A molecular arms race between host innate antiviral response and emerging human coronaviruses

Virologica Sinica

Volumn 31, Issue 1, 2016, Pages 12-23

  Wong, Lok Yin Roy ^a   Lui, Pak Yin ^a   Jin, Dong Yan ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

immune evasion; innate antiviral response; MERS CoV; SARS CoV; type I interferons

Indexed keywords

RECEPTOR; RECOMBINANT INTERFERON; RIG I LIKE RECEPTOR; STRUCTURAL PROTEIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; ANTIVIRUS AGENT;

CORONAVIRIDAE; CORONAVIRIDAE INFECTION; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; INNATE IMMUNITY; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; REVIEW; SARS CORONAVIRUS; SIGNAL TRANSDUCTION; ANIMAL; CORONAVIRUS INFECTION; DRUG EFFECTS; HUMAN; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIROLOGY;

ANIMALS; ANTIVIRAL AGENTS; CORONAVIRUS; CORONAVIRUS INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE;

EID: 84959187921     PISSN: 16740769     EISSN: 1995820X     Source Type: Journal    
DOI: 10.1007/s12250-015-3683-3     Document Type: Review

References (112)

1. Almazán F, DeDiego ML, Galán C, Escors D, álvarez E, Ortego J, Sola I, Zuniga S, Alonso S, Moreno JL, Nogales A, Capiscol C, Enjuanes L. 2006. Construction of a severe acute respiratory syndrome coronavirus infectious cDNA clone and a replicon to study coronavirus RNA synthesis. J Virol, 80: 10900–10906.
2. Almazán F, DeDiego ML, Sola I, Zuñiga S, Nieto-Torres JL, Marquez- Jurado S, Andrés G, Enjuanes L. 2013. Engineering a replication- competent, propagation-defective Middle East respiratory syndrome coronavirus as a vaccine candidate. MBio, 4: 00650–13.
3. Almazán, F, Sola I, Zuñiga S, Marquez-Jurado S, Morales L, Becares M, Enjuanes, L. 2014. Coronavirus reverse genetic systems: infectious clones and replicons. Virus Res, 189: 262–270.
4. Báez-Santos YM, Mielech AM, Deng X, Baker S, Mesecar AD. 2014. Catalytic function and substrate specificity of the papainlike protease domain of nsp3 from the Middle East respiratory syndrome coronavirus. J Virol, 88: 12511–12527.
5. Berke IC, Yu X, Modis Y, Egelman EH. 2012. MDA5 assembles into a polar helical filament on dsRNA. Proc Natl Acad Sci USA, 109: 18437–18441.
6. Boehme KW, Compton T. 2004. Innate sensing of viruses by Tolllike receptors. J Virol, 78: 7867–7873.
7. Bosch BJ, van der Zee R, de Haan CAM, Rottier PJM. 2003. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J Virol, 77: 8801–8811.
8. Bradburne AF, Bynoe ML, Tyrrell DA. 1967. Effects of a “new” human respiratory virus in volunteers. Br Med J, 3: 767–769.
9. Bruns AM, Leser GP, Lamb RA, Horvath CM. 2014. The innate immune sensor LGP2 activates antiviral signaling by regulating MDA5-RNA interaction and filament assembly. Mol Cell, 55: 771–781.
10. Burkard C, Verheije MH, Wicht O, van Kasteren SI, van Kuppeveld FJ, Haagmans BL, Pelkmans L, Rottier PJM, Bosch BJ, de Haan CAM. 2014. Coronavirus cell entry occurs through the endo-lysosomal pathway in a proteolysis-dependent manner. PLoS Pathog, 10: e1004502.
11. Chan CP, Siu KL, Chin KT, Yuen KY, Zheng B, Jin DY. 2006. Modulation of the unfolded protein response by the severe acute respiratory syndrome coronavirus spike protein. J Virol, 80: 9279–9287.
12. Chan JF, To KK, Tse H, Jin DY, Yuen KY. 2013. Interspecies transmission and emergence of novel viruses: lessons from bats and birds. Trends Microbiol, 21: 544–555.
