IFN-γ-mediated suppression of coronavirus replication in glial-committed progenitor cells

Virology

Volumn 384, Issue 1, 2009, Pages 209-215

  Whitman, Lucia ^a   Zhou, Haixia ^b   Perlman, Stanley ^b   Lane, Thomas E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Central nervous system; Interferons; Neural progenitor cells; Virus

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GAMMA INTERFERON;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GLIA CELL; IMMUNOHISTOCHEMISTRY; INFECTION SENSITIVITY; INOCULATION; KNOCKOUT MOUSE; MOUSE; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; PRIORITY JOURNAL; STEM CELL; VIRUS INFECTION; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; ANTIVIRAL AGENTS; ASTROCYTES; CELLS, CULTURED; CORONAVIRUS; INTERFERON-GAMMA; MICE; MURINE HEPATITIS VIRUS; NEUROGLIA; STEM CELLS; VIRUS REPLICATION;

CORONAVIRUS; MURINE HEPATITIS VIRUS; MUS;

EID: 58549107360     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.10.036     Document Type: Article

References (51)

1. Aharonowiz M., Einstein O., Fainstein N., Lassmann H., Reubinoff B., and Ben-Hur T. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS ONE 3 9 (2008) e3145
2. Ben-Hur T., Rogister B., Murray K., Rougon G., and Dubois-Dalcq M. Growth and fate of PSA-NCAM+ precursors of the postnatal brain. J. Neurosci. 18 15 (1998) 5777-5788
3. Ben-Hur T., Einstein O., Mizrachi-Kol R., Ben-Menachem O., Reinhartz E., Karussis D., and Abramsky O. Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia 41 1 (2003) 73-80
4. Bergmann C.C., Parra B., Hinton D.R., Chandran R., Morrison M., and Stohlman S.A. Perforin-mediated effector function within the central nervous system requires IFN-gamma-mediated MHC up-regulation. J. Immunol. 170 6 (2003) 3204-3213
5. Bhowmick S., Duseja R., Das S., Appaiahgiri M.B., Vrati S., and Basu A. Induction of IP-10 (CXCL10) in astrocytes following Japanese encephalitis. Neurosci. Lett. 414 1 (2007) 45-50
6. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., and McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 285 5428 (1999) 754-756
7. Buchmeier M.J., and Lane T.E. Viral-induced neurodegenerative disease. Curr. Opin. Microbiol. 2 4 (1999) 398-402
8. 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 11 (2007) 5628-5636
9. Byrnes A.P., Durbin J.E., and Griffin D.E. Control of Sindbis virus infection by antibody in interferon-deficient mice. J. Virol. 74 8 (2000) 3905-3908
10. Cervantes-Barragan L., Zust 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 3 (2007) 1131-1137
11. Cheever F.S., Daniels J.B., Pappenheimer A.M., and Bailey O.T. A murine virus (JHM) causing disseminated encephalomyelitis with extensive destruction of myelin. J. Exp. Med. 90 3 (1949) 181-210
12. Dietrich J., Blumberg B.M., Roshal M., Baker J.V., Hurley S.D., Mayer-Proschel M., and Mock D.J. Infection with an endemic human herpesvirus disrupts critical glial precursor cell properties. J. Neurosci. 24 20 (2004) 4875-4883
13. Dubois-Dalcq M.E., Doller E.W., Haspel M.V., and Holmes K.V. Cell tropism and expression of mouse hepatitis viruses (MHV) in mouse spinal cord cultures. Virology 119 2 (1982) 317-331
14. Einstein O., Grigoriadis N., Mizrachi-Kol R., Reinhartz E., Polyzoidou E., Lavon I., Milonas I., Karussis D., Abramsky O., and Ben-Hur T. Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp. Neurol. 198 2 (2006) 275-284
15. Fleming J.O., Stohlman S.A., Harmon R.C., Lai M.M., Frelinger J.A., and Weiner L.P. Antigenic relationships of murine coronaviruses: analysis using monoclonal antibodies to JHM (MHV-4) virus. Virology 131 2 (1983) 296-307
16. Fleming J.O., Trousdale M.D., el-Zaatari F.A., Stohlman S.A., and Weiner L.P. Pathogenicity of antigenic variants of murine coronavirus JHM selected with monoclonal antibodies. J. Virol. 58 3 (1986) 869-875
