1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Myeloid Cell Phenotypes in Susceptibility and Resistance to Helminth Parasite Infections

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Authors: Rick M. Maizels1, James P. Hewitson2
  • Editor: Siamon Gordon3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Wellcome Trust Centre for Molecular Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow G12 8TA, United Kingdom; 2: Department of Biology, University of York, York YO10 5DD, United Kingdom; 3: Oxford University, Oxford, United Kingdom
  • Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.MCHD-0043-2016
  • Received 15 July 2016 Accepted 28 September 2016 Published 23 November 2016
  • Rick M. Maizels, rick.maizels@glasgow.ac.uk
image of Myeloid Cell Phenotypes in Susceptibility and Resistance to Helminth Parasite Infections
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    Myeloid Cell Phenotypes in Susceptibility and Resistance to Helminth Parasite Infections, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/4/6/MCHD-0043-2016-1.gif /docserver/preview/fulltext/microbiolspec/4/6/MCHD-0043-2016-2.gif
  • Abstract:

    Many major tropical diseases are caused by long-lived helminth parasites that are able to survive by modulation of the host immune system, including the innate compartment of myeloid cells. In particular, dendritic cells and macrophages show markedly altered phenotypes during parasite infections. In addition, many specialized subsets such as eosinophils and basophils expand dramatically in response to these pathogens. The changes in phenotype and function, and their effects on both immunity to infection and reactivity to bystander antigens such as allergens, are discussed.

  • Citation: Maizels R, Hewitson J. 2016. Myeloid Cell Phenotypes in Susceptibility and Resistance to Helminth Parasite Infections. Microbiol Spectrum 4(6):MCHD-0043-2016. doi:10.1128/microbiolspec.MCHD-0043-2016.

Key Concept Ranking

Innate Immune System
0.7243851
Infection and Immunity
0.68110466
Immune Systems
0.53957814
Mast Cells
0.5106358
Tumor Necrosis Factor
0.462458
Interferon Regulatory Factors
0.43754342
0.7243851

References

1. Gomez Perdiguero E, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L, Garner H, Trouillet C, de Bruijn MF, Geissmann F, Rodewald HR. 2015. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518:547–551. [PubMed]
2. Bain CC, Hawley CA, Garner H, Scott CL, Schridde A, Steers NJ, Mack M, Joshi A, Guilliams M, Mowat AM, Geissmann F, Jenkins SJ. 2016. Long-lived self-renewing bone marrow-derived macrophages displace embryo-derived cells to inhabit adult serous cavities. Nat Commun 7:ncomms11852. doi:10.1038/ncomms11852.
3. Merad M, Sathe P, Helft J, Miller J, Mortha A. 2013. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 31:563–604. [PubMed]
4. Bogdan C. 2008. Mechanisms and consequences of persistence of intracellular pathogens: leishmaniasis as an example. Cell Microbiol 10:1221–1234. [PubMed]
5. Mashayekhi M, Sandau MM, Dunay IR, Frickel EM, Khan A, Goldszmid RS, Sher A, Ploegh HL, Murphy TL, Sibley LD, Murphy KM. 2011. CD8α+ dendritic cells are the critical source of interleukin-12 that controls acute infection by Toxoplasma gondii tachyzoites. Immunity 35:249–259. [PubMed]
6. Ribeiro-Gomes FL, Sacks D. 2012. The influence of early neutrophil-Leishmania interactions on the host immune response to infection. Front Cell Infect Microbiol 2:59. doi:10.3389/fcimb.2012.00059.
