Inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels

Journal of Virology

Volumn 81, Issue 13, 2007, Pages 7189-7199

  Roth Cross, Jessica K ^a   Martínez Sobrido, Luis ^b   Scott, Erin P ^a   García Sastre, Adolfo ^b   Weiss, Susan R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; INTERFERON REGULATORY FACTOR 3; MESSENGER RNA; PROTEASOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CELL LINE; CONTROLLED STUDY; CORONAVIRUS; INNATE IMMUNITY; INTERFERON INDUCTION; MALE; MESSENGER RNA SYNTHESIS; MOUSE; MURINE HEPATITIS CORONAVIRUS; NEWCASTLE DISEASE PARAMYXOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN TRANSPORT; SENDAI VIRUS; VIRUS REPLICATION; VIRUS STRAIN;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTIVIRAL AGENTS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; FIBROBLASTS; HEPATITIS, VIRAL, ANIMAL; INTERFERON REGULATORY FACTOR-3; INTERFERON-ALPHA; INTERFERON-BETA; MALE; MICE; MURINE HEPATITIS VIRUS; NEWCASTLE DISEASE VIRUS; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA STABILITY; RNA, MESSENGER; SENDAI VIRUS; VERO CELLS; VIRUS REPLICATION;

ANIMALIA; MURINE HEPATITIS VIRUS; NEWCASTLE DISEASE VIRUS; SENDAI VIRUS;

EID: 34250836810     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00013-07     Document Type: Article

References (82)

1. Aurisicchio, L., P. Delmastro, V. Salucci, O. G. Paz, P. Rovere, G. Ciliberto, N. La Monica, and F. Palombo. 2000. Liver-specific alpha 2 interferon gene expression results in protection from induced hepatitis. J. Virol. 74:4816-4823.
2. Baigent, S. J., G. Zhang, M. D. Fray, H. Flick-Smith, S. Goodbourn, and J. W. McCauley. 2002. Inhibition of beta interferon transcription by noncytopathogenic bovine viral diarrhea virus is through an interferon regulatory factor 3-dependent mechanism. J. Virol. 76:8979-8988.
3. Barchet, W., M. Cella, and M. Colonna. 2005. Plasmacytoid dendritic cells - virus experts of innate immunity. Semin. Immunol. 17:253-261.
4. Basler, C. F., A. Mikulasova, L. Martinez-Sobrido, J. Paragas, E. Muhl berger, M. Bray, H. D. Klenk, P. Palese, and A. Garcia-Sastre. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
5. Baudoux, P., C. Carrat, L. Besnardeau, B. Charley, and H. Laude. 1998. Coronavirus pseudoparticles formed with recombinant M and E proteins induce alpha interferon synthesis by leukocytes. J. Virol. 72:8636-8643.
6. Biron, C. A. 2001. Interferons alpha and beta as immune regulators - a new look. Immunity 14:661-664.
7. Brzozka, K., S. Finke, and K. K. Conzelmann. 2005. Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J. Virol. 79:7673-7681.
8. Cervantes-Barragan, L., R. Zust, F. Weber, M. Spiegel, K. S. Lang, S. Akira, V. Thiel, and B. Ludewig. 2007. Control of coronavirus infection through plasmacytoid dendritic cell-derived type I interferon. Blood 109:1131-1137.
9. Cheung, C. Y., L. L. Poon, I. H. Ng, W. Luk, S. F. Sia, M. H. Wu, K. H. Chan, K. Y. Yuen, S. Gordon, Y. Guan, and J. S. Peiris. 2005. Cytokine responses in severe acute respiratory syndrome coronavirus-infected macrophages in vitro: possible relevance to pathogenesis. J. Virol. 79:7819-7826.
10. Choe, S. S., D. A. Dodd, and K. Kirkegaard. 2005. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology 337:18-29.
11. De Albuquerque, N., E. Baig, X. Ma, J. Zhang, W. He, A. Rowe, M. Habal, M. Liu, I. Shalev, G. P. Downey, R. Gorcynski, J. Butany, J. Leibowitz, S. R. Weiss, I. D. McGilvray, M. J. Phillips, E. N. Fish, and G. A. Levy. 2006. Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice. J. Virol. 80:10382-10394.
