Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection

Journal of Experimental Medicine

Volumn 206, Issue 2, 2009, Pages 313-328

  Hou, Wanqiu ^a   Kang, Hyun Seok ^a   Kim, Byung S ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG ANTIBODY; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 6; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DEMYELINATING DISEASE; DISEASE SEVERITY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MOLECULE; MOUSE; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; PATHOGENESIS; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; TARGET CELL DESTRUCTION; TH17 CELL; UPREGULATION; VIRUS NEUTRALIZATION; ANIMAL; COMPARATIVE STUDY; CYTOTOXICITY TEST; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; HELPER CELL; IMMUNOLOGY; TRANSGENIC MOUSE; VIROLOGY; VIRUS INFECTION;

ANIMALS; CARDIOVIRUS INFECTIONS; CYTOTOXICITY TESTS, IMMUNOLOGIC; DEMYELINATING DISEASES; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; INTERLEUKIN-17; INTERLEUKIN-6; MICE; MICE, TRANSGENIC; T-LYMPHOCYTES, HELPER-INDUCER; THEILOVIRUS;

EID: 63049129392     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20082030     Document Type: Article

References (70)

1. Abbas, A.K., K.M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature. 383:787-793.
2. Harrington, L.E., R.D. Hatton, P.R. Mangan, H. Turner, T.L. Murphy, K.M. Murphy, and C.T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6:1123-1132.
3. Weaver, C.T., L.E. Harrington, P.R. Mangan, M. Gavrieli, and K.M. Murphy. 2006. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity. 24:677-688.
4. Steinman, L. 2007. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat. Med. 13:139-145.
5. Park, H., Z. Li, X.O. Yang, S.H. Chang, R. Nurieva, Y.H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing in- terleukin 17. Nat. Immunol. 6:1133-1141.
6. Veldhoen, M., R.J. Hocking, C.J. Atkins, R.M. Locksley, and B. Stockinger. 2006. TGFbeta in the context of an inflammatory kine milieu supports de novo differentiation of IL-17-producing T cells. Immunity. 24:179-189.
7. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T.B. Strom, M. Oukka, H.L. Weiner, and V.K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 441:235-238.
8. Mangan, P.R., L.E. Harrington, D.B. O'Quinn, W.S. Helms, D.C. Bullard, C.O. Elson, R.D. Hatton, S.M. Wahl, T.R. Schoeb, and C.T. Weaver. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature. 441:231-234.
9. McGeachy, M.J., and D.J. Cua. 2008. Th17 cell differentiation: the long and winding road. Immunity. 28:445-453.
10. 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.
11. Bettelli, E., M. Oukka, and V.K. Kuchroo. 2007. T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8:345-350.
12. Dong, C. 2008. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 8:337-348.
13. Bettelli, E., T. Korn, M. Oukka, and V.K. Kuchroo. 2008. Induction and effector functions of T(H)17 cells. Nature. 453:1051-1057.
14. Maek-A-Nantawat, W., S. Buranapraditkun, J. Klaewsongkram, and K. Ruxrungthum. 2007. Increased interleukin-17 production both in helper T cell subset Th17 and CD4-negative T cells in human immunodeficiency virus infection. Viral Immunol. 20:66-75.
15. Ndhlovu, L.C., J.M. Chapman, A.R. J ha, J.E. Snyder-Cappione, M. Pagan, F.E. Leal, B.S. Boland, P.J. Norris, M.G. Rosenberg, and D.F. Nixon. 2008. Suppression of HIV-1 plasma viral load below detection preserves IL-17 producing T cells in HIV-1 infection. AIDS. 22:990-992.
