Host factors in coronavirus replication

Current Topics in Microbiology and Immunology

Volumn 419, Issue , 2018, Pages 1-42

  de Wilde, Adriaan H ^a   Snijder, Eric J ^a   Kikkert, Marjolein ^a   van Hemert, Martijn J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN; HOST FACTOR; VIRUS GLYCOPROTEIN;

ALPHACORONAVIRUS; AMINO TERMINAL SEQUENCE; BETACORONAVIRUS; CARBOXY TERMINAL SEQUENCE; CELL CYCLE REGULATION; CELL MEMBRANE; CORONAVIRINAE; DELTACORONAVIRUS; GAMMACORONAVIRUS; HOST CELL; HUMAN; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; UNFOLDED PROTEIN RESPONSE; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS EXPRESSION; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION; ANIMAL; CORONAVIRUS INFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; SEVERE ACUTE RESPIRATORY SYNDROME; VIROLOGY;

ANIMALS; CORONAVIRUS; CORONAVIRUS INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS REPLICATION;

EID: 85058412933     PISSN: 0070217X     EISSN: 21969965     Source Type: Book Series    
DOI: 10.1007/82_2017_25     Document Type: Chapter

References (260)

1. Altan-Bonnet N, Balla T (2012) Phosphatidylinositol 4-kinases: hostages harnessed to build panviral replication platforms. Trends Biochem Sci 37:293–302
2. Angelini MM, Akhlaghpour M, Neuman BW, Buchmeier MJ (2013) Severe acute respiratory syndrome coronavirus nonstructural proteins 3, 4, and 6 induce double-membrane vesicles. MBio 4:e00513–e00524
3. Baas T, Taubenberger JK, Chong PY, Chui P, Katze MG (2006) SARS-CoV virus-host interactions and comparative etiologies of acute respiratory distress syndrome as determined by transcriptional and cytokine profiling of formalin-fixed paraffin-embedded tissues. J Interferon Cytokine Res: The Official Journal of The International Society for Interferon and Cytokine Research 26:309–317
4. Bagga S, Bouchard MJ (2014) Cell cycle regulation during viral infection. Methods Mol Biol 1170:165–227
5. Bailey-Elkin BA, Knaap RC, Johnson GG, Dalebout TJ, Ninaber DK, van Kasteren PB, Bredenbeek PJ, Snijder EJ, Kikkert M, Mark BL (2014) Crystal structure of the Middle East respiratory syndrome coronavirus (MERS-CoV) papain-like protease bound to ubiquitin facilitates targeted disruption of deubiquitinating activity to demonstrate its role in innate immune suppression. J Biol Chem 289:34667–34682
6. Bakkers MJ, Zeng Q, Feitsma LJ, Hulswit RJ, Li Z, Westerbeke A, van Kuppeveld FJ, Boons GJ, Langereis MA, Huizinga EG, de Groot RJ (2016) Coronavirus receptor switch explained from the stereochemistry of protein-carbohydrate interactions and a single mutation. Proc Natl Acad Sci U S A 113:E3111–E3119
7. Barik S (2006) Immunophilins: for the love of proteins. Cell Mol Life Sci 63:2889–2900
8. Baugh J, Gallay P (2012) Cyclophilin involvement in the replication of hepatitis C virus and other viruses. Biol Chem 393:579–587
9. Bechill J, Chen Z, Brewer JW, Baker SC (2008) Coronavirus infection modulates the unfolded protein response and mediates sustained translational repression. J Virol 82:4492–4501
10. Berger KL, Cooper JD, Heaton NS, Yoon R, Oakland TE, Jordan TX, Mateu G, Grakoui A, Randall G (2009) Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. Proc Natl Acad Sci U S A 106:7577–7582
11. Bertram S, Dijkman R, Habjan M, Heurich A, Gierer S, Glowacka I, Welsch K, Winkler M, Schneider H, Hofmann-Winkler H, Thiel V, Pohlmann S (2013) TMPRSS2 activates the human coronavirus 229E for cathepsin-independent host cell entry and is expressed in viral target cells in the respiratory epithelium. J Virol 87:6150–6160
12. Bhardwaj K, Liu P, Leibowitz JL, Kao CC (2012) The coronavirus endoribonuclease Nsp15 interacts with retinoblastoma tumor suppressor protein. J Virol 86:4294–4304
13. Brian DA, Baric RS (2005) Coronavirus genome structure and replication. Curr Top Microbiol Immunol 287:1–30
14. Brierley I, Dos Ramos FJ (2006) Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Virus Res 119:29–42
15. Brierley I, Digard P, Inglis SC (1989) Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell 57:537–547
16. Brockway SM, Clay CT, Lu XT, Denison MR (2003) Characterization of the expression, intracellular localization, and replication complex association of the putative mouse hepatitis virus RNA-dependent RNA polymerase. J Virol 77:10515–10527
17. Bruns AM, Horvath CM (2014) Antiviral RNA recognition and assembly by RLR family innate immune sensors. Cytokine Growth Factor Rev 25:507–512
18. Burkard C, Verheije MH, Wicht O, van Kasteren SI, van Kuppeveld FJ, Haagmans BL, Pelkmans L, Rottier PJ, Bosch BJ, de Haan CA (2014) Coronavirus cell entry occurs through the endo-/lysosomal pathway in a proteolysis-dependent manner. PLoS Pathog 10:e1004502
19. Cali T, Galli C, Olivari S, Molinari M (2008) Segregation and rapid turnover of EDEM1 by an autophagy-like mechanism modulates standard ERAD and folding activities. Biochem Biophys Res Commun 371:405–410
20. Carbajo-Lozoya J, Muller MA, Kallies S, Thiel V, Drosten C, von Brunn A (2012) Replication of human coronaviruses SARS-CoV, HCoV-NL63 and HCoV-229E is inhibited by the drug FK506. Virus Res 165:112–117
21. Carbajo-Lozoya J, Ma-Lauer Y, Malesevic M, Theuerkorn M, Kahlert V, Prell E, von Brunn B, Muth D, Baumert TF, Drosten C, Fischer G, von Brunn A (2014) Human coronavirus NL63 replication is cyclophilin A-dependent and inhibited by non-immunosuppressive cyclosporine A-derivatives including alisporivir. Virus Res 184C:44–53
22. Carette JE, Guimaraes CP, Varadarajan M, Park AS, Wuethrich I, Godarova A, Kotecki M, Cochran BH, Spooner E, Ploegh HL, Brummelkamp TR (2009) Haploid genetic screens in human cells identify host factors used by pathogens. Science 326:1231–1235
23. Chan SW (2014) Unfolded protein response in hepatitis C virus infection. Front Microbiol 5:233
24. 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
25. Chang YJ, Liu CY, Chiang BL, Chao YC, Chen CC (2004) 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 173:7602–7614
26. Chen CJ, Makino S (2004) Murine coronavirus replication induces cell cycle arrest in G0/G1 phase. J Virol 78:5658–5669
27. Chen CJ, Sugiyama K, Kubo H, Huang C, Makino S (2004) Murine coronavirus nonstructural protein p28 arrests cell cycle in G0/G1 phase. J Virol 78:10410–10419
28. Chen Z, Wang Y, Ratia K, Mesecar AD, Wilkinson KD, Baker SC (2007) Proteolytic processing and deubiquitinating activity of papain-like proteases of human coronavirus NL63. J Virol 81:6007–6018