7. Beattie L, d’El-Rei Hermida M, Moore JW, Maroof A, Brown N, Lagos D, Kaye PM. 2013. A transcriptomic network identified in uninfected macrophages responding to inflammation controls intracellular pathogen survival. Cell Host Microbe 14:357–368. [PubMed]
8. Cadman ET, Lawrence RA. 2010. Granulocytes: effector cells or immunomodulators in the immune response to helminth infection? Parasite Immunol 32:1–19. [PubMed]
9. Barron L, Wynn TA. 2011. Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. Eur J Immunol 41:2509–2514. [PubMed]
10. Brown TR. 1898. Studies on trichinosis, with especial reference to the increase of the eosinophilic cells in the blood and the muscle, the origin of these cells and their diagnostic importance. J Exp Med 3:315–347. [PubMed]
11. Klion AD, Nutman TB. 2004. The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol 113:30–37. [PubMed]
12. Huang L, Appleton JA. 2016. Eosinophils in helminth infection: defenders and dupes. Trends Parasitol 32:798–807. [PubMed]
13. Ohnmacht C, Voehringer D. 2009. Basophil effector function and homeostasis during helminth infection. Blood 113:2816–2825. [PubMed]
14. Miller HR. 1996. Mucosal mast cells and the allergic response against nematode parasites. Vet Immunol Immunopathol 54:331–336. [PubMed]
15. van Panhuys N, Prout M, Forbes E, Min B, Paul WE, Le Gros G. 2011. Basophils are the major producers of IL-4 during primary helminth infection. J Immunol 186:2719–2728. [PubMed]
16. Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, Chawla A, Locksley RM. 2011. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332:243–247. [PubMed]
17. Allen JE, Maizels RM. 2011. Diversity and dialogue in immunity to helminths. Nat Rev Immunol 11:375–388. [PubMed]
18. Cook PC, Jones LH, Jenkins SJ, Wynn TA, Allen JE, MacDonald AS. 2012. Alternatively activated dendritic cells regulate CD4+ T-cell polarization in vitro and in vivo. Proc Natl Acad Sci U S A 109:9977–9982. [PubMed]
19. Chen F, Wu W, Millman A, Craft JF, Chen E, Patel N, Boucher JL, Urban JF, Jr, Kim CC, Gause WC. 2014. Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat Immunol 15:938–946. [PubMed]
20. Allen JE, Wynn TA. 2011. Evolution of Th2 immunity: a rapid repair response to tissue destructive pathogens. PLoS Pathog 7:e1002003. doi:10.1371/journal.ppat.1002003. [PubMed]
21. Saenz SA, Taylor BC, Artis D. 2008. Welcome to the neighborhood: epithelial cell-derived cytokines license innate and adaptive immune responses at mucosal sites. Immunol Rev 226:172–190. [PubMed]
22. MacDonald AS, Straw AD, Bauman B, Pearce EJ. 2001. CD8 dendritic cell activation status plays an integral role in influencing Th2 response development. J Immunol 167:1982–1988. [PubMed]
23. Balic A, Harcus Y, Holland MJ, Maizels RM. 2004. Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur J Immunol 34:3047–3059. [PubMed]
24. Phythian-Adams AT, Cook PC, Lundie RJ, Jones LH, Smith KA, Barr TA, Hochweller K, Anderton SM, Hämmerling GJ, Maizels RM, MacDonald AS. 2010. CD11c depletion severely disrupts Th2 induction and development in vivo. J Exp Med 207:2089–2096. [PubMed]
25. Smith KA, Hochweller K, Hämmerling GJ, Boon L, Macdonald AS, Maizels RM. 2011. Chronic helminth infection mediates tolerance in vivo through dominance of CD11clo CD103 DC population. J Immunol 186:7098–7109. [PubMed]
26. Smith KA, Harcus Y, Garbi N, Hämmerling GJ, MacDonald AS, Maizels RM. 2012. Type 2 innate immunity in helminth infection is induced redundantly and acts autonomously following CD11c+ cell depletion. Infect Immun 80:3481–3489. [PubMed]
27. Hammad H, Plantinga M, Deswarte K, Pouliot P, Willart MA, Kool M, Muskens F, Lambrecht BN. 2010. Inflammatory dendritic cells—not basophils—are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J Exp Med 207:2097–2111. [PubMed]
28. Kumamoto Y, Linehan M, Weinstein JS, Laidlaw BJ, Craft JE, Iwasaki A. 2013. CD301b+ dermal dendritic cells drive T helper 2 cell-mediated immunity. Immunity 39:733–743. [PubMed]
29. Everts B, Tussiwand R, Dreesen L, Fairfax KC, Huang SC, Smith AM, O’Neill CM, Lam WY, Edelson BT, Urban JF, Jr, Murphy KM, Pearce EJ. 2016. Migratory CD103+ dendritic cells suppress helminth-driven type 2 immunity through constitutive expression of IL-12. J Exp Med 213:35–51. [PubMed]
30. Gao Y, Nish SA, Jiang R, Hou L, Licona-Limón P, Weinstein JS, Zhao H, Medzhitov R. 2013. Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 39:722–732. [PubMed]
31. Tussiwand R, Everts B, Grajales-Reyes GE, Kretzer NM, Iwata A, Bagaitkar J, Wu X, Wong R, Anderson DA, Murphy TL, Pearce EJ, Murphy KM. 2015. Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses. Immunity 42:916–928. [PubMed]