16. Alfano, M., A. Crotti, E. Vicenzi, and G. Poli. 2008. New players in cytokine control of HIV infection. Curr. HIV/AIDS Res. 5:27-32.
17. Yue, F.Y., A. Merchant, C.M. Kovacs, M. Loutfy, D. Persad, and M.A. Ostrowski. 2008. Virus-specific interleukin-17-producing CD4+ T cells are detectable in early human immunodeficiency virus type 1 infection. J. Virol. 82:6767-6771.
18. Molesworth-Kenyon, S.J., R. Yin, J.E. Oakes, and R.N. Lausch. 2008. IL-17 receptor signaling influences virus-induced corneal inflammation. J. Leukoc. Biol. 83:401-408.
19. Hashimoto, K., J.E. Durbin, W. Zhou, R.D. Collins, S.B. Ho, J.K. Kolls, P.J. Dubin, J.R. Sheller, K. Goleniewska, J.F. O'Neal, et al. 2005. Respiratory syncytial virus infection in the absence of STAT 1 results in airway dysfunction, airway mucus, and augmented IL-17 levels. J. Allergy Clin. Immunol. 116:550-557.
20. Doherty, P.C., W. Allan, M. Eichelberger, and S.R. Carding. 1992. Roles of alpha beta and gamma delta T cell subsets in viral immunity. Annu. Rev. Immunol. 10:123-151.
21. Raffatellu, M., R.L. Santos, D.E. Verhoeven, M.D. George, R.P. Wilson, S.E. Winter, I. Godinez, S. Sankaran, T.A. Paixao, M.A. Gordon, et al. 2008. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat. Med. 14:421-428.
22. Guo, B., E.Y. Chang, and G. Cheng. 2008. The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J. Clin. Invest. 118:1680-1690.
23. Shinohara, M.L., J.H. Kim, V.A. Garcia, and H. Cantor. 2008. Engagement of the type I interferon receptor on dendritic cells inhibits T helper 17 cell development: role of intracellular osteopontin. Immunity. 29:68-78.
24. Sen, G.C. 2001. Viruses and interferons. Annu. Rev. Microbiol. 55: 255-281.
25. Intlekofer, A.M., A. Banerjee, N. Takemoto, S.M. Gordon, C.S. Dejong, H. Shin, C.A. Hunter, E.J. Wherry, T. Lindsten, and S.L. Reiner. 2008. Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science. 321:408-411.
26. Stumhofer, J.S., A. Laurence, E.H. Wilson, E. Huang, C.M. Tato, L.M. Johnson, A.V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, et al. 2006. Interleukin 27 negatively regulates the development of interleukin 17- producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7:937-945.
27. Pene, J., S. Chevalier, L. Preisser, E. Venereau, M.H. Guilleux, S. Ghannam, J.P. Moles, Y. Danger, E. Ravon, S. Lesaux, et al. 2008. Chronically inflamed human tissues are infiltrated by highly differentiated Th17 lymphocytes. J. Immunol. 180:7423-7430.
28. Dal Canto, M.C., B.S. Kim, S.D. Miller, and R.W. Melvold. 1996. Theiler's murine encephalomyelitis virus (TMEV)-induced demyelin- ation: a model for human multiple sclerosis. Methods. 10:453-461.
29. Brahic, M., J.F. Bureau, and T. Michiels. 2005. The genetics of the persistent infection and demyelinating disease caused by Theiler's virus. Annu. Rev. Microbiol. 59:279-298.
30. Hou, W., E.Y. So, and B.S. Kim. 2007. Role of dendritic cells in differential susceptibility to viral demyelinating disease. PLoS Pathog. 3:e124.
31. Whitton, J.L., C.T. Cornell, and R. Feuer. 2005. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 3:765-776.
32. Pullen, L.C., S.H. Park, S.D. Miller, M.C. Dal Canto, and B.S. Kim. 1995. Treatment with bacterial LPS renders genetically resistant C57BL/6 mice susceptible to Theiler's virus-induced demyelinating disease. J. Immunol. 155:4497-4503.
33. Kroenke, M.A., T.J. Carlson, A.V. Andjelkovic, and B.M. Segal. 2008. IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 205:1535-1541.
