Interferon and cytokine responses to SARS-coronavirus infection

Cytokine and Growth Factor Reviews

Volumn 19, Issue 2, 2008, Pages 121-132

  Thiel, Volker ^a   Weber, Friedemann ^b  

^a CANTONAL HOSPITAL ST GALLEN   (Switzerland)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Chemokines; Coronaviruses; Interferon; SARS; Viral countermeasures

Indexed keywords

ALPHA INTERFERON; ANTIVIRUS AGENT; BETA INTERFERON; CHEMOKINE; CYTOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 5; INTERLEUKIN 8;

ADAPTIVE IMMUNITY; CELL INFILTRATION; DISEASE SEVERITY; HUMAN; IN VIVO STUDY; INNATE IMMUNITY; INTERFERON INDUCTION; PRIORITY JOURNAL; REVIEW; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; SIGNAL TRANSDUCTION; VIREMIA;

ANIMALS; CORONAVIRUS INFECTIONS; CYTOKINES; HUMANS; IMMUNE SYSTEM; IMMUNITY, NATURAL; INTERFERONS; MODELS, BIOLOGICAL; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME;

CORONAVIRIDAE; CORONAVIRUS; SARS CORONAVIRUS;

EID: 40849119477     PISSN: 13596101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2008.01.001     Document Type: Review

References (181)

1. Siddell S.G., Ziebuhr J., and Snijder E.J. Coronaviruses, toroviruses, and arteriviruses. In: Mahy B.W.J., and ter Meulen V. (Eds). Topley and Wilson's microbiology and microbial infections (2005), Hodder Arnold, London 823-856
2. Weiss S.R., and Navas-Martin S. Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol Mol Biol Rev 69 (2005) 635-664
3. Fouchier R.A., Kuiken T., Schutten M., van Amerongen G., van Doornum G.J., van den Hoogen B.G., et al. Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423 (2003) 240
4. Marra M.A., Jones S.J., Astell C.R., Holt R.A., Brooks-Wilson A., Butterfield Y.S., et al. The Genome sequence of the SARS-associated coronavirus. Science 300 (2003) 1399-1404
5. Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., et al. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300 (2003) 1394-1399
6. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J.H., et al. Bats are natural reservoirs of SARS-like coronaviruses. Science 310 (2005) 676-679
7. Perlman S., and Dandekar A.A. Immunopathogenesis of coronavirus infections: implications for SARS. Nat Rev Immunol 5 (2005) 917-927
8. Snijder E.J., Bredenbeek P.J., Dobbe J.C., Thiel V., Ziebuhr J., Poon L.L., et al. 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 (2003) 991-1004
9. Thiel V., Ivanov K.A., Putics A., Hertzig T., Schelle B., Bayer S., et al. Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol 84 (2003) 2305-2315
10. Gorbalenya A.E., Enjuanes L., Ziebuhr J., and Snijder E.J. Nidovirales: evolving the largest RNA virus genome. Virus Res 117 (2006) 17-37
11. Ziebuhr J. The coronavirus replicase. Curr Top Microbiol Immunol 287 (2005) 57-94
12. Sawicki S.G., Sawicki D.L., and Siddell S.G. A contemporary view of coronavirus transcription. J Virol 81 (2006) 20-29
13. Almazan F., Galan C., and Enjuanes L. The nucleoprotein is required for efficient coronavirus genome replication. J Virol 78 (2004) 12683-12688
14. Schelle B., Karl N., Ludewig B., Siddell S.G., and Thiel V. Selective replication of coronavirus genomes that express nucleocapsid protein. J Virol 79 (2005) 6620-6630
15. Ziebuhr J., and Snijder E. The coronavirus replicase gene: special enzymes for special viruses. In: Thiel V. (Ed). Coronaviruses: molecular and cellular biology (2007), Caister scientific press, Norwich, UK
16. Gorbalenya A.E., Snijder E.J., and Spaan W.J. Severe acute respiratory syndrome coronavirus phylogeny: toward consensus. J Virol 78 (2004) 7863-7866
17. Bergmann C.C., Lane T.E., and Stohlman S.A. Coronavirus infection of the central nervous system: host-virus stand-off. Nat Rev Microbiol 4 (2006) 121-132
18. Hemmila E., Turbide C., Olson M., Jothy S., Holmes K.V., and Beauchemin N. Ceacam1a-/- mice are completely resistant to infection by murine coronavirus mouse hepatitis virus A59. J Virol 78 (2004) 10156-10165
19. Barthold S.W., Beck D.S., and Smith A.L. Enterotropic coronavirus (mouse hepatitis virus) in mice: influence of host age and strain on infection and disease. Lab Anim Sci 43 (1993) 276-284
