Regulatory T cells and Th17 cells in viral infections: Implications for multiple sclerosis and myocarditis

Future Virology

Volumn 7, Issue 6, 2012, Pages 593-608

  Martinez, Nicholas E ^a   Sato, Fumitaka ^a   Kawai, Eiichiro ^a   Omura, Seiichi ^a   Chervenak, Robert P ^a   Tsunoda, Ikuo ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

autoimmunity; Cardiovirus infections; CNS demyelinating disease; coinfection; experimental nervous system autoimmune disease; immunology; inflammation; Picornaviridae infections; regulatory T lymphocyte; Th17 cells

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; BETA GALACTOSIDE; CD4 ANTIGEN; CHOLINERGIC RECEPTOR; ECALECTIN; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 6; INTERLEUKIN 8; RECOMBINANT BLOOD CLOTTING FACTOR 8; RETINOIC ACID; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

BONE MARROW CELL; CANDIDA ALBICANS; HEART ARRHYTHMIA; HEPATITIS; HEPATITIS VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN PARVOVIRUS B19; IMMUNE RESPONSE; IN VITRO STUDY; KLEBSIELLA PNEUMONIAE; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; STROMA CELL; TH17 CELL; THORAX PAIN; VIRAL CLEARANCE; VIRUS INFECTION; VIRUS LOAD; VIRUS MYOCARDITIS; VIRUS REPLICATION; WEST NILE FLAVIVIRUS;

CARDIOVIRUS; PICORNAVIRIDAE;

EID: 84862015936     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.12.44     Document Type: Review

References (125)

1. Crowe CR, Chen K, Pociask DA et al. Critical role of IL-17RA in immunopathology of influenza infection. J. Immunol. 183(8), 5301-5310 (2009).
2. Sato F, Omura S, Martinez NE, Tsunoda I. Animal models of multiple sclerosis. In: Neuroinflammation. Minager A (Ed.). Elsevier, Amsterdam, The Netherlands, 55-80 (2011).
3. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8(9), 942-949 (2007).
4. Wilson NJ, Boniface K, Chan JR et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8(9), 950-957 (2007).
5. + Treg in the presence of lineage-specific polarizing factors. Proc. Natl Acad. Sci. USA 107(45), 19402-19407 (2010).
6. Ghoreschi K, Laurence A, Yang XP et al. Generation of pathogenic Th17 cells in the absence of TGF-beta signalling. Nature 467(7318), 967-971 (2010).
7. Volpe E, Servant N, Zollinger R et al. A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human Th-17 responses. Nat. Immunol. 9(6), 650-657 (2008).
8. Yang L, Anderson DE, Baecher-Allan C et al. IL-21 and TGF-beta are required for differentiation of human Th17 cells. Nature 454(7202), 350-352 (2008).
9. Manel N, Unutmaz D, Littman DR. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat. Immunol. 9(6), 641-649 (2008).
10. Zou W, Restifo NP. Th17 cells in tumour immunity and immunotherapy. Nat. Immunol. 10(4), 248-256 (2010).
11. Karlsson F, Robinson-Jackson SA, Gray L, Zhang S, Grisham MB. Ex vivo generation of regulatory T cells: characterization and therapeutic evaluation in a model of chronic colitis. Method Mol. Biol. 677, 47-61 (2011). Demonstrates a method for generating approximately 20 million highly purified Tregs from one mouse spleen.
12. Hogquist KA, Baldwin TA, Jameson SC. Central tolerance: learning self-control in the thymus. Nat. Immunol. 5(10), 772-782 (2005).
13. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA. Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 24, 99-146 (2006).
14. Peng Y, Laouar Y, Li MO, Green EA, Flavell RA. TGF-beta regulates in vivo expansion of FOXP3-expressing CD4+CD25+ regulatory T cells responsible for protection against diabetes. Proc. Natl Acad. Sci. USA 101(13), 4572-4577 (2004).
