Differential regulation of self-reactive CD4+ T cells in cervical lymph nodes and central nervous system during viral encephalomyelitis

Frontiers in Immunology

Volumn 7, Issue SEP, 2016, Pages

  Savarin, Carine ^a   Bergmann, Cornelia C ^a   Hinton, David R ^b   Stohlman, Stephen A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Autoimmunity; CD4+ T cells; Central nervous system; Foxp3+ regulatory T cells; Tr1 cells; Viral infection

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; TRANSCRIPTION FACTOR FOXP3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM; CERVICAL LYMPH NODE; DEMYELINATION; ENCEPHALOMYELITIS; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; HISTOPATHOLOGY; MOUSE; MULTIPLE SCLEROSIS; MURINE HEPATITIS VIRUS; NONHUMAN; REVERSE TRANSCRIPTION;

EID: 84992034216     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00370     Document Type: Article

References (52)

1. Virtanen JO, Jacobson S. Viruses and multiple sclerosis. CNS Neurol Disord Drug Targets (2012) 11(5):528-44. doi: 10.2174/187152712801661220
2. Getts DR, Chastain EM, Terry RL, Miller SD. Virus infection, antiviral immunity, and autoimmunity. Immunol Rev (2013) 255(1):197-209. doi:10.1111/imr.12091
3. Vartdal F, Vandvik B, Norrby E. Viral and bacterial antibody responses in multiple sclerosis. Ann Neurol (1980) 8(3):248-55. doi:10.1002/ana.410080305
4. Murray RS, Brown B, Brian D, Cabirac GF. Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann Neurol (1992) 31(5):525-33. doi:10.1002/ana.410310511
5. Serafini B, Rosicarelli B, Franciotta D, Magliozzi R, Reynolds R, Cinque P, et al. Dysregulated Epstein-Barr virus infection in the multiple sclerosis brain. J Exp Med (2007) 204(12):2899-912. doi:10.1084/jem.20071030
6. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med (2002) 347(12):911-20. doi:10.1056/NEJMra020100
7. Okada H, Kuhn C, Feillet H, Bach JF. The 'hygiene hypothesis' for autoimmune and allergic diseases: an update. Clin Exp Immunol (2010) 160(1):1-9. doi:10.1111/j.1365-2249.2010.04139.x
8. Kivity S, Agmon-Levin N, Blank M, Shoenfeld Y. Infections and autoimmunity-friends or foes? Trends Immunol (2009) 30(8):409-14. doi:10.1016/j.it.2009.05.005
9. Miller SD, Vanderlugt CL, Begolka WS, Pao W, Yauch RL, Neville KL, et al. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat Med (1997) 3(10):1133-6. doi:10.1038/nm1097-1133
10. Oleszak EL, Chang JR, Friedman H, Katsetos CD, Platsoucas CD. Theiler's virus infection: a model for multiple sclerosis. Clin Microbiol Rev (2004) 17(1):174-207. doi:10.1128/CMR.17.1.174-207.2004
11. Stohlman SA, Hinton DR. Viral induced demyelination. Brain Pathol (2001) 11(1):92-106. doi:10.1111/j.1750-3639.2001.tb00384.x
12. Bergmann CC, Lane TE, Stohlman SA. Coronavirus infection of the central nervous system: host-virus stand-off. Nat Rev Microbiol (2006) 4(2):121-32. doi:10.1038/nrmicro1343
13. Savarin C, Bergmann CC, Gaignage M, Stohlman SA. Self-reactive CD4(+) T cells activated during viral-induced demyelination do not prevent clinical recovery. J Neuroinflammation (2015) 12:207. doi:10.1186/s12974-015-0426-1
14. Puntambekar SS, Bergmann CC, Savarin C, Karp CL, Phares TW, Parra GI, et al. Shifting hierarchies of interleukin-10-producing T cell populations in the central nervous system during acute and persistent viral encephalomyelitis. J Virol (2011) 85(13):6702-13. doi:10.1128/JVI.00200-11
15. de Aquino MT, Kapil P, Hinton DR, Phares TW, Puntambekar SS, Savarin C, et al. IL-27 limits central nervous system viral clearance by promoting IL-10 and enhances demyelination. J Immunol (2014) 193(1):285-94. doi:10.4049/jimmunol.1400058
