Pathogenic role for virus-specific CD4 T cells in mice with coronavirus-induced acute encephalitis

American Journal of Pathology

Volumn 169, Issue 1, 2006, Pages 209-222

  Anghelina, Daniela ^a   Pewe, Lecia ^b   Perlman, Stanley ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 5; RNA; TUMOR NECROSIS FACTOR ALPHA; VIRUS ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN DETECTION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM INFECTION; CORONAVIRUS; CYTOTOXIC T LYMPHOCYTE; ENCEPHALITIS; ENZYME LINKED IMMUNOSPOT ASSAY; GENE MUTATION; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; LISTERIA MONOCYTOGENES; MACROPHAGE; MICROGLIA; MOUSE; MURINE HEPATITIS CORONAVIRUS; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; RNA SYNTHESIS; VIRUS ENCEPHALITIS; VIRUS RECOMBINANT;

EID: 33745714786     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.051308     Document Type: Article

References (55)

1. Stohlman SA, Hinton DR: Viral induced demyelination. Brain Pathol 2001, 11:92-106
2. Stohlman SA, Bergmann CC, Perlman S: Mouse Hepatitis Virus. Edited by R Ahmed, I Chen. New York, John Wiley & Sons, Ltd., 1998, pp 537-557
3. Barnett E, Cassell M, Perlman S: Two neurotropic viruses, herpes simplex virus type I and mouse hepatitis virus, spread along different neural pathways from the main olfactory bulb. Neuroscience 1993, 157:1007-1025
4. Barnett E, Perlman S: The olfactory nerve and not the trigeminal nerve is the major site of CNS entry for mouse hepatitis virus, strain JHM. Virology 1993, 194:185-191
5. Perlman S, Evans G, Afifi A: Effect of olfactory bulb ablation on spread of a neurotropic coronavirus into the mouse brain. J Exp Med 1990, 172:1127-1132
6. Williamson JS, Sykes KC, Stohlman SA: Characterization of brain-infiltrating mononuclear cells during infection with mouse hepatitis virus strain JHM. J Neuroimmunol 1991, 32:199-207
7. Haring JS, Pewe LL, Perlman S: High magnitude, virus-specific CD4 T-cell response in the central nervous system of coronavirus-infected mice. J Virol 2001, 75:3043-3047
8. Rempel JD, Murray SJ, Meisner J, Buchmeier MJ: Differential regulation of innate and adaptive immune responses in viral encephalitis. Virology 2004, 318:381-392
9. Weiner LP: Pathogenesis of demyelination induced by a mouse hepatitis virus (JHM virus). Arch Neurol 1973, 28:298-303
10. + T cells. J Virol 1990, 64:4589-4592
11. Pewe L, Haring J, Perlman S: CD4 T-cell-mediated demyelination is increased in the absence of gamma interferon in mice infected with mouse hepatitis virus. J Virol 2002, 76:7329-7333
12. Wu GF, Dandekar AA, Pewe L, Perlman S: CD4 and CD8 T cells have redundant but not identical roles in virus-induced demyelination. J Immunol 2000, 165:2278-2286
13. Wu GF, Perlman S: Macrophage infiltration, but not apoptosis, is correlated with immune-mediated demyelination following murine infection with a neurotropic coronavirus. J Virol 1999, 73:8771-8780
14. Xue S, Perlman S: Antigen specificity of CD4 T cell response in the central nervous system of mice infected with mouse hepatitis virus. Virology 1997, 238:68-78
15. Njenga MK, Pavelko K, Baisch J, Lin X, David C, Leibowitz JL, Rodriguez M: Theiler's virus persistence and demyelination in major histocompatibility complex class II-deficient mice. J Virol 1996, 70:1729-1737
16. Houtman JJ, Fleming JO: Dissociation of demyelination and viral clearance in congenitally immunodeficient mice infected with murine coronavirus JHM. J Neurovirol 1996, 2:101-110
