunol 183:6639–6645 http://dx.doi.org/10.4049/jimmunol.0902587.
280. Denis M. 1994. Interleukin-12 (IL-12) augments cytolytic activity of natural killer cells toward Mycobacterium tuberculosis-infected human monocytes. Cell Immunol 156:529–536 http://dx.doi.org/10.1006/cimm.1994.1196.
281. Katz P, Yeager H Jr, Whalen G, Evans M, Swartz RP, Roecklein J. 1990. Natural killer cell-mediated lysis of Mycobacterium-avium complex-infected monocytes. J Clin Immunol 10:71–77 http://dx.doi.org/10.1007/BF00917500.
282. Molloy A, Meyn PA, Smith KD, Kaplan G. 1993. Recognition and destruction of Bacillus Calmette-Guerin-infected human monocytes. J Exp Med 177:1691–1698 http://dx.doi.org/10.1084/jem.177.6.1691.
283. Brill KJ, Li Q, Larkin R, Canaday DH, Kaplan DR, Boom WH, Silver RF. 2001. Human natural killer cells mediate killing of intracellular Mycobacterium tuberculosis H37Rv via granule-independent mechanisms. Infect Immun 69:1755–1765 http://dx.doi.org/10.1128/IAI.69.3.1755-1765.2001.
284. Bermudez LE, Wu M, Young LS. 1995. Interleukin-12-stimulated natural killer cells can activate human macrophages to inhibit growth of Mycobacterium avium. Infect Immun 63:4099–4104.
285. Esin S, Batoni G, Källenius G, Gaines H, Campa M, Svenson SB, Andersson R, Wigzell H. 1996. Proliferation of distinct human T cell subsets in response to live, killed or soluble extracts of Mycobacterium tuberculosis and Myco. avium. Clin Exp Immunol 104:419–425 http://dx.doi.org/10.1046/j.1365-2249.1996.d01-691.x.
286. Esin S, Batoni G, Pardini M, Favilli F, Bottai D, Maisetta G, Florio W, Vanacore R, Wigzell H, Campa M. 2004. Functional characterization of human natural killer cells responding to Mycobacterium bovis bacille Calmette-Guérin. Immunology 112:143–152 http://dx.doi.org/10.1111/j.1365-2567.2004.01858.x.
287. Batoni G, Esin S, Favilli F, Pardini M, Bottai D, Maisetta G, Florio W, Campa M. 2005. Human CD56bright and CD56dim natural killer cell subsets respond differentially to direct stimulation with Mycobacterium bovis bacillus Calmette-Guérin. Scand J Immunol 62:498–506 http://dx.doi.org/10.1111/j.1365-3083.2005.01692.x.
288. Portevin D, Young D. 2013. Natural killer cell cytokine response to M. bovis BCG is associated with inhibited proliferation, increased apoptosis and ultimate depletion of NKp44(+)CD56(bright) cells. PLoS One 8:e68864. doi:10.1371/journal.pone.0068864 http://dx.doi.org/10.1371/journal.pone.0068864.
289. Portevin D, Via LE, Eum S, Young D. 2012. Natural killer cells are recruited during pulmonary tuberculosis and their ex vivo responses to mycobacteria vary between healthy human donors in association with KIR haplotype. Cell Microbiol 14:1734–1744 http://dx.doi.org/10.1111/j.1462-5822.2012.01834.x.
290. Sun JC, Lopez-Verges S, Kim CC, DeRisi JL, Lanier LL. 2011. NK cells and immune “memory”. J Immunol 186:1891–1897 http://dx.doi.org/10.4049/jimmunol.1003035.
291. Esin S, Batoni G, Counoupas C, Stringaro A, Brancatisano FL, Colone M, Maisetta G, Florio W, Arancia G, Campa M. 2008. Direct binding of human NK cell natural cytotoxicity receptor NKp44 to the surfaces of mycobacteria and other bacteria. Infect Immun 76:1719–1727 http://dx.doi.org/10.1128/IAI.00870-07.
