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PMID: 20208000 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Regulatory T cells inhibit T cell proliferation and decrease demyelination in mice chronically infected with a coronavirus.

Journal of immunology (Baltimore, Md. : 1950) ·Vol. 184 ·No. 8 ·2010-04-15 ·Pages 4391-400

Trandem K, Anghelina D, Zhao J, Perlman S

Abstract

Mice infected with the neurotropic JHM strain of mouse hepatitis virus (JHMV) develop acute and chronic demyelinating diseases with histopathological similarities to multiple sclerosis. The process of demyelination is largely immune-mediated, as immunodeficient mice (RAG1(-/-) mice) do not develop demyelination upon infection; however, demyelination develops if these mice are reconstituted with either JHMV-immune CD4 or CD8 T cells. Because myelin destruction is a consequence of the inflammatory response associated with virus clearance, we reasoned that decreasing the amount of inflammation would diminish clinical disease and demyelination. Given that regulatory T cells (Tregs) have potent anti-inflammatory effects, we adoptively transferred Tregs into infected C57BL/6 and RAG1(-/-) mice. In both instances, transfer of Tregs decreased weight loss, clinical scores, and demyelination. Transferred Tregs were not detected in the CNS of infected RAG1(-/-) mice, but rather appeared to mediate their effects in the draining cervical lymph nodes. We show that Tregs dampen the inflammatory response mediated by transferred JHMV-immune splenocytes in infected RAG1(-/-) mice by decreasing T cell proliferation, dendritic cell activation, and proinflammatory cytokine/chemokine production, without inducing apoptosis. By extension, decreasing inflammation, whether by Treg transfer or by otherwise enhancing the anti-inflammatory milieu, could contribute to improved clinical outcomes in patients with virus-induced demyelination.

