SARS vaccines: Where are we?

Expert Review of Vaccines

Volumn 8, Issue 7, 2009, Pages 887-898

  Roper, Rachel L ^a   Rehm, Kristina E ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Animal model; Antibody; Efficacy; SARS; T lymphocyte; Vaccine

Indexed keywords

ADENOVIRUS VECTOR; DNA VACCINE; GAMMA INTERFERON; HLA ANTIGEN; INACTIVATED VIRUS VACCINE; M PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEUTRALIZING ANTIBODY; RECOMBINANT VACCINE; SEVERE ACUTE RESPIRATORY SYNDROME VACCINE;

ANTIBODY RESPONSE; DNA IMMUNIZATION; DRUG RESEARCH; HUMAN; IMMUNOGENICITY; INTERFERON PRODUCTION; NONHUMAN; OPEN READING FRAME; POXVIRUS; PRIORITY JOURNAL; REVIEW; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; T LYMPHOCYTE ACTIVATION; VACCINATION; VACCINE PRODUCTION;

ANIMALS; HUMANS; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VACCINES, ATTENUATED; VACCINES, DNA; VACCINES, INACTIVATED; VACCINES, SUBUNIT; VACCINES, SYNTHETIC; VIRAL VACCINES;

EID: 67650462880     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.43     Document Type: Review

References (142)

1. Marra MA, Jones SJ, Astell CR et al. The genome sequence of the SARS-associated coronavirus. Science 300(5624), 1399-1404 (2003).
2. Rota PA, Oberste MS, Monroe SS et al. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300(5624), 1394-1399 (2003). (Pubitemid 36638152)
3. Fouchier RA, Kuiken T, Schutten M et al. Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423(6937), 240 (2003). (Pubitemid 40852688)
4. Zheng BJ, Wong KH, Zhou J et al. SARS-related virus predating SARS outbreak, Hong Kong. Emerg. Infect. Dis. 10(2), 176-178 (2004). (Pubitemid 38176951)
5. Fleck F. SARS virus returns to China as scientists race to find effective vaccine. Bull. World Health Organ. 82(2), 152-153 (2004).
6. Guan YJ, Tang XP, Zhang FC et al. Study of laboratory characteristic of 4 patients with sporadic severe acute respiratory syndrome in 2004. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue 17(6), 332-334 (2005).
7. Che XY, Di B, Zhao GP et al. A patient with asymptomatic severe acute respiratory syndrome (SARS) and antigenemia from the 2003-2004 community outbreak of SARS in Guangzhou, China. Clin. Infect. Dis. 43(1), e1-e5 (2006).
8. Chen W, Yan M, Yang L et al. SARSassociated coronavirus transmitted from human to pig. Emerg. Infect. Dis. 11(3), 446-448 (2005). (Pubitemid 40315732)
9. Martina BE, Haagmans BL, Kuiken T et al. Virology: SARS virus infection of cats and ferrets. Nature 425(6961), 915 (2003). (Pubitemid 37376916)
10. Wang M, Jing HQ, Xu HF et al. Surveillance on severe acute respiratory syndrome associated coronavirus in animals at a live animal market of Guangzhou in 2004. Zhonghua Liu Xing Bing Xue Za Zhi 26(2), 84-87 (2005).
11. Guan Y, Zheng BJ, He YQ et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302(5643), 276-278 (2003). (Pubitemid 37248756)
12. Lau SK, Woo PC, Li KS et al. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl Acad. Sci. USA 102(39), 14040-14045 (2005). (Pubitemid 41377699)
13. Drosten C, Gunther S, Preiser W et al. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348(20), 1967-1976 (2003).
14. Ksiazek TG, Erdman D, Goldsmith CS et al. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348(20), 1953-1966 (2003).