15. Bettelli E, Carrier Y, Gao W et al. Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature 441(7090), 235-238 (2006).
16. + regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6(4), 345-352 (2005).
17. Schwele S, Fischer AM, Brestrich G et al. Cytomegalovirus-specific regulatory and effector T cells share TCR clonality-possible relation to repetitive CMV infections. Am. J. Transplant. 12(3), 669-681 (2012).
18. Long SA, Buckner JH. CD4+FOXP3+ T regulatory cells in human autoimmunity: more than a numbers game. J. Immunol. 187(5), 2061-2066 (2011).
19. Sharma R, Ju ST. Genetic control of the inflammatory T-cell response in regulatory T-cell deficient scurfy mice. Clin. Immunol. 136(2), 162-169 (2010).
20. Ziegler SF. FOXP3: of mice and men. Annu. Rev. Immunol. 24, 209-226 (2006).
21. Unutmaz D. RORC2: the master of human Th17 cell programming. Eur. J. Immunol. 39(6), 1452-1455 (2009).
22. Harrington LE, Mangan PR, Weaver CT. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr. Opin. Immunol. 18(3), 349-356 (2006).
23. Happel KI, Dubin PJ, Zheng M et al. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202(6), 761-769 (2005).
24. Huang W, Na L, Fidel PL, Schwarzenberger P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190(3), 624-631 (2004).
25. Puel A, Cypowyj S, Bustamante J et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332(6025), 65-68 (2011).
26. + regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity 34(3), 422-434 (2011).
27. Kryczek I, Banerjee M, Cheng P et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 114(6), 1141-1149 (2009).
28. Sfanos KS, Bruno TC, Maris CH et al. Phenotypic analysis of prostate-infiltrating lymphocytes reveals Th17 and Treg skewing. Clin. Cancer Res. 14(11), 3254-3261 (2008).
29. Chen JG, Xia JC, Liang XT et al. Intratumoral expression of IL-17 and its prognostic role in gastric adenocarcinoma patients. Int. J. Biol. Sci. 7(1), 53-60 (2011).
30. + T cells in malignant pleural effusion. J. Immunol. 185(10), 6348-6354 (2010).
31. Wu S, Rhee KJ, Albesiano E et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat. Med. 15(9), 1016-1022 (2009).
32. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 cells. Annu. Rev. Immunol. 27, 485-517 (2009).
33. Ichiyama K, Yoshida H, Wakabayashi Y et al. FOXP3 inhibits RORgammat-mediated IL-17A mRNA transcription through direct interaction with RORgammat. J. Biol. Chem. 283(25), 17003-17008 (2008).
34. Zhou L, Lopes JE, Chong MM et al. TGF-beta-induced FOXP3 inhibits Th17 cell differentiation by antagonizing RORgammat function. Nature 453(7192), 236-240 (2008).
35. Sun CM, Hall JA, Blank RB et al. Small intestine lamina propria dendritic cells promote de novo generation of FOXP3 T reg cells via retinoic acid. J. Exp. Med. 204(8), 1775-1785 (2007).
36. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24(2), 179-189 (2006).
37. + lymphocyte targets. Retrovirology 7, 97 (2010).
38. +) IFN-gamma production during acute and chronic FIV infection utilizing a membrane TGF-beta-dependent mechanism. AIDS Res. Hum. Retroviruses 26(2), 201-216 (2010).
39. + T cells and reduces chronic retroviral set points. Proc. Natl Acad. Sci. USA 108(6), 2420-2425 (2011).
40. Jin Y-H, Kang HS, Mohindru M, Kim BS. Preferential induction of protective T cell responses to Theiler's virus in resistant (C57BL/6 x SJL)F1 mice. J. Virol. 85(6), 3033-3040 (2011).
41. Kriegs M, Burckstummer T, Himmelsbach K et al. The hepatitis C virus non-structural NS5A protein impairs both the innate and adaptive hepatic immune response in vivo. J. Biol. Chem. 284(41), 28343-28351 (2009).
