Neuroimmunology of central nervous system viral infections: the cells, molecules and mechanisms involved

Current Opinion in Pharmacology

Volumn 8, Issue 4, 2008, Pages 472-479

  Savarin, Carine ^a   Bergmann, Cornelia C ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ANTIBODY; BETA INTERFERON; CHEMOKINE; CHEMOKINE RECEPTOR; CYTOKINE; METALLOPROTEINASE; PATTERN RECOGNITION RECEPTOR; VIRUS ANTIGEN;

ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; BRAIN CELL; CELL INFILTRATION; CELL TYPE; CENTRAL NERVOUS SYSTEM INFECTION; CYTOKINE RELEASE; DRUG TARGETING; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOPATHOLOGY; IMMUNOREGULATION; INNATE IMMUNITY; INTERFERON INDUCTION; INTERVENTION STUDY; LYMPHOCYTE FUNCTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR MECHANICS; NEGATIVE FEEDBACK; NEUROIMMUNOLOGY; NONHUMAN; PATTERN RECOGNITION; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BLOCKING; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TISSUE INJURY; VIROGENESIS; VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANIMALS; ANTIVIRAL AGENTS; CENTRAL NERVOUS SYSTEM VIRAL DISEASES; CHEMOKINES; HUMANS; IMMUNITY, CELLULAR; IMMUNOLOGIC FACTORS; INFLAMMATION MEDIATORS; INTERFERONS; RECEPTORS, CHEMOKINE; RECEPTORS, PATTERN RECOGNITION;

EID: 51449097093     PISSN: 14714892     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coph.2008.05.002     Document Type: Review

References (60)