15. Peiris JS, Lai ST, Poon LL et al. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361(9366), 1319-1325 (2003). (Pubitemid 36514862)
16. Peiris JS, Chu CM, Cheng VC et al. Clinical progression and viral load in a community outbreak of coronavirusassociated SARS pneumonia: a prospective study. Lancet 361(9371), 1767-1772 (2003). (Pubitemid 36638424)
17. Yam WC, Chan KH, Poon LL et al. Evaluation of reverse transcription-PCR assays for rapid diagnosis of severe acute respiratory syndrome associated with a novel coronavirus. J. Clin. Microbiol. 41(10), 4521-4524 (2003). (Pubitemid 37259751)
18. Ding Y, He L, Zhang Q et al. Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J. Pathol. 203(2), 622-630 (2004). (Pubitemid 38714098)
19. Wang JT, Chang SC. Severe acute respiratory syndrome. Curr. Opin. Infect. Dis. 17(2), 143-148 (2004).
20. Knudsen TB, Kledal TN, Andersen O, Eugen-Olsen J, Kristiansen TB. Severe acute respiratory syndrome - a new coronavirus from the Chinese dragon's lair. Scand. J. Immunol. 58(3), 277-284 (2003). (Pubitemid 37100362)
21. Nicholls J, Dong XP, Jiang G, Peiris M. SARS: clinical virology and pathogenesis. Respirology 8(Suppl.), S6-S8 (2003).
22. Lee N, Hui D, Wu A et al. A major outbreak of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 348(20), 1986-1994 (2003).
23. Pearson H, Clarke T, Abbott A, Knight J, Cyranoski D. SARS: what have we learned? Nature 424(6945), 121-126 (2003).
24. Rabenau HF, Cinatl J, Morgenstern B et al. Stability and inactivation of SARS coronavirus. Med. Microbiol. Immunol. (Berl.) 194(1-2), 1-6 (2005).
25. Hon KL, Leung CW, Cheng WT et al. Clinical presentations and outcome of severe acute respiratory syndrome in children. Lancet 361(9370), 1701-1703 (2003). (Pubitemid 36577444)
26. Olsen CW, Corapi WV, Jacobson RH et al. Identification of antigenic sites mediating antibody-dependent enhancement of feline infectious peritonitis virus infectivity. J. Gen. Virol. 74(Pt 4), 745-749 (1993). (Pubitemid 23113380)
27. Anton IM, Gonzalez S, Bullido MJ et al. Cooperation between transmissible gastroenteritis coronavirus (TGEV) structural proteins in the in vitro induction of virus-specific antibodies. Virus Res. 46(1-2), 111-124 (1996). (Pubitemid 27072718)
28. Cavanagh D. Severe acute respiratory syndrome vaccine development: experiences of vaccination against avian infectious bronchitis coronavirus. Avian Pathol. 32(6), 567-582 (2003). (Pubitemid 38119096)
29. Lai MM, Holmes KV. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott-Raven, PA, USA, 1163-1203 (2001).
30. Lai MMC, Perlman S, Anderson LJ. Coronaviridae. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott Williams & Wilkins, PA, USA 1305-1335 (2007).
31. Wong SK, Li W, Moore MJ, Choe H, Farzan M. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 279(5), 3197-3201 (2004). (Pubitemid 38140552)
32. Jeffers SA, Tusell SM, Gillim-Ross L et al. CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl Acad. Sci. USA, 101(44), 15748-15753 (2004). (Pubitemid 39473559)
33. Holmes KV. SARS coronavirus: a new challenge for prevention and therapy. J. Clin. Invest. 111(11), 1605-1609 (2003). (Pubitemid 38057739)
34. Navas-Martin SR, Weiss S. Coronavirus replication and pathogenesis: implications for the recent outbreak of severe acute respiratory syndrome (SARS), and the challenge for vaccine development. J. Neurovirol. 10(2), 75-85 (2004). (Pubitemid 38515066)
35. Guo JP, Petric M, Campbell W, McGeer PL. SARS corona virus peptides recognized by antibodies in the sera of convalescent cases. Virology 324(2), 251-256 (2004). • Other potential targets for severe acute respiratory syndrome (SARS) vaccine development. (Pubitemid 38797843)
