IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge

Journal of Immunology

Volumn 182, Issue 12, 2009, Pages 7353-7363

  McKinstry, K Kai ^a   Strutt, Tara M ^a   Buck, Amanda ^a   Curtis, Jonathan D ^a   Dibble, John P ^a   Huston, Gail ^a   Tighe, Michael ^a   Hamada, Hiromasa ^a   Sell, Stewart ^b   Dutton, Richard W ^a   Swain, Susan L ^a  

^a TRUDEAU INSTITUTE   (United States)

^b ORDWAY RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; TRANSCRIPTION FACTOR FOXP3; VIRUS ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 17;

ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL POLARITY; CELL SURVIVAL; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; INFLUENZA; INFLUENZA VIRUS A H1N1; LUNG; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; TH17 CELL; WILD TYPE; ANIMAL; GENETICS; HELPER CELL; IMMUNOLOGY; METABOLISM; ORTHOMYXOVIRUS INFECTION; SURVIVAL RATE;

ANIMALS; ANTIGENS, VIRAL; FORKHEAD TRANSCRIPTION FACTORS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INTERLEUKIN-10; INTERLEUKIN-17; MICE; ORTHOMYXOVIRIDAE INFECTIONS; SURVIVAL RATE; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 67649226607     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900657     Document Type: Article

References (74)

