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The Immune Interaction between HIV-1 Infection and

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  • Authors: Elsa Du Bruyn1, Robert John Wilkinson2
  • Editors: William R. Jacobs Jr.4, Helen McShane5, Valerie Mizrahi6, Ian M. Orme7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Clinical Infectious Diseases Research Initiative, Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Observatory 7925, Republic of South Africa; 2: Clinical Infectious Diseases Research Initiative, Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Observatory 7925, Republic of South Africa; 3: Department of Medicine, Imperial College London, London W2 1PG and The Francis Crick Institute Mill Hill Laboratory, London NW7 1AA, United Kingdom; 4: Howard Hughes Medical Institute, Albert Einstein School of Medicine, Bronx, NY 10461; 5: University of Oxford, Oxford OX3 7DQ, United Kingdom; 6: University of Cape Town, Rondebosch 7701, South Africa; 7: Colorado State University, Fort Collins, CO 80523
  • Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0012-2016
  • Received 31 January 2016 Accepted 13 February 2016 Published 16 December 2016
  • E. du Bruyn, elsa.dubruyn@uct.ac.za
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  • Abstract:

    The modulation of tuberculosis (TB)-induced immunopathology caused by human immunodeficiency virus (HIV)-1 coinfection remains incompletely understood but underlies the change seen in the natural history, presentation, and prognosis of TB in such patients. The deleterious combination of these two pathogens has been dubbed a “deadly syndemic,” with each favoring the replication of the other and thereby contributing to accelerated disease morbidity and mortality. HIV-1 is the best-recognized risk factor for the development of active TB and accounts for 13% of cases globally. The advent of combination antiretroviral therapy (ART) has considerably mitigated this risk. Rapid roll-out of ART globally and the recent recommendation by the World Health Organization (WHO) to initiate ART for everyone living with HIV at any CD4 cell count should lead to further reductions in HIV-1-associated TB incidence because susceptibility to TB is inversely proportional to CD4 count. However, it is important to note that even after successful ART, patients with HIV-1 are still at increased risk for TB. Indeed, in settings of high TB incidence, the occurrence of TB often remains the first presentation of, and thereby the entry into, HIV care. As advantageous as ART-induced immune recovery is, it may also give rise to immunopathology, especially in the lower-CD4-count strata in the form of the immune reconstitution inflammatory syndrome. TB-immune reconstitution inflammatory syndrome will continue to impact the HIV-TB syndemic.

  • Citation: Du Bruyn E, Wilkinson R. 2016. The Immune Interaction between HIV-1 Infection and . Microbiol Spectrum 4(6):TBTB2-0012-2016. doi:10.1128/microbiolspec.TBTB2-0012-2016.

