Recombinant live vaccines to protect against the severe acute respiratory syndrome coronavirus

Birkhauser Advances in Infectious Diseases

Volumn , Issue , 2011, Pages 73-97

  Enjuanes, Luis ^a   Nieto Torres, Jose L ^a   Jimenez Guardeño, Jose M ^a   Dediego, Marta L ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 2; SEVERE ACUTE RESPIRATORY SYNDROME VACCINE; VIRUS ENVELOPE PROTEIN;

ANTIBODY PRODUCTION; ARTICLE; BIOSAFETY; CODON; DIARRHEA; DRUG EFFICACY; DRUG SAFETY; EPIDEMIC; GENE DELETION; HUMAN; IMMUNOGENICITY; INFECTION PREVENTION; MORTALITY; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN MODIFICATION; REGULATORY SEQUENCE; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRUS ATTENUATION; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS GENOME; VIRUS LIKE AGENT; VIRUS PNEUMONIA; VIRUS RECOMBINANT; VIRUS RECOMBINATION; VIRUS REPLICATION; VIRUS VIRULENCE;

EID: 79960054246     PISSN: None     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-0346-0277-8_4     Document Type: Article

References (148)

1. Peiris JS, Yuen KY, Osterhaus AD, Stohr K (2003) The severe acute respiratory syndrome. N Engl J Med 349:2431-2441
2. Woo PC, Lau SK, Li KS, Poon RW, Wong BH, Tsoi HW, Yip BC, Huang Y, Chan KH, Yuen KY (2006) Molecular diversity of coronaviruses in bats. Virology 351:180-187
3. 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
4. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H et al (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676-679
5. Drosten C, Gunther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA et al (2003) Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348:1967-1976
6. Fouchier RA, Kuiken T, Schutten M, van Amerongen G, van Doornum GJ, van den Hoogen BG, Peiris M, Lim W, Stohr K, Osterhaus AD (2003) Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423:240
7. Ksiazek TG, Erdman D, Goldsmith C, Zaki S, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W et al (2003) A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348:1953-1966
8. Kuiken T, Fouchier RAM, Schutten M, Rimmelzwaan GF, van Amerongen G, van Riel D, Laman JD, de Jong T, van Doornum G, LimWet al (2003) Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263-270
9. Marra MA, Jones SJM, Astell CR, Holt RA, Brooks-Wilson A, Butterfield YSN, Khattra J, Asano JK, Barber SA, Chan SY et al (2003) The genome sequence of the SARS-associated coronavirus. Science 300:1399-1404
10. Peiris JSM, Lai ST, Poon LLM, Guan Y, Yam LYC, Lim W, Nicholls J, Yee WKS, Yan WW, Cheung MT (2003) Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-1325
11. Weiss SR, Navas-Martin S (2005) Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol Mol Biol Rev 69:635-664
12. 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
13. Graham RL, Baric RS (2010) Recombination, reservoirs, and the modular spike: Mechanisms of coronavirus cross-species transmission. J Virol 84(7):3134-3146
14. Tong S, Conrardy C, Ruone S, Kuzmin IV, Guo X, Tao Y, Niezgoda M, Haynes L, Agwanda B, Breiman RF et al (2009) Detection of novel SARS-like and other coronaviruses in bats from Kenya. Emerg Infect Dis 15:482-485
15. Muller MA, Paweska JT, Leman PA, Drosten C, Grywna K, Kemp A, Braack L, Sonnenberg K, Niedrig M, Swanepoel R (2007) Coronavirus antibodies in African bat species. Emerg Infect Dis 13:1367-1370
16. Jiang S, He Y, Liu S (2005) SARS vaccine development. Emerg Infect Dis 11:1016-1020
17. Enjuanes L, DeDiego ML, Alvarez E, Deming D, Sheahan T, Baric R (2007) Vaccines to prevent severe acute respiratory syndrome coronavirus-induced disease. Virus Res 133: 45-62
18. Enjuanes L, DeDiego ML, Alvarez E, Capiscol C, Baric R (2008) Vaccines for severe acute respiratory syndrome virus and other coronaviruses. In: Perlman S, Gallagher TM, Snijder EJ (eds) Nidoviruses. ASM Press, Washington, pp 379-408