17. Fragkoudis R., Breakwell L., McKimmie C., Boyd A., Barry G., Kohl A., Merits A., and Fazakerley J.K. The type I interferon system protects mice from Semliki Forest virus by preventing widespread virus dissemination in extraneural tissues, but does not mediate the restricted replication of avirulent virus in central nervous system neurons. J. Gen. Virol. 88 Pt 12 (2007) 3373-3384
18. Gilden D.H. Infectious causes of multiple sclerosis. Lancet Neurol. 4 3 (2005) 195-202
19. Gonzalez J.M., Bergmann C.C., Fuss B., Hinton D.R., Kangas C., Macklin W.B., and Stohlman S.A. Expression of a dominant negative IFN-gammareceptor on mouse oligodendrocytes. Glia 51 1 (2005) 22-34
20. 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 3 (2006) 796-804
21. Hardison J.L., Nistor G., Gonzalez R., Keirstead H.S., and Lane T.E. Transplantation of glial-committed progenitor cells into a viral model of multiple sclerosis induces remyelination in the absence of an attenuated inflammatory response. Exp. Neurol. 197 2 (2006) 420-429
22. Hirano N., Murakami T., Fujiwara K., and Matsumoto M. Utility of mouse cell line DBT for propagation and assay of mouse hepatitis virus. Jpn. J. Exp. Med. 48 1 (1978) 71-75
23. 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 1 (2008) 300-310
24. Keirstead H.S., Ben-Hur T., Rogister B., O'Leary M.T., Dubois-Dalcq M., and Blakemore W.F. Polysialylated neural cell adhesion molecule-positive CNS precursors generate both oligodendrocytes and Schwann cells to remyelinate the CNS after transplantation. J. Neurosci. 19 17 (1999) 7529-7536
25. Knobler R.L., Dubois-Dalcq M., Haspel M.V., Claysmith A.P., Lampert P.W., and Oldstone M.B. Selective localization of wild type and mutant mouse hepatitis virus (JHM strain) antigens in CNS tissue by fluorescence, light and electron microscopy. J. Neuroimmunol. 1 1 (1981) 81-92
26. Lane T.E., Asensio V.C., Yu N., Paoletti A.D., Campbell I.L., and Buchmeier M.J. Dynamic regulation of alpha- and beta-chemokine expression in the central nervous system during mouse hepatitis virus-induced demyelinating disease. J. Immunol. 160 2 (1998) 970-978
27. Lane T.E., Liu M.T., Chen B.P., Asensio V.C., Samawi R.M., Paoletti A.D., Campbell I.L., Kunkel S.L., Fox H.S., and Buchmeier M.J. A central role for CD4(+) T cells and RANTES in virus-induced central nervous system inflammation and demyelination. J. Virol. 74 3 (2000) 1415-1424
28. Lavi E., and Wang Q. The protective role of cytotoxic T cells and interferon against coronavirus invasion of the brain. Adv. Exp. Med. Biol. 380 (1995) 145-149
29. Lavi E., Suzumura A., Hirayama M., Highkin M.K., Dambach D.M., Silberberg D.H., and Weiss S.R. Coronavirus mouse hepatitis virus (MHV)-A59 causes a persistent, productive infection in primary glial cell cultures. Microb. Pathog. 3 2 (1987) 79-86
30. Levine J.M., Enquist L.W., and Card J.P. Reactions of oligodendrocyte precursor cells to alpha herpesvirus infection of the central nervous system. Glia 23 4 (1998) 316-328
31. Lin M.T., Stohlman S.A., and Hinton D.R. Mouse hepatitis virus is cleared from the central nervous systems of mice lacking perforin-mediated cytolysis. J. Virol. 71 1 (1997) 383-391
32. Liu M.T., Chen B.P., Oertel P., Buchmeier M.J., Armstrong D., Hamilton T.A., and Lane T.E. The T cell chemoattractant IFN-inducible protein 10 is essential in host defense against viral-induced neurologic disease. J. Immunol. 165 5 (2000) 2327-2330
33. Liu M.T., Armstrong D., Hamilton T.A., and Lane T.E. Expression of Mig (monokine induced by interferon-gamma) is important in T lymphocyte recruitment and host defense following viral infection of the central nervous system. J. Immunol. 166 3 (2001) 1790-1795
