The immunobiology of SARS

Annual Review of Immunology

Volumn 25, Issue , 2007, Pages 443-472

  Chen, Jun ^a   Subbarao, Kanta ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

ACE2; Chemokines; Cytokines; Immune response; SARS CoV

Indexed keywords

CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; SEVERE ACUTE RESPIRATORY SYNDROME VACCINE; TUMOR NECROSIS FACTOR ALPHA; ANGIOTENSIN CONVERTING ENZYME 2; CD209 ANTIGEN; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; CHEMOKINE; CLEC4M PROTEIN, HUMAN; DC-SPECIFIC ICAM-3 GRABBING NONINTEGRIN; DIPEPTIDYL CARBOXYPEPTIDASE; INTERFERON; LECTIN; UNCLASSIFIED DRUG; VIRUS ANTIBODY;

ACUTE RESPIRATORY TRACT DISEASE; BLOOD; CLINICAL FEATURE; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; GASTROINTESTINAL TRACT; HUMAN; IMMUNOBIOLOGY; INNATE IMMUNITY; KIDNEY; LIVER; LUNG; LUNG ALVEOLUS; MORTALITY; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; REVIEW; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS REPLICATION; ANIMAL; ANTIBODY SPECIFICITY; DISEASE MODEL; IMMUNOLOGY; INFLAMMATION;

ANIMALS; ANTIBODIES, VIRAL; CELL ADHESION MOLECULES; CHEMOKINES; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; INTERFERON TYPE I; LECTINS, C-TYPE; ORGAN SPECIFICITY; PEPTIDYL-DIPEPTIDASE A; RECEPTORS, CELL SURFACE; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME;

EID: 34247842741     PISSN: 07320582     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.immunol.25.022106.141706     Document Type: Review

References (176)

1. Tsang KW, Ho PL, Ooi GC, Yee WK, Wang T, et al. 2003. A cluster of cases of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 348:1977-85
2. Lee N, Hui D, Wu A, Chan P, Cameron P, et al. 2003. A major outbreak of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 348:1986-94
3. Poutanen SM, Low DE, Henry B, Finkelstein S, Rose D, et al. 2003. Identification of severe acute respiratory syndrome in Canada. N. Engl. J. Med. 348:1995-2005
4. Drosten C, Gunther S, Preiser W, van der Werf S, Brodt HR, et al. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967-76
5. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, et al. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953-66
6. Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, et al. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-25
7. Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, et al. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-99
8. Marra MA, Jones SJ, Astell CR, Holt RA, Brooks-Wilson A, et al. 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399-404
9. Peiris JS, Yuen KY, Osterhaus AD, Stohr K. 2003. The severe acute respiratory syndrome. N. Engl. J. Med. 349:2431-41
10. Poon LL, Guan Y, Nicholls JM, Yuen KY, Peiris JS. 2004. The etiology, origins, and diagnosis of severe acute respiratory syndrome. Lancet Infect. Dis. 4:663-71
11. Donnelly CA, Fisher MC, Fraser C, Ghani AC, Riley S, et al. 2004. Epidemiological and genetic analysis of severe acute respiratory syndrome. Lancet Infect. Dis. 4:672-83
12. Subbarao K, Roberts A. 2006. Is there an ideal animal model for SARS? Trends Microbiol. 14:299-303
13. Peiris JS, Guan Y, Yuen KY. 2004. Severe acute respiratory syndrome. Nat. Med. 10:S88-97
14. Lau YL. 2004. SARS: future research and vaccine. Paediatr. Respir. Rev. 5:300-3
15. Weinstein RA. 2004. Planning for epidemics - the lessons of SARS. N. Engl. J. Med. 350:2332-34
16. Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, et al. 2003. Isolation and characterization of viruses related to the SARS Coronavirus from animals in southern China. Science 302:276-78