29. Chen JY, Chen WN, Poon KM, Zheng BJ, Lin X, Wang YX, Wen YM (2009) Interaction between SARS-CoV helicase and a multifunctional cellular protein (Ddx5) revealed by yeast and mammalian cell two-hybrid systems. Arch Virol 154:507–512
30. Choi KS, Huang P, Lai MM (2002) Polypyrimidine-tract-binding protein affects transcription but not translation of mouse hepatitis virus RNA. Virology 303:58–68
31. Choi KS, Mizutani A, Lai MM (2004) SYNCRIP, a member of the heterogeneous nuclear ribonucleoprotein family, is involved in mouse hepatitis virus RNA synthesis. J Virol 78:13153–13162
32. 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
33. 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 LV, Leroy EM, Thiel V, van der Hoek L, Poon LL, Tschapka M, Drosten C, Drexler JF (2015) Evidence for an ancestral association of human coronavirus 229E with bats. J Virol 89:11858–11870
34. Corman VM, Eckerle I, Memish ZA, Liljander AM, Dijkman R, Jonsdottir H, Juma Ngeiywa KJ, Kamau E, Younan M, Al Masri M, Assiri A, Gluecks I, Musa BE, Meyer B, Muller MA, Hilali M, Bornstein S, Wernery U, Thiel V, Jores J, Drexler JF, Drosten C (2016) Link of a ubiquitous human coronavirus to dromedary camels. Proc Natl Acad Sci U S A 113:9864– 9869
35. Cottam EM, Maier HJ, Manifava M, Vaux LC, Chandra-Schoenfelder P, Gerner W, Britton P, Ktistakis NT, Wileman T (2011) Coronavirus nsp6 proteins generate autophagosomes from the endoplasmic reticulum via an omegasome intermediate. Autophagy 7:1335–1347
36. Cottam EM, Whelband MC, Wileman T (2014) Coronavirus NSP6 restricts autophagosome expansion. Autophagy 10:1426–1441
37. Cruz JL, Sola I, Becares M, Alberca B, Plana J, Enjuanes L, Zuniga S (2011) Coronavirus gene 7 counteracts host defenses and modulates virus virulence. PLoS Pathog 7:e1002090
38. Davis TL, Walker JR, Campagna-Slater V, Finerty PJ, Paramanathan R, Bernstein G, MacKenzie F, Tempel W, Ouyang H, Lee WH, Eisenmesser EZ, Dhe-Paganon S (2010) Structural and biochemical characterization of the human cyclophilin family of peptidyl-prolyl isomerases. PLoS Biol 8:e1000439
39. de Groot RJ, Baker SC, Baric RS, Brown CS, Drosten C, Enjuanes L, Fouchier RA, Galiano M, Gorbalenya AE, Memish ZA, Perlman S, Poon LL, Snijder EJ, Stephens GM, Woo PC, 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
40. de Haan CA, Reggiori F (2008) Are nidoviruses hijacking the autophagy machinery? Autophagy 4:276–279
41. de Wilde AH, Zevenhoven-Dobbe JC, van der Meer Y, Thiel V, Narayanan K, Makino S, Snijder EJ, van Hemert MJ (2011) Cyclosporin A inhibits the replication of diverse coronaviruses. J Gen Virol 92:2542–2548
42. de Wilde AH, Li Y, van der Meer Y, Vuagniaux G, Lysek R, Fang Y, Snijder EJ, van Hemert MJ (2013a) Cyclophilin inhibitors block arterivirus replication by interfering with viral RNA synthesis. J Virol 87:1454–1464
43. de Wilde AH, Raj VS, Oudshoorn D, Bestebroer TM, van Nieuwkoop S, Limpens RW, Posthuma CC, van der Meer Y, Barcena M, Haagmans BL, Snijder EJ, van den Hoogen BG (2013b) MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J Gen Virol 94:1749–1760
44. de Wilde AH, Jochmans D, Posthuma CC, Zevenhoven-Dobbe JC, van Nieuwkoop S, Bestebroer TM, van den Hoogen BG, Neyts J, Snijder EJ (2014) Screening of an FDA-approved compound library identifies four small-molecule inhibitors of Middle East respiratory syndrome coronavirus replication in cell culture. Antimicrob Agents Chemother 58:4875–4884
45. de Wilde AH, Wannee KF, Scholte FE, Goeman JJ, Ten Dijke P, Snijder EJ, Kikkert M, van Hemert MJ (2015) A kinome-wide siRNA screen identifies proviral and antiviral host factors in SARS-coronavirus replication, including PKR and early secretory pathway proteins. J Virol 89:8318–8333
46. de Wilde AH, Falzarano D, Zevenhoven-Dobbe JC, Beugeling C, Fett C, Martellaro C, Posthuma CC, Feldmann H, Perlman S, Snijder EJ (2017) Alisporivir inhibits MERS-and SARS-coronavirus replication in cell culture, but not SARS-coronavirus infection in a mouse model. Virus Res 228:7–13
47. Delmas B, Gelfi J, L’Haridon R, Vogel LK, Sjostrom H, Noren O, Laude H (1992) Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357:417–420
48. den Boon JA, Ahlquist P (2010) Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol 64:241–256
49. Ding L, Huang Y, Dai M, Zhao X, Du Q, Dong F, Wang L, Huo R, Zhang W, Xu X, Tong D (2013) Transmissible gastroenteritis virus infection induces cell cycle arrest at S and G2/M phases via p53-dependent pathway. Virus Res 178:241–251
50. Ding L, Huang Y, Du Q, Dong F, Zhao X, Zhang W, Xu X, Tong D (2014) TGEV nucleocapsid protein induces cell cycle arrest and apoptosis through activation of p53 signaling. Biochem Biophys Res Commun 445:497–503
51. Dosch SF, Mahajan SD, Collins AR (2009) SARS coronavirus spike protein-induced innate immune response occurs via activation of the NF-kappaB pathway in human monocyte macrophages in vitro. Virus Res 142:19–27
52. Dove B, Brooks G, Bicknell K, Wurm T, Hiscox JA (2006) Cell cycle perturbations induced by infection with the coronavirus infectious bronchitis virus and their effect on virus replication. J Virol 80:4147–4156
53. Drosten C, Gunther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA, Berger A, Burguiere AM, Cinatl J, Eickmann M, Escriou N, Grywna K, Kramme S, Manuguerra JC, Muller S, Rickerts V, Sturmer M, Vieth S, Klenk HD, Osterhaus AD, Schmitz H, Doerr HW (2003) Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348:1967–1976
54. Du L, He Y, Zhou Y, Liu S, Zheng BJ, Jiang S (2009) The spike protein of SARS-CoV–a target for vaccine and therapeutic development. Nat Rev Microbiol 7:226–236
55. Dusheiko G (1997) Side effects of alpha interferon in chronic hepatitis C. Hepatology 26:112S– 121S
56. Emmott E, Rodgers MA, Macdonald A, McCrory S, Ajuh P, Hiscox JA (2010) Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals changes in the cytoplasmic, nuclear, and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Mol Cell Proteomics 9:1920–1936
57. Emmott E, Munday D, Bickerton E, Britton P, Rodgers MA, Whitehouse A, Zhou EM, Hiscox JA (2013) The cellular interactome of the coronavirus infectious bronchitis virus nucleocapsid protein and functional implications for virus biology. J Virol 87:9486–9500
