Strongyloides ratti infection induces transient nematode-specific Th2 response and reciprocal suppression of IFN-γ production in mice

Parasite Immunology

Volumn 32, Issue 5, 2010, Pages 370-383

  Eschbach, M L ^a   Klemm, U ^a   Kolbaum, J ^a   Blankenhaus, B ^a   Brattig, N ^a   Breloer, M ^a  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

Author keywords

Immune modulation; Nematode infection; Strongyloides ratti; Th2 response

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; FECES ANALYSIS; FEMALE; HOST PARASITE INTERACTION; HUMORAL IMMUNITY; INTERFERON PRODUCTION; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; STRONGYLOIDIASIS; TH2 CELL;

ANIMALS; ANTIBODIES, HELMINTH; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERFERON-GAMMA; INTERLEUKINS; LARVA; MAST CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; STRONGYLOIDES RATTI; STRONGYLOIDIASIS; TH2 CELLS;

MAMMALIA; MURINAE; MUS; STRONGYLOIDES; STRONGYLOIDES RATTI; VERMES;

EID: 77950649421     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2010.01199.x     Document Type: Article

References (54)

1. Viney ME Lok JB. Strongyloides spp (May 23, 2007), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.141.1. Available at http://www.wormbook.org.
2. Viney ME. The biology and genomics of Strongyloides. Med Microbiol Immunol 2006 195 : 49 54.
3. Grove DI. Strongyloidasis a Major Roundworm Infection of man. Taylor and Francis, London, 1989.
4. Streit A. Reproduction in Strongyloides (Nematoda): a life between sex and parthenogenesis. Parasitology 2008 135 : 285 294. (Pubitemid 351311235)
5. Marcos LA, Terashima A, Dupont HL Gotuzzo E. Strongyloides hyperinfection syndrome: an emerging global infectious disease. Trans R Soc Trop Med Hyg 2008 102 : 314 318.
6. Vadlamudi RS, Chi DS Krishnaswamy G. Intestinal strongyloidiasis and hyperinfection syndrome. Clin Mol Allergy 2006 4 : 8. (Pubitemid 44219611)
7. Ramanathan R Nutman T. Strongyloides stercoralis Infection in the Immunocompromised Host. Curr Infect Dis Rep 2008 10 : 105 110.
8. Sheldon A. Studies on active acquiered resistance, natural and artificial, in the rat to infection with Strongyloides ratti. Am J Hyg 1937 25 : 53 65.
9. Machado ER, Ueta MT, Lourenco EV, Anibal FF, Roque-Barreira MC Faccioli LH. Comparison of immune responses in mice infected with different strains of Strongyloides venezuelensis. Parasite Immunol 2007 29 : 549 557.
10. Wilkes CP, Bleay C, Paterson S Viney ME. The immune response during a Strongyloides ratti infection of rats. Parasite Immunol 2007 29 : 339 346. (Pubitemid 46944444)
11. Dawkins HJ, Grove DI, Dunsmore JD Mitchell GF. Strongyloides ratti: susceptibility to infection and resistance to reinfection in inbred strains of mice as assessed by excretion of larvae. Int J Parasitol 1980 10 : 125 129.
12. Dawkins HJ Grove DI. Kinetics of primary and secondary infections with Strongyloides ratti in mice. Int J Parasitol 1981 11 : 89 96.
13. Dawkins HJ, Mitchell GF Grove DI. Strongyloides ratti infections in congenitally hypothymic (nude) mice. Aust J Exp Biol Med Sci 1982 60 : 181 186.
14. Dawkins HJ Grove DI. Attempts to establish infections with Strongyloides stercoralis in mice and other laboratory animals. J Helminthol 1982 56 : 23 26.
15. Abraham D, Rotman HL, Haberstroh HF, et al. Strongyloides stercoralis: protective immunity to third-stage larvae in BALB/cByJ mice. Exp Parasitol 1995 80 : 297 307.