17. Stadler K, Masignani V, Eickmann M, Becker S, Abrignani S, et al. 2003. SARS - beginning to understand a new virus. Nat. Rev. Microbiol. 1:209-18
18. Yu IT, Li Y, Wong TW, Tam W, Chan AT, et al. 2004. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N. Engl. J. Med. 350:1731-39
19. Peiris JS, Chu CM, Cheng VC, Chan KS, Hung IF, et al. 2003. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 361:1767-72
20. Poon LL, Wong OK, Chan KH, Luk W, Yuen KY, et al. 2003. Rapid diagnosis of a coronavirus associated with severe acute respiratory syndrome (SARS). Clin. Chem. 49:953-55
21. Nicholls JM, Poon LL, Lee KC, Ng WF, Lai ST, et al. 2003. Lung pathology of fatal severe acute respiratory syndrome. Lancet 361:1773-78
22. Ng EK, Hui DS, Chan KC, Hung EC, Chiu RW, et al. 2003. Quantitative analysis and prognostic implication of SARS coronavirus RNA in the plasma and serum of patients with severe acute respiratory syndrome. Clin. Chem. 49:1976-80
23. Gu J, Gong E, Zhang B, Zheng J, Gao Z, et al. 2005. Multiple organ infection and the pathogenesis of SARS. J. Exp. Med. 202:415-24
24. Wong RS, Wu A, To KF, Lee N, Lam CW, et al. 2003. Haematological manifestations in patients with severe acute respiratory syndrome: retrospective analysis. BMJ 326:1358-62
25. Leung GM, Hedley AJ, Ho LM, Chau P, Wong IO, et al. 2004. The epidemiology of severe acute respiratory syndrome in the 2003 Hong Kong epidemic: an analysis of all 1755 patients. Ann. Intern. Med. 141:662-73
26. Hon KL, Leung CW, Cheng WT, Chan PK, Chu WC, et al. 2003. Clinical presentations and outcome of severe acute respiratory syndrome in children. Lancet 361:1701-3
27. Yilla M, Harcourt BH, Hickman CJ, McGrew M, Tamin A, et al. 2005. SARS-coronavirus replication in human peripheral monocytes/macrophages. Virus Res. 107:93-101
28. Zhong NS, Zheng BJ, Li YM, Poon, Xie ZH, et al. 2003. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. Lancet 362:1353-58
29. Breiman RF, Evans MR, Preiser W, Maguire J, Schnur A, et al. 2003. Role of China in the quest to define and control severe acute respiratory syndrome. Emerg. Infect. Dis. 9:1037-41
30. Xu RH, He JF, Evans MR, Peng GW, Field HE, et al. 2004. Epidemiologic clues to SARS origin in China. Emerg. Infect. Dis. 10:1030-37
31. Tu C, Crameri G, Kong X, Chen J, Sun Y, et al. 2004. Antibodies to SARS coronavirus in civets. Emerg. Infect. Dis. 10:2244-48
32. Wu D, Tu C, Xin C, Xuan H, Meng Q, et al. 2005. Civets are equally susceptible to experimental infection by two different severe acute respiratory syndrome coronavirus isolates. J. Virol. 79:2620-25
33. Li W, Shi Z, Yu M, Ren W, Smith C, et al. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676-79
34. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, et al. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. USA 102:14040-45
35. Murray K, Selleck P, Hooper P, Hyatt A, Gould A, et al. 1995. A morbillivirus that caused fatal disease in horses and humans. Science 268:94-97
36. Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A, et al. 2000. Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432-35
37. Sulkin SE, Allen R. 1974. Virus infections in bats. Monogr. Virol. 8:1-103
38. Simmons G, Reeves JD, Rennekamp AJ, Amberg SM, Piefer AJ, Bates P. 2004. Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. Proc. Natl. Acad. Sci. USA 101:4240-45
39. Yang ZY, Huang Y, Ganesh L, Leung K, Kong WP, et al. 2004. pH-dependent entry of severe acute respiratory syndrome coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC-SIGN. J. Virol. 78:5642-50
