T-cell-specific deletion of gp130 renders the highly susceptible IL-10-deficient mouse resistant to intestinal nematode infection

European Journal of Immunology

Volumn 39, Issue 8, 2009, Pages 2173-2183

  Fasnacht, Nicolas ^a   Greweling, Marina C ^a   Bollati Fogolín, Mariela ^a,b   Schippers, Angela ^a,c   Müller, Werner ^a,d  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cytokine receptor; Helminthic infection; Inflammation Th1 Th2 Th17 cells; Transgenic mice

Indexed keywords

CYTOKINE; GLYCOPROTEIN GP 130; INTERLEUKIN 10; INTERLEUKIN 6; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 17;

ACUTE PHASE RESPONSE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CECUM; CELLULAR IMMUNITY; CONTROLLED STUDY; DATA ANALYSIS; IN VIVO STUDY; INFECTION RESISTANCE; INFECTION SENSITIVITY; INFLAMMATION; INTESTINE INFECTION; MOUSE; NEMATODIASIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; TRICHURIS; WORM EXPULSION; ANIMAL; C57BL MOUSE; FEMALE; FLOW CYTOMETRY; GENETICS; HELPER CELL; HOST PARASITE INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; MALE; METABOLISM; MOUSE MUTANT; PARASITOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; TRICHINOSIS;

ANIMALS; CYTOKINE RECEPTOR GP130; CYTOKINES; FEMALE; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; INTERLEUKIN-10; INTERLEUKIN-17; INTESTINAL DISEASES, PARASITIC; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS; TH2 CELLS; TRICHINOSIS; TRICHURIS;

EID: 70249104692     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838710     Document Type: Article

References (49)