16. Long SA, Buckner JH. CD4+FOXP3+ T regulatory cells in human autoimmunity: more than a numbers game. J Immunol (2011) 187(5):2061-6. doi:10.4049/jimmunol.1003224
17. Bayry J. Repressing immunity in autoimmune disease. N Engl J Med (2016) 374(21):2090-2. doi:10.1056/NEJMcibr1602864
18. Anghelina D, Zhao J, Trandem K, Perlman S. Role of regulatory T cells in coronavirus-induced acute encephalitis. Virology (2009) 385(2):358-67. doi:10.1016/j.virol.2008.12.014
19. de Aquino MT, Puntambekar SS, Savarin C, Bergmann CC, Phares TW, Hinton DR, et al. Role of CD25(+) CD4(+) T cells in acute and persistent coronavirus infection of the central nervous system. Virology (2013) 447(1-2):112-20. doi:10.1016/j.virol.2013.08.030
20. 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 (2010) 184(8):4391-400. doi:10.4049/jimmunol.0903918
21. Cervantes-Barragan L, Firner S, Bechmann I, Waisman A, Lahl K, Sparwasser T, et al. Regulatory T cells selectively preserve immune privilege of self-antigens during viral central nervous system infection. J Immunol (2012) 188(8):3678-85. doi:10.4049/jimmunol.1102422
22. Lahl K, Loddenkemper C, Drouin C, Freyer J, Arnason J, Eberl G, et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med (2007) 204(1):57-63. doi:10.1084/jem.20061852
23. Mayer CT, Ghorbani P, Kuhl AA, Stuve P, Hegemann M, Berod L, et al. Few Foxp3(+) regulatory T cells are sufficient to protect adult mice from lethal autoimmunity. Eur J Immunol (2014) 44(10):2990-3002. doi:10.1002/eji.201344315
24. Mayer CT, Lahl K, Milanez-Almeida P, Watts D, Dittmer U, Fyhrquist N, et al. Advantages of Foxp3(+) regulatory T cell depletion using DEREG mice. Immun Inflamm Dis (2014) 2(3):162-5. doi:10.1002/iid3.33
25. Fleming JO, Trousdale MD, el-Zaatari FA, Stohlman SA, Weiner LP. Pathogenicity of antigenic variants of murine coronavirus JHM selected with monoclonal antibodies. J Virol (1986) 58(3):869-75.
26. Savarin C, Stohlman SA, Atkinson R, Ransohoff RM, Bergmann CC. Monocytes regulate T cell migration through the glia limitans during acute viral encephalitis. J Virol (2010) 84(10):4878-88. doi:10.1128/JVI.00051-10
27. Bergmann CC, Altman JD, Hinton D, Stohlman SA. Inverted immunodominance and impaired cytolytic function of CD8+ T cells during viral persistence in the central nervous system. J Immunol (1999) 163(6):3379-87.
28. Lahl K, Sparwasser T. In vivo depletion of FoxP3+ Tregs using the DEREG mouse model. Methods Mol Biol (2011) 707:157-72. doi:10.1007/978-1-61737-979-6_10
29. Zhao J, Zhao J, Perlman S. Virus-specific regulatory T cells ameliorate encephalitis by repressing effector T cell functions from priming to effector stages. PLoS Pathog (2014) 10(8):e1004279. doi:10.1371/journal.ppat.1004279
30. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, et al. Structural and functional features of central nervous system lymphatic vessels. Nature (2015) 523(7560):337-41. doi:10.1038/nature14432
31. Parra B, Hinton DR, Marten NW, Bergmann CC, Lin MT, Yang CS, et al. IFN-gamma is required for viral clearance from central nervous system oligodendroglia. J Immunol (1999) 162(3):1641-7.
32. Savarin C, Bergmann CC, Hinton DR, Ransohoff RM, Stohlman SA. Memory CD4+ T-cell-mediated protection from lethal coronavirus encephalomyelitis. J Virol (2008) 82(24):12432-40. doi:10.1128/JVI.01267-08
33. Chen BP, Kuziel WA, Lane TE. Lack of CCR2 results in increased mortality and impaired leukocyte activation and trafficking following infection of the central nervous system with a neurotropic coronavirus. J Immunol (2001) 167(8):4585-92. doi:10.4049/jimmunol.167.8.4585
34. Glass WG, Lane TE. Functional expression of chemokine receptor CCR5 on CD4(+) T cells during virus-induced central nervous system disease. J Virol (2003) 77(1):191-8. doi:10.1128/JVI.77.1.191-198.2003
