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PMID: 18305050 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells.

Journal of virology ·Vol. 82 ·No. 9 ·2008-05-00 ·Pages 4471-9

Narayanan K, Huang C, Lokugamage K, Kamitani W, Ikegami T, Tseng CT, Makino S

Abstract

The severe acute respiratory syndrome coronavirus (SARS-CoV) nsp1 protein has unique biological functions that have not been described in the viral proteins of any RNA viruses; expressed SARS-CoV nsp1 protein has been found to suppress host gene expression by promoting host mRNA degradation and inhibiting translation. We generated an nsp1 mutant (nsp1-mt) that neither promoted host mRNA degradation nor suppressed host protein synthesis in expressing cells. Both a SARS-CoV mutant virus, encoding the nsp1-mt protein (SARS-CoV-mt), and a wild-type virus (SARS-CoV-WT) replicated efficiently and exhibited similar one-step growth kinetics in susceptible cells. Both viruses accumulated similar amounts of virus-specific mRNAs and nsp1 protein in infected cells, whereas the amounts of endogenous host mRNAs were clearly higher in SARS-CoV-mt-infected cells than in SARS-CoV-WT-infected cells, in both the presence and absence of actinomycin D. Further, SARS-CoV-WT replication strongly inhibited host protein synthesis, whereas host protein synthesis inhibition in SARS-CoV-mt-infected cells was not as efficient as in SARS-CoV-WT-infected cells. These data revealed that nsp1 indeed promoted host mRNA degradation and contributed to host protein translation inhibition in infected cells. Notably, SARS-CoV-mt infection, but not SARS-CoV-WT infection, induced high levels of beta interferon (IFN) mRNA accumulation and high titers of type I IFN production. These data demonstrated that SARS-CoV nsp1 suppressed host innate immune functions, including type I IFN expression, in infected cells and suggested that SARS-CoV nsp1 most probably plays a critical role in SARS-CoV virulence.

