Cell-type-specific type I interferon antagonism influences organ tropism of murine coronavirus

Journal of Virology

Volumn 85, Issue 19, 2011, Pages 10058-10068

  Zhao, Ling ^a   Rose, Kristine M ^a   Elliott, Ruth ^a   van Rooijen, Nico ^b   Weiss, Susan R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; INTERFERON; INTERFERON RECEPTOR; NONSTRUCTURAL PROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; FIBROBLAST; IN VITRO STUDY; IN VIVO STUDY; INTERFERON INDUCTION; INTERFERON PRODUCTION; LIVER; MACROPHAGE; MOUSE; MURINE HEPATITIS CORONAVIRUS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; VIRAL TROPISM; VIRUS REPLICATION; VIRUS VIRULENCE;

ANIMALS; CELLS, CULTURED; CORONAVIRUS INFECTIONS; FIBROBLASTS; HEPATITIS, VIRAL, ANIMAL; INTERFERON TYPE I; LEUKOCYTE REDUCTION PROCEDURES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MURINE HEPATITIS VIRUS; RECEPTOR, INTERFERON ALPHA-BETA; RODENT DISEASES; VIRAL NONSTRUCTURAL PROTEINS; VIRAL TROPISM;

MURINE HEPATITIS VIRUS; MUS;

EID: 80053932661     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05075-11     Document Type: Article

References (50)

