Interleukin-10 limits local and body cavity inflammation during infection with muscle-stage Trichinella spiralis

Infection and Immunity

Volumn 72, Issue 6, 2004, Pages 3129-3137

  Beiting, Daniel P ^a   Bliss, Susan K ^a   Schlafer, Donald H ^a   Roberts, Victoria L ^a   Appleton, Judith A ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G1; INTERLEUKIN 10;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CHRONIC INFLAMMATION; CONTROLLED STUDY; DIAPHRAGM; IMMUNE RESPONSE; INFLAMMATION; LARVA; MOUSE; MYOSITIS; NONHUMAN; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PRIORITY JOURNAL; RAT; TH2 CELL; TRICHINELLA SPIRALIS;

ACUTE DISEASE; ANIMALS; CHRONIC DISEASE; INFLAMMATION; INTERLEUKIN-10; LARVA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MUSCLES; PERITONEAL CAVITY; PLEURAL CAVITY; RATS; TRICHINELLA SPIRALIS; TRICHINOSIS;

EID: 2542583988     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.6.3129-3137.2004     Document Type: Article

References (57)

1. Almond, N. M., and R. M. Parkhouse. 1986. Immunoglobulin class specific responses to biochemically defined antigens of Trichinella spiralis. Parasite Immunol. 8:391-406.
2. Appleton, J. A., L. R. Schain, and D. D. McGregor. 1988. Rapid expulsion of Trichinella spiralis in suckling rats: mediation by monoclonal antibodies. Immunology 65:487-492.
3. Appleton, J. A., and L. Usack. 1993. Identification of potential antigenic targets for rapid expulsion of Trichinella spiralis. Mol. Biochem. Parasitol. 58:53-62.
4. Baruch, A. M., and D. D. Despommier. 1991. Blood vessels in Trichinella spiralis infections: a study using vascular casts. J. Parasitol. 77:99-103.
5. Bell, R. G., and C. H. Wang. 1987. The Trichinella spiralis newborn larvae: production, migration and immunity in vivo. Wiad. Parazytol. 33:453-478.
6. Berland, R., and H. H. Wortis. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20:253-300.
7. Bliss, S. K., A. Alcaraz, and J. A. Appleton. 2003. IL-10 prevents liver necrosis during murine infection with Trichinella spiralis. J. Immunol. 171:3142-3147.
8. Bliss, S. K., Y. Zhang, and E. Y. Denkers. 1999. Murine neutrophil stimulation by Toxoplasma gondii antigen drives high level production of IFN-gamma-independent IL-12. J. Immunol. 163:2081-2088.
9. Bogdan, C., Y. Vodovotz, and C. Nathan. 1991. Macrophage deactivation by interleukin 10. J. Exp. Med. 174:1549-1555.
10. Bruschi, F., S. Solfanelli, and R. A. Binaghi. 1992. Trichinella spiralis: modifications of the cuticle of the newborn larva during passage through the lung. Exp. Parasitol. 75:1-9.
11. Capo, V. A., D. D. Despommier, and R. I. Polvere. 1998. Trichinella spiralis: vascular endothelial growth factor is up-regulated within the nurse cell during the early phase of its formation. J. Parasitol. 84:209-214.
12. Chang, N. C., S. I. Hung, K. Y. Hwa, I. Kato, J. E. Chen, C. H. Liu, and A. C. Chang. 2001. A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin. J. Biol. Chem. 276:17497-17506.
13. Crum, E. D., D. D. Despommier, and D. D. McGregor. 1977. Immunity to Trichinella spiralis. I. Transfer of resistance by two classes of lymphocytes. Immunology 33:787-795.
14. Cunha, F. Q., S. Moncada, and F. Y. Liew. 1992. Interleukin-10 (IL-10) inhibits the induction of nitric oxide synthase by interferon-gamma in murine macrophages. Biochem. Biophys. Res. Commun. 182:1155-1159.
15. Ding, L., P. S. Linsley, L. Y. Huang, R. N. Germain, and E. M. Shevach. 1993. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol. 151:1224-1234.
16. Denkers, E. Y., D. L. Wassom, C. J. Krco, and C. E. Hayes. 1990. The mouse antibody response to Trichinella spiralis defines a single, immunodominant epitope shared by multiple antigens. J. Immunol. 144:3152-3159.