1. 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.
2. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
3. Couper, K. N., D. G. Blount, and E. M. Riley. 2008. IL-10: the master regulator of immunity to infection. J. Immunol. 180: 5771-5777.
4. Li, C., I. Corraliza, and J. Langhorne. 1999. A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect. Immun. 67: 4435-4442. (Pubitemid 29400417)
5. Hunter, C. A., L. A. Ellis-Neyes, T. Slifer, S. Kanaly, G. Grunig, M. Fort, D. Rennick, and F. G. Araujo. 1997. IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. J. Immunol. 158: 3311-3316.
6. Holscher, C., M. Mohrs, W. J. Dai, G. Kohler, B. Ryffel, G. A. Schaub, H. Mossmann, and F. Brombacher. 2000. Tumor necrosis factor α-mediated toxic shock in Trypanosoma cruzi-infected interleukin 10-deficient mice. Infect. Immun. 68: 4075-4083.
7. Suzuki, Y., A. Sher, G. Yap, D. Park, L. E. Neyer, O. Liesenfeld, M. Fort, H. Kang, and E. Gufwoli. 2000. IL-10 is required for prevention of necrosis in the small intestine and mortality in both genetically resistant BALB/c and susceptible C57BL/6 mice following peroral infection with Toxoplasma gondii. J. Immunol. 164: 5375-5382.
8. + T cells and accompanied by overproduction of IL-12, IFN-γ and TNF-α. J. Immunol. 157: 798-805.
9. Deckert, M., S. Soltek, G. Geginat, S. Lutjen, M. Montesinos-Rongen, H. Hof, and D. Schluter. 2001. Endogenous interleukin-10 is required for prevention of a hyperinflammatory intracerebral immune response in Listeria monocytogenes meningoencephalitis. Infect. Immun. 69: 4561-4571.
10. Kuhn, R., J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
11. Kullberg, M. C., J. M. Ward, P. L. Gorelick, P. Caspar, S. Hieny, A. Cheever, D. Jankovic, and A. Sher. 1998. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and γ interferon-dependent mechanism. Infect. Immun. 66: 5157-5166.
12. Trinchieri, G. 2007. Interleukin-10 production by effector T cells: Th1 cells show self control. J. Exp. Med. 204: 239-243.
13. H1 cells control themselves by producing interleukin-10. Nat. Rev. 7: 425-428.
14. Roncarolo, M. G., S. Gregori, M. Battaglia, R. Bacchetta, K. Fleischhauer, and M. K. Levings. 2006. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol. Rev. 212: 28-50.
15. Denis, M., and E. Ghadirian. 1993. IL-10 neutralization augments mouse resistance to systemic Mycobacterium avium infections. J. Immunol. 151: 5425-5430. (Pubitemid 23332352)
16. Bermudez, L. E., and J. Champsi. 1993. Infection with Mycobacterium avium induces production of interleukin-10 (IL-10), and administration of anti-IL-10 antibody is associated with enhanced resistance to infection in mice. Infect. Immun. 61: 3093-3097.
17. Murray, P. J., and R. A. Young. 1999. Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect. Immun. 67: 3087-3095.
18. Wagner, R. D., N. M. Maroushek, J. F. Brown, and C. J. Czuprynski. 1994. Treatment with anti-interleukin-10 monoclonal antibody enhances early resistance to but impairs complete clearance of Listeria monocytogenes infection in mice. Infect. Immun. 62: 2345-2353.
19. Dai, W. J., G. Kohler, and F. Brombacher. 1997. Both innate and acquired immunity to Listeria monocytogenes infection are increased in IL-10-deficient mice. J. Immunol. 158: 2259-2267. (Pubitemid 127470010)
20. Brown, J. P., J. F. Zachary, C. Teuscher, J. J. Weis, and R. M. Wooten. 1999. Dual role of interleukin-10 in murine Lyme disease: regulation of arthritis severity and host defense. Infect. Immun. 67: 5142-5150.
21. Blackburn, S. D., and E. J. Wherry. 2007. IL-10, T cell exhaustion and viral persistence. Trends Microbiol. 15: 143-146.
22. Belkaid, Y., K. F. Hoffmann, S. Mendez, S. Kamhawi, M. C. Udey, T. A. Wynn, and D. L. Sacks. 2001. The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J. Exp. Med. 194: 1497-1506.
23. Brooks, D. G., M. J. Trifilo, K. H. Edelmann, L. Teyton, D. B. McGavern, and M. B. Oldstone. 2006. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 12: 1301-1309.
24. Ejrnaes, M., C. M. Filippi, M. M. Martinic, E. M. Ling, L. M. Togher, S. Crotty, and M. G. von Herrath. 2006. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203: 2461-2472.
25. Uzonna, J. E., G. Wei, D. Yurkowski, and P. Bretscher. 2001. Immune elimination of Leishmania major in mice: implications for immune memory, vaccination, and reactivation disease. J. Immunol. 167: 6967-6974.