1. Taga, T. and Kishimoto, T., Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 1997. 15: 797-819.
2. Kastelein, R. A., Hunter, C. A. and Cua, D. J., Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu. Rev. Immunol. 2007. 25: 221-242.
3. Naka, T., Nishimoto, N. and Kishimoto, T., The paradigm of IL-6: from basic science to medicine. Arthritis Res. 2002. 4: S233-S242.
4. Kishimoto, T., Akira, S., Narazaki, M. and Taga, T., Interleukin-6 family of cytokines and gp130. Blood 1995. 86: 1243-1254.
5. Betz,U. A., Bloch,W., vanden Broek, M.,Yoshida,K., Taga,T., Kishimoto,T., Addicks, K. et al., Postnatally induced inactivation of gp130 in mice results in neurological, cardiac, hematopoietic, immunological, hepatic, and pulmonary defects. J. Exp. Med. 1998. 188: 1955-1965.
6. Yoshida, K., Taga, T., Saito, M., Suematsu, S., Kumanogoh, A., Tanaka, T., Fujiwara, H. et al., Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc. Natl. Acad. Sci. USA 1996. 93: 407-411.
7. Hirano, T., Interleukin 6 and its receptor: ten years later. Int. Rev. Immunol. 1998. 16: 249-284.
8. Fasnacht, N. and Muller,W., Conditional gp130 deficient mouse mutants. Semin. Cell Dev. Biol. 2008. 19: 379-384.
9. Rose-John, S., Scheller, J., Elson, G. and Jones, S. A., Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J. Leukoc. Biol. 2006. 80: 227-236.
10. Sawa, S., Kamimura, D., Jin, G. H., Morikawa, H., Kamon, H., Nishihara,M., Ishihara, K. et al., Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+T cells. J. Exp. Med. 2006. 203: 1459-1470.
11. Mitsuyama, K., Sata, M. and Rose-John, S., Interleukin-6 trans-signaling in inflammatory bowel disease. Cytokine Growth Factor Rev. 2006. 17: 451-461. (Pubitemid 44793118)
12. Weaver, C. T., Hatton, R. D., Mangan, P. R. and Harrington, L. E., IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 2007. 25: 821-852.
13. Bettelli, E., Korn, T. and Kuchroo, V. K., Th17: the third member of the effector T cell trilogy. Curr. Opin. Immunol. 2007. 19: 652-657.
14. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L. and Kuchroo, V. K., Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006. 441: 235-238.
15. Veldhoen,M., Hocking, R. J., Atkins, C. J., Locksley, R. M. and Stockinger, B., TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006. 24: 179-189. (Pubitemid 43214587)
16. Mangan,P. R., Harrington,L. E., O'Quinn,D. B., Helms,W. S., Bullard,D. C., Elson,C. O., Hatton,R. D. et al., Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006. 441: 231-234.
17. Ivanov, II, McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J. and Littman, D. R., The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+T helper cells. Cell 2006. 126: 1121-1133. (Pubitemid 44380299)
18. Nishihara, M., Ogura, H., Ueda, N., Tsuruoka, M., Kitabayashi, C., Tsuji, F., Aono, H. et al., IL-6-gp130-STAT3 in T cells directs the development of IL-17+Th with a minimum effect on that of Treg in the steady state. Int. Immunol. 2007. 19: 695-702.
19. Stumhofer, J. S., Laurence, A., Wilson, E. H., Huang, E., Tato, C. M., Johnson, L. M., Villarino, A. V. et al., Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 2006. 7: 937-945.
20. Li, M. O., Wan, Y. Y. and Flavell, R. A., T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 2007. 26: 579-591.
21. Fontenot, J. D., Gavin, M. A. and Rudensky, A. Y., Foxp3 programs the development and function of CD4+CD25+regulatory T cells. Nat. Immunol. 2003. 4: 330-336.
22. Cliffe, L. J. and Grencis, R. K., The Trichuris muris system: a paradigm of resistance and susceptibility to intestinal nematode infection. Adv. Parasitol. 2004. 57: 255-307.
23. Cliffe, L. J., Humphreys, N. E., Lane, T. E., Potten, C. S., Booth, C. and Grencis, R. K., Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 2005. 308: 1463-1465. (Pubitemid 40791299)
24. Bancroft, A. J., Artis, D., Donaldson, D. D., Sypek, J. P. and Grencis, R. K., Gastrointestinal nematode expulsion in IL-4 knockout mice is IL-13 dependent. Eur. J. Immunol. 2000. 30: 2083-2091.
25. Else, K. J., Finkelman, F. D., Maliszewski, C. R. and Grencis, R. K., Cytokine-mediated regulation of chronic intestinal helminth infection. J. Exp. Med. 1994. 179: 347-351.
26. Schopf, L. R., Hoffmann, K. F., Cheever, A. W., Urban, Jr. J. F., and Wynn, T. A., IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. J. Immunol. 2002. 168: 2383-2392.
27. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K. and Muller,W., Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993. 75: 263-274.
28. 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.