19. Roper RL, Rehm KE (2009) SARS vaccines: where are we? Expert Rev Vaccines 8:887-898
20. Deming D, Sheahan T, Heise M, Yount B, Davis N, Sims A, Suthar M, Harkema J, Whitmore A, Pickles R et al (2006) Vaccine efficacy in senescent mice challenged with recombinant SARS-CoV bearing epidemic and zoonotic spike variants. PLoS Med 3:2359-2375
21. Rockx B, Baas T, Zornetzer GA, Haagmans B, Sheahan T, Frieman M, Dyer MD, Teal TH, Proll S, van den Brand J et al (2009) Early upregulation of acute respiratory distress syndrome-associated cytokines promotes lethal disease in an aged-mouse model of severe acute respiratory syndrome coronavirus infection. J Virol 83:7062-7074
22. Roberts A, Deming D, Paddock CD, Cheng A, Yount B, Vogel L, Herman BD, Sheahan T, Heise M, Genrich GL et al (2007) A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog 3:23-37
23. Roberts A, Lamirande EW, Vogel L, Jackson JP, Paddock CD, Guarner J, Zaki SR, Sheahan T, Baric R, Subbarao K (2008) Animal models and vaccines for SARS-CoV infection. Virus Res 133:20-32
24. See RH, Zakhartchouk AN, Petric M, Lawrence DJ, Mok CP, Hogan RJ, Rowe T, Zitzow LA, Karunakaran KP, Hitt MM et al (2006) Comparative evaluation of two severe acute respiratory syndrome (SARS) vaccine candidates in mice challenged with SARS coronavirus. J Gen Virol 87:641-650
25. See RH, Petric M, Lawrence DJ, Mok CP, Rowe T, Zitzow LA, Karunakaran KP, Voss TG, Brunham RC, Gauldie J et al (2008) Severe acute respiratory syndrome vaccine efficacy in ferrets: whole killed virus and adenovirus-vectored vaccines. J Gen Virol 89:2136-2146
26. Darnell ME, Plant EP, Watanabe H, Byrum R, St Claire M, Ward JM, Taylor DR (2007) Severe acute respiratory syndrome coronavirus infection in vaccinated ferrets. J Infect Dis 196:1329-1338
27. Lawler JV, Endy TP, Hensley LE, Garrison A, Fritz EA, Lesar M, Baric RS, Kulesh DA, Norwood DA, Wasieloski LP et al (2006) Cynomolgus macaque as an animal model for severe acute respiratory syndrome. PLoS Med 3:e149
28. Zhou J, Wang W, Zhong Q, Hou W, Yang Z, Xiao SY, Zhu R, Tang Z, Wang Y, Xian Q et al (2005) Immunogenicity, safety, and protective efficacy of an inactivated SARS-associated coronavirus vaccine in rhesus monkeys. Vaccine 23:3202-3209
29. Lin JT, Zhang JS, Su N, Xu JG, Wang N, Chen JT, Chen X, Liu YX, Gao H, Jia YP et al (2007) Safety and immunogenicity from a phase I trial of inactivated severe acute respiratory syndrome coronavirus vaccine. Antivir Ther 12:1107-1113
30. Du L, He Y, Jiang S, Zheng BJ (2008) Development of subunit vaccines against severe acute respiratory syndrome. Drugs Today (Barc) 44:63-73
31. He Y, Jiang S (2005) Vaccine design for severe acute respiratory syndrome coronavirus. Viral Immunol 18:327-332
32. Zhou Z, Post P, Chubet R, Holtz K, McPherson C, Petric M, Cox M (2006) A recombinant baculovirus-expressed S glycoprotein vaccine elicits high titers of SARS-associated coronavirus (SARS-CoV) neutralizing antibodies in mice. Vaccine 24:3624-3631
33. Du L, Zhao G, Lin Y, Chan C, He Y, Jiang S, Wu C, Jin DY, Yuen KY, Zhou Y et al (2008) Priming with rAAV encoding RBD of SARS-CoV S protein and boosting with RBD-specific peptides for T cell epitopes elevated humoral and cellular immune responses against SARS-CoV infection. Vaccine 26:1644-1651
34. Du L, Zhao G, Lin Y, Sui H, Chan C, Ma S, He Y, Jiang S, Wu C, Yuen KY et al (2008) Intranasal vaccination of recombinant adeno-associated virus encoding receptor-binding domain of severe acute respiratory syndrome coronavirus (SARS-CoV) spike protein induces strong mucosal immune responses and provides long-term protection against SARS-CoV infection. J Immunol 180:948-956