36. Kamitani W, Narayanan K, Huang C et al. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc. Natl Acad. Sci. USA 103(34), 12885-12890 (2006). (Pubitemid 44298656)
37. Huang J, Cao Y, Du J et al. Priming with SARS CoV S DNA and boosting with SARS CoV S epitopes specific for CD4+ and CD8+ T cells promote cellular immune responses. Vaccine 25(39-40), 6981-6991 (2007). (Pubitemid 47391096)
38. Ito N, Mossel EC, Narayanan K et al. Severe acute respiratory syndrome coronavirus 3a protein is a viral structural protein. J. Virol. 79(5), 3182-3186 (2005). (Pubitemid 40270598)
39. Schaecher SR, Mackenzie JM, Pekosz A. The ORF7b protein of severe acute respiratory syndrome coronavirus (SARS-CoV) is expressed in virus-infected cells and incorporated into SARS-CoV particles. J. Virol. 81(2), 718-731 (2007). (Pubitemid 46067898)
40. Shen S, Lin PS, Chao YC et al. The severe acute respiratory syndrome coronavirus 3a is a novel structural protein. Biochem. Biophys. Res. Commun. 330(1), 286-292 (2005). (Pubitemid 40394964)
41. Xiong S, Wang YF, Zhang MY et al. Immunogenicity of SARS inactivated vaccine in BALB/c mice. Immunol. Lett. 95(2), 139-143 (2004). (Pubitemid 39237658)
42. Tsunetsugu-Yokota Y. Large-scale preparation of UV-inactivated SARS coronavirus virions for vaccine antigen. Methods Mol. Biol. 454, 1-8 (2008).
43. He Y, Zhou Y, Siddiqui P, Jiang S. Inactivated SARS-CoV vaccine elicits high titers of spike protein-specific antibodies that block receptor binding and virus entry. Biochem. Biophys. Res. Commun. 325(2), 445-452 (2004). (Pubitemid 39458016)
44. Takasuka N, Fujii H, Takahashi Y et al. A subcutaneously injected UV-inactivated SARS coronavirus vaccine elicits systemic humoral immunity in mice. Int. Immunol. 16(10), 1423-1430 (2004). (Pubitemid 39341555)
45. Tang L, Zhu Q, Qin E et al. Inactivated SARS-CoV vaccine prepared from whole virus induces a high level of neutralizing antibodies in BALB/c mice. DNA Cell. Biol. 23(6), 391-394 (2004). (Pubitemid 38850386)
46. Qu D, Zheng B, Yao X et al. Intranasal immunization with inactivated SARS-CoV (SARS-associated coronavirus) induced local and serum antibodies in mice. Vaccine 23(7), 924-931 (2005). (Pubitemid 39643181)
47. Zhang CH, Lu JH, Wang YF et al. Immune responses in Balb/c mice induced by a candidate SARS-CoV inactivated vaccine prepared from F69 strain. Vaccine 23(24), 3196-3201 (2005).
48. Stadler K, Roberts A, Becker S et al. SARS vaccine protective in mice. Emerg. Infect. Dis. 11(8), 1312-1314 (2005).
49. See RH, Zakhartchouk AN, Petric M et al. Comparative evaluation of two severe acute respiratory syndrome (SARS) vaccine candidates in mice challenged with SARS coronavirus. J. Gen. Virol. 87(Pt 3), 641-650 (2006). (Pubitemid 43308858)
50. Lokugamage KG, Yoshikawa-Iwata N, Ito N et al. Chimeric coronavirus-like particles carrying severe acute respiratory syndrome coronavirus (SCoV) S protein protect mice against challenge with SCoV. Vaccine 26(6), 797-808 (2008).
51. Kobinger GP, Figueredo JM, Rowe T et al. Adenovirus-based vaccine prevents pneumonia in ferrets challenged with the SARS coronavirus and stimulates robust immune responses in macaques. Vaccine 25(28), 5220-5231 (2007). (Pubitemid 46915465)
52. See RH, Petric M, Lawrence DJ et al. Severe acute respiratory syndrome vaccine efficacy in ferrets: whole killed virus and adenovirus-vectored vaccines. J. Gen. Virol. 89(Pt 9), 2136-2146 (2008). • Recent data on ferrets as a model for SARS infection and vaccine testing, including data on the importance of mucosal immunity.
53. Darnell ME, Plant EP, Watanabe H et al. Severe acute respiratory syndrome coronavirus infection in vaccinated ferrets. J. Infect. Dis. 196(9), 1329-1338 (2007).