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References

1. WHO. 2015. Global tuberculosis report 2015. WHO, Geneva, Switzerland. http://www.who.int/tb/publications/global_report/en/. [PubMed]
2. Sonnenberg P, Glynn JR, Fielding K, Murray J, Godfrey-Faussett P, Shearer S. 2005. How soon after infection with HIV does the risk of tuberculosis start to increase? A retrospective cohort study in South African gold miners. J Infect Dis 191:150–158. http://dx.doi.org/10.1086/426827.
3. UNAIDS. UNAIDS fact sheet 2015: the Joint United Nations Programme on HIV/AIDS 2015. http://www.unaids.org/sites/default/files/media_asset/20150901_FactSheet_2015_en.pdf.
4. WHO. 2015. Guideline on When to Start Antiretroviral Therapy and on Pre-Exposure Prophylaxis for HIV. World Health Organization, Geneva, Switzerland.
5. Lawn SD, Harries AD, Williams BG, Chaisson RE, Losina E, De Cock KM, Wood R. 2011. Antiretroviral therapy and the control of HIV-associated tuberculosis. Will ART do it? Int J Tuberc Lung Dis 15:571–581. http://dx.doi.org/10.5588/ijtld.10.0483.
6. Gupta A, Wood R, Kaplan R, Bekker LG, Lawn SD. 2012. Tuberculosis incidence rates during 8 years of follow-up of an antiretroviral treatment cohort in South Africa: comparison with rates in the community. PLoS One 7:e34156. doi:10.1371/journal.pone.0034156 http://dx.doi.org/10.1371/journal.pone.0034156.
7. Selwyn PA, Hartel D, Lewis VA, Schoenbaum EE, Vermund SH, Klein RS, Walker AT, Friedland GH. 1989. A prospective study of the risk of tuberculosis among intravenous drug users with human immunodeficiency virus infection. N Engl J Med 320:545–550 http://dx.doi.org/10.1056/NEJM198903023200901.
8. Girardi E, Raviglione MC, Antonucci G, Godfrey-Faussett P, Ippolito G. 2000. Impact of the HIV epidemic on the spread of other diseases: the case of tuberculosis. AIDS 14(Suppl 3):S47–S56. [PubMed]
9. Houben RM, Crampin AC, Ndhlovu R, Sonnenberg P, Godfrey-Faussett P, Haas WH, Engelmann G, Lombard CJ, Wilkinson D, Bruchfeld J, Lockman S, Tappero J, Glynn JR. 2011. Human immunodeficiency virus associated tuberculosis more often due to recent infection than reactivation of latent infection. Int J Tuberc Lung Dis 15:24–31. [PubMed]
10. Charalambous S, Grant AD, Moloi V, Warren R, Day JH, van Helden P, Hayes RJ, Fielding KL, De Cock KM, Chaisson RE, Churchyard GJ. 2008. Contribution of reinfection to recurrent tuberculosis in South African gold miners. Int J Tuberc Lung Dis 12:942–948. [PubMed]
11. Crampin AC, Mwaungulu JN, Mwaungulu FD, Mwafulirwa DT, Munthali K, Floyd S, Fine PE, Glynn JR. 2010. Recurrent TB: relapse orreinfection? The effect of HIV in a general population cohort in Malawi. AIDS 24:417–426 http://dx.doi.org/10.1097/QAD.0b013e32832f51cf.
12. Narayanan S, Swaminathan S, Supply P, Shanmugam S, Narendran G, Hari L, Ramachandran R, Locht C, Jawahar MS, Narayanan PR. 2010. Impact of HIV infection on the recurrence of tuberculosis in South India. J Infect Dis 201:691–703 http://dx.doi.org/10.1086/650528. [PubMed]
13. Lawn SD, Myer L, Edwards D, Bekker LG, Wood R. 2009. Short-term and long-term risk of tuberculosis associated with CD4 cell recovery during antiretroviral therapy in South Africa. AIDS 23:1717–1725 http://dx.doi.org/10.1097/QAD.0b013e32832d3b6d.
14. Lawn SD, Badri M, Wood R. 2005. Tuberculosis among HIV-infected patients receiving HAART: long term incidence and risk factors in a South African cohort. AIDS 19:2109–2116 http://dx.doi.org/10.1097/01.aids.0000194808.20035.c1.
15. Wood R, Maartens G, Lombard CJ. 2000. Risk factors for developing tuberculosis in HIV-1-infected adults from communities with a low or very high incidence of tuberculosis. J Acquir Immune Defic Syndr 23:75–80 http://dx.doi.org/10.1097/00126334-200001010-00010.
16. Chang CA, Meloni ST, Eisen G, Chaplin B, Akande P, Okonkwo P, Rawizza HE, Tchetgen Tchetgen E, Kanki PJ. 2015. Tuberculosis incidence and risk factors among human immunodeficiency virus (HIV)-infected adults receiving antiretroviral therapy in a large HIV program in Nigeria. Open Forum Infect Dis 2:ofv154. doi:10.1093/ofid/ofv154 http://dx.doi.org/10.1093/ofid/ofv154.
17. Martín-Echevarria E, Serrano-Villar S, Sainz T, Moreno A, Casado JL, Dronda F, Elías MJ, Navas E, Zapata MR, Moreno S. 2014. Development of tuberculosis in human immunodeficiency virus infected patients receiving antiretroviral therapy. Int J Tuberc Lung Dis 18:1080–1084 http://dx.doi.org/10.5588/ijtld.13.0757.
18. Akolo C, Adetifa I, Shepperd S, Volmink J. 2010. Treatment of latent tuberculosis infection in HIV infected persons. Cochrane Database Syst Rev (1):CD000171. [PubMed]
19. Rangaka MX, Wilkinson RJ, Boulle A, Glynn JR, Fielding K, van Cutsem G, Wilkinson KA, Goliath R, Mathee S, Goemaere E, Maartens G. 2014. Isoniazid plus antiretroviral therapy to prevent tuberculosis: a randomised double-blind, placebo-controlled trial. Lancet 384:682–690 http://dx.doi.org/10.1016/S0140-6736(14)60162-8.
20. Briggs MA, Emerson C, Modi S, Taylor NK, Date A. 2015. Use of isoniazid preventive therapy for tuberculosis prophylaxis among people living with HIV/AIDS: a review of the literature. J Acquir Immune Defic Syndr 68(Suppl 3):S297–S305 http://dx.doi.org/10.1097/QAI.0000000000000497.
21. Lagrange PH, Herrmann JL. 2008. Diagnosing latent tuberculosis infection in the HIV era. Open Respir Med J 2:52–59 http://dx.doi.org/10.2174/1874306400802010052.
22. Wejse C, Patsche CB, Kühle A, Bamba FJ, Mendes MS, Lemvik G, Gomes VF, Rudolf F. 2015. Impact of HIV-1, HIV-2, and HIV-1+2 dual infection on the outcome of tuberculosis. Int J Infect Dis 32:128–134 http://dx.doi.org/10.1016/j.ijid.2014.12.015.
23. Marlink R, Kanki P, Thior I, Travers K, Eisen G, Siby T, Traore I, Hsieh C, Dia M, Gueye E, et. 1994. Reduced rate of disease development after HIV-2 infection as compared to HIV-1. Science 265:1587–1590 http://dx.doi.org/10.1126/science.7915856.
24. Campbell-Yesufu OT, Gandhi RT. 2011. Update on human immunodeficiency virus (HIV)-2 infection. Clin Infect Dis 52:780–787 http://dx.doi.org/10.1093/cid/ciq248.
25. Ekouevi DK, Tchounga BK, Coffie PA, Tegbe J, Anderson AM, Gottlieb GS, Vitoria M, Dabis F, Eholie SP. 2014. Antiretroviral therapy response among HIV-2 infected patients: a systematic review. BMC Infect Dis 14:461. doi:10.1186/1471-2334-14-461 http://dx.doi.org/10.1186/1471-2334-14-461. [PubMed]
26. Girard MP, Osmanov S, Assossou OM, Kieny MP. 2011. Human immunodeficiency virus (HIV) immunopathogenesis and vaccine development: a review. Vaccine 29:6191–6218 http://dx.doi.org/10.1016/j.vaccine.2011.06.085.
27. Dezzutti CS, Hladik F. 2013. Use of human mucosal tissue to study HIV-1 pathogenesis and evaluate HIV-1 prevention modalities. Curr HIV/AIDS Rep 10:12–20 http://dx.doi.org/10.1007/s11904-012-0148-2.
28. Cicala C, Arthos J, Fauci AS. 2011. HIV-1 envelope, integrins and co-receptor use in mucosal transmission of HIV. J Transl Med 9(Suppl 1):S2 http://dx.doi.org/10.1186/1479-5876-9-S1-S2.
29. Monteiro P, Gosselin A, Wacleche VS, El-Far M, Said EA, Kared H, Grandvaux N, Boulassel MR, Routy JP, Ancuta P. 2011. Memory CCR6+CD4+ T cells are preferential targets for productive HIV type 1 infection regardless of their expression of integrin β7. J Immunol 186:4618–4630 http://dx.doi.org/10.4049/jimmunol.1004151.
30. Ruibal-Ares BH, Belmonte L, Baré PC, Parodi CM, Massud I, de Bracco MM. 2004. HIV-1 infection and chemokine receptor modulation. Curr HIV Res 2:39–50 http://dx.doi.org/10.2174/1570162043484997.
31. Hazenberg MD, Otto SA, Hamann D, Roos MT, Schuitemaker H, de Boer RJ, Miedema F. 2003. Depletion of naive CD4 T cells by CXCR4-using HIV-1 variants occurs mainly through increased T-cell death and activation. AIDS 17:1419–1424 http://dx.doi.org/10.1097/00002030-200307040-00001.
32. Okoye AA, Picker LJ. 2013. CD4(+) T-cell depletion in HIV infection: mechanisms of immunological failure. Immunol Rev 254:54–64 http://dx.doi.org/10.1111/imr.12066.
33. Krebs SJ, Ananworanich J. 2015. Immune activation during acute HIV infection and the impact of early antiretroviral therapy. Curr Opin HIV AIDS 11:163–172. [PubMed]
34. Brenchley JM, Price DA, Douek DC. 2006. HIV disease: fallout from a mucosal catastrophe? Nat Immunol 7:235–239 http://dx.doi.org/10.1038/ni1316.
35. Koziel H, Kim S, Reardon C, Li X, Garland R, Pinkston P, Kornfeld H. 1999. Enhanced in vivo human immunodeficiency virus-1 replication in the lungs of human immunodeficiency virus-infected persons with Pneumocystis carinii pneumonia. Am J Respir Crit Care Med 160:2048–2055 http://dx.doi.org/10.1164/ajrccm.160.6.9902099.
36. Jambo KC, Banda DH, Kankwatira AM, Sukumar N, Allain TJ, Heyderman RS, Russell DG, Mwandumba HC. 2014. Small alveolar macrophages are infected preferentially by HIV and exhibit impaired phagocytic function. Mucosal Immunol 7:1116–1126 http://dx.doi.org/10.1038/mi.2013.127.
37. Azzam R, Kedzierska K, Leeansyah E, Chan H, Doischer D, Gorry PR, Cunningham AL, Crowe SM, Jaworowski A. 2006. Impaired complement-mediated phagocytosis by HIV type-1-infected human monocyte-derived macrophages involves a cAMP-dependent mechanism. AIDS Res Hum Retroviruses 22:619–629 http://dx.doi.org/10.1089/aid.2006.22.619.
38. Leeansyah E, Wines BD, Crowe SM, Jaworowski A. 2007. The mechanism underlying defective Fcgamma receptor-mediated phagocytosis by HIV-1-infected human monocyte-derived macrophages. J Immunol 178:1096–1104 http://dx.doi.org/10.4049/jimmunol.178.2.1096.
39. Patel NR, Zhu J, Tachado SD, Zhang J, Wan Z, Saukkonen J, Koziel H. 2007. HIV impairs TNF-alpha mediated macrophage apoptotic response to Mycobacterium tuberculosis. J Immunol 179:6973–6980 http://dx.doi.org/10.4049/jimmunol.179.10.6973.
40. Biggs BA, Hewish M, Kent S, Hayes K, Crowe SM. 1995. HIV-1 infection of human macrophages impairs phagocytosis and killing of Toxoplasma gondii. J Immunol 154:6132–6139. [PubMed]
41. Noursadeghi M, Tsang J, Miller RF, Straschewski S, Kellam P, Chain BM, Katz DR. 2009. Genome-wide innate immune responses in HIV-1-infected macrophages are preserved despite attenuation of the NF-kappa B activation pathway. J Immunol 182:319–328 http://dx.doi.org/10.4049/jimmunol.182.1.319.
42. Harding CV, Boom WH. 2010. Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat Rev Microbiol 8:296–307 http://dx.doi.org/10.1038/nrmicro2321.
43. Podinovskaia M, Lee W, Caldwell S, Russell DG. 2013. Infection of macrophages with Mycobacterium tuberculosis induces global modifications to phagosomal function. Cell Microbiol 15:843–859 http://dx.doi.org/10.1111/cmi.12092.
44. Mwandumba HC, Russell DG, Nyirenda MH, Anderson J, White SA, Molyneux ME, Squire SB. 2004. Mycobacterium tuberculosis resides in nonacidified vacuoles in endocytically competent alveolar macrophages from patients with tuberculosis and HIV infection. J Immunol 172:4592–4598 http://dx.doi.org/10.4049/jimmunol.172.7.4592.
45. Parandhaman DK, Narayanan S. 2014. Cell death paradigms in the pathogenesis of Mycobacterium tuberculosis infection. Front Cell Infect Microbiol 4:31 http://dx.doi.org/10.3389/fcimb.2014.00031.
46. Behar SM, Martin CJ, Booty MG, Nishimura T, Zhao X, Gan HX, 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.
47. Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG. 1998. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol 161:2636–2641. [PubMed]
48. Geleziunas R, Xu W, Takeda K, Ichijo H, Greene WC. 2001. HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infected host cell. Nature 410:834–838 http://dx.doi.org/10.1038/35071111.
49. Mehto S, Antony C, Khan N, Arya R, Selvakumar A, Tiwari BK, Vashishta M, Singh Y, Jameel S, Natarajan K. 2015. Mycobacterium tuberculosis and human immunodeficiency virus type 1 cooperatively modulate macrophage apoptosis via toll like receptor 2 and calcium homeostasis. PLoS One 10:e0131767. doi:10.1371/journal.pone.0131767. http://dx.doi.org/10.1371/journal.pone.0131767.
50. Brigino E, Haraguchi S, Koutsonikolis A, Cianciolo GJ, Owens U, Good RA, Day NK. 1997. Interleukin 10 is induced by recombinant HIV-1 Nef protein involving the calcium/calmodulin-dependent phosphodiesterase signal transduction pathway. Proc Natl Acad Sci USA 94:3178–3182 http://dx.doi.org/10.1073/pnas.94.7.3178.
51. Bennasser Y, Bahraoui E. 2002. HIV-1 Tat protein induces interleukin-10 in human peripheral blood monocytes: involvement of protein kinase C-betaII and -delta. FASEB J 16:546–554 http://dx.doi.org/10.1096/fj.01-0775com.
52. Patel NR, Swan K, Li X, Tachado SD, Koziel H. 2009. Impaired M. tuberculosis-mediated apoptosis in alveolar macrophages from HIV+ persons: potential role of IL-10 and BCL-3. J Leukoc Biol 86:53–60 http://dx.doi.org/10.1189/jlb.0908574.
53. Anandaiah A, Sinha S, Bole M, Sharma SK, Kumar N, Luthra K, Li X, Zhou X, Nelson B, Han X, Tachado SD, Patel NR, Koziel H. 2013. Vitamin D rescues impaired Mycobacterium tuberculosis-mediated tumor necrosis factor release in macrophages of HIV-seropositive individuals through an enhanced Toll-like receptor signaling pathway in vitro. Infect Immun 81:2–10 http://dx.doi.org/10.1128/IAI.00666-12.
54. Campbell GR, Spector SA. 2012. Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog 8:e1002689. doi:10.1371/journal.ppat.1002689 http://dx.doi.org/10.1371/journal.ppat.1002689.
55. Campbell GR, Spector SA. 2012. Toll-like receptor 8 ligands activate a vitamin D mediated autophagic response that inhibits human immunodeficiency virus type 1. PLoS Pathog 8:e1003017. doi:10.1371/journal.ppat.1003017 http://dx.doi.org/10.1371/journal.ppat.1003017.
56. Eklund D, Persson HL, Larsson M, Welin A, Idh J, Paues J, Fransson SG, Stendahl O, Schön T, Lerm M. 2013. Vitamin D enhances IL-1β secretion and restricts growth of Mycobacterium tuberculosis in macrophages from TB patients. Int J Mycobacteriol 2:18–25 http://dx.doi.org/10.1016/j.ijmyco.2012.11.001.
57. Martineau AR, Wilkinson KA, Newton SM, Floto RA, Norman AW, Skolimowska K, Davidson RN, Sørensen OE, Kampmann B, Griffiths CJ, Wilkinson RJ. 2007. IFN-gamma- and TNF-independent vitamin D-inducible human suppression of mycobacteria: the role of cathelicidin LL-37. J Immunol 178:7190–7198 http://dx.doi.org/10.4049/jimmunol.178.11.7190.
58. Tachado SD, Zhang J, Zhu J, Patel N, Koziel H. 2005. HIV impairs TNF-alpha release in response to Toll-like receptor 4 stimulation in human macrophages in vitro. Am J Respir Cell Mol Biol 33:610–621 http://dx.doi.org/10.1165/rcmb.2004-0341OC. [PubMed]
59. Song CH, Lee JS, Lee SH, Lim K, Kim HJ, Park JK, Paik TH, Jo EK. 2003. Role of mitogen-activated protein kinase pathways in the production of tumor necrosis factor-alpha, interleukin-10, and monocyte chemotactic protein-1 by Mycobacterium tuberculosis H37Rv-infected human monocytes. J Clin Immunol 23:194–201 http://dx.doi.org/10.1023/A:1023309928879.
60. Tomlinson GS, Bell LC, Walker NF, Tsang J, Brown JS, Breen R, Lipman M, Katz DR, Miller RF, Chain BM, Elkington PT, Noursadeghi M. 2014. HIV-1 infection of macrophages dysregulates innate immune responses to Mycobacterium tuberculosis by inhibition of interleukin-10. J Infect Dis 209:1055–1065 http://dx.doi.org/10.1093/infdis/jit621.
61. Chetty S, Porichis F, Govender P, Zupkosky J, Ghebremichael M, Pillay M, Walker BD, Ndung’u T, Kaufmann DE, Kasprowicz VO. 2014. Tuberculosis distorts the inhibitory impact of interleukin-10 in HIV infection. AIDS 28:2671–2676 http://dx.doi.org/10.1097/QAD.0000000000000437.