35. Stiles LN, Hosking MP, Edwards RA, Strieter RM, Lane TE. Differential roles for CXCR3 in CD4+ and CD8+ T cell trafficking following viral infection of the CNS. Eur J Immunol (2006) 36(3):613-22. doi:10.1002/eji.200535509
36. Lund JM, Hsing L, Pham TT, Rudensky AY. Coordination of early protective immunity to viral infection by regulatory T cells. Science (2008) 320(5880):1220-4. doi:10.1126/science.1155209
37. Luster AD, Unkeless JC, Ravetch JV. Gamma-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins. Nature (1985) 315(6021):672-6. doi:10.1038/315672a0
38. Carter SL, Muller M, Manders PM, Campbell IL. Induction of the genes for Cxcl9 and Cxcl10 is dependent on IFN-gamma but shows differential cellular expression in experimental autoimmune encephalomyelitis and by astrocytes and microglia in vitro. Glia (2007) 55(16):1728-39. doi:10.1002/glia.20587
39. Groom JR, Richmond J, Murooka TT, Sorensen EW, Sung JH, Bankert K, et al. CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity (2012) 37:1091-103. doi:10.1016/j.immuni.2012.8.016
40. Pot C, Apetoh L, Kuchroo VK. Type 1 regulatory T cells (Tr1) in autoimmunity. Semin Immunol (2011) 23(3):202-8. doi:10.1016/j.smim.2011.07.005
41. Kleinewietfeld M, Hafler DA. Regulatory T cells in autoimmune neuroinflammation. Immunol Rev (2014) 259(1):231-44. doi:10.1111/imr.12169
42. Puntambekar SS, Hinton DR, Yin X, Savarin C, Bergmann CC, Trapp BD, et al. Interleukin-10 is a critical regulator of white matter lesion containment following viral induced demyelination. Glia (2015) 63:2106-20. doi:10.1002/glia.22880
43. Estes JD, Li Q, Reynolds MR, Wietgrefe S, Duan L, Schacker T, et al. Premature induction of an immunosuppressive regulatory T cell response during acute simian immunodeficiency virus infection. J Infect Dis (2006) 193(5):703-12. doi:10.1086/500368
44. Ke X, Wang J, Li L, Chen IH, Wang H, Yang XF. Roles of CD4+CD25(high) FOXP3+ Tregs in lymphomas and tumors are complex. Front Biosci (2008) 13:3986-4001. doi:10.2741/2986
45. Alissafi T, Hatzioannou A, Ioannou M, Sparwasser T, Grun JR, Grutzkau A, et al. De novo-induced self-antigen-specific Foxp3+ regulatory T cells impair the accumulation of inflammatory dendritic cells in draining lymph nodes. J Immunol (2015) 194(12):5812-24. doi:10.4049/jimmunol.1500111
46. Phares TW, DiSano KD, Stohlman SA, Bergmann CC. Progression from IgD+ IgM+ to isotype-switched B cells is site specific during coronavirus-induced encephalomyelitis. J Virol (2014) 88(16):8853-67. doi:10.1128/JVI.00861-14
47. Davidson TS, Shevach EM. Polyclonal Treg cells modulate T effector cell trafficking. Eur J Immunol (2011) 41(10):2862-70. doi:10.1002/eji.201141503
48. Korn T, Reddy J, Gao W, Bettelli E, Awasthi A, Petersen TR, et al. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat Med (2007) 13(4):423-31. doi:10.1038/nm1564
49. Parra B, Hinton DR, Lin MT, Cua DJ, Stohlman SA. Kinetics of cytokine mRNA expression in the central nervous system following lethal and nonlethal coronavirus-induced acute encephalomyelitis. Virology (1997) 233(2):260-70. doi:10.1006/viro.1997.8613
50. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature (1997) 389(6652):737-42. doi:10.1038/39614
51. Gagliani N, Jofra T, Stabilini A, Valle A, Atkinson M, Roncarolo MG, et al. Antigen-specific dependence of Tr1-cell therapy in preclinical models of islet transplant. Diabetes (2010) 59(2):433-9. doi:10.2337/db09-1168
52. Zeng H, Zhang R, Jin B, Chen L. Type 1 regulatory T cells: a new mechanism of peripheral immune tolerance. Cell Mol Immunol (2015) 12(5):566-71. doi:10.1038/cmi.2015.44