54. Zhou J, Wang W, Zhong Q et al. Immunogenicity, safety, and protective efficacy of an inactivated SARS-associated coronavirus vaccine in rhesus monkeys. Vaccine 23(24), 3202-3209 (2005). (Pubitemid 40504064)
55. Lin JT, Zhang JS, Su N et al. Safety and immunogenicity from a Phase I trial of inactivated severe acute respiratory syndrome coronavirus vaccine. Antivir. Ther. 12(7), 1107-1113 (2007). (Pubitemid 350114991)
56. Rocha CD, Caetano BC, Machado AV, Bruna-Romero O. Recombinant viruses as tools to induce protective cellular immunity against infectious diseases. Int. Microbiol. 7(2), 83-94 (2004). (Pubitemid 38980508)
57. Zakhartchouk AN, Viswanathan S, Mahony JB, Gauldie J, Babiuk LA. Severe acute respiratory syndrome coronavirus nucleocapsid protein expressed by an adenovirus vector is phosphorylated and immunogenic in mice. J. Gen. Virol. 86(Pt 1), 211-215 (2005). (Pubitemid 40081167)
58. Rolph MS, Ramshaw IA. Recombinant viruses as vaccines and immunological tools. Curr. Opin. Immunol. 9(4), 517-524 (1997). (Pubitemid 27390047)
59. Imler JL. Adenovirus vectors as recombinant viral vaccines. Vaccine 13(13), 1143-1151 (1995).
60. Gao W, Tamin A, Soloff A et al. Effects of a SARS-associated coronavirus vaccine in monkeys. Lancet 362(9399), 1895-1896 (2003).
61. Hogan RJ, Gao G, Rowe T et al. Resolution of primary severe acute respiratory syndrome-associated coronavirus infection requires stat1. J. Virol. 78(20), 11416-11421 (2004). (Pubitemid 39299685)
62. Bisht H, Roberts A, Vogel L et al. Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice. Proc. Natl Acad. Sci. USA 101(17), 6641-6646 (2004). (Pubitemid 38586027)
63. Czub M, Weingartl H, Czub S, He R, Cao J. Evaluation of modified vaccinia virus Ankara based recombinant SARS vaccine in ferrets. Vaccine 23(17-18), 2273-2279 (2005). (Pubitemid 40341466)
64. Bukreyev A, Lamirande EW, Buchholz UJ et al. 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(9427), 2122-2127 (2004). (Pubitemid 38844152)
65. Buchholz UJ, Bukreyev A, Yang L et al. Contributions of the structural proteins of severe acute respiratory syndrome coronavirus to protective immunity. Proc. Natl Acad. Sci. USA 101(26), 9804-9809 (2004). (Pubitemid 38869317)
66. Du L, Zhao G, Lin Y et al. 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(2), 948-956 (2008).
67. DiNapoli JM, Kotelkin A, Yang L et al. Newcastle disease virus, a host rangerestricted virus, as a vaccine vector for intranasal immunization against emerging pathogens. Proc. Natl Acad. Sci. USA 104(23), 9788-9793 (2007). (Pubitemid 47175345)
68. Kapadia SU, Simon ID, Rose JK. SARS vaccine based on a replication-defective recombinant vesicular stomatitis virus is more potent than one based on a replication-competent vector. Virology 376(1), 165-172 (2008).
69. Liniger M, Zuniga A, Tamin A et al. Induction of neutralising antibodies and cellular immune responses against SARS coronavirus by recombinant measles viruses. Vaccine 26(17), 2164-2174 (2008).
70. Faber M, Lamirande EW, Roberts A et al. A single immunization with a rhabdovirusbased vector expressing severe acute respiratory syndrome coronavirus (SARS-CoV) S protein results in the production of high levels of SARS-CoVneutralizing antibodies. J. Gen. Virol. 86(Pt 5), 1435-1440 (2005). (Pubitemid 40613261)
71. Bai B, Lu X, Meng J et al. Vaccination of mice with recombinant baculovirus expressing spike or nucleocapsid protein of SARS-like coronavirus generates humoral and cellular immune responses. Mol. Immunol. 45(4), 868-875 (2008). (Pubitemid 350016349)
72. Luo F, Feng Y, Liu M et al. Type IVB pilus operon promoter controlling expression of the severe acute respiratory syndromeassociated coronavirus nucleocapsid gene in Salmonella enterica serovar Typhi elicits full immune response by intranasal vaccination. Clin. Vaccine Immunol. 14(8), 990-997 (2007).