17. Despommier, D. 1975. Adaptive changes in muscle fibers infected with Trichinella spiralis. Am. J. Pathol. 78:477-496.
18. Despommier, D., W. F. Symmans, and R. Dell. 1991. Changes in nurse cell nuclei during synchronous infection with Trichinella spiralis. J. Parasitol. 77:290-295.
19. Despommier, D. D. 1983. Biology, p. 75-151. In W. C. Campbell (ed.), Trichinella and trichinosis, vol. 75. Plenum Press, New York, N.Y.
20. de Waal Malefyt, R., J. Abrams, B. Bennett, C. G. Figdor, and J. E. de Vries. 1991. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174:1209-1220.
21. de Waal Malefyt, R., C. G. Figdor, R. Huijbens, S. Mohan-Peterson, B. Bennett, J. Culpepper, W. Dang, G. Zurawski, and J. E. de Vries. 1993. Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-gamma or IL-10. J. Immunol. 151:6370-6381.
22. Di Santo, E., C. Meazza, M. Sironi, P. Fruscella, A. Mantovani, J. D. Sipe, and P. Ghezzi. 1997. IL-13 inhibits TNF production but potentiates that of IL-6 in vivo and ex vivo in mice. J. Immunol. 159:379-382.
23. Drachman, D. A., and T. O. Tuncbay. 1965. The remote myopathy of trichinosis. Neurology 15:1127-1135.
24. Falcone, F. H., P. Loke, X. Zang, A. S. MacDonald, R. M. Maizels, and J. E. Allen. 2001. A Brugia malayi homolog of macrophage migration inhibitory factor reveals an important link between macrophages and eosinophil recruitment during nematode infection. J. Immunol. 167:5348-5354.
25. Fiorentino, D. F., M. W. Bond, and T. R. Mosmann. 1989. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J. Exp. Med. 170:2081-2095.
26. Fiorentino, D. F., A. Zlotnik, T. R. Mosmann, M. Howard, and A. O'Garra. 1991. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147:3815-3822.
27. Fuss, I. J., M. Boirivant, B. Lacy, and W. Strober. 2002. The interrelated roles of TGF-beta and IL-10 in the regulation of experimental colitis. J. Immunol. 168:900-908.
28. Gazzinelli, R. T., I. P. Oswald, S. L. James, and A. Sher. 1992. IL-10 inhibits parasite killing and nitrogen oxide production by IFN- gamma-activated macrophages. J. Immunol. 148:1792-1796.
29. Hara, M., C. I. Kingsley, M. Niimi, S. Read, S. E. Turvey, A. R. Bushell, P. J. Morris, F. Powrie, and K. J. Wood. 2001. IL-10 is required for regulatory T cells to mediate tolerance to alloantigens in vivo. J. Immunol. 166:3789-3796.
30. Helmby, H., and R. K. Grencis. 2003. Contrasting roles for IL-10 in protective immunity to different life cycle stages of intestinal nematode parasites. Eur. J. Immunol. 33:2382-2390.
31. Hesse, M., M. Modolell, A. C. La Flamme, M. Schito, J. M. Fuentes, A. W. Cheever, E. J. Pearce, and T. A. Wynn. 2001. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol. 167:6533-6544.
32. Humes, A. G., and R. P. Akers. 1952. Vascular changes in the cheek pouch of the golden hamster during infection with Trichinella spiralis larvae. Anat. Rec. 114:103-113.
33. Jasmer, D. P. 1993. Trichinella spiralis infected skeletal muscle cells arrest in G2/M and cease muscle gene expression. J. Cell Biol. 121:785-793.
34. Jasmer, D. P. 1990. Trichinella spiralis: altered expression of muscle proteins in trichinosis. Exp. Parasitol. 70:452-465.
35. Levine, S. J., T. Wu, and J. H. Shelhamer. 1997. Extracellular release of the type I intracellular IL-1 receptor antagonist from human airway epithelial cells: differential effects of IL-4, IL-13, IFN-gamma, and corticosteroids. J. Immunol. 158:5949-5957.
36. Mariano, M. 1995. The experimental granuloma. A hypothesis to explain the persistence of the lesion. Rev. Inst. Med. Trop. Sao Paulo 37:161-176.
37. Mercolino, T. J., L. W. Arnold, L. A. Hawkins, and G. Haughton. 1988. Normal mouse peritoneum contains a large population of Ly-1+ (CD5) B cells that recognize phosphatidyl choline. Relationship to cells that secrete hemolytic antibody specific for autologous erythrocytes. J. Exp. Med. 168:687-698.