MeSH Terms
Cell Line Gene Expression Regulation Humans Interferon Type I/genetics Mutation Protein Biosynthesis RNA Stability RNA, Messenger/metabolism RNA-Dependent RNA Polymerase/physiology SARS Virus/pathogenicity,physiology Viral Nonstructural Proteins/physiology
Chemicals
Interferon Type I RNA, Messenger Viral Nonstructural Proteins Nsp1 protein, SARS coronavirus RNA-Dependent RNA Polymerase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Narayanan Krishna
Department of Microbiology and Immunology, The University of Texas Medical Branch at Galveston, Galveston, TX 77555-1019, USA. shmakino@utmb.edu
Huang Cheng
Lokugamage Kumari
Kamitani Wataru
Ikegami Tetsuro
Tseng Chien-Te K
Makino Shinji
References (57)
57 references, click to expand
  1. A cluster of cases of severe acute respiratory syndrome in Hong Kong.
    N Engl J Med. 2003 May 15;348(20):1977-85 PMID: 12671062
  2. Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase.
    J Virol. 2004 Jun;78(11):5619-32 PMID: 15140959
  3. Thermal aggregation of SARS-CoV membrane protein.
    J Virol Methods. 2005 Nov;129(2):152-61 PMID: 16023741
  4. Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus.
    J Virol. 2007 Jan;81(2):813-21 PMID: 17079315
  5. Novel beta-barrel fold in the nuclear magnetic resonance structure of the replicase nonstructural protein 1 from the severe acute respiratory syndrome coronavirus.
    J Virol. 2007 Apr;81(7):3151-61 PMID: 17202208
  6. Severe acute respiratory syndrome coronavirus fails to activate cytokine-mediated innate immune responses in cultured human monocyte-derived dendritic cells.
    J Virol. 2005 Nov;79(21):13800-5 PMID: 16227300
  7. Control of coronavirus infection through plasmacytoid dendritic-cell-derived type I interferon.
    Blood. 2007 Feb 1;109(3):1131-7 PMID: 16985170
  8. The severe acute respiratory syndrome coronavirus Nsp15 protein is an endoribonuclease that prefers manganese as a cofactor.
    J Virol. 2004 Nov;78(22):12218-24 PMID: 15507608
  9. The interaction of cytoplasmic RNA viruses with the nucleus.
    Virus Res. 2003 Sep;95(1-2):75-85 PMID: 12921997
  10. 7a protein of severe acute respiratory syndrome coronavirus inhibits cellular protein synthesis and activates p38 mitogen-activated protein kinase.
    J Virol. 2006 Jan;80(2):785-93 PMID: 16378980
  11. Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus.
    J Biol Chem. 2007 Nov 2;282(44):32208-21 PMID: 17761676
  12. A novel coronavirus associated with severe acute respiratory syndrome.
    N Engl J Med. 2003 May 15;348(20):1953-66 PMID: 12690092
  13. Subversion of innate host antiviral strategies by the hepatitis C virus.
    Arch Biochem Biophys. 2007 Jun 15;462(2):254-65 PMID: 17467654
  14. Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human Angiotensin-converting enzyme 2 virus receptor.
    J Virol. 2007 Feb;81(3):1162-73 PMID: 17108019
  15. Comparative host gene transcription by microarray analysis early after infection of the Huh7 cell line by severe acute respiratory syndrome coronavirus and human coronavirus 229E.
    J Virol. 2005 May;79(10):6180-93 PMID: 15858003
  16. Group 2 coronaviruses prevent immediate early interferon induction by protection of viral RNA from host cell recognition.
    Virology. 2007 Apr 25;361(1):18-26 PMID: 17316733
  17. Viruses know it all: new insights into IFN networks.
    Trends Immunol. 2005 Jul;26(7):396-401 PMID: 15922665
  18. Deubiquitination, a new function of the severe acute respiratory syndrome coronavirus papain-like protease?
    J Virol. 2005 Apr;79(7):4550-1 PMID: 15767458
  19. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage.
    J Mol Biol. 2003 Aug 29;331(5):991-1004 PMID: 12927536
  20. Mouse hepatitis coronavirus A59 nucleocapsid protein is a type I interferon antagonist.
    J Virol. 2007 Mar;81(6):2554-63 PMID: 17182678
  21. Biosynthesis, purification, and substrate specificity of severe acute respiratory syndrome coronavirus 3C-like proteinase.
    J Biol Chem. 2004 Jan 16;279(3):1637-42 PMID: 14561748
  22. Inhibition of cytokine gene expression and induction of chemokine genes in non-lymphatic cells infected with SARS coronavirus.
    Virol J. 2006 Mar 29;3:17 PMID: 16571117
  23. Toll-like receptors, RIG-I-like RNA helicases and the antiviral innate immune response.
    Immunol Cell Biol. 2007 Aug-Sep;85(6):435-45 PMID: 17667934
  24. Severe acute respiratory syndrome coronavirus 3a protein is a viral structural protein.
    J Virol. 2005 Mar;79(5):3182-6 PMID: 15709039
  25. Interaction of severe acute respiratory syndrome-associated coronavirus with dendritic cells.
    J Gen Virol. 2006 Jul;87(Pt 7):1953-1960 PMID: 16760397
  26. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase?
    J Virol. 2004 Feb;78(3):1063-8 PMID: 14722261