13. Chen Y, Cai H, Pan J, Xiang N, Tien P, Ahola T, Guo D. 2009. Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proceedings of the National Academy of Sciences of the United States of America, 106: 3484–3489.
14. Chen Y, Rajashankar KR, YangY, Agnihothram SS, Liu C, Lin YL, Baric RS, Li F. 2013. Crystal structure of the receptor-binding domain from newly emerged Middle East respiratory syndrome coronavirus. J Virol, 87: 10777–10783.
15. Chen Y, Su C, Ke M, Jin X, Xu L, Zhang Z, Wu A, Sun Y, Yang Z, Tien P, Ahola T, Liang Y, Liu X, Guo D. 2011. Biochemical and Structural Insights into the Mechanisms of SARS Coronavirus RNA Ribose 2′-O-Methylation by nsp16/nsp10 Protein Complex. PLoS Pathog, 7: e1002294.
16. Cheng VCC, Lau SKP, Woo PCY, Yuen KY. 2007. Severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection. Clin Microbiol Rev, 20: 660–694.
17. Clementz MA, Chen Z, Banach BS, Wang Y, Sun L, Ratia K, Baez-Santos YM, Wang J, Takayama J, Ghosh AK, Li K, Mesecar AD, Baker SC. 2010. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J Virol, 84: 4619–4629.
18. Corman VM, Baldwin HJ, Tateno AF, Zerbinati RM, Annan A, Owusu M, Nkrumah EE, Maganga GD, Oppong S, Adu-Sarkodie Y, Vallo P, da Silva Filho LVRF, Leroy EM, Thiel V, van der Hoek L, Poon LLM, Tschapka CD, Drexler JF. 2015. Evidence for an ancestral association of human coronavirus 229E with bats. J Virol, 89: 11858–11870.
19. Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, Errett J, Lin TY, Schneller S, Zust R, Dong H, Thiel V, Pierson TC, Muller RM, Gale MJ, Shi PY, Diamond MS. 2010. 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature, 468: 452–456.
20. Decroly E, Debarnot C, Ferron F, Bouvet M, Coutard B, Imbert I, Gluais L, Papageorgiou N, Sharff A, Bricogne G, Ortiz-Lombardia M, Lescar J, Canard, B. 2011. Crystal Structure and Functional Analysis of the SARS-Coronavirus RNA Cap 2′-OMethyltransferase nsp10/nsp16 Complex. PLoS Pathog, 7: 1002059.
21. de Groot RJ, Baker SC, Baric RS, Brown CS, Drosten C, Enjuanes L, Fouchier RAM, Galiano M, Gorbalenya AE, Memish ZA, Perlman S, Poon LLM, Snijder EJ, Stephens GM, Woo PCY, Zaki AM, Zambon M, Ziebuhr J. 2013. Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the coronavirus study group. J Virol, 87: 7790–7792.
22. Durai P, Batool M, Shah M, Choi S. 2015. Middle East respiratory syndrome coronavirus: transmission, virology and therapeutic targeting to aid in outbreak control. Exp Mol Med, 47: e181.
23. Falzarano D, de WitE, Martellaro C, Callison J, Munster VJ, Feldmann H. 2013. Inhibition of novel β coronavirus replication by a combination of interferon-α2b and ribavirin. Sci Rep, 3: 1686.
24. Faure E, Poissy J, Goffard A, Fournier C, Kipnis E, Titecat M, Bortolotti P, Martinez L, Dubucquoi S, Dessein R, Gosset P, Mathieu D, Guery B. 2014. Distinct immune response in two MERS-CoV-infected patients: Can we go from bench to bedside? PLoS ONE, 9: e88716.
25. Ford E, Thanos D. 2010. The transcriptional code of human IFN-β gene expression. Biochim Biophys Acta, 1799: 328–336.
26. Fouchier RAM, Hartwig NG, Bestebroer TM, Niemeyer B, de Jong JC, Simon JH, Osterhaus ADME. 2004. A previously undescribed coronavirus associated with respiratory disease in humans. Proc Natl Acad Sci USA, 101: 6212–6216.