17. Liu T, Chambers TJ: Yellow fever virus encephalitis: properties of the brain-associated T-cell response during virus clearance in normal and gamma interferon-deficient mice and requirement for CD4+ lymphocytes. J Virol 2001, 75:2107-2118
18. Murali-Krishna K, Ravi V, Manjunath R: Protection of adult but not newborn mice against lethal intracerebral challenge with Japanese encephalitis virus by adoptively transferred virus-specific cytotoxic T lymphocytes: requirement for L3T4+ T cells. J Gen Virol 1996, 77:705-714
19. Weidinger G, Henning G, ter Meulen V, Niewiesk S: Inhibition of major histocompatibility complex class II-dependent antigen presentation by neutralization of gamma interferon leads to breakdown of resistance against measles virus-induced encephalitis. J Virol 2001, 75:3059-3065
20. Perlman S, Schelper R, Bolger E, Ries D: Late onset, symptomatic, demyelinating encephalomyelitis in mice infected with MHV-JHM in the presence of maternal antibody. Microb Pathog 1987, 2:185-194
21. Ontiveros E, Kuo L, Masters PS, Perlman S: Inactivation of expression of gene 4 of mouse hepatitis virus strain JHM does not affect virulence in the murine CNS. Virology 2001, 290:230-238
22. Kuo L, Godeke GJ, Raamsman MJ, Masters PS, Rottier PJ: Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. J Virol 2000, 74:1393-1406
23. Geginat G, Schenk S, Skoberne M, Goebel W, Hof H: A novel approach of direct ex vivo epitope mapping identifies dominant and subdominant CD4 and CD8 T cell epitopes from Listeria monocytogenes. J Immunol 2001, 166:1877-1884
24. Pewe L, Wu G, Barnett EM, Castro R, Perlman S: Cytotoxic T cell-resistant variants are selected in a virus-induced demyelinating disease. Immunity 1996, 5:253-262
25. Krueger DK, Kelly SM, Lewicki DN, Ruffolo R, Gallagher TM: Variations in disparate regions of the murine coronavirus spike protein impact the initiation of membrane fusion. J Virol 2001, 75:2792-2802
26. Pewe L, Heard SB, Bergmann CC, Dailey MO, Perlman S: Selection of CTL escape mutants in mice infected with a neurotropic coronavirus: quantitative estimate of TCR diversity in the infected CNS. J. Immunol 1999, 163:6106-6113
27. Castro RF, Perlman S: CD8+ T cell epitopes within the surface glycoprotein of a neurotropic coronavirus and correlation with pathogenicity. J Virol 1995, 69:8127-8131
28. Varga SM, Wissinger EL, Braciale TJ: The attachment (G) glycoprotein of respiratory syncytial virus contains a single immunodominant epitope that elicits both Th1 and Th2 CD4+ T cell responses. J Immunol 2000, 165:6487-6495
29. Pewe L, Zhou H, Netland J, Tangadu C, Olivares H, Shi L, Look D, Gallagher TM, Perlman S: A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. J Virol 2005, 79:11335-11342
30. Masters PS: Reverse genetics of the largest RNA viruses. Adv Virus Res 1999, 53:245-264
31. Yount B, Denison MR, Weiss SR, Baric RS: Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J Virol 2002, 76:11065-11078
32. b binding, self-nonself discrimination, and TCR antagonism. J Immunol 1994, 152:4526-4536
33. Vennema H, Godeke G-J, Rossen JWA, Voorhout WF, Horzinek MC, Opstelten D-JE, Rottier PJM: Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J 1996, 15:2020-2028
34. Ontiveros E, Kim TS, Gallagher TM, Perlman S: Enhanced virulence mediated by the murine coronavirus, mouse hepatitis virus strain JHM, is associated with a glycine at residue 310 of the spike glycoprotein. J Virol 2003, 77:10260-10269