26. Foulds, K. E., M. J. Rotte, and R. A. Seder. 2006. IL-10 is required for optimal CD8 T cell memory following Listeria monocytogenes infection. J. Immunol. 177: 2565-2574.
27. Baumgarth, N., L. Brown, D. Jackson, and A. Kelso. 1994. Novel features of the respiratory tract T-cell response to influenza virus infection: lung T cells increase expression of γ interferon mRNA in vivo and maintain high levels of mRNA expression for interleukin-5 (IL-5) and IL-10. J. Virol. 68: 7575-7581.
28. Sarawar, S. R., and P. C. Doherty. 1994. Concurrent production of interleukin-2, interleukin-10, and γ interferon in the regional lymph nodes of mice with influenza pneumonia. J. Virol. 68: 3112-3119.
29. Sarawar, S. R., S. R. Carding, W. Allan, A. McMickle, K. Fujihashi, H. Kiyono, J. R. McGhee, and P. C. Doherty. 1993. Cytokine profiles of bronchoalveolar lavage cells from mice with influenza pneumonia: consequences of CD4+ and CD8+ T cell depletion. Reg. Immunol. 5: 142-150.
30. Carding, S. R., W. Allan, A. McMickle, and P. C. Doherty. 1993. Activation of cytokine genes in T cells during primary and secondary murine influenza pneumonia. J. Exp. Med. 177: 475-482.
31. Jelley-Gibbs, D. M., D. M. Brown, J. P. Dibble, L. Haynes, S. M. Eaton, and S. L. Swain. 2005. Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J. Exp. Med. 202: 697-706.
32. Scott, B., R. Liblau, S. Degermann, L. A. Marconi, L. Ogata, A. J. Caton, H. O. McDevitt, and D. Lo. 1994. A role for non-MHC genetic polymorphism in susceptibility to spontaneous autoimmunity. Immunity 1: 73-83.
33. Roman, E., E. Miller, A. Harmsen, J. Wiley, U. H. Von Andrian, G. Huston, and S. L. Swain. 2002. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J. Exp. Med. 196: 957-968.
34. Lyons, A. B., and C. R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 171: 131-137.
35. McKinstry, K. K., S. Golech, W. H. Lee, G. Huston, N. P. Weng, and S. L. Swain. 2007. Rapid default transition of CD4 T cell effectors to functional memory cells. J. Exp. Med. 204: 2199-2211.
36. Kamperschroer, C., J. P. Dibble, D. L. Meents, P. L. Schwartzberg, and S. L. Swain. 2006. SAP is required for Th cell function and for immunity to influenza. J. Immunol. 177: 5317-5327. (Pubitemid 44527604)
37. Cottey, R., C. A. Rowe, and B. S. Bender. 2001. Influenza virus. In Current Protocols in Immunology. G. E. Coligan, A. M. Kruisbeek, E. M. Shevach, and W. Stober, eds. Wiley, New York, pp. 1-32.
38. Jelley-Gibbs, D. M., J. P. Dibble, D. M. Brown, T. M. Strutt, K. K. McKinstry, and S. L. Swain. 2007. Persistent depots of influenza antigen fail to induce a cytotoxic CD8 T cell response. J. Immunol. 178: 7563-7570.
39. Sell, S. 2001. T-cell mediated cytotoxicity. In Immunology, Immunopathology, and Immunity, 6th Ed. ASM Press, Washington, DC, pp. 401-430.
40. Williman, J., S. Young, G. Buchan, L. Slobbe, M. Wilson, P. Pang, J. Austyn, S. Preston, and M. Baird. 2008. DNA fusion vaccines incorporating IL-23 or RANTES for use in immunization against influenza. Vaccine 26: 5153-5158.
41. Schmitz, N., M. Kurrer, M. F. Bachmann, and M. Kopf. 2005. Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J. Virol. 79: 6441-6448.
42. Jayasekera, J. P., C. G. Vinuesa, G. Karupiah, and N. J. King. 2006. Enhanced antiviral antibody secretion and attenuated immunopathology during influenza virus infection in nitric oxide synthase-2-deficient mice. J. Gen. Virol. 87: 3361-3371.
43. H17 cell differentiation by antagonizing RORγt function. Nature 453: 236-240.
44. Liu, S. J., J. P. Tsai, C. R. Shen, Y. P. Sher, C. L. Hsieh, Y. C. Yeh, A. H. Chou, S. R. Chang, K. N. Hsiao, F. W. Yu, and H. W. Chen. 2007. Induction of a distinct CD8 Tnc17 subset by transforming growth factor-β and interleukin-6. J. Leukocyte Biol. 82: 354-360.
45. Brown, D. M., A. M. Dilzer, D. L. Meents, and S. L. Swain. 2006. CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. J. Immunol. 177: 2888-2898.
46. Shi, G., C. A. Cox, B. P. Vistica, C. Tan, E. F. Wawrousek, and I. Gery. 2008. Phenotype switching by inflammation-inducing polarized Th17 cells, but not by Th1 cells. J. Immunol. 181: 7205-7213.
47. Lee, Y. K., H. Turner, C. L. Maynard, J. R. Oliver, D. Chen, C. O. Elson, and C. T. Weaver. 2008. Late developmental plasticity in the T helper 17 lineage. Immunity 30: 92-107.
48. + T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8: 369-377.