73. Enjuanes L, Smerdou C, Castilla J et al. Development of protection against coronavirus induced diseases. A review. Adv. Exp. Med. Biol. 380, 197-211 (1995).
74. Navas-Martin S, Weiss SR. SARS: lessons learned from other coronaviruses. Viral Immunol. 16(4), 461-474 (2003). (Pubitemid 38036774)
75. See R, Roper RL, Brunham RC, Finlay BB. Rapid response research - SARS coronavirus vaccines and application of processes to other emerging infectious diseases. Curr. Immunol. Rev. 1(2), 185-200 (2005).
76. Li W, Moore MJ, Vasilieva N et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426(6965), 450-454 (2003). (Pubitemid 37490132)
77. Berger A, Drosten C, Doerr HW, Sturmer M, Preiser W. Severe acute respiratory syndrome (SARS) - paradigm of an emerging viral infection. J. Clin. Virol. 29(1), 13-22 (2004). (Pubitemid 37524081)
78. Yang ZY, Kong WP, Huang Y et al. A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice. Nature 428(6982), 561-564 (2004). (Pubitemid 38480539)
79. Pang H, Liu Y, Han X et al. Protective humoral responses to severe acute respiratory syndrome-associated coronavirus: implications for the design of an effective protein-based vaccine. J. Gen. Virol. 85(Pt 10), 3109-3113 (2004). (Pubitemid 39360055)
80. Olsen CW. A review of feline infectious peritonitis virus: molecular biology, immunopathogenesis, clinical aspects, and vaccination. Vet. Microbiol. 36(1-2), 1-37 (1993). (Pubitemid 23244362)
81. Wesseling JG, Godeke GJ, Schijns VE et al. Mouse hepatitis virus spike and nucleocapsid proteins expressed by adenovirus vectors protect mice against a lethal infection. J. Gen. Virol. 74, 2061-2069 (1993). (Pubitemid 23299883)
82. Stohlman SA, Bergmann CC, van der Veen RC, Hinton DR. Mouse hepatitis virus-specific cytotoxic T lymphocytes protect from lethal infection without eliminating virus from the central nervous system. J. Virol. 69(2), 684-694 (1995).
83. Stohlman SA, Kyuwa S, Polo JM et al. Characterization of mouse hepatitis virus-specific cytotoxic T cells derived from the central nervous system of mice infected with the JHM strain. J. Virol. 67(12), 7050-7059 (1993). (Pubitemid 23343830)
84. Seo SH, Wang L, Smith R, Collisson EW. The carboxyl-terminal 120-residue polypeptide of infectious bronchitis virus nucleocapsid induces cytotoxic T lymphocytes and protects chickens from acute infection. J. Virol. 71(10), 7889-7894 (1997). (Pubitemid 27391739)
85. Boots AM, Kusters JG, van Noort JM et al. Localization of a T-cell epitope within the nucleocapsid protein of avian coronavirus. Immunology 74(1), 8-13 (1991).
86. Collisson EW, Pei J, Dzielawa J, Seo SH. Cytotoxic T lymphocytes are critical in the control of infectious bronchitis virus in poultry. Dev. Comp. Immunol. 24(2-3), 187-200 (2000). (Pubitemid 30136300)
87. Zhu MS, Pan Y, Chen HQ et al. Induction of SARS-nucleoprotein-specific immune response by use of DNA vaccine. Immunol. Lett. 92(3), 237-243 (2004). (Pubitemid 38471964)
88. Kim TW, Lee JH, Hung CF et al. Generation and characterization of DNA vaccines targeting the nucleocapsid protein of severe acute respiratory syndrome coronavirus. J. Virol. 78(9), 4638-4645 (2004). (Pubitemid 38501085)
89. Du L, He Y, Jiang S, Zheng BJ. Development of subunit vaccines against severe acute respiratory syndrome. Drugs Today (Barc.) 44(1), 63-73 (2008).