27. Frieman M, Heise M, Baric R. 2008. SARS coronavirus and innate immunity. Virus Res, 133: 101–112.
28. Frieman MB, Chen J, Morrison TE, Whitmore A, Funkhouser W, Ward JM, Lamirande EW, Roberts A, Heise M, Subbarao K, Baric RS. 2010. SARS-CoV pathogenesis is regulated by a STAT1 dependent but a type I, II and III interferon receptor independent mechanism. PLoS Pathog, 6: e1000849.
29. Fung TS, Huang M, Liu DX. 2014. Coronavirus-induced ER stress response and its involvement in regulation of coronavirus-host interactions. Virus Res, 194: 110–123.
30. Graham R, Donaldson EF, Baric RS. 2013. A decade after SARS: strategies for controlling emerging coronaviruses. Nat Rev Microbiol, 11: 836–848.
31. Gusho E, Zhang R, Jha BK, Thornbrough JM, Dong B, Gaughan C, Elliott R, Weiss SR, Silverman RH. 2014. Murine AKAP7 has a 2′, 5′-phosphodiesterase domain that can complement an inactive murine coronavirus ns2 gene. MBio, 5: e01312–14.
32. Hamre D, Procknow JJ. 1966. A new virus isolated from the human respiratory tract. Proc Soc Exp Biol Med, 121: 190–193.
33. Hsu PD, Lander ES, Zhang F. 2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell, 157: 1262–1278.
34. Huang C, Lokugamage KG, Rozovics JM, Narayanan K, Semler BL, Makino S. 2011. SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: Viral mRNAs are resistant to nsp1-induced RNA cleavage. PLoS Pathog, 7: e1002433.
35. Huynh J, Li S, Yount B, Smith A, Sturges L, Olsen JC, Nagel J, Johnson JB, Ggnihothram S, Gates JE, Frieman MB, Baric RS, Donaldson EF. 2012. Evidence supporting a zoonotic origin of human coronavirus strain NL63. J Virol, 86: 12816–12825.
36. Ivashkiv LB, Donlin LT. 2014. Regulation of type I interferon responses. Nature Rev Immunol, 14: 36–49.
37. Jiang F, Ramanathan A, Miller MT, Tang GQ, Gale M, Patel SS, Marcotrigiano J. 2011. Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature, 479: 423–427.
38. Kawai T, Akira S. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol, 11: 373–384.
39. Kell A, Stoddard M, Li H, Marcotrigiano J, Shaw GM, Gale M. 2015. Pathogen-associated molecular pattern recognition of hepatitis C virus transmitted/founder variants by RIG-I is dependent on U-core length. J Virol, 89: 11056–11068.
40. Kindler E, Jónsdóttir HR, Muth D, Hamming OJ, Hartmann R, Rodriguez R, Geffers R, Fouchier RAM, Drosten C, Muller MA, Dijkman R, Thiel V. 2013. Efficient replication of the novel human betacoronavirus EMC on primary human epithelium highlights its zoonotic potential. MBio, 4: e00611.12.
41. Kopecky-Bromberg SA, Martínez-Sobrido L, Frieman M, Baric RA, Palese P. 2007. Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J Virol, 81: 548–557.
42. Kowalinski E, Lunardi T, McCarthy Andrew A, Louber J, Brunel J, Grigorov B, Gerlier D, Cusack S. 2011. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell, 147: 423–435.
43. Lau SKP, Woo PCY, Yip CCY, Tse H, Tsoi H, Cheng VCC, Lee P, Tang BSF, Cheung CHY, Lee RA, So LY, Lau YL, Chan KH, Yuen KY. 2006. Coronavirus HKU1 and other coronavirus infections in Hong Kong. J Clin Microbiol, 44: 2063–2071.
44. Levy DE, Garcia-Sastre A. 2001. The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev, 12: 143–156.
45. Li J, Liu Y, Zhang X. 2010. Murine coronavirus induces type I interferon in oligodendrocytes through recognition by RIG-I and MDA5. J Virol, 84: 6472–6482.
46. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature, 426: 450–454.