58. Enjuanes L (2005) Coronavirus replication and reverse genetics. Current Topics in Microbiology and Immunology, vol 287. Springer. doi:10.1007/b138038
59. Favreau DJ, Meessen-Pinard M, Desforges M, Talbot PJ (2012) Human coronavirus-induced neuronal programmed cell death is cyclophilin d dependent and potentially caspase dispensable. J Virol 86:81–93
60. Flisiak R, Jaroszewicz J, Flisiak I, Lapinski T (2012) Update on alisporivir in treatment of viral hepatitis C. Expert Opin Investig Drugs 21:375–382
61. Follis KE, York J, Nunberg JH (2006) Furin cleavage of the SARS coronavirus spike glycoprotein enhances cell-cell fusion but does not affect virion entry. Virology 350:358–369
62. Frieman M, Yount B, Heise M, Kopecky-Bromberg SA, Palese P, Baric RS (2007) Severe acute respiratory syndrome coronavirus ORF6 antagonizes STAT1 function by sequestering nuclear import factors on the rough endoplasmic reticulum/Golgi membrane. J Virol 81:9812–9824
63. Frieman M, Ratia K, Johnston RE, Mesecar AD, Baric RS (2009) Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-kappaB signaling. J Virol 83:6689–6705
64. Fung TS, Liao Y, Liu DX (2016) Regulation of stress responses and translational control by coronavirus. Viruses 8:184
65. Furuya T, Lai MM (1993) Three different cellular proteins bind to complementary sites on the 5′-end-positive and 3′-end-negative strands of mouse hepatitis virus RNA. J Virol 67:7215–7222
66. Galan C, Sola I, Nogales A, Thomas B, Akoulitchev A, Enjuanes L, Almazan F (2009) Host cell proteins interacting with the 3′ end of TGEV coronavirus genome influence virus replication. Virology 391:304–314
67. Garlinghouse LE Jr, Smith AL, Holford T (1984) The biological relationship of mouse hepatitis virus (MHV) strains and interferon: in vitro induction and sensitivities. Arch Virol 82:19–29
68. Ge XY, Li JL, Yang XL, Chmura AA, Zhu G, Epstein JH, Mazet JK, Hu B, Zhang W, Peng C, Zhang YJ, Luo CM, Tan B, Wang N, Zhu Y, Crameri G, Zhang SY, Wang LF, Daszak P, Shi ZL (2013) Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503:535–538
69. Glowacka I, Bertram S, Muller MA, Allen P, Soilleux E, Pfefferle S, Steffen I, Tsegaye TS, He Y, Gnirss K, Niemeyer D, Schneider H, Drosten C, Pohlmann S (2011) Evidence that TMPRSS2 activates the severe acute respiratory syndrome coronavirus spike protein for membrane fusion and reduces viral control by the humoral immune response. J Virol 85:4122–4134
70. Gosert R, Kanjanahaluethai A, Egger D, Bienz K, Baker SC (2002) RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 76:3697–3708
71. Gralinski LE, Ferris MT, Aylor DL, Whitmore AC, Green R, Frieman MB, Deming D, Menachery VD, Miller DR, Buus RJ, Bell TA, Churchill GA, Threadgill DW, Katze MG, McMillan L, Valdar W, Heise MT, Pardo-Manuel de Villena F, Baric RS (2015) Genome wide identification of SARS-CoV susceptibility loci using the collaborative cross. PLoS Genet 11: e1005504
72. Haagmans BL, Kuiken T, Martina BE, Fouchier RA, Rimmelzwaan GF, van Amerongen G, van Riel D, de Jong T, Itamura S, Chan KH, Tashiro M, Osterhaus AD (2004) Pegylated interferon-alpha protects type 1 pneumocytes against SARS coronavirus infection in macaques. Nat Med 10:290–293
73. Hagemeijer MC, Rottier PJ, de Haan CA (2012) Biogenesis and dynamics of the coronavirus replicative structures. Viruses 4:3245–3269
74. Hagemeijer MC, Monastyrska I, Griffith J, van der Sluijs P, Voortman J, van Bergen en Henegouwen PM, Vonk AM, Rottier PJ, Reggiori F, de Haan CA (2014) Membrane rearrangements mediated by coronavirus nonstructural proteins 3 and 4. Virology 458– 459:125–135
75. Hamre D, Procknow JJ (1966) A new virus isolated from the human respiratory tract. Proc Soc Exp Biol Med 121:190–193
76. Hopkins S, Gallay PA (2015) The role of immunophilins in viral infection. Biochim Biophys Acta 1850:2103–2110
77. Horowitz DS, Lee EJ, Mabon SA, Misteli T (2002) A cyclophilin functions in pre-mRNA splicing. EMBO J 21:470–480
78. Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, Takvorian PM, Pau C, van der Schaar H, Kaushik-Basu N, Balla T, Cameron CE, Ehrenfeld E, van Kuppeveld FJ, Altan-Bonnet N (2010) Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:799–811
79. Huang P, Lai MM (1999) Polypyrimidine tract-binding protein binds to the complementary strand of the mouse hepatitis virus 3′ untranslated region, thereby altering RNA conformation. J Virol 73:9110–9116
80. Huang P, Lai MM (2001) Heterogeneous nuclear ribonucleoprotein a1 binds to the 3′-untranslated region and mediates potential 5′-3′-end cross talks of mouse hepatitis virus RNA. J Virol 75:5009–5017
81. Huang IC, Bosch BJ, Li F, Li W, Lee KH, Ghiran S, Vasilieva N, Dermody TS, Harrison SC, Dormitzer PR, Farzan M, Rottier PJ, Choe H (2006a) SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J Biol Chem 281:3198–3203
82. Huang IC, Bosch BJ, Li W, Farzan M, Rottier PM, Choe H (2006b) SARS-CoV, but not HCoV-NL63, utilizes cathepsins to infect cells: viral entry. Adv Exp Med Biol 581:335–338
83. Huang SH, Lee TY, Lin YJ, Wan L, Lai CH, Lin CW (2015a) Phage display technique identifies the interaction of severe acute respiratory syndrome coronavirus open reading frame 6 protein with nuclear pore complex interacting protein NPIPB3 in modulating type I interferon antagonism. J Microbiol Immunol Infect. doi:10.1016/j.jmii.2015.07.002
84. Huang X, Dong W, Milewska A, Golda A, Qi Y, Zhu QK, Marasco WA, Baric RS, Sims AC, Pyrc K, Li W, Sui J (2015b) Human coronavirus HKU1 spike protein uses O-acetylated sialic acid as an attachment receptor determinant and employs hemagglutinin-esterase protein as a receptor-destroying enzyme. J Virol 89:7202–7213
85. Hulswit RJ, de Haan CA, Bosch BJ (2016) Coronavirus spike protein and tropism changes. Adv Virus Res 96:29–57
86. Huynh J, Li S, Yount B, Smith A, Sturges L, Olsen JC, Nagel J, Johnson JB, Agnihothram 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
87. Jackson AL, Linsley PS (2010) Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat Rev Drug Discov 9:57–67
88. Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11:113–127
89. Jiang X, Chen ZJ (2012) The role of ubiquitylation in immune defence and pathogen evasion. Nat Rev Immunol 12:35–48
90. Jimenez-Guardeno JM, Nieto-Torres JL, DeDiego ML, Regla-Nava JA, Fernandez-Delgado R, Castano-Rodriguez C, Enjuanes L (2014) The PDZ-binding motif of severe acute respiratory syndrome coronavirus envelope protein is a determinant of viral pathogenesis. PLoS Pathog 10:e1004320