35. Bisht H, Roberts A, Vogel L, Bukreyev A, Collins PL, Murphy BR, Subbarao K, Moss B (2004) Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice. Proc Natl Acad Sci USA 101:6641-6646
36. Subbarao K, McAuliffe J, Vogel L, Fahle G, Fischer S, Tatti K, Packard M, Shieh WJ, Zaki S, Murphy B (2004) Prior infection and passive transfer of neutralizing antibody prevent replication of severe acute respiratory syndrome coronavirus in the respiratory tract of mice. J Virol 78:3572-3577
37. Rockx B, Corti D, Donaldson E, Sheahan T, Stadler K, Lanzavecchia A, Baric R (2008) Structural basis for potent cross-neutralizing human monoclonal antibody protection against lethal human and zoonotic severe acute respiratory syndrome coronavirus challenge. J Virol 82:3220-3235
38. Greenough TC, Babcock GJ, Roberts A, Hernandez HJ, Thomas WD Jr, Coccia JA, Graziano RF, Srinivasan M, Lowy I, Finberg RW et al (2005) Development and characterization of a severe acute respiratory syndrome-associated coronavirus-neutralizing human monoclonal antibody that provides effective immunoprophylaxis in mice. J Infect Dis 191: 507-514
39. ter Meulen J, van den Brink EN, Poon LL, Marissen WE, Leung CS, Cox F, Cheung CY, Bakker AQ, Bogaards JA, van Deventer E et al (2006) Human monoclonal antibody combination against SARS coronavirus: synergy and coverage of escape mutants. PLoS Med 3:e237
40. Sui J, Aird DR, Tamin A, Murakami A, Yan M, Yammanuru A, Jing H, Kan B, Liu X, Zhu Q et al (2008) Broadening of neutralization activity to directly block a dominant antibodydriven SARS-coronavirus evolution pathway. PLoS Pathog 4:e1000197
41. Hwang WC, Lin Y, Santelli E, Sui J, Jaroszewski L, Stec B, Farzan M, Marasco WA, Liddington RC (2006) Structural basis of neutralization by a human anti-severe acute respiratory syndrome spike protein antibody, 80R. J Biol Chem 281:34610-34616
42. Akerstrom S, Tan YJ, Mirazimi A (2006) Amino acids 15-28 in the ectodomain of SARS coronavirus 3a protein induces neutralizing antibodies. FEBS Lett 580:3799-3803
43. Lu X, Chen Y, Bai B, Hu H, Tao L, Yang J, Chen J, Chen Z, Hu Z, Wang H (2007) Immune responses against severe acute respiratory syndrome coronavirus induced by virus-like particles in mice. Immunology 122:496-502
44. Yang ZY, Kong WP, Huang Y, Roberts A, Murphy BR, Subbarao K, Nabel GJ (2004) A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice. Nature 428:561-564
45. Okada M, Okuno Y, Hashimoto S, Kita Y, Kanamaru N, Nishida Y, Tsunai Y, Inoue R, Nakatani H, Fukamizu R et al (2007) Development of vaccines and passive immunotherapy against SARS corona virus using SCID-PBL/hu mouse models. Vaccine 25:3038-3040
46. Yasui F, Kai C, Kitabatake M, Inoue S, Yoneda M, Yokochi S, Kase R, Sekiguchi S, Morita K, Hishima T et al (2008) Prior immunization with severe acute respiratory syndrome (SARS)-associated coronavirus (SARS-CoV) nucleocapsid protein causes severe pneumonia in mice infected with SARS-CoV. J Immunol 181:6337-6348
47. Wang X, Xu W, Tong D, Ni J, Gao H, Wang Y, Chu Y, Li P, Yang X, Xiong S (2008) A chimeric multi-epitope DNA vaccine elicited specific antibody response against severe acute respiratory syndrome-associated coronavirus which attenuated the virulence of SARS-CoV in vitro. Immunol Lett 119:71-77
48. Czub M, Weingartl H, Czub S, He R, Cao J (2005) Evaluation of modified vaccinia virus Ankara based recombinant SARS vaccine in ferrets. Vaccine 23:2273-2279
49. Buchholz UJ, Bukreyev A, Yang L, Lamirande EW, Murphy BR, Subbarao K, Collins PL (2004) Contributions of the structural proteins of severe acute respiratory syndrome coronavirus to protective immunity. Proc Natl Acad Sci USA 101:9804-9809
50. Bukreyev A, Lamirande EW, Buchholz UJ, Vogel LN, Elkins WR, St Claire M, Murphy BR, Subbarao K, Collins PL (2004) Mucosal immunisation of African green monkeys (Cercopithecus aethiops) with an attenuated parainfluenza virus expressing the SARS coronavirus spike protein for the prevention of SARS. Lancet 363:2122-2127