32. Chan PY, Carrera Silva EA, De Kouchkovsky D, Joannas LD, Hao L, Hu D, Huntsman S, Eng C, Licona-Limón P, Weinstein JS, Herbert DR, Craft JE, Flavell RA, Repetto S, Correale J, Burchard EG, Torgerson DG, Ghosh S, Rothlin CV. 2016. The TAM family receptor tyrosine kinase TYRO3 is a negative regulator of type 2 immunity. Science 352:99–103. [PubMed]
33. Zaccone P, Burton O, Miller N, Jones FM, Dunne DW, Cooke A. 2009. Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice. Eur J Immunol 39:1098–1107. [PubMed]
34. Dowling DJ, Hamilton CM, Donnelly S, La Course J, Brophy PM, Dalton J, O’Neill SM. 2010. Major secretory antigens of the helminth Fasciola hepatica activate a suppressive dendritic cell phenotype that attenuates Th17 cells but fails to activate Th2 immune responses. Infect Immun 78:793–801. [PubMed]
35. Falcón C, Carranza F, Martínez FF, Knubel CP, Masih DT, Motrán CC, Cervi L. 2010. Excretory-secretory products (ESP) from Fasciola hepatica induce tolerogenic properties in myeloid dendritic cells. Vet Immunol Immunopathol 137:36–46. [PubMed]
36. Gruden-Movsesijan A, Ilic N, Colic M, Majstorovic I, Vasilev S, Radovic I, Sofronic-Milosavljevic L. 2011. The impact of Trichinella spiralis excretory-secretory products on dendritic cells. Comp Immunol Microbiol Infect Dis 34:429–439. [PubMed]
37. Aranzamendi C, Fransen F, Langelaar M, Franssen F, van der Ley P, van Putten JP, Rutten V, Pinelli E. 2012. Trichinella spiralis-secreted products modulate DC functionality and expand regulatory T cells in vitro. Parasite Immunol 34:210–223. [PubMed]
38. Blum AM, Hang L, Setiawan T, Urban JP, Jr, Stoyanoff KM, Leung J, Weinstock JV. 2012. Heligmosomoides polygyrus bakeri induces tolerogenic dendritic cells that block colitis and prevent antigen-specific gut T cell responses. J Immunol 189:2512–2520. [PubMed]
39. Matisz CE, Leung G, Reyes JL, Wang A, Sharkey KA, McKay DM. 2015. Adoptive transfer of helminth antigen-pulsed dendritic cells protects against the development of experimental colitis in mice. Eur J Immunol 45:3126–3139. [PubMed]
40. Sofronic-Milosavljevic LJ, Radovic I, Ilic N, Majstorovic I, Cvetkovic J, Gruden-Movsesijan A. 2013. Application of dendritic cells stimulated with Trichinella spiralis excretory-secretory antigens alleviates experimental autoimmune encephalomyelitis. Med Microbiol Immunol (Berl) 202:239–249. [PubMed]
41. Everts B, Smits HH, Hokke CH, Yazdankbakhsh M. 2010. Sensing of helminth infections by dendritic cells via pattern recognition receptors and beyond: consequences for T helper 2 and regulatory T cell polarization. Eur J Immunol 40:1525–1537. [PubMed]
42. Marshall FA, Pearce EJ. 2008. Uncoupling of induced protein processing from maturation in dendritic cells exposed to a highly antigenic preparation from a helminth parasite. J Immunol 181:7562–7570.
43. Cervi L, MacDonald AS, Kane C, Dzierszinski F, Pearce EJ. 2004. Cutting edge: dendritic cells copulsed with microbial and helminth antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments, and concurrently induce microbe-specific Th1 and helminth-specific Th2 responses. J Immunol 172:2016–2020. [PubMed]
44. Segura M, Su Z, Piccirillo C, Stevenson MM. 2007. Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. Eur J Immunol 37:1887–1904. [PubMed]
45. Langelaar M, Aranzamendi C, Franssen F, Van Der Giessen J, Rutten V, van der Ley P, Pinelli E. 2009. Suppression of dendritic cell maturation by Trichinella spiralis excretory/secretory products. Parasite Immunol 31:641–645. [PubMed]
46. Terrazas CA, Alcántara-Hernández M, Bonifaz L, Terrazas LI, Satoskar AR. 2013. Helminth-excreted/secreted products are recognized by multiple receptors on DCs to block the TLR response and bias Th2 polarization in a cRAF dependent pathway. FASEB J 27:4547–4560. [PubMed]
47. Everts B, Perona-Wright G, Smits HH, Hokke CH, van der Ham AJ, Fitzsimmons CM, Doenhoff MJ, van der Bosch J, Mohrs K, Haas H, Mohrs M, Yazdanbakhsh M, Schramm G. 2009. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J Exp Med 206:1673–1680. [PubMed]
48. Steinfelder S, Andersen JF, Cannons JL, Feng CG, Joshi M, Dwyer D, Caspar P, Schwartzberg PL, Sher A, Jankovic D. 2009. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J Exp Med 206:1681–1690. [PubMed]
49. Everts B, Hussaarts L, Driessen NN, Meevissen MH, Schramm G, van der Ham AJ, van der Hoeven B, Scholzen T, Burgdorf S, Mohrs M, Pearce EJ, Hokke CH, Haas H, Smits HH, Yazdanbakhsh M. 2012. Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. J Exp Med 209:1753–1767, S1.