38. Mizoguchi, A., E. Mizoguchi, H. Takedatsu, R. S. Blumberg, and A. K. Bhan. 2002. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16:219-230.
39. Morelle, W., S. M. Haslam, V. Olivier, J. A. Appleton, H. R. Morris, and A. Dell. 2000. Phosphorylcholine-containing N-glycans of Trichinella spiralis: identification of multiantennary lacdiNAc structures. Glycobiology 10:941-950.
40. Oswald, I. P., T. A. Wynn, A. Sher, and S. L. James. 1992. Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proc. Natl. Acad. Sci. USA 89:8676-8680.
41. Polvere, R. I., C. A. Kabbash, V. A. Capo, I. Kadan, and D. D. Despommier. 1997. Trichinella spiralis: synthesis of type IV and type VI collagen during nurse cell formation. Exp. Parasitol. 86:191-199.
42. Pontoux, C., A. Banz, and M. Papiernik. 2002. Natural CD4 CD25(+) regulatory T cells control the burst of superantigen-induced cytokine production: the role of IL-10. Int. Immunol. 14:233-239.
43. Purkerson, M., and D. D. Despommier. 1974. Fine structure of the muscle phase of Trichinella spiralis in the mouse, p. 7-23. In C. Kim (ed.), Trichinellosis. Intext Educational Publishers, New York, N.Y.
44. Reason, A. J., L. A. Ellis, J. A. Appleton, N. Wisnewski, R. B. Grieve, M. McNeil, D. L. Wassom, H. R. Morris, and A. Dell. 1994. Novel tyvelose-containing tri- and tetra-antennary N-glycans in the immunodominant antigens of the intracellular parasite Trichinella spiralis. Glycobiology 4:593-603.
45. Redpath, S., A. Angulo, N. R. Gascoigne, and P. Ghazal. 1999. Murine cytomegalovirus infection down-regulates MHC class II expression on macrophages by induction of IL-10. J. Immunol. 162:6701-6707.
46. Ritterson, A. L. 1966. Nature of the cyst of Trichinella spiralis. J. Parasitol. 52:157-161.
47. Rumbley, C. A., and S. M. Phillips. 1999. The schistosome granuloma: an immunoregulatory organelle. Microbes Infect. 1:499-504.
48. Shinohara, H. 1997. Lymphatic system of the mouse diaphragm: morphology and function of the lymphatic sieve. Anat. Rec. 249:6-15.
49. Snapper, C. M., F. D. Finkelman, D. Stefany, D. H. Conrad, and W. E. Paul. 1988. IL-4 induces co-expression of intrinsic membrane IgG1 and IgE by murine B cells stimulated with lipopolysaccharide. J. Immunol. 141:489-498.
50. Stewart, G. L., and L. M. Charniga. 1980. Distribution of Trichinella spiralis in muscles of the mouse. J. Parasitol. 66:688-689.
51. Sutterwala, F. S., G. J. Noel, P. Salgame, and D. M. Mosser. 1998. Reversal of proinflammatory responses by ligating the macrophage Fcgamma receptor type I. J. Exp. Med. 188:217-222.
52. Tawill, S., L. Le Goff, F. Ali, M. Blaxter, and J. E. Allen. 2004. Both free-living and parasitic nematodes induce a characteristic Th2 response that is dependent on the presence of intact glycans. Infect. Immun. 72:398-407.
53. Toossi, Z. 2000. The inflammatory response in Mycobacterium tuberculosis infection. Arch. Immunol. Ther. Exp. 48:513-519.
54. Tsunawaki, S., M. Sporn, A. Ding, and C. Nathan. 1988. Deactivation of macrophages by transforming growth factor-beta. Nature 334:260-262.
55. Vannier, E., R. de Waal Malefyt, A. Salazar-Montes, J. E. de Vries, and C. A. Dinarello. 1996. Interleukin-13 (IL-13) induces IL-1 receptor antagonist gene expression and protein synthesis in peripheral blood mononuclear cells: inhibition by an IL-4 mutant protein. Blood 87:3307-3315.
56. Wing, E. J., J. L. Krahenbuhl, and J. S. Remington. 1979. Studies of macrophage function during Trichinella spiralis infection in mice. Immunology 36:479-485.
57. Wynn, T. A., A. W. Cheever, M. E. Williams, S. Hieny, P. Caspar, R. Kuhn, W. Muller, and A. Sher. 1998. IL-10 regulates liver pathology in acute murine schistosomiasis mansoni but is not required for immune down-modulation of chronic disease. J. Immunol. 160:4473-4480.