1. Griffin D.E. Immune responses to RNA-virus infections of the CNS. Nat Rev Immunol 3 (2003) 493-502
2. Galea I., Bechmann I., and Perry V.H. What is immune privilege (not)?. Trends Immunol 28 (2007) 12-18
3. Pichlmair A., and Reis e Sousa C. Innate recognition of viruses. Immunity 27 (2007) 370-383
4. Takeuchi O., and Akira S. MDA5/RIG-I and virus recognition. Curr Opin Immunol 20 (2008) 17-22
5. Paul S., Ricour C., Sommereyns C., Sorgeloos F., and Michiels T. Type I interferon response in the central nervous system. Biochimie 89 (2007) 770-778. A review of protective and toxic effects of IFN-α/β responses during CNS diseases, including cell types expressing TLRs, IFNs and ISGs.
6. Samuel M.A., and Diamond M.S. Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J Virol 79 (2005) 13350-13361
7. Ireland D.D., Stohlman S.A., Hinton D.R., Atkinson R., and Bergmann C.C. Type I interferons are essential in controlling neurotropic coronavirus infection irrespective of functional CD8 T cells. J Virol 82 (2008) 300-310. This study demonstrates the importance of IFN-α/β in controlling cell tropism and the inability of functional T cells to compensate for the lack of IFN-α/β mediated viral control.
8. Cervantes-Barragan L., Züst R., Weber F., Spiegel M., Lang K.S., Akira S., Thiel V., and Ludewig B. Control of coronavirus infection through plasmacytoid dendritic-cell-derived type I interferon. Blood 109 (2007) 1131-1137
9. Borden E.C., Sen G.C., Uze G., Silverman R.H., Ransohoff R.M., Foster G.R., and Stark G.R. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov 6 (2007) 975-990. A review on the diversity of cellular components regulating IFN signaling pathways with an emphasis on the potential for drug development to customize TLR activation and IFN responsiveness for clinical purposes.
10. McKimmie C.S., Johnson N., Fooks A.R., and Fazakerley J.K. Viruses selectively upregulate Toll-like receptors in the central nervous system. Biochem Biophys Res Commun 336 (2005) 925-933
11. Prehaud C., Megret F., Lafage M., and Lafon M. Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J Virol 79 (2005) 12893-12904
12. Carpentier P.A., Williams B.R., and Miller S.D. Distinct roles of protein kinase R and Toll-like receptor 3 in the activation of astrocytes by viral stimuli. Glia 55 (2007) 239-252
13. Town T., Jeng D., Alexopoulou L., Tan J., and Flavell R.A. Microglia recognize double-stranded RNA via TLR3. J Immunol 176 (2006) 3804-3812
14. Edelmann K.H., Richardson-Burns S., Alexopoulou L., Tyler K.L., Flavell R.A., and Oldstone M.B. Does Toll-like receptor 3 play a biological role in virus infections?. Virology 322 (2004) 231-238
15. Wang T., Town T., Alexopoulou L., Anderson J.F., Fikrig E., and Flavell R.A. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10 (2004) 1366-1373. This study reveals how exuberant TLR signaling during peripheral infection may enhance CNS inflammation and subsequent virus mediated CNS pathology.
16. Yoshida H., Imaizumi T., Lee S.J., Tanji K., Sakaki H., Matsumiya T., Ishikawa A., Taima K., Yuzawa E., Mori F., et al. Retinoic acid-inducible gene-I mediates RANTES/CCL5 expression in U373MG human astrocytoma cells stimulated with double-stranded RNA. Neurosci Res 58 (2007) 199-206
17. Daffis S., Samuel M.A., Keller B.C., Gale Jr. M., and Diamond M.S. Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-dependent and -independent mechanisms. PLoS Pathog 3 (2007) e106. This paper highlights how constitutive expression of PRRs and ISGs affects viral control in a cell type specific manner.
18. Delhaye S., Paul S., Blakqori G., Minet M., Weber F., Staeheli P., and Michiels T. Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci U S A 103 (2006) 7835-7840
19. Ousman S.S., Wang J., and Campbell I.L. Differential regulation of interferon regulatory factor (IRF)-7 and IRF-9 gene expression in the central nervous system during viral infection. J Virol 79 (2005) 7514-7527
20. Wacher C., Müller M., Hofer M.J., Getts D.R., Zabaras R., Ousman S.S., Terenzi F., Sen G.C., King N.J., and Campbell I.L. Coordinated regulation and widespread cellular expression of interferon-stimulated genes (ISG) ISG-49, ISG-54, and ISG-56 in the central nervous system after infection with distinct viruses. J Virol 81 (2007) 860-871