62. Ramaseri Sunder S, Hanumanth SR, Nagaraju RT, Venkata SKN, Suryadevara NC, Pydi SS, Gaddam S, Jonnalagada S, Valluri VL. 2012. IL-10 high producing genotype predisposes HIV infected individuals to TB infection. Hum Immunol 73:605–611 http://dx.doi.org/10.1016/j.humimm.2012.03.012.
63. Maddocks S, Scandurra GM, Nourse C, Bye C, Williams RB, Slobedman B, Cunningham AL, Britton WJ. 2009. Gene expression in HIV-1/Mycobacterium tuberculosis co-infected macrophages is dominated by M. tuberculosis. Tuberculosis (Edinb) 89:285–293 http://dx.doi.org/10.1016/j.tube.2009.05.003.
64. Tsang J, Chain BM, Miller RF, Webb BL, Barclay W, Towers GJ, Katz DR, Noursadeghi M. 2009. HIV-1 infection of macrophages is dependent on evasion of innate immune cellular activation. AIDS 23:2255–2263 http://dx.doi.org/10.1097/QAD.0b013e328331a4ce.
65. Ranjbar S, Boshoff HI, Mulder A, Siddiqi N, Rubin EJ, Goldfeld AE. 2009. HIV-1 replication is differentially regulated by distinct clinical strains of Mycobacterium tuberculosis. PLoS One 4:e6116. doi:10.1371/journal.pone.0006116 http://dx.doi.org/10.1371/journal.pone.0006116.
66. Toossi Z, Wu M, Liu S, Hirsch CS, Walrath J, van Ham M, Silver RF. 2014. Role of protease inhibitor 9 in survival and replication of Mycobacterium tuberculosis in mononuclear phagocytes from HIV-1-infected patients. AIDS 28:679–687 http://dx.doi.org/10.1097/QAD.0000000000000192.
67. Pathak S, Wentzel-Larsen T, Asjö B. 2010. Effects of in vitro HIV-1 infection on mycobacterial growth in peripheral blood monocyte-derived macrophages. Infect Immun 78:4022–4032 http://dx.doi.org/10.1128/IAI.00106-10.
68. Meylan PR, Munis JR, Richman DD, Kornbluth RS. 1992. Concurrent human immunodeficiency virus and mycobacterial infection of macrophages in vitro does not reveal any reciprocal effect. J Infect Dis 165:80–86 http://dx.doi.org/10.1093/infdis/165.1.80.
69. Ryndak MB, Singh KK, Peng Z, Zolla-Pazner S, Li H, Meng L, Laal S. 2014. Transcriptional profiling of Mycobacterium tuberculosis replicating ex vivo in blood from HIV- and HIV+ subjects. PLoS One 9:e94939. doi:10.1371/journal.pone.0094939 http://dx.doi.org/10.1371/journal.pone.0094939.
70. Hoshino Y, Tse DB, Rochford G, Prabhakar S, Hoshino S, Chitkara N, Kuwabara K, Ching E, Raju B, Gold JA, Borkowsky W, Rom WN, Pine R, Weiden M. 2004. Mycobacterium tuberculosis-induced CXCR4 and chemokine expression leads to preferential X4 HIV-1 replication in human macrophages. J Immunol 172:6251–6258 http://dx.doi.org/10.4049/jimmunol.172.10.6251.
71. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Di Marzio P, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, Landau NR. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661–666 http://dx.doi.org/10.1038/381661a0. [PubMed]
72. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, Cayanan C, Maddon PJ, Koup RA, Moore JP, Paxton WA. 1996. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667–673 http://dx.doi.org/10.1038/381667a0.
73. Collins KR, Quiñones-Mateu ME, Wu M, Luzze H, Johnson JL, Hirsch C, Toossi Z, Arts EJ. 2002. Human immunodeficiency virus type 1 (HIV-1) quasispecies at the sites of Mycobacterium tuberculosis infection contribute to systemic HIV-1 heterogeneity. J Virol 76:1697–1706 http://dx.doi.org/10.1128/JVI.76.4.1697-1706.2002.
74. Toossi Z, Johnson JL, Kanost RA, Wu M, Luzze H, Peters P, Okwera A, Joloba M, Mugyenyi P, Mugerwa RD, Aung H, Ellner JJ, Hirsch CS. 2001. Increased replication of HIV-1 at sites of Mycobacterium tuberculosis infection: potential mechanisms of viral activation. J Acquir Immune Defic Syndr 28:1–8 http://dx.doi.org/10.1097/00042560-200109010-00001.
75. Mayanja-Kizza H, Wajja A, Wu M, Peters P, Nalugwa G, Mubiru F, Aung H, Vanham G, Hirsch C, Whalen C, Ellner J, Toossi Z. 2001. Activation of beta-chemokines and CCR5 in persons infected with human immunodeficiency virus type 1 and tuberculosis. J Infect Dis 183:1801–1804 http://dx.doi.org/10.1086/320724.
76. Juffermans NP, Paxton WA, Dekkers PE, Verbon A, de Jonge E, Speelman P, van Deventer SJ, van der Poll T. 2000. Up-regulation of HIV coreceptors CXCR4 and CCR5 on CD4(+) T cells during human endotoxemia and after stimulation with (myco)bacterial antigens: the role of cytokines. Blood 96:2649–2654. [PubMed]
77. Rosas-Taraco AG, Arce-Mendoza AY, Caballero-Olín G, Salinas-Carmona MC. 2006. Mycobacterium tuberculosis upregulates coreceptors CCR5 and CXCR4 while HIV modulates CD14 favoring concurrent infection. AIDS Res Hum Retroviruses 22:45–51 http://dx.doi.org/10.1089/aid.2006.22.45.
78. Wolday D, Tegbaru B, Kassu A, Messele T, Coutinho R, van Baarle D, Miedema F. 2005. Expression of chemokine receptors CCR5 and CXCR4 on CD4+ T cells and plasma chemokine levels during treatment of active tuberculosis in HIV-1-coinfected patients. J Acquir Immune Defic Syndr 39:265–271 http://dx.doi.org/10.1097/01.qai.0000163027.47147.2e.
79. Imperiali FG, Zaninoni A, La Maestra L, Tarsia P, Blasi F, Barcellini W. 2001. Increased Mycobacterium tuberculosis growth in HIV-1-infected human macrophages: role of tumour necrosis factor-alpha. Clin Exp Immunol 123:435–442 http://dx.doi.org/10.1046/j.1365-2249.2001.01481.x.
80. Lederman MM, Georges DL, Kusner DJ, Mudido P, Giam CZ, Toossi Z. 1994. Mycobacterium tuberculosis and its purified protein derivative activate expression of the human immunodeficiency virus. J Acquir Immune Defic Syndr 7:727–733. [PubMed]
81. Mancino G, Placido R, Bach S, Mariani F, Montesano C, Ercoli L, Zembala M, Colizzi V. 1997. Infection of human monocytes with Mycobacterium tuberculosis enhances human immunodeficiency virus type 1 replication and transmission to T cells. J Infect Dis 175:1531–1535 http://dx.doi.org/10.1086/516494.
82. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, Wilkinson KA, Banchereau R, Skinner J, Wilkinson RJ, Quinn C, Blankenship D, Dhawan R, Cush JJ, Mejias A, Ramilo O, Kon OM, Pascual V, Banchereau J, Chaussabel D, O’Garra A. 2010. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466:973–977 http://dx.doi.org/10.1038/nature09247.
83. Kerkhoff AD, Wood R, Lowe DM, Vogt M, Lawn SD. 2013. Blood neutrophil counts in HIV-infected patients with pulmonary tuberculosis: association with sputum mycobacterial load. PLoS One 8:e67956. doi:10.1371/journal.pone.0067956 http://dx.doi.org/10.1371/journal.pone.0067956.
84. Lowe DM, Bandara AK, Packe GE, Barker RD, Wilkinson RJ, Griffiths CJ, Martineau AR. 2013. Neutrophilia independently predicts death in tuberculosis. Eur Respir J 42:1752–1757 http://dx.doi.org/10.1183/09031936.00140913.
85. 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]
86. Crump JA, Ramadhani HO, Morrissey AB, Saganda W, Mwako MS, Yang LY, Chow SC, Njau BN, Mushi GS, Maro VP, Reller LB, Bartlett JA. 2012. Bacteremic disseminated tuberculosis in sub-Saharan Africa: a prospective cohort study. Clin Infect Dis 55:242–250 http://dx.doi.org/10.1093/cid/cis409.
87. Bouza E, Díaz-López MD, Moreno S, Bernaldo de Quirós JC, Vicente T, Berenguer J. 1993. Mycobacterium tuberculosis bacteremia in patients with and without human immunodeficiency virus infection. Arch Intern Med 153:496–500 http://dx.doi.org/10.1001/archinte.1993.00410040062009.
88. Lowe DM, Bangani N, Goliath R, Kampmann B, Wilkinson KA, Wilkinson RJ, Martineau AR. 2015. Effect of antiretroviral therapy on HIV-mediated impairment of the neutrophil antimycobacterial response. Ann Am Thorac Soc 12:1627–1637.
89. Baldelli F, Preziosi R, Francisci D, Tascini C, Bistoni F, Nicoletti I. 2000. Programmed granulocyte neutrophil death in patients at different stages of HIV infection. AIDS 14:1067–1069 http://dx.doi.org/10.1097/00002030-200005260-00024.
90. Pitrak DL, Tsai HC, Mullane KM, Sutton SH, Stevens P. 1996. Accelerated neutrophil apoptosis in the acquired immunodeficiency syndrome. J Clin Invest 98:2714–2719 http://dx.doi.org/10.1172/JCI119096.
91. Mastroianni CM, Mengoni F, Lichtner M, D’Agostino C, d’Ettorre G, Forcina G, Marzi M, Russo G, Massetti AP, Vullo V. 2000. Ex vivo and in vitro effect of human immunodeficiency virus protease inhibitors on neutrophil apoptosis. J Infect Dis 182:1536–1539 http://dx.doi.org/10.1086/315858.
92. 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.
93. Alemán M, García A, Saab MA, De La Barrera SS, Finiasz M, Abbate E, Sasiain MC. 2002. Mycobacterium tuberculosis-induced activation accelerates apoptosis in peripheral blood neutrophils from patients with active tuberculosis. Am J Respir Cell Mol Biol 27:583–592 http://dx.doi.org/10.1165/rcmb.2002-0038OC.
94. Persson A, Blomgran-Julinder R, Eklund D, Lundström C, Stendahl O. 2009. Induction of apoptosis in human neutrophils by Mycobacterium tuberculosis is dependent on mature bacterial lipoproteins. Microb Pathog 47:143–150 http://dx.doi.org/10.1016/j.micpath.2009.05.006.
95. 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.
96. Hedlund S, Persson A, Vujic A, Che KF, Stendahl O, Larsson M. 2010. Dendritic cell activation by sensing Mycobacterium tuberculosis-induced apoptotic neutrophils via DC-SIGN. Hum Immunol 71:535–540 http://dx.doi.org/10.1016/j.humimm.2010.02.022. [PubMed]
97. Heath WR, Carbone FR. 2001. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol 19:47–64 http://dx.doi.org/10.1146/annurev.immunol.19.1.47.
98. 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.
99. Pacanowski J, Kahi S, Baillet M, Lebon P, Deveau C, Goujard C, Meyer L, Oksenhendler E, Sinet M, Hosmalin A. 2001. Reduced blood CD123+ (lymphoid) and CD11c+ (myeloid) dendritic cell numbers in primary HIV-1 infection. Blood 98:3016–3021 http://dx.doi.org/10.1182/blood.V98.10.3016. [PubMed]
100. Chehimi J, Campbell DE, Azzoni L, Bacheller D, Papasavvas E, Jerandi G, Mounzer K, Kostman J, Trinchieri G, Montaner LJ. 2002. Persistent decreases in blood plasmacytoid dendritic cell number and function despite effective highly active antiretroviral therapy and increased blood myeloid dendritic cells in HIV-infected individuals. J Immunol 168:4796–4801 http://dx.doi.org/10.4049/jimmunol.168.9.4796.
101. Smed-Sörensen A, Loré K, Vasudevan J, Louder MK, Andersson J, Mascola JR, Spetz AL, Koup RA. 2005. Differential susceptibility to human immunodeficiency virus type 1 infection of myeloid and plasmacytoid dendritic cells. J Virol 79:8861–8869 http://dx.doi.org/10.1128/JVI.79.14.8861-8869.2005.
102. Turville SG, Santos JJ, Frank I, Cameron PU, Wilkinson J, Miranda-Saksena M, Dable J, Stössel H, Romani N, Piatak M Jr, Lifson JD, Pope M, Cunningham AL. 2004. Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 103:2170–2179 http://dx.doi.org/10.1182/blood-2003-09-3129.
103. Izquierdo-Useros N, Naranjo-Gómez M, Erkizia I, Puertas MC, Borràs FE, Blanco J, Martinez-Picado J. 2010. HIV and mature dendritic cells: Trojan exosomes riding the Trojan horse? PLoS Pathog 6:e1000740. doi:10.1371/journal.ppat.1000740 http://dx.doi.org/10.1371/journal.ppat.1000740. [PubMed]
104. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, Mammano F, Schwartz O. 2005. Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J Virol 79:5386–5399 http://dx.doi.org/10.1128/JVI.79.9.5386-5399.2005.
105. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587–597 http://dx.doi.org/10.1016/S0092-8674(00)80694-7.
106. Gurney KB, Elliott J, Nassanian H, Song C, Soilleux E, McGowan I, Anton PA, Lee B. 2005. Binding and transfer of human immunodeficiency virus by DC-SIGN+ cells in human rectal mucosa. J Virol 79:5762–5773 http://dx.doi.org/10.1128/JVI.79.9.5762-5773.2005.
107. Wu L, Bashirova AA, Martin TD, Villamide L, Mehlhop E, Chertov AO, Unutmaz D, Pope M, Carrington M, KewalRamani VN. 2002. Rhesus macaque dendritic cells efficiently transmit primate lentiviruses independently of DC-SIGN. Proc Natl Acad Sci USA 99:1568–1573 http://dx.doi.org/10.1073/pnas.032654399.
108. Gummuluru S, Rogel M, Stamatatos L, Emerman M. 2003. Binding of human immunodeficiency virus type 1 to immature dendritic cells can occur independently of DC-SIGN and mannose binding C-type lectin receptors via a cholesterol-dependent pathway. J Virol 77:12865–12874 http://dx.doi.org/10.1128/JVI.77.23.12865-12874.2003.
109. Pustylnikov S, Dave RS, Khan ZK, Porkolab V, Rashad AA, Hutchinson M, Fieschi F, Chaiken I, Jain P. 2016. Short communication: inhibition of DC-SIGN-mediated HIV-1 infection by complementary actions of dendritic cell receptor antagonists and env-targeting virus inactivators. AIDS Res Hum Retroviruses 32:93–100 http://dx.doi.org/10.1089/aid.2015.0184.
110. Geijtenbeek TB, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, 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.
111. Nigou J, Zelle-Rieser C, Gilleron M, Thurnher M, Puzo G. 2001. Mannosylated lipoarabinomannans inhibit IL-12 production by human dendritic cells: evidence for a negative signal delivered through the mannose receptor. J Immunol 166:7477–7485 http://dx.doi.org/10.4049/jimmunol.166.12.7477.
112. Driessen NN, Ummels R, Maaskant JJ, Gurcha SS, Besra GS, Ainge GD, Larsen DS, Painter GF, Vandenbroucke-Grauls CM, Geurtsen J, Appelmelk BJ. 2009. Role of phosphatidylinositol mannosides in the interactionbetween mycobacteria and DC-SIGN. Infect Immun 77:4538–4547 http://dx.doi.org/10.1128/IAI.01256-08.
113. Schaefer M, Reiling N, Fessler C, Stephani J, Taniuchi I, Hatam F, Yildirim AO, Fehrenbach H, Walter K, Ruland J, Wagner H, Ehlers S, Sparwasser T. 2008. Decreased pathology and prolonged survival of human DC-SIGN transgenic mice during mycobacterial infection. J Immunol 180:6836–6845 http://dx.doi.org/10.4049/jimmunol.180.10.6836.
114. Ehlers S. 2010. DC-SIGN and mannosylated surface structures of Mycobacterium tuberculosis: a deceptive liaison. Eur J Cell Biol 89:95–101 http://dx.doi.org/10.1016/j.ejcb.2009.10.004.
115. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. 2008. Functions of natural killer cells. Nat Immunol 9:503–510 http://dx.doi.org/10.1038/ni1582.
116. De Maria A, Fogli M, Costa P, Murdaca G, Puppo F, Mavilio D, Moretta A, Moretta L. 2003. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur J Immunol 33:2410–2418 http://dx.doi.org/10.1002/eji.200324141.
117. Fogli M, Costa P, Murdaca G, Setti M, Mingari MC, Moretta L, Moretta A, De Maria A. 2004. Significant NK cell activation associated with decreased cytolytic function in peripheral blood of HIV-1-infected patients. Eur J Immunol 34:2313–2321 http://dx.doi.org/10.1002/eji.200425251.
118. Lopez-Vergès S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, Norris PJ, Nixon DF, Lanier LL. 2010. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 116:3865–3874 http://dx.doi.org/10.1182/blood-2010-04-282301.
119. Milush JM, López-Vergès S, York VA, Deeks SG, Martin JN, Hecht FM, Lanier LL, Nixon DF. 2013. CD56negCD16+ NK cells are activated mature NK cells with impaired effector function during HIV-1 infection. Retrovirology 10:158 http://dx.doi.org/10.1186/1742-4690-10-158.
120. Bhat R, Watzl C. 2007. Serial killing of tumor cells by human natural killer cells: enhancement by therapeutic antibodies. PLoS One 2:e326. doi:10.1371/journal.pone.0000326 http://dx.doi.org/10.1371/journal.pone.0000326.
121. Zocchi MR, Rubartelli A, Morgavi P, Poggi A. 1998. HIV-1 Tat inhibits human natural killer cell function by blocking L-type calcium channels. J Immunol 161:2938–2943. [PubMed]
122. Poggi A, Carosio R, Spaggiari GM, Fortis C, Tambussi G, Dell’Antonio G, Dal Cin E, Rubartelli A, Zocchi MR. 2002. NK cell activation by dendritic cells is dependent on LFA-1-mediated induction of calcium-calmodulin kinase II: inhibition by HIV-1 Tat C-terminal domain. J Immunol 168:95–101 http://dx.doi.org/10.4049/jimmunol.168.1.95.