42. Kijak GH, Walsh AM, Koehler RN et al. HLA class I allele and haplotype diversity in Ugandans supports the presence of a major east African genetic cluster. Tissue Antigens 73(3), 262-269 (2009).
43. Mccormick S, Shaler CR, Small CL et al. Control of pathogenic CD4 T cells and lethal immunopathology by signaling immunoadaptor DAP12 during influenza infection. J. Immunol. 187(8), 4280-4292 (2011).
44. + T cells. PLoS One 6(9), e24772 (2011).
45. + CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J. Immunol. 185(4), 2382-2392 (2010).
46. Lanteri MC, O'Brien KM, Purtha WE et al. Tregs control the development of symptomatic West Nile virus infection in humans and mice. J. Clin. Invest. 119(11), 3266-3277 (2009). Tregs prevent immunopathology, which causes the clinical signs in West Nile virus infection.
47. Lund JM, Hsing L, Pham TT, Rudensky AY. Coordination of early protective immunity to viral infection by regulatory T cells. Science 320(5880), 1220-1224 (2008). Tregs modulate the immune response and increase its effectiveness in a viral infection.
48. Zelinskyy G, Dietze KK, Husecken YP et al. The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood 114(15), 3199-3207 (2009). First publication to demonstrate Treg ablation decreased viral load and did not increase immunopathology.
49. Zelinskyy G, Dietze K, Sparwasser T, Dittmer U. Regulatory T cells suppress antiviral immune responses and increase viral loads during acute infection with a lymphotropic retrovirus. PLoS Pathog. 5(8), e1000406 (2009).
50. + T cell dysfunction and chronic retrovirus loads. J. Immunol. 183(3), 1636-1643 (2009).
51. + T cells evade Treg cell suppression. Nat. Med. 17(8), 989-995 (2011).
52. Kanwar B, Favre D, McCune JM. Th17 and regulatory T cells: implications for AIDS pathogenesis. Curr. Opin. HIV AIDs 5(2), 151-157 (2010).
53. Brandt L, Benfield T, Mens H et al. Low level of regulatory T cells and maintenance of balance between regulatory T cells and Th17 cells in HIV-1-infected elite controllers. J. Acquir. Immune Defific. Syndr. 57(2), 101-108 (2011).
54. He Y, Li J, Zheng Y et al. A randomized case-control study of dynamic changes in peripheral blood Th17/Treg cell balance and interleukin-17 levels in highly active antiretroviral-treated HIV type 1/AIDS patients. AIDS Res. Hum. Retroviruses 28(4), 339-345 (2012).
55. Salagianni M, Lekka E, Moustaki A et al. NK cell adoptive transfer combined with Ontak-mediated regulatory T cell elimination induces effective adaptive antitumor immune responses. J. Immunol. 186(6), 3327-3335 (2011).
56. Yang W, Ding X, Deng J et al. Interferon-gamma negatively regulates Th17-mediated immunopathology during mouse hepatitis virus infection. J. Mol. Med. 89(4), 399-409 (2011).
57. Chang Q, Wang YK, Zhao Q, Wang CZ, Hu YZ, Wu BY. Th17 cells are increased with severity of liver inflammation in patients with chronic hepatitis C. J. Gastroenterol. Hepatol. 27(2), 273-278 (2012).
58. Ryzhakov G, Lai CC, Blazek K, To KW, Hussell T, Udalova I. IL-17 boosts proinflammatory outcome of antiviral response in human cells. J. Immunol. 187(10), 5357-5362 (2011).
59. Suryawanshi A, Veiga-Parga T, Rajasagi NK et al. Role of IL-17 and Th17 cells in herpes simplex virus-induced corneal immunopathology. J. Immunol. 187(4), 1919-1930 (2011).
60. Abbas AK, Lichtman AH, Pillai S. Cellular and Molecular Immunology (7th Edition). Elsevier/Saunders, PA, USA (2012).
61. + T cells are detectable in early human immunodeficiency virus type 1 infection. J. Virol. 82(13), 6767-6771 (2008).
