Interleukin-10 (IL-10) counterregulates IL-4-dependent effector mechanisms in murine filariasis

Infection and Immunity

Volumn 72, Issue 11, 2004, Pages 6287-6293

  Specht, Sabine ^a,b   Volkmann, Lars ^a   Wynn, Tom ^c   Hoerauf, Achim ^a,b  

^a UNIVERSITY OF BONN   (Germany)

^b BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FILARIASIS; HELMINTHIASIS; IMMUNOSUPPRESSIVE TREATMENT; INTERFERON PRODUCTION; KNOCKOUT MOUSE; LITOMOSOIDES SIGMODONTIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; TH1 CELL; TH2 CELL;

ANIMALS; FILARIASIS; FILARIOIDEA; HUMANS; INTERLEUKIN-10; INTERLEUKIN-4; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 7044264675     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.11.6287-6293.2004     Document Type: Article

References (42)

1. Al-Qaoud, K. M., E. Pearlman, J. Klukowski, T. Hartung, B. Fleischer, and A. Hoerauf. 2000. A new mechanism for IL-5 dependent helminth control: neutrophil accumulation and neutrophil-mediated worm encapsulation in murine fllariasis are abolished in the absence of IL-5. Int. Immunol. 12:899-908.
2. + T cells in controlling larval development. Infect. Immun. 65:2457-2461.
3. Babu, S., L. M. Ganley, T. R. Klei, L. D. Shultz, and T. V. Rajan. 2000. Role of gamma interferon and interleukin-4 in host defense against the human filarial parasite Brugia malayi. Infect. Immun. 68:3034-3035.
4. Brattig, N., C. Nietz, S. Hounkpatin, R. Lucius, F. Seeber, U. Pichlmeier, and T. Pogonka. 1997. Differences in cytokine responses to Onchocerca volvulus extract and recombinant Ov33 and OvL3-1 proteins in exposed subjects with various parasitologic and clinical states. J. Infect. Dis. 176:838-842.
5. Brattig, N. W., B. Lepping, C. Timmann, D. W. Büttner, Y. Marfo, C. Hamelmann, and R. D. Horstmann. 2002. Onchocerca volvulus-exposed persons fail to produce interferon-gamma in response to O. volvulus antigen but mount proliferative responses with interleukin-5 and IL-13 production that decrease with increasing microfilarial density. J. Infect. Dis. 185:1148-1154.
6. Chandrashekar, R., U. R. Rao, P. B. Parab, and D. Subrahmanyam. 1986. Brugia malayi: rat cell interactions with infective larvae mediated by complement. Exp. Parasitol. 62:362-369.
7. Chiaramonte, M. G., M. Mentink-Kane, B. A. Jacobson, A. W. Cheever, M. J. Whitters, M. E. Goad, A. Wong, M. Collins, D. D. Donaldson, M. J. Grusby, and T. A. Wynn. 2003. Regulation and function of the interleukin 13 receptor alpha 2 during a T helper cell type 2-dominant immune response. J. Exp. Med. 197:687-701.
8. Cottrez, F., S. D. Hurst, R. L. Coffman, and H. Groux. 2000. T regulatory cells 1 inhibit a Th2-specific response in vivo. J. Immunol. 165:4848-4853.
9. Doetze, A., J. Satoguina, G. Burchard, T. Rau, C. Löliger, B. Fleischer, and A. Hoerauf. 2000. Antigen-specific cellular hyporesponsiveness in generalized onchocerciasis is mediated by Th3/Tr1-type cytokines IL-10 and TGF-beta but not by a Th1 to Th2 shift. Int. Immunol. 12:623-630.
10. Groux, H. 2001. An overview of regulatory T cells. Microbes Infect. 3:883-889.