50. Cook PC, Owen H, Deaton AM, Borger JG, Brown SL, Clouaire T, Jones GR, Jones LH, Lundie RJ, Marley AK, Morrison VL, Phythian-Adams AT, Wachter E, Webb LM, Sutherland TE, Thomas GD, Grainger JR, Selfridge J, McKenzie AN, Allen JE, Fagerholm SC, Maizels RM, Ivens AC, Bird A, MacDonald AS. 2015. A dominant role for the methyl-CpG-binding protein Mbd2 in controlling Th2 induction by dendritic cells. Nat Commun 6:6920. doi:10.1038/ncomms7920.
51. Gordon S. 2003. Alternative activation of macrophages. Nat Rev Immunol 3:23–35. [PubMed]
52. Martinez FO, Helming L, Gordon S. 2009. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27:451–483. [PubMed]
53. Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, Locati M, Mantovani A, Martinez FO, Mege JL, Mosser DM, Natoli G, Saeij JP, Schultze JL, Shirey KA, Sica A, Suttles J, Udalova I, van Ginderachter JA, Vogel SN, Wynn TA. 2014. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41:14–20. [PubMed]
54. Allen JE, Lawrence RA, Maizels RM. 1996. Antigen presenting cells from mice harboring the filarial nematode, Brugia malayi, prevent cellular proliferation but not cytokine production. Int Immunol 8:143–151. [PubMed]
55. Kreider T, Anthony RM, Urban JF, Jr, Gause WC. 2007. Alternatively activated macrophages in helminth infections. Curr Opin Immunol 19:448–453. [PubMed]
56. Raes G, De Baetselier P, Noël W, Beschin A, Brombacher F, Hassanzadeh Gh G. 2002. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukoc Biol 71:597–602. [PubMed]
57. Raes G, Beschin A, Ghassabeh GH, De Baetselier P. 2007. Alternatively activated macrophages in protozoan infections. Curr Opin Immunol 19:454–459. [PubMed]
58. Nair MG, Gallagher IJ, Taylor MD, Loke P, Coulson PS, Wilson RA, Maizels RM, Allen JE. 2005. Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infect Immun 73:385–394. [PubMed]
59. Sutherland TE, Maizels RM, Allen JE. 2009. Chitinases and chitinase-like proteins: potential therapeutic targets for the treatment of T-helper type 2 allergies. Clin Exp Allergy 39:943–955. [PubMed]
60. Pesce JT, Ramalingam TR, Mentink-Kane MM, Wilson MS, El Kasmi KC, Smith AM, Thompson RW, Cheever AW, Murray PJ, Wynn TA. 2009. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog 5:e1000371. doi:10.1371/journal.ppat.1000371. [PubMed]
61. Herbert DR, Orekov T, Roloson A, Ilies M, Perkins C, O’Brien W, Cederbaum S, Christianson DW, Zimmermann N, Rothenberg ME, Finkelman FD. 2010. Arginase I suppresses IL-12/IL-23p40-driven intestinal inflammation during acute schistosomiasis. J Immunol 184:6438–6446. [PubMed]
62. O’Neill LA, Pearce EJ. 2016. Immunometabolism governs dendritic cell and macrophage function. J Exp Med 213:15–23. [PubMed]
63. Gondorf F, Berbudi A, Buerfent BC, Ajendra J, Bloemker D, Specht S, Schmidt D, Neumann AL, Layland LE, Hoerauf A, Hübner MP. 2015. Chronic filarial infection provides protection against bacterial sepsis by functionally reprogramming macrophages. PLoS Pathog 11:e1004616. doi:10.1371/journal.ppat.1004616.
64. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, MacDonald AS, Allen JE. 2011. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332:1284–1288. [PubMed]
65. Girgis NM, Gundra UM, Ward LN, Cabrera M, Frevert U, Loke P. 2014. Ly6Chigh monocytes become alternatively activated macrophages in schistosome granulomas with help from CD4+ cells. PLoS Pathog 10:e1004080. doi:10.1371/journal.ppat.1004080.