34. Majumder S., Zhou L.Z., Chaturvedi P., Babcock G., Aras S., and Ransohoff R.M. Regulation of human IP-10 gene expression in astrocytoma cells by inflammatory cytokines. J. Neurosci. Res. 54 2 (1998) 169-180
35. Matsuyama S., Henmi S., Ichihara N., Sone S., Kikuchi T., Ariga T., and Taguchi F. Protective effects of murine recombinant interferon-beta administered by intravenous, intramuscular or subcutaneous route on mouse hepatitis virus infection. Antivir. Res. 47 2 (2000) 131-137
36. Mock D.J., Strathmann F., Blumberg B.M., and Mayer-Proschel M. Infection of murine oligodendroglial precursor cells with Human Herpesvirus 6 (HHV-6) - establishment of a murine in vitro model. J. Clin. Virol. 37 Suppl 1 (2006) S17-S23
37. Olson J.K., Ercolini A.M., and Miller S.D. A virus-induced molecular mimicry model of multiple sclerosis. Curr. Top. Microbiol. Immunol. 296 (2005) 39-53
38. Palma J.P., Kwon D., Clipstone N.A., and Kim B.S. Infection with Theiler's murine encephalomyelitis virus directly induces proinflammatory cytokines in primary astrocytes via NF-kappaB activation: potential role for the initiation of demyelinating disease. J. Virol. 77 11 (2003) 6322-6331
39. Parra B., Hinton D.R., Marten N.W., Bergmann C.C., Lin M.T., Yang C.S., and Stohlman S.A. IFN-gamma is required for viral clearance from central nervous system oligodendroglia. J. Immunol. 162 3 (1999) 1641-1647
40. Perlman S.R., Lane T.E., and Buchmeier M.J. Coronaviruses: hepatitis, peritonitis, and central nervous system disease. In: Cunningham M.W., and Fujinami R.S. (Eds). Effects of Microbes on the Immune System Vol. 1 (1999), Lippincott Williams & Wilkins, Philadelphia 331-348
41. Pluchino S., Quattrini A., Brambilla E., Gritti A., Salani G., Dina G., Galli R., Del Carro U., Amadio S., Bergami A., Furlan R., Comi G., Vescovi A.L., and Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422 6933 (2003) 688-694
42. Rempel J.D., Quina L.A., Blakely-Gonzales P.K., Buchmeier M.J., and Gruol D.L. Viral induction of central nervous system innate immune responses. J. Virol. 79 7 (2005) 4369-4381
43. Roth-Cross J.K., Martinez-Sobrido L., Scott E.P., Garcia-Sastre A., and Weiss S.R. Inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels. J. Virol. 81 13 (2007) 7189-7199
44. 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 21 (2005) 13350-13361
45. Smith A.L., Barthold S.W., and Beck D.S. Intranasally administered alpha/beta interferon prevents extension of mouse hepatitis virus, strain JHM, into the brains of BALB/cByJ mice. Antivir. Res. 8 5-6 (1987) 239-245
46. Totoiu M.O., Nistor G.I., Lane T.E., and Keirstead H.S. Remyelination, axonal sparing, and locomotor recovery following transplantation of glial-committed progenitor cells into the MHV model of multiple sclerosis. Exp. Neurol. 187 2 (2004) 254-265
47. Vanguri P., and Farber J.M. IFN and virus-inducible expression of an immediate early gene, crg-2/IP-10, and a delayed gene, I-A alpha in astrocytes and microglia. J. Immunol. 152 3 (1994) 1411-1418
48. Versteeg G.A., Bredenbeek P.J., van den Worm S.H., and Spaan W.J. Group 2 coronaviruses prevent immediate early interferon induction by protection of viral RNA from host cell recognition. Virology 361 1 (2007) 18-26
49. 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 2 (2007) 1155-1165
50. Ye Y., Hauns K., Langland J.O., Jacobs B.L., and Hogue B.G. Mouse hepatitis coronavirus A59 nucleocapsid protein is a type I interferon antagonist. J. Virol. 81 6 (2007) 2554-2563
51. Zhou H., and Perlman S. Mouse hepatitis virus does not induce Beta interferon synthesis and does not inhibit its induction by double-stranded RNA. J. Virol. 81 2 (2007) 568-574