51. Liniger M, Zuniga A, Tamin A, Azzouz-Morin TN, Knuchel M, Marty RR, Wiegand M, Weibel S, Kelvin D, Rota PA et al (2008) Induction of neutralising antibodies and cellular immune responses against SARS coronavirus by recombinant measles viruses. Vaccine 26:2164-2174
52. DiNapoli JM, Kotelkin A, Yang L, Elankumaran S, Murphy BR, Samal SK, Collins PL, Bukreyev A (2007) Newcastle disease virus, a host range-restricted virus, as a vaccine vector for intranasal immunization against emerging pathogens. Proc Natl Acad Sci USA 104: 9788-9793
53. Kapadia SU, Rose JK, Lamirande E, Vogel L, Subbarao K, Roberts A (2005) Long-term protection from SARS coronavirus infection conferred by a single immunization with an attenuated VSV-based vaccine. Virology 340:174-182
54. Kapadia SU, Simon ID, Rose JK (2008) SARS vaccine based on a replication-defective recombinant vesicular stomatitis virus is more potent than one based on a replicationcompetent vector. Virology 376:165-172
55. Brian DA, Baric RS (2005) Coronavirus genome structure and replication. Curr Top Microbiol Immunol 287:1-30
56. Enjuanes L, Spaan W, Snijder E, Cavanagh D (2000) Nidovirales. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR et al (eds) Virus taxonomy. Seventh report of the international committee on taxonomy of viruses. Academic Press, New York, pp 827-834
57. Enjuanes L, Gorbalenya AE, de Groot RJ, Cowley JA, Ziebuhr J, Snijder EJ (2008) The Nidovirales. In: Mahy BWJ, Van Regenmortel M, Walker P, Majumder-Russell D (eds) Encyclopedia of Virology, 3rd edn. Elsevier, Oxford, pp 419-430
58. Brierley I, Digard P, Inglis SC (1989) Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell 57:537-547
59. Thiel V, Ivanov KA, Putics A, Hertzig T, Schelle B, Bayer S, Wessbrich B, Snijder EJ, Rabenau H, Doerr HW et al (2003) Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol 84:2305-2315
60. Ziebuhr J (2005) The coronavirus replicase. In: Enjuanes L (ed) Coronavirus replication and reverse genetics. Springer, Berlin, pp 57-94
61. Ziebuhr J, Snijder EJ, Gorbalenya AE (2000) Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81:853-879
62. 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
63. Ito N, Mossel EC, Narayanan K, Popov VL, Huang C, Inoue T, Peters CJ, Makino S (2005) Severe acute respiratory syndrome coronavirus 3a protein is a viral structural protein. J Virol 79:3182-3186
64. Huang C, Ito N, Tseng CT, Makino S (2006) Severe acute respiratory syndrome coronavirus 7a accessory protein is a viral structural protein. J Virol 80:7287-7294
65. Huang C, Peters CJ, Makino S (2007) Severe acute respiratory syndrome coronavirus accessory protein 6 is a virion-associated protein and is released from 6 protein-expressing cells. J Virol 81:5423-5426
66. Shen S, Lin PS, Chao YC, Zhang A, Yang X, Lim SG, Hong W, Tan YJ (2005) The severe acute respiratory syndrome coronavirus 3a is a novel structural protein. Biochem Biophys Res Commun 330:286-292
67. Schaecher SR, Mackenzie JM, PekoszA (2007) The ORF7b protein of SARS-CoV is expressed in virus-infected cells and incorporated into SARS-CoV particles. J Virol 81:718-731
68. 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
69. Kopecky-Bromberg SA, Martinez-Sobrido L, Palese P (2006) 7a protein of severe acute respiratory syndrome coronavirus inhibits cellular protein synthesis and activates p38 mitogen- activated protein kinase. J Virol 80:785-793
70. Hussain S, Perlman S, Gallagher TM (2008) Severe acute respiratory syndrome coronavirus protein 6 accelerates murine hepatitis virus infections by more than one mechanism. J Virol 82:7212-7222
71. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC et al (2003) Angiotensin-converting enzyme 2 is a functional receptor for de SARS coronavirus. Nature 426:450-454
72. Jeffers SA, Tusell SM, Gillim-Ross L, Hemmila EM, Achenbach JE, Babcock GJ, Thomas WD Jr, Thackray LB, Young MD, Mason RJ et al (2004) CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci USA 101:15748-15753
73. Saif LJ (2004) Animal coronavirus vaccines: lessons for SARS. Dev Biol (Basel) 119:129-140
74. Cavanagh D (2003) Severe acute respiratory syndrome vaccine development: experiences of vaccination against avian infectious bronchitis coronavirus. Avian Pathol 32:567-582
75. Enjuanes L, Smerdou C, Castilla J, Anton IM, Torres JM, Sola I, Golvano J, Sanchez JM, Pintado B (1995) Development of protection against coronavirus induced diseases. A Review. Adv Exp Med Biol 380:197-211
76. Almazan F, DeDiego ML, Galan C, Alvarez E, Enjuanes L (2006) Identification of essential genes as a strategy to select a SARS candidate vaccine using a SARS-CoV infectious cDNA. Adv Exp Med Biol 581:579-583
77. Almazan F, Galan C, Enjuanes L (2008) Engineering infectious cDNA of coronavirus as bacterial artificial chromosomes. In: Cavanagh D (ed) SARS and other coronaviruses: laboratory protocols. Humana Press, Washington, pp 275-291
78. Almazan F, Gonzalez JM, Penzes Z, Izeta A, Calvo E, Plana-Duran J, Enjuanes L (2000) Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc Natl Acad Sci USA 97:5516-5521
79. DeDiego ML, Alvarez E, Almazan F, Rejas MT, Lamirande E, Roberts A, Shieh WJ, Zaki SR, Subbarao K, Enjuanes L (2007) A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J Virol 81:1701-1713
80. Gonzalez JM, Penzes Z, Almazan F, Calvo E, Enjuanes L (2002) Stabilization of a fulllength infectious cDNA clone of transmissible gastroenteritis coronavirus by insertion of an intron. J Virol 76:4655-4661
81. Yount B, Curtis KM, Baric RS (2000) Strategy for systematic assembly of large RNA and DNA genomes: the transmissible gastroenteritis virus model. J Virol 74:10600-10611
82. Thiel V, Herold J, Schelle B, Siddell S (2001) Infectious RNA transcribed in vitro from a cDNA copy of the human coronavirus genome cloned in vaccinia virus. J Gen Virol 82: 1273-1281
83. Casais R, Thiel V, Siddell SG, Cavanagh D, Britton P (2001) Reverse genetics system for the avian coronavirus infectious bronchitis virus. J Virol 75:12359-12369
84. Yount B, Roberts RS, Lindesmith L, Baric RS (2006) Rewiring the severe acute respiratory syndrome coronavirus (SARS-CoV) transcription circuit: engineering a recombinationresistant genome. Proc Natl Acad Sci USA 103:12546-12551
85. DeDiego ML, Pewe L, Alvarez E, Rejas MT, Perlman S, Enjuanes L (2008) Pathogenicity of severe acute respiratory coronavirus deletion mutants in hACE-2 transgenic mice. Virology 376:379-389
86. Lamirande EW, DeDiego ML, Roberts A, Jackson JP, Alvarez E, Sheahan T, Shieh WJ, Zaki SR, Baric R, Enjuanes L et al (2008) A live attenuated SARS coronavirus is immunogenic and efficacious in golden Syrian hamsters. J Virol 82:7721-7724
87. Netland J, DeDiego ML, Zhao J, Fett C, Álvarez E, Nieto-Torres JL, Enjuanes L, Perlman S (2010) Immunization with an attenuated severe acute respiratory syndrome coronavirus deleted in E protein protects against lethal respiratory disease. Virology 399(1):120-128
88. Yount B, Roberts RS, Sims AC, Deming D, Frieman MB, Sparks J, Denison MR, Davis N, Baric RS (2005) Severe acute respiratory syndrome coronavirus group-specific open reading frames encode nonessential functions for replication in cell cultures and mice. J Virol 79:14909-14922
89. Sims AC, Burkett SE, Yount B, Pickles RJ (2007) SARS-CoV replication and pathogenesis in an in vitro model of the human conducting airway epithelium. Virus Res 133:33-44
