Contrasting roles for IL-10 in protective immunity to different life cycle stages of intestinal nematode parasites

European Journal of Immunology

Volumn 33, Issue 9, 2003, Pages 2382-2390

  Helmby, Helena ^a,b   Grencis, Richard K ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

Cytokines; Mucosa; Parasitic helminth; Th1; Th2 cells

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 10 RECEPTOR; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; INFECTION SENSITIVITY; JEJUNUM; KNOCKOUT MOUSE; LARVAL STAGE; LIFE CYCLE; MALE; MAST CELL; MOUSE; NEMATODE; NEMATODIASIS; NONHUMAN; PARASITE IMMUNITY; PRIORITY JOURNAL; TH1 CELL; TH2 CELL; TRICHINELLA SPIRALIS; WORM EXPULSION;

ANIMALS; CYTOKINES; INTERLEUKIN-10; INTESTINAL DISEASES, PARASITIC; LARVA; LYMPH NODES; MAST CELLS; MESENTERY; MICE; MICE, KNOCKOUT; MUCOUS MEMBRANE; MUSCLE, SKELETAL; NEMATODE INFECTIONS; TRICHINELLA SPIRALIS;

EID: 0141539376     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200324082     Document Type: Article

References (50)

1. Grencis, R. K., Hultner, L. and Else, K. J., Host protective immunity to Trichinella spiralis in mice: activation of Th cell subsets and lymphokine secretion in mice expressing different response phenotypes. Immunology 1991. 74: 329-332.
2. Finkelman, F. D., Shea-Donohue, T., Goldhill, J., Sullivan, C. A., Morris, S. C., Madden, K. B., Gause, W. C. and Urban, J. F., Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 1997. 15: 505-533.
3. Faulkner, H., Humphreys, N., Renauld, J.-C., Van Snick, J. and Grencis, R., Interleukin-9 is involved in host protective immunity to intestinal nematode infection. Eur. J. Immunol. 1997. 27: 2536-2540.
4. Urban, J. F., Schopf, L., Morris, S. C., Orekhova, T., Madden, K. B., Betts, C. J., Gamble, H. R., Byrd, C., Donaldson, D., Else, K. and Finkelman, F. D., Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. J. Immunol. 2000. 164: 2046-2052.
5. Helmby, H. and Grencis, R. K., Interleukin-18 regulates intestinal mastocytosis and Th2 cytokine production independently of IFN-γ during Trichinella spiralis infection. J. Immunol. 2002. 169: 2553-2560.
6. Grencis, R. K., Else, K. J., Huntley, J. F. and Nishikawa, S. I., The in vivo role of stem cell factor (c-kit ligand) on mastocytosis and host protective immunity to the intestinal nematode Trichinella spiralis in mice. Parasite Immunol. 1993. 15: 55-59.
7. Donaldson, L. E., Schmitt, E., Huntley, J. F., Newlands, G. F. J. and Grencis, R. K., A critical role for stem cell factor and c-kit in host protective immunity to an intestinal helminth. Int. Immunol. 1995. 8: 559-567.
8. v mice. J. Helminth. 1985. 59: 233-239.
9. Fiorentino, D. F., Bond, M. W. and Mosmann, T. R., Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J. Exp. Med 1989. 170: 2081-2095.
10. Fiorentino, D. F., Zlotnik, A., Mosmann, T. R., Howard, M. and O'Garra, A., IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 1991. 147: 3815-3822.
11. de Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. G. and de Vries, J. E., Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med 1991. 174: 1209-1220.
12. de Waal Malefyt, R., Haanen, J., Spits, H., Roncarolo, M. -G., te Velde, A., Figdor, C., Johnson, K., Kastelein, R., Yssel, H. and de Vries, J. E., Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 1991. 174: 915-924.
13. Ding, L., Linsley, P. S., Huang, L., Germain, R. N. and Shevach, E. M., IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol. 1993. 151: 1224-1234.