34. Son, K.N., R.P. Becker, P. Kallio, and H.L. Lipton. 2008. Theiler's virus-induced intrinsic apoptosis in M1-D macrophages is Bax mediated and restricts virus infectivity: a mechanism for persistence of a cytolytic virus. J. Virol. 82:4502-4510.
35. Kolls, J.K., and A. Linden. 2004. Interleukin-17 family members and inflammation. Immunity. 21:467-476.
36. Lowin, B., C. Mattman, M. Hahne, and J. Tschopp. 1996. Comparison of Fas(Apo-1/CD95)- and perforin-mediated cytotoxicity in primary T lymphocytes. Int. Immunol. 8:57-63.
37. Jellison, E.R., S.K. Kim, and R.M. Welsh. 2005. Cutting edge: MHC class II-restricted killing in vivo during viral infection. J. Immunol. 174:614-618.
38. Palma, J.P., R.L. Yauch, S. Lang, and B.S. Kim. 1999. Potential role of CD4+ T cell-mediated apoptosis of activated astrocytes in Theiler's virus-induced demyelination. J. Immunol. 162:6543-6551.
39. Chang, J.R., E. Zaczynska, C.D. Katsetos, C.D. Platsoucas, and E.L. Oleszak. 2000. Differential expression of TGF-beta, IL-2, and other cytokines in the CNS of Theiler' s murine encephalomyelitis virus-infected susceptible and resistant strains of mice. Virology. 278:346-360.
40. Jin, Y.H., M. Mohindru, M.H. Kang, A.C. Fuller, B. Kang, D. Gallo, and B.S. Kim. 2007. Differential virus replication, cytokine production, and antigen-presenting function by microglia from susceptible and resistant mice infected with Theiler's virus. J. Virol. 81:11690-11702.
41. Kang, M.H., E.Y. So, H. Park, and B.S. Kim. 2008. Replication of Theiler's virus requires NF-kappaB-activation: higher viral replication and spreading in astrocytes from susceptible mice. Glia. 56:942-953.
42. So, E.Y., M.H. Kang, and B.S. Kim. 2006. Induction of chemokine and cytokine genes in astrocytes following infection with Theiler' s murine encephalomyelitis virus is mediated by the Toll-like receptor 3. Glia. 53:858-867.
43. Trottier, M., B.P. Schlitt, A.Y. Kung, and H.L. Lipton. 2004. Transition from acute to persistent Theiler' s virus infection requires active viral replication that drives proinflammatory cytokine expression and chronic demyelinating disease. J. Virol. 78:12480-12488.
44. Wiehler, S., and D. Proud. 2007. Interleukin-17A modulates human airway epithelial responses to human rhinovirus infection. Am. J. Physiol. Lung Cell. Mol. Physiol. 293:L505-L515.
45. Mohindru, M., B. Kang, and B.S. Kim. 2006. Initial capsid-specific CD4(+) T cell responses protect against Theiler's murine encephalomyeli- tisvirus-induced demyelinating disease. Eur. J. Immunol. 36:2106-2115.
46. Buljevac, D., H.Z. Flach, W.C. Hop, D. Hijdra, J.D. Laman, H.F. Savelkoul, F.G. van Der Meche, P.A. van Doorn, and R.Q. Hintzen. 2002. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain. 125:952-960.
47. Correale, J., M. Fiol, and W. Gilmore. 2006. The risk of relapses in multiple sclerosis during systemic infections. Neurology. 67:652-659.
48. Stuve, O., and S.S. Zamvil. 1999. Pathogenesis, diagnosis, and treatment of acute disseminated encephalomyelitis. Curr. Opin. Neurol. 12:395-401.
49. Young, N.P., B.G. Weinshenker, and C.F. Lucchinetti. 2008. Acute disseminated encephalomyelitis: current understanding and controversies. Semin. Neurol. 28:84-94.
50. Numasaki, M., J.-i. Fukushi, M. Ono, S.K. Narula, P.J. Zavodny, T. Kudo, P.D. Robbins, H. Tahara, and M.T. Lotze. 2003. Interleukin-17 promotes angiogenesis and tumor growth. Blood. 101:2620-2627.
51. Numasaki, M., M. Watanabe, T. Suzuki, H. Takahashi, A. Nakamura, F. McAllister, T. Hishinuma, J. Goto, M.T. Lotze, J.K. Kolls, and H. Sasaki. 2005. IL-17 enhances the net angiogenic activity and in vivo growth of human non-small cell lung cancer in SCID mice through promoting CXCR-2-dependent angiogenesis. J. Immunol. 175:6177-6189.