20. De Albuquerque N., Baig E., Ma X., Zhang J., He W., Rowe A., et al. Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice. J Virol 80 (2006) 10382-10394
21. Homberger F.R. Enterotropic mouse hepatitis virus. Lab Anim 31 (1997) 97-115
22. Homberger F.R., Zhang L., and Barthold S.W. Prevalence of enterotropic and polytropic mouse hepatitis virus in enzootically infected mouse colonies. Lab Anim Sci 48 (1998) 50-54
23. Sarma J.D., Fu L., Hingley S.T., and Lavi E. Mouse hepatitis virus type-2 infection in mice: an experimental model system of acute meningitis and hepatitis. Exp Mol Pathol 71 (2001) 1-12
24. Falsey A.R., McCann R.M., Hall W.J., Criddle M.M., Formica M.A., Wycoff D., et al. The "common cold" in frail older persons: impact of rhinovirus and coronavirus in a senior daycare center. J Am Geriatr Soc 45 (1997) 706-711
25. van der Hoek L., Pyrc K., and Berkhout B. Human coronavirus NL63, a new respiratory virus. FEMS Microbiol Rev 30 (2006) 760-773
26. van der Hoek L., Sure K., Ihorst G., Stang A., Pyrc K., Jebbink M.F., et al. Croup is associated with the novel coronavirus NL63. PLoS Med 2 (2005) e240
27. Haller O., Kochs G., and Weber F. The interferon response circuit: Induction and suppression by pathogenic viruses. Virology 344 (2006) 119-130
28. Samuel C.E. Antiviral actions of interferons. Clin Microbiol Rev 14 (2001) 778-809
29. Weber F., Kochs G., and Haller O. Inverse interference: how viruses fight the interferon system. Viral Immunol 17 (2004) 498-515
30. Hertzog P.J., O'Neill L.A., and Hamilton J.A. The interferon in TLR signaling: more than just antiviral. Trends Immunol 24 (2003) 534-539
31. Le Bon A., and Tough D.F. Links between innate and adaptive immunity via type I interferon. Curr Opin Immunol 14 (2002) 432-436
32. Stark G.R., Kerr I.M., Williams B.R., Silverman R.H., and Schreiber R.D. How cells respond to interferons. Annu Rev Biochem 67 (1998) 227-264
33. Roberts R.M., Ezashi T., Rosenfeld C.S., Ealy A.D., and Kubisch H.M. Evolution of the interferon tau genes and their promoters, and maternal-trophoblast interactions in control of their expression. Reprod Suppl 61 (2003) 239-251
34. van Pesch V., Lanaya H., Renauld J.C., and Michiels T. Characterization of the murine alpha interferon gene family. J Virol 78 (2004) 8219-8228
35. van Pesch V., and Michiels T. Characterization of interferon-alpha 13, a novel constitutive murine interferon-alpha subtype. J Biol Chem 278 (2003) 46321-46328
36. Delhaye S., Paul S., Blakqori G., Minet M., Weber F., Staeheli P., et al. Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci USA 103 (2006) 7835-7840
37. Marie I., Durbin J.E., and Levy D.E. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J 17 (1998) 6660-6669
38. Colonna M., Krug A., and Cella M. Interferon-producing cells: on the front line in immune responses against pathogens. Curr Opin Immunol 14 (2002) 373-379
39. Diebold S.S., Montoya M., Unger H., Alexopoulou L., Roy P., Haswell L.E., et al. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 424 (2003) 324-328
40. Hornung V., Ellegast J., Kim S., Brzozka K., Jung A., Kato H., et al. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314 (2006) 994-997
41. Pichlmair A., Schulz O., Tan C.P., Naslund T.I., Liljestrom P., Weber F., et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′ phosphates. Science 314 (2006) 997-1001
42. Plumet S., Herschke F., Bourhis J.M., Valentin H., Longhi S., and Gerlier D. Cytosolic 5′-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS ONE 2 (2007) e279
43. Weber F., Wagner V., Rasmussen S.B., Hartmann R., and Paludan S.R. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 80 (2006) 5059-5064
44. Andrejeva J., Childs K.S., Young D.F., Carlos T.S., Stock N., Goodbourn S., et al. 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 (2004) 17264-17269
45. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441 (2006) 101-105
46. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5 (2004) 730-737
47. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., et al. Shared and unique functions of the DExD/H-Box Helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175 (2005) 2851-2858
48. Gitlin L., Barchet W., Gilfillan S., Cella M., Beutler B., Flavell R.A., et al. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci USA 103 (2006) 8459-8464
49. Fitzgerald K.A., McWhirter S.M., Faia K.L., Rowe D.C., Latz E., Golenbock D.T., et al. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4 (2003) 491-496
50. Sharma S., TenOever B.R., Grandvaux N., Zhou G.P., Lin R., and Hiscott J. Triggering the interferon antiviral response through an IKK-related pathway. Science 300 (2003) 1148-1151
51. Ozato K., Tailor P., and Kubota T. The interferon regulatory factor family in host defense: the mechanism of action. J Biol Chem 282 (2007) 20065-20069
52. Paun A., and Pitha P.M. The IRF family, revisited. Biochimie 89 (2007) 744-753
53. Hiscott J. Triggering the innate antiviral response through IRF-3 activation. J Biol Chem 282 (2007) 15325-15329
54. Sato M., Suemori H., Hata N., Asagiri M., Ogasawara K., Nakao K., et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13 (2000) 539-548
55. Iwamura T., Yoneyama M., Yamaguchi K., Suhara W., Mori W., Shiota K., et al. Induction of IRF-3/-7 kinase and NF-kappaB in response to double- stranded RNA and virus infection: common and unique pathways. Genes Cells 6 (2001) 375-388
56. tenOever B.R., Sharma S., Zou W., Sun Q., Grandvaux N., Julkunen I., et al. Activation of TBK1 and IKK epsilon kinases by vesicular stomatitis virus infection and the role of viral ribonucleoprotein in the development of interferon antiviral immunity. J Virol 78 (2004) 10636-10649
57. Chu W.M., Ostertag D., Li Z.W., Chang L., Chen Y., Hu Y., et al. JNK2 and IKKbeta are required for activating the innate response to viral infection. Immunity 11 (1999) 721-731
58. Paladino P., Cummings D.T., Noyce R.S., and Mossman K.L. The IFN-independent response to virus particle entry provides a first line of antiviral defense that is independent of TLRs and retinoic acid-inducible gene I. J Immunol 177 (2006) 8008-8016
59. Alexopoulou L., Holt A.C., Medzhitov R., and Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 (2001) 732-738
60. Iwasaki A., and Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 5 (2004) 987-995
61. Uematsu S., and Akira S. Toll-like receptors and type I interferons. J Biol Chem 282 (2007) 15319-15323
62. Kerkmann M., Rothenfusser S., Hornung V., Towarowski A., Wagner M., Sarris A., et al. Activation with CpG-A and CpG-B oligonucleotides reveals two distinct regulatory pathways of type I IFN synthesis in human plasmacytoid dendritic cells. J Immunol 170 (2003) 4465-4474
63. Prakash A., Smith E., Lee C.K., and Levy D.E. Tissue-specific positive feedback requirements for production of type I interferon following virus infection. J Biol Chem 280 (2005) 18651-18657
64. Asselin-Paturel C., and Trinchieri G. Production of type I interferons: plasmacytoid dendritic cells and beyond. J Exp Med 202 (2005) 461-465
65. Tsujimura H., Tamura T., and Ozato K. Cutting edge: IFN consensus sequence binding protein/IFN regulatory factor 8 drives the development of type I IFN-producing plasmacytoid dendritic cells. J Immunol 170 (2003) 1131-1135
66. Honda K., Ohba Y., Yanai H., Negishi H., Mizutani T., Takaoka A., et al. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434 (2005) 1035-1040
67. de Weerd N.A., Samarajiwa S.A., and Hertzog P.J. Type I interferon receptors: biochemistry and biological functions. J Biol Chem 282 (2007) 20053-20057
68. Levy D.E., and Darnell Jr. J.E. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3 (2002) 651-662
69. Schindler C., Levy D.E., and Decker T. JAK-STAT signaling: from interferons to cytokines. J Biol Chem 282 (2007) 20059-20063
70. Der S.D., Zhou A., Williams B.R., and Silverman R.H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 95 (1998) 15623-15628
71. Haller O., and Kochs G. Interferon-induced mx proteins: dynamin-like GTPases with antiviral activity. Traffic 3 (2002) 710-717