14. + T cell subset inhibits antigen-specific T cell responses and prevents colitis. Nature 1997. 389: 737-742.
15. Asseman, C., Mauze, S., Leach, M. W., Coffman, R. L. and Powrie, F., An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 1999. 190: 995-1004.
16. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K. and Muller, W., Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993. 75: 263-274.
17. + T cells. Immunity 1994. 1: 553-562.
18. Ribbons, K. A., Thompson, J. H., Liu, X., Pennline, K., Clark, D. A. and Miller, M. J., Anti-inflammatory properties of interleukin-10 administration in hapten-induced colitis. Eur. J. Pharmacol. 1997. 323: 245-254.
19. Tuohy, M., Lammas, D. A., Wakelin, D., Huntley, J. F., Newlands, G. F. J. and Miller, H. R. P., Functional correlations between mucosal mast cell activity and immunity to Trichinella spiralis in high and low responder mice. Parasite Immunol. 1990. 12: 675-685.
20. Madden, K. B., Urban, J. F., Ziltener, H. J., Schrader, J. W., Finkelman, F. D. and Katona, I. M., Antibodies to IL-3 and IL-4 suppress helminth-induced intestinal mastocytosis. J. Immunol. 1991. 147: 1387-1391.
21. Ghildyal, N., McNeil, H. P., Stechschulte, S., Austen, K. F., Silberstein, D., Gurish, M. F., Somerville, L. L. and Stevens, R. L., IL-10 induces transcription of the gene for mouse mast cell protease-1, a serine protease preferentially expressed in mucosal mast cells of Trichinella spiralis-infected mice. J. Immunol. 1992. 149: 2123-2129.
22. Helmby, H., Takeda, K., Akira, S. and Grencis, R. K., Interleukin (IL)-18 promotes the development of chronic gastrointestinal helminth infection by downregulating IL-13. J. Exp. Med. 2001. 194: 355-364.
23. Moore, K. W., O'Garra, A., de Waal Malefyt, R., Vieira, P. and Mosmann, T. R., Interleukin-10. Annu. Rev. Immunol. 1993. 11: 165-190.
24. Moore, K. W., de Waal Malefyt, R., Coffman, R. L. and O'Garra, A., Interleukin-10 and the Interleukin-10 receptor. Annu. Rev. Immunol. 2001. 19: 683-765.
25. Lammas, D. A., Wakelin, D., Mitchell, L. A., Tuohy, M., Else, K. J. and Grencis, R. K., Genetic influences upon eosinophilia in mice infected with Trichinella spiralis. Parasitology 1992. 105: 117-124.
26. Khan, W. I., Vallance, B. A., Blennerhassett, P., Deng, Y., Verdu, E. F., Matthaei, K. I. and Collins, S. M., Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infect. Immun. 2001. 69: 838-844.
27. O'Farrell, A. M., Liu, Y., Moore, K. W. and Mui, A. L., IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for Stat3-dependent and -independent pathways. EMBO J 1998. 17: 1006-1018.
28. Hansen, G., Berry, G., DeKruyff, R. H. and Umetsu, D. T., Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J. Clin. Invest. 1999. 103: 175-183.
29. Ford, J. G., Rennick, D., Donaldson, D. D., Venkayya, R., McArthur, C., Hansell, E., Kurup, V. P., Warnock, M. and Grunig, G., IL-13 and IFN-gamma: interactions in lung inflammation. J. Immunol. 2001. 167: 1769-1777.
30. Grunig, G., Corry, D. B., Leach, M. W., Seymour, B. W., Kurup, V. P. and Rennick, D. M., Interleukin-10 is a natural suppressor of cytokine production and inflammation in a murine model of allergic bronchopulmonary aspergillosis. J. Exp. Med. 1997. 185: 1089-1099.
31. Eklund, K. K., Ghildyal, N., Austen, K. F. and Stevens, R. L., Induction by IL-9 and suppression by IL-3 and IL-4 of the levels of chromosome 14-derived transcripts that encode late-expressed mouse mast cell proteases. J. Immunol. 1993. 151: 4266-4273.