52. Wong, P., and E.G. Pamer. 2003. CD8 T cell responses to infectious pathogens. Annu. Rev. Immunol. 21:29-70.
53. Kagi, D., F. Vignaux, B. Ledermann, K. Burki, V. Depraetere, S. Nagata, H. Hengartner, and P. Golstein. 1994. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science. 265:528-530.
54. Lowin, B., M. Hahne, C. Mattmann, and J. Tschopp. 1994. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature. 370:650-652.
55. Harty, J.T., A.R. Tvinnereim, and D.W. White. 2000. CD8+ T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 18:275-308.
56. van de Berg, P.J., E.M. van Leeuwen, I.J. Ten Berge, and R. van Lier. 2008. Cytotoxic human CD4(+) T cells. Curr. Opin. Immunol. 20:339-343.
57. You, Z., X.-B. Shi, G. DuRaine, D. Haudenschild, C.G. Tepper, S.H. Lo, R. Gandour-Edwards, R.W. de Vere White, and A.H. Reddi. 2006. Interleukin-17 receptor-like gene is a novel antiapoptotic gene highly expressed in androgen-independent prostate cancer. Cancer Res. 66:175-183.
58. Palmer, M.T., and C.T. Weaver. 2007. Immunology: narcissistic helpers. Nature. 448:416-418.
59. Nurieva, R., X.O. Yang, G. Martinez, Y. Zhang, A.D. Panopoulos, L. Ma, K. Schluns, Q. Tian, S.S. Watowich, A.M. Jetten, and C. Dong. 2007.
60. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature. 448:480-483.
61. Korn, T., E. Bettelli, W. Gao, A. Awasthi, A. Jager, T.B. Strom, M. Oukka, and V.K. Kuchroo. 2007. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature. 448:484-487.
62. Barker, B.R., J.G. Parvani, D. Meyer, A.S. Hey, K. Skak, and N.L. Letvin. 2007. IL-21 induces apoptosis of antigen-specific CD8+ T lymphocytes. J. Immunol. 179:3596-3603.
63. Levillayer, F., M. Mas, F. Levi-Acobas, M. Brahic, and J.F. Bureau. 2007. Interleukin 22 is a candidate gene for Tmevp3, a locus controlling Theiler's virus-induced neurological diseases. Genetics. 176:1835-1844.
64. Kang, J.A., M. Mohindru, B.S. Kang, S.H. Park, and B.S. Kim. 2000. Clonal expansion of infiltrating T cells in the spinal cords of SJL/J mice infected with Theiler's virus. J. Immunol. 165:583-590.
65. Hou, W., Y. Wu, S. Sun, M. Shi, Y. Sun, C. Yang, G. Pei, Y. Gu, C. Zhong, and B. Sun. 2003. Pertussis toxin enhances Th1 responses by stimulation of dendritic cells. J. Immunol. 170:1728-1736.
66. Crane, M.A., C. J ue, M. Mitchell, H. Lipton, and B.S. Kim. 1990. Detection of restricted predominant epitopes of Theiler' s murine en-cephalomyelitis virus capsid proteins expressed in the lambda gt11 system: differential patterns of antibody reactivity among different mouse strains. J. Neuroimmunol. 27:173-186.
67. Myoung, J., Y. Il Bahk, H.S. Kang, M.C. Dal Canto, and B.S. Kim. 2008. Anti-capsid immunity level, not viral persistence level, correlates with the progression of Theiler's virus-induced demyelinating disease in viral P1-transgenic mice. J. Virol. 82:5606-5617.
68. Myoung, J., W. Hou, B. Kang, M.A. Lyman, J.A. Kang, and B.S. Kim. 2007. The immunodominant CD8+ T cell epitope region of Theiler's virus in resistant C57BL/6 mice is critical for anti-viral immune responses, viral persistence, and binding to the host cells. Virology. 360:159-171.
69. Ivanov, B.S. McKenzie, L. Zhou, C.E. Tadokoro, A. Lepelley, J.J. Lafaille, D.J. Cua, and D.R. Littman. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell. 126:1121-1133.
70. Zhao, D.-M., A.M. Thornton, R.J. DiPaolo, and E.M. Shevach. 2006. Activated CD4+CD25+ T cells selectively kill B lymphocytes. Blood. 107:3925-3932.