12. Deonarain, R., A. Alcami, M. Alexiou, M. J. Dallman, D. R. Gewert, and A. C. Porter. 2000. Impaired antiviral response and alpha/beta interferon induction in mice lacking beta interferon. J. Virol. 74:3404-3409.
13. de Veer, M. J., M. Holko, M. Frevel, E. Walker, S. Der, J. M. Paranjape, R. H. Silverman, and B. R. Williams. 2001. Functional classification of interferon-stimulated genes identified using microarrays. J. Leukoc. Biol. 69:912-920.
14. Diebold, S. S., M. Montoya, H. Unger, L. Alexopoulou, P. Roy, L. E. Haswell, A. Al-Shamkhani, R. Flavell, P. Borrow, and C. Reis e Sousa. 2003. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 424:324-328.
15. Dodd, D. A., T. H. Giddings, Jr., and K. Kirkegaard. 2001. Poliovirus 3A protein limits interleukin-6 (IL-6), IL-8, and beta interferon secretion during viral infection. J. Virol. 75:8158-8165.
16. Doedens, J. R., T. H. Giddings, Jr., and K. Kirkegaard. 1997. Inhibition of endoplasmic reticulum-to-Golgi traffic by poliovirus protein 3A: genetic and ultrastructural analysis. J. Virol. 71:9054-9064.
17. Erlandsson, L., R. Blumenthal, M. L. Eloranta, H. Engel, G. Alm, S. Weiss, and T. Leanderson. 1998. Interferon-beta is required for interferon-alpha production in mouse fibroblasts. Curr. Biol. 8:223-226.
18. Esper, F., C. Weibel, D. Ferguson, M. L. Landry, and J. S. Kahn. 2006. Coronavirus HKU1 infection in the United States. Emerg. Infect. Dis. 12: 775-779.
19. Fernandez-Sesma, A., S. Marukian, B. J. Ebersole, D. Kaminski, M. S. Park, T. Yuen, S. C. Sealfon, A. Garcia-Sastre, and T. M. Moran. 2006. Influenza virus evades innate and adaptive immunity via the NS1 protein. J. Virol. 80:6295-6304.
20. Garcia-Sastre, A., and C. A. Biron. 2006. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312:879-882.
21. Garlinghouse, L. E., Jr., A. L. Smith, and T. Holford. 1984. The biological relationship of mouse hepatitis virus (MHV) strains and interferon: in vitro induction and sensitivities. Arch. Virol. 82:19-29.
22. Gombold, J. L., S. T. Hingley, and S. R. Weiss. 1993. Fusion-defective mutants of mouse hepatitis virus A59 contain a mutation in the spike protein cleavage signal. J. Virol. 67:4504-4512.
23. Hilton, A., L. Mizzen, G. MacIntyre, S. Cheley, and R. Anderson. 1986. Translational control in murine hepatitis virus infection. J. Gen. Virol. 67: 923-932.
24. Hilton, L., K. Moganeradj, G. Zhang, Y. H. Chen, R. E. Randall, J. W. McCauley, and S. Goodbourn. 2006. The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J. Virol. 80:11723-11732.
25. Iacono, K. T., L. Kazi, and S. R. Weiss. 2006. Both spike and background genes contribute to murine coronavirus neurovirulence. J. Virol. 80:6834-6843.
26. Jackson, R. J., and N. Standart. 2007. How do microRNAs regulate gene expression? Sci. STKE 2007:re1.
27. Johnson, C. L., and M. Gale, Jr. 2006. CARD games between virus and host get a new player. Trends Immunol. 27:1-4.
28. Juang, Y. T., W. Lowther, M. Kellum, W. C. Au, R. Lin, J. Hiscott, and P. M. Pitha. 1998. Primary activation of interferon α and interferon β gene transcription by interferon regulatory factor 3. Proc. Natl. Acad. Sci. USA 95: 9837-9842.