91. Kamitani W, Narayanan K, Huang C, Lokugamage K, Ikegami T, Ito N, Kubo H, Makino S (2006) Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Natl Acad Sci USA 103:12885–12890
92. Kamitani W, Huang C, Narayanan K, Lokugamage KG, Makino S (2009) A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat Struct Mol Biol 16:1134–1140
93. Keogh-Brown MR, Smith RD (2008) The economic impact of SARS: how does the reality match the predictions? Health Policy 88:110–120
94. Keyaerts E, Vijgen L, Maes P, Neyts J, Van Ranst M (2004) In vitro inhibition of severe acute respiratory syndrome coronavirus by chloroquine. Biochem Biophys Res Commun 323: 264–268
95. Keyaerts E, Li S, Vijgen L, Rysman E, Verbeeck J, Van Ranst M, Maes P (2009) Antiviral activity of chloroquine against human coronavirus OC43 infection in newborn mice. Antimicrob Agents Chemother 53:3416–3421
96. Khanolkar A, Hartwig SM, Haag BA, Meyerholz DK, Harty JT, Varga SM (2009) Toll-like receptor 4 deficiency increases disease and mortality after mouse hepatitis virus type 1 infection of susceptible C3H mice. J Virol 83:8946–8956
97. Kim Y, Lee C (2014) Porcine epidemic diarrhea virus induces caspase-independent apoptosis through activation of mitochondrial apoptosis-inducing factor. Virology 460–461:180–193
98. Kim Y, Liu H, Galasiti Kankanamalage AC, Weerasekara S, Hua DH, Groutas WC, Chang KO, Pedersen NC (2016) Reversal of the progression of fatal coronavirus infection in cats by a broad-spectrum coronavirus protease inhibitor. PLoS Pathog 12:e1005531
99. Kindler E, Thiel V (2014) To sense or not to sense viral RNA–essentials of coronavirus innate immune evasion. Curr Opin Microbiol 20:69–75
100. Knoops K, Kikkert M, van den Worm SH, Zevenhoven-Dobbe JC, van der Meer Y, Koster AJ, Mommaas AM, Snijder EJ (2008) SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol 6:e226
101. Knoops K, Swett-Tapia C, van den Worm SH, te Velthuis AJ, Koster AJ, Mommaas AM, Snijder EJ, Kikkert M (2010) Integrity of the early secretory pathway promotes, but is not required for, severe acute respiratory syndrome coronavirus RNA synthesis and virus-induced remodeling of endoplasmic reticulum membranes. J Virol 84:833–846
102. Kono M, Tatsumi K, Imai AM, Saito K, Kuriyama T, Shirasawa H (2008) Inhibition of human coronavirus 229E infection in human epithelial lung cells (L132) by chloroquine: involvement of p38 MAPK and ERK. Antiviral Res 77:150–152
103. Kopecky-Bromberg SA, Martinez-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
104. Krempl C, Schultze B, Herrler G (1995) Analysis of cellular receptors for human coronavirus OC43. Adv Exp Med Biol 380:371–374
105. Krzystyniak K, Dupuy JM (1984) Entry of mouse hepatitis virus 3 into cells. J Gen Virol 65: 227–231
106. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W, Rollin PE, Dowell SF, Ling AE, Humphrey CD, Shieh WJ, Guarner J, Paddock CD, Rota P, Fields B, DeRisi J, Yang JY, Cox N, Hughes JM, LeDuc JW, Bellini WJ, Anderson LJ, Group SW (2003) A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348:1953–1966
107. Kuiken T, Fouchier RA, Schutten M, Rimmelzwaan GF, van Amerongen G, van Riel D, Laman JD, de Jong T, van Doornum G, Lim W, Ling AE, Chan PK, Tam JS, Zambon MC, Gopal R, Drosten C, van der Werf S, Escriou N, Manuguerra JC, Stohr K, Peiris JS, Osterhaus AD (2003) Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263–270
108. Kwak H, Park MW, Jeong S (2011) Annexin A2 binds RNA and reduces the frameshifting efficiency of infectious bronchitis virus. PLoS ONE 6:e24067
109. Langereis MA, van Vliet AL, Boot W, de Groot RJ (2010) Attachment of mouse hepatitis virus to O-acetylated sialic acid is mediated by hemagglutinin-esterase and not by the spike protein. J Virol 84:8970–8974
110. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY (2005) Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci USA 102:14040–14045
111. Li F (2008) Structural analysis of major species barriers between humans and palm civets for severe acute respiratory syndrome coronavirus infections. J Virol 82:6984–6991
112. Li F (2016) Structure, function, and evolution of coronavirus spike proteins. Annu Rev Virol 3:237–261
113. Li Y, Weiss SR (2016) Antagonism of RNase L Is required for murine coronavirus replication in kupffer cells and liver sinusoidal endothelial cells but not in hepatocytes. J Virol 90:9826–9832
114. Li HP, Zhang X, Duncan R, Comai L, Lai MM (1997) Heterogeneous nuclear ribonucleoprotein A1 binds to the transcription-regulatory region of mouse hepatitis virus RNA. Proc Natl Acad Sci USA 94:9544–9549
115. Li HP, Huang P, Park S, Lai MM (1999) Polypyrimidine tract-binding protein binds to the leader RNA of mouse hepatitis virus and serves as a regulator of viral transcription. J Virol 73: 772–777
116. 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
117. Li Q, Wang L, Dong C, Che Y, Jiang L, Liu L, Zhao H, Liao Y, Sheng Y, Dong S, Ma S (2005a) The interaction of the SARS coronavirus non-structural protein 10 with the cellular oxido-reductase system causes an extensive cytopathic effect. J Clin Virol: The Official Publication of the Pan American Society for Clinical Virology 34:133–139
118. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF (2005b) Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676–679
119. Li W, Zhang C, Sui J, Kuhn JH, Moore MJ, Luo S, Wong SK, Huang IC, Xu K, Vasilieva N, Murakami A, He Y, Marasco WA, Guan Y, Choe H, Farzan M (2005c) Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J 24:1634–1643
120. Li BX, Ge JW, Li YJ (2007) Porcine aminopeptidase N is a functional receptor for the PEDV coronavirus. Virology 365:166–172
121. 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
122. Li SW, Wang CY, Jou YJ, Huang SH, Hsiao LH, Wan L, Lin YJ, Kung SH, Lin CW (2016) SARS coronavirus papain-like protease inhibits the TLR7 signaling pathway through removing Lys63-linked polyubiquitination of TRAF3 and TRAF6. Int J Mol Sci 17:678
123. Liao Y, Wang X, Huang M, Tam JP, Liu DX (2011) Regulation of the p38 mitogen-activated protein kinase and dual-specificity phosphatase 1 feedback loop modulates the induction of interleukin 6 and 8 in cells infected with coronavirus infectious bronchitis virus. Virology 420:106–116