40. Kielian M, Rey FA. 2006. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4:67-76
41. Liu S, Xiao G, Chen Y, He Y, Niu J, et al. 2004. Interaction between heptad repeat 1 and 2 regions in spike protein of SARS-associated coronavirus: implications for virus fusogenic mechanism and identification of fusion inhibitors. Lancet 363:938-47
42. Bosch BJ, Martina BE, van der Zee R, Lepault J, Haijema BJ, et al. 2004. Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc. Natl. Acad. Sci. USA 101:8455-60
43. 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. USA 102:11876-81
44. Tripet B, Howard MW, Jobling M, Holmes RK, Holmes KV, Hodges RS. 2004. Structural characterization of the SARS-coronavirus spike S fusion protein core. J. Biol. Chem. 279:20836-49
45. Bosch BJ, van der Zee R, de Haan CA, Rottier PJ. 2003. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77:8801-11
46. Hofmann H, Pohlmann S. 2004. Cellular entry of the SARS coronavirus. Trends Microbiol. 12:466-72
47. Dimitrov DS. 2003. The secret life of ACE2 as a receptor for the SARS virus. Cell 115:652-53
48. Xiao X, Chakraborti S, Dimitrov AS, Gramatikoff K, Dimitrov DS. 2003. The SARS-CoV S glycoprotein: expression and functional characterization. Biochem. Biophys. Res. Commun. 312:1159-64
49. Dveksler GS, Dieffenbach CW, Cardellichio CB, McCuaig K, Pensiero MN, et al. 1993. Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus-A59. J. Virol. 67:1-8
50. Delmas B, Gelfi J, L'Haridon R, Vogel LK, Sjostrom H, et al. 1992. Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357:417-20
51. 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. 70:8669-74
52. Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, et al. 1992. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357:420-22
53. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, et al. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-54
54. Wang P, Chen J, Zheng A, Nie Y, Shi X, et al. 2004. Expression cloning of functional receptor used by SARS coronavirus. Biochem. Biophys. Res. Commun. 315:439-44
55. Babcock GJ, Esshaki DJ, Thomas WDJ, Ambrosino DM. 2004. Amino acids 270 to 510 of the severe acute respiratory syndrome coronavirus spike protein are required for interaction with receptor. J. Virol. 78:4552-60
56. Hamming I, Timens W, Bulthuis ML, Lely AT, Navis GJ, van Goor H. 2004. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 203:631-37
57. Ding Y, He L, Zhang Q, Huang Z, Che X, et al. 2004. Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J. Pathol. 203:622-30
58. Sims AC, Baric RS, Yount B, Burkett SE, Collins PL, Pickles RJ. 2005. Severe acute respiratory syndrome coronavirus infection of human ciliated airway epithelia: role of ciliated cells in viral spread in the conducting airways of the lungs. J. Virol. 79:15511-24
59. Jia HP, Look DC, Shi L, Hickey M, Pewe L, et al. 2005. ACE2 receptor expression and severe acute respiratory syndrome coronavirus infection depend on differentiation of human airway epithelia. J. Virol. 79:14614-21
60. Leung WK, To KF, Chan PK, Chan HL, Wu AK, et al. 2003. Enteric involvement of severe acute respiratory syndrome-associated coronavirus infection. Gastroenterology 125:1011-17
61. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, et al. 2002. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 417:822-28
62. Yagil Y, Yagil C. 2003. Hypothesis: ACE2 modulates blood pressure in the mammalian organism. Hypertension 41:871-73
63. Imai Y, Kuba K, Rao S, Huan Y, Guo F, et al. 2005. Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 436:112-16