90. Qiu M, Shi Y, Guo Z, Chen Z, He R, Chen R, Zhou D, Dai E, Wang X, Si B et al (2005) Antibody responses to individual proteins of SARS coronavirus and their neutralization activities. Microbes Infect 7:882-889
91. Lu W, Zheng BJ, Xu K, Schwarz W, Du L, Wong CK, Chen J, Duan S, Deubel V, Sun B (2006) Severe acute respiratory syndrome-associated coronavirus 3a protein forms an ion channel and modulates virus release. Proc Natl Acad Sci USA 103:12540-12545
92. Kuo L, Masters PS (2003) The small envelope protein E is not essential for murine coronavirus replication. J Virol 77:4597-4608
93. Curtis KM, Yount B, Baric RS (2002) Heterologous gene expression from transmissible gastroenteritis virus replicon particles. J Virol 76:1422-1434
94. Ortego J, Escors D, Laude H, Enjuanes L (2002) Generation of a replication-competent, propagation-deficient virus vector based on the transmissible gastroenteritis coronavirus genome. J Virol 76:11518-11529
95. Subbarao K, Roberts A (2006) Is there an ideal animal model for SARS? Trends Microbiol 14:299-303
96. Roberts A, Vogel L, Guarner J, Hayes N, Murphy B, Zaki S, Subbarao K (2005) Severe acute respiratory syndrome coronavirus infection of golden Syrian hamsters. J Virol 79:503-511
97. Roberts A, Thomas WD, Guarner J, Lamirande EW, Babcock GJ, Greenough TC, Vogel L, Hayes N, Sullivan JL, Zaki S et al (2006) Therapy with a severe acute respiratory syndromeassociated coronavirus-neutralizing human monoclonal antibody reduces disease severity and viral burden in golden Syrian hamsters. J Infect Dis 193:685-692
98. McCray PB Jr, Pewe L, Wohlford-Lenane C, Hickey M, Manzel L, Shi L, Netland J, Jia HP, Halabi C, Sigmund CD et al (2007) Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J Virol 81:813-821
99. Chu CM, Poon LL, Cheng VC, Chan KS, Hung IF, Wong MM, Chan KH, Leung WS, Tang BS, Chan VL et al (2004) Initial viral load and the outcomes of SARS. Can Med Assoc J 171:1349-1352
100. Hung IF, Cheng VC, Wu AK, Tang BS, Chan KH, Chu CM, Wong MM, Hui WT, Poon LL, Tse DM et al (2004) Viral loads in clinical specimens and SARS manifestations. Emerg Infect Dis 10:1550-1557
101. Tseng CT, Huang C, Newman P, Wang N, Narayanan K, Watts DM, Makino S, Packard MM, Zaki SR, Chan TS et al (2007) Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human Angiotensin-converting enzyme 2 virus receptor. J Virol 81:1162-1173
102. Nagata N, Iwata N, Hasegawa H, Fukushi S, Harashima A, Sato Y, Saijo M, Taguchi F, Morikawa S, Sata T (2008) Mouse-passaged severe acute respiratory syndrome-associated coronavirus leads to lethal pulmonary edema and diffuse alveolar damage in adult but not young mice. Am J Pathol 172:1625-1637
103. Nagata N, Iwata N, Hasegawa H, Fukushi S, Yokoyama M, Harashima A, Sato Y, Saijo M, Morikawa S, Sata T (2007) Participation of both host and virus factors in induction of severe acute respiratory syndrome (SARS) in F344 rats infected with SARS coronavirus. J Virol 81:1848-1857
104. DeDiego ML, Nieto-Torres JL, Enjuanes L (2010) Modulation of host stress and immune responses by severe acute respiratory syndrome coronavirus envelope E protein. Submitted
105. Asea A (2006) Initiation of the Immune Response by Extracellular Hsp72: Chaperokine Activity of Hsp72. Curr Immunol Rev 2:209-215
106. Callahan MK, Garg M, Srivastava PK (2008) Heat-shock protein 90 associates with N-terminal extended peptides and is required for direct and indirect antigen presentation. Proc Natl Acad Sci USA 105:1662-1667
107. Moseley P (2000) Stress proteins and the immune response. Immunopharmacology 48:299-302
108. Zugel U, Kaufmann SH (1999) Role of heat shock proteins in protection fromand pathogenesis of infectious diseases. Clin Microbiol Rev 12:19-39
109. Eckerle LD, Lu X, Sperry SM, Choi L, Denison MR (2007) High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J Virol 81:12135-12144