292. Esin S, Counoupas C, Aulicino A, Brancatisano FL, Maisetta G, Bottai D, Di Luca M, Florio W, Campa M, Batoni G. 2013. Interaction of Mycobacterium tuberculosis cell wall components with the human natural killer cell receptors NKp44 and Toll-like receptor 2. Scand J Immunol 77:460–469 http://dx.doi.org/10.1111/sji.12052.
293. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G. 2002. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 195:327–333 http://dx.doi.org/10.1084/jem.20010938.
294. Zhang R, Zheng X, Li B, Wei H, Tian Z. 2006. Human NK cells positively regulate gammadelta T cells in response to Mycobacterium tuberculosis. J Immunol 176:2610–2616 http://dx.doi.org/10.4049/jimmunol.176.4.2610.
295. Boom WH, Balaji KN, Nayak R, Tsukaguchi K, Chervenak KA. 1994. Characterization of a 10- to 14-kilodalton protease-sensitive Mycobacterium tuberculosis H37Ra antigen that stimulates human gamma delta T cells. Infect Immun 62:5511–5518. [PubMed]
296. Vankayalapati R, Klucar P, Wizel B, Weis SE, Samten B, Safi H, Shams H, Barnes PF. 2004. NK cells regulate CD8+ T cell effector function in response to an intracellular pathogen. J Immunol 172:130–137 http://dx.doi.org/10.4049/jimmunol.172.1.130. [PubMed]
297. Roy S, Barnes PF, Garg A, Wu S, Cosman D, Vankayalapati R. 2008. NK cells lyse T regulatory cells that expand in response to an intracellular pathogen. J Immunol 180:1729–1736 http://dx.doi.org/10.4049/jimmunol.180.3.1729.
298. Barrios-Payán J, Aguilar-León D, Lascurain-Ledezma R, Hernández-Pando R. 2006. Neutrophil participation in early control and immune activation during experimental pulmonary tuberculosis. Gac Med Mex 142:273–281. (In Spanish.) [PubMed]
299. Pedrosa J, Saunders BM, Appelberg R, Orme IM, Silva MT, Cooper AM. 2000. Neutrophils play a protective nonphagocytic role in systemic Mycobacterium tuberculosis infection of mice. Infect Immun 68:577–583 http://dx.doi.org/10.1128/IAI.68.2.577-583.2000.
300. Fulton SA, Reba SM, Martin TD, Boom WH. 2002. Neutrophil-mediated mycobacteriocidal immunity in the lung during Mycobacterium bovis BCG infection in C57BL/6 mice. Infect Immun 70:5322–5327 http://dx.doi.org/10.1128/IAI.70.9.5322-5327.2002.
301. Seiler P, Aichele P, Raupach B, Odermatt B, Steinhoff U, Kaufmann SHE. 2000. Rapid neutrophil response controls fast-replicating intracellular bacteria but not slow-replicating Mycobacterium tuberculosis. J Infect Dis 181:671–680 http://dx.doi.org/10.1086/315278. [PubMed]
302. Zhang X, Majlessi L, Deriaud E, Leclerc C, Lo-Man R. 2009. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 31:761–771 http://dx.doi.org/10.1016/j.immuni.2009.09.016.
303. Barnes PF, Leedom JM, Chan LS, Wong SF, Shah J, Vachon LA, Overturf GD, Modlin RL. 1988. Predictors of short-term prognosis in patients with pulmonary tuberculosis. J Infect Dis 158:366–371 http://dx.doi.org/10.1093/infdis/158.2.366. [PubMed]
304. Antony VB, Sahn SA, Harada RN, Repine JE. 1983. Lung repair and granuloma formation. Tubercle bacilli stimulated neutrophils release chemotactic factors for monocytes. Chest 83(Suppl):95S–96S.