64. Kuba K, Imai Y, Rao S, Gao H, Guo F, et al. 2005. A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat. Med. 11:875-79
65. Perlman S, Dandekar AA. 2005. Immunopathogenesis of coronavirus infections: implications for SARS. Nat. Rev. Immunol. 5:917-27
66. Nicholls J, Peiris M. 2005. Good ACE, bad ACE do battle in lung injury, SARS. Nat. Med. 11:821-22
67. Harmer D, Gilbert M, Borman R, Clark KL. 2002. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett. 532:107-10
68. Subbarao K, McAuliffe J, Vogel L, Fahle G, Fischer S, et al. 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. 78:3572-77
69. Hofmann H, Pyrc K, van der Hoek L, Geier M, Berkhout B, Pohlmann S. 2005. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl. Acad. Sci. USA 102:7988-93
70. Li W, Zhang C, Sui J, Kuhn JH, Moore MJ, et al. 2005. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 24:1634-43
71. Li W, Wong SK, Li F, Kuhn JH, Huang IC, et al. 2006. Animal origins of the severe acute respiratory syndrome coronavirus: insight from ACE2-S-protein interactions. J. Virol. 80:4211-19
72. van Kooyk Y, Geijtenbeek TB. 2003. DC-SIGN: escape mechanism for pathogens. Nat. Rev. Immunol. 3:697-709
73. Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, et al. 2000. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100:575-85
74. Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, et al. 2003. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am. J. Pathol. 162:887-96
75. Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J, et al. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197:823-29
76. Alvarez CP, Lasala F, Carrillo J, Muniz O, Corbi AL, Delgado R. 2002. C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J. Virol. 76:6841-44
77. Halary F, Amara A, Lortat-Jacob H, Messerle M, Delaunay T, et al. 2002. Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity 17:653-64
78. Pohlmann S, Zhang J, Baribaud F, Chen Z, Leslie GJ, et al. 2003. Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J. Virol. 77:4070-80
79. Simmons G, Reeves JD, Grogan CC, Vandenberghe LH, Baribaud F, et al. 2003. DC-SIGN and DC-SIGNR bind Ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 305:115-23
80. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, et al. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587-97
81. Soilleux EJ, Barten R, Trowsdale J. 2000. DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J. Immunol. 165:2937-42
82. Soilleux EJ. 2003. DC-SIGN (dendritic cell-specific ICAM-grabbing nonintegrin) and DC-SIGN-related (DC-SIGNR): friend or foe? Clin. Sci. 104:437-46
83. Bashirova AA, Geijtenbeek TB, van Duijnhoven GC, van Vliet SJ, Eilering JB, et al. 2001. A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J. Exp. Med. 193:671-78
84. Gramberg T, Hofmann H, Moller P, Lalor PF, Marzi A, et al. 2005. LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus. Virology 340:224-36
85. Jeffers SA, Tusell SM, Gillim-Ross L, Hemmila EM, Achenbach JE, et al. 2004. CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 101:15748-53
86. Cheng PK, Wong DA, Tong LK, Ip SM, Lo AC, et al. 2004. Viral shedding patterns of coronavirus in patients with probable severe acute respiratory syndrome. Lancet 363:1699-700
87. Hung IF, Cheng VC, Wu AK, Tang BS, Chan KH, et al. 2004. Viral loads in clinical specimens and SARS manifestations. Emerg. Infect. Dis. 10:1550-57
88. Drosten C, Chiu LL, Panning M, Leong HN, Preiser W, et al. 2004. Evaluation of advanced reverse transcription-PCR assays and an alternative PCR target region for detection of severe acute respiratory syndrome-associated coronavirus. J. Clin. Microbiol. 42:2043-47