35. Lane TE, Liu MT, Chen BP, Asensio VC, Samawi RM, Paoletti AD, Campbell IL, Kunkel SL, Fox HS, Buchmeier MJ: A central role for CD4+ T-cells and RANTES in virus-induced central nervous system inflammation and demyelination. J Virol 2000, 74:1415-1424
36. Tran EH, Prince EN, Owens T: IFN-gamma shapes immune invasion of the central nervous system via regulation of chemokines. J Immunol 2000, 164:2759-2768
37. Van der Veen RC: Immunogenicity of JHM virus proteins: characterization of a CD4+ T cell epitope on nucleocapsid protein which induces different T-helper cell subsets. Virology 1996, 225:339-346
38. + cytotoxic T cells is defined by peptide length. Immunology 1995, 85:517-522
39. Stohlman SA, Bergmann CC, Lin MT, Cua DJ, Hinton DR: CTL effector function within the central nervous system requires CD4+ T cells. J Immunol 1998, 160:2896-2904
40. b-restricted CTL response. J Gen Virol 1996, 77:315-325
41. Yamaguchi K, Goto N, Kyuwa S, Hayami M, Toyoda Y: Protection of mice from a lethal coronavirus infection in the central nervous system by adoptive transfer of virus-specific T cell clones. J Neuroimmunol 1991, 32:1-9
42. Badovinac VP, Porter BB, Harty JT: CD8+ T cell contraction is controlled by early inflammation. Nat Immunol 2004, 5:809-817
43. Corbin GA, Harty JT: T cells undergo rapid ON/OFF but not ON/OFF/ON cycling of cytokine production in response to antigen. J Immunol 2005, 174:718-726
44. Dinarello CA: Cytokines as mediators in the pathogenesis of septic shock, Curr Top Microbiol Immunol 1996, 216:133-165
45. Beutler B, Cerami A: The biology of cachectin/TNF-a primary mediator of the host response. Annu Rev Immunol 1989, 7:625-655
46. Haring JS, Pewe LL, Perlman S: Bystander CD8 T cell-mediated demyelination after viral infection of the central nervous system. J Immunol 2002, 169:1550-1555
47. Palma JP, Yauch RL, Kang HK, Lee HG, Kim BS: Preferential induction of IL-10 in APC correlates with a switch from Th1 to Th2 response following infection with a low pathogenic variant of Theiler's virus. J Immunol 2002, 168:4221-4230
48. Varga SM, Wang X, Welsh RM, Braciale TJ: Immunopathology in RSV infection is mediated by a discrete oligoclonal subset of antigen-specific CD4(+) T cells. Immunity 2001, 15:637-646
49. Recher M, Lang KS, Hunziker L, Freigang S, Eschli B, Harris NL, Navarini A, Senn BM, Fink K, Lotscher M, Hangartner L, Zellweger R, Hersberger M, Theocharides A, Hengartner H, Zinkernagel RM: Deliberate removal of T cell help improves virus-neutralizing antibody production. Nat Immunol 2004, 5:934-942.
50. Rutigliano JA, Graham BS: Prolonged production of TNF-alpha exacerbates illness during respiratory syncytial virus infection. J Immunol 2004, 173:3408-3417
51. Hehlgans T, Pfeffer K: The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: players, rules and the games. Immunology 2005, 115:1-20
52. Balosso S, Ravizza T, Perego C, Peschon J, Campbell IL, De Simoni MG, Vezzani A: Tumor necrosis factor-alpha inhibits seizures in mice via p75 receptors. Ann Neurol 2005, 57:804-812
53. Conti B, Tabarean I, Andrei C, Bartfai T: Cytokines and fever. Front Biosci 2004, 9:1433-1449
54. Marchetti L, Klein M, Schlett K, Pfizenmaier K, Eisel UL: Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-D-aspartate receptor activation: essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J Biol Chem 2004, 279:32869-32881
55. Kaul M, Garden GA, Lipton SA: Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 2001, 410:988-994