124. Lin CM, Saif LJ, Marthaler D, Wang Q (2016) Evolution, antigenicity and pathogenicity of global porcine epidemic diarrhea virus strains. Virus Res 226:20–39
125. Liu C, Tang J, Ma Y, Liang X, Yang Y, Peng G, Qi Q, Jiang S, Li J, Du L, Li F (2015) Receptor usage and cell entry of porcine epidemic diarrhea coronavirus. J Virol 89:6121–6125
126. Lokugamage KG, Narayanan K, Huang C, Makino S (2012) SARS coronavirus nsp1 protein is a novel eukaryotic translation inhibitor that represses multiple steps of translation initiation. J Virol 86:13598–13608
127. Lokugamage KG, Narayanan K, Nakagawa K, Terasaki K, Ramirez SI, Tseng CT, 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
128. Lu X, Pan J, Tao J, Guo D (2011) SARS-CoV nucleocapsid protein antagonizes IFN-beta response by targeting initial step of IFN-beta induction pathway, and its C-terminal region is critical for the antagonism. Virus Genes 42:37–45
129. Lui PY, Wong LY, Fung CL, Siu KL, Yeung ML, Yuen KS, Chan CP, Woo PC, Yuen KY, Jin DY (2016) Middle East respiratory syndrome coronavirus M protein suppresses type I interferon expression through the inhibition of TBK1-dependent phosphorylation of IRF3. Emerg Microbes Infect 5:e39
130. Luo C, Luo H, Zheng S, Gui C, Yue L, Yu C, Sun T, He P, Chen J, Shen J, Luo X, Li Y, Liu H, Bai D, Yang Y, Li F, Zuo J, Hilgenfeld R, Pei G, Chen K, Shen X, Jiang H (2004) Nucleocapsid protein of SARS coronavirus tightly binds to human cyclophilin A. Biochem Biophys Res Commun 321:557–565
131. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, Zona L, Davis C, Mee CJ, Turek M, Gorke S, Royer C, Fischer B, Zahid MN, Lavillette D, Fresquet J, Cosset FL, Rothenberg SM, Pietschmann T, Patel AH, Pessaux P, Doffoel M, Raffelsberger W, Poch O, McKeating JA, Brino L, Baumert TF (2011) EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 17:589–595
132. Maier HJ, Britton P (2012) Involvement of autophagy in coronavirus replication. Viruses 4:3440– 3451
133. Maier HJ, Hawes PC, Cottam EM, Mantell J, Verkade P, Monaghan P, Wileman T, Britton P (2013) Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes. MBio 4:e00801–e00813
134. Ma-Lauer Y, Carbajo-Lozoya J, Hein MY, Muller MA, Deng W, Lei J, Meyer B, Kusov Y, von Brunn B, Bairad DR, Hunten S, Drosten C, Hermeking H, Leonhardt H, Mann M, Hilgenfeld R, von Brunn A (2016) p53 down-regulates SARS coronavirus replication and is targeted by the SARS-unique domain and PLpro via E3 ubiquitin ligase RCHY1. Proc Natl Acad Sci USA 113:E5192–E5201
135. Matthews K, Schafer A, Pham A, Frieman M (2014a) The SARS coronavirus papain like protease can inhibit IRF3 at a post activation step that requires deubiquitination activity. Virol J 11:209
136. Matthews KL, Coleman CM, van der Meer Y, Snijder EJ, Frieman MB (2014b) 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 95:874–882
137. 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
138. 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
139. Menachery VD, Yount BL Jr, Josset L, Gralinski LE, Scobey T, Agnihothram S, Katze MG, Baric RS (2014) Attenuation and restoration of severe acute respiratory syndrome coronavirus mutant lacking 2′-o-methyltransferase activity. J Virol 88:4251–4264
140. Menachery VD, Yount BL Jr, Debbink K, Agnihothram S, Gralinski LE, Plante JA, Graham RL, Scobey T, Ge XY, Donaldson EF, Randell SH, Lanzavecchia A, Marasco WA, Shi ZL, Baric RS (2015) A SARS-like cluster of circulating bat coronaviruses shows potential for human emergence. Nat Med 21:1508–1513
141. Mielech AM, Chen Y, Mesecar AD, Baker SC (2014) Nidovirus papain-like proteases: multifunctional enzymes with protease, deubiquitinating and deISGylating activities. Virus Res 194:184–190
142. Mizutani T (2007) Signal transduction in SARS-CoV-infected cells. Ann N Y Acad Sci 1102: 86–95
143. Monastyrska I, Ulasli M, Rottier PJ, Guan JL, Reggiori F, de Haan CA (2013) An autophagy-independent role for LC3 in equine arteritis virus replication. Autophagy 9:164–174
144. Moser TS, Jones RG, Thompson CB, Coyne CB, Cherry S (2010) A kinome RNAi screen identified AMPK as promoting poxvirus entry through the control of actin dynamics. PLoS Pathog 6:e1000954
145. Muller MA, Corman VM, Jores J, Meyer B, Younan M, Liljander A, Bosch BJ, Lattwein E, Hilali M, Musa BE, Bornstein S, Drosten C (2014) MERS coronavirus neutralizing antibodies in camels, Eastern Africa, 1983–1997. Emerg Infect Dis 20:2093–2095
146. Nanda SK, Leibowitz JL (2001) Mitochondrial aconitase binds to the 3′ untranslated region of the mouse hepatitis virus genome. J Virol 75:3352–3362
147. Nanda SK, Johnson RF, Liu Q, Leibowitz JL (2004) Mitochondrial HSP70, HSP40, and HSP60 bind to the 3′ untranslated region of the murine hepatitis virus genome. Arch Virol 149:93–111
148. Narayanan K, Ramirez SI, Lokugamage KG, Makino S (2015) Coronavirus nonstructural protein 1: common and distinct functions in the regulation of host and viral gene expression. Virus Res 202:89–100
149. Neuman BW, Joseph JS, Saikatendu KS, Serrano P, Chatterjee A, Johnson MA, Liao L, Klaus JP, Yates JR 3rd, Wuthrich K, Stevens RC, Buchmeier MJ, Kuhn P (2008) Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J Virol 82:5279–5294
150. Ng LF, Hibberd ML, Ooi EE, Tang KF, Neo SY, Tan J, Murthy KR, Vega VB, Chia JM, Liu ET, Ren EC (2004) A human in vitro model system for investigating genome-wide host responses to SARS coronavirus infection. BMC Infect Dis 4:34
151. Niemeyer D, Zillinger T, Muth D, Zielecki F, Horvath G, Suliman T, Barchet W, Weber F, Drosten C, Muller MA (2013) Middle East respiratory syndrome coronavirus accessory protein 4a is a type I interferon antagonist. J Virol 87:12489–12495
152. Nieto-Torres JL, Verdia-Baguena C, Jimenez-Guardeno JM, Regla-Nava JA, Castano-Rodriguez C, Fernandez-Delgado R, Torres J, Aguilella VM, Enjuanes L (2015) Severe acute respiratory syndrome coronavirus E protein transports calcium ions and activates the NLRP3 inflammasome. Virology 485:330–339
153. Nigg EA (1995) Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 17:471–480
154. Oostra M, te Lintelo EG, Deijs M, Verheije MH, Rottier PJ, de Haan CA (2007) Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J Virol 81:12323–12336
155. Paeshuyse J, Kaul A, De Clercq E, Rosenwirth B, Dumont JM, Scalfaro P, Bartenschlager R, Neyts J (2006) The non-immunosuppressive cyclosporin DEBIO-025 is a potent inhibitor of hepatitis C virus replication in vitro. Hepatology 43:761–770
