Advertisement

Virologica Sinica

, Volume 31, Issue 1, pp 12–23 | Cite as

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

  • Lok-Yin Roy Wong
  • Pak-Yin Lui
  • Dong-Yan Jin
Review

Abstract

Coronaviruses have been closely related with mankind for thousands of years. Communityacquired human coronaviruses have long been recognized to cause common cold. However, zoonotic coronaviruses are now becoming more a global concern with the discovery of highly pathogenic severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) coronaviruses causing severe respiratory diseases. Infections by these emerging human coronaviruses are characterized by less robust interferon production. Treatment of patients with recombinant interferon regimen promises beneficial outcomes, suggesting that compromised interferon expression might contribute at least partially to the severity of disease. The mechanisms by which coronaviruses evade host innate antiviral response are under intense investigations. This review focuses on the fierce arms race between host innate antiviral immunity and emerging human coronaviruses. Particularly, the host pathogen recognition receptors and the signal transduction pathways to mount an effective antiviral response against SARS and MERS coronavirus infection are discussed. On the other hand, the counter-measures evolved by SARS and MERS coronaviruses to circumvent host defense are also dissected. With a better understanding of the dynamic interaction between host and coronaviruses, it is hoped that insights on the pathogenesis of newly-identified highly pathogenic human coronaviruses and new strategies in antiviral development can be derived.

Keywords

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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  6. Boehme KW, Compton T. 2004. Innate sensing of viruses by Tolllike receptors. J Virol, 78: 7867–7873.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  8. Bradburne AF, Bynoe ML, Tyrrell DA. 1967. Effects of a “new” human respiratory virus in volunteers. Br Med J, 3: 767–769.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  25. Ford E, Thanos D. 2010. The transcriptional code of human IFN-β gene expression. Biochim Biophys Acta, 1799: 328–336.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  27. Frieman M, Heise M, Baric R. 2008. SARS coronavirus and innate immunity. Virus Res, 133: 101–112.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  30. Graham R, Donaldson EF, Baric RS. 2013. A decade after SARS: strategies for controlling emerging coronaviruses. Nat Rev Microbiol, 11: 836–848.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  32. Hamre D, Procknow JJ. 1966. A new virus isolated from the human respiratory tract. Proc Soc Exp Biol Med, 121: 190–193.PubMedCrossRefGoogle Scholar
  33. Hsu PD, Lander ES, Zhang F. 2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell, 157: 1262–1278.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  36. Ivashkiv LB, Donlin LT. 2014. Regulation of type I interferon responses. Nature Rev Immunol, 14: 36–49.CrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  50. Loo YM, Gale M. 2011. Immune signaling by RIG-I-like receptors. Immunity, 34: 680–692.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  59. Menachery VD, Debbink K, Baric RS. 2014a. Coronavirus nonstructural protein 16: Evasion, attenuation, and possible treat-ments. Virus Res, 194: 191–199.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  64. Narayanan K, Huang C, Makino S. 2008b. SARS coronavirus accessory proteins. Virus Res, 133: 113–121.PubMedCentralPubMedCrossRefGoogle Scholar
  65. Neuman BW, Chamberlain P, Bowden F, Joseph J. 2014. Atlas of coronavirus replicase structure. Virus Res, 194: 49–66.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  70. Perlman S, Zhao J. 2013. Human coronavirus EMC is not the same as severe acute respiratory syndrome coronavirus. MBio, 4: e00002–13.PubMedCentralPubMedGoogle Scholar
  71. Pyrc K, Berkhout B, van der Hoek L. 2007. The novel human coronaviruses NL63 and HKU1. J Virol, 81: 3051–3057.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  74. Samuel CE. 1991. Antiviral actions of interferon interferon-regulated cellular proteins and their surprisingly selective antiviral activities. Virology, 183: 1–11.PubMedCrossRefGoogle Scholar
  75. Samuel CE. 2001. Antiviral actions of interferons. Clin Microbiol Rev, 14: 778–809.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  78. Schneider WM, Chevillotte MD, Rice CM. 2014. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol, 32: 513–545.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.Google Scholar
  90. Tyrrell DAJ, Bynoe ML. 1965. Cultivation of a novel type of common-cold virus in organ cultures. Br Med J, 1: 1467–1470.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  95. Woo PCY, Lau SKP, Huang Y, Yuen KY. 2009. Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med (Maywood), 234: 1117–1127.CrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  99. Xagorari A, Chlichlia K. 2008. Toll-like receptors and viruses: induction of innate antiviral immune responses. Open Microbiol J, 2: 49–59.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  110. Zhong Y, Tan YW, Liu DX. 2012. Recent progress in studies of arterivirus- and coronavirus-host interactions. Viruses, 4: 980–1010.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer Science+Business Media Singapore 2016

Authors and Affiliations

  1. 1.School of Biomedical SciencesThe University of Hong KongHong Kong SARChina

Personalised recommendations