29. Kamitani, W., K. Narayanan, C. Huang, K. Lokugamage, T. Ikegami, N. Ito, H. Kubo, and S. Makino. 2006. Severe acute respiratory syndrome coronavirus Nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc. Natl. Acad. Sci. USA 103:12885-12890.
30. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, O. Yamaguchi, K. Otsu, T. Tsujimura, C. S. Koh, C. Reis e Sousa, Y. Matsuura, T. Fujita, and S. Akira. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
31. Knobler, R. L., P. W. Lampert, and M. B. Oldstone. 1982. Virus persistence and recurring demyelination produced by a temperature-sensitive mutant of MHV-4. Nature 298:279-280.
32. Kopecky-Bromberg, S. A., L. Martinez-Sobrido, M. Frieman, R. A. Baric, and P. Palese. 2007. SARS coronavirus proteins Orf 3b, Orf 6, and nucleocapsid function as interferon antagonists. J. Virol. 81:548-557.
33. Kovacsovics, M., F. Martinon, O. Micheau, J. L. Bodmer, K. Hofmann, and J. Tschopp. 2:002. Overexpression of Helicard, a CARD-containing helicase cleaved during apoptosis, accelerates DNA degradation. Curr. Biol. 12:838-843.
34. Lavi, E., and Q. Wang. 1995. The protective role of cytotoxic T cells and interferon against coronavirus invasion of the brain. Adv. Exp. Med. Biol. 380:145-149.
35. Liu, Y. J. 2005. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23:275-306.
36. Marie, I., J. E. Durbin, and D. E. Levy. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17:6660-6669.
37. Matsumoto, M., K. Funami, H. Oshiumi, and T. Seya. 2004. Toll-like receptor 3: a link between toll-like receptor, interferon and viruses. Microbiol. Immunol. 48:147-154.
38. Matsuyama, S., S. Henmi, N. Ichihara, S. Sone, T. Kikuchi, T. Ariga, and F. Taguchi. 2000. Protective effects of murine recombinant interferon-beta administered by intravenous, intramuscular or subcutaneous route on mouse hepatitis virus infection. Antivir. Res. 47:131-137.
39. Mibayashi, M., L. Martinez-Sobrido, Y. M. Loo, W. B. Cardenas, M. Gale, Jr., and A. Garcia-Sastre. 2007. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 81:514-524.
40. Minagawa, H., A. Takenaka, S. Mohri, and R. Mori. 1987. Protective effect of recombinant murine interferon beta against mouse hepatitis virus infection. Antivir. Res. 8:85-95.
41. Navas, S., and S. R. Weiss. 2003. Murine coronavirus-induced hepatitis: JHM genetic background eliminates A59 spike-determined hepatotropism. J. Virol. 77:4972-4978.
42. Park, M. S., M. L. Shaw, J. Munoz-Jordan, J. F. Cros, T. Nakaya, N. Bouvier, P. Palese, A. Garcia-Sastre, and C. F. Basler. 2003. Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J. Virol. 77:1501-1511.
43. Peiris, J. S., S. T. Lai, L. L. Poon, Y. Guan, L. Y. Yam, W. Lim, J. Nicholls, W. K. Yee, W. W. Yan, M. T. Cheung, V. C. Cheng, K. H. Chan, D. N. Tsang, R. W. Yung, T. K. Ng, and K. Y. Yuen. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-1325.
44. Peiris, J. S., K. Y. Yuen, A. D. Osterhaus, and K. Stohr. 2003. The severe acute respiratory syndrome. N. Engl. J. Med. 349:2431-2441.
45. Peng, T., S. Kotla, R. E. Bumgarner, and K. E. Gustin. 2006. Human rhinovirus attenuates the type I interferon response by disrupting activation of interferon regulatory factor 3. J. Virol. 80:5021-5031.
46. Phillips, J. J., M. M. Chua, E. Lavi, and S. R. Weiss. 1999. Pathogenesis of chimeric MHV4/MHV-A59 recombinant viruses: the murine coronavirus spike protein is a major determinant of neurovirulence. J. Virol. 73:7752-7760.