11. Heinzmann, A., X. Q. Mao, M. Akaiwa, R. T. Kreomer, P. S. Gao, K. Ohshima, R. Umeshita, Y. Abe, S. Braun, T. Yamashita, M. H. Roberts, R. Sugimoto, K. Arima, Y. Arinobu, B. Yu, S. Kruse, T. Enomoto, Y. Dake, M. Kawai, S. Shimazu, S. Sasaki, C. N. Adra, M. Kitaichi, H. Inoue, K. Yamauchi, N. Tomichi, F. Kurimoto, N. Hamasaki, J. M. Hopkin, K. Izuhara, T. Shirakawa, and K. A. Deichmann. 2000. Genetic variants of IL-13 signalling and human asthma and atopy. Hum. Mol. Genet. 9:549-559.
12. Hoerauf, A. 2002. Immune effectors important in protective resistance, p. 109-125. In T. Klei and T. V. Rajan (ed.), World class parasites: the filariae. Kluwer Academic Press, New York, N.Y.
13. Hoerauf, A., and N. Brattig. 2002. Resistance and susceptibility in human onchocerciasis-beyond Th1 vs. Th2. Trends Parasitol. 18:25-31.
14. Hoerauf, A., S. Kruse, N. W. Brattig, A. Heinzmann, B. Mueller-Myhsok, and K. A. Deichmann. 2002. The variant Arg110Gln of human IL-13 is associated with an immunologically hyper-reactive form of onchocerciasis (sowda). Microbes Infect. 4:37-42.
15. Hoffmann, K. F., A. W. Cheever, and T. A. Wynn. 2000. IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J. Immunol. 164:6406-6416.
16. Hoffmann, K. F., S. L. James, A. W. Cheever, and T. A. Wynn. 1999. Studies with double cytokine-deficient mice reveal that highly polarized Th1- and Th2-type cytokine and antibody responses contribute equally to vaccine-induced immunity to Schistosoma mansoni. J. Immunol. 163:927-938.
17. 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.
18. King, C. L., S. Mahanty, V. Kumaraswami, J. S. Abrams, J. Regunathan, K. Jayaraman, E. A. Ottesen, and T. B. Nutman. 1993. Cytokine control of parasite-specific anergy in human lymphatic filariasis. Preferential induction of a regulatory T helper type 2 lymphocyte subset. J. Clin. Investig. 92:1667-1673.
19. Kuhn, R., J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75:263-274.
20. Lawrence, R. A., J. E. Allen, and C. A. Gray. 2000. Requirements for in vivo IFN-gamma induction by live microfilariae of the parasitic nematode, Brugia malayi. Parasitology 120:631-640.
21. Lawrence, R. A., J. E. Allen, J. Osborne, and R. A. Maizels. 1994. Adult and microfilarial stages of the filarial parasite Brugia malayi stimulate contrasting cytokine and Ig isotype responses in BALB/c mice. J. Immunol. 153:1216-1224.
22. 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.
23. Mahanty, S., H. E. Luke, V. Kumaraswami, P. R. Narayanan, V. Vyayshekaran, and T. B. Nutman. 1996. Stage-specific induction of cytokines regulates the immune response in lymphatic filariasis. Exp. Parasitol. 84:282-290.
24. Martin, C., K. M. Al-Qaoud, O. Bain, K. Paehle, B. Fleischer, and A. Hoerauf. 2000. IL-5 is essential for protection after immunization against murine filariasis but not during primary infection. Med. Microbiol. Immunol. 189:67-74.
25. Martin, C., L. Le Goff, M. N. Ungeheuer, P. N. Vuong, and O. Bain. 2000. Drastic reduction of a filarial infection in eosinophilic interleukin-5 transgenic mice. Infect. Immun. 68:3651-3656.
26. Martin, C., M. Saeftel, P. N. Vuong, S. Babayan, K. Fischer, O. Bain, and A. Hoerauf. 2001. B-cell deficiency suppresses vaccine-induced protection against murine filariasis but does not increase the recovery rate for primary infection. Infect. Immun. 69:7067-7073.
27. Osborne, J., S. J. Hunter, and E. Devaney. 1996. Anti-interleukin-4 modulation of the Th2 polarized response to the parasitic nematode Brugia pahangi. Infect. Immun. 64:3461-3466.
