Pathogenic nematodes suppress humoral responses to third-party antigens in vivo by IL-10-mediated interference with Th cell function

Journal of Immunology

Volumn 187, Issue 8, 2011, Pages 4088-4099

  Hartmann, Wiebke ^a   Haben, Irma ^a   Fleischer, Bernhard ^a,b   Breloer, Minka ^a  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DINITROPHENOL; IMMUNOGLOBULIN G; INTERLEUKIN 10; KEYHOLE LIMPET HEMOCYANIN; PARASITE ANTIGEN; TRANSCRIPTION FACTOR FOXP3;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL FUNCTION; CELL PROLIFERATION; CELL TRANSFER; CONTROLLED STUDY; ENZYME REPRESSION; HELPER CELL; HOST PARASITE INTERACTION; HUMORAL IMMUNITY; IMMUNIZATION; IN VIVO STUDY; LITOMOSOIDES SIGMODONTIS; MOUSE; NEMATODIASIS; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS; B-LYMPHOCYTES; CELL SEPARATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FILARIASIS; FILARIOIDEA; FLOW CYTOMETRY; IMMUNITY, HUMORAL; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 80054760360     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1004136     Document Type: Article

References (61)

1. Maizels, R. M., A. Balic, N. Gomez-Escobar, M. Nair, M. D. Taylor, and J. E. Allen. 2004. Helminth parasites - masters of regulation. Immunol. Rev. 201: 89-116. (Pubitemid 39318446)
2. Hoerauf, A., J. Satoguina, M. Saeftel, and S. Specht. 2005. Immunomodulation by filarial nematodes. Parasite Immunol. 27: 417-429. (Pubitemid 41413489)
3. van Riet, E., F. C. Hartgers, and M. Yazdanbakhsh. 2007. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 212: 475-490. (Pubitemid 46825248)
4. Elias, D., H. Akuffo, and S. Britton. 2006. Helminthes could influence the outcome of vaccines against TB in the tropics. Parasite Immunol. 28: 507-513. (Pubitemid 44370856)
5. Cooper, P. J., M. Chico, C. Sandoval, I. Espinel, A. Guevara, M. M. Levine, G. E. Griffin, and T. B. Nutman. 2001. Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect. Immun. 69: 1574-1580. (Pubitemid 32187611)
6. Elias, D., D. Wolday, H. Akuffo, B. Petros, U. Bronner, and S. Britton. 2001. Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after bacille Calmette-Guérin (BCG) vaccination. Clin. Exp. Immunol. 123: 219-225. (Pubitemid 32174772)
7. Wammes, L. J., F. Hamid, A. E. Wiria, B. de Gier, E. Sartono, R. M. Maizels, A. J. Luty, Y. Fillié, G. T. Brice, T. Supali, et al. 2010. Regulatory T cells in human geohelminth infection suppress immune responses to BCG and Plasmodium falciparum. Eur. J. Immunol. 40: 437-442.
8. Cooper, P. J., I. Espinel, W. Paredes, R. H. Guderian, and T. B. Nutman. 1998. Impaired tetanus-specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role for interleukin-10. J. Infect. Dis. 178: 1133-1138. (Pubitemid 28452209)
9. Cooper, P. J., I. Espinel, M. Wieseman, W. Paredes, M. Espinel, R. H. Guderian, and T. B. Nutman. 1999. Human onchocerciasis and tetanus vaccination: impact on the postvaccination antitetanus antibody response. Infect. Immun. 67: 5951-5957. (Pubitemid 29508123)
10. Nookala, S., S. Srinivasan, P. Kaliraj, R. B. Narayanan, and T. B. Nutman. 2004. Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis. Infect. Immun. 72: 2598-2604. (Pubitemid 38542386)
11. Specht, S., and A. Hoerauf. 2007. Does helminth elimination promote or prevent malaria? Lancet 369: 446-447. (Pubitemid 46209300)
12. Hartgers, F. C., and M. Yazdanbakhsh. 2006. Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunol. 28: 497-506. (Pubitemid 44370855)
13. McKay, D. M. 2009. The therapeutic helminth? Trends Parasitol. 25: 109-114.
14. Flohr, C., L. N. Tuyen, R. J. Quinnell, S. Lewis, T. T. Minh, J. Campbell, C. Simmons, G. Telford, A. Brown, T. T. Hien, et al. 2010. Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double-blind, placebo-controlled trial in Vietnam. Clin. Exp. Allergy 40: 131-142.