47. Pirhonen, J., S. Matikainen, and I. Julkunen. 2002. Regulation of virus-induced IL-12 and IL-23 expression in human macrophages. J. Immunol. 169:5673-5678.
48. Rempel, J. D., S. J. Murray, J. Meisner, and M. J. Buchmeier. 2004. Differential regulation of innate and adaptive immune responses in viral encephalitis. Virology 318:381-392.
49. Rempel, J. D., S. J. Murray, J. Meisner, and M. J. Buchmeier. 2004. Mouse hepatitis virus neurovirulence: evidence of a linkage between S glycoprotein expression and immunopathology. Virology 318:45-54.
50. Riffault, S., C. Carrat, K. van Reeth, M. Pensaert, and B. Charley. 2001. Interferon-alpha-producing cells are localized in gut-associated lymphoid tissues in transmissible gastroenteritis virus (TGEV) infected piglets. Vet. Res. 32:71-79.
51. Sarma, J. D., L. Fu, S. T. Hingley, and E. Lavi. 2001. Mouse hepatitis virus type-2 infection in mice: an experimental model system of acute meningitis and hepatitis. Exp. Mol. Pathol. 71:1-12.
52. Sarma, J. D., E. Scheen, S. H. Seo, M. Koval, and S. R. Weiss. 2002. Enhanced green fluorescent protein expression may be used to monitor murine coronavirus spread in vitro and in the mouse central nervous system. J. Neurovirol. 8:381-391.
53. Schafer, S. L., R. Lin, P. A. Moore, J. Hiscott, and P. M. Pitha. 1998. Regulation of type I interferon gene expression by interferon regulatory factor-3. J. Biol. Chem. 273:2714-2720.
54. Schindler, L., H. Engler, and H. Kirchner. 1982. Activation of natural killer cells and induction of interferon after injection of mouse hepatitis virus type 3 in mice. Infect. Immun. 35:869-873.
55. Schweizer, M., P. Matzener, G. Pfaffen, H. Stalder, and E. Peterhans. 2006. "Self" and "nonself" manipulation of interferon defense during persistent infection: bovine viral diarrhea virus resists alpha/beta interferon without blocking antiviral activity against unrelated viruses replicating in its host cells. J. Virol. 80:6926-6935.
56. Siddell, S., H. Wege, A. Barthel, and V. ter Meulen. 1981. Intracellular protein synthesis and the in vitro translation of coronavirus JHM mRNA. Adv. Exp. Med. Biol. 142:193-207.
57. Smith, A. L., S. W. Barthold, and D. S. Beck. 1987. Intranasally administered alpha/beta interferon prevents extension of mouse hepatitis virus, strain JHM, into the brains of BALB/cByJ mice. Antivir. Res. 8:239-245.
58. Smith, E. J., I. Marie, A. Prakash, A. Garcia-Sastre, and D. E. Levy. 2001. IRF3 and IRF7 phosphorylation in virus-infected cells does not require double-stranded RNA-dependent protein kinase R or Iκ B kinase but is blocked by vaccinia virus E3L protein. J. Biol. Chem. 276:8951-8957.
59. Spiegel, M., A. Pichlmair, L. Martinez-Sobrido, J. Cros, A. Garcia-Sastre, O. Haller, and F. Weber. 2005. Inhibition of beta interferon induction by severe acute respiratory syndrome coronavirus suggests a two-step model for activation of interferon regulatory factor 3. J. Virol. 79:2079-2086.
60. Spiegel, M., K. Schneider, F. Weber, M. Weidmann, and F. T. Hufert. 2006. Interaction of severe acute respiratory syndrome-associated coronavirus with dendritic cells. J. Gen. Virol. 87:1953-1960.
61. Spiegel, M., and F. Weber. 2006. Inhibition of cytokine gene expression and induction of chemokine genes in non-lymphatic cells infected with SARS coronavirus. Virol. J. 3:17.
62. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67:227-264.
63. Stohlman, S. A., A. Y. Sakaguchi, and A. Hiti. 1978. Interferon production and activity in mouse neuroblastoma cells. Arch. Virol. 57:91-96.