72. Haller O., Staeheli P., and Kochs G. Interferon-induced Mx proteins in antiviral host defense. Biochimie 89 (2007) 812-818
73. Kochs G., and Haller O. Interferon-induced human MxA GTPase blocks nuclear import of Thogoto virus nucleocapsids. Proc Natl Acad Sci USA 96 (1999) 2082-2086
74. Reichelt M., Stertz S., Krijnse-Locker J., Haller O., and Kochs G. Missorting of LaCrosse virus nucleocapsid protein by the interferon-induced MxA GTPase involves smooth ER membranes. Traffic 5 (2004) 772-784
75. Garcia M.A., Meurs E.F., and Esteban M. The dsRNA protein kinase PKR: virus and cell control. Biochimie 89 (2007) 799-811
76. Williams B.R. PKR; a sentinel kinase for cellular stress. Oncogene 18 (1999) 6112-6120
77. Hovanessian A.G., and Justesen J. The human 2′-5′oligoadenylate synthetase family: unique interferon-inducible enzymes catalyzing 2′-5′ instead of 3′-5′ phosphodiester bond formation. Biochimie 89 (2007) 779-788
78. Bisbal C., and Silverman R.H. Diverse functions of RNase L and implications in pathology. Biochimie 89 (2007) 789-798
79. Sarkar S.N., and Sen G.C. Novel functions of proteins encoded by viral stress-inducible genes. Pharmacol Ther 103 (2004) 245-259
80. Terenzi F., Pal S., and Sen G.C. Induction and mode of action of the viral stress-inducible murine proteins, P56 and P54. Virology 340 (2005) 116-124
81. Degols G., Eldin P., and Mechti N. ISG20, an actor of the innate immune response. Biochimie 89 (2007) 831-835
82. Espert L., Degols G., Gongora C., Blondel D., Williams B.R., Silverman R.H., et al. ISG20, a new interferon-induced RNase specific for single-stranded RNA, defines an alternative antiviral pathway against RNA genomic viruses. J Biol Chem 278 (2003) 16151-16158
83. Espert L., Degols G., Lin Y.L., Vincent T., Benkirane M., and Mechti N. Interferon-induced exonuclease ISG20 exhibits an antiviral activity against human immunodeficiency virus type 1. J Gen Virol 86 (2005) 2221-2229
84. Aurisicchio L., Delmastro P., Salucci V., Paz O.G., Rovere P., Ciliberto G., et al. Liver-specific alpha 2 interferon gene expression results in protection from induced hepatitis. J Virol 74 (2000) 4816-4823
85. Fuchizaki U., Kaneko S., Nakamoto Y., Sugiyama Y., Imagawa K., Kikuchi M., et al. Synergistic antiviral effect of a combination of mouse interferon-alpha and interferon-gamma on mouse hepatitis virus. J Med Virol 69 (2003) 188-194
86. Pei J., Sekellick M.J., Marcus P.I., Choi I.S., and Collisson E.W. Chicken interferon type I inhibits infectious bronchitis virus replication and associated respiratory illness. J Interferon Cytokine Res 21 (2001) 1071-1077
87. Cinatl J., Morgenstern B., Bauer G., Chandra P., Rabenau H., and Doerr H.W. Treatment of SARS with human interferons. Lancet 362 (2003) 293-294
88. Hensley L.E., Fritz L.E., Jahrling P.B., Karp C.L., Huggins J.W., and Geisbert T.W. Interferon-beta 1a and SARS coronavirus replication. Emerg Infect Dis 10 (2004) 317-319
89. Spiegel M., Pichlmair A., Mühlberger E., Haller O., and Weber F. The antiviral effect of interferon-beta against SARS-coronavirus is not mediated by MxA. J Clinical Virol 30 (2004) 211-213
90. Stroher U., DiCaro A., Li Y., Strong J.E., Aoki F., Plummer F., et al. Severe acute respiratory syndrome-related coronavirus is inhibited by interferon-alpha. J Infect Dis 189 (2004) 1164-1167
91. Zheng B., He M.L., Wong K.L., Lum C.T., Poon L.L., Peng Y., et al. Potent inhibition of SARS-associated coronavirus (SCOV) infection and replication by type I interferons (IFN-alpha/beta) but not by type II interferon (IFN-gamma). J Interferon Cytokine Res 24 (2004) 388-390
92. Cervantes-Barragan L., Zust R., Weber F., Spiegel M., Lang K.S., Akira S., et al. Control of coronavirus infection through plasmacytoid dendritic-cell-derived type I interferon. Blood 109 (2007) 1131-1137
93. Hogan R.J., Gao G., Rowe T., Bell P., Flieder D., Paragas J., et al. Resolution of primary severe acute respiratory syndrome-associated coronavirus infection requires Stat1. J Virol 78 (2004) 11416-11421