47. Liu G, Park HS, Pyo HM, Liu Q, Zhou Y. 2015b. Influenza A virus panhandle structure is directly involved in RIG-I activation and interferon induction. J Virol, 89: 6067–6079.
48. Liu S, Cai X, Wu J, Cong Q, Chen X, Li T, Du F, Ren J, Wu YT, Grishin NV, Chen ZJ. 2015a. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science, 347: 6227.
49. Lokugamage KG, Narayanan K, Nakagawa K, Terasaki K, Ramirez SI, Tseng CTK, Makino S. 2015. Middle East respiratory syndrome coronavirus nsp1 inhibits host gene expression by selectively targeting mRNAs transcribed in the nucleus while sparing mRNAs of cytoplasmic origin. J Virol, 89: 10970–10981.
50. Loo YM, Gale M. 2011. Immune signaling by RIG-I-like receptors. Immunity, 34: 680–692.
51. Lu X, Pan J, Tao J, Guo D. 2011. SARS-CoV nucleocapsid protein antagonizes IFN-β response by targeting initial step of IFN-β induction pathway, and its C-terminal region is critical for the antagonism. Virus Genes, 42: 37–45.
52. Luo D, Ding SC, Vela A, Kohlway A, Lindenbach BD, Pyle AM. 2011. Structural insights into RNA recognition by RIG-I. Cell, 147: 409–422.
53. Ma F, Li B, Liu SY, Iyer SS, Yu Y, Wu A, Cheng G. 2015a. Positive feedback regulation of type I IFN production by the IFN-inducible DNA sensor cGAS. J Immunol, 194: 1545–1554.
54. Ma F, Li B, Yu Y, Iyer SS, Sun M, Cheng G. 2015b. Positive feedback regulation of type I interferon by the interferonstimulated gene STING. EMBO Rep, 16: 202–212.
55. Matthews KL, Coleman CM, van der Meer Y, Snijder EJ, Frieman MB. 2014. The ORF4b-encoded accessory proteins of Middle East respiratory syndrome coronavirus and two related bat coronaviruses localize to the nucleus and inhibit innate immune signalling. J Gen Virol, 4: 874–882.
56. Mazaleuskaya L, Veltrop R, Ikpeze N, Martin-Garcia J, Navas-Martin S. 2012. Protective role of Toll-like receptor 3-induced type I interferon in murine coronavirus infection of macrophages. Viruses, 4: 901–923.
57. McIntosh K, Dees JH, Becker WB, Kapikian AZ, Chanock RM. 1967. Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proc Natl Acad Sci USA, 57: 933–940.
58. Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V, Epstein JH, AlHakeem R, Durosinloun A, Asmari MA, Islam A, Kapoor A, Briese T, Daszak P, Al Rabeeah AA, Lipkin WI. 2013. Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis, 19: 1819–1823.
59. Menachery VD, Debbink K, Baric RS. 2014a. Coronavirus nonstructural protein 16: Evasion, attenuation, and possible treat-ments. Virus Res, 194: 191–199.
60. Menachery VD, Eisfeld AJ, Schäfer A, Josset L, Sims AC, Proll S, Fan S, Li C, Neumann G, Tilton SC, Chang J, Gralinski LE, Long CG, Richard WCM, Weiss J, Matzke MM, Webb-Robertson BJ, Schepmoes AA, Shukla AK, Metz TO, Smith RD, Waters KM, Katze MG, Kawaoka Y, Baric RS. 2014b. Pathogenic influenza viruses and coronaviruses utilize similar and contrasting approaches to control interferon-stimulated gene responses. MBio, 5: e01174.14.
61. Menachery VD, Yount, BL, Josset, L, Gralinski LE, Scobey T, Agnihothram S, Katze MG, Baric RS. 2014c. Attenuation and restoration of severe acute respiratory syndrome coronavirus mutant lacking 2′-O-methyltransferase activity. J Virol, 88: 4251–4264.
62. Mielech AM, Kilianski A, Baez-Santos YM, Mesecar AD, Baker SC. 2014. MERS-CoV papain-like protease has deISGylating and deubiquitinating activities. Virology, 450–451: 64–70.