123. Poggi A, Zocchi MR. 2006. HIV-1 Tat triggers TGF-beta production and NK cell apoptosis that is prevented by pertussis toxin B. Clin Dev Immunol 13:369–372 http://dx.doi.org/10.1080/17402520600645712.
124. Kottilil S, Shin K, Jackson JO, Reitano KN, O’Shea MA, Yang J, Hallahan CW, Lempicki R, Arthos J, Fauci AS. 2006. Innate immune dysfunction in HIV infection: effect of HIV envelope-NK cell interactions. J Immunol 176:1107–1114 http://dx.doi.org/10.4049/jimmunol.176.2.1107. [PubMed]
125. Hogg A, Huante M, Ongaya A, Williams J, Ferguson M, Cloyd M, Amukoye E, Endsley J. 2011. Activation of NK cell granulysin by mycobacteria and IL-15 is differentially affected by HIV. Tuberculosis (Edinb) 91(Suppl 1):S75–S81 http://dx.doi.org/10.1016/j.tube.2011.10.015.
126. 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.
127. 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.
128. 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.
129. Yoneda T, Ellner JJ. 1998. CD4(+) T cell and natural killer cell-dependent killing of Mycobacterium tuberculosis by human monocytes. Am J Respir Crit Care Med 158:395–403 http://dx.doi.org/10.1164/ajrccm.158.2.9707102.
130. 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. [PubMed]
131. 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.
132. Venketaraman V, Millman A, Salman M, Swaminathan S, Goetz M, Lardizabal A, David Hom, Connell ND. 2008. Glutathione levels and immune responses in tuberculosis patients. Microb Pathog 44:255–261 http://dx.doi.org/10.1016/j.micpath.2007.09.002.
133. Morris D, Guerra C, Donohue C, Oh H, Khurasany M, Venketaraman V. 2012. Unveiling the mechanisms for decreased glutathione in individuals with HIV infection. Clin Dev Immunol 2012:734125. doi:10.1155/2012/734125.
134. Morris D, Guerra C, Khurasany M, Guilford F, Saviola B, Huang Y, Venketaraman V. 2013. Glutathione supplementation improves macrophage functions in HIV. J Interferon Cytokine Res 33:270–279 http://dx.doi.org/10.1089/jir.2012.0103.
135. Dayaram YK, Talaue MT, Connell ND, Venketaraman V. 2006. Characterization of a glutathione metabolic mutant of Mycobacterium tuberculosis and its resistance to glutathione and nitrosoglutathione. J Bacteriol 188:1364–1372 http://dx.doi.org/10.1128/JB.188.4.1364-1372.2006.
136. Spallholz JE. 1987. Glutathione: is it an evolutionary vestige of the penicillins? Med Hypotheses 23:253–257 http://dx.doi.org/10.1016/0306-9877(87)90016-8.
137. Guerra C, Johal K, Morris D, Moreno S, Alvarado O, Gray D, Tanzil M, Pearce D, Venketaraman V. 2012. Control of Mycobacterium tuberculosis growth by activated natural killer cells. Clin Exp Immunol 168:142–152 http://dx.doi.org/10.1111/j.1365-2249.2011.04552.x.
138. Palanisamy GS, Kirk NM, Ackart DF, Shanley CA, Orme IM, Basaraba RJ. 2011. Evidence for oxidative stress and defective antioxidant response in guinea pigs with tuberculosis. PLoS One 6:e26254. doi:10.1371/journal.pone.0026254. http://dx.doi.org/10.1371/journal.pone.0026254.
139. Zhang Y, Nakata K, Weiden M, Rom WN. 1995. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication by transcriptional activation at the long terminal repeat. J Clin Invest 95:2324–2331 http://dx.doi.org/10.1172/JCI117924.
140. Honda Y, Rogers L, Nakata K, Zhao BY, Pine R, Nakai Y, Kurosu K, Rom WN, Weiden M. 1998. Type I interferon induces inhibitory 16-kD CCAAT/ enhancer binding protein (C/EBP)beta, repressing the HIV-1 long terminal repeat in macrophages: pulmonary tuberculosis alters C/EBP expression, enhancing HIV-1 replication. J Exp Med 188:1255–1265 http://dx.doi.org/10.1084/jem.188.7.1255.
141. Wu Y. 2004. HIV-1 gene expression: lessons from provirus and non-integrated DNA. Retrovirology 1:13 http://dx.doi.org/10.1186/1742-4690-1-13.
142. Tesmer VM, Rajadhyaksha A, Babin J, Bina M. 1993. NF-IL6-mediated transcriptional activation of the long terminal repeat of the human immunodeficiency virus type 1. Proc Natl Acad Sci USA 90:7298–7302 http://dx.doi.org/10.1073/pnas.90.15.7298.
143. Ossipow V, Descombes P, Schibler U. 1993. CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proc Natl Acad Sci USA 90:8219–8223 http://dx.doi.org/10.1073/pnas.90.17.8219.
144. Hoshino Y, Nakata K, Hoshino S, Honda Y, Tse DB, Shioda T, Rom WN, Weiden M. 2002. Maximal HIV-1 replication in alveolar macrophages during tuberculosis requires both lymphocyte contact and cytokines. J Exp Med 195:495–505 http://dx.doi.org/10.1084/jem.20011614.
145. Hoshino Y, Hoshino S, Gold JA, Raju B, Prabhakar S, Pine R, Rom WN, Nakata K, Weiden M. 2007. Mechanisms of polymorphonuclear neutrophil-mediated induction of HIV-1 replication in macrophages during pulmonary tuberculosis. J Infect Dis 195:1303–1310 http://dx.doi.org/10.1086/513438.
146. Lawn SD, Pisell TL, Hirsch CS, Wu M, Butera ST, Toossi Z. 2001. Anatomically compartmentalized human immunodeficiency virus replication in HLA-DR+ cells and CD14+ macrophages at the site of pleural tuberculosis coinfection. J Infect Dis 184:1127–1133 http://dx.doi.org/10.1086/323649.
147. Toossi Z, Wu M, Hirsch CS, Mayanja-Kizza H, Baseke J, Aung H, Canaday DH, Fujinaga K. 2012. Activation of P-TEFb at sites of dual HIV/TB infection, and inhibition of MTB-induced HIV transcriptional activation by the inhibitor of CDK9, Indirubin-3′-monoxime. AIDS Res Hum Retroviruses 28:182–187 http://dx.doi.org/10.1089/aid.2010.0211.
148. Rodriguez ME, Loyd CM, Ding X, Karim AF, McDonald DJ, Canaday DH, Rojas RE. 2013. Mycobacterial phosphatidylinositol mannoside 6 (PIM6) up-regulates TCR-triggered HIV-1 replication in CD4+ T cells. PLoS One 8:e80938. doi:10.1371/journal.pone.0080938 http://dx.doi.org/10.1371/journal.pone.0080938.
149. Bhat KH, Chaitanya CK, Parveen N, Varman R, Ghosh S, Mukhopadhyay S. 2012. Proline-proline-glutamic acid (PPE) protein Rv1168c of Mycobacterium tuberculosis augments transcription from HIV-1 long terminal repeat promoter. J Biol Chem 287:16930–16946 http://dx.doi.org/10.1074/jbc.M111.327825.
150. Falvo JV, Ranjbar S, Jasenosky LD, Goldfeld AE. 2011. Arc of a vicious circle: pathways activated by Mycobacterium tuberculosis that target the HIV-1 long terminal repeat. Am J Respir Cell Mol Biol 45:1116–1124 http://dx.doi.org/10.1165/rcmb.2011-0186TR.
151. Toor JS, Singh S, Sharma A, Arora SK. 2014. Mycobacterium tuberculosis modulates the gene interactions to activate the HIV replication and faster disease progression in a co-infected host. PLoS One 9:e106815. doi:10.1371/journal.pone.0106815. http://dx.doi.org/10.1371/journal.pone.0106815.
152. Ranjbar S, Jasenosky LD, Chow N, Goldfeld AE. 2012. Regulation of Mycobacterium tuberculosis-dependent HIV-1 transcription reveals a new role for NFAT5 in the toll-like receptor pathway. PLoS Pathog 8:e1002620. doi:10.1371/journal.ppat.1002620. http://dx.doi.org/10.1371/journal.ppat.1002620.
153. Mamik MK, Ghorpade A. 2014. Chemokine CXCL8 promotes HIV-1 replication in human monocyte-derived macrophages and primary microglia via nuclear factor-κB pathway. PLoS One 9:e92145. doi:10.1371/journal.pone.0092145 http://dx.doi.org/10.1371/journal.pone.0092145.
154. Robichaud GA, Barbeau B, Fortin JF, Rothstein DM, Tremblay MJ. 2002. Nuclear factor of activated T cells is a driving force for preferential productive HIV-1 infection of CD45RO-expressing CD4+ T cells. J Biol Chem 277:23733–23741 http://dx.doi.org/10.1074/jbc.M201563200.
155. Costello R, Lipcey C, Algarté M, Cerdan C, Baeuerle PA, Olive D, Imbert J. 1993. Activation of primary human T-lymphocytes through CD2 plus CD28 adhesion molecules induces long-term nuclear expression of NF-kappa B. Cell Growth Differ 4:329–339. [PubMed]
156. Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, Narváez AB, Hunt P, Martin JN, Kahn JO, Levy J, McGrath MS, Hecht FM. 2004. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 104:942–947 http://dx.doi.org/10.1182/blood-2003-09-3333.
157. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, Shih R, Lewis J, Wiley DJ, Phair JP, Wolinsky SM, Detels R. 1999. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 179:859–870 http://dx.doi.org/10.1086/314660.
158. Nakata K, Rom WN, Honda Y, Condos R, Kanegasaki S, Cao Y, Weiden M. 1997. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. Am J Respir Crit Care Med 155:996–1003 http://dx.doi.org/10.1164/ajrccm.155.3.9117038.
159. Collins KR, Mayanja-Kizza H, Sullivan BA, Quiñones-Mateu ME, Toossi Z, Arts EJ. 2000. Greater diversity of HIV-1 quasispecies in HIV-infected individuals with active tuberculosis. J Acquir Immune Defic Syndr 24:408–417 http://dx.doi.org/10.1097/00126334-200008150-00002.
160. Biru T, Lennemann T, Stürmer M, Stephan C, Nisius G, Cinatl J, Staszewski S, Gürtler LG. 2010. Human immunodeficiency virus type-1 group M quasispecies evolution: diversity and divergence in patients co-infected with active tuberculosis. Med Microbiol Immunol (Berl) 199:323–332 http://dx.doi.org/10.1007/s00430-010-0167-9.
161. Danaviah S, Sacks JA, Kumar KP, Taylor LM, Fallows DA, Naicker T, Ndung’u T, Govender S, Kaplan G. 2013. Immunohistological characterization of spinal TB granulomas from HIV-negative and -positive patients. Tuberculosis (Edinb) 93:432–441 http://dx.doi.org/10.1016/j.tube.2013.02.009.
162. Danaviah S, de Oliveira T, Gordon M, Govender S, Chelule P, Pillay S, Naicker T, Cassol S, Ndung’u T. 2015. Analysis of dominant HIV quasispecies suggests independent viral evolution within spinal granulomas coinfected with Mycobacterium tuberculosis and HIV-1 subtype C. AIDS Res Hum Retroviruses 32:262–270. [PubMed]
163. Lawn SD, Butera ST, Shinnick TM. 2002. Tuberculosis unleashed: the impact of human immunodeficiency virus infection on the host granulomatous response to Mycobacterium tuberculosis. Microbes Infect 4:635–646 http://dx.doi.org/10.1016/S1286-4579(02)01582-4.
164. Kizza HM, Rodriguez B, Quinones-Mateu M, Mirza M, Aung H, Yen-Lieberman B, Starkey C, Horter L, Peters P, Baseke J, Johnson JL, Toossi Z. 2005. Persistent replication of human immunodeficiency virus type 1 despite treatment of pulmonary tuberculosis in dually infected subjects. Clin Diagn Lab Immunol 12:1298–1304.
165. Collins KR, Quiñones-Mateu ME, Toossi Z, Arts EJ. 2002. Impact of tuberculosis on HIV-1 replication, diversity, and disease progression. AIDS Rev 4:165–176. [PubMed]
166. Badri M, Ehrlich R, Wood R, Pulerwitz T, Maartens G. 2001. Association between tuberculosis and HIV disease progression in a high tuberculosis prevalence area. Int J Tuberc Lung Dis 5:225–232. [PubMed]
167. Whalen C, Horsburgh CR, Hom D, Lahart C, Simberkoff M, Ellner J. 1995. Accelerated course of human immunodeficiency virus infection after tuberculosis. Am J Respir Crit Care Med 151:129–135 http://dx.doi.org/10.1164/ajrccm.151.1.7812542.
168. Toossi Z, Mayanja-Kizza H, Lawn SD, Hirsch CS, Lupo LD, Butera ST. 2007. Dynamic variation in the cellular origin of HIV type 1 during treatment of tuberculosis in dually infected subjects. AIDS Res Hum Retroviruses 23:93–100 http://dx.doi.org/10.1089/aid.2006.0050.
169. Sullivan ZA, Wong EB, Ndung’u T, Kasprowicz VO, Bishai WR. 2015. Latent and active tuberculosis infection increase immune activation in individuals co-infected with HIV. EBioMedicine 2:334–340 http://dx.doi.org/10.1016/j.ebiom.2015.03.005.
170. Srivastava S, Ernst JD. 2014. Cell-to-cell transfer of M. tuberculosis antigens optimizes CD4 T cell priming. Cell Host Microbe 15:741–752 http://dx.doi.org/10.1016/j.chom.2014.05.007.
171. Harding JS, Rayasam A, Schreiber HA, Fabry Z, Sandor M. 2015. Mycobacterium-infected dendritic cells disseminate granulomatous inflammation. Sci Rep 5:15248. doi:10.1038/srep15248 http://dx.doi.org/10.1038/srep15248.
172. Krishnan N, Robertson BD, Thwaites G. 2010. The mechanisms and consequences of the extra-pulmonary dissemination of Mycobacterium tuberculosis. Tuberculosis (Edinb) 90:361–366 http://dx.doi.org/10.1016/j.tube.2010.08.005.
173. Volkman HE, Pozos TC, Zheng J, Davis JM, Rawls JF, Ramakrishnan L. 2010. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 327:466–469 http://dx.doi.org/10.1126/science.1179663.
174. Datta M, Via LE, Kamoun WS, Liu C, Chen W, Seano G, Weiner DM, Schimel D, England K, Martin JD, Gao X, Xu L, Barry CE III, Jain RK. 2015. Anti-vascular endothelial growth factor treatment normalizes tuberculosis granuloma vasculature and improves small molecule delivery. Proc Natl Acad Sci USA 112:1827–1832 http://dx.doi.org/10.1073/pnas.1424563112.
175. Oehlers SH, Cronan MR, Scott NR, Thomas MI, Okuda KS, Walton EM, Beerman RW, Crosier PS, Tobin DM. 2015. Interception of host angiogenic signalling limits mycobacterial growth. Nature 517:612–615 http://dx.doi.org/10.1038/nature13967.
176. Isaakidis P, Casas EC, Das M, Tseretopoulou X, Ntzani EE, Ford N. 2015. Treatment outcomes for HIV and MDR-TB co-infected adults and children: systematic review and meta-analysis. Int J Tuberc Lung Dis 19:969–978 http://dx.doi.org/10.5588/ijtld.15.0123. [PubMed]
177. Munier ML, Kelleher AD. 2007. Acutely dysregulated, chronically disabled by the enemy within: t-cell responses to HIV-1 infection. Immunol Cell Biol 85:6–15 http://dx.doi.org/10.1038/sj.icb.7100015.
178. Clerici M, Stocks NI, Zajac RA, Boswell RN, Lucey DR, Via CS, Shearer GM. 1989. Detection of three distinct patterns of T helper cell dysfunction in asymptomatic, human immunodeficiency virus-seropositive patients. Independence of CD4+ cell numbers and clinical staging. J Clin Invest 84:1892–1899 http://dx.doi.org/10.1172/JCI114376.
179. Isgrò A, Leti W, De Santis W, Marziali M, Esposito A, Fimiani C, Luzi G, Pinti M, Cossarizza A, Aiuti F, Mezzaroma I. 2008. Altered clonogenic capability and stromal cell function characterize bone marrow of HIV-infected subjects with low CD4+ T cell counts despite viral suppression during HAART. Clin Infect Dis 46:1902–1910 http://dx.doi.org/10.1086/588480.
180. Hellerstein M, Hanley MB, Cesar D, Siler S, Papageorgopoulos C, Wieder E, Schmidt D, Hoh R, Neese R, Macallan D, Deeks S, McCune JM. 1999. Directly measured kinetics of circulating T lymphocytes in normal and HIV-1-infected humans. Nat Med 5:83–89 http://dx.doi.org/10.1038/4772.
181. Hellerstein MK, Hoh RA, Hanley MB, Cesar D, Lee D, Neese RA, McCune JM. 2003. Subpopulations of long-lived and short-lived T cells in advanced HIV-1 infection. J Clin Invest 112:956–966 http://dx.doi.org/10.1172/JCI200317533.
182. Schacker TW, Nguyen PL, Beilman GJ, Wolinsky S, Larson M, Reilly C, Haase AT. 2002. Collagen deposition in HIV-1 infected lymphatic tissues and T cell homeostasis. J Clin Invest 110:1133–1139 http://dx.doi.org/10.1172/JCI0216413.
183. Schacker TW, Reilly C, Beilman GJ, Taylor J, Skarda D, Krason D, Larson M, Haase AT. 2005. Amount of lymphatic tissue fibrosis in HIV infection predicts magnitude of HAART-associated change in peripheral CD4 cell count. AIDS 19:2169–2171 http://dx.doi.org/10.1097/01.aids.0000194801.51422.03.
184. Estes JD, Reilly C, Trubey CM, Fletcher CV, Cory TJ, Piatak M Jr, Russ S, Anderson J, Reimann TG, Star R, Smith A, Tracy RP, Berglund A, Schmidt T, Coalter V, Chertova E, Smedley J, Haase AT, Lifson JD, Schacker TW. 2015. Antifibrotic therapy in simian immunodeficiency virus infection preserves CD4+ T-cell populations and improves immune reconstitution with antiretroviral therapy. J Infect Dis 211:744–754 http://dx.doi.org/10.1093/infdis/jiu519.
185. Doitsh G, Cavrois M, Lassen KG, Zepeda O, Yang Z, Santiago ML, Hebbeler AM, Greene WC. 2010. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 143:789–801 http://dx.doi.org/10.1016/j.cell.2010.11.001. (Erratum, 156:1112–1113.)