156. Paragas J, Blatt LM, Hartmann C, Huggins JW, Endy TP (2005) Interferon alfacon1 is an inhibitor of SARS-corona virus in cell-based models. Antiviral Res 66:99–102
157. Park JE, Li K, Barlan A, Fehr AR, Perlman S, McCray PB Jr, Gallagher T (2016) Proteolytic processing of Middle East respiratory syndrome coronavirus spikes expands virus tropism. Proc Natl Acad Sci USA 113:12262–12267
158. Paul D, Madan V, Bartenschlager R (2014) Hepatitis C virus RNA replication and assembly: living on the fat of the land. Cell Host Microbe 16:569–579
159. Payne HR, Storz J, Henk WG (1990) Initial events in bovine coronavirus infection: analysis through immunogold probes and lysosomotropic inhibitors. Arch Virol 114:175–189
160. Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, Lim W, Nicholls J, Yee WK, Yan WW, Cheung MT, Cheng VC, Chan KH, Tsang DN, Yung RW, Ng TK, Yuen KY, group Ss (2003) Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319–1325
161. Perlman S, Netland J (2009) Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol 7:439–450
162. Pfefferle S, Schopf J, Kogl M, Friedel CC, Muller MA, Carbajo-Lozoya J, Stellberger T, von Dall’armi E, Herzog P, Kallies S, Niemeyer D, Ditt V, Kuri T, Zust R, Pumpor K, Hilgenfeld R, Schwarz F, Zimmer R, Steffen I, Weber F, Thiel V, Herrler G, Thiel HJ, Schwegmann-Wessels C, Pohlmann S, Haas J, Drosten C, von Brunn A (2011) The SARS-coronavirus-host interactome: identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog 7:e1002331
163. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR (2004) Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 279:10136–10141
164. Raaben M, Groot Koerkamp MJ, Rottier PJ, de Haan CA (2007) Mouse hepatitis coronavirus replication induces host translational shutoff and mRNA decay, with concomitant formation of stress granules and processing bodies. Cell Microbiol 9:2218–2229
165. Rabouw HH, Langereis MA, Knaap RC, Dalebout TJ, Canton J, Sola I, Enjuanes L, Bredenbeek PJ, Kikkert M, de Groot RJ, van Kuppeveld FJ (2016) Middle East respiratory coronavirus accessory protein 4a inhibits PKR-mediated antiviral stress responses. PLoS Pathog 12:e1005982
166. Raj VS, Mou H, Smits SL, Dekkers DH, Muller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, Thiel V, Drosten C, Rottier PJ, Osterhaus AD, Bosch BJ, Haagmans BL (2013) Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251–254
167. Reggiori F, Monastyrska I, Verheije MH, Cali T, Ulasli M, Bianchi S, Bernasconi R, de Haan CA, Molinari M (2010) Coronaviruses Hijack the LC3-I-positive EDEMosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 7:500–508
168. Reid CR, Airo AM, Hobman TC (2015) The virus-host interplay: biogenesis of +RNA replication complexes. Viruses 7:4385–4413
169. Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H, Matula P, Kaderali L, Poenisch M, Blankenburg H, Hiet MS, Longerich T, Diehl S, Ramirez F, Balla T, Rohr K, Kaul A, Buhler S, Pepperkok R, Lengauer T, Albrecht M, Eils R, Schirmacher P, Lohmann V, Bartenschlager R (2011) Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 9:32–45
170. Rempel JD, Quina LA, Blakely-Gonzales PK, Buchmeier MJ, Gruol DL (2005) Viral induction of central nervous system innate immune responses. J Virol 79:4369–4381
171. Romero-Brey I, Bartenschlager R (2016) Endoplasmic reticulum: the favorite intracellular niche for viral replication and assembly. Viruses 8:E160
172. Sawicki SG, Sawicki DL (1995) Coronaviruses use discontinuous extension for synthesis of subgenome-length negative strands. Adv Exp Med Biol 380:499–506
173. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ (2005) Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci USA 102:12005–12010
174. Schoggins JW, Rice CM (2011) Interferon-stimulated genes and their antiviral effector functions. Curr opin virol 1:519–525
175. Schultze B, Herrler G (1992) Bovine coronavirus uses N-acetyl-9-O-acetylneuraminic acid as a receptor determinant to initiate the infection of cultured cells. J Gen Virol 73(Pt 4):901–906
176. Schultze B, Enjuanes L, Cavanagh D, Herrler G (1993) N-acetylneuraminic acid plays a critical role for the haemagglutinating activity of avian infectious bronchitis virus and porcine transmissible gastroenteritis virus. Adv Exp Med Biol 342:305–310
177. Schultze B, Krempl C, Ballesteros ML, Shaw L, Schauer R, Enjuanes L, Herrler G (1996) Transmissible gastroenteritis coronavirus, but not the related porcine respiratory coronavirus, has a sialic acid (N-glycolylneuraminic acid) binding activity. J Virol 70:5634–5637
178. Selinger C, Tisoncik-Go J, Menachery VD, Agnihothram S, Law GL, Chang J, Kelly SM, Sova P, Baric RS, Katze MG (2014) Cytokine systems approach demonstrates differences in innate and pro-inflammatory host responses between genetically distinct MERS-CoV isolates. BMC Genom 15:1161
179. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87
180. Shen X, Masters PS (2001) Evaluation of the role of heterogeneous nuclear ribonucleoprotein A1 as a host factor in murine coronavirus discontinuous transcription and genome replication. Proc Natl Acad Sci USA 98:2717–2722
181. Shi ST, Huang P, Li HP, Lai MM (2000) Heterogeneous nuclear ribonucleoprotein A1 regulates RNA synthesis of a cytoplasmic virus. EMBO J 19:4701–4711
182. Shi ST, Yu GY, Lai MM (2003) Multiple type A/B heterogeneous nuclear ribonucleoproteins (hnRNPs) can replace hnRNP A1 in mouse hepatitis virus RNA synthesis. J Virol 77:10584– 10593
183. 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
184. Simmons G, Gosalia DN, Rennekamp AJ, Reeves JD, Diamond SL, Bates P (2005) Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc Natl Acad Sci U S A 102:11876–11881
185. Siu KL, Kok KH, Ng MH, Poon VK, 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/IKKepsilon complex. J Biol Chem 284:16202–16209
186. Siu KL, Yeung ML, Kok KH, Yuen KS, Kew C, Lui PY, Chan CP, Tse H, Woo PC, Yuen KY, Jin DY (2014) 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
187. Snijder EJ, van der Meer Y, Zevenhoven-Dobbe J, Onderwater JJ, van der Meulen J, Koerten HK, Mommaas AM (2006) Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol 80:5927–5940
188. Snijder EJ, Decroly E, Ziebuhr J (2016) The nonstructural proteins directing coronavirus RNA synthesis and processing. Adv Virus Res 96:59–126