21. Dafny N., and Yang P.B. Interferon and the central nervous system. Eur J Pharmacol 523 (2005) 1-15
22. Weber F., and Haller O. Viral suppression of the interferon system. Biochimie 89 (2007) 836-842
23. Yang M.S., Min K.J., and Joe E. Multiple mechanisms that prevent excessive brain inflammation. J Neurosci Res 85 (2007) 2298-2305
24. Ashkar A.A., Yao X.D., Gill N., Sajic D., Patrick A.J., and Rosenthal K.L. Toll-like receptor (TLR)-3, but not TLR4, agonist protects against genital herpes infection in the absence of inflammation seen with CpG DNA. J Infect Dis 190 (2004) 1841-1849
25. Bergmann C.C., Lane T.E., and Stohlman S.A. Coronavirus infection of the central nervous system: host-virus stand-off. Nat Rev Microbiol 4 (2006) 121-132. Review demonstrating the interplay of various pro-inflammatory mediators, innate and adaptive immune responses controlling acute and persistent infection in a model of virus induced demyelinating disease.
26. Schindler C., Levy D.E., and Decker T. JAK-STAT signaling: from interferons to cytokines. J Biol Chem 282 (2007) 20059-20063
27. Ishihara K., and Hirano T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 13 (2002) 357-368
28. Agrawal S.M., Lau L., and Yong V.W. MMPs in the central nervous system: where the good guys go bad. Semin Cell Dev Biol 19 (2008) 42-51
29. Zhou J., Stohlman S.A., Hinton D.R., and Marten N.W. Neutrophils promote mononuclear cell infiltration during viral-induced encephalitis. J Immunol 170 (2003) 3331-3336
30. Khuth S.T., Akaoka H., Pagenstecher A., Verlaeten O., Belin M.F., Giraudon P., and Bernard A. Morbillivirus infection of the mouse central nervous system induces region-specific upregulation of MMPs and TIMPs correlated to inflammatory cytokine expression. J Virol 75 (2001) 8268-8282
31. Hu J., Van den Steen P.E., Sang Q.X., and Opdenakker G. Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 6 (2007) 480-498
32. Gran B., Tabibzadeh N., Martin A., Ventura E.S., Ware J.H., Zhang G.X., Parr J.L., Kennedy A.R., and Rostami A.M. The protease inhibitor, Bowman-Birk Inhibitor, suppresses experimental autoimmune encephalomyelitis: a potential oral therapy for multiple sclerosis. Mult Scler 12 (2006) 688-697
33. Lane T.E., Hardison J.L., and Walsh K.B. Functional diversity of chemokines and chemokine receptors in response to viral infection of the central nervous system. Curr Top Microbiol Immunol 303 (2006) 1-27. Review dissecting the roles of various chemokine-receptor interactions in viral control and CNS disease at distinct phases of CNS infection.
34. Klein R.S., Lin E., Zhang B., Luster A.D., Tollett J., Samuel M.A., Engle M., and Diamond M.S. Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J Virol 79 (2005) 11457-11466
35. Glass W.G., Lim J.K., Cholera R., Pletnev A.G., Gao J.L., and Murphy P.M. Chemokine receptor CCR5 promotes leucocyte trafficking to the brain and survival in West Nile virus infection. J Exp Med 202 (2005) 1087-1098
36. Zhang B., Chan Y.K., Lu B., Diamond M.S., and Klein R.S. CXCR3 mediates region-specific antiviral T cell trafficking within the central nervous system during West Nile virus encephalitis. J Immunol 180 (2008) 2641-2649
37. Stiles L.N., Hosking M.P., Edwards R.A., Strieter R.M., and Lane T.E. Differential roles for CXCR3 in CD4+ and CD8+ T cell trafficking following viral infection of the CNS. Eur J Immunol 36 (2006) 613-622
38. Bennett J.L., Elhofy A., Canto M.C., Tani M., Ransohoff R.M., and Karpus W.J. CCL2 transgene expression in the central nervous system directs diffuse infiltration of CD45 (high)CD11b(+) monocytes and enhanced Theiler's murine encephalomyelitis virus-induced demyelinating disease. J Neurovirol 9 (2003) 623-636
39. Bennett J.L., Elhofy A., Charo I., Miller S.D., Dal Canto M.C., and Karpus W.J. CCR2 regulates development of Theiler's murine encephalomyelitis virus-induced demyelinating disease. Viral Immunol 20 (2007) 19-33
40. Hickey M.J., Held K.S., Baum E., Gao J.L., Murphy P.M., and Lane T.E. CCR1 deficiency increases susceptibility to fatal coronavirus infection of the central nervous system. Viral Immunol 20 (2007) 599-608
41. Walsh K.B., Edwards R.A., Romero K.M., Kotlajich M.V., Stohlman S.A., and Lane T.E. Expression of CXC chemokine ligand 10 from the mouse hepatitis virus genome results in protection from viral-induced neurological and liver disease. J Immunol 179 (2007) 1155-1165