62. Brenchley JM, Paiardini M, Knox KS et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112(7), 2826-2835 (2008).
63. El Hed A, Khaitan A, Kozhaya L et al. Susceptibility of human Th17 cells to human immunodeficiency virus and their perturbation during infection. J. Infect. Dis. 201(6), 843-854 (2010).
64. Favre D, Lederer S, Kanwar B et al. Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog. 5(2), e1000295 (2009).
65. + T cells with protection against rotavirus shedding in mice intranasally immunized with VP6 and the adjuvant LT(R192G). J. Virol. 81(8), 3740-3748 (2007).
66. + T cells.
67. Kosiewicz MM, Zirnheld AL, Alard P. Gut microbiota, immunity, and disease: a complex relationship. Front. Microbiol. 2, 180 (2011).
68. + regulatory T cell population during remission but not during relapse. J. Neuroimmunol. 240-241, 97-103 (2011).
69. Murray TJ. The history of multiple sclerosis: the changing frame of the disease over the centuries. J. Neuro. Sci. 277(Suppl. 1), S3-S8 (2009).
70. Pohl D. Epstein-Barr virus and multiple sclerosis. J. Neurol. Sci. 286(1-2), 62-64 (2009).
71. Tselis A. Evidence for viral etiology of multiple sclerosis. Semin. Neurol. 31(3), 307-316 (2011).
72. Lipton HL, Liang Z, Hertzler S, Son KN. A specific viral cause of multiple sclerosis: one virus, one disease. Ann. Neurol. 61(6), 514-523 (2007).
73. Saadatnia M, Najafi MR, Najafi F, Davoudi V, Keyhanian K, Maghzi AH. CD24 gene allele variation is not associated with oligoclonal IgG bands and IgG index of multiple sclerosis patients. Neuroimmunomodulation 19(3), 195-199 (2012).
74. Axthelm MK, Bourdette DN, Marracci GH et al. Japanese macaque encephalomyelitis: a spontaneous multiple sclerosis-like disease in a nonhuman primate. Ann. Neurol. 70(3), 362-373 (2011). Monkeys with a naturally occurring multiple sclerosis-like disease were found to be infected with a gammaherpes virus.
75. Martinez NE, Sato F, Omura S, Minigar A, Alexander JS, Tsunoda I. Immunopathological patterns from EAE and Theiler's virus infection: is multiple sclerosis a homogenous 1-stage or heterogenous 2-stage disease? Pathophysiology (2012) (In press).
76. Trandem K, Anghelina D, Zhao J, Perlman S. Regulatory T cells inhibit T cell proliferation and decrease demyelination in mice chronically infected with a coronavirus. J. Immunol. 184(8), 4391-4400 (2010).
77. Anghelina D, Zhao J, Trandem K, Perlman S. Role of regulatory T cells in coronavirus-induced acute encephalitis. Virology 385(2), 358-367 (2009).
78. Richards MH, Getts MT, Podojil JR, Jin YH, Kim BS, Miller SD. Virus expanded regulatory T cells control disease severity in the Theiler's virus mouse model of MS. J. Autoimmun. 36(2), 142-154 (2011).
79. Hou W, Kang HS, Kim BS. Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection. J. Exp. Med. 206(2), 313-328 (2009). Th17 immune responses inhibit Th1 immune responses and facilitate a chronic viral infection.
80. + T cells lacking T-bet and eomesodermin. Science 321(5887), 408-411 (2008). Mice lacking Th1 immune responses mounted Th17-like immune responses against a viral infection.
81. Lindsley MD, Thiemann R, Rodriguez M. Cytotoxic T cells isolated from the central nervous systems of mice infected with Theiler's virus. J. Virol. 65(12), 6612-6620 (1991).
82. Venken K, Hellings N, Liblau R, Stinissen P. Disturbed regulatory T cell homeostasis in multiple sclerosis. Trends Mol. Med. 16(2), 58-68 (2010).