15. Aoyama, H., T. Hirata, H. Sakugawa, T. Watanabe, S. Miyagi, T. Maeshiro, T. Chinen, M. Kawane, O. Zaha, T. Nakayoshi, et al. 2007. An inverse relationship between autoimmune liver diseases and Strongyloides stercoralis infection. Am. J. Trop. Med. Hyg. 76: 972-976. (Pubitemid 351627689)
16. Helmby, H. 2009. Helminths and our immune system: friend or foe? Parasitol. Int. 58: 121-127.
17. Hoffmann, W., G. Petit, H. Schulz-Key, D. Taylor, O. Bain, and L. Le Goff. 2000. Litomosoides sigmodontis in mice: reappraisal of an old model for filarial research. Parasitol. Today (Regul. Ed.) 16: 387-389.
18. Allen, J. E., O. Adjei, O. Bain, A. Hoerauf, W. H. Hoffmann, B. L. Makepeace, H. Schulz-Key, V. N. Tanya, A. J. Trees, S. Wanji, and D. W. Taylor. 2008. Of mice, cattle, and humans: the immunology and treatment of river blindness. PLoS Negl. Trop. Dis. 2: e217.
19. Petit, G., M. Diagne, P. Maréchal, D. Owen, D. Taylor, and O. Bain. 1992. Maturation of the filaria Litomosoides sigmodontis in BALB/c mice; comparative susceptibility of nine other inbred strains. Ann. Parasitol. Hum. Comp. 67: 144-150.
20. Al-Qaoud, K. M., A. Taubert, H. Zahner, B. Fleischer, and A. Hoerauf. 1997. Infection of BALB/c mice with the filarial nematode Litomosoides sigmodontis: role of CD4+ T cells in controlling larval development. Infect. Immun. 65: 2457-2461. (Pubitemid 27237337)
21. Babayan, S., T. Attout, S. Specht, A. Hoerauf, G. Snounou, L. Rénia, M. Korenaga, O. Bain, and C. Martin. 2005. Increased early local immune responses and altered worm development in high-dose infections of mice susceptible to the filaria Litomosoides sigmodontis. Med. Microbiol. Immunol. (Berl.) 194: 151-162. (Pubitemid 41202532)
22. Hübner, M. P., B. Pasche, S. Kalaydjiev, P. T. Soboslay, A. Lengeling, H. Schulz-Key, E. Mitre, and W. H. Hoffmann. 2008. Microfilariae of the filarial nematode Litomosoides sigmodontis exacerbate the course of lipopolysaccharide-induced sepsis in mice. Infect. Immun. 76: 1668-1677. (Pubitemid 351562011)
23. Bain, O., S. Wanji, P. N. Vuong, P. Maréchal, L. Le Goff, and G. Petit. 1994. Larval biology of six filariae of the sub-family Onchocercinae in a vertebrate host. Parasite 1: 241-254.
24. Maréchal, P., L. Le Goff, G. Petit, M. Diagne, D. W. Taylor, and O. Bain. 1996. The fate of the filaria Litomosoides sigmodontis in susceptible and naturally resistant mice. Parasite 3: 25-31. (Pubitemid 126437179)
25. Le Goff, L., T. J. Lamb, A. L. Graham, Y. Harcus, and J. E. Allen. 2002. IL-4 is required to prevent filarial nematode development in resistant but not susceptible strains of mice. Int. J. Parasitol. 32: 1277-1284. (Pubitemid 35232179)
26. Taylor, M. D., L. LeGoff, A. Harris, E. Malone, J. E. Allen, and R. M. Maizels. 2005. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 174: 4924-4933.
27. Taylor, M. D., A. Harris, S. A. Babayan, O. Bain, A. Culshaw, J. E. Allen, and R. M. Maizels. 2007. CTLA-4 and CD4+ CD25+ regulatory T cells inhibit protective immunity to filarial parasites in vivo. J. Immunol. 179: 4626-4634.
28. Taylor, M. D., N. van der Werf, A. Harris, A. L. Graham, O. Bain, J. E. Allen, and R. M. Maizels. 2009. Early recruitment of natural CD4+ Foxp3+ Treg cells by infective larvae determines the outcome of filarial infection. Eur. J. Immunol. 39: 192-206.
29. Hoffmann, W. H., A. W. Pfaff, H. Schulz-Key, and P. T. Soboslay. 2001. Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis. Parasitology 122: 641-649. (Pubitemid 32612508)
30. Dittrich, A. M., A. Erbacher, S. Specht, F. Diesner, M. Krokowski, A. Avagyan, P. Stock, B. Ahrens, W. H. Hoffmann, A. Hoerauf, and E. Hamelmann. 2008. Helminth infection with Litomosoides sigmodontis induces regulatory T cells and inhibits allergic sensitization, airway inflammation, and hyperreactivity in a murine asthma model. J. Immunol. 180: 1792-1799.