16. Brigandi RA, Rotman HL, Yutanawiboonchai W, et al. Strongyloides stercoralis: role of antibody and complement in immunity to the third stage of larvae in BALB/cByJ mice. Exp Parasitol 1996 82 : 279 289. (Pubitemid 26161943)
17. Galioto AM, Hess JA, Nolan TJ, Schad GA, Lee JJ Abraham D. Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval Strongyloides stercoralis in mice. Infect Immun 2006 74 : 5730 5738. (Pubitemid 44484558)
18. Kerepesi LA, Hess JA, Nolan TJ, Schad GA Abraham D. Complement component C3 is required for protective innate and adaptive immunity to larval Strongyloides stercoralis in mice. J Immunol 2006 176 : 4315 4322. (Pubitemid 44264410)
19. Herbert DR, Lee JJ, Lee NA, Nolan TJ, Schad GA Abraham D. Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J Immunol 2000 165 : 4544 4551.
20. Herbert DR, Nolan TJ, Schad GA Abraham D. The role of B cells in immunity against larval Strongyloides stercoralis in mice. Parasite Immunol 2002 24 : 95 101. (Pubitemid 34225278)
21. Padigel UM, Hess JA, Lee JJ, et al. Eosinophils act as antigen-presenting cells to induce immunity to Strongyloides stercoralis in mice. J Infect Dis 2007 196 : 1844 1851.
22. Padigel UM, Lee JJ, Nolan TJ, Schad GA Abraham D. Eosinophils can function as antigen-presenting cells to induce primary and secondary immune responses to Strongyloides stercoralis. Infect Immun 2006 74 : 3232 3238. (Pubitemid 43794511)
23. Watanabe K, Noda K, Hamano S, et al. The crucial role of granulocytes in the early host defense against Strongyloides ratti infection in mice. Parasitol Res 2000 86 : 188 193.
24. Watanabe K, Sasaki O, Hamano S, et al. Strongyloides ratti: the role of interleukin-5 in protection against tissue migrating larvae and intestinal adult worms. J Helminthol 2003 77 : 355 361. (Pubitemid 37463214)
25. Ovington KS, McKie K, Matthaei KI, Young IG Behm CA. Regulation of primary Strongyloides ratti infections in mice: a role for interleukin-5. Immunology 1998 95 : 488 493.
26. Korenaga M, Hitoshi Y, Yamaguchi N, Sato Y, Takatsu K Tada I. The role of interleukin-5 in protective immunity to Strongyloides venezuelensis infection in mice. Immunology 1991 72 : 502 507.
27. Yoshimoto T, Yoshimoto T, Yasuda K, Mizuguchi J Nakanishi K. IL-27 suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation. J Immunol 2007 179 : 4415 4423.
28. Nawa Y, Kiyota M, Korenaga M Kotani M. Defective protective capacity of W/Wv mice against Strongyloides ratti infection and its reconstitution with bone marrow cells. Parasite Immunol 1985 7 : 429 438. (Pubitemid 16242728)
29. Fukao T, Yamada T, Tanabe M, et al. Selective loss of gastrointestinal mast cells and impaired immunity in PI3K-deficient mice. Nat Immun 2002 3 : 295 304. (Pubitemid 34213432)
30. Abe T, Sugaya H, Ishida K, Khan WI, Tasdemir I Yoshimura K. Intestinal protection against Strongyloides ratti and mastocytosis induced by administration of interleukin-3 in mice. Immunology 1993 80 : 116 121. (Pubitemid 23284198)
31. Sasaki Y, Yoshimoto T, Maruyama H, et al. IL-18 with IL-2 protects against Strongyloides venezuelensis infection by activating mucosal mast cell-dependent type 2 innate immunity. J Exp Med 2005 202 : 607 616. (Pubitemid 41248412)
32. Lantz CS, Boesiger J, Song CH, et al. Role for interleukin-3 in mast-cell and basophil development and in immunity to parasites. Nature 1998 392 : 90 93.
33. Maruyama H, Yabu Y, Yoshida A, Nawa Y Ohta N. A role of mast cell glycosaminoglycans for the immunological expulsion of intestinal nematode, Strongyloides venezuelensis. J Immunol 2000 164 : 3749 3754. (Pubitemid 30169831)