89. To KF, Tong JH, Chan PK, Au FW, Chim SS, et al. 2004. Tissue and cellular tropism of the coronavirus associated with severe acute respiratory syndrome: an in-situ hybridization study of fatal cases. J. Pathol. 202:157-63
90. Nicholls JM, Butany J, Poon LL, Chan KH, Beh SL, et al. 2006. Time course and cellular localization of SARS-CoV nucleoprotein and RNA in lungs from fatal cases of SARS. PLoS Med. 3:e27
91. Shieh WJ, Hsiao CH, Paddock CD, Guarner J, Goldsmith CS, et al. 2005. Immunohistochemical, in situ hybridization, and ultrastructural localization of SARS-associated coronavirus in lung of a fatal case of severe acute respiratory syndrome in Taiwan. Hum. Pathol. 36:303-9
92. Mazzulli T, Farcas GA, Poutanen SM, Willey BM, Low DE, et al. 2004. Severe acute respiratory syndrome-associated coronavirus in lung tissue. Emerg. Infect. Dis. 10:20-24
93. Farcas GA, Poutanen SM, Mazzulli T, Willey BM, Butany J, et al. 2005. Fatal severe acute respiratory syndrome is associated with multiorgan involvement by coronavirus. J. Infect. Dis. 191:193-97
94. Law PT, Wong CH, Au TC, Chuck CP, Kong SK, et al. 2005. The 3a protein of severe acute respiratory syndrome-associated coronavirus induces apoptosis in Vero E6 cells. J. Gen. Virol. 86:1921-30
95. Tan YJ, Fielding BC, Goh PY, Shen S, Tan TH, et al. 2004. Overexpression of 7a, a protein specifically encoded by the severe acute respiratory syndrome coronavirus, induces apoptosis via a caspase-dependent pathway. J. Virol. 78:14043-47
96. 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. 80:785-93
97. Cheung OY, Chan JW, Ng CK, Koo CK. 2004. The spectrum of pathological changes in severe acute respiratory syndrome (SARS). Histopathology 45:119-24
98. Hwang DM, Chamberlain DW, Poutanen SM, Low DE, Asa SL, Butany J. 2005. Pulmonary pathology of severe acute respiratory syndrome in Toronto. Mod. Pathol. 18:1-10
99. Tse GM, To KF, Chan PK, Lo AW, Ng KC, et al. 2004. Pulmonary pathological features in coronavirus associated severe acute respiratory syndrome (SARS). J. Clin. Pathol. 57:260-65
100. Chu KH, Tsang WK, Tang CS, Lam MF, Lai FM, et al. 2005. Acute renal impairment in coronavirus-associated severe acute respiratory syndrome. Kidney Int. 67:698-705
101. Leung TW, Wong KS, Hui AC, To KF, Lai ST, et al. 2005. Myopathic changes associated with severe acute respiratory syndrome: a postmortem case series. Arch. Neurol. 62:1113-17
102. Ng WF, To KF, Lam WW, Ng TK, Lee KC. 2006. The comparative pathology of severe acute respiratory syndrome and avian influenza A subtype H5N1 - a review. Hum. Pathol. 37:381-90
103. Lang Z, Zhang L, Zhang S, Meng X, Li J, et al. 2003. Pathological study on severe acute respiratory syndrome. Chin. Med. J. 116:976-80
104. To KF, Chan PK, Chan KF, Lee WK, Lam WY, et al. 2001. Pathology of fatal human infection associated with avian influenza A H5N1 virus. J. Med. Virol. 63:242-46
105. Peiris JS, Yu WC, Leung CW, Cheung CY, Ng WF, et al. 2004. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 363:617-19
106. Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W, et al. 2005. Probable person-to-person transmission of avian influenza A (H5N1). N. Engl. J. Med. 352:333-40
107. Chokephaibulkit K, Uiprasertkul M, Puthavathana P, Chearskul P, Auewarakul P, et al. 2005. A child with avian influenza A (H5N1) infection. Pediatr. Infect. Dis. J. 24:162-66
108. Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, et al. 2005. Influenza A H5N1 replication sites in humans. Emerg. Infect. Dis. 11:1036-41