90. Gurunathan S, Klinman DM, Seder RA. DNA vaccines: immunology, application, and optimization. Annu. Rev. Immunol. 18, 927-974 (2000). (Pubitemid 30365401)
91. Zeng F, Chow KY, Hon CC et al. Characterization of humoral responses in mice immunized with plasmid DNAs encoding SARS-CoV spike gene fragments. Biochem. Biophys. Res. Commun. 315(4), 1134-1139 (2004). (Pubitemid 38249421)
92. Zakhartchouk AN, Viswanathan S, Moshynskyy I, Petric M, Babiuk LA. Optimization of a DNA vaccine against SARS. DNA Cell. Biol. 26(10), 721-726 (2007).
93. Callendret B, Lorin V, Charneau P et al. Heterologous viral RNA export elements improve expression of severe acute respiratory syndrome (SARS) coronavirus spike protein and protective efficacy of DNA vaccines against SARS. Virology 363(2), 288-302 (2007). (Pubitemid 46764943)
94. Wang Z, Yuan Z, Matsumoto M, Hengge UR, Chang YF. Immune responses with DNA vaccines encoded different gene fragments of severe acute respiratory syndrome coronavirus in BALB/c mice. Biochem. Biophys. Res. Commun. 327(1), 130-135 (2005). (Pubitemid 40051362)
95. Wang X, Xu W, Tong D et al. 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(1-2), 71-77 (2008).
96. Zhao P, Cao J, Zhao LJ et al. Immune responses against SARS-coronavirus nucleocapsid protein induced by DNA vaccine. Virology 331(1), 128-135 (2005). (Pubitemid 39593638)
97. Gupta V, Tabiin TM, Sun K et al. SARS coronavirus nucleocapsid immunodominant T-cell epitope cluster is common to both exogenous recombinant and endogenous DNA-encoded immunogens. Virology 347(1), 127-139 (2006).
98. Cheung YK, Cheng SC, Sin FW, Chan KT, Xie Y. Induction of T-cell response by a DNA vaccine encoding a novel HLA-A*0201 severe acute respiratory syndrome coronavirus epitope. Vaccine 25(32), 6070-6077 (2007). (Pubitemid 47079137)
99. Okada M, Okuno Y, Hashimoto S et al. Development of vaccines and passive immunotherapy against SARS corona virus using SCID-PBL/hu mouse models. Vaccine 25(16), 3038-3040 (2007). (Pubitemid 46509464)
100. Zakhartchouk AN, Liu Q, Petric M, Babiuk LA. Augmentation of immune responses to SARS coronavirus by a combination of DNA and whole killed virus vaccines. Vaccine 23(35), 4385-4391 (2005). (Pubitemid 40991225)
101. Ma C, Yao K, Zhou F, Zhu M. Comparative immunization in BALB/c mice with recombinant replicationdefective adenovirus vector and DNA plasmid expressing a SARS-CoV nucleocapsid protein gene. Cell Mol. Immunol. 3(6), 459-465 (2006).
102. DeDiego ML, Alvarez E, Almazan F et al. A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J. Virol. 81(4), 1701-1713 (2007). (Pubitemid 46214445)
103. Dediego ML, Pewe L, Alvarez E et al. Pathogenicity of severe acute respiratory coronavirus deletion mutants in hACE-2 transgenic mice. Virology 376(2), 379-389 (2008).