189. Sola I, Almazan F, Zuniga S, Enjuanes L (2015) Continuous and discontinuous RNA synthesis in coronaviruses. Annu Rev Virol 2:265–288
190. Song S, Bi J, Wang D, Fang L, Zhang L, Li F, Chen H, Xiao S (2013) Porcine reproductive and respiratory syndrome virus infection activates IL-10 production through NF-kappaB and p38 MAPK pathways in porcine alveolar macrophages. Dev Comp Immunol 39:265–272
191. Spagnolo JF, Hogue BG (2000) Host protein interactions with the 3′ end of bovine coronavirus RNA and the requirement of the poly(A) tail for coronavirus defective genome replication. J Virol 74:5053–5065
192. Stertz S, Reichelt M, Spiegel M, Kuri T, Martinez-Sobrido L, Garcia-Sastre A, Weber F, Kochs G (2007) The intracellular sites of early replication and budding of SARS-coronavirus. Virology 361:304–315
193. Supekova L, Supek F, Lee J, Chen S, Gray N, Pezacki JP, Schlapbach A, Schultz PG (2008) Identification of human kinases involved in hepatitis C virus replication by small interference RNA library screening. J Biol Chem 283:29–36
194. Surjit M, Liu B, Chow VT, Lal SK (2006) The nucleocapsid protein of severe acute respiratory syndrome-coronavirus inhibits the activity of cyclin-cyclin-dependent kinase complex and blocks S phase progression in mammalian cells. J Biol Chem 281:10669–10681
195. Taguchi F, Siddell SG (1985) Difference in sensitivity to interferon among mouse hepatitis viruses with high and low virulence for mice. Virology 147:41–48
196. Takano T, Katoh Y, Doki T, Hohdatsu T (2013) Effect of chloroquine on feline infectious peritonitis virus infection in vitro and in vivo. Antiviral Res 99:100–107
197. Tan YW, Hong W, Liu DX (2012) Binding of the 5′-untranslated region of coronavirus RNA to zinc finger CCHC-type and RNA-binding motif 1 enhances viral replication and transcription. Nucleic Acids Res 40:5065–5077
198. Tanaka Y, Sato Y, Osawa S, Inoue M, Tanaka S, Sasaki T (2012) Suppression of feline coronavirus replication in vitro by cyclosporin A. Vet Res 43:41
199. Tanaka Y, Sato Y, Sasaki T (2013) Suppression of coronavirus replication by cyclophilin inhibitors. Viruses 5:1250–1260
200. Tanaka Y, Sato Y, Sasaki T (2016) Feline coronavirus replication is affected by both cyclophilin A and cyclophilin B. J Gen Virol 98:190–200
201. Teigelkamp S, Achsel T, Mundt C, Gothel SF, Cronshagen U, Lane WS, Marahiel M, Luhrmann R (1998) The 20kD protein of human [U4/U6.U5] tri-snRNPs is a novel cyclophilin that forms a complex with the U4/U6-specific 60kD and 90kD proteins. RNA 4:127–141
202. Thornbrough JM, Jha BK, Yount B, Goldstein SA, Li Y, Elliott R, Sims AC, Baric RS, Silverman RH, Weiss SR (2016) Middle East respiratory syndrome coronavirus NS4b protein inhibits host RNase L activation. MBio 7:e00258
203. Totura AL, Baric RS (2012) SARS coronavirus pathogenesis: host innate immune responses and viral antagonism of interferon. Curr Opin Virol 2:264–275
204. Totura AL, Whitmore A, Agnihothram S, Schafer A, Katze MG, Heise MT, 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:e00638–e00615
205. Tresnan DB, Levis R, Holmes KV (1996) Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J Virol 70:8669–8674
206. Ulasli M, Verheije MH, de Haan CA, Reggiori F (2010) Qualitative and quantitative ultrastructural analysis of the membrane rearrangements induced by coronavirus. Cell Microbiol 12:844–861
207. van Boheemen S, de Graaf M, Lauber C, Bestebroer TM, Raj VS, Zaki AM, Osterhaus AD, Haagmans BL, Gorbalenya AE, Snijder EJ, Fouchier RA (2012) Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. MBio 3:e00412–e00473
208. van der Hoek L (2007) Human coronaviruses: what do they cause? Antiviral therapy 12:651–658
209. van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJ, Wolthers KC, Wertheim-van Dillen PM, Kaandorp J, Spaargaren J, Berkhout B (2004) Identification of a new human coronavirus. Nat Med 10:368–373
210. van der Hoeven B, Oudshoorn D, Koster AJ, Snijder EJ, Kikkert M, Barcena M (2016) Biogenesis and architecture of arterivirus replication organelles. Virus Res 220:70–90
211. van der Meer Y, Snijder EJ, Dobbe JC, Schleich S, Denison MR, Spaan WJ, Krijnse Locker J (1999) Localization of mouse hepatitis virus nonstructural proteins and RNA synthesis indicates a role for late endosomes in viral replication. J Virol 73:7641–7657
212. van der Schaar HM, Dorobantu CM, Albulescu L, Strating JR, van Kuppeveld FJ (2016) Fat(al) attraction: picornaviruses usurp lipid transfer at membrane contact sites to create replication organelles. Trends Microbiol 24:535–546
213. van Hemert MJ, van den Worm SH, Knoops K, Mommaas AM, Gorbalenya AE, Snijder EJ (2008) SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro. PLoS Pathog 4:e1000054
214. van Kasteren PB, Bailey-Elkin BA, James TW, Ninaber DK, Beugeling C, Khajehpour M, Snijder EJ, Mark BL, Kikkert M (2013) Deubiquitinase function of arterivirus papain-like protease 2 suppresses the innate immune response in infected host cells. Proc Natl Acad Sci USA 110:E838–E847
215. Verheije MH, Raaben M, Mari M, Te Lintelo EG, Reggiori F, van Kuppeveld FJ, Rottier PJ, de Haan CA (2008) Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathog 4:e1000088
216. Versteeg GA, Slobodskaya O, Spaan WJ (2006) Transcriptional profiling of acute cytopathic murine hepatitis virus infection in fibroblast-like cells. J Gen Virol 87:1961–1975
217. Vijay R, Perlman S (2016) Middle East respiratory syndrome and severe acute respiratory syndrome. Curr Opin Virol 16:70–76
218. Vijgen L, Keyaerts E, Lemey P, Maes P, Van Reeth K, Nauwynck H, Pensaert M, Van Ranst M (2006) Evolutionary history of the closely related group 2 coronaviruses: porcine hemagglu-tinating encephalomyelitis virus, bovine coronavirus, and human coronavirus OC43. J Virol 80:7270–7274
219. Vogels MW, van Balkom BW, Kaloyanova DV, Batenburg JJ, Heck AJ, Helms JB, Rottier PJ, de Haan CA (2011) Identification of host factors involved in coronavirus replication by quantitative proteomics analysis. Proteomics 11:64–80
220. von Brunn A, Ciesek S, von Brunn B, Carbajo-Lozoya J (2015) Genetic deficiency and polymorphisms of cyclophilin a reveal its essential role for human coronavirus 229E replication. Curr Opin Virol 14:56–61
221. Walls AC, Tortorici MA, Bosch BJ, Frenz B, Rottier PJ, DiMaio F, Rey FA, Veesler D (2016) Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531:114–117