  27. Cytokine responses in severe acute respiratory syndrome coronavirus-infected macrophages in vitro: possible relevance to pathogenesis.
    J Virol. 2005 Jun;79(12):7819-26 PMID: 15919935
  28. A human in vitro model system for investigating genome-wide host responses to SARS coronavirus infection.
    BMC Infect Dis. 2004 Sep 09;4:34 PMID: 15357874
  29. Mouse hepatitis virus does not induce Beta interferon synthesis and does not inhibit its induction by double-stranded RNA.
    J Virol. 2007 Jan;81(2):568-74 PMID: 17079305
  30. Identification of a novel coronavirus in patients with severe acute respiratory syndrome.
    N Engl J Med. 2003 May 15;348(20):1967-76 PMID: 12690091
  31. TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus.
    Cell. 2004 Feb 20;116(4):541-50 PMID: 14980221
  32. Identification of severe acute respiratory syndrome in Canada.
    N Engl J Med. 2003 May 15;348(20):1995-2005 PMID: 12671061
  33. Discovery of an RNA virus 3'->5' exoribonuclease that is critically involved in coronavirus RNA synthesis.
    Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):5108-13 PMID: 16549795
  34. 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. 2005 Feb;79(4):2079-86 PMID: 15681410
  35. Assay of human interferon in Vero cells by several methods.
    J Clin Microbiol. 1979 Apr;9(4):471-5 PMID: 222803
  36. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation.
    Proc Natl Acad Sci U S A. 2006 Aug 22;103(34):12885-90 PMID: 16912115
  37. The U(L)41 protein of herpes simplex virus 1 degrades RNA by endonucleolytic cleavage in absence of other cellular or viral proteins.
    Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2827-32 PMID: 16477041
  38. Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins.
    J Virol. 2004 Sep;78(18):9977-86 PMID: 15331731
  39. Translational control in murine hepatitis virus infection.
    J Gen Virol. 1986 May;67 ( Pt 5):923-32 PMID: 3009691
  40. Inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels.
    J Virol. 2007 Jul;81(13):7189-99 PMID: 17459917
  41. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus.
    Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12995-3000 PMID: 14569023
  42. Chemokine up-regulation in SARS-coronavirus-infected, monocyte-derived human dendritic cells.
    Blood. 2005 Oct 1;106(7):2366-74 PMID: 15860669
  43. mRNA degradation by the virion host shutoff (Vhs) protein of herpes simplex virus: genetic and biochemical evidence that Vhs is a nuclease.
    J Virol. 2002 Sep;76(17):8560-71 PMID: 12163576
  44. Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists.
    J Virol. 2007 Jan;81(2):548-57 PMID: 17108024
  45. The innate antiviral response: new insights into a continuing story.
    Adv Virus Res. 2007;69:1-66 PMID: 17222691
  46. Mechanisms and enzymes involved in SARS coronavirus genome expression.
    J Gen Virol. 2003 Sep;84(Pt 9):2305-2315 PMID: 12917450
  47. Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines.
    PLoS Pathog. 2007 Aug 10;3(8):e109 PMID: 17696607
  48. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity.
    J Virol. 2005 Dec;79(24):15189-98 PMID: 16306590
  49. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice.
    PLoS Pathog. 2007 Jan;3(1):e5 PMID: 17222058
  50. Signaling pathways activated by microorganisms.
    Curr Opin Cell Biol. 2007 Apr;19(2):185-91 PMID: 17303405
  51. Genetic evidence for an interferon-antagonistic function of rift valley fever virus nonstructural protein NSs.
    J Virol. 2001 Feb;75(3):1371-7 PMID: 11152510
  52. The coronavirus replicase: insights into a sophisticated enzyme machinery.
    Adv Exp Med Biol. 2006;581:3-11 PMID: 17037497
  53. Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid.
    J Virol. 1980 Jan;33(1):449-62 PMID: 6245243
  54. Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain.
    J Virol. 2007 Nov;81(21):11620-33 PMID: 17715225
  55. Synthetic reconstruction of zoonotic and early human severe acute respiratory syndrome coronavirus isolates that produce fatal disease in aged mice.
    J Virol. 2007 Jul;81(14):7410-23 PMID: 17507479
  56. The papain-like protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme.
    J Virol. 2005 Dec;79(24):15199-208 PMID: 16306591
  57. The nsp2 replicase proteins of murine hepatitis virus and severe acute respiratory syndrome coronavirus are dispensable for viral replication.
    J Virol. 2005 Nov;79(21):13399-411 PMID: 16227261
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
1098-5514
Published
2008-05-00
Epub
2008-00-27
Pages
4471-9
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC2293030
Subset
IM
Grants
NIAID NIH HHS · AI72493 · United States
NIAID NIH HHS · R01 AI072493 · United States
NIAID NIH HHS · AI29984 · United States
NIAID NIH HHS · R21 AI029984 · United States
NIAID NIH HHS · R01 AI029984 · United States
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