305. Abadie V, Badell E, Douillard P, Ensergueix D, Leenen PJM, Tanguy M, Fiette L, Saeland S, Gicquel B, Winter N. 2005. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 106:1843–1850 http://dx.doi.org/10.1182/blood-2005-03-1281.
306. Silva MT. 2010. Neutrophils and macrophages work in concert as inducers and effectors of adaptive immunity against extracellular and intracellular microbial pathogens. J Leukoc Biol 87:805–813 http://dx.doi.org/10.1189/jlb.1109767.
307. Lemon WS, Feldman WH. 1943. Experimental tuberculosis pleural effusion. Am Rev Tuberc 48:177–183.
308. Cruz A, Fraga AG, Fountain JJ, Rangel-Moreno J, Torrado E, Saraiva M, Pereira DR, Randall TD, Pedrosa J, Cooper AM, Castro AG. 2010. Pathological role of interleukin 17 in mice subjected to repeated BCG vaccination after infection with Mycobacterium tuberculosis. J Exp Med 207:1609–1616 http://dx.doi.org/10.1084/jem.20100265.
309. de Vallière S, Abate G, Blazevic A, Heuertz RM, Hoft DF. 2005. Enhancement of innate and cell-mediated immunity by antimycobacterial antibodies. Infect Immun 73:6711–6720 http://dx.doi.org/10.1128/IAI.73.10.6711-6720.2005.
310. Sugawara I, Udagawa T, Yamada H. 2004. Rat neutrophils prevent the development of tuberculosis. Infect Immun 72:1804–1806 http://dx.doi.org/10.1128/IAI.72.3.1804-1806.2004.
311. Shigenaga T, Dannenberg AM, Lowrie DB, Said W, Urist MJ, Abbey H, Schofield BH, Mounts P, Sugisaki K. 2001. Immune responses in tuberculosis: antibodies and CD4-CD8 lymphocytes with vascular adhesion molecules and cytokines (chemokines) cause a rapid antigen-specific cell infiltration at sites of bacillus Calmette-Guérin reinfection. Immunology 102:466–479 http://dx.doi.org/10.1046/j.1365-2567.2001.01195.x.
312. Lyons MJ, Yoshimura T, McMurray DN. 2004. Interleukin (IL)-8 (CXCL8) induces cytokine expression and superoxide formation by guinea pig neutrophils infected with Mycobacterium tuberculosis. Tuberculosis (Edinb) 84:283–292 http://dx.doi.org/10.1016/j.tube.2003.09.003.
313. Kisich KO, Higgins M, Diamond G, Heifets L. 2002. Tumor necrosis factor alpha stimulates killing of Mycobacterium tuberculosis by human neutrophils. Infect Immun 70:4591–4599 http://dx.doi.org/10.1128/IAI.70.8.4591-4599.2002.
314. Jones GS, Amirault HJ, Andersen BR. 1990. Killing of Mycobacterium tuberculosis by neutrophils: a nonoxidative process. J Infect Dis 162:700–704 http://dx.doi.org/10.1093/infdis/162.3.700. [PubMed]
315. Denis M. 1991. Human neutrophils, activated with cytokines or not, do not kill virulent Mycobacterium tuberculosis. J Infect Dis 163:919–920 http://dx.doi.org/10.1093/infdis/163.4.919.
316. Aston C, Rom WN, Talbot AT, Reibman J. 1998. Early inhibition of mycobacterial growth by human alveolar macrophages is not due to nitric oxide. Am J Respir Crit Care Med 157:1943–1950 http://dx.doi.org/10.1164/ajrccm.157.6.9705028. [PubMed]
317. Neufert C, Pai RK, Noss EH, Berger M, Boom WH, Harding CV. 2001. Mycobacterium tuberculosis 19-kDa lipoprotein promotes neutrophil activation. J Immunol 167:1542–1549 http://dx.doi.org/10.4049/jimmunol.167.3.1542.