110. Almazan F, DeDiego ML, Galan C, Escors D, Alvarez E, Ortego J, Sola I, Zuñiga S, Alonso S, Moreno JL et al (2006) Construction of a SARS-CoV infectious cDNA clone and a replicon to study coronavirus RNA synthesis. J Virol 80:10900-10906
111. 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
112. Alvarez E, DeDiego ML, Nieto-Torres JL, Jiménez-Guardeño JM, Marcos-Villar L, Enjuanes L (2010) The envelope protein of severe acute respiratory syndrome coronavirus interacts with the nonstructural protein 3 and is ubiquitinated. Virology 402(2):281-291
113. Konig R, Zhou Y, Elleder D, Diamond TL, Bonamy GM, Irelan JT, Chiang CY, Tu BP, De Jesus PD, Lilley CE et al (2008) Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 135:49-60
114. Zust R, Cervantes-Barragan L, Kuri T, Blakqori G, Weber F, Ludewig B, Thiel V (2007) Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines. PLoS Pathog 3:e109
115. 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
116. Brockway SM, Denison MR (2005) Mutagenesis of the murine hepatitis virus nsp1-coding region identifies residues important for protein processing, viral RNA synthesis, and viral replication. Virology 340:209-223
117. Graham RL, Sims AC, Brockway SM, Baric RS, Denison MR (2005) The nsp2 replicase proteins of murine hepatitis virus and severe acute respiratory syndrome coronavirus are dispensable for viral replication. J Virol 79:13399-13411
118. Hertzig T, Scandella E, Schelle B, Ziebuhr J, Siddell SG, Ludewig B, Thiel V (2004) Rapid identification of coronavirus replicase inhibitors using a selectable replicon RNA. J Gen Virol 85:1717-1725
119. Gadlage MJ, Graham RL, Denison MR (2008) Murine coronaviruses encoding nsp2 at different genomic loci have altered replication, protein expression, and localization. J Virol 82:11964-11969
120. Gu J, Korteweg C (2007) Pathology and pathogenesis of severe acute respiratory syndrome. Am J Pathol 170:1136-1147
121. Kanzawa N, Nishigaki K, Hayashi T, Ishii Y, Furukawa S, Niiro A, Yasui F, Kohara M, Morita K, Matsushima K et al (2006) Augmentation of chemokine production by severe acute respiratory syndrome coronavirus 3a/X1 and 7a/X4 proteins through NF-kappaB activation. FEBS Lett 580:6807-6812
122. Law HK, Cheung CY, Ng HY, Sia SF, Chan YO, Luk W, Nicholls JM, Peiris JS, Lau YL (2005) Chemokine up-regulation in SARS-coronavirus-infected, monocyte-derived human dendritic cells. Blood 106:2366-2374
123. Narayanan K, Huang C, Makino S (2008) SARS coronavirus accessory proteins. Virus Res 133:113-121
124. O'Connor A, Martin SW, Nagy E, Menzies P, Harland R (2001) The relationship between the occurrence of undifferentiated bovine respiratory disease and titer changes to bovine coronavirus and bovine viral diarrhea virus in 3 Ontario feedlots. Can J Vet Res 65: 137-142
125. Pedersen NC, Boyle JF, Floyd K, Fudge A, Barker J (1981) An enteric coronavirus infection of cats and its relationship to feline infectious peritonitis. Am J Vet Res 42:368-377
126. Weiss RC, Dodds WJ, Scott FW (1980) Disseminated intravascular coagulation in experimentally induced feline infectious peritonitis. Am J Vet Res 41:663-671
127. Porterfield JS (1986) Antibody-dependent enhancement of viral infectivity. Adv Virus Res 31:335-355
128. Vennema H, de Groot RJ, Harbour DA, Dalderup M, Gruffydd-Jones T, Horzinek MC, Spaan WJ (1990) Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. J Virol 64:1407-1409
129. Weiss RC, Scott FW (1981) Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp Immunol Microbiol Infect Dis 4:175-189
130. Corapi WV, Darteil RJ, Audonnet J-C, Chappuis GE (1995) Localization of antigenic sites of the S glycoprotein of feline infectious peritonitis virus involved in neutralization and antibody-dependent enhancement. J Virol 69:2858-2862