63. Narayanan K, Huang C, Lokugamage K, Kamitani W, Ikegami T, Tseng CTK, Makino S. 2008a. Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J Virol, 82: 4471–4479.
64. Narayanan K, Huang C, Makino S. 2008b. SARS coronavirus accessory proteins. Virus Res, 133: 113–121.
65. Neuman BW, Chamberlain P, Bowden F, Joseph J. 2014. Atlas of coronavirus replicase structure. Virus Res, 194: 49–66.
66. Niemeyer D, Zillinger T, Muth D, Zielecki F, Horvath G, SulimanT, Barchet W, Weber F, Drosten C, Müller MA. 2013. Middle East respiratory syndrome coronavirus accessory protein 4a is a type I interferon antagonist. J Virol, 87: 12489–12495.
67. Omrani AS, Saad MM, Baig K, Bahloul A, Abdul-Matin M, Alaidaroos AY, Almakhlafi GA, Albarrak MM, Memish ZA, Albarrak AM. 2014. Ribavirin and interferon alfa-2a for severe Middle East respiratory syndrome coronavirus infection: a retrospective cohort study. Lancet Infect Dis, 14: 1090–1095.
68. Peisley A, Wu B, Yao H, Walz T, Hur S. 2013. RIG-I forms signaling-competent filaments in an ATP-dependent, ubiquitin-independent manner. Mol Cell, 51: 573–583.
69. Pepin KM, Lass S, Pulliam JRC, Read AF, Lloyd-Smith JO. 2010. Identifying genetic markers of adaptation for surveillance of viral host jumps. Nat Rev Microbiol, 8: 802–813.
70. Perlman S, Zhao J. 2013. Human coronavirus EMC is not the same as severe acute respiratory syndrome coronavirus. MBio, 4: e00002–13.
71. Pyrc K, Berkhout B, van der Hoek L. 2007. The novel human coronaviruses NL63 and HKU1. J Virol, 81: 3051–3057.
72. Raj VS, Mou H, Smits SL, Dekkers DHW, Muller MA, Dijkman R, Muth D, Demmers JAA, Zaki A, Fouchier RAM, Thiel V, Drosten C, Rottire PJM, Osterhaus ADME, Bosch BJ, Haagmans BL. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature, 495: 251–254.
73. Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, Icenogle JP, Peñaranda S, Bankamo B, Maher K, Chen MH, Ton SX, Tamin A, Lowe L, Frace M, DeRisi JL, Chen Q, Wang D, Erdman DD, Peret TCT, Burns C, Ksiazek TG, Rollin PE, Sanchez A, Liffick S, Holloway B, Limor J, McCaustland K, Olsen-Rasmussen M, Fouchier R, Gunther S, Osterhaus ADME, Drosten C, Pallansch MA, Anderson LJ, Bellini WJ. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science, 300: 1394–1399.
74. Samuel CE. 1991. Antiviral actions of interferon interferon-regulated cellular proteins and their surprisingly selective antiviral activities. Virology, 183: 1–11.
75. Samuel CE. 2001. Antiviral actions of interferons. Clin Microbiol Rev, 14: 778–809.
76. Satoh T, Kato H, Kumagai Y, Yoneyama M, Sato S, Matsushita K, Tsujimura T, Fujuta T, Akira S, Takeuchi O. 2010. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc Natl Acad Sci USA, 107: 1512–1517.
77. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M. 2008. Innate immunity induced by composition-dependent RIG-I recognition of Hepatitis C virus RNA. Nature, 454: 523–527.
78. Schneider WM, Chevillotte MD, Rice CM. 2014. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol, 32: 513–545.
79. Schoggins, JW, MacDuff DA, Imanaka N, Gainey MD, Shrestha B, Eitson JL, Mar KB, Richardson RB, Ratushny AV, Litvak V, Dabelic R, Manicassamy B, Aitchison JD, Aderem A, Elliott RM, García-Sastre A, Racaniello V, Snijder EJ, Yokoyama WM, Diamond MS, Virgin HW, Rice CM. 2014. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature, 505: 691–695.
