Mouse hepatitis virus does not induce beta interferon synthesis and does not inhibit its induction by double-stranded RNA

Journal of Virology

Volumn 81, Issue 2, 2007, Pages 568-574

  Zhou, Haixia ^a   Perlman, Stanley ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; DOUBLE STRANDED RNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; PATTERN RECOGNITION RECEPTOR; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN MDA 5; PROTEIN RIG I; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG;

ARTICLE; BONE MARROW CELL; CYTOKINE PRODUCTION; DENDRITIC CELL; FIBROBLAST; GENE INDUCTION; GENE TRANSLOCATION; HOST; HUMAN; HUMAN CELL; INHIBITION KINETICS; MOLECULAR RECOGNITION; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; PRIORITY JOURNAL; VIRUS INFECTION;

ANIMALS; CELL LINE; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; MEMBRANE PROTEINS; MICE; MURINE HEPATITIS VIRUS; NERVE TISSUE PROTEINS; NF-KAPPA B; POLY I-C; RNA, DOUBLE-STRANDED; TOLL-LIKE RECEPTOR 3;

MURINE HEPATITIS VIRUS;

EID: 33846070661     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01512-06     Document Type: Article

References (63)

1. Alexopoulou, L., A, C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
2. Andrejeva, J., K. S. Childs, D. F. Young, T. S. Carlos, N. Stock, S. Goodbourn, and R. E. Randall. 2004. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. USA 101:17264-17269.
3. Baigent, S. J., S. Goodbourn, and J. W. McCauley. 2004. Differential activation of interferon regulatory factors-3 and -7 by non-cytopathogenic and cytopathogenic bovine viral diarrhoea virus. Vet. Immunol. Immunopathol. 100:135-144.
4. 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.
5. Banerjee, S., K. Narayanan, T. Mizutani, and S. Makino. 2002. Murine coronavirus replication-induced p38 mitogen-activated protein kinase activation promotes interleukin-6 production and virus replication in cultured cells. J. Virol. 76:5937-5948.
6. Basler, C. F., A. Mikulasova, L. Martinez-Sobrido, J. Paragas, E. Muhlberger, 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.
7. Cervantes-Barragan, L., R. Zust, F. Weber, M. Spiegel, K. S. Lang, S. Akira, V. Thiel, and B. Ludewig. 10 September 2006. Control of coronavirus infection through plasmacytoid dendritic cell-derived type I interferon. Blood doi:10.1182/blood-2006-05-023770.
8. 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.
9. de Haan, C. A., M. de Wit, L. Kuo, C. Montalto-Morrison, B. L. Haagmans, S. R. Weiss, P. S. Masters, and P. J. Rottier. 2003. The glycosylation status of the murine hepatitis coronavirus M protein affects the interferogenic capacity of the virus in vitro and its ability to replicate in the liver but not the brain. Virology 312:395-406.
10. Dubois-Dalcq, M., E. Doller, M. Haspel, and K. V. Holmes. 1982. Cell tropism and expression of mouse hepatitis viruses (MHV) in mouse spinal cord cultures. Virology 119:317-331.
11. Edelmann, K. H., S. Richardson-Burns, L. Alexopoulou, K. L. Tyler, R. A. Flavell, and M. B. Oldstone. 2004. Does Toll-like receptor 3 play a biological role in virus infections? Virology 322:231-238.
12. Fensterl, V., D. Grotheer, I. Berk, S. Schlemminger, A. Vallbracht, and A. Dotzauer. 2005. Hepatitis A virus suppresses RIG-I-mediated IRF-3 activation to block induction of beta interferon. J. Virol. 79:10968- 10977.
13. Fitzgerald, K. A., S. M. McWhirter, K. L. Faia, D. C. Rowe, E. Latz, D. T. Golenbock, A. J. Coyle, S. M. Liao, and T. Maniatis. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491-496.
14. Garcia-Sastre, A., and C. A. Biron. 2006. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312:879-882.
15. 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.
16. -/- mice are completely resistant to infection by murine coronavirus mouse hepatitis virus A59. J. Virol. 78:10156-10165.