109. National Research Project for SARS, Beijing Group. 2004. The involvement of natural killer cells in the pathogenesis of severe acute respiratory syndrome. Am. J. Clin. Pathol. 121:507-11
110. Glass WG, Subbarao K, Murphy B, Murphy PM. 2004. Mechanisms of host defense following severe acute respiratory syndrome-coronavirus (SARS-CoV) pulmonary infection of mice. J. Immunol. 173:4030-39
111. Chen JH, Chang YW, Yao CW, Chiueh TS, Huang SC, et al. 2004. Plasma proteome of severe acute respiratory syndrome analyzed by two-dimensional gel electrophoresis and mass spectrometry. Proc. Natl. Acad. Sci. USA 101:17039-44
112. Cinatl J Jr, Michaelis M, Scholz M, Doerr HW. 2004. Role of interferons in the treatment of severe acute respiratory syndrome. Expert. Opin. Biol. Ther. 4:827-36
113. Spiegel M, Pichlmair A, Martinez-Sobrido L, Cros J, Garcia-Sastre A, et al. 2005. Inhibition of beta interferon induction by severe acute respiratory syndrome coronavirus suggests a two-step model for activation of interferon regulatory factor 3. J. Virol. 79:2079-86
114. Cinatl J, Morgenstern B, Bauer G, Chandra P, Rabenau H, Doerr HW. 2003. Treatment of SARS with human interferons. Lancet 362:293-94
115. Haagmans BL, Kuiken T, Martina BE, Fouchier RA, Rimmelzwaan GF, et al. 2004. Pegylated interferon-α protects type 1 pneumocytes against SARS coronavirus infection in macaques. Nat. Med. 10:290-93
116. Cheung CY, Poon LL, Ng IH, Luk W, Sia SF, et al. 2005. Cytokine responses in severe acute respiratory syndrome coronavirus-infected macrophages in vitro: possible relevance to pathogenesis. J. Virol. 79:7819-26
117. Tseng CT, Perrone LA, Zhu H, Makino S, Peters CJ. 2005. Severe acute respiratory syndrome and the innate immune responses: modulation of effector cell function without productive infection. J. Immunol. 174:7977-85
118. Law HK, Cheung CY, Ng HY, Sia SF, Chan YO, et al. 2005. Chemokine up-regulation in SARS-coronavirus-infected, monocyte-derived human dendritic cells. Blood 106:2366-74
119. Ng LF, Hibberd ML, Ooi EE, Tang KF, Neo SY, et al. 2004. A human in vitro model system for investigating genome-wide host responses to SARS coronavirus infection. BMC Infect. Dis. 4:34
120. Tang NL, Chan PK, Wong CK, To KF, Wu AK, et al. 2005. Early enhanced expression of interferon-inducible protein-10 (CXCL-10) and other chemokines predicts adverse outcome in severe acute respiratory syndrome. Clin. Chem. 51:2333-40
121. Jiang Y, Xu J, Zhou C, Wu Z, Zhong S, et al. 2005. Characterization of cytokine/chemokine profiles of severe acute respiratory syndrome. Am. J. Respir. Crit. Care Med. 171:850-57
122. Wong CK, Lam CW, Wu AK, Ip WK, Lee NL, et al. 2004. Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome. Clin. Exp. Immunol. 136:95-103
123. Huang KJ, Su IJ, Theron M, Wu YC, Lai SK, et al. 2005. An interferon-γ-related cytokine storm in SARS patients. J. Med. Virol. 75:185-94
124. Ng PC, Lam CW, Li AM, Wong CK, Cheng FW, et al. 2004. Inflammatory cytokine profile in children with severe acute respiratory syndrome. Pediatrics 113:e7-14
125. Zhang Y, Li J, Zhan Y, Wu L, Yu X, et al. 2004. Analysis of serum cytokines in patients with severe acute respiratory syndrome. Infect. Immun. 72:4410-15
126. Lee CH, Chen RF, Liu JW, Yeh WT, Chang JC, et al. 2004. Altered p38 mitogen-activated protein kinase expression in different leukocytes with increment of immunosuppressive mediators in patients with severe acute respiratory syndrome. J. Immunol. 172:7841-47