94. Haagmans B.L., Kuiken T., Martina B.E., Fouchier R.A., Rimmelzwaan G.F., Van Amerongen G., et al. Pegylated interferon-alpha protects type 1 pneumocytes against SARS coronavirus infection in macaques. Nat Med 10 (2004) 290-293
95. Zhou H., and Perlman S. Preferential infection of mature dendritic cells by the JHM strain of mouse hepatitis virus. Adv Exp Med Biol 581 (2006) 411-414
96. Stockman L.J., Bellamy R., and Garner P. SARS: systematic review of treatment effects. PLoS Med 3 (2006) e343
97. Loutfy M.R., Blatt L.M., Siminovitch K.A., Ward S., Wolff B., Lho H., et al. Interferon alfacon-1 plus corticosteroids in severe acute respiratory syndrome: a preliminary study. JAMA 290 (2003) 3222-3228
98. Pestka S. The interferons: 50 years after their discovery, there is much more to learn. J Biol Chem 282 (2007) 20047-20051
99. Akerstrom S., Mousavi-Jazi M., Klingstrom J., Leijon M., Lundkvist A., and Mirazimi A. Nitric oxide inhibits the replication cycle of severe acute respiratory syndrome coronavirus. J Virol 79 (2005) 1966-1969
100. 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 (2007) 18-26
101. Garcia-Sastre A., and Biron C.A. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312 (2006) 879-882
102. Spiegel M., Pichlmair A., Martinez-Sobrido L., Cros J., Garcia-Sastre A., Haller O., et al. 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 (2005) 2079-2086
103. Versteeg G.A., Slobodskaya O., and Spaan W.J. Transcriptional profiling of acute cytopathic murine hepatitis virus infection in fibroblast-like cells. J Gen Virol 87 (2006) 1961-1975
104. 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 (2007) 568-574
105. Cheung C.Y., Poon L.L., Ng I.H., Luk W., Sia S.F., Wu M.H., et al. Cytokine responses in severe acute respiratory syndrome coronavirus-infected macrophages in vitro: possible relevance to pathogenesis. J Virol 79 (2005) 7819-7826
106. Ziegler T., Matikainen S., Ronkko E., Osterlund P., Sillanpaa M., Siren J., et al. Severe acute respiratory syndrome coronavirus fails to activate cytokine-mediated innate immune responses in cultured human monocyte-derived dendritic cells. J Virol 79 (2005) 13800-13805
107. Spiegel M., and Weber F. Inhibition of cytokine gene expression and induction of chemokine genes in non-lymphatic cells infected with SARS coronavirus. Virol J 3 (2006) 17
108. Gosert R., Kanjanahaluethai A., Egger D., Bienz K., and Baker S.C. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 76 (2002) 3697-3708
109. Prentice E., Jerome W.G., Yoshimori T., Mizushima N., and Denison M.R. Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 279 (2004) 10136-10141
110. Snijder E.J., van der Meer Y., Zevenhoven-Dobbe J., Onderwater J.J., van der Meulen J., Koerten H.K., et al. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol 80 (2006) 5927-5940
111. Stertz S., Reichelt M., Spiegel M., Kuri T., Martinez-Sobrido L., Garcia-Sastre A., et al. The intracellular sites of early replication and budding of SARS-coronavirus. Virology 361 (2007) 304-315
112. 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 (2007) 7189-7199
113. Kopecky-Bromberg S.A., Martinez-Sobrido L., Frieman M., Baric R.A., and Palese P. Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J Virol 81 (2007) 548-557
114. Frieman M., Yount B., Heise M., Kopecky-Bromberg S.A., Palese P., and Baric R.S. SARSCoV ORF6 antagonizes STAT1 function by sequestering nuclear import factors on the rER/golgi membrane. J Virol 81 (2007) 9812-9824
115. Kopecky-Bromberg S.A., Martinez-Sobrido L., and Palese P. 7a protein of severe acute respiratory syndrome coronavirus inhibits cellular protein synthesis and activates p38 mitogen-activated protein kinase. J Virol 80 (2006) 785-793
116. Kamitani W., Narayanan K., Huang C., Lokugamage K., Ikegami T., Ito N., et al. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Natl Acad Sci USA 103 (2006) 12885-12890
117. Züst R., Cervantes-Barragan L., Kuri T., Blakqori G., Weber F., Ludewig B., et al. Identification of coronavirus non-structural protein 1 as a major pathogenicity factor-implications for the rational design of live attenuated coronavirus vaccines. PlOS Pathogens 3 (2007) e109