32. Thompson-Snipes, L., Dhar, V., Bond, M. W., Mosmann, T. R., Moore, K. W. and Rennick, D. M., Interleukin 10: a novel stimulatory factor for mast cells and their progenitors. J. Exp. Med 1991. 173: 507-510.
33. + stem cells. Exp. Hematol. 1994. 22: 136-141.
34. Rennick, D., Hunte, B., Holland, G. and Thompson-Snipes, L., Cofactors are essential for stem cell factor-dependent growth and maturation of mast cell progenitors: comparative effects of interleukin-3 (IL-3), IL-4, IL-10, and fibroblasts. Blood 1995. 85: 57-65.
35. Ghildyal, N., Friend, D. S., Nicodemus, C. F., Austen, K. F. and Stevens, R. L., Reversible expression of mouse mast cell protease 2 mRNA and protein in cultured mast cells exposed to IL-10. J. Immunol. 1993. 151: 3206-3214.
36. Eklund, K. K., Humphries, D. E., Xia, Z., Ghildyal, N., Friend, D. S., Gross, V. and Stevens, R. L., Glucocorticoids inhibit the cytokine-induced proliferation of mast cells, the high affinity IgE receptor-mediated expression of TNF-α, and the IL-10 induced expression of chymases. J. Immunol. 1997. 158: 4373-4380.
37. Lin, T. J. and Befus, A. D., Differential regulation of mast cell function by IL-10 and stem cell factor. J. Immunol. 1997. 159: 4015-4023.
38. James, E. R. and Denham, D. A., Immunity to Trichinella spiralis. VI. The specificity of the immune response stimulated by the intestinal stage. J. Helminth. 1975. 49: 43-47.
39. James, E. R. and Denham, D. A., Antigenicity of the newborn larvae of Trichinella spiralis. J. Parasitol. 1975. 61: 354.
40. James, E. R., Moloney, A. and Denham, D. A., Immunity to Trichinella spiralis. VII. Resistance stimulated by the parenteral stages of the infection. J. Parasitol. 1977. 63: 720-723.
41. Mackenzie, C. D., Preston, P. M. and Ogilvie, B. M., Immunological properties of the surface of parasitic nematodes. Nature 1978. 276: 826-828.
42. Bell, R. G. and McGregor, D. D., Trichinella spiralis: role of different life cycle phases in induction, maintenance, and expression of rapid expulsion in rat. Exp. Parasitol. 1979. 48: 51-60.
43. Kazura, J. W. and Aikawa, M., Host defense mechanisms against Trichinella spiralis infection in the mouse: eosinophil-mediated destruction of newborn larvae in vitro. J. Immunol. 1980. 124: 355-361.
44. Wang, C. H. and Bell, R. G., Trichinella spiralis: intestinal expression of systemic stage-specific immunity to newborn larvae. Parasite Immunol. 1987. 9: 465-475.
45. Grove, D. I., Mahmoud, A. A. and Warren, K. S., Eosinophils and resistance to Trichinella spiralis. J. Exp. Med. 1977. 145: 755-759.
46. Kazura, J. W. and Grove, D. I., Stage-specific antibody-dependent eosinophil-mediated destruction of Trichinella spiralis. Nature 1978. 274: 588-589.
47. Gansmuller, A., Anteunis, A., Venturiello, S. M., Bruschi, F. and Binaghi, R. A., Antibody-dependent in-vitro cytotoxicity of newborn Trichinella spiralis larvae: nature of the cells involved. Parasite Immunol. 1987. 9: 281-292.
48. Venturiello, S. M., Giambartolomei, G. H. and Costantino, S. N., Immune killing of newborn Trichinella larvae by human leukocytes. Parasite Immunol. 1993. 15: 559-564.
49. Venturiello, S. M., Giambartolomei, G. H. and Costantino, S. N., Immune cytotoxic activity of human eosinophils against Trichinella spiralis newborn larvae. Parasite Immunol. 1995. 17: 555-559.
50. Wakelin, D. and Wilson, M. M., Transfer of immunity to Trichinella spiralis in the mouse with mesenteric lymph node cells in donors, and expression of immunity in recipients. Parasitology 1977. 74: 215-234.