64. Taguchi, F, and S. G. Siddell. 1985. Difference in sensitivity to interferon among mouse hepatitis viruses with high and low virulence for mice. Virology 147:41-48.
65. Talon, J., C. M. Horvath, R. Polley, C. F. Basler, T. Muster, P. Palese, and A. Garcia-Sastre. 2000. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 74:7989-7996.
66. Theofilopoulos, A. N., R. Baccala, B. Beutler, and D. H. Kono. 2005. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 23:307-336.
67. Traven, M., K. Naslund, N. Linde, B. Linde, A. Silvan, C. Fossum, K. O. Hedlund, and B. Larsson. 2001. Experimental reproduction of winter dysentery in lactating cows using BCV - comparison with BCV infection in milk-fed calves. Vet. Microbiol. 81:127-151.
68. Uetsuka, K., H. Nakayama, and N. Goto. 1996. Protective effect of recombinant interferon (IFN)-alpha/beta on MHV-2cc-induced chronic hepatitis in athymic nude mice. Exp. Anim. 45:293-297.
69. van der Hoek, L., K. Pyrc, and B. Berkhout. 2006. Human coronavirus NL63, a new respiratory virus. FEMS Microbiol. Rev. 30:760-773.
70. van der Hoek, L., K. Pyrc, M. F. Jebbink, W. Vermeulen-Oost, R. J. Berkhout, K. C. Wolthers, P. M. Wertheim-van Dillen, J. Kaandorp, J. Spaargaren, and B. Berkhout. 2004. Identification of a new human coronavirus. Nat. Med. 10:368-373.
71. Versteeg, G. A., P. J. Bredenbeek, S. H. van den Worm, and W. J. Spaan. 2007. Group 2 coronaviruses prevent immediate early interferon induction by protection of viral RNA from host cell recognition. Virology 361:18-26.
72. Versteeg, G. A., O. Slobodskaya, and W. J. Spaan. 2006. Transcriptional profiling of acute cytopathic murine hepatitis virus infection in fibroblast-like cells. J. Gen. Virol. 87:1961-1975.
73. Virelizier, J. L. 1981. Role of macrophages and interferon in natural resistance to mouse hepatitis virus infection. Curr. Top. Microbiol. Immunol. 92:53-64.
74. Virelizier, J. L., and A. C. Allison. 1976. Correlation of persistent mouse hepatitis virus (MHV-3) infection with its effect on mouse macrophage cultures. Arch. Virol. 50:279-285.
75. Wang, Q., J. A. Haluskey, and E. Lavi. 1998. Coronavirus MHV-A59 causes upregulation of interferon-beta RNA in primary glial cell cultures. Adv. Exp. Med. Biol. 440:451-454.
76. Weiss, S. R., and S. Navas-Martin. 2005. Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol. Mol. Biol. Rev. 69:635-664.
77. Woo, P. C., S. K. Lau, C. M. Chu, K. H. Chan, H. W. Tsoi, Y. Huang, B. H. Wong, R. W. Poon, J. J. Cai, W. K. Luk, L. L. Poon, S. S. Wong, Y. Guan, J. S. Peiris, and K. Y. Yuen. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79:884-895.
78. Ye, Y., K. Hauns, J. O. Langland, B. L. Jacobs, and B. G. Hogue. 2007. Mouse hepatitis coronavirus A59 nucleocapsid protein is a type I interferon antagonist. J. Virol. 81:2554-2563.
79. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737.
80. Zhong, N. S., B. J. Zheng, Y. M. Li, Poon, Z. H. Xie, K. H. Chan, P. H. Li, S. Y. Tan, Q. Chang, J. P. Xie, X. Q. Liu, J. Xu, D. X. Li, K. Y. Yuen, J. S. Peiris, and Y. Guan. 2003. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. Lancet 362:1353-1358.
81. Zhou, H., and S. Perlman. 2007. Mouse hepatitis virus does not induce beta interferon synthesis and does not inhibit its induction by double-stranded RNA. J. Virol. 81:568-574.
82. Zhou, H., and S. Perlman. 2006. Preferential infection of mature dendritic cells by mouse hepatitis virus strain JHM. J. Virol. 80:2506-2514.