118. Weber F., and Haller O. Viral suppression of the interferon system. Biochimie 89 (2007) 836-842
119. 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 (2007) 2554-2563
120. Lee H.K., Lund J.M., Ramanathan B., Mizushima N., and Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315 (2007) 1398-1401
121. Taguchi F., and Siddell S.G. Difference in sensitivity to interferon among mouse hepatitis viruses with high and low virulence for mice. Virology 147 (1985) 41-48
122. Cameron M.J., Ran L., Xu L., Danesh A., Bermejo-Martin J.F., Cameron C.M., et al. Interferon-mediated immunopathological events are associated with atypical innate and adaptive immune responses in severe acute respiratory syndrome (SARS) patients. J Virol 81 (2007) 8692-8706
123. Ebihara H., Takada A., Kobasa D., Jones S., Neumann G., Theriault S., et al. Molecular determinants of Ebola virus virulence in mice. PLoS Pathog 2 (2006) e73
124. Kash J.C., Mühlberger E., Carter V., Grosch M., Perwitasari O., Proll S.C., et al. Global suppression of the host anti-viral response by Ebola and Marburg viruses: increased antagonism of the type I IFN response is associated with enhanced virulence. J Virol 80 (2006) 3009-3020
125. Lin R., Heylbroeck C., Genin P., Pitha P.M., and Hiscott J. Essential role of interferon regulatory factor 3 in direct activation of RANTES chemokine transcription. Mol Cell Biol 19 (1999) 959-966
126. Leung T.H., Hoffmann A., and Baltimore D. One nucleotide in a kappaB site can determine cofactor specificity for NF-kappaB dimers. Cell 118 (2004) 453-464
127. Cinatl Jr. J., Hoever G., Morgenstern B., Preiser W., Vogel J.U., Hofmann W.K., et al. Infection of cultured intestinal epithelial cells with severe acute respiratory syndrome coronavirus. Cell Mol Life Sci 61 (2004) 2100-2112
128. Stiles L.N., Hardison J.L., Schaumburg C.S., Whitman L.M., and Lane T.E. T cell antiviral effector function is not dependent on CXCL10 following murine coronavirus infection. J Immunol 177 (2006) 8372-8380
129. Cinatl Jr. J., Michaelis M., Morgenstern B., and Doerr H.W. High-dose hydrocortisone reduces expression of the pro-inflammatory chemokines CXCL8 and CXCL10 in SARS coronavirus-infected intestinal cells. Int J Mol Med 15 (2005) 323-327
130. 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 (2005) 4369-4381
131. Frieman M., Heise M., and Baric R. SARS coronavirus and innate immunity. Virus Res (2007)
132. Barnes B.J., Moore P.A., and Pitha P.M. Virus-specific activation of a novel interferon regulatory factor, IRF-5, results in the induction of distinct interferon alpha genes. J Biol Chem 276 (2001) 23382-23390
133. Takaoka A., Yanai H., Kondo S., Duncan G., Negishi H., Mizutani T., et al. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434 (2005) 243-249
134. Chang Y.J., Liu C.Y., Chiang B.L., Chao Y.C., and Chen C.C. Induction of IL-8 release in lung cells via activator protein-1 by recombinant baculovirus displaying severe acute respiratory syndrome-coronavirus spike proteins: identification of two functional regions. J Immunol 173 (2004) 7602-7614
135. He R., Leeson A., Andonov A., Li Y., Bastien N., Cao J., et al. Activation of AP-1 signal transduction pathway by SARS coronavirus nucleocapsid protein. Biochem Biophys Res Commun 311 (2003) 870-876
136. Polyak S.J., Khabar K.S., Paschal D.M., Ezelle H.J., Duverlie G., Barber G.N., et al. Hepatitis C virus nonstructural 5A protein induces interleukin-8, leading to partial inhibition of the interferon-induced antiviral response. J Virol 75 (2001) 6095-6106
137. Stiles L.N., Hosking M.P., Edwards R.A., Strieter R.M., and Lane T.E. Differential roles for CXCR3 in CD4+ and CD8+ T cell trafficking following viral infection of the CNS. Eur J Immunol 36 (2006) 613-622
138. Sanda C., Weitzel P., Tsukahara T., Schaley J., Edenberg H.J., Stephens M.A., et al. Differential gene induction by type I and type II interferons and their combination. J Interferon Cytokine Res 26 (2006) 462-472