66. Nascimento M, Huang SC, Smith A, Everts B, Lam W, Bassity E, Gautier EL, Randolph GJ, Pearce EJ. 2014. Ly6Chi monocyte recruitment is responsible for Th2 associated host-protective macrophage accumulation in liver inflammation due to schistosomiasis. PLoS Pathog 10:e1004282. doi:10.1371/journal.ppat.1004282.
67. Gundra UM, Girgis NM, Ruckerl D, Jenkins S, Ward LN, Kurtz ZD, Wiens KE, Tang MS, Basu-Roy U, Mansukhani A, Allen JE, Loke P. 2014. Alternatively activated macrophages derived from monocytes and tissue macrophages are phenotypically and functionally distinct. Blood 123:e110–e122. doi:10.1182/blood-2013-08-520619.
68. Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, Jung S, Amit I. 2014. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159:1312–1326. [PubMed]
69. van de Laar L, Saelens W, De Prijck S, Martens L, Scott CL, Van Isterdael G, Hoffmann E, Beyaert R, Saeys Y, Lambrecht BN, Guilliams M. 2016. Yolk sac macrophages, fetal liver, and adult monocytes can colonize an empty niche and develop into functional tissue-resident macrophages. Immunity 44:755–768. [PubMed]
70. Reece JJ, Siracusa MC, Scott AL. 2006. Innate immune responses to lung-stage helminth infection induce alternatively activated alveolar macrophages. Infect Immun 74:4970–4981. [PubMed]
71. Chen F, Liu Z, Wu W, Rozo C, Bowdridge S, Millman A, Van Rooijen N, Urban JF, Jr, Wynn TA, Gause WC. 2012. An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat Med 18:260–266. [PubMed]
72. Bouchery T, Kyle R, Camberis M, Shepherd A, Filbey K, Smith A, Harvie M, Painter G, Johnston K, Ferguson P, Jain R, Roediger B, Delahunt B, Weninger W, Forbes-Blom E, Le Gros G. 2015. ILC2s and T cells cooperate to ensure maintenance of M2 macrophages for lung immunity against hookworms. Nat Commun 6:6970. doi:10.1038/ncomms7970.
73. Steinfelder S, O’Regan NL, Hartmann S. 2016. Diplomatic assistance: can helminth-modulated macrophages act as treatment for inflammatory disease? PLoS Pathog 12:e1005480. doi:10.1371/journal.ppat.1005480.
74. Smith P, Mangan NE, Walsh CM, Fallon RE, McKenzie AN, van Rooijen N, Fallon PG. 2007. Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism. J Immunol 178:4557–4566. [PubMed]
75. Ziegler T, Rausch S, Steinfelder S, Klotz C, Hepworth MR, Kühl AA, Burda PC, Lucius R, Hartmann S. 2015. A novel regulatory macrophage induced by a helminth molecule instructs IL-10 in CD4+ T cells and protects against mucosal inflammation. J Immunol 194:1555–1564. [PubMed]
76. Wolfs IM, Stöger JL, Goossens P, Pöttgens C, Gijbels MJ, Wijnands E, van der Vorst EP, van Gorp P, Beckers L, Engel D, Biessen EA, Kraal G, van Die I, Donners MM, de Winther MP. 2014. Reprogramming macrophages to an anti-inflammatory phenotype by helminth antigens reduces murine atherosclerosis. FASEB J 28:288–299. [PubMed]
77. Ishii M, Wen H, Corsa CA, Liu T, Coelho AL, Allen RM, Carson WF IV, Cavassani KA, Li X, Lukacs NW, Hogaboam CM, Dou Y, Kunkel SL. 2009. Epigenetic regulation of the alternatively activated macrophage phenotype. Blood 114:3244–3254. [PubMed]
78. Filbey KJ, Grainger JR, Smith KA, Boon L, van Rooijen N, Harcus Y, Jenkins S, Hewitson JP, Maizels RM. 2014. Innate and adaptive type 2 immune cell responses in genetically controlled resistance to intestinal helminth infection. Immunol Cell Biol 92:436–448. [PubMed]
79. Anthony RM, Urban JF, Jr, Alem F, Hamed HA, Rozo CT, Boucher JL, Van Rooijen N, Gause WC. 2006. Memory TH2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat Med 12:955–960. [PubMed]
80. Yang Z, Grinchuk V, Urban JF, Jr, Bohl J, Sun R, Notari L, Yan S, Ramalingam T, Keegan AD, Wynn TA, Shea-Donohue T, Zhao A. 2013. Macrophages as IL-25/IL-33-responsive cells play an important role in the induction of type 2 immunity. PLoS One 8:e59441. doi:10.1371/journal.pone.0059441.