318. Yang C-T, Cambier CJ, Davis JM, Hall CJ, Crosier PS, Ramakrishnan L. 2012. Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe 12:301–312 http://dx.doi.org/10.1016/j.chom.2012.07.009.
319. Mattila JT, Maiello P, Sun T, Via LE, Flynn JL. 2015. Granzyme B-expressing neutrophils correlate with bacteria load in granulomas from Mycobacterium tuberculosis-infected cynomolgus macaques. Cell Microbiol 17:1085–1097. [PubMed]
320. Mantovani A, Cassatella MA, Costantini C, Jaillon S. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11:519–531 http://dx.doi.org/10.1038/nri3024.
321. Sawant KV, McMurray DN. 2007. Guinea pig neutrophils infected with Mycobacterium tuberculosis produce cytokines which activate alveolar macrophages in noncontact cultures. Infect Immun 75:1870–1877 http://dx.doi.org/10.1128/IAI.00858-06.
322. De Santo C, Arscott R, Booth S, Karydis I, Jones M, Asher R, Salio M, Middleton M, Cerundolo V. 2010. Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat Immunol 11:1039–1046 http://dx.doi.org/10.1038/ni.1942.
323. Doz E, Lombard R, Carreras F, Buzoni-Gatel D, Winter N. 2013. Mycobacteria-infected dendritic cells attract neutrophils that produce IL-10 and specifically shut down Th17 CD4 T cells through their IL-10 receptor. J Immunol 191:3818–3826 http://dx.doi.org/10.4049/jimmunol.1300527.
324. D’Avila H, Roque NR, Cardoso RM, Castro-Faria-Neto HC, Melo RCN, Bozza PT. 2008. Neutrophils recruited to the site of Mycobacterium bovis BCG infection undergo apoptosis and modulate lipid body biogenesis and prostaglandin E production by macrophages. Cell Microbiol 10:2589–2604 http://dx.doi.org/10.1111/j.1462-5822.2008.01233.x.
325. Perskvist N, Long M, Stendahl O, Zheng L. 2002. Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol 168:6358–6365 http://dx.doi.org/10.4049/jimmunol.168.12.6358.
326. Persson YAZ, Blomgran-Julinder R, Rahman S, Zheng L, Stendahl O. 2008. Mycobacterium tuberculosis-induced apoptotic neutrophils trigger a proinflammatory response in macrophages through release of heat shock protein 72, acting in synergy with the bacteria. Microbes Infect 10:233–240 http://dx.doi.org/10.1016/j.micinf.2007.11.007.
327. Petrofsky M, Bermudez LE. 1999. Neutrophils from Mycobacterium avium-infected mice produce TNF-alpha, IL-12, and IL-1 beta and have a putative role in early host response. Clin Immunol 91:354–358 http://dx.doi.org/10.1006/clim.1999.4709. [PubMed]
328. Seiler P, Aichele P, Bandermann S, Hauser AE, Lu B, Gerard NP, Gerard C, Ehlers S, Mollenkopf HJ, Kaufmann SHE. 2003. Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur J Immunol 33:2676–2686 http://dx.doi.org/10.1002/eji.200323956.
329. Morel C, Badell E, Abadie V, Robledo M, Setterblad N, Gluckman JC, Gicquel B, Boudaly S, Winter N. 2008. Mycobacterium bovis BCG-infected neutrophils and dendritic cells cooperate to induce specific T cell responses in humans and mice. Eur J Immunol 38:437–447 http://dx.doi.org/10.1002/eji.200737905.
330. Alemán M, de la Barrera S, Schierloh P, Yokobori N, Baldini M, Musella R, Abbate E, Sasiain M. 2007. Spontaneous or Mycobacterium tuberculosis-induced apoptotic neutrophils exert opposite effects on the dendritic cell-mediated immune response. Eur J Immunol 37:1524–1537 http://dx.doi.org/10.1002/eji.200636771.