17. Hengel, H., U. H. Koszinowski, and K. K. Conzelmann. 2005. Viruses know it all: new insights into IFN networks. Trends Immunol. 26:396-401.
18. Jackson, W. T., T. H. Giddings, Jr., M. P. Taylor, S. Mulinyawe, M. Rabinovitch, R. R. Kopito, and K. Kirkegaard. 2005. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3:e156.
19. Kang, D. C., R. V. Gopalkrishnan, Q. Wu, E. Jankowsky, A. M. Pyle, and P. B. Fisher. 2002. mda-5: an interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. USA 99:637-642.
20. 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.
21. Kawai, T., and S. Akira. 2006. Innate immune recognition of viral infection. Nat. Immunol. 7:131-137.
22. Kawai, T., K. Takahashi, S. Sato, C. Coban, H. Kumar, H. Kato, K. J. Ishii, O. Takeuchi, and S. Akira. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981-988.
23. Kumar, K. P., K. M. McBride, B. K. Weaver, C. Dingwall, and N. C. Reich. 2000. Regulated nuclear-cytoplasmic localization of interferon regulatory factor 3, a subunit of double-stranded RNA-activated factor 1. Mol. Cell. Biol. 20:4159-4168.
24. pro. J. Virol. 79:7239-7247.
25. Laude, H., J. Gelfi, L. Lavenant, and B. Charley. 1992. Single amino acid changes in the viral glycoprotein M affect induction of alpha interferon by the coronavirus transmissible gastroenteritis virus. J. Virol. 66:743-749.
26. Law, H. K., C. Y. Cheung, H. Y. Ng, S. F. Sia, Y. O. Chan, W. Luk, J. M. Nicholls, J. S. Peiris, and Y. L. Lau. 2005. Chemokine upregulation in SARS coronavirus infected human monocyte derived dendritic cells. Blood 106: 2366-2376.
27. Lee, S. M., and S. B. Kleiboeker. 2005. Porcine arterivirus activates the NF-kappaB pathway through IkappaB degradation. Virology 342:47-59.
28. Maniatis, T., J. V. Falvo, T. H. Kim, T. K. Kim, C. H. Lin, B. S. Parekh, and M. G. Wathelet. 1998. Structure and function of the interferon-beta enhanceosome. Cold Spring Harbor Symp. Quant. Biol. 63:609-620.
29. Matsumoto, M.. K. Funami, M. Tanabe, H. Oshiumi, M. Shingai, Y. Seto, A. Yamamoto, and T. Seya. 2003. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J. Immunol. 171:3154-3162.
30. May, M. J., and S. Ghosh. 1998. Signal transduction through NF-kappa B. Immunol. Today 19:80-88.
31. Meylan, E., J. Curran, K. Hofmann, D. Moradpour, M. Binder, R. Bartenschlager, and J. Tschopp. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172.
32. Milone, M. C., and P. Fitzgerald-Bocarsly. 1998. The mannose receptor mediates induction of IFN-alpha in peripheral blood dendritic cells by enveloped RNA and DNA viruses. J. Immunol. 161:2391-2399.
33. Muller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
34. Ontiveros, E., T. S. Kim, T. M. Gallagher, and S. Perlman. 2003. 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. 77:10260-10269.
35. Ontiveros, E., L. Kuo, P. S. Masters, and S. Perlman. 2001. Inactivation of expression of gene 4 of mouse hepatitis virus strain JHM does not affect virulence in the murine CNS. Virology 290:230-238.
36. Pedersen, K. W., Y. van der Meer, N. Roos, and E. J. Snijder. 1999. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J. Virol. 73:2016-2026.
37. Peng, T., S. Kotla, R. E. Bumgarner, and K. E. Gustin. 2006. Human rhinovirus attenuates the type 1 interferon response by disrupting activation of interferon regulatory factor 3. J. Virol. 80:5021-5031.
38. Perlman, S., and D. Ries. 1987. The astrocyte is a target cell in mice persistently infected with mouse hepatitis virus, strain JHM. Microb. Pathog. 3:309-314.
39. Perlman, S., D. Ries, E. Bolger, L. J. Chang, and C. M. Stoltrfus. 1986. MHV nucleocapsid synthesis in the presence of cycloheximide and accumulation of negative strand MHV RNA. Virus Res. 6:261-272.
40. Perry, A. K., G. Chen, D. Zheng, H. Tang, and G. Cheng. 2005. The host type I interferon response to viral and bacterial infections. Cell Res. 15:407-422.
41. Pewe, L., H. Zhou, J. Netland, C. Tangadu, H. Olivares, L. Shi, D. Look, T. M. Gallagher, and S. Perlman. 2005. A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. J. Virol. 79:11335-11342.