28. Pearlman, E., F. E. Hazlett, W. H. Boom, and J. W. Kazura. 1993. Induction of murine T helper cell responses to the filarial nematode Brugia malayi. Infect. Immun. 61:1105-1112.
29. Saeftel, M., L. Volkmann, S. Korten, N. Brattig, K. M. Al-Qaoud, B. Fleischer, and A. Hoerauf. 2001. Lack of IFN-γ confers impaired neutrophil granulocyte function and imparts prolonged survival of adult filarial worms in murine filariasis. Microbes Infect. 3:203-213.
30. Sartono, E., Y. C. Kruize, A. Kurniawan, R. M. Maizels, and M. Yazdanbakhsh. 1997. Depression of antigen-specific interleukin-5 and interferon-gamma responses in human lymphatic filariasis as a function of clinical status and age. J. Infect. Dis. 175:1276-1280.
31. Satoguina, J., M. Mempel, J. Larbi, M. Badusche, C. Loliger, 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.
32. Schandene, L., C. Alonso-Vega, F. Willems, C. Gerard, A. Delvaux, T. Velu, R. Devos, M. de Boer, and M. Goldman. 1994. B7/CD28-dependent IL-5 production by human resting T cells is inhibited by IL-10. J. Immunol. 152:4368-4374.
33. Schopf, L. R., K. F. Hoffmann, A. W. Cheever, J. F. Urban, Jr., and T. A. Wynn. 2002. IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. J. Immunol. 168:2383-2392.
34. Stampfli, M. R., M. Cwiartka, B. U. Gajewska, D. Alvarez, S. A. Ritz, M. D. Inman, Z. Xing, and M. Jordana. 1999. Interleukin-10 gene transfer to the airway regulates allergic mucosal sensitization in mice. Am. J. Respir. Cell Mol. Biol. 21:586-596.
35. Steel, C., and T. B. Nutman. 2003. Ctla-4 in filarial infections: implications for a role in diminished T cell reactivity. J. Immunol. 170:1930-1938.
36. Volkmann, L., O. Bain, M. Saeftel, S. Specht, K. Fischer, F. Brombacher, K. I. Matthaei, and A. Hoerauf. 2003. Murine filariasis: interleukin 4 and interleukin 5 lead to containment of different worm developmental stages. Med. Microbiol. Immunol. 192:23-31.
37. Volkmann, L., M. Saeftel, B. Fleischer, and A. Hoerauf. 2001. Interleukin-4 is essential for the control of microfilariae in murine infection with the filaria Litomosoides sigmodontis. Infect. Immun. 69:2950-2956.
38. Wang, P., P. Wu, M. I. Siegel, R. W. Egan, and M. M. Billah. 1995. Interleukin (IL)-10 inhibits nuclear factor kappa B (NF kappa B) activation in human monocytes. IL-10 and IL-4 suppress cytokine synthesis by different mechanisms. J. Biol. Chem. 270:9558-9563.
39. Williams, L., L. Bradley, A. Smith, and B. Foxwell. 2004. Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J. Immunol. 172:567-576.
40. Wynn, T. A., and K. F. Hoffmann. 2000. Defining a schistosomiasis vaccination strategy-is it really Th1 versus Th2? Parasitol. Today 16:497-501.
41. Zuany-Amorim, C., C. Creminon, M. C. Nevers, M. A. Nahori, B. B. Vargaftig, and M. Pretolani. 1996. Modulation by IL-10 of antigen-induced IL-5 generation, and CD4+ T lymphocyte and eosinophil infiltration into the mouse peritoneal cavity. J. Immunol. 157:377-384.
42. Zuany-Amorim, C., S. Haile, D. Leduc, C. Dumarey, M. Huerre, B. B. Vargaftig, and M. Pretolani. 1995. Interleukin-10 inhibits antigen-induced cellular recruitment into the airways of sensitized mice. J. Clin. Investig. 95:2644-2651.