331. Blomgran R, Ernst JD. 2011. Lung neutrophils facilitate activation of naive antigen-specific CD4+ T cells during Mycobacterium tuberculosis infection. J Immunol 186:7110–7119 http://dx.doi.org/10.4049/jimmunol.1100001.
332. Yang C-W, Strong BSI, Miller MJ, Unanue ER. 2010. Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J Immunol 185:2927–2934 http://dx.doi.org/10.4049/jimmunol.1001289.
333. Eum SY, Kong J-H, Hong M-S, Lee Y-J, Kim JH, Hwang S-H, Cho S-N, Via LE, Barry CE III. 2010. Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 137:122–128 http://dx.doi.org/10.1378/chest.09-0903.
334. Condos R, Rom WN, Liu YM, Schluger NW. 1998. Local immune responses correlate with presentation and outcome in tuberculosis. Am J Respir Crit Care Med 157:729–735 http://dx.doi.org/10.1164/ajrccm.157.3.9705044.
335. Martineau AR, Timms PM, Bothamley GH, Hanifa Y, Islam K, Claxton AP, Packe GE, Moore-Gillon JC, Darmalingam M, Davidson RN, Milburn HJ, Baker LV, Barker RD, Woodward NJ, Venton TR, Barnes KE, Mullett CJ, Coussens AK, Rutterford CM, Mein CA, Davies GR, Wilkinson RJ, Nikolayevskyy V, Drobniewski FA, Eldridge SM, Griffiths CJ. 2011. High-dose vitamin D(3) during intensive-phase antimicrobial treatment of pulmonary tuberculosis: a double-blind randomised controlled trial. Lancet 377:242–250 http://dx.doi.org/10.1016/S0140-6736(10)61889-2.
336. Eruslanov EB, Lyadova IV, Kondratieva TK, Majorov KB, Scheglov IV, Orlova MO, Apt AS. 2005. Neutrophil responses to Mycobacterium tuberculosis infection in genetically susceptible and resistant mice. Infect Immun 73:1744–1753 http://dx.doi.org/10.1128/IAI.73.3.1744-1753.2005.
337. Keller C, Hoffmann R, Lang R, Brandau S, Hermann C, Ehlers S. 2006. Genetically determined susceptibility to tuberculosis in mice causally involves accelerated and enhanced recruitment of granulocytes. Infect Immun 74:4295–4309 http://dx.doi.org/10.1128/IAI.00057-06.
338. Ramakrishnan L. 2012. Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 12:352–366.
339. Tsai MC, Chakravarty S, Zhu G, Xu J, Tanaka K, Koch C, Tufariello J, Flynn J, Chan J. 2006. Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell Microbiol 8:218–232 http://dx.doi.org/10.1111/j.1462-5822.2005.00612.x.
340. Guirado E, Schlesinger LS. 2013. Modeling the Mycobacterium tuberculosis granuloma: the critical battlefield in host immunity and disease. Front Immunol 4:98 http://dx.doi.org/10.3389/fimmu.2013.00098.
341. Kaplan G, Post FA, Moreira AL, Wainwright H, Kreiswirth BN, Tanverdi M, Mathema B, Ramaswamy SV, Walther G, Steyn LM, Barry CE III, Bekker L-G. 2003. Mycobacterium tuberculosis growth at the cavity surface: a microenvironment with failed immunity. Infect Immun 71:7099–7108 http://dx.doi.org/10.1128/IAI.71.12.7099-7108.2003.
342. Orme IM, Basaraba RJ. 2014. The formation of the granuloma in tuberculosis infection. Semin Immunol 26:601–609 http://dx.doi.org/10.1016/j.smim.2014.09.009.
343. Russell DG. 2007. Who puts the tubercle in tuberculosis? Nat Rev Microbiol 5:39–47 http://dx.doi.org/10.1038/nrmicro1538.