81. Bonne-Année S, Kerepesi LA, Hess JA, O’Connell AE, Lok JB, Nolan TJ, Abraham D. 2013. Human and mouse macrophages collaborate with neutrophils to kill larval Strongyloides stercoralis. Infect Immun 81:3346–3355. [PubMed]
82. Zhao A, Urban JF, Jr, Anthony RM, Sun R, Stiltz J, van Rooijen N, Wynn TA, Gause WC, Shea-Donohue T. 2008. Th2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages. Gastroenterology 135:217–225.e1. doi:10.1053/j.gastro.2008.03.077.
83. Esser-von Bieren J, Volpe B, Kulagin M, Sutherland DB, Guiet R, Seitz A, Marsland BJ, Verbeek JS, Harris NL. 2015. Antibody-mediated trapping of helminth larvae requires CD11b and Fcγ receptor I. J Immunol 194:1154–1163. [PubMed]
84. Reyes JL, Terrazas CA, Alonso-Trujillo J, van Rooijen N, Satoskar AR, Terrazas LI. 2010. Early removal of alternatively activated macrophages leads to Taenia crassiceps cysticercosis clearance in vivo. Int J Parasitol 40:731–742. [PubMed]
85. Sullivan BM, Locksley RM. 2009. Basophils: a nonredundant contributor to host immunity. Immunity 30:12–20. [PubMed]
86. Voehringer D. 2013. Protective and pathological roles of mast cells and basophils. Nat Rev Immunol 13:362–375. [PubMed]
87. Min B, Prout M, Hu-Li J, Zhu J, Jankovic D, Morgan ES, Urban JF, Jr, Dvorak AM, Finkelman FD, LeGros G, Paul WE. 2004. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J Exp Med 200:507–517. [PubMed]
88. Wada T, Ishiwata K, Koseki H, Ishikura T, Ugajin T, Ohnuma N, Obata K, Ishikawa R, Yoshikawa S, Mukai K, Kawano Y, Minegishi Y, Yokozeki H, Watanabe N, Karasuyama H. 2010. Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks. J Clin Invest 120:2867–2875. [PubMed]
89. Karasuyama H, Mukai K, Obata K, Tsujimura Y, Wada T. 2011. Nonredundant roles of basophils in immunity. Annu Rev Immunol 29:45–69. [PubMed]
90. Ohnmacht C, Schwartz C, Panzer M, Schiedewitz I, Naumann R, Voehringer D. 2010. Basophils orchestrate chronic allergic dermatitis and protective immunity against helminths. Immunity 33:364–374. [PubMed]
91. Hewitson JP, Filbey KJ, Esser-von Bieren J, Camberis M, Schwartz C, Murray J, Reynolds LA, Blair N, Robertson E, Harcus Y, Boon L, Huang SC, Yang L, Tu Y, Miller MJ, Voehringer D, Le Gros G, Harris N, Maizels RM. 2015. Concerted activity of IgG1 antibodies and IL-4/IL-25-dependent effector cells trap helminth larvae in the tissues following vaccination with defined secreted antigens, providing sterile immunity to challenge infection. PLoS Pathog 11:e1004676. doi:10.1371/journal.ppat.1004676.
92. Schwartz C, Turqueti-Neves A, Hartmann S, Yu P, Nimmerjahn F, Voehringer D. 2014. Basophil-mediated protection against gastrointestinal helminths requires IgE-induced cytokine secretion. Proc Natl Acad Sci U S A 111:E5169–E5177. doi:10.1073/pnas.1412663111.