139. Yu S.Y., Hu Y.W., Liu X.Y., Xiong W., Zhou Z.T., and Yuan Z.H. Gene expression profiles in peripheral blood mononuclear cells of SARS patients. World J Gastroenterol 11 (2005) 5037-5043
140. Huang K.J., Su I.J., Theron M., Wu Y.C., Lai S.K., Liu C.C., et al. An interferon-gamma-related cytokine storm in SARS patients. J Med Virol 75 (2005) 185-194
141. Jiang Y., Xu J., Zhou C., Wu Z., Zhong S., Liu J., et al. Characterization of cytokine/chemokine profiles of severe acute respiratory syndrome. Am J Respir Crit Care Med 171 (2005) 850-857
142. Tang N.L., Chan P.K., Wong C.K., To K.F., Wu A.K., Sung Y.M., et al. Early enhanced expression of interferon-inducible protein-10 (CXCL-10) and other chemokines predicts adverse outcome in severe acute respiratory syndrome. Clin Chem 51 (2005) 2333-2340
143. Christensen J.E., de Lemos C., Moos T., Christensen J.P., and Thomsen A.R. CXCL10 is the key ligand for CXCR3 on CD8+ effector T cells involved in immune surveillance of the lymphocytic choriomeningitis virus-infected central nervous system. J Immunol 176 (2006) 4235-4243
144. Jones B.M., Ma E.S., Peiris J.S., Wong P.C., Ho J.C., Lam B., et al. Prolonged disturbances of in vitro cytokine production in patients with severe acute respiratory syndrome (SARS) treated with ribavirin and steroids. Clin Exp Immunol 135 (2004) 467-473
145. Reghunathan R., Jayapal M., Hsu L.Y., Chng H.H., Tai D., Leung B.P., et al. Expression profile of immune response genes in patients with severe acute respiratory syndrome. BMC Immunol 6 (2005) 2
146. SARS BGoNRPf. Dynamic changes in blood cytokine levels as clinical indicators in severe acute respiratory syndrome. Chin Med J (Engl) 116 (2003) 1283-1287
147. Ward S.E., Loutfy M.R., Blatt L.M., Siminovitch K.A., Chen J., Hinek A., et al. Dynamic changes in clinical features and cytokine/chemokine responses in SARS patients treated with interferon alfacon-1 plus corticosteroids. Antivir Ther 10 (2005) 263-275
148. Wong C.K., Lam C.W., Wu A.K., Ip W.K., Lee N.L., Chan I.H., et al. Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome. Clin Exp Immunol 136 (2004) 95-103
149. Hsueh P.R., Chen P.J., Hsiao C.H., Yeh S.H., Cheng W.C., Wang J.L., et al. Patient data, early SARS epidemic. Taiwan. Emerg Infect Dis 10 (2004) 489-493
150. Wang W.K., Chen S.Y., Liu I.J., Kao C.L., Chen H.L., Chiang B.L., et al. Temporal relationship of viral load, ribavirin, interleukin (IL)-6, IL-8, and clinical progression in patients with severe acute respiratory syndrome. Clin Infect Dis 39 (2004) 1071-1075
151. Xu L., Ran L., Cameron M.J., Persad D., Danesh A., Gold W., et al. Proinflammatory gene expression profiles and severity of disease course in SARS patients. International Conference on SARS, One Year After the (first) Outbreak. Luebeck, Germany (2004)
152. Yen Y.T., Liao F., Hsiao C.H., Kao C.L., Chen Y.C., and Wu-Hsieh B.A. Modeling the early events of severe acute respiratory syndrome coronavirus infection in vitro. J Virol 80 (2006) 2684-2693
153. Zhang Y., Li J., Zhan Y., Wu L., Yu X., Zhang W., et al. Analysis of serum cytokines in patients with severe acute respiratory syndrome. Infect Immun 72 (2004) 4410-4415
154. Ng L.F., Hibberd M.L., Ooi E.E., Tang K.F., Neo S.Y., Tan J., et al. A human in vitro model system for investigating genome-wide host responses to SARS coronavirus infection. BMC Infect Dis 4 (2004) 34
155. Tang B.S., Chan K.H., Cheng V.C., Woo P.C., Lau S.K., Lam C.C., et al. 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 79 (2005) 6180-6193
156. Law H.K., Cheung C.Y., Ng H.Y., Sia S.F., Chan Y.O., Luk W., et al. Chemokine upregulation in SARS coronavirus infected human monocyte derived dendritic cells. Blood 106 (2005) 2366-2374
157. Tseng C.T., Perrone L.A., Zhu H., Makino S., and Peters C.J. Severe acute respiratory syndrome and the innate immune responses: modulation of effector cell function without productive infection. J Immunol 174 (2005) 7977-7985
158. Ding Y., He L., Zhang Q., Huang Z., Che X., Hou J., et al. Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J Pathol 203 (2004) 622-630