344. Silva Miranda M, Breiman A, Allain S, Deknuydt F, Altare F. 2012. The tuberculous granuloma: an unsuccessful host defence mechanism providing a safety shelter for the bacteria? Clin Dev Immunol 2012:139127 http://dx.doi.org/10.1155/2012/139127.
345. Paige C, Bishai WR. 2010. Penitentiary or penthouse condo: the tuberculous granuloma from the microbe’s point of view. Cell Microbiol 12:301–309 http://dx.doi.org/10.1111/j.1462-5822.2009.01424.x.
346. Heitmann L, Abad Dar M, Schreiber T, Erdmann H, Behrends J, Mckenzie AN, Brombacher F, Ehlers S, Hölscher C. 2014. The IL-13/IL-4Rα axis is involved in tuberculosis-associated pathology. J Pathol 234:338–350 http://dx.doi.org/10.1002/path.4399. [PubMed]
347. Cyktor JC, Carruthers B, Kominsky RA, Beamer GL, Stromberg P, Turner J. 2013. IL-10 inhibits mature fibrotic granuloma formation during Mycobacterium tuberculosis infection. J Immunol 190:2778–2790 http://dx.doi.org/10.4049/jimmunol.1202722.
348. Pan H, Yan B-S, Rojas M, Shebzukhov YV, Zhou H, Kobzik L, Higgins DE, Daly MJ, Bloom BR, Kramnik I. 2005. Ipr1 gene mediates innate immunity to tuberculosis. Nature 434:767–772 http://dx.doi.org/10.1038/nature03419.
349. Manabe YC, Kesavan AK, Lopez-Molina J, Hatem CL, Brooks M, Fujiwara R, Hochstein K, Pitt MLM, Tufariello J, Chan J, McMurray DN, Bishai WR, Dannenberg AM Jr, Mendez S. 2008. The aerosol rabbit model of TB latency, reactivation and immune reconstitution inflammatory syndrome. Tuberculosis (Edinb) 88:187–196 http://dx.doi.org/10.1016/j.tube.2007.10.006.
350. Scanga CA, Flynn JL. 2014. Modeling tuberculosis in nonhuman primates. Cold Spring Harb Perspect Med 4:a018564. doi:10.1101/cshperspect.a018564 http://dx.doi.org/10.1101/cshperspect.a018564.
351. McMurray D. 1994. Guinea pig model of tuberculosis, p 135–147. In Bloom B (ed), Tuberculosis. ASM Press, Washington, DC. http://dx.doi.org/10.1128/9781555818357.ch9
352. Guirado E, Mbawuike U, Keiser TL, Arcos J, Azad AK, Wang S-H, Schlesinger LS. 2015. Characterization of host and microbial determinants in individuals with latent tuberculosis infection using a human granuloma model. MBio 6:e02537–14. doi:10.1128/mBio.02537-14.
353. Puissegur M-P, Botanch C, Duteyrat J-L, Delsol G, Caratero C, Altare F. 2004. An in vitro dual model of mycobacterial granulomas to investigate the molecular interactions between mycobacteria and human host cells. Cell Microbiol 6:423–433 http://dx.doi.org/10.1111/j.1462-5822.2004.00371.x.
354. Marino S, Linderman JJ, Kirschner DE. 2011. A multifaceted approach to modeling the immune response in tuberculosis. Wiley Interdiscip Rev Syst Biol Med 3:479–489 http://dx.doi.org/10.1002/wsbm.131. [PubMed]
355. Marino S, El-Kebir M, Kirschner D. 2011. A hybrid multi-compartment model of granuloma formation and T cell priming in tuberculosis. J Theor Biol 280:50–62 http://dx.doi.org/10.1016/j.jtbi.2011.03.022.
356. Israel HL, Hetherington HW, Ord JG. 1941. A study of tuberculosis among students of nursing. JAMA 117:839–844 http://dx.doi.org/10.1001/jama.1941.02820360021007.