42. Prentice, E., W. G. Jerome, T. Yoshimori, N. Mizushima, and M. R. Denison. 2004. Coronavirus replication complex formation utilizes components of cellular autophagy. J. Biol. Chem. 279:10136-10141.
43. 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.
44. Sarkar, S. N., and G. C. Sen. 2004. Novel functions of proteins encoded by viral stress-inducible genes. Pharmacol. Ther. 103:245-259.
45. Schwartz, M., J. Chen, M. Janda, M. Sullivan, J. den Boon, and P. Ahlquist. 2002. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell 9:505-514.
46. Schwartz, M., J. Chen, W. M. Lee, M. Janda, and P. Ahlquist. 2004. Alternate, virus-induced membrane rearrangements support positive-strand RNA virus genome replication. Proc. Natl. Acad. Sci. USA 101:11263-11268.
47. Schwarz, B., E. Routledge, and S. G. Siddell. 1990. Murine coronavirus nonstructural protein ns2 is not essential for virus replication in transformed cells. J. Virol. 64:4784-4791.
48. Seth, R. B., L. Sun, C. K. Ea, and Z. J. Chen. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122:669-682.
49. Siddell, S., H. Wege, A. Barthel, and V. ter Meulen. 1981. Coronavirus JHM: intracellular protein synthesis. J. Gen. Virol. 53:145-155.
50. Sims, A. C., J. Ostermann, and M. R. Denison. 2000. Mouse hepatitis virus replicase proteins associate with two distinct populations of intracellular membranes. J. Virol. 74:5647-5654.
51. Snijder, E. J., Y. van der Meer, J. Zevenhoven-Dobbe, J. J. underwater, J. van der Meulen, H. K. Koerten, and A. M. Mommaas. 2006. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J. Virol. 80:5927-5940.
52. Spann, K. M., K. C. Tran, and P. L. Collins. 2005. Effects of nonstructural proteins NS1 and NS2 of human respiratory syncytial virus on Interferon regulatory factor 3, NF-κB, and proinflammatory cytokines. J. Virol. 79: 5353-5362.
53. 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.
54. Tabeta, K., P. Georgel, E. Janssen, X. Du, K. Hoebe, K. Crozat, S. Mudd, L. Shamel, S. Sovath, J. Goode, L. Alexopoulou, R. A. Flavell, and B. Beutler. 2004. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 101:3516-3521.
55. van der Meer, Y., E. J. Snijder, J. C. Dobbe, S. Schleich, M. R. Denison, W. J. Spaan, and J. K. Locker. 1999. Localization of mouse hepatitis virus non-structural proteins and RNA synthesis indicates a role for late endosomes in viral replication. J. Virol. 73:7641-7657.
56. 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.
57. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIP in the MyD88-independent toll-like receptor signaling pathway. Science 301:640-643.
58. Yang, H., G. Ma, C. H. Lin, M. Orr, and M. G. Wathelet. 2004. Mechanism for transcriptional synergy between interferon regulatory factor (IRF)-3 and IRF-7 in activation of the interferon-beta gene promoter. Eur. J. Biochem. 271:3693-3703.
59. Yokomori, K., and M. M. C. Lai. 1991. Mouse hepatitis virus S RNA sequence reveals that nonstructural protein ns4 and ns5a are not essential for murine coronavirus replication. J. Virol. 65:5605-5608.
60. Yoneyama, M., M. Kikuchi, K. Matsumoto, T. Imaizumi, M. Miyagishi, K. Taira, E. Foy, Y. M. Loo, M. Gale, Jr., S. Akira, S. Yonehara, A. Kato, and T. Fujita. 2005. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175: 2851-2858.
61. 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.
62. Zhou, H., and S. Perlman. 2006. Preferential infection of mature dendritic cells by mouse hepatitis virus strain JHM. J. Virol. 80:2506-2514.
63. Ziegler, T., S. Matikainen, E. Ronkko, P. Osterlund, M. Sillanpaa, J. Siren, R. Fagerlund, M. Immonen, K. Melen, and I. Julkunen. 2005. Severe acute respiratory syndrome coronavirus fails to activate cytokine-mediated innate immune responses in cultured human monocyte-derived dendritic cells. J. Virol. 79:13800-13805.