31. Hübner, M. P., J. T. Stocker, and E. Mitre. 2009. Inhibition of type 1 diabetes in filaria-infected non-obese diabetic mice is associated with a T helper type 2 shift and induction of FoxP3+ regulatory T cells. Immunology 127: 512-522.
32. Specht, S., D. F. Ruiz, B. Dubben, S. Deininger, and A. Hoerauf. 2010. Filaria-induced IL-10 suppresses murine cerebral malaria. Microbes Infect. 12: 635-642.
33. Kühn, R., J. Löhler, D. Rennick, K. Rajewsky, and W. Müller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274. (Pubitemid 23320290)
34. Mond, J. J., A. Lees, and C. M. Snapper. 1995. T cell-independent antigens type 2. Annu. Rev. Immunol. 13: 655-692.
35. Robertson, J. M., P. E. Jensen, and B. D. Evavold. 2000. DO11.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J. Immunol. 164: 4706-4712. (Pubitemid 30238071)
36. King, C., S. G. Tangye, and C. R. Mackay. 2008. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu. Rev. Immunol. 26: 741-766. (Pubitemid 351600391)
37. Allen, J. E., and R. M. Maizels. 2011. Diversity and dialogue in immunity to helminths. Nat. Rev. Immunol. 11: 375-388.
38. Lahl, K., C. Loddenkemper, C. Drouin, J. Freyer, J. Arnason, G. Eberl, A. Hamann, H. Wagner, J. Huehn, and T. Sparwasser. 2007. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J. Exp. Med. 204: 57-63. (Pubitemid 46148756)
39. Rausch, S., J. Huehn, C. Loddenkemper, M. R. Hepworth, C. Klotz, T. Sparwasser, A. Hamann, R. Lucius, and S. Hartmann. 2009. Establishment of nematode infection despite increased Th2 responses and immunopathology after selective depletion of Foxp3+ cells. Eur. J. Immunol. 39: 3066-3077.
40. Urban, J. F., Jr., N. R. Steenhard, G. I. Solano-Aguilar, H. D. Dawson, O. I. Iweala, C. R. Nagler, G. S. Noland, N. Kumar, R. M. Anthony, T. Shea-Donohue, et al. 2007. Infection with parasitic nematodes confounds vaccination efficacy. Vet. Parasitol. 148: 14-20. (Pubitemid 47023025)
41. Hartmann, W. E., M. L. Eschbach, and M. Breloer. 2011. Strongyloides ratti infection modulates B and T cell responses to third party antigens. Exp. Parasitol. In press. .
42. Marshall, F. A., A. M. Grierson, P. Garside, W. Harnett, and M. M. Harnett. 2005. ES-62, an immunomodulator secreted by filarial nematodes, suppresses clonal expansion and modifies effector function of heterologous antigen-specific T cells in vivo. J. Immunol. 175: 5817-5826. (Pubitemid 41508066)
43. Specht, S., L. Volkmann, T. Wynn, and A. Hoerauf. 2004. Interleukin-10 (IL-10) counterregulates IL-4-dependent effector mechanisms in murine filariasis. Infect. Immun. 72: 6287-6293. (Pubitemid 39425406)
44. Schnoeller, C., S. Rausch, S. Pillai, A. Avagyan, B. M.Wittig, C. Loddenkemper, A. Hamann, E. Hamelmann, R. Lucius, and S. Hartmann. 2008. A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. J. Immunol. 180: 4265-4272.
45. Fernández Ruiz, D., B. Dubben, M. Saeftel, E. Endl, S. Deininger, A. Hoerauf, and S. Specht. 2009. Filarial infection induces protection against P. berghei liver stages in mice. Microbes Infect. 11: 172-180.
46. Satoguina, J., M. Mempel, J. Larbi, M. Badusche, C. Löliger, O. Adjei, G. Gachelin, B. Fleischer, and A. Hoerauf. 2002. Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect. 4: 1291-1300. (Pubitemid 35356455)
47. Satoguina, J. S., E. Weyand, J. Larbi, and A. Hoerauf. 2005. T regulatory-1 cells induce IgG4 production by B cells: role of IL-10. J. Immunol. 174: 4718-4726. (Pubitemid 40514459)
48. Metenou, S., B. Dembele, S. Konate, H. Dolo, S. Y. Coulibaly, Y. I. Coulibaly, A. A. Diallo, L. Soumaoro, M. E. Coulibaly, D. Sanogo, et al. 2010. At homeostasis filarial infections have expanded adaptive T regulatory but not classical Th2 cells. J. Immunol. 184: 5375-5382.