357. Morrison J, Pai M, Hopewell PC. 2008. Tuberculosis and latent tuberculosis infection in close contacts of people with pulmonary tuberculosis in low-income and middle-income countries: a systematic review and meta-analysis. Lancet Infect Dis 8:359–368 http://dx.doi.org/10.1016/S1473-3099(08)70071-9.
358. van Crevel R, van der Ven-Jongekrijg J, Netea MG, de Lange W, Kullberg BJ, van der Meer JW. 1999. Disease-specific ex vivo stimulation of whole blood for cytokine production: applications in the study of tuberculosis. J Immunol Methods 222:145–153 http://dx.doi.org/10.1016/S0022-1759(98)00192-6.
359. Wilkinson RJ, Llewelyn M, Toossi Z, Patel P, Pasvol G, Lalvani A, Wright D, Latif M, Davidson RN. 2000. Influence of vitamin D deficiency and vitamin D receptor polymorphisms on tuberculosis among Gujarati Asians in west London: a case-control study. Lancet 355:618–621 http://dx.doi.org/10.1016/S0140-6736(99)02301-6.
360. Azad AK, Sadee W, Schlesinger LS. 2012. Innate immune gene polymorphisms in tuberculosis. Infect Immun 80:3343–3359 http://dx.doi.org/10.1128/IAI.00443-12.
361. Alemán M, Schierloh P, de la Barrera SS, Musella RM, Saab MA, Baldini M, Abbate E, Sasiain MC. 2004. Mycobacterium tuberculosis triggers apoptosis in peripheral neutrophils involving toll-like receptor 2 and p38 mitogen protein kinase in tuberculosis patients. Infect Immun 72:5150–5158 http://dx.doi.org/10.1128/IAI.72.9.5150-5158.2004.
362. Majeed M, Perskvist N, Ernst JD, Orselius K, Stendahl O. 1998. Roles of calcium and annexins in phagocytosis and elimination of an attenuated strain of Mycobacterium tuberculosis in human neutrophils. Microb Pathog 24:309–320 http://dx.doi.org/10.1006/mpat.1997.0200.
363. Martineau AR, Newton SM, Wilkinson KA, Kampmann B, Hall BM, Nawroly N, Packe GE, Davidson RN, Griffiths CJ, Wilkinson RJ. 2007. Neutrophil-mediated innate immune resistance to mycobacteria. J Clin Invest 117:1988–1994 http://dx.doi.org/10.1172/JCI31097. [PubMed]
364. Dong Y, Cirimotich CM, Pike A, Chandra R, Dimopoulos G. 2012. Anopheles NF-κB-regulated splicing factors direct pathogen-specific repertoires of the hypervariable pattern recognition receptor AgDscam. Cell Host Microbe 12:521–530 http://dx.doi.org/10.1016/j.chom.2012.09.004.
365. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS. 2007. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3:e26. doi:10.1371/journal.ppat.0030026 http://dx.doi.org/10.1371/journal.ppat.0030026. [PubMed]
366. Leclerc V, Reichhart J-M. 2004. The immune response of Drosophila melanogaster. Immunol Rev 198:59–71 http://dx.doi.org/10.1111/j.0105-2896.2004.0130.x.
367. Netea MG. 2013. Training innate immunity: the changing concept of immunological memory in innate host defence. Eur J Clin Invest 43:881–884 http://dx.doi.org/10.1111/eci.12132.
368. Kleinnijenhuis J, Quintin J, Preijers F, Joosten LAB, Ifrim DC, Saeed S, Jacobs C, van Loenhout J, de Jong D, Stunnenberg HG, Xavier RJ, van der Meer JWM, van Crevel R, Netea MG. 2012. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci USA 109:17537–17542 http://dx.doi.org/10.1073/pnas.1202870109.