186. Monroe KM, Yang Z, Johnson JR, Geng X, Doitsh G, Krogan NJ, Greene WC. 2014. IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343:428–432 http://dx.doi.org/10.1126/science.1243640.
187. Kalsdorf B, Scriba TJ, Wood K, Day CL, Dheda K, Dawson R, Hanekom WA, Lange C, Wilkinson RJ. 2009. HIV-1 infection impairs the bronchoalveolar T-cell response to mycobacteria. Am J Respir Crit Care Med 180:1262–1270 http://dx.doi.org/10.1164/rccm.200907-1011OC. [PubMed]
188. Jambo KC, Sepako E, Fullerton DG, Mzinza D, Glennie S, Wright AK, Heyderman RS, Gordon SB. 2011. Bronchoalveolar CD4+ T cell responses to respiratory antigens are impaired in HIV-infected adults. Thorax 66:375–382 http://dx.doi.org/10.1136/thx.2010.153825.
189. Law KF, Jagirdar J, Weiden MD, Bodkin M, Rom WN. 1996. Tuberculosis in HIV-positive patients: cellular response and immune activation in the lung. Am J Respir Crit Care Med 153:1377–1384 http://dx.doi.org/10.1164/ajrccm.153.4.8616569.
190. Breen RA, Janossy G, Barry SM, Cropley I, Johnson MA, Lipman MC. 2006. Detection of mycobacterial antigen responses in lung but not blood in HIV-tuberculosis co-infected subjects. AIDS 20:1330–1332 http://dx.doi.org/10.1097/01.aids.0000232243.51286.32. [PubMed]
191. Diedrich CR, Mattila JT, Klein E, Janssen C, Phuah J, Sturgeon TJ, Montelaro RC, Lin PL, Flynn JL. 2010. Reactivation of latent tuberculosis in cynomolgus macaques infected with SIV is associated with early peripheral T cell depletion and not virus load. PLoS One 5:e9611. doi:10.1371/journal.pone.0009611 http://dx.doi.org/10.1371/journal.pone.0009611.
192. Mondal K, Mandal R. 2015. Cytopathological and microbiological profile of tuberculous lymphadenitis in HIV-infected patients with special emphasis on its corroboration with CD4+ T-cell counts. Acta Cytol 59:156–162 http://dx.doi.org/10.1159/000380938.
193. Rao JS, Kumari S J, Kini U. 2015. Correlation of CD4 counts with the FNAC patterns of tubercular lymphadenitis in patients with HIV: a cross sectional pilot study. Diagn Cytopathol 43:16–20 http://dx.doi.org/10.1002/dc.23177.
194. Geldmacher C, Schuetz A, Ngwenyama N, Casazza JP, Sanga E, Saathoff E, Boehme C, Geis S, Maboko L, Singh M, Minja F, Meyerhans A, Koup RA, Hoelscher M. 2008. Early depletion of Mycobacterium tuberculosis-specific T helper 1 cell responses after HIV-1 infection. J Infect Dis 198:1590–1598 http://dx.doi.org/10.1086/593017.
195. Yang YF, Tomura M, Iwasaki M, Mukai T, Gao P, Ono S, Zou JP, Shearer GM, Fujiwara H, Hamaoka T. 2001. IL-12 as well as IL-2 upregulates CCR5 expression on T cell receptor-triggered human CD4+ and CD8+ T cells. J Clin Immunol 21:116–125 http://dx.doi.org/10.1023/A:1011059906777.
196. Casazza JP, Brenchley JM, Hill BJ, Ayana R, Ambrozak D, Roederer M, Douek DC, Betts MR, Koup RA. 2009. Autocrine production of beta-chemokines protects CMV-specific CD4 T cells from HIV infection. PLoS Pathog 5:e1000646. doi:10.1371/journal.ppat.1000646 http://dx.doi.org/10.1371/journal.ppat.1000646.
197. Geldmacher C, Ngwenyama N, Schuetz A, Petrovas C, Reither K, Heeregrave EJ, Casazza JP, Ambrozak DR, Louder M, Ampofo W, Pollakis G, Hill B, Sanga E, Saathoff E, Maboko L, Roederer M, Paxton WA, Hoelscher M, Koup RA. 2010. Preferential infection and depletion of Mycobacterium tuberculosis-specific CD4 T cells after HIV-1 infection. J Exp Med 207:2869–2881 http://dx.doi.org/10.1084/jem.20100090.
198. Ramilo O, Bell KD, Uhr JW, Vitetta ES. 1993. Role of CD25+ and CD25-T cells in acute HIV infection in vitro. J Immunol 150:5202–5208. [PubMed]
199. Arlen PA, Brooks DG, Gao LY, Vatakis D, Brown HJ, Zack JA. 2006. Rapid expression of human immunodeficiency virus following activation of latently infected cells. J Virol 80:1599–1603 http://dx.doi.org/10.1128/JVI.80.3.1599-1603.2006.
200. Goletti D, Weissman D, Jackson RW, Graham NM, Vlahov D, Klein RS, Munsiff SS, Ortona L, Cauda R, Fauci AS. 1996. Effect of Mycobacterium tuberculosis on HIV replication. Role of immune activation. J Immunol 157:1271–1278. [PubMed]
201. Hammond AS, McConkey SJ, Hill PC, Crozier S, Klein MR, Adegbola RA, Rowland-Jones S, Brookes RH, Whittle H, Jaye A. 2008. Mycobacterial T cell responses in HIV-infected patients with advanced immunosuppression. J Infect Dis 197:295–299 http://dx.doi.org/10.1086/524685. [PubMed]
202. Rangaka MX, Diwakar L, Seldon R, van Cutsem G, Meintjes GA, Morroni C, Mouton P, Shey MS, Maartens G, Wilkinson KA, Wilkinson RJ. 2007. Clinical, immunological, and epidemiological importance of antituberculosis T cell responses in HIV-infected Africans. Clin Infect Dis 44:1639–1646 http://dx.doi.org/10.1086/518234.
203. Chaudhry A, Das SR, Hussain A, Mayor S, George A, Bal V, Jameel S, Rath S. 2005. The Nef protein of HIV-1 induces loss of cell surface costimulatory molecules CD80 and CD86 in APCs. J Immunol 175:4566–4574 http://dx.doi.org/10.4049/jimmunol.175.7.4566.
204. Chaudhry A, Verghese DA, Das SR, Jameel S, George A, Bal V, Mayor S, Rath S. 2009. HIV-1 Nef promotes endocytosis of cell surface MHC class II molecules via a constitutive pathway. J Immunol 183:2415–2424 http://dx.doi.org/10.4049/jimmunol.0804014.
205. Oyaizu N, Chirmule N, Kalyanaraman VS, Hall WW, Pahwa R, Shuster M, Pahwa S. 1990. Human immunodeficiency virus type 1 envelope glycoprotein gp120 produces immune defects in CD4+ T lymphocytes by inhibiting interleukin 2 mRNA. Proc Natl Acad Sci USA 87:2379–2383 http://dx.doi.org/10.1073/pnas.87.6.2379.
206. Puri RK, Leland P, Aggarwal BB. 1995. Constitutive expression of human immunodeficiency virus type 1 tat gene inhibits interleukin 2 and interleukin 2 receptor expression in a human CD4+ T lymphoid (H9) cell line. AIDS Res Hum Retroviruses 11:31–40 http://dx.doi.org/10.1089/aid.1995.11.31.
207. Pollock KM, Montamat-Sicotte DJ, Grass L, Cooke GS, Kapembwa MS, Kon OM, Sampson RD, Taylor GP, Lalvani A. 2016. PD-1 expression and cytokine secretion profiles of Mycobacterium tuberculosis-specific CD4+ T-cell subsets: potential correlates of containment in HIV-TB co-infection. PLoS One 11:e0146905. doi:10.1371/journal.pone.0146905. http://dx.doi.org/10.1371/journal.pone.0146905.
208. Fife BT, Pauken KE. 2011. The role of the PD-1 pathway in autoimmunity and peripheral tolerance. Ann N Y Acad Sci 1217:45–59 http://dx.doi.org/10.1111/j.1749-6632.2010.05919.x.
209. Nakanjako D, Ssewanyana I, Mayanja-Kizza H, Kiragga A, Colebunders R, Manabe YC, Nabatanzi R, Kamya MR, Cao H. 2011. High T-cell immune activation and immune exhaustion among individuals with suboptimal CD4 recovery after 4 years of antiretroviral therapy in an African cohort. BMC Infect Dis 11:43. doi:10.1186/1471-2334-11-43 http://dx.doi.org/10.1186/1471-2334-11-43.
210. Grabmeier-Pfistershammer K, Steinberger P, Rieger A, Leitner J, Kohrgruber N. 2011. Identification of PD-1 as a unique marker for failing immune reconstitution in HIV-1-infected patients on treatment. J Acquir Immune Defic Syndr 56:118–124 http://dx.doi.org/10.1097/QAI.0b013e3181fbab9f.
211. Robbins GK, Spritzler JG, Chan ES, Asmuth DM, Gandhi RT, Rodriguez BA, Skowron G, Skolnik PR, Shafer RW, Pollard RB, AIDS Clinical Trials Group 384 Team. 2009. Incomplete reconstitution of T cell subsets on combination antiretroviral therapy in the AIDS Clinical Trials Group protocol 384. Clin Infect Dis 48:350–361 http://dx.doi.org/10.1086/595888.
212. Riou C, Tanko RF, Soares AP, Masson L, Werner L, Garrett NJ, Samsunder N, Abdool Karim Q, Abdool Karim SS, Burgers WA. 2015. Restoration of CD4+ responses to copathogens in HIV-infected individuals on antiretroviral therapy is dependent on T cell memory phenotype. J Immunol 195:2273–2281 http://dx.doi.org/10.4049/jimmunol.1500803.
213. Wilkinson KA, Seldon R, Meintjes G, Rangaka MX, Hanekom WA, Maartens G, Wilkinson RJ. 2009. Dissection of regenerating T-cell responses against tuberculosis in HIV-infected adults sensitized by Mycobacterium tuberculosis. Am J Respir Crit Care Med 180:674–683 http://dx.doi.org/10.1164/rccm.200904-0568OC.
214. Evans TG, Bonnez W, Soucier HR, Fitzgerald T, Gibbons DC, Reichman RC. 1998. Highly active antiretroviral therapy results in a decrease in CD8+ T cell activation and preferential reconstitution of the peripheral CD4+ T cell population with memory rather than naive cells. Antiviral Res 39:163–173 http://dx.doi.org/10.1016/S0166-3542(98)00035-7.
215. Rönsholt FF, Ullum H, Katzenstein TL, Gerstoft J, Ostrowski SR. 2012. T-cell subset distribution in HIV-1-infected patients after 12 years of treatment-induced viremic suppression. J Acquir Immune Defic Syndr 61:270–278 http://dx.doi.org/10.1097/QAI.0b013e31825e7ac1.
216. Wendland T, Furrer H, Vernazza PL, Frutig K, Christen A, Matter L, Malinverni R, Pichler WJ. 1999. HAART in HIV-infected patients: restoration of antigen-specific CD4 T-cell responses in vitro is correlated with CD4 memory T-cell reconstitution, whereas improvement in delayed type hypersensitivity is related to a decrease in viraemia. AIDS 13:1857–1862 http://dx.doi.org/10.1097/00002030-199910010-00007.
217. Li TS, Tubiana R, Katlama C, Calvez V, Ait Mohand H, Autran B. 1998. Long-lasting recovery in CD4 T-cell function and viral-load reduction after highly active antiretroviral therapy in advanced HIV-1 disease. Lancet 351:1682–1686 http://dx.doi.org/10.1016/S0140-6736(97)10291-4.
218. Hsu DC, Kerr SJ, Thongpaeng P, Iampornsin T, Pett SL, Zaunders JJ, Avihingsanon A, Ubolyam S, Ananworanich J, Kelleher AD, Cooper DA. 2014. Incomplete restoration of Mycobacterium tuberculosis-specific-CD4 T cell responses despite antiretroviral therapy. J Infect 68:344–354 http://dx.doi.org/10.1016/j.jinf.2013.11.016.
219. Sutherland JS, Young JM, Peterson KL, Sanneh B, Whittle HC, Rowland-Jones SL, Adegbola RA, Jaye A, Ota MO. 2010. Polyfunctional CD4(+) and CD8(+) T cell responses to tuberculosis antigens in HIV-1-infected patients before and after anti-retroviral treatment. J Immunol 184:6537–6544 http://dx.doi.org/10.4049/jimmunol.1000399.
220. Sutherland R, Yang H, Scriba TJ, Ondondo B, Robinson N, Conlon C, Suttill A, McShane H, Fidler S, McMichael A, Dorrell L. 2006. Impaired IFN-gamma-secreting capacity in mycobacterial antigen-specific CD4 T cells during chronic HIV-1 infection despite long-term HAART. AIDS 20:821–829 http://dx.doi.org/10.1097/01.aids.0000218545.31716.a4.
221. Mendonça M, Tanji MM, Silva LC, Silveira GG, Oliveira SC, Duarte AJ, Benard G. 2007. Deficient in vitro anti-mycobacterial immunity despite successful long-term highly active antiretroviral therapy in HIV-infected patients with past history of tuberculosis infection or disease. Clin Immunol 125:60–66 http://dx.doi.org/10.1016/j.clim.2007.06.002.
222. Jambo KC, Banda DH, Afran L, Kankwatira AM, Malamba RD, Allain TJ, Gordon SB, Heyderman RS, Russell DG, Mwandumba HC. 2014. Asymptomatic HIV-infected individuals on antiretroviral therapy exhibit impaired lung CD4(+) T-cell responses to mycobacteria. Am J Respir Crit Care Med 190:938–947 http://dx.doi.org/10.1164/rccm.201405-0864OC.
223. Day CL, Mkhwanazi N, Reddy S, Mncube Z, van der Stok M, Klenerman P, Walker BD. 2008. Detection of polyfunctional Mycobacterium tuberculosis-specific T cells and association with viral load in HIV-1-infected persons. J Infect Dis 197:990–999 http://dx.doi.org/10.1086/529048.
224. Canaday DH, Wilkinson RJ, Li Q, Harding CV, Silver RF, Boom WH. 2001. CD4(+) and CD8(+) T cells kill intracellular Mycobacterium tuberculosis by a perforin and Fas/Fas ligand-independent mechanism. J Immunol 167:2734–2742 http://dx.doi.org/10.4049/jimmunol.167.5.2734.
225. Woodworth JS, Wu Y, Behar SM. 2008. Mycobacterium tuberculosis-specific CD8+ T cells require perforin to kill target cells and provide protection in vivo. J Immunol 181:8595–8603 http://dx.doi.org/10.4049/jimmunol.181.12.8595.
226. Gulzar N, Copeland KF. 2004. CD8+ T-cells: function and response to HIV infection. Curr HIV Res 2:23–37 http://dx.doi.org/10.2174/1570162043485077.
227. Kalokhe AS, Adekambi T, Ibegbu CC, Ray SM, Day CL, Rengarajan J. 2015. Impaired degranulation and proliferative capacity of Mycobacterium tuberculosis-specific CD8+ T cells in HIV-infected individuals with latent tuberculosis. J Infect Dis 211:635–640 http://dx.doi.org/10.1093/infdis/jiu505.
228. van Pinxteren LA, Cassidy JP, Smedegaard BH, Agger EM, Andersen P. 2000. Control of latent Mycobacterium tuberculosis infection is dependent on CD8 T cells. Eur J Immunol 30:3689–3698 http://dx.doi.org/10.1002/1521-4141(200012)30:12<3689::AID-IMMU3689>3.0.CO;2-4.
229. Mogues T, Goodrich ME, Ryan L, LaCourse R, North RJ. 2001. The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J Exp Med 193:271–280 http://dx.doi.org/10.1084/jem.193.3.271.
230. Bruns H, Meinken C, Schauenberg P, Härter G, Kern P, Modlin RL, Antoni C, Stenger S. 2009. Anti-TNF immunotherapy reduces CD8+ T cell-mediated antimicrobial activity against Mycobacterium tuberculosis in humans. J Clin Invest 119:1167–1177 http://dx.doi.org/10.1172/JCI38482.
231. Chiacchio T, Petruccioli E, Vanini V, Cuzzi G, Pinnetti C, Sampaolesi A, Antinori A, Girardi E, Goletti D. 2014. Polyfunctional T-cells and effector memory phenotype are associated with active TB in HIV-infected patients. J Infect 69:533–545 http://dx.doi.org/10.1016/j.jinf.2014.06.009.
232. Suarez GV, Angerami MT, Vecchione MB, Laufer N, Turk G, Ruiz MJ, Mesch V, Fabre B, Maidana P, Ameri D, Cahn P, Sued O, Salomón H, Bottasso OA, Quiroga MF. 2015. HIV-TB coinfection impairs CD8(+) T-cell differentiation and function while dehydroepiandrosterone improves cytotoxic antitubercular immune responses. Eur J Immunol 45:2529–2541 http://dx.doi.org/10.1002/eji.201545545.
233. Wu L, Fu J, Shen SH. 2002. SKAP55 coupled with CD45 positively regulates T-cell receptor-mediated gene transcription. Mol Cell Biol 22:2673–2686 http://dx.doi.org/10.1128/MCB.22.8.2673-2686.2002.
234. Wang Y, Johnson P. 2005. Expression of CD45 lacking the catalytic protein tyrosine phosphatase domain modulates Lck phosphorylation and T cell activation. J Biol Chem 280:14318–14324 http://dx.doi.org/10.1074/jbc.M413265200.
235. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, Freeman GJ, Ahmed R. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:682–687 http://dx.doi.org/10.1038/nature04444.
236. Prasad KV, Ao Z, Yoon Y, Wu MX, Rizk M, Jacquot S, Schlossman SF. 1997. CD27, a member of the tumor necrosis factor receptor family, induces apoptosis and binds to Siva, a proapoptotic protein. Proc Natl Acad Sci USA 94:6346–6351 http://dx.doi.org/10.1073/pnas.94.12.6346.
237. Meintjes G, Lawn SD, Scano F, Maartens G, French MA, Worodria W, Elliott JH, Murdoch D, Wilkinson RJ, Seyler C, John L, van der Loeff MS, Reiss P, Lynen L, Janoff EN, Gilks C, Colebunders R, International Network for the Study of HIV-associated IRIS. 2008. Tuberculosis-associated immune reconstitution inflammatory syndrome: case definitions for use in resource-limited settings. Lancet Infect Dis 8:516–523 http://dx.doi.org/10.1016/S1473-3099(08)70184-1.
238. Marais S, Meintjes G, Pepper DJ, Dodd LE, Schutz C, Ismail Z, Wilkinson KA, Wilkinson RJ. 2013. Frequency, severity, and prediction of tuberculous meningitis immune reconstitution inflammatory syndrome. Clin Infect Dis 56:450–460 http://dx.doi.org/10.1093/cid/cis899.
239. Asselman V, Thienemann F, Pepper DJ, Boulle A, Wilkinson RJ, Meintjes G, Marais S. 2010. Central nervous system disorders after starting antiretroviral therapy in South Africa. AIDS 24:2871–2876 http://dx.doi.org/10.1097/QAD.0b013e328340fe76.