34. Lok JB. Strongyloides stercoralis: a model for translational research on parasitic nematode biology (February 17, 2007). WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.134.1. Available at http://www.wormbook.org.
35. Sato Y Toma H. Strongyloides venezuelensis infections in mice. Int J Parasitol 1990 20 : 57 62.
36. Khan AI, Horii Y, Tiuria R, Sato Y Nawa Y. Mucosal mast cells and the expulsive mechanisms of mice against Strongyloides venezuelensis. Int J Parasitol 1993 23 : 551 555.
37. Negrao-Correa D, Pinho V, Souza DG, et al. Expression of IL-4 receptor on non-bone marrow-derived cells is necessary for the timely elimination of Strongyloides venezuelensis in mice, but not for intestinal IL-4 production. Int J Parasitol 2006 36 : 1185 1195.
38. Machado ER, Carlos D, Lourenco EV, et al. Counterregulation of Th2 immunity by interleukin 12 reduces host defenses against Strongyloides venezuelensis infection. Microbes Infect 2009 11 : 571 578.
39. Watanabe K, Hamano S, Yada S, et al. The effect of interleukin-4 on the induction of intestinal mast cells and chronological cytokine profiles during intestinal nematode Strongyloides ratti infection. Parasitol Res 2001 87 : 149 154.
40. Rotman HL, Yutanawiboonchai W, Brigandi RA, et al. Strongyloides stercoralis: eosinophil-dependent immune-mediated killing of third stage larvae in BALB/cByJ mice. Exp Parasitol 1996 82 : 267 278. (Pubitemid 26161942)
41. Dawkins HJ Grove DI. Immunisation of mice against Strongyloides ratti. Zeitschrift fur Parasitenkunde (Berlin, Germany) 1982 66 : 327 333.
42. Bleay C, Wilkes CP, Paterson S Viney ME. Density-dependent immune responses against the gastrointestinal nematode Strongyloides ratti. Int J Parasitol 2007 13 : 1501 1509.
43. Paterson S, Wilkes C, Bleay C Viney ME. Immunological responses elicited by different infection regimes with Strongyloides ratti. PLoS ONE 2008 3 : e2509.
44. Bancroft AJ, Else KJ Grencis RK. Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response. Eur J Immunol 1994 24 : 3113 3118.
45. Grove DI Dawkins HJ. Effects of prednisolone on murine strongyloidiasis. Parasitology 1981 83 : 401 409.
46. Uchikawa R, Ichiki H Komaki E. Antibody responses and protective immunity in rats receiving repeated inoculations of Strongyloides ratti. J Parasitol 1991 77 : 737 741.
47. Pestka S, Krause CD, Sarkar D, Walter MR, Shi Y Fisher PB. Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 2004 22 : 929 979.
48. O'Garra A, Vieira PL, Vieira P Goldfeld AE. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J Clin Invest 2004 114 : 1372 1378.
49. Hoerauf A, Satoguina J, Saeftel M Specht S. Immunomodulation by filarial nematodes. Parasite Immunol 2005 27 : 417 429.
50. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD Allen JE. Helminth parasites - masters of regulation. Immunol Rev 2004 201 : 89 116.
51. Rausch S, Huehn J, Kirchhoff D, et al. Functional analysis of effector and regulatory T cells in a parasitic nematode infection. Infect Immun 2008 76 : 1908 1919.
52. Finney CA, Taylor MD, Wilson MS Maizels RM. Expansion and activation of CD4(+)CD25(+) regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol 2007 37 : 1874 1886.
53. Setiawan T, Metwali A, Blum AM, et al. Heligmosomoides polygyrus promotes regulatory T-cell cytokine production in the murine normal distal intestine. Infect Immun 2007 75 : 4655 4663.
54. Elliott DE, Metwali A, Leung J, et al. Colonization with Heligmosomoides polygyrus suppresses mucosal IL-17 production. J Immunol 2008 181 : 2414 2419.