MeSH Terms
Adoptive Transfer Animals Cell Proliferation Chronic Disease Coronavirus Infections/immunology,physiopathology,therapy Encephalomyelitis, Autoimmune, Experimental/immunology,physiopathology,therapy HeLa Cells Humans Immune Tolerance Inflammation Mediators/antagonists & inhibitors,physiology Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Knockout Murine hepatitis virus/immunology,pathogenicity T-Lymphocytes, Regulatory/immunology,pathology,transplantation Viral Load/immunology Virulence/immunology
Chemicals
Inflammation Mediators
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Trandem Kathryn
University of Iowa, Iowa City, IA 52242, USA.
Anghelina Daniela
Zhao Jingxian
Perlman Stanley
References (48)
48 references, click to expand
  1. How regulatory T cells work.
    Nat Rev Immunol. 2008 Jul;8(7):523-32 PMID: 18566595
  2. De novo recruitment of antigen-experienced and naive T cells contributes to the long-term maintenance of antiviral T cell populations in the persistently infected central nervous system.
    J Immunol. 2009 Oct 15;183(8):5163-70 PMID: 19786545
  3. Regulatory T cells promote early influx of CD8+ T cells in the lungs of respiratory syncytial virus-infected mice and diminish immunodominance disparities.
    J Virol. 2009 Apr;83(7):3019-28 PMID: 19153229
  4. Curing CNS autoimmune disease with myelin-reactive Foxp3+ Treg.
    Eur J Immunol. 2009 Apr;39(4):1108-17 PMID: 19350586
  5. Coronaviruses post-SARS: update on replication and pathogenesis.
    Nat Rev Microbiol. 2009 Jun;7(6):439-50 PMID: 19430490
  6. Mechanisms of foxp3+ T regulatory cell-mediated suppression.
    Immunity. 2009 May;30(5):636-45 PMID: 19464986
  7. Selection of CTL escape mutants in mice infected with a neurotropic coronavirus: quantitative estimate of TCR diversity in the infected central nervous system.
    J Immunol. 1999 Dec 1;163(11):6106-13 PMID: 10570300
  8. CD4 and CD8 T cells have redundant but not identical roles in virus-induced demyelination.
    J Immunol. 2000 Aug 15;165(4):2278-86 PMID: 10925317
  9. Viral induced demyelination.
    Brain Pathol. 2001 Jan;11(1):92-106 PMID: 11145206
  10. 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 Oct 15;167(8):4585-92 PMID: 11591787
  11. Cutting edge: CD8 T cell-mediated demyelination is IFN-gamma dependent in mice infected with a neurotropic coronavirus.
    J Immunol. 2002 Feb 15;168(4):1547-51 PMID: 11823480
  12. CD4 T-cell-mediated demyelination is increased in the absence of gamma interferon in mice infected with mouse hepatitis virus.
    J Virol. 2002 Jul;76(14):7329-33 PMID: 12072531
  13. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis.
    J Immunol. 2002 Nov 1;169(9):4712-6 PMID: 12391178
  14. Control of regulatory T cell development by the transcription factor Foxp3.
    Science. 2003 Feb 14;299(5609):1057-61 PMID: 12522256
  15. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells.
    Science. 2003 Feb 14;299(5609):1033-6 PMID: 12532024
  16. Perforin and gamma interferon-mediated control of coronavirus central nervous system infection by CD8 T cells in the absence of CD4 T cells.
    J Virol. 2004 Feb;78(4):1739-50 PMID: 14747539
  17. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis.
    J Exp Med. 2004 Apr 5;199(7):971-9 PMID: 15067033
  18. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes.
    J Exp Med. 2004 Jun 7;199(11):1455-65 PMID: 15184499
  19. Late onset, symptomatic, demyelinating encephalomyelitis in mice infected with MHV-JHM in the presence of maternal antibody.
    Microb Pathog. 1987 Mar;2(3):185-94 PMID: 2853274
  20. Demyelination induced by murine hepatitis virus JHM strain (MHV-4) is immunologically mediated.
    J Neuroimmunol. 1990 Nov;30(1):31-41 PMID: 2172304
  21. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5533-6 PMID: 1648219
  22. Sequential infection of glial cells by the murine hepatitis virus JHM strain (MHV-4) leads to a characteristic distribution of demyelination.
    Lab Invest. 1992 Jun;66(6):744-54 PMID: 1318460
  23. Quantification of cytokine mRNA expression by RT PCR in samples of previously frozen blood.
    J Immunol Methods. 1997 Dec 29;210(2):195-203 PMID: 9520302
  24. Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis.
    J Exp Med. 1998 Nov 16;188(10):1883-94 PMID: 9815266
  25. Depletion of blood-borne macrophages does not reduce demyelination in mice infected with a neurotropic coronavirus.
    J Virol. 1999 Aug;73(8):6327-34 PMID: 10400724
  26. Macrophage infiltration, but not apoptosis, is correlated with immune-mediated demyelination following murine infection with a neurotropic coronavirus.
    J Virol. 1999 Oct;73(10):8771-80 PMID: 10482631
  27. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients.
    J Immunol. 2005 Mar 15;174(6):3143-7 PMID: 15749840
  28. Viral expression of CCL2 is sufficient to induce demyelination in RAG1-/- mice infected with a neurotropic coronavirus.
    J Virol. 2005 Jun;79(11):7113-20 PMID: 15890951
  29. Decreased FOXP3 levels in multiple sclerosis patients.
    J Neurosci Res. 2005 Jul 1;81(1):45-52 PMID: 15952173
  30. Control of homeostatic proliferation by regulatory T cells.
    J Clin Invest. 2005 Dec;115(12):3517-26 PMID: 16294223
  31. Coronavirus infection of the central nervous system: host-virus stand-off.
    Nat Rev Microbiol. 2006 Feb;4(2):121-32 PMID: 16415928
  32. Premature induction of an immunosuppressive regulatory T cell response during acute simian immunodeficiency virus infection.
    J Infect Dis. 2006 Mar 1;193(5):703-12 PMID: 16453267
  33. In vitro suppression of CD8+ T cell function by Friend virus-induced regulatory T cells.
    J Immunol. 2006 Mar 15;176(6):3342-9 PMID: 16517701
  34. Infected site-restricted Foxp3+ natural regulatory T cells are specific for microbial antigens.
    J Exp Med. 2006 Mar 20;203(3):777-88 PMID: 16533885
  35. Pathogenic role for virus-specific CD4 T cells in mice with coronavirus-induced acute encephalitis.
    Am J Pathol. 2006 Jul;169(1):209-22 PMID: 16816374
  36. Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation.
    Immunol Rev. 2006 Aug;212:256-71 PMID: 16903919
  37. From vanilla to 28 flavors: multiple varieties of T regulatory cells.
    Immunity. 2006 Aug;25(2):195-201 PMID: 16920638
  38. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation.
    Nat Med. 2007 Apr;13(4):423-31 PMID: 17384649
  39. The inflamed central nervous system drives the activation and rapid proliferation of Foxp3+ regulatory T cells.
    J Immunol. 2007 Jul 15;179(2):958-66 PMID: 17617587
  40. Pathogenesis of acute and chronic central nervous system infection with variants of mouse hepatitis virus, strain JHM.
    Immunol Res. 2007;39(1-3):160-72 PMID: 17917063
  41. CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells.
    Nat Immunol. 2007 Dec;8(12):1353-62 PMID: 17982458
  42. Natural regulatory T cells and persistent viral infection.
    J Virol. 2008 Jan;82(1):21-30 PMID: 17855537
  43. Maturation and localization of macrophages and microglia during infection with a neurotropic murine coronavirus.
    Brain Pathol. 2008 Jan;18(1):40-51 PMID: 17935605
  44. The Foxp3+ regulatory T cell: a jack of all trades, master of regulation.
    Nat Immunol. 2008 Mar;9(3):239-44 PMID: 18285775
  45. Coordination of early protective immunity to viral infection by regulatory T cells.
    Science. 2008 May 30;320(5880):1220-4 PMID: 18436744
  46. Foxp3+ regulatory T cells: differentiation, specification, subphenotypes.
    Nat Immunol. 2009 Jul;10(7):689-95 PMID: 19536194
  47. Human regulatory T cell suppressive function is independent of apoptosis induction in activated effector T cells.
    PLoS One. 2009;4(9):e7183 PMID: 19779623
  48. Role of regulatory T cells in coronavirus-induced acute encephalitis.
    Virology. 2009 Mar 15;385(2):358-67 PMID: 19141357
Article Info
Journal
Journal of immunology (Baltimore, Md. : 1950)
Abbr.
J Immunol
ISSN
1550-6606
Published
2010-04-15
Epub
2010-00-05
Pages
4391-400
Language
English
Region
United States
NLM ID
2985117R
PMCID
PMC2851486
Subset
IM
Grants
NINDS NIH HHS · R01 NS036592-12 · United States
NINDS NIH HHS · R01 NS036592 · United States
NINDS NIH HHS · NS36592 · United States
NIAID NIH HHS · T32 AI007511 · United States
NIGMS NIH HHS · T32 GM007337 · United States
NIAID NIH HHS · T32 AI007511-14 · United States
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