240. Pepper DJ, Marais S, Maartens G, Rebe K, Morroni C, Rangaka MX, Oni T, Wilkinson RJ, Meintjes G. 2009. Neurologic manifestations of paradoxical tuberculosis-associated immune reconstitution inflammatory syndrome: a case series. Clin Infect Dis 48:e96–e107 http://dx.doi.org/10.1086/598988.
241. Lawn SD, Myer L, Bekker LG, Wood R. 2007. Tuberculosis-associated immune reconstitution disease: incidence, risk factors and impact in an antiretroviral treatment service in South Africa. AIDS 21:335–341 http://dx.doi.org/10.1097/QAD.0b013e328011efac.
242. Ratnam I, Chiu C, Kandala NB, Easterbrook PJ. 2006. Incidence and risk factors for immune reconstitution inflammatory syndrome in an ethnically diverse HIV type 1-infected cohort. Clin Infect Dis 42:418–427 http://dx.doi.org/10.1086/499356.
243. Namale PE, Abdullahi LH, Fine S, Kamkuemah M, Wilkinson RJ, Meintjes G. 2015. Paradoxical TB-IRIS in HIV-infected adults: a systematic review and meta-analysis. Future Microbiol 10:1077–1099 http://dx.doi.org/10.2217/fmb.15.9. [PubMed]
244. Burman W, Weis S, Vernon A, Khan A, Benator D, Jones B, Silva C, King B, LaHart C, Mangura B, Weiner M, El-Sadr W. 2007. Frequency, severity and duration of immune reconstitution events in HIV-related tuberculosis. Int J Tuberc Lung Dis 11:1282–1289. [PubMed]
245. Manosuthi W, Kiertiburanakul S, Phoorisri T, Sungkanuparph S. 2006. Immune reconstitution inflammatory syndrome of tuberculosis among HIV-infected patients receiving antituberculous and antiretroviral therapy. J Infect 53:357–363 http://dx.doi.org/10.1016/j.jinf.2006.01.002.
246. Naidoo K, Yende-Zuma N, Padayatchi N, Naidoo K, Jithoo N, Nair G, Bamber S, Gengiah S, El-Sadr WM, Friedland G, Abdool Karim S. 2012. The immune reconstitution inflammatory syndrome after antiretroviral therapy initiation in patients with tuberculosis: findings from the SAPiT trial. Ann Intern Med 157:313–324 http://dx.doi.org/10.7326/0003-4819-157-5-201209040-00004.
247. Abay SM, Deribe K, Reda AA, Biadgilign S, Datiko D, Assefa T, Todd M, Deribew A. 2015. The effect of early initiation of antiretroviral therapy in TB/HIV-coinfected patients: a systematic review and meta-analysis. J Int Assoc Provid AIDS Care 14:560–570 http://dx.doi.org/10.1177/2325957415599210.
248. Lai RP, Meintjes G, Wilkinson KA, Graham CM, Marais S, Van der Plas H, Deffur A, Schutz C, Bloom C, Munagala I, Anguiano E, Goliath R, Maartens G, Banchereau J, Chaussabel D, O’Garra A, Wilkinson RJ. 2015. HIV-tuberculosis-associated immune reconstitution inflammatory syndrome is characterized by Toll-like receptor and inflammasome signalling. Nat Commun 6:8451 http://dx.doi.org/10.1038/ncomms9451.
249. Andrade BB, Singh A, Narendran G, Schechter ME, Nayak K, Subramanian S, Anbalagan S, Jensen SM, Porter BO, Antonelli LR, Wilkinson KA, Wilkinson RJ, Meintjes G, van der Plas H, Follmann D, Barber DL, Swaminathan S, Sher A, Sereti I. 2014. Mycobacterial antigen driven activation of CD14++CD16- monocytes is a predictor of tuberculosis-associated immune reconstitution inflammatory syndrome. PLoS Pathog 10:e1004433. doi:10.1371/journal.ppat.1004433 http://dx.doi.org/10.1371/journal.ppat.1004433.
250. Tan DB, Lim A, Yong YK, Ponnampalavanar S, Omar S, Kamarulzaman A, French MA, Price P. 2011. TLR2-induced cytokine responses may characterize HIV-infected patients experiencing mycobacterial immune restoration disease. AIDS 25:1455–1460 http://dx.doi.org/10.1097/QAD.0b013e328348fb18.
251. Conradie F, Foulkes AS, Ive P, Yin X, Roussos K, Glencross DK, Lawrie D, Stevens W, Montaner LJ, Sanne I, Azzoni L. 2011. Natural killer cell activation distinguishes Mycobacterium tuberculosis-mediated immune reconstitution syndrome from chronic HIV and HIV/MTB coinfection. J Acquir Immune Defic Syndr 58:309–318 http://dx.doi.org/10.1097/QAI.0b013e31822e0d15.
252. Pean P, Nerrienet E, Madec Y, Borand L, Laureillard D, Fernandez M, Marcy O, Sarin C, Phon K, Taylor S, Pancino G, Barré-Sinoussi F, Scott-Algara D, Cambodian Early versus Late Introduction of Antiretroviral Drugs (CAMELIA) Study Team. 2012. Natural killer cell degranulation capacity predicts early onset of the immune reconstitution inflammatory syndrome (IRIS) in HIV-infected patients with tuberculosis. Blood 119:3315–3320 http://dx.doi.org/10.1182/blood-2011-09-377523.
253. Wilkinson KA, Walker NF, Meintjes G, Deffur A, Nicol MP, Skolimowska KH, Matthews K, Tadokera R, Seldon R, Maartens G, Rangaka MX, Besra GS, Wilkinson RJ. 2015. Cytotoxic mediators in paradoxical HIV-tuberculosis immune reconstitution inflammatory syndrome. J Immunol 194:1748–1754 http://dx.doi.org/10.4049/jimmunol.1402105.
254. Marais S, Wilkinson KA, Lesosky M, Coussens AK, Deffur A, Pepper DJ, Schutz C, Ismail Z, Meintjes G, Wilkinson RJ. 2014. Neutrophil-associated central nervous system inflammation in tuberculous meningitis immune reconstitution inflammatory syndrome. Clin Infect Dis 59:1638–1647 http://dx.doi.org/10.1093/cid/ciu641.
255. Tadokera R, Meintjes G, Skolimowska KH, Wilkinson KA, Matthews K, Seldon R, Chegou NN, Maartens G, Rangaka MX, Rebe K, Walzl G, Wilkinson RJ. 2011. Hypercytokinaemia accompanies HIV-tuberculosis immune reconstitution inflammatory syndrome. Eur Respir J 37:1248–1259 http://dx.doi.org/10.1183/09031936.00091010.
256. Ravimohan S, Tamuhla N, Steenhoff AP, Letlhogile R, Nfanyana K, Bellamy SL, MacGregor RR, Gross R, Weissman D, Bisson GP. 2015. Immunological profiling of tuberculosis-associated immune reconstitution inflammatory syndrome and non-immune reconstitution inflammatory syndrome death in HIV-infected adults with pulmonary tuberculosis starting antiretroviral therapy: a prospective observational cohort study. Lancet Infect Dis 15:429–438 http://dx.doi.org/10.1016/S1473-3099(15)70008-3.
257. Conesa-Botella A, Meintjes G, Coussens AK, van der Plas H, Goliath R, Schutz C, Moreno-Reyes R, Mehta M, Martineau AR, Wilkinson RJ, Colebunders R, Wilkinson KA. 2012. Corticosteroid therapy, vitamin D status, and inflammatory cytokine profile in the HIV-tuberculosis immune reconstitution inflammatory syndrome. Clin Infect Dis 55:1004–1011 http://dx.doi.org/10.1093/cid/cis577.
258. Meintjes G, Skolimowska KH, Wilkinson KA, Matthews K, Tadokera R, Conesa-Botella A, Seldon R, Rangaka MX, Rebe K, Pepper DJ, Morroni C, Colebunders R, Maartens G, Wilkinson RJ. 2012. Corticosteroid-modulated immune activation in the tuberculosis immune reconstitution inflammatory syndrome. Am J Respir Crit Care Med 186:369–377 http://dx.doi.org/10.1164/rccm.201201-0094OC.
259. Oliver BG, Elliott JH, Price P, Phillips M, Saphonn V, Vun MC, Kaldor JM, Cooper DA, French MA. 2010. Mediators of innate and adaptive immune responses differentially affect immune restoration disease associated with Mycobacterium tuberculosis in HIV patients beginning antiretroviral therapy. J Infect Dis 202:1728–1737 http://dx.doi.org/10.1086/657082.
260. Oliver BG, Elliott JH, Price P, Phillips M, Cooper DA, French MA. 2012. Tuberculosis after commencing antiretroviral therapy for HIV infection is associated with elevated CXCL9 and CXCL10 responses to Mycobacterium tuberculosis antigens. J Acquir Immune Defic Syndr 61:287–292 http://dx.doi.org/10.1097/QAI.0b013e31826445ef.
261. Tan HY, Yong YK, Andrade BB, Shankar EM, Ponnampalavanar S, Omar SF, Narendran G, Kamarulzaman A, Swaminathan S, Sereti I, Crowe SM, French MA. 2015. Plasma interleukin-18 levels are a biomarker of innate immune responses that predict and characterize tuberculosis-associated immune reconstitution inflammatory syndrome. AIDS 29:421–431 http://dx.doi.org/10.1097/QAD.0000000000000557.
262. Lande R, Giacomini E, Grassi T, Remoli ME, Iona E, Miettinen M, Julkunen I, Coccia EM. 2003. IFN-alpha beta released by Mycobacterium tuberculosis-infected human dendritic cells induces the expression of CXCL10: selective recruitment of NK and activated T cells.J Immunol 170:1174–1182 http://dx.doi.org/10.4049/jimmunol.170.3.1174.
263. Moser B, Loetscher P. 2001. Lymphocyte traffic control by chemokines. Nat Immunol 2:123–128 http://dx.doi.org/10.1038/84219.
264. Mayer-Barber KD, Andrade BB, Barber DL, Hieny S, Feng CG, Caspar P, Oland S, Gordon S, Sher A. 2011. Innate and adaptive interferons suppress IL-1α and IL-1β production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 35:1023–1034 http://dx.doi.org/10.1016/j.immuni.2011.12.002.
265. McNab FW, Ewbank J, Howes A, Moreira-Teixeira L, Martirosyan A, Ghilardi N, Saraiva M, O’Garra A. 2014. Type I IFN induces IL-10 production in an IL-27-independent manner and blocks responsiveness to IFN-γ for production of IL-12 and bacterial killing in Mycobacterium tuberculosis-infected macrophages. J Immunol 193:3600–3612 http://dx.doi.org/10.4049/jimmunol.1401088.
266. Haridas V, Pean P, Jasenosky LD, Madec Y, Laureillard D, Sok T, Sath S, Borand L, Marcy O, Chan S, Tsitsikov E, Delfraissy JF, Blanc FX, Goldfeld AE, CAPRI-T (ANRS 12164) Study Team. 2015. TB-IRIS, T-cell activation, and remodeling of the T-cell compartment in highly immunosuppressed HIV-infected patients with TB. AIDS 29:263–273 http://dx.doi.org/10.1097/QAD.0000000000000546.
267. Elkington P, Shiomi T, Breen R, Nuttall RK, Ugarte-Gil CA, Walker NF, Saraiva L, Pedersen B, Mauri F, Lipman M, Edwards DR, Robertson BD, D’Armiento J, Friedland JS. 2011. MMP-1 drives immunopathology in human tuberculosis and transgenic mice. J Clin Invest 121:1827–1833 http://dx.doi.org/10.1172/JCI45666.
268. Elkington PT, Nuttall RK, Boyle JJ, O’Kane CM, Horncastle DE, Edwards DR, Friedland JS. 2005. Mycobacterium tuberculosis, but not vaccine BCG, specifically upregulates matrix metalloproteinase-1. Am J Respir Crit Care Med 172:1596–1604 http://dx.doi.org/10.1164/rccm.200505-753OC.
269. Walker NF, Clark SO, Oni T, Andreu N, Tezera L, Singh S, Saraiva L, Pedersen B, Kelly DL, Tree JA, D’Armiento JM, Meintjes G, Mauri FA, Williams A, Wilkinson RJ, Friedland JS, Elkington PT. 2012. Doxycycline and HIV infection suppress tuberculosis-induced matrix metalloproteinases. Am J Respir Crit Care Med 185:989–997 http://dx.doi.org/10.1164/rccm.201110-1769OC.
270. Tadokera R, Meintjes GA, Wilkinson KA, Skolimowska KH, Walker N, Friedland JS, Maartens G, Elkington PT, Wilkinson RJ. 2014. Matrix metalloproteinases and tissue damage in HIV-tuberculosis immune reconstitution inflammatory syndrome. Eur J Immunol 44:127–136 http://dx.doi.org/10.1002/eji.201343593.
271. Bourgarit A, Carcelain G, Martinez V, Lascoux C, Delcey V, Gicquel B, Vicaut E, Lagrange PH, Sereni D, Autran B. 2006. Explosion of tuberculin-specific Th1-responses induces immune restoration syndrome in tuberculosis and HIV co-infected patients. AIDS 20:F1–F7 http://dx.doi.org/10.1097/01.aids.0000202648.18526.bf.
272. Meintjes G, Wilkinson KA, Rangaka MX, Skolimowska K, van Veen K, Abrahams M, Seldon R, Pepper DJ, Rebe K, Mouton P, van Cutsem G, Nicol MP, Maartens G, Wilkinson RJ. 2008. Type 1 helper T cells and FoxP3-positive T cells in HIV-tuberculosis-associated immune reconstitution inflammatory syndrome. Am J Respir Crit Care Med 178:1083–1089 http://dx.doi.org/10.1164/rccm.200806-858OC.
273. Tieu HV, Ananworanich J, Avihingsanon A, Apateerapong W, Sirivichayakul S, Siangphoe U, Klongugkara S, Boonchokchai B, Hammer SM, Manosuthi W. 2009. Immunologic markers as predictors of tuberculosis-associated immune reconstitution inflammatory syndrome in HIV and tuberculosis coinfected persons in Thailand. AIDS Res Hum Retroviruses 25:1083–1089 http://dx.doi.org/10.1089/aid.2009.0055.
274. Elliott JH, Vohith K, Saramony S, Savuth C, Dara C, Sarim C, Huffam S, Oelrichs R, Sophea P, Saphonn V, Kaldor J, Cooper DA, Chhi Vun M, French MA. 2009. Immunopathogenesis and diagnosis of tuberculosis and tuberculosis-associated immune reconstitution inflammatory syndrome during early antiretroviral therapy. J Infect Dis 200:1736–1745 http://dx.doi.org/10.1086/644784.
275. Antonelli LR, Mahnke Y, Hodge JN, Porter BO, Barber DL, DerSimonian R, Greenwald JH, Roby G, Mican J, Sher A, Roederer M, Sereti I. 2010. Elevated frequencies of highly activated CD4+ T cells in HIV+ patients developing immune reconstitution inflammatory syndrome. Blood 116:3818–3827 http://dx.doi.org/10.1182/blood-2010-05-285080.
276. Seddiki N, Sasson SC, Santner-Nanan B, Munier M, van Bockel D, Ip S, Marriott D, Pett S, Nanan R, Cooper DA, Zaunders JJ, Kelleher AD. 2009. Proliferation of weakly suppressive regulatory CD4+ T cells is associated with over-active CD4+ T-cell responses in HIV-positive patients with mycobacterial immune restoration disease. Eur J Immunol 39:391–403 http://dx.doi.org/10.1002/eji.200838630.
277. Tan DB, Yong YK, Tan HY, Kamarulzaman A, Tan LH, Lim A, James I, French M, Price P. 2008. Immunological profiles of immune restoration disease presenting as mycobacterial lymphadenitis and cryptococcal meningitis. HIV Med 9:307–316 http://dx.doi.org/10.1111/j.1468-1293.2008.00565.x.
278. Takahashi Y, Tanaka Y, Yamashita A, Koyanagi Y, Nakamura M, Yamamoto N. 2001. OX40 stimulation by gp34/OX40 ligand enhances productive human immunodeficiency virus type 1 infection. J Virol 75:6748–6757 http://dx.doi.org/10.1128/JVI.75.15.6748-6757.2001.
279. Kabelitz D, Wesch D. 2003. Features and functions of gamma delta T lymphocytes: focus on chemokines and their receptors. Crit Rev Immunol 23:339–370 http://dx.doi.org/10.1615/CritRevImmunol.v23.i56.10.
280. Saunders BM, Frank AA, Cooper AM, Orme IM. 1998. Role of gamma delta T cells in immunopathology of pulmonary Mycobacterium avium infection in mice. Infect Immun 66:5508–5514. [PubMed]
281. 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.
282. Gioia C, Agrati C, Casetti R, Cairo C, Borsellino G, Battistini L, Mancino G, Goletti D, Colizzi V, Pucillo LP, Poccia F. 2002. Lack of CD27-CD45RA-V gamma 9V delta 2+ T cell effectors in immunocompromised hosts and during active pulmonary tuberculosis. J Immunol 168:1484–1489 http://dx.doi.org/10.4049/jimmunol.168.3.1484.
283. Rojas RE, Chervenak KA, Thomas J, Morrow J, Nshuti L, Zalwango S, Mugerwa RD, Thiel BA, Whalen CC, Boom WH. 2005. Vdelta2+ gammadelta T cell function in Mycobacterium tuberculosis- and HIV-1-positive patients in the United States and Uganda: application of a whole-blood assay. J Infect Dis 192:1806–1814 http://dx.doi.org/10.1086/497146.
284. Bourgarit A, Carcelain G, Samri A, Parizot C, Lafaurie M, Abgrall S, Delcey V, Vicaut E, Sereni D, Autran B, PARADOX Study Group. 2009. Tuberculosis-associated immune restoration syndrome in HIV-1-infected patients involves tuberculin-specific CD4 Th1 cells and KIR-negative gammadelta T cells. J Immunol 183:3915–3923 http://dx.doi.org/10.4049/jimmunol.0804020.
285. Espinosa E, Ormsby CE, Vega-Barrientos RS, Ruiz-Cruz M, Moreno-Coutiño G, Peña-Jiménez A, Peralta-Prado AB, Cantoral-Díaz M, Romero-Rodríguez DP, Reyes-Terán G. 2010. Risk factors for immune reconstitution inflammatory syndrome under combination antiretroviral therapy can be aetiology-specific. Int J STD AIDS 21:573–579 http://dx.doi.org/10.1258/ijsa.2010.010135.
286. Deffur A, Mulder NJ, Wilkinson RJ. 2013. Co-infection with Mycobacterium tuberculosis and human immunodeficiency virus: an overview and motivation for systems approaches. Pathog Dis 69:101–113 http://dx.doi.org/10.1111/2049-632X.12060.
287. Lai RP, Meintjes G, Wilkinson RJ. 2015. HIV-1 tuberculosis-associated immune reconstitution inflammatory syndrome. Semin Immunopathol 38:185–198. [PubMed]
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/content/journal/microbiolspec/10.1128/microbiolspec.TBTB2-0012-2016
2016-12-16
2017-11-24