80. Scobey T, Yount BL, Sims AC, Donaldson EF, Agnihothram SS, MenacheryVD, Graham RL, Swanstrom J, Bove PF, Kim JD, Grego S, Randell SH, Baric RS. 2013. Reverse genetics with a full-length infectious cDNA of the Middle East respiratory syndrome coronavirus. Proc Natl Acad Sci USA, 110: 16157–16162.
81. Sevajol M, Subissi L, Decroly E, Canard B, Imbert I. 2014. Insights into RNA synthesis, capping, and proofreading mechanisms of SARS-coronavirus. Virus Res, 194: 90–99.
82. Shirato K, Kawase M, Matsuyama S. 2013. Middle East respiratory syndrome coronavirus infection mediated by the transmembrane serine protease TMPRSS2. J Virol, 87: 12552–12561.
83. Siu KL, Chan CP, Kok KH, Woo PCY, Jin DY. 2014a. Suppression of innate antiviral response by severe acute respiratory syndrome coronavirus M protein is mediated through the first transmembrane domain. Cell Mol Immunol, 11: 141–149.
84. Siu KL, Chan CP, Kok KH, Woo PC, Jin DY. 2014b. Comparative analysis of the activation of unfolded protein response by spike proteins of severe acute respiratory syndrome coronavirus and human coronavirus HKU1. Cell Biosci, 4: 3.
85. Siu KL, Kok KH, Ng MHJ, Poon VKM, Yuen, KY, Zheng BJ, Jin DY. 2009. Severe acute respiratory syndrome coronavirus m protein inhibits type I interferon production by impeding the formation of TRAF3·TANK·TBK1/IKK complex. J Biol Chem, 284: 16202–16209.
86. Siu KL, Yeung ML, Kok KH, Yuen KS, Kew C, Lui PY, Chan CP, Tse H, Woo PCY, Yuen KY, Jin DY. 2014c. Middle East respiratory syndrome coronavirus 4a protein is a double-stranded RNA-binding protein that suppresses pact-induced activation of RIG-I and MDA5 in the innate antiviral response. J Virol, 88: 4866–4876.
87. Takaoka A, Hayakawa S, Yanai H, Stoiber D, Negishi H, Kikuchi H, Sasaki S, Imai K, Shibue T, Honda K, Taniguchi T. 2003. Integration of interferon-α/β signalling to p53 responses in tumour suppression and antiviral defence. Nature, 424: 516–523.
88. Tanaka T, Kamitani W, DeDiego ML, Enjuanes L, Matsuura Y. 2012. Severe acute respiratory syndrome coronavirus nsp1 facilitates efficient propagation in cells through a specific translational shutoff of host mRNA. J Virol, 86: 11128–11137.
89. Totura AL, Whitmore A, Agnihothram S, Schäfer A, Katze MG, HeiseMT, Baric RS. 2015. Toll-like receptor 3 signaling via TRIF contributes to a protective innate immune response to severe acute respiratory syndrome coronavirus infection. MBio, 6: 00638–15.
90. Tyrrell DAJ, Bynoe ML. 1965. Cultivation of a novel type of common-cold virus in organ cultures. Br Med J, 1: 1467–1470.
91. van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJM, Wolthers KC, Wertheim-van Dillen PME, Kaandorp J, Spaargaren J, Berkhout B. 2004. Identification of a new human coronavirus. Nat Med, 10: 368–373.
92. Wang Y, Sun Y, Wu A, Xu S, Pan R, Zeng C, Jin X, Ge X, Shi Z, Ahola T, Chen Y, Guo D. 2015. Coronavirus nsp10/nsp16 methyltransferase can be targeted by nsp10-derived peptide in vitro and in vivo to reduce replication and pathogenesis. J Virol, 89: 8416–8427.
93. Weber M, Gawanbacht A, Habjan M, Rang A, Borner C, Schmidt AM, Veitinger S, Jacob R, Devignot S, Kochs G, Weber F. 2013. Incoming RNA virus nucleocapsids containing a 5′-triphosphorylated genome activate RIG-I and antiviral signaling. Cell Host Microbe, 13: 336–346.