127. Cheng VC, Hung IF, Tang BS, Chu CM, Wong MM, et al. 2004. Viral replication in the nasopharynx is associated with diarrhea in patients with severe acute respiratory syndrome. Clin. Infect. Dis. 38:467-75
128. Reghunathan R, Jayapal M, Hsu LY, Chng HH, Tai D, et al. 2005. Expression profile of immune response genes in patients with severe acute respiratory syndrome. BMC Immunol. 6:2
129. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, et al. 2002. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360:1831-37
130. Wang YD, Sin WY, Xu GB, Yang HH, Wong TY, et al. 2004. T-cell epitopes in severe acute respiratory syndrome (SARS) coronavirus spike protein elicit a specific T-cell immune response in patients who recover from SARS. J. Virol. 78:5612-18
131. + T cells to severe acute respiratory syndrome (SARS) coronavirus in recovered SARS patients and healthy individuals. J. Immunol. 175:591-98
132. Poccia F, Agrati C, Castilletti C, Bordi L, Gioia C, et al. 2006. Anti-severe acute respiratory syndrome coronavirus immune responses: the role played by Vγ9Vδ2 T cells. J. Infect. Dis. 193:1244-49
133. Peng H, Yang LT, Wang LY, Li J, Huang J, et al. 2006. Long-lived memory T lymphocyte responses against SARS coronavirus nucleocapsid protein in SARS-recovered patients. Virology 351:466-75
134. He Z, Zhao C, Dong Q, Zhuang H, Song S, et al. 2005. Effects of severe acute respiratory syndrome (SARS) coronavirus infection on peripheral blood lymphocytes and their subsets. Int. J. Infect. Dis. 9:323-30
135. Hsueh PR, Huang LM, Chen PJ, Kao CL, Yang PC. 2004. Chronological evolution of IgM, IgA, IgG and neutralization antibodies after infection with SARS-associated coronavirus. Clin. Microbiol. Infect. 10:1062-66
136. Liu W, Fontanet A, Zhang PH, Zhan L, Xin ZT, et al. 2006. Two-year prospective study of the humoral immune response of patients with severe acute respiratory syndrome. J. Infect. Dis. 193:792-95
137. Nie Y, Wang G, Shi X, Zhang H, Qiu Y, et al. 2004. Neutralizing antibodies in patients with severe acute respiratory syndrome-associated coronavirus infection. J. Infect. Dis. 190:1119-26
138. Buchholz UJ, Bukreyev A, Yang L, Lamirande EW, Murphy BR, et al. 2004. Contributions of the structural proteins of severe acute respiratory syndrome coronavirus to protective immunity. Proc. Natl. Acad. Sci. USA 101:9804-9
139. Lu L, Manopo I, Leung BP, Chng HH, Ling AE, et al. 2004. Immunological characterization of the spike protein of the severe acute respiratory syndrome coronavirus. J. Clin. Microbiol. 42:1570-76
140. Vennema H, de Groot RJ, Harbour DA, Dalderup M, Gruffydd-Jones T, et al. 1990. Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. J. Virol. 64:1407-9
141. Bisht H, Roberts A, Vogel L, Bukreyev A, Collins PL, et al. 2004. Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice. Proc. Natl. Acad. Sci. USA 101:6641-46
142. Stadler K, Roberts A, Becker S, Vogel L, Eickmann M, et al. 2005. SARS vaccine protective in mice. Emerg. Infect. Dis. 11:1312-14
143. Yang ZY, Kong WP, Huang Y, Roberts A, Murphy BR, et al. 2004. A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice. Nature 428:561-64
144. Greenough TC, Babcock GJ, Roberts A, Hernandez HJ, Thomas WD Jr, 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. 191:507-14
145. Kuiken T, Fouchier RA, Schutten M, Rimmelzwaan GF, van Amerongen G, et al. 2003. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263-70
146. Rowe T, Gao G, Hogan RJ, Crystal RG, Voss TG, et al. 2004. Macaque model for severe acute respiratory syndrome. J. Virol. 78:11401-4