1. Bender, S. J., J. M. Phillips, E. P. Scott, and S. R. Weiss. 2010. Murine coronavirus receptors are differentially expressed in the central nervous system and play virus strain-dependent roles in neuronal spread. J. Virol. 84:11030-11044.
2. Bender, S. J., and S. R. Weiss. 2010. Pathogenesis of murine coronavirus in the central nervous system. J. Neuroimmune Pharmacol. 5:336-354.
3. Caamano, J., J. Alexander, L. Craig, R. Bravo, and C. A. Hunter. 1999. The NF-kappa B family member RelB is required for innate and adaptive immunity to Toxoplasma gondii. J. Immunol. 163:4453-4461.
4. Cervantes-Barragan, L., et al. 2009. Type I IFN-mediated protection of macrophages and dendritic cells secures control of murine coronavirus infection. J. Immunol. 182:1099-1106.
5. Cervantes-Barragan, L., et al. 2007. Control of coronavirus infection through plasmacytoid dendritic-cell-derived type I interferon. Blood 109: 1131-1137.
6. Cheon, H., and G. R. Stark. 2009. Unphosphorylated STAT1 prolongs the expression of interferon-induced immune regulatory genes. Proc. Natl. Acad. Sci. U. S. A. 106:9373-9378.
7. Cowley, T. J., S. Y. Long, and S. R. Weiss. 2010. The murine coronavirus nucleocapsid gene is a determinant of virulence. J. Virol. 84:1752-1763.
8. De Albuquerque, N., et al. 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.
9. de Veer, M. J., et al. 2001. Functional classification of interferon-stimulated genes identified using microarrays. J. Leukoc. Biol. 69:912-920.
10. Fraser, I. D., et al. 1998. A novel lipid-anchored A-kinase anchoring protein facilitates cAMP-responsive membrane events. EMBO J. 17:2261-2272.
11. Frieman, M., M. Heise, and R. Baric. 2008. SARS coronavirus and innate immunity. Virus Res. 133:101-112.
12. 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.
13. Hingley, S. T., J. L. Gombold, E. Lavi, and S. R. Weiss. 1994. MHV-A59 fusion mutants are attenuated and display altered hepatotropism. Virology 200:1-10.
14. Ida-Hosonuma, M., et al. 2005. The alpha/beta interferon response controls tissue tropism and pathogenicity of poliovirus. J. Virol. 79:4460-4469.
15. Kamitani, W., et al. 2006. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc. Natl. Acad. Sci. U. S. A. 103:12885-12890.
16. Kim, H. J., et al. 1999. Activating signal cointegrator 1, a novel transcription coactivator of nuclear receptors, and its cytosolic localization under conditions of serum deprivation. Mol. Cell. Biol. 19:6323-6332.
17. Koetzner, C. A., et al. 2010. Accessory protein 5a is a major antagonist of the antiviral action of interferon against murine coronavirus. J. Virol. 84:8262-8274.
18. Kuri, T., et al. 2009. Interferon priming enables cells to partially overturn the SARS coronavirus-induced block in innate immune activation. J. Gen. Virol. 90:2686-2694.
19. Lang, P. A., et al. 2010. Tissue macrophages suppress viral replication and prevent severe immunopathology in an interferon-I-dependent manner in mice. Hepatology 52:25-32.
20. Mazumder, R., L. M. Iyer, S. Vasudevan, and L. Aravind. 2002. Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily. Nucleic Acids Res. 30:5229-5243.
21. Navas, S., et al. 2001. Murine coronavirus spike protein determines the ability of the virus to replicate in the liver and cause hepatitis. J. Virol. 75:2452-2457.
22. Navas, S., and S. R. Weiss. 2003. Murine coronavirus-induced hepatitis: JHM genetic background eliminates A59 spike-determined hepatotropism. J. Virol. 77:4972-4978.
23. Navas-Martin, S., et al. 2007. Replicase genes of murine coronavirus strains A59 and JHM are interchangeable: differences in pathogenesis map to the 3 one third of the genome. J. Virol. 81:1022-1026.
24. Park, M. S., A. Garcia-Sastre, J. F. Cros, C. F. Basler, and P. Palese. 2003. Newcastle disease virus V protein is a determinant of host range restriction. J. Virol. 77:9522-9532.
25. 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.
26. Phillips, J. J., M. M. Chua, G. F. Rall, and S. R. Weiss. 2002. Murine coronavirus spike glycoprotein mediates degree of viral spread, inflammation, and virus-induced immunopathology in the central nervous system. Virology 301:109-120.
27. Phipps-Yonas, H., J. Seto, S. C. Sealfon, T. M. Moran, and A. Fernandez-Sesma. 2008. Interferon-beta pretreatment of conventional and plasmacytoid human dendritic cells enhances their activation by influenza virus. PLoS Pathog. 4:e1000193.
28. Racanelli, V., and B. Rehermann. 2006. The liver as an immunological organ. Hepatology 43:S54-S62.
29. Rose, K. M., R. Elliott, L. Martinez-Sobrido, A. Garcia-Sastre, and S. R. Weiss. 2010. Murine coronavirus delays expression of a subset of interferonstimulated genes. J. Virol. 84:5656-5669.
30. Rose, K. M., and S. R. Weiss. 2009. Murine coronavirus cell type dependent interaction with the type I interferon response. Viruses 1:689-712.
31. Roth-Cross, J. K., S. J. Bender, and S. R. Weiss. 2008. Murine coronavirus mouse hepatitis virus is recognized by MDA5 and induces type I interferon in brain macrophages/microglia. J. Virol. 82:9829-9838.
32. Roth-Cross, J. K., L. Martinez-Sobrido, E. P. Scott, A. Garcia-Sastre, and S. R. Weiss. 2007. Inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels. J. Virol. 81:7189-7199.
33. Roth-Cross, J. K., et al. 2009. Organ-specific attenuation of murine hepatitis virus strain A59 by replacement of catalytic residues in the putative viral cyclic phosphodiesterase ns2. J. Virol. 83:3743-3753.
34. Sasaki, A., et al. 1999. Cytokine-inducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells 4:339-351.
35. Scherbik, S. V., B. M. Stockman, and M. A. Brinton. 2007. Differential expression of interferon (IFN) regulatory factors and IFN-stimulated genes at early times after West Nile virus infection of mouse embryo fibroblasts. J. Virol. 81:12005-12018.
36. 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.
37. Seki, E., et al. 2007. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat. Med. 13:1324-1332.
38. Selmi, C., I. R. Mackay, and M. E. Gershwin. 2007. The immunological milieu of the liver. Semin. Liver Dis. 27:129-139.
39. Snijder, E. J., et al. 2003. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331:991-1004.
40. Tenoever, B. R., et al. 2007. Multiple functions of the IKK-related kinase IKKepsilon in interferon-mediated antiviral immunity. Science 315:1274-1278.
41. van Boxel-Dezaire, A. H., M. R. Rani, and G. R. Stark. 2006. Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 25:361-372.
42. Van Rooijen, N., and A. Sanders. 1996. Kupffer cell depletion by liposomedelivered drugs: comparative activity of intracellular clodronate, propamidine, and EDTA. Hepatology 23:1239-1243.
43. 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.
44. 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.
45. 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.
46. Zheng, D., G. Chen, B. Guo, G. Cheng, and H. Tang. 2008. PLP2, a potent deubiquitinase from murine hepatitis virus, strongly inhibits cellular type I interferon production. Cell Res. 18:1105-1113.
47. 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.
48. Zurney, J., T. Kobayashi, G. H. Holm, T. S. Dermody, and B. Sherry. 2009. Reovirus mu2 protein inhibits interferon signaling through a novel mechanism involving nuclear accumulation of interferon regulatory factor 9. J. Virol. 83:2178-2187.
49. Zust, R., et al. 2011. Ribose 2 -O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol. 12:137-143.
50. Zust, R., et al. 2007. Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines. PLoS Pathog. 3:e109.