Abstract:

The modulation of tuberculosis (TB)-induced immunopathology caused by human immunodeficiency virus (HIV)-1 coinfection remains incompletely understood but underlies the change seen in the natural history, presentation, and prognosis of TB in such patients. The deleterious combination of these two pathogens has been dubbed a “deadly syndemic,” with each favoring the replication of the other and thereby contributing to accelerated disease morbidity and mortality. HIV-1 is the best-recognized risk factor for the development of active TB and accounts for 13% of cases globally. The advent of combination antiretroviral therapy (ART) has considerably mitigated this risk. Rapid roll-out of ART globally and the recent recommendation by the World Health Organization (WHO) to initiate ART for everyone living with HIV at any CD4 cell count should lead to further reductions in HIV-1-associated TB incidence because susceptibility to TB is inversely proportional to CD4 count. However, it is important to note that even after successful ART, patients with HIV-1 are still at increased risk for TB. Indeed, in settings of high TB incidence, the occurrence of TB often remains the first presentation of, and thereby the entry into, HIV care. As advantageous as ART-induced immune recovery is, it may also give rise to immunopathology, especially in the lower-CD4-count strata in the form of the immune reconstitution inflammatory syndrome. TB-immune reconstitution inflammatory syndrome will continue to impact the HIV-TB syndemic.