83. Huan J, Culbertson N, Spencer L et al. Decreased FOXP3 levels in multiple sclerosis patients. J. Neurosci. Res. 81(1), 45-52 (2005).
84. + regulatory T cells in patients with multiple sclerosis. J. Exp. Med. 199(7), 971-979 (2004).
85. Bendig JW, O'Brien PS, Muir P, Porter HJ, Caul EO. Enterovirus sequences resembling coxsackievirus A2 detected in stool and spleen from a girl with fatal myocarditis. J. Med. Virol. 64(4), 482-486 (2001).
86. Ward C. Severe arrhythmias in coxsackievirus B3 myopericarditis. Arch. Dis. Child. 53(2), 174-176 (1978).
87. Whitton JL, Feuer R. Myocarditis, microbes and autoimmunity. Autoimmunity 37(5), 375-386 (2004).
88. Dennert R, Crijns HJ, Heymans S. Acute viral myocarditis. Eur. Heart J. 29(17), 2073-2082 (2008).
89. Cooper LT Jr. Myocarditis. N. Engl. J. Med. 360(15), 1526-1538 (2009).
90. Huber SA, Gauntt CJ, Sakkinen P. Enteroviruses and myocarditis: viral pathogenesis through replication, cytokine induction, and immunopathogenicity. Adv. Viral Res. 51, 35-80 (1998).
91. Yajima T, Knowlton KU. Viral myocarditis: from the perspective of the virus. Circulation 119(19), 2615-2624 (2009).
92. Taylor LA, Carthy CM, Yang D et al. Host gene regulation during coxsackievirus B3 infection in mice: assessment by microarrays. Circulation Res. 87(4), 328-334 (2000).
93. + Th1 cells. J. Virol. 76(21), 10785-10790 (2002).
94. + T helper cell and IL-2 independent in BALB/c mice. Am. J. Pathol. 127(2), 335-341 (1987).
95. Yue Y, Gui J, Ai W, Xu W, Xiong S. Direct gene transfer with IP-10 mutant ameliorates mouse CVB3-induced myocarditis by blunting Th1 immune responses. PLoS One 6(3), e18186 (2011).
96. Fairweather D, Frisancho-Kiss S, Yusung SA et al. IL-12 protects against coxsackievirus B3-induced myocarditis by increasing IFN-gamma and macrophage and neutrophil populations in the heart. J. Immunol. 174(1), 261-269 (2005).
97. Mason JW, O'Connell JB, Herskowitz A et al. A clinical trial of immunosuppressive therapy for myocarditis. The Myocarditis Treatment Trial Investigators. N. Engl. J. Med. 333(5), 269-275 (1995).
98. Liu PP, Mason JW. Advances in the understanding of myocarditis. Circulation 104(9), 1076-1082 (2001).
99. Rangachari M, Mauermann N, Marty RR et al. T-bet negatively regulates autoimmune myocarditis by suppressing local production of interleukin 17. J. Exp. Med. 203(8), 2009-2019 (2006).
100. Chang H, Hanawa H, Yoshida T et al. Alteration of IL-17 related protein expressions in experimental autoimmune myocarditis and inhibition of IL-17 by IL-10-Ig fusion gene transfer. Circ. J. 72(5), 813-819 (2008).
101. Yuan J, Cao AL, Yu M et al. Th17 cells facilitate the humoral immune response in patients with acute viral myocarditis. J. Clin. Immunol. 30(2), 226-234 (2010).
102. Yuan J, Yu M, Lin QW et al. Th17 cells contribute to viral replication in coxsackievirus B3-induced acute viral myocarditis. J. Immunol. 185(7), 4004-4010 (2010).
103. Fan Y, Weifeng W, Yuluan Y, Qing K, Yu P, Yanlan H. Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of coxsackievirus B3-induced viral myocarditis reduces myocardium inflammation. Virol. J. 8, 17 (2011).