42. Cardona A.E., Sasse M.E., Mizutani M., Cardona S.M., Liping L., Savarin C., Taofang H., and Ransohoff R.M. Scavenging roles of chemokine receptors: chemokine receptor deficiency is associated with increased levels of ligand in circulation and tissues. Blood 112 (2008) 256-263. This study demonstrates the complex outcomes of disequilibrium in the chemokine network established following abrogation of individual receptors.
43. Chen A.M., Khanna N., Stohlman S.A., and Bergmann C.C. Virus-specific and bystander CD8 T cells recruited during virus induced encephalomyelitis. J Virol 79 (2005) 4700-4708
44. Burdeinick-Kerr R., Wind J., and Griffin D.E. Synergistic roles of antibody and interferon in noncytolytic clearance of Sindbis virus from different regions of the central nervous system. J Virol 81 (2007) 5628-5636
45. Hausmann J., Pagenstecher A., Baur K., Richter K., Rziha H.J., and Staeheli P. CD8 T cells require gamma interferon to clear borna disease virus from the brain and prevent immune system-mediated neuronal damage. J Virol 79 (2005) 13509-13518
46. Samuel M.A., and Diamond M.S. Pathogenesis of West Nile Virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J Virol 80 (2006) 9349-9360
47. Divito S., Cherpes T.L., and Hendricks R.L. A triple entente: virus, neurons, and CD8+ T cells maintain HSV-1 latency. Immunol Res 36 (2006) 119-126
48. McMahon E.J., Bailey S.L., Castenada C.V., Waldner H., and Miller S.D. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 11 (2005) 335-339
49. Gonzalez J.M., Bergmann C.C., Ramakrishna C., Hinton D.R., Atkinson R., Hoskin J., Macklin W.B., and Stohlman S.A. Inhibition of interferon-gamma signaling in oligodendroglia delays coronavirus clearance without altering demyelination. Am J Pathol 168 (2006) 796-804
50. Ramakrishna C., Atkinson R.A., Stohlman S.A., and Bergmann C.C. Vaccine-induced memory CD8+ T cells cannot prevent central nervous system virus reactivation. J Immunol 176 (2006) 3062-3069
51. Hamo L., Stohlman S.A., Otto-Duessel M., and Bergmann C.C. Distinct regulation of MHC molecule expression on astrocytes and microglia during viral encephalomyelitis. Glia 55 (2007) 1169-1177
52. Malone K.E., Stohlman S.A., Ramakrishna C., Macklin W., and Bergmann C.C. Induction of class I antigen processing components in oligodendroglia and microglia during viral encephalomyelitis. Glia 56 (2008) 426-435. This study is the first to demonstrate distinct in vivo regulation of class I antigen presentation in glia subsets during CNS infection.
53. Suvas S., Azkur A.K., and Rouse B.T. Qa-1b and CD94-NKG2a interaction regulate cytolytic activity of herpes simplex virus-specific memory CD8+ T cells in the latently infected trigeminal ganglia. J Immunol 176 (2006) 1703-1711
54. Walsh K.B., Lanier L.L., and Lane T.E. NKG2D receptor signaling enhances cytolytic activity by virus-specific CD8+ T cells: evidence for a protective role in virus-induced encephalitis. J Virol 82 (2008) 3031-3044
55. Antoniou A.N., and Powis S.J. Pathogen evasion strategies for the major histocompatibility complex class I assembly pathway. Immunology 124 (2008) 1-12
56. Doom C.M., and Hill A.B. MHC class I immune evasion in MCMV infection. Med Microbiol Immunol 197 (2008) 191-204
57. Barcia C., Thomas C.E., Curtin J.F., King G.D., Wawrowsky K., Candolfi M., Xiong W.D., Liu C., Kroeger K., Boyer O., et al. In vivo mature immunological synapses forming SMACs mediate clearance of virally infected astrocytes from the brain. J Exp Med 203 (2006) 2095-2107. This paper is the first to demonstrate MHC dependent CD8 T cell interactions with astrocytes at the single cell level in CNS tissue.
58. Barcia C., Wawrowsky K., Barrett R.J., Liu C., Castro M.G., and Lowenstein P.R. In vivo polarization of IFN-gamma at Kupfer and non-Kupfer immunological synapses during the clearance of virally infected brain cells. J Immunol 180 (2008) 1344-1352
59. Barber D.L., Wherry E.J., Masopust D., Zhu B., Allison J.P., Sharpe A.H., Freeman G.J., and Ahmed R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439 (2006) 682-687
60. Tschen S.I., Stohlman S.A., Ramakrishna C., Hinton D.R., Atkinson R.D., and Bergmann C.C. CNS viral infection diverts homing of antibody-secreting cells from lymphoid organs to the CNS. Eur J Immunol 36 (2006) 603-612