93. Perrigoue JG, Saenz SA, Siracusa MC, Allenspach EJ, Taylor BC, Giacomin PR, Nair MG, Du Y, Zaph C, van Rooijen N, Comeau MR, Pearce EJ, Laufer TM, Artis D. 2009. MHC class II-dependent basophil-CD4+ T cell interactions promote TH2 cytokine-dependent immunity. Nat Immunol 10:697–705. [PubMed]
94. Sokol CL, Chu NQ, Yu S, Nish SA, Laufer TM, Medzhitov R. 2009. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat Immunol 10:713–720. [PubMed]
95. Sullivan BM, Liang HE, Bando JK, Wu D, Cheng LE, McKerrow JK, Allen CD, Locksley RM. 2011. Genetic analysis of basophil function in vivo. Nat Immunol 12:527–535. [PubMed]
96. Kim S, Prout M, Ramshaw H, Lopez AF, LeGros G, Min B. 2010. Cutting edge: basophils are transiently recruited into the draining lymph nodes during helminth infection via IL-3, but infection-induced Th2 immunity can develop without basophil lymph node recruitment or IL-3. J Immunol 184:1143–1147. [PubMed]
97. Egawa M, Mukai K, Yoshikawa S, Iki M, Mukaida N, Kawano Y, Minegishi Y, Karasuyama H. 2013. Inflammatory monocytes recruited to allergic skin acquire an anti-inflammatory M2 phenotype via basophil-derived interleukin-4. Immunity 38:570–580. [PubMed]
98. Khodoun MV, Orekhova T, Potter C, Morris S, Finkelman FD. 2004. Basophils initiate IL-4 production during a memory T-dependent response. J Exp Med 200:857–870. [PubMed]
99. Abraham SN, St John AL. 2010. Mast cell-orchestrated immunity to pathogens. Nat Rev Immunol 10:440–452. [PubMed]
100. Abe T, Nawa Y. 1988. Worm expulsion and mucosal mast cell response induced by repetitive IL-3 administration in Strongyloides ratti-infected nude mice. Immunology 63:181–185. [PubMed]
101. Borriello F, Longo M, Spinelli R, Pecoraro A, Granata F, Staiano RI, Loffredo S, Spadaro G, Beguinot F, Schroeder J, Marone G. 2015. IL-3 synergises with basophil-derived IL-4 and IL-13 to promote the alternative activation of human monocytes. Eur J Immunol 45:2042–2051. [PubMed]
102. Faulkner H, Humphreys N, Renauld J-C, Van Snick J, Grencis R. 1997. Interleukin-9 is involved in host protective immunity to intestinal nematode infection. Eur J Immunol 27:2536–2540. [PubMed]
103. Turner J-E, Morrison PJ, Wilhelm C, Wilson M, Ahlfors H, Renauld J-C, Panzer U, Helmby H, Stockinger B. 2013. IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J Exp Med 210:2951–2965. [PubMed]
104. Reber LL, Sibilano R, Mukai K, Galli SJ. 2015. Potential effector and immunoregulatory functions of mast cells in mucosal immunity. Mucosal Immunol 8:444–463. [PubMed]
105. Hepworth MR, Daniłowicz-Luebert E, Rausch S, Metz M, Klotz C, Maurer M, Hartmann S. 2012. Mast cells orchestrate type 2 immunity to helminths through regulation of tissue-derived cytokines. Proc Natl Acad Sci U S A 109:6644–6649. [PubMed]
106. Huang L, Gebreselassie NG, Gagliardo LF, Ruyechan MC, Luber KL, Lee NA, Lee JJ, Appleton JA. 2015. Eosinophils mediate protective immunity against secondary nematode infection. J Immunol 194:283–290. [PubMed]
107. Cadman ET, Thysse KA, Bearder S, Cheung AY, Johnston AC, Lee JJ, Lawrence RA. 2014. Eosinophils are important for protection, immunoregulation and pathology during infection with nematode microfilariae. PLoS Pathog 10:e1003988. doi:10.1371/journal.ppat.1003988.
108. Capron M, Capron A. 1992. Effector functions of eosinophils in schistosomiasis. Mem Inst Oswaldo Cruz 87(Suppl 4):167–170. [PubMed]
109. Swartz JM, Dyer KD, Cheever AW, Ramalingam T, Pesnicak L, Domachowske JB, Lee JJ, Lee NA, Foster PS, Wynn TA, Rosenberg HF. 2006. Schistosoma mansoni infection in eosinophil lineage-ablated mice. Blood 108:2420–2427. [PubMed]
110. Dent LA, Daly CM, Mayrhofer G, Zimmerman T, Hallett A, Bignold LP, Creaney J, Parsons JC. 1999. Interleukin-5 transgenic mice show enhanced resistance to primary infections with Nippostrongylus brasiliensis but not primary infections with Toxocara canis. Infect Immun 67:989–993. [PubMed]
111. Fattah DI, Maizels RM, McLaren DJ, Spry CJ. 1986. Toxocara canis: interaction of human blood eosinophils with the infective larvae. Exp Parasitol 61:421–431. [PubMed]
112. Gebreselassie NG, Moorhead AR, Fabre V, Gagliardo LF, Lee NA, Lee JJ, Appleton JA. 2012. Eosinophils preserve parasitic nematode larvae by regulating local immunity. J Immunol 188:417–425. [PubMed]
113. Penttila IA, Ey PL, Jenkin CR. 1984. Infection of mice with Nematospiroides dubius: demonstration of neutrophil-mediated immunity in vivo in the presence of antibodies. Immunology 53:147–154. [PubMed]