49. Powell, T. J., T. Strutt, J. Reome, J. A. Hollenbaugh, A. D. Roberts, D. L. Woodland, S. L. Swain, and R. W. Dutton. 2007. Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J. Immunol. 178: 1030-1038.
50. de Jong, M. D., C. P. Simmons, T. T. Thanh, V. M. Hien, G. J. Smith, T. N. Chau, D. M. Hoang, N. V. Chau, T. H. Khanh, V. C. Dong, et al. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12: 1203-1207.
51. Salomon, R., E. Hoffmann, and R. G. Webster. 2007. Inhibition of the cytokine response does not protect against lethal H5N1 influenza infection. Proc. Natl. Acad. Sci. USA 104: 12479-12481.
52. Szretter, K. J., S. Gangappa, X. Lu, C. Smith, W. J. Shieh, S. R. Zaki, S. Sambhara, T. M. Tumpey, and J. M. Katz. 2007. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J. Virol. 81: 2736-2744.
53. - Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med.
54. - Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204: 285-297.
55. Wu, C. Y., J. R. Kirman, M. J. Rotte, D. F. Davey, S. P. Perfetto, E. G. Rhee, B. L. Freidag, B. J. Hill, D. C. Douek, and R. A. Seder. 2002. Distinct lineages of TH1 cells have differential capacities for memory cell generation in vivo. Nat. Immunol. 3: 852-858.
56. Awasthi, A., Y. Carrier, J. P. Peron, E. Bettelli, M. Kamanaka, R. A. Flavell, V. K. Kuchroo, M. Oukka, and H. L. Weiner. 2007. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat. Immunol. 8: 1380-1389.
57. Meyaard, L., E. Hovenkamp, S. A. Otto, and F. Miedema. 1996. IL-12-induced IL-10 production by human T cells as a negative feedback for IL-12-induced immune responses. J. Immunol. 156: 2776-2782. (Pubitemid 126660624)
58. Peritt, D., M. Aste-Amezaga, F. Gerosa, C. Paganin, and G. Trinchieri. 1996. Interleukin-10 induction by IL-12: a possible modulatory mechanism? Ann. NY Acad. Sci. 795: 387-389.
59. Stumhofer, J. S., J. S. Silver, A. Laurence, P. M. Porrett, T. H. Harris, L. A. Turka, M. Ernst, C. J. Saris, J. J. O'Shea, and C. A. Hunter. 2007. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat. Immunol. 8: 1363-1371.
60. Levings, M. K., R. Sangregorio, F. Galbiati, S. Squadrone, R. de Waal Malefyt, and M. G. Roncarolo. 2001. IFN-α and IL-10 induce the differentiation of human type 1 T regulatory cells. J. Immunol. 166: 5530-5539.
61. Kadowaki, N., S. Antonenko, J. Y. Lau, and Y. J. Liu. 2000. Natural interferon α/β-producing cells link innate and adaptive immunity. J. Exp. Med. 192: 219-226.
62. Ouyang, W., J. K. Kolls, and Y. Zheng. 2008. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467.
63. Muranski, P., A. Boni, P. A. Antony, L. Cassard, K. R. Irvine, A. Kaiser, C. M. Paulos, D. C. Palmer, C. E. Touloukian, K. Ptak, et al. 2008. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 112: 362-373.
64. Brown, D. M., E. Roman, and S. L. Swain. 2004. CD4 T cell responses to influenza infection. Semin. Immunol. 16: 171-177.
65. Inoue, D., M. Numasaki, M. Watanabe, H. Kubo, T. Sasaki, H. Yasuda, M. Yamaya, and H. Sasaki. 2006. IL-17A promotes the growth of airway epithelial cells through ERK-dependent signaling pathway. Biochem. Biophys. Res. Commun. 347: 852-858.
66. Aujla, S. J., Y. R. Chan, M. Zheng, M. Fei, D. J. Askew, D. A. Pociask, T. A. Reinhart, F. McAllister, J. Edeal, K. Gaus, et al. 2008. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 14: 275-281.
67. + T cell-mediated suppression by dendritic cells. Science 299: 1033-1036.
68. Jones, S. A. 2005. Directing transition from innate to acquired immunity: defining a role for IL-6. J. Immunol. 175: 3463-3468. (Pubitemid 41292002)
69. Kolls, J. K., P. B. McCray, Jr., and Y. R. Chan. 2008. Cytokine-mediated regulation of antimicrobial proteins. Nat. Rev. 8: 829-835.
70. Sun, J., R. Madan, C. L. Karp, and T. J. Braciale. 2009. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat. Med. 15: 277-284.
71. Ivanov, I. I., L. Frutos Rde, N. Manel, K. Yoshinaga, D. B. Rifkin, R. B. Sartor, B. B. Finlay, and D. R. Littman. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4: 337-349.
72. + memory T lymphocytes. J. Immunol. 179: 2389-2396.
73. Jelley-Gibbs, D. M., T. M. Strutt, K. K. McKinstry, and S. L. Swain. 2008. Influencing the fates of CD4 T cells on the path to memory: lessons from influenza. Immunol. Cell Biol. 86: 343-352.
74. Gu, Y., J. Yang, X. Ouyang, W. Liu, H. Li, J. Yang, J. Bromberg, S. H. Chen, L. Mayer, J. C. Unkeless, and H. Xiong. 2008. Interleukin 10 suppresses Th17 cytokines secreted by macrophages and T cells. Eur. J. Immunol.