369. Dieli F, Troye-Blomberg M, Ivanyi J, Fournié JJ, Bonneville M, Peyrat MA, Sireci G, Salerno A. 2000. Vgamma9/Vdelta2 T lymphocytes reduce the viability of intracellular Mycobacterium tuberculosis. Eur J Immunol 30:1512–1519 http://dx.doi.org/10.1002/(SICI)1521-4141(200005)30:5<1512::AID-IMMU1512>3.0.CO;2-3.
370. Spencer CT, Abate G, Sakala IG, Xia M, Truscott SM, Eickhoff CS, Linn R, Blazevic A, Metkar SS, Peng G, Froelich CJ, Hoft DF. 2013. Granzyme A produced by γ(9)δ(2) T cells induces human macrophages to inhibit growth of an intracellular pathogen. PLoS Pathog 9:e1003119. doi:10.1371/journal.ppat.1003119. http://dx.doi.org/10.1371/journal.ppat.1003119. [PubMed]
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/content/journal/microbiolspec/10.1128/microbiolspec.TBTB2-0010-2016
2016-12-09
2017-09-19

Abstract:

Tuberculosis remains one of the greatest threats to human health. The causative bacterium, , is acquired by the respiratory route. It is exquisitely adapted to humans and is a prototypic intracellular pathogen of macrophages, with alveolar macrophages being the primary conduit of infection and disease. However, bacilli interact with and are affected by several soluble and cellular components of the innate immune system which dictate the outcome of primary infection, most commonly a latently infected healthy human host, in whom the bacteria are held in check by the host immune response within the confines of tissue granuloma, the host histopathologic hallmark. Such individuals can develop active TB later in life with impairment in the immune system. In contrast, in a minority of infected individuals, the early host immune response fails to control bacterial growth, and progressive granulomatous disease develops, facilitating spread of the bacilli via infectious aerosols. The molecular details of the -host innate immune system interaction continue to be elucidated, particularly those occurring within the lung. However, it is clear that a number of complex processes are involved at the different stages of infection that may benefit either the bacterium or the host. In this article, we describe a contemporary view of the molecular events underlying the interaction between and a variety of cellular and soluble components and processes of the innate immune system.

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Figures

Image of FIGURE 1
FIGURE 1

Schematic of the lung and the role of pulmonary innate immune cells during infection. From left to right: branching of the airways, culminating in the alveolar sacs and the alveolus. Also depicted are the cells in the alveolus. Abbreviations: AEC I and II, type I and II alveolar epithelial cell; AM, alveolar macrophage; DC, dendritic cell; IM, interstitial macrophage; IVM, intravascular macrophage.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0010-2016
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Image of FIGURE 2
FIGURE 2

Macrophage receptors known to engage () or its components and the downstream effects of receptor engagement on cytokine production, phagosome-lysosome fusion, and inflammation. Engagement of different receptors results in a macrophage response that can either promote or limit host immunity to infection.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0010-2016
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Image of FIGURE 3
FIGURE 3

() fate upon macrophage infection. Following phagocytosis, resides within a modified phagosome which may allow mycobacterial components to enter the cytosol in an ESX-1-dependent manner. The phagosome is also connected to the early endosomal network because membrane compartments can both fuse and bud from the phagosome, allowing exposure to important nutrients such as iron as well as removal of mycobacterial components. Endosomes containing mycobacterial components can fuse with multivesicular bodies (MVBs), leading to their incorporation into intraluminal vesicles, and upon MVB fusion with the plasma membrane, they can be released within exosomes (indicated as red circles in the figure). The phagosome has limited fusion with lysosomes, but with activation by IFN-γ or antibiotic treatment the -containing phagosome may undergo autophagosome formation and following lysosome fusion can limit growth, a process known as autophagy. There are also data suggesting that can escape into the cytosol, although this has been observed in only a limited number of studies.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0010-2016
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Image of FIGURE 4
FIGURE 4

Responses of innate immune cells to (), BCG, or their products, demonstrating both the beneficial and detrimental roles these cells have on controlling an infection.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0010-2016
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