104. Lamirande EW, DeDiego ML, Roberts A et al. A live attenuated severe acute respiratory syndrome coronavirus is immunogenic and efficacious in golden Syrian hamsters. J. Virol. 82(15), 7721-7724 (2008). (Pubitemid 352031238)
105. Zust R, Cervantes-Barragan L, Kuri T et al. Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines. PLoS Pathog. 3(8), e109 (2007). (Pubitemid 47359084)
106. Yount B, Roberts RS, Sims AC et al. Severe acute respiratory syndrome coronavirus group-specific open reading frames encode nonessential functions for replication in cell cultures and mice. J. Virol. 79(23), 14909-14922 (2005). (Pubitemid 41636288)
107. de Haan CA, Masters PS, Shen X, Weiss S, Rottier PJ. The group-specific murine coronavirus genes are not essential, but their deletion, by reverse genetics, is attenuating in the natural host. Virology 296(1), 177-189 (2002). (Pubitemid 34936777)
108. Enjuanes L, Dediego ML, Alvarez E et al. Vaccines to prevent severe acute respiratory syndrome coronavirus-induced disease. Virus Res. 133(1), 45-62 (2008). •• Excellent comprehensive review also covering serotypes and attenuated SARS vaccines.
109. Kuiken T, Fouchier RA, Schutten M et al. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362(9380), 263-270 (2003). (Pubitemid 36936836)
110. McAuliffe J, Vogel L, Roberts A et al. Replication of SARS coronavirus administered into the respiratory tract of African Green, rhesus and cynomolgus monkeys. Virology 330(1), 8-15 (2004). (Pubitemid 39446562)
111. Subbarao K, McAuliffe J, Vogel L et al. 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(7), 3572-3577 (2004). (Pubitemid 38568299)
112. Glass WG, Subbarao K, Murphy B, Murphy PM. Mechanisms of host defense following severe acute respiratory syndrome-coronavirus (SARS-CoV) pulmonary infection of mice. J. Immunol. 173(6), 4030-4039 (2004). (Pubitemid 39280767)
113. Roberts A, Vogel L, Guarner J et al. Severe acute respiratory syndrome coronavirus infection of golden Syrian hamsters. J. Virol. 79(1), 503-511 (2005). (Pubitemid 39648403)
114. Xiao Y, Meng Q, Yin X et al. Pathological changes in masked palm civets experimentally infected by severe acute respiratory syndrome (SARS) coronavirus. J. Comp. Pathol. 138(4), 171-179 (2008).
115. Roberts A, Lamirande EW, Vogel L et al. Animal models and vaccines for SARS-CoV infection. Virus Res. 133(1), 20-32 (2008). •• Excellent review focusing on different animal models up to early 2008.
116. Rockx B, Sheahan T, Donaldson E et al. Synthetic reconstruction of zoonotic and early human severe acute respiratory syndrome coronavirus isolates that produce fatal disease in aged mice. J. Virol. 81(14), 7410-7423 (2007). (Pubitemid 47047830)
117. McCray PB Jr, Pewe L, Wohlford-Lenane C et al. Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J. Virol. 81(2), 813-821 (2007). (Pubitemid 46067907)
118. Tseng CT, Huang C, Newman P et al. Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human angiotensin-converting enzyme 2 virus receptor. J. Virol. 81(3), 1162-1173 (2007). (Pubitemid 46167838)
119. Yang XH, Deng W, Tong Z et al. Mice transgenic for human angiotensinconverting enzyme 2 provide a model for SARS coronavirus infection. Comp. Med. 57(5), 450-459 (2007). (Pubitemid 351773338)
120. ter Meulen J, Bakker AB, van den Brink EN et al. Human monoclonal antibody as prophylaxis for SARS coronavirus infection in ferrets. Lancet 363(9427), 2139-2141 (2004).