104. Xie Y, Chen R, Zhang X et al. The role of Th17 cells and regulatory T cells in coxsackievirus B3-induced myocarditis. Virology 421(1), 78-84 (2011).
105. Mena I, Perry CM, Harkins S, Rodriguez F, Gebhard J, Whitton JL. The role of B lymphocytes in coxsackievirus B3 infection. Am. J. Pathol. 155(4), 1205-1215 (1999).
106. Schwimmbeck PL, Bigalke B, Schulze K, Pauschinger M, Kuhl U, Schultheiss HP. The humoral immune response in viral heart disease: characterization and pathophysiological significance of antibodies. Med. Microbiol. Immunol. 193(2-3), 115-119 (2004).
107. Rose NR. Autoimmunity in coxsackievirus infection. Curr. Top. Microbiol. Immunol. 323, 293-314 (2008).
108. Rose NR, Hill SL. The pathogenesis of postinfectious myocarditis. Clin. Immunol. Immunopathol. 80(3 Pt 2), S92-S99 (1996).
109. Rose NR, Hill SL. Autoimmune myocarditis. Int. J. Cardiol. 54(2), 171-175 (1996).
110. Liao YH. Functional analysis of autoantibodies against ADP/ATP carrier from dilated cardiomyopathy. Int. J. Cardiol. 54(2), 165-169 (1996).
111. Hsu HC, Yang P, Wang J et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. 9(2), 166-175 (2008).
112. Doreau A, Belot A, Bastid J et al. Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nat. Immunol. 10(7), 778-785 (2009).
113. Yuan J, Yu M, Lin QW et al. Neutralization of IL-17 inhibits the production of anti-ANT autoantibodies in CVB3-induced acute viral myocarditis. Int. Immunopharmacol. 10(3), 272-276 (2010).
114. - regulatory T cells. J. Immunol. 176(8), 4748-4756 (2006).
115. + T lymphocyte by adenovirus-mediated gene transfer of CTLA4Ig fusion protein in experimental autoimmune myocarditis. Autoimmunity 39(4), 289-298 (2006).
116. Wang S, Liu J, Wang M, Zhang J, Wang Z. Treatment and prevention of experimental autoimmune myocarditis with CD28 superagonists. Cardiology 115(2), 107-113 (2010).
117. Lv K, Xu W, Wang C, Niki T, Hirashima M, Xiong S. Galectin-9 administration ameliorates CVB3 induced myocarditis by promoting the proliferation of regulatory T cells and alternatively activated Th2 cells. Clin. Immunol. 140(1), 92-101 (2011).
118. Shi Y, Fukuoka M, Li G et al. Regulatory T cells protect mice against coxsackievirus-induced myocarditis through the transforming growth factor beta-coxsackie-adenovirus receptor pathway. Circulation 121(24), 2624-2634 (2010).
119. Horwitz MS, Knudsen M, Ilic A, Fine C, Sarvetnick N. Transforming growth factor-beta inhibits coxsackievirus-mediated autoimmune myocarditis. Viral Immunol. 19(4), 722-733 (2006).
120. Begum-Haque S, Sharma A, Kasper IR et al. Downregulation of IL-17 and IL-6 in the central nervous system by glatiramer acetate in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 204(1-2), 58-65 (2008).
121. + T-cells in patients with multiple sclerosis. J. Neuroimmunol. 216(1-2), 113-117 (2009).
122. + regulatory T cells, which suppress induction of contact hypersensitivity. J. Dermatol. Sci. 39(2), 105-112 (2005).
123. Nakayamada S, Takahashi H, Kanno Y, O'Shea JJ. Helper T cell diversity and plasticity. Curr. Opin. Immunol. doi:10.1016/j.coi.2012.01.014 (2012) (Epub ahead of print).
124. +) T cells reflects promiscuous Foxp3 expression in conventional T cells but not reprogramming of regulatory T cells. Immunity 36(2), 262-275 (2012).
125. + regulatory T cells in the microenvironments of chronic inflammation and cancer. J. Immunol. 186(7), 4388-4395 (2011).