94. Woo PCY, La, SKP, Chu C, Chan K, Tsoi H, Huang Y, Wong BHK, Poon RWS, Cai JJ, Luk WK, Poon LLM, Wong SSY, Guan Y, Peiris JSM, Yuen KY. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J Virol, 79: 884–895.
95. Woo PCY, Lau SKP, Huang Y, Yuen KY. 2009. Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med (Maywood), 234: 1117–1127.
96. Woo PCY, Lau SKP, Lam CSF, Lau CCY, Tsang AKL, Lau JHN, Bai R, Teng JLL, Tsang CCC, Wang M, Zheng BJ, Chan KH, Yuen KY. 2012. Discovery of seven novel mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus. J Virol, 86: 3995–4008.
97. Wu B, Peisley A, Richards C, Yao H, Zeng X, Lin C, Chu F, Walz T, Hur S. 2013. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell, 152: 276–289.
98. Wu B, Peisley A, Tetrault D, Li Z, Egelman EH, Magor KE, Walz T, Penczek PA, Hur S. 2014. Molecular imprinting as a signalactivation mechanism of the viral RNA sensor RIG-I. Mol Cell, 55: 511–523.
99. Xagorari A, Chlichlia K. 2008. Toll-like receptors and viruses: induction of innate antiviral immune responses. Open Microbiol J, 2: 49–59.
100. Yang Y, Ye F, Zhu N, Wang W, Deng Y, Zhao Z, Tan W. 2015. Middle East respiratory syndrome coronavirus ORF4b protein inhibits type I interferon production through both cytoplasmic and nuclear targets. Sci Rep, 5: 17554.
101. Yang Y, Zhang L, Geng H, Deng Y, Huang B, Guo Y, Zhao Z, Tan W. 2013. The structural and accessory proteins M, ORF 4a, ORF 4b, and ORF 5 of Middle East respiratory syndrome coronavirus (MERS-CoV) are potent interferon antagonists. Protein Cell, 4: 951–961.
102. Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, Look AT, Holmes KV. 1992. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature, 357: 420–422.
103. Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M, Taira K, Foy E, Loo YM, Gale M Jr, Akira S, Yonehara S, Kato A, Fujita T. 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.
104. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNAinduced innate antiviral responses. Nat Immunol, 5: 730–737.
105. Yount B, Curtis KM, Fritz EA, Hensley LE, Jahrling PB, Prentice E, Denison MR, Geisbert TW, Baric RS. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci USA, 100: 12995–13000.
106. Yuen KS, Chan CP, Wong NHM, Ho CH, Ho TH, Lei T, Deng W, Tsao SW, Chen H, Kok KH, Jin DY. 2015. CRISPR/Cas9-mediated genome editing of Epstein-Barr virus in human cells. J Gen Virol, 96: 626–636.
107. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med, 367: 1814–1820.
108. Zhang R, Jha BK, Ogden KM, Dong B, Zhao L, Elliott R, Patton JT, Silverman RH, Weiss SR. 2013. Homologous 2′, 5′-phosphodiesterases from disparate RNA viruses antagonize antiviral innate immunity. Proc Natl Acad Sci USA, 110: 13114–13119.
109. Zhao L, Jha BK, Wu A, Elliott R, Ziebuhr J, Gorbalenya AE, Silverman RH, Weiss SR. 2012. Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host Microbe, 11: 607–616.
110. Zhong Y, Tan YW, Liu DX. 2012. Recent progress in studies of arterivirus- and coronavirus-host interactions. Viruses, 4: 980–1010.
111. Zornetzer GA, Frieman MB, Rosenzweig E, Korth MJ, Page C, Baric RS, Katze MG. 2010. Transcriptomic analysis reveals a mechanism for a prefibrotic phenotype in STAT1 knockout mice during severe acute respiratory syndrome coronavirus infection. J Virol, 84: 11297–11309.
112. Züst R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW, Ziebuhr J, Szretter KJ, Baker SC, Barchet W, Diamond MS, Siddell SG, Ludewig B, Thiel V. 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.