121. Weingartl H, Czub M, Czub S et al. Immunization with modified vaccinia virus Ankara-based recombinant vaccine against severe acute respiratory syndrome is associated with enhanced hepatitis in ferrets. J. Virol. 78(22), 12672-12676 (2004). (Pubitemid 39458786)
122. To KF, Tong JH, Chan PK et al. Tissue and cellular tropism of the coronavirus associated with severe acute respiratory syndrome: an in-situ hybridization study of fatal cases. J. Pathol. 202(2), 157-163 (2004). (Pubitemid 38208652)
123. Skowronski DM, Astell C, Brunham RC et al. Severe acute respiratory syndrome (SARS): a year in review. Annu. Rev. Med. 56, 357-381 (2005). (Pubitemid 40299788)
124. Lawler JV, Endy TP, Hensley LE et al. Cynomolgus macaque as an animal model for severe acute respiratory syndrome. PLoS Med. 3(5), e149 (2006). (Pubitemid 43807037)
125. Weiss RC, Scott FW. Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp. Immunol. Microbiol. Infect. Dis. 4(2), 175-189 (1981). (Pubitemid 11024966)
126. Kam YW, Kien F, Roberts A et al. Antibodies against trimeric S glycoprotein protect hamsters against SARS-CoV challenge despite their capacity to mediate FcgRII-dependent entry into B cells in vitro. Vaccine 25(4), 729-740 (2007). (Pubitemid 44856104)
127. Deming D, Sheahan T, Heise M et al. Vaccine efficacy in senescent mice challenged with recombinant SARS-CoV bearing epidemic and zoonotic spike variants. PLoS Med. 3(12), 525 (2006). (Pubitemid 46028512)
128. Tan YJ, Goh PY, Fielding BC et al. Profiles of antibody responses against severe acute respiratory syndrome coronavirus recombinant proteins and their potential use as diagnostic markers. Clin. Diagn. Lab. Immunol. 11(2), 362-371 (2004). (Pubitemid 38380819)
129. Woo PC, Lau SK, Wong BH et al. Detection of specific antibodies to severe acute respiratory syndrome (SARS) coronavirus nucleocapsid protein for serodiagnosis of SARS coronavirus pneumonia. J. Clin. Microbiol. 42(5), 2306-2309 (2004). (Pubitemid 38637872)
130. Liu X, Shi Y, Li P et al. Profile of antibodies to the nucleocapsid protein of the severe acute respiratory syndrome (SARS)-associated coronavirus in probable SARS patients. Clin. Diagn. Lab. Immunol. 11(1), 227-228 (2004). (Pubitemid 38090680)
131. Greenough TC, Carville A, Coderre J et al. Pneumonitis and multi-organ system disease in common marmosets (Callithrix jacchus) infected with the severe acute respiratory syndrome-associated coronavirus. Am J. Pathol. 167(2), 455-463 (2005). (Pubitemid 43026101)
132. Sui J, Li W, Murakami A et al. Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc. Natl Acad. Sci. USA 101(8), 2536-2541 (2004). (Pubitemid 38269346)
133. Traggiai E, Becker S, Subbarao K et al. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat. Med. 10(8), 871-875 (2004). (Pubitemid 39070862)
134. Roper RL, Payne LG, Moss B. Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene. J. Virol. 70(6), 3753-3762 (1996). (Pubitemid 26157355)
135. Fogg C, Lustig S, Whitbeck JC et al. Protective immunity to vaccinia virus induced by vaccination with multiple recombinant outer membrane proteins of intracellular and extracellular virions. J. Virol. 78(19), 10230-10237 (2004). (Pubitemid 39258347)
136. Golden JW, Hooper JW. Heterogeneity in the A33 protein impacts the cross-protective efficacy of a candidate smallpox DNA vaccine. Virology 377(1), 19-29 (2008).
137. Hu MC, Jones T, Kenney RT et al. Intranasal protollin-formulated recombinant SARS S-protein elicits respiratory and serum neutralizing antibodies and protection in mice. Vaccine 25(34), 6334-6340 (2007). • Shows the importance of mucosal immunity. (Pubitemid 47088756)
138. + T-cell responses in recovered severe acute respiratory syndrome (SARS) patients to SARS coronavirus M antigen. J. Gen.Virol. 88(Pt 10), 2740-2748 (2007).
139. Qiu M, Shi Y, Guo Z et al. Antibody responses to individual proteins of SARS coronavirus and their neutralization activities. Microbes Infect. 7(5-6), 882-889 (2005). (Pubitemid 40826655)
140. WHO. Annex Table 2. Deaths by cause, sex and mortality stratum www.who.int/whr/2004/en/09-annexes- en.pdf
141. WHO. Update 4: review of probable and laboratory-confirmed SARS cases in southern China. Epidemic and pandemic alert and response (2004) www.who.int/csr/don/2004-2001-2027/ en/
142. WHO. Summary of probable SARS cases with onset of illness from 1 November 2002 to 31 July 2003. 26 September 2003. www.who.int/csr/sars/country/ table2003-09-23/en/