131. Corapi WV, Olsen CW, Scott FW (1992) Monoclonal antibody analysis of neutralization and antibody-dependent enhancement of feline infectious peritonitis virus. J Virol 66: 6695-6705
132. Olsen CW, Corapi WV, Ngichabe CK, Baines JD, Scott FW (1992) Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J Virol 66:956-965
133. Olsen CW, Corapi WV, Jacobson RH, Simkins RA, Saif LJ, Scott FW (1993) Identification of antigenic sites mediating antibody-dependent enhancement of feline infectious peritonitis virus infectivity. J Gen Virol 74:745-749
134. Zhong X, Yang H, Guo ZF, Sin WY, Chen W, Xu J, Fu L, Wu J, Mak CK, Cheng CS et al (2005) B-cell responses in patients who have recovered from severe acute respiratory syndrome target a dominant site in the S2 domain of the surface spike glycoprotein. J Virol 79:3401-3408
135. Yang ZY, Werner HC, Kong WP, Leung K, Traggiai E, Lanzavecchia A, Nabel GJ (2005) Evasion of antibody neutralization in emerging severe acute respiratory syndrome coronaviruses. Proc Natl Acad Sci USA 102:797-801
136. Weingartl H, Czub M, Czub S, Neufeld J, Marszal P, Gren J, Smith G, Jones S, Proulx R, Deschambault Y et al (2004) Immunization with modified vaccinia virus Ankara-based recombinant vaccine against severe acute respiratory syndrome is associated with enhanced hepatitis in ferrets. J Virol 78:12672-12676
137. Martina BE, Haagmans BL, Kuiken T, Fouchier RA, Rimmelzwaan GF, Van Amerongen G, Peiris JS, Lim W, Osterhaus AD (2003) SARS virus infection of cats and ferrets. Nature 425:915
138. He Y, Li J, Li W, Lustigman S, Farzan M, Jiang S (2006) Cross-neutralization of human and palm civet severe acute respiratory syndrome coronaviruses by antibodies targeting the receptor-binding domain of spike protein. J Immunol 176:6085-6092
139. McAuliffe J, Vogel L, Roberts A, Fahle G, Fischer S, Shieh WJ, Butler E, Zaki S, St Claire M, Murphy B et al (2004) Replication of SARS coronavirus administered into the respiratory tract of African Green, rhesus and cynomolgus monkeys. Virology 330:8-15
140. Qin E, Shi H, Tang L, Wang C, Chang G, Ding Z, Zhao K, Wang J, Chen Z, Yu M et al (2006) Immunogenicity and protective efficacy in monkeys of purified inactivated Vero-cell SARS vaccine. Vaccine 24:1028-1034
141. Hancock GE, Speelman DJ, Heers K, Bortell E, Smith J, Cosco C (1996) Generation of atypical pulmonary inflammatory responses in BALB/c mice after immunization with the native attachment (G) glycoprotein of respiratory syncytial virus. J Virol 70:7783-7791
142. De Swart RL, Kuiken T, Timmerman HH, van Amerongen G, Van Den Hoogen BG, Vos HW, Neijens HJ, Andeweg AC, Osterhaus AD (2002) Immunization of macaques with formalin-inactivated respiratory syncytial virus (RSV) induces interleukin-13-associated hypersensitivity to subsequent RSV infection. J Virol 76:11561-11569
143. Kim HW, Canchola JG, Brandt CD, Pyles G, Chanock RM, Jensen K, Parrott RH (1969) Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol 89:422-434
144. de Haan CAM, Volders H, Koetzner CA, Masters PS, Rottier PJM (2002) Coronavirus maintain viability despite dramatic rearrangements of the strictly conserved genome organization. J Virol 76:12491-12502
145. Mueller S, Papamichail D, Coleman JR, Skiena S, Wimmer E (2006) Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J Virol 80:9687-9696
146. Gustafsson C, Govindarajan S, Minshull J (2004) Codon bias and heterologous protein expression. Trends Biotechnol 22:346-353
147. Plotkin JB, Robins H, Levine AJ (2004) Tissue-specific codon usage and the expression of human genes. Proc Natl Acad Sci USA 101:12588-12591
148. Enjuanes L, Sola I, Alonso S, Escors D, Zuñiga S (2005) Coronavirus reverse genetics and development of vectors for gene expression. In: Enjuanes L (ed) Coronavirus replication and reverse genetics. Springer, Berlin, pp 161-197