222. Walsh D, Mohr I (2011) Viral subversion of the host protein synthesis machinery. Nat Rev Microbiol 9:860–875
223. Wang Y, Liu L (2016) The membrane protein of severe acute respiratory syndrome coronavirus functions as a novel cytosolic pathogen-associated molecular pattern to promote beta interferon induction via a toll-like-receptor-related TRAF3-independent mechanism. MBio 7:e01872– e01815
224. Wang X, Liao Y, Yap PL, Png KJ, Tam JP, Liu DX (2009) Inhibition of protein kinase R activation and upregulation of GADD34 expression play a synergistic role in facilitating coronavirus replication by maintaining de novo protein synthesis in virus-infected cells. J Virol 83:12462–12472
225. Wang G, Chen G, Zheng D, Cheng G, Tang H (2011) PLP2 of mouse hepatitis virus A59 (MHV-A59) targets TBK1 to negatively regulate cellular type I interferon signaling pathway. PLoS ONE 6:e17192
226. Wang D, Fang L, Shi Y, Zhang H, Gao L, Peng G, Chen H, Li K, Xiao S (2015) Porcine epidemic diarrhea virus 3C-like protease regulates its interferon antagonism by cleaving NEMO. J Virol 90:2090–2101
227. Wathelet MG, Orr M, Frieman MB, Baric RS (2007) Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J Virol 81:11620–11633
228. WHO (2004) SARS website. http://www.who.int/csr/sars/country/table2004_04_21/
229. WHO (2016) http://www.who.int/emergencies/mers-cov/en/
230. Wilkins C, Gale M Jr (2010) Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 22:41–47
231. Williams RK, Jiang GS, Holmes KV (1991) Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc Natl Acad Sci U S A 88:5533–5536
232. Wong HH, Kumar P, Tay FP, Moreau D, Liu DX, Bard F (2015) Genome-wide screen reveals valosin-containing protein requirement for coronavirus exit from endosomes. J Virol 89:11116–11128
233. Woo PC, Lau SK, Chu CM, Chan KH, Tsoi HW, Huang Y, Wong BH, Poon RW, Cai JJ, Luk WK, Poon LL, Wong SS, Guan Y, Peiris JS, Yuen KY (2005) Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J Virol 79:884–895
234. Wu K, Li W, Peng G, Li F (2009) Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor. Proc Natl Acad Sci U S A 106:19970–19974
235. Wu CH, Chen PJ, Yeh SH (2014) Nucleocapsid phosphorylation and RNA helicase DDX1 recruitment enables coronavirus transition from discontinuous to continuous transcription. Cell Host Microbe 16:462–472
236. Xiao H, Xu LH, Yamada Y, Liu DX (2008) Coronavirus spike protein inhibits host cell translation by interaction with eIF3f. PLoS ONE 3:e1494
237. Xu L, Khadijah S, Fang S, Wang L, Tay FP, Liu DX (2010) The cellular RNA helicase DDX1 interacts with coronavirus nonstructural protein 14 and enhances viral replication. J Virol 84:8571–8583
238. Xu LH, Huang M, Fang SG, Liu DX (2011) Coronavirus infection induces DNA replication stress partly through interaction of its nonstructural protein 13 with the p125 subunit of DNA polymerase delta. J Biol Chem 286:39546–39559
239. Yang D, Leibowitz JL (2015) The structure and functions of coronavirus genomic 3′ and 5′ ends. Virus Res 206:120–133
240. Yang N, Ma P, Lang J, Zhang Y, Deng J, Ju X, Zhang G, Jiang C (2012) Phosphatidylinositol 4-kinase IIIbeta is required for severe acute respiratory syndrome coronavirus spike-mediated cell entry. J Biol Chem 287:8457–8467
241. 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
242. Yang Y, Du L, Liu C, Wang L, Ma C, Tang J, Baric RS, Jiang S, Li F (2014) Receptor usage and cell entry of bat coronavirus HKU4 provide insight into bat-to-human transmission of MERS coronavirus. Proc Natl Acad Sci U S A 111:12516–12521
243. Yang Y, Liu C, Du L, Jiang S, Shi Z, Baric RS, Li F (2015) Two mutations were critical for bat-to-human transmission of middle east respiratory syndrome coronavirus. J Virol 89: 9119–9123
244. Ye Y, Hauns K, Langland JO, Jacobs BL, Hogue BG (2007) Mouse hepatitis coronavirus A59 nucleocapsid protein is a type I interferon antagonist. J Virol 81:2554–2563
245. 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
246. Yu W, Leibowitz JL (1995) Specific binding of host cellular proteins to multiple sites within the 3′ end of mouse hepatitis virus genomic RNA. J Virol 69:2016–2023
247. Yuan X, Yao Z, Wu J, Zhou Y, Shan Y, Dong B, Zhao Z, Hua P, Chen J, Cong Y (2007) G1 phase cell cycle arrest induced by SARS-CoV 3a protein via the cyclin D3/pRb pathway. Am J Respir Cell Mol Biol 37:9–19
248. Yuan L, Chen Z, Song S, Wang S, Tian C, Xing G, Chen X, Xiao ZX, He F, Zhang L (2015) p53 degradation by a coronavirus papain-like protease suppresses type I interferon signaling. J Biol Chem 290:3172–3182
249. 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
250. Zalinger ZB, Elliott R, Rose KM, Weiss SR (2015) MDA5 is critical to host defense during infection with murine coronavirus. J Virol 89:12330–12340
251. Zeng Q, Langereis MA, van Vliet AL, Huizinga EG, de Groot RJ (2008) Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution. Proc Natl Acad Sci U S A 105:9065–9069
252. Zhang X, Lai MM (1995) Interactions between the cytoplasmic proteins and the intergenic (promoter) sequence of mouse hepatitis virus RNA: correlation with the amounts of subgenomic mRNA transcribed. J Virol 69:1637–1644
253. Zhang X, Wu K, Wang D, Yue X, Song D, Zhu Y, Wu J (2007) Nucleocapsid protein of SARS-CoV activates interleukin-6 expression through cellular transcription factor NF-kappaB. Virology 365:324–335
254. Zhang L, Zhang ZP, Zhang XE, Lin FS, Ge F (2010) Quantitative proteomics analysis reveals BAG3 as a potential target to suppress severe acute respiratory syndrome coronavirus replication. J Virol 84:6050–6059
255. Zhao Z, Thackray LB, Miller BC, Lynn TM, Becker MM, Ward E, Mizushima NN, Denison MR, Virgin HWt (2007) Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3:581–585
256. 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
257. Zheng B, He ML, Wong KL, Lum CT, Poon LL, Peng Y, Guan Y, Lin MC, Kung HF (2004) 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 24:388–390
258. Zheng D, Chen G, Guo B, Cheng G, Tang H (2008) PLP2, a potent deubiquitinase from murine hepatitis virus, strongly inhibits cellular type I interferon production. Cell Res 18:1105–1113
259. Zhou P, Li H, Wang H, Wang LF, Shi Z (2012) Bat severe acute respiratory syndrome-like coronavirus ORF3b homologues display different interferon antagonist activities. J Gen Virol 93:275–281
260. Zust 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