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Figures

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FIGURE 1

Spectrum of disease in HIV-TB coinfection. The axis represents stages of tuberculosis, from infection through to active disease, while the axis represents stages of HIV-1 infection. bacterial burden and CD4 count are shown in blue along the respective axes. The spectrum of latent TB is represented as follows: infection eliminated without priming antigen-specific T cells; infection eliminated in association with T-cell priming; infection contained with some bacteria persisting in a nonreplicating form; bacterial replication maintained at the subclinical level by the immune system. Clinical disease (pulmonary and extrapulmonary tuberculosis) occurs in a subset of individuals who are latently infected or who develop primary tuberculosis directly following infection or reinfection. The annual risk is represented as follows: HIV-1-uninfected: about 10% lifetime risk or about 1% per annum (p/a); shortly after HIV-1 infection and prior to substantial CD4 T-cell depletion, the risk of active tuberculosis increases; during the early stages of HIV-1 infection, this risk rises to approximately 10% p/a; in late-stage HIV-1 infection, the risk of active tuberculosis increases to 30% p/a. The effects of HIV-1 on tuberculosis and of tuberculosis on HIV-1 disease are shown by the red arrows. Reproduced from ( 286 ) with permission of the publisher.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0012-2016
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Image of FIGURE 2
FIGURE 2

A model of innate receptor signaling in mediating TB-IRIS pathogenesis as proposed by Lai et al. Microarray profiling revealed that TLR signaling and inflammasome activation are critical in mediating TB-IRIS pathogenesis. The proposed model begins with antigen recognition by surface-expressing TLRs, which triggers the downstream signaling cascade with adaptor molecules such as MyD88 and IRAK4 to activate IRF7, thereby triggering the production of type I IFN. Paracrine signaling of type I IFN to IFNAR recruits and phosphorylates STAT1/2 dimers, leading to further recruitment of IRF9 and the formation of ISGF3, thereby inducing pro-caspase-11 (caspase-4/5 in human) and AIM-2 inflammasome (caspase-1). Caspase-11 cleaves IL-1α into its mature form and can lead to pyroptosis. The noncanonical inflammasome (caspase-11) can also activate the canonical inflammasome (caspase-1), which cleaves IL-1β and IL-18 into their mature form. Alternatively, TLR signaling via MyD88 can also activate NF-κB via the TAK1/IKK complex. Activation of NF-κB triggers the production of an array of cytokines, including TNF-α, IL-6, and IL-12. In addition, NF-κB also activates NLRP1/3 inflammasomes and subsequently leads to the production of IL-1β and IL-18. Reproduced from ( 287 ) with permission of the publisher.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0012-2016
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Tables

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TABLE 1

-derived PAMPs and cytokines mediating enhanced HIV-1 replication : PAMP-mediated activation of HIV-LTR

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0012-2016
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TABLE 2

-derived cytokines mediating enhanced HIV-1 replication: cytokines produced in response activating HIV-1 LTR

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0012-2016
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TABLE 3

T lymphocyte dysfunction in the setting of HIV-TB coinfection and the effect of ART

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.TBTB2-0012-2016

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