49. Metenou, S., B. Dembélé, S. Konate, H. Dolo, S. Y. Coulibaly, Y. I. Coulibaly, A. A. Diallo, L. Soumaoro, M. E. Coulibaly, D. Sanogo, et al. 2009. Patent filarial infection modulates malaria-specific type 1 cytokine responses in an IL-10-dependent manner in a filaria/malaria-coinfected population. J. Immunol. 183: 916-924.
50. Blankenhaus, B., U. Klemm, M. L. Eschbach, T. Sparwasser, J. Huehn, A. A. Kühl, C. Loddenkemper, T. Jacobs, and M. Breloer. 2011. Strongyloides ratti infection induces expansion of Foxp3+ regulatory T cells that interfere with immune response and parasite clearance in BALB/c mice. J. Immunol. 186: 4295-4305.
51. Ince, M. N., D. E. Elliott, T. Setiawan, A. Metwali, A. Blum, H. L. Chen, J. F. Urban, R. A. Flavell, and J. V. Weinstock. 2009. Role of T cell TGF-beta signaling in intestinal cytokine responses and helminthic immune modulation. Eur. J. Immunol. 39: 1870-1878.
52. Setiawan, T., A. Metwali, A. M. Blum, M. N. Ince, J. F. Urban, Jr., D. E. Elliott, and J. V. Weinstock. 2007. Heligmosomoides polygyrus promotes regulatory Tcell cytokine production in the murine normal distal intestine. Infect. Immun. 75: 4655-4663. (Pubitemid 47378127)
53. Elliott, D. E., A. Metwali, J. Leung, T. Setiawan, A. M. Blum, M. N. Ince, L. E. Bazzone, M. J. Stadecker, J. F. Urban, Jr., and J. V. Weinstock. 2008. Colonization with Heligmosomoides polygyrus suppresses mucosal IL-17 production. J. Immunol. 181: 2414-2419.
54. Wilson, M. S., M. D. Taylor, A. Balic, C. A. Finney, J. R. Lamb, and R. M. Maizels. 2005. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J. Exp. Med. 202: 1199-1212. (Pubitemid 41586951)
55. Wilson, M. S., M. D. Taylor, M. T. O'Gorman, A. Balic, T. A. Barr, K. Filbey, S. M. Anderton, and R. M. Maizels. 2010. Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur. J. Immunol. 40: 1682-1696.
56. Tetsutani, K., K. Ishiwata, H. Ishida, L. Tu, M. Torii, S. Hamano, K. Himeno, and H. Hisaeda. 2009. Concurrent infection with Heligmosomoides polygyrus suppresses anti-Plasmodium yoelii protection partially by induction of CD4(+) CD25(+)Foxp3(+) Treg in mice. Eur. J. Immunol. 39: 2822-2830.
57. Liu, Q., K. Sundar, P. K. Mishra, G. Mousavi, Z. Liu, A. Gaydo, F. Alem, D. Lagunoff, D. Bleich, and W. C. Gause. 2009. Helminth infection can reduce insulitis and type 1 diabetes through CD25- and IL-10-independent mechanisms. Infect. Immun. 77: 5347-5358.
58. Collison, L.W.,V. Chaturvedi,A. L.Henderson, P. R.Giacomin, C. Guy, J. Bankoti, D. Finkelstein, K. Forbes, C. J.Workman, S. A. Brown, et al. 2010. IL-35-mediated induction of a potent regulatory T cell population. Nat. Immunol. 11: 1093-1101.
59. McSorley, H. J., Y. M. Harcus, J. Murray, M. D. Taylor, and R. M. Maizels. 2008. Expansion of Foxp3+ regulatory T cells in mice infected with the filarial parasite Brugia malayi. J. Immunol. 181: 6456-6466.
60. Grainger, J. R., K. A. Smith, J. P. Hewitson, H. J. McSorley, Y. Harcus, K. J. Filbey, C. A. Finney, E. J. Greenwood, D. P. Knox, M. S. Wilson, et al. 2010. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-b pathway. J. Exp. Med. 207: 2331-2341.
61. Graham, A. L., M. D. Taylor, L. Le Goff, T. J. Lamb, M. Magennis, and J. E. Allen. 2005. Quantitative appraisal of murine filariasis confirms host strain differences but reveals that BALB/c females are more susceptible than males to Litomosoides sigmodontis. Microbes Infect. 7: 612-618. (Pubitemid 40720414)