114. Penttila IA, Ey PL, Jenkin CR. 1984. Reduced infectivity of Nematospiroides dubius larvae after incubation in vitro with neutrophils or eosinophils from infected mice and a lack of effect by neutrophils from normal mice. Parasite Immunol 6:295–308. [PubMed]
115. Bonne-Année S, Kerepesi LA, Hess JA, Wesolowski J, Paumet F, Lok JB, Nolan TJ, Abraham D. 2014. Extracellular traps are associated with human and mouse neutrophil and macrophage mediated killing of larval Strongyloides stercoralis. Microbes Infect 16:502–511. [PubMed]
116. Sutherland TE, Logan N, Rückerl D, Humbles AA, Allan SM, Papayannopoulos V, Stockinger B, Maizels RM, Allen JE. 2014. Chitinase-like proteins promote IL-17-mediated neutrophilia in a tradeoff between nematode killing and host damage. Nat Immunol 15:1116–1125. [PubMed]
117. Van Ginderachter JA, Beschin A, De Baetselier P, Raes G. 2010. Myeloid-derived suppressor cells in parasitic infections. Eur J Immunol 40:2976–2985. [PubMed]
118. Saleem SJ, Martin RK, Morales JK, Sturgill JL, Gibb DR, Graham L, Bear HD, Manjili MH, Ryan JJ, Conrad DH. 2012. Cutting edge: mast cells critically augment myeloid-derived suppressor cell activity. J Immunol 189:511–515. [PubMed]
119. Morales JK, Saleem SJ, Martin RK, Saunders BL, Barnstein BO, Faber TW, Pullen NA, Kolawole EM, Brooks KB, Norton SK, Sturgill J, Graham L, Bear HD, Urban JF, Jr, Lantz CS, Conrad DH, Ryan JJ. 2014. Myeloid-derived suppressor cells enhance IgE-mediated mast cell responses. J Leukoc Biol 95:643–650. [PubMed]
120. Valanparambil RM, Tam M, Jardim A, Geary TG, Stevenson MM. 2016. Primary Heligmosomoides polygyrus bakeri infection induces myeloid-derived suppressor cells that suppress CD4+ Th2 responses and promote chronic infection. Mucosal Immunol doi:10.1038/mi.2016.36. [PubMed]
121. Reece JJ, Siracusa MC, Southard TL, Brayton CF, Urban JF, Jr, Scott AL. 2008. Hookworm-induced persistent changes to the immunological environment of the lung. Infect Immun 76:3511–3524. [PubMed]
122. Marsland BJ, Kurrer M, Reissmann R, Harris NL, Kopf M. 2008. Nippostrongylus brasiliensis infection leads to the development of emphysema associated with the induction of alternatively activated macrophages. Eur J Immunol 38:479–488. [PubMed]
123. Netea MG, Quintin J, van der Meer JW. 2011. Trained immunity: a memory for innate host defense. Cell Host Microbe 9:355–361. [PubMed]
124. Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F, Cheng SC, Ratter J, Berentsen K, van der Ent MA, Sharifi N, Janssen-Megens EM, Ter Huurne M, Mandoli A, van Schaik T, Ng A, Burden F, Downes K, Frontini M, Kumar V, Giamarellos-Bourboulis EJ, Ouwehand WH, van der Meer JW, Joosten LA, Wijmenga C, Martens JH, Xavier RJ, Logie C, Netea MG, Stunnenberg HG. 2014. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 345:1251086. doi:10.1126/science.1251086.
125. Manoury B, Gregory WF, Maizels RM, Watts C. 2001. Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Curr Biol 11:447–451.
126. Klotz C, Ziegler T, Figueiredo AS, Rausch S, Hepworth MR, Obsivac N, Sers C, Lang R, Hammerstein P, Lucius R, Hartmann S. 2011. A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages. PLoS Pathog 7:e1001248. doi:10.1371/journal.ppat.1001248.
127. Sun Y, Liu G, Li Z, Chen Y, Liu Y, Liu B, Su Z. 2012. Modulation of dendritic cell function and immune response by cysteine protease inhibitor from murine nematode parasite Heligmosomoides polygyrus. Immunology 138:370–381. [PubMed]
microbiolspec.MCHD-0043-2016.citations
cm/4/6
content/journal/microbiolspec/10.1128/microbiolspec.MCHD-0043-2016
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MCHD-0043-2016
2016-11-23
2017-09-19

Abstract:

Many major tropical diseases are caused by long-lived helminth parasites that are able to survive by modulation of the host immune system, including the innate compartment of myeloid cells. In particular, dendritic cells and macrophages show markedly altered phenotypes during parasite infections. In addition, many specialized subsets such as eosinophils and basophils expand dramatically in response to these pathogens. The changes in phenotype and function, and their effects on both immunity to infection and reactivity to bystander antigens such as allergens, are discussed.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error