29. Sonderegger, I., Iezzi, G., Maier, R., Schmitz, N., Kurrer, M. and Kopf, M., GM-CSF mediates autoimmunity by enhancing IL-6-dependent Th17 cell development and survival. J. Exp. Med. 2008. 205: 2281-2294.
30. Korn, T., Bettelli, E., Oukka, M. and Kuchroo, V. K., IL-17 and Th17 Cells. Annu. Rev. Immunol. 2009. 27: 485-517.
31. Stark, M. A., Huo, Y., Burcin, T. L., Morris, M. A., Olson, T. S. and Ley, K., Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 2005. 22: 285-294. (Pubitemid 40387471)
32. Whittaker, L., Niu, N., Temann, U. A., Stoddard, A., Flavell, R. A., Ray, A., Homer, R. J. and Cohn, L., Interleukin-13 mediates a fundamental pathway for airway epithelial mucus induced by CD4 T cells and interleukin-9. Am. J. Respir. Cell Mol. Biol. 2002. 27: 593-602.
33. Hurst, S. M., Wilkinson, T. S., McLoughlin, R. M., Jones, S., Horiuchi, S., Yamamoto, N., Rose-John, S. et al., Il-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 2001. 14: 705-714. (Pubitemid 32592418)
34. Rabe, B., Chalaris, A., May, U.,Waetzig, G. H., Seegert, D.,Williams, A. S., Jones, S. A. et al., Transgenic blockade of Interleukin-6-trans-signaling abrogates inflammation. Blood 2008. 111: 1021-1028. (Pubitemid 351213379)
35. Xing, Z., Gauldie, J., Cox, G., Baumann, H., Jordana, M., Lei, X. F. and Achong, M. K., IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J. Clin. Invest. 1998. 101: 311-320.
36. Artis, D., Villarino, A., Silverman, M., He, W., Thornton, E. M., Mu, S., Summer, S. et al., The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. J. Immunol. 2004. 173: 5626-5634. (Pubitemid 39392150)
37. Yoshimoto, T., Yoshimoto, T., Yasuda, K., Mizuguchi, J. and 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.
38. Lucas, S., Ghilardi, N., Li, J. and de Sauvage, F. J., IL-27 regulates IL-12 responsiveness of naive CD4+T cells through Stat1-dependent and - independent mechanisms. Proc. Natl. Acad. Sci. USA 2003. 100: 15047-15052.
39. Anderson, C. F., Oukka, M., Kuchroo, V. J. and Sacks, D., CD4(+)CD25 (-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 2007. 204: 285-297.
40. Jankovic, D., Kullberg, M. C., Feng, C. G., Goldszmid, R. S., Collazo, C. M., Wilson, M.,Wynn, T. A. et al., Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 2007. 204: 273-283.
41. Dominitzki, S., Fantini, M. C., Neufert, C., Nikolaev, A., Galle, P. R., Scheller, J., Monteleone, G. et al., Cutting edge: trans-signaling via the soluble IL-6R abrogates the induction of FoxP3 in naive CD4+CD25 T cells. J. Immunol. 2007. 179: 2041-2045.
42. Xu, L., Kitani, A., Fuss, I. and Strober,W., Cutting Edge: Regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J. Immunol. 2007. 178: 6725-6729.
43. Jenkins, B. J., Grail, D., Nheu, T., Najdovska, M., Wang,B., Waring,P., Inglese,M. et al., Hyperactivation of Stat3 in gp130 mutant mice promotes gastric hyperproliferation and desensitizes TGF-beta signaling. Nat. Med. 2005. 11: 845-852.
44. Korn, T., Mitsdoerffer, M., Croxford, A. L., Awasthi, A., Dardalhon, V. A., Galileos, G., Vollmar, P. et al., IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3+regulatory T cells. Proc. Natl. Acad. Sci. USA 2008. 105: 18460-18465.
45. Artis, D., New weapons in the war on worms: identification of putative mechanisms of immune-mediated expulsion of gastrointestinal nematodes. Int. J. Parasitol. 2006. 36: 723-733.
46. Schmidt, C., Giese, T., Ludwig, B.,Mueller-Molaian, I.,Marth, T., Zeuzem, S., Meuer, S. C. and Stallmach,A., Expression of interleukin-12-related cytokine transcripts in inflammatory bowel disease: elevated interleukin-23p19 and interleukin-27p28 in Crohn's disease but not in ulcerative colitis. Inflamm. Bowel Dis. 2005. 11: 16-23.
47. Ito, H., Takazoe, M., Fukuda, Y., Hibi, T., Kusugami, K., Andoh, A., Matsumoto, T. et al., A pilot randomized trial of a human anti-interleukin-6 receptor monoclonal antibody in active Crohn's disease. Gastroenterology 2004. 126: 989-996; discussion 947. (Pubitemid 38451170)
48. Mazurier, F., Fontanellas, A., Salesse, S., Taine, L., Landriau, S., Moreau-Gaudry, F., Reiffers, J. et al., A novel immunodeficient mouse model - RAG2 x common cytokine receptor gamma chain double mutants - requiring exogenous cytokine administration for human hematopoietic stem cell engraftment. J. Interferon Cytokine Res. 1999. 19: 533-541. (Pubitemid 29269944)
49. Lee, P. P., Fitzpatrick, D. R., Beard, C., Jessup, H. K., Lehar, S., Makar, K. W., Perez-Melgosa, M. et al., A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 2001. 15: 763-774. (Pubitemid 34008504)