159. Drosten C., Gunther S., Preiser W., van der Werf S., Brodt H.R., Becker S., et al. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348 (2003) 1967-1976
160. Farcas G.A., Poutanen S.M., Mazzulli T., Willey B.M., Butany J., Asa S.L., et al. Fatal severe acute respiratory syndrome is associated with multiorgan involvement by coronavirus. J Infect Dis 191 (2005) 193-197
161. Gu J., Gong E., Zhang B., Zheng J., Gao Z., Zhong Y., et al. Multiple organ infection and the pathogenesis of SARS. J Exp Med 202 (2005) 415-424
162. Lau Y.L., and Peiris J.S. Pathogenesis of severe acute respiratory syndrome. Curr Opin Immunol 17 (2005) 404-410
163. Li T., Qiu Z., Zhang L., Han Y., He W., Liu Z., et al. Significant changes of peripheral T lymphocyte subsets in patients with severe acute respiratory syndrome. J Infect Dis 189 (2004) 648-651
164. Peiris J.S., Yuen K.Y., Osterhaus A.D., and Stohr K. The severe acute respiratory syndrome. N Engl J Med 349 (2003) 2431-2441
165. Tsui P.T., Kwok M.L., Yuen H., and Lai S.T. Severe acute respiratory syndrome: clinical outcome and prognostic correlates. Emerg Infect Dis 9 (2003) 1064-1069
166. Wong R.S., Wu A., To K.F., Lee N., Lam C.W., Wong C.K., et al. Haematological manifestations in patients with severe acute respiratory syndrome: retrospective analysis. BMJ 326 (2003) 1358-1362
167. Chan K.H., Poon L.L., Cheng V.C., Guan Y., Hung I.F., Kong J., et al. Detection of SARS coronavirus in patients with suspected SARS. Emerg Infect Dis 10 (2004) 294-299
168. Ding Y., Wang H., Shen H., Li Z., Geng J., Han H., et al. The clinical pathology of severe acute respiratory syndrome (SARS): a report from China. J Pathol 200 (2003) 282-289
169. Lang Z.W., Zhang L.J., Zhang S.J., Meng X., Li J.Q., Song C.Z., et al. A clinicopathological study of three cases of severe acute respiratory syndrome (SARS). Pathology 35 (2003) 526-531
170. Nicholls J.M., Poon L.L., Lee K.C., Ng W.F., Lai S.T., Leung C.Y., et al. Lung pathology of fatal severe acute respiratory syndrome. Lancet 361 (2003) 1773-1778
171. Bermejo J.F., and Munoz-Fernandez M.A. Severe acute respiratory syndrome, a pathological immune response to the new coronavirus-implications for understanding of pathogenesis, therapy, design of vaccines, and epidemiology. Viral Immunol 17 (2004) 535-544
172. Ng M.L., Tan S.H., See E.E., Ooi E.E., and Ling A.E. Proliferative growth of SARS coronavirus in Vero E6 cells. J Gen Virol 84 (2003) 3291-3303
173. Mazzulli T., Farcas G.A., Poutanen S.M., Willey B.M., Low D.E., Butany J., et al. Severe acute respiratory syndrome-associated coronavirus in lung tissue. Emerg Infect Dis 10 (2004) 20-24
174. Hung I.F., Cheng V.C., Wu A.K., Tang B.S., Chan K.H., Chu C.M., et al. Viral loads in clinical specimens and SARS manifestations. Emerg Infect Dis 10 (2004) 1550-1557
175. Peiris J.S., Guan Y., and Yuen K.Y. Severe acute respiratory syndrome. Nat Med 10 (2004) S88-S97
176. Lee C.H., Chen R.F., Liu J.W., Yeh W.T., Chang J.C., Liu P.M., et al. Altered p38 mitogen-activated protein kinase expression in different leukocytes with increment of immunosuppressive mediators in patients with severe acute respiratory syndrome. J Immunol 172 (2004) 7841-7847
177. de Lang A., Baas T., Teal T., Leijten L.M., Rain B., Osterhaus A.D., et al. Functional genomics highlights differential induction of antiviral pathways in the lungs of SARS-CoV infected macaques. PlOS Pathogens 3 (2007) e112
178. Roberts A., Deming D., Paddock C.D., Cheng A., Yount B., Vogel L., et al. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog 3 (2007) e5
179. Tseng C.T., Huang C., Newman P., Wang N., Narayanan K., Watts D.M., et al. Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human angiotensin-converting enzyme 2 virus receptor. J Virol 81 (2007) 1162-1173
180. McCray Jr. P.B., Pewe L., Wohlford-Lenane C., Hickey M., Manzel L., Shi L., et al. Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J Virol 81 (2007) 813-821
181. Yoneyama M., and Fujita T. Function of RIG-I-like receptors in antiviral innate immunity. J Biol Chem 282 (2007) 15315-15318