147. Qin C, Wang J, Wei Q, She M, Marasco WA, et al. 2005. An animal model of SARS produced by infection of Macaca mulatta with SARS coronavirus. J. Pathol. 206:251-59
148. McAuliffe J, Vogel L, Roberts A, Fahle G, Fischer S, et al. 2004. Replication of SARS coronavirus administered into the respiratory tract of African green, rhesus and cynomolgus monkeys. Virology 330:8-15
149. Greenough TC, Carville A, Coderre J, Somasundaran M, Sullivan JL, et al. 2005. Pneumonitis and multi-organ system disease in common marmosets (Callithrix jacchus) infected with the severe acute respiratory syndrome-associated coronavirus. Am. J. Pathol. 167:455-63
150. Martina BE, Haagmans BL, Kuiken T, Fouchier RA, Rimmelzwaan GF, et al. 2003. Virology: SARS virus infection of cats and ferrets. Nature 425:915
151. Roberts A, Vogel L, Guarner J, Hayes N, Murphy B, et al. 2005. Severe acute respiratory syndrome coronavirus infection of golden Syrian hamsters. J. Virol. 79:503-11
152. Roberts A, Paddock C, Vogel L, Butler E, Zaki S, Subbarao K. 2005. Aged BALB/c mice as a model for increased severity of severe acute respiratory syndrome in elderly humans. J. Virol. 79:5833-38
153. Hogan RJ, Gao G, Rowe T, Bell P, Flieder D, et al. 2004. Resolution of primary severe acute respiratory syndrome-associated coronavirus infection requires Stat1. J. Virol. 78:11416-21
154. Yen YT, Liao F, Hsiao CH, Kao CL, Chen YC, Wu-Hsieh BA. 2006. Modeling the early events of severe acute respiratory syndrome coronavirus infection in vitro. J. Virol. 80:2684-93
155. Lau YL, Peiris JS. 2005. Pathogenesis of severe acute respiratory syndrome. Curr. Opin. Immunol. 17:404-10
156. Lin M, Tseng HK, Trejaut JA, Lee HL, Loo JH, et al. 2003. Association of HLA class I with severe acute respiratory syndrome coronavirus infection. BMC Med. Genet. 4:9
157. Ng MH, Lau KM, Li L, Cheng SH, Chan WY, et al. 2004. Association of human-leukocyte-antigen class I (B*0703) and class II (DRB1*0301) genotypes with susceptibility and resistance to the development of severe acute respiratory syndrome. J. Infect. Dis. 190:515-18
158. Ip WK, Chan KH, Law HK, Tso GH, Kong EK, et al. 2005. Mannose-binding lectin in severe acute respiratory syndrome coronavirus infection. J. Infect. Dis. 191:1697-704
159. Chiu RW, Tang NL, Hui DS, Chung GT, Chim SS, et al. 2004. ACE2 gene polymorphisms do not affect outcome of severe acute respiratory syndrome. Clin. Chem. 50:1683-86
160. Tsui PT, Kwok ML, Yuen H, Lai ST. 2003. Severe acute respiratory syndrome: clinical outcome and prognostic correlates. Emerg. Infect. Dis. 9:1064-69
161. Bukreyev A, Lamirande EW, Buchholz UJ, Vogel LN, Elkins WR, et al. 2004. Mucosal immunization of African green monkeys (Cercopithecus aethiops) with an attenuated parainfluenza virus expressing the SARS coronavirus spike protein for the prevention of SARS. Lancet 363:2122-27
162. Kim TW, Lee JH, Hung CF, Peng S, Roden R, et al. 2004. Generation and characterization of DNA vaccines targeting the nucleocapsid protein of severe acute respiratory syndrome coronavirus. J. Virol. 78:4638-45
163. Zeng F, Chow KY, Hon CC, Law KM, Yip CW, et al. 2004. Characterization of humoral responses in mice immunized with plasmid DNAs encoding SARS-CoV spike gene fragments. Biochem. Biophys. Res. Commun. 315:1134-39
164. Zhu MS, Pan Y, Chen HQ, Shen Y, Wang XC, et al. 2004. Induction of SARS-nucleoprotein-specific immune response by use of DNA vaccine. Immunol. Lett. 92:237-43
165. Tang L, Zhu Q, Qin E, Yu M, Ding Z, et al. 2004. Inactivated SARS-CoV vaccine prepared from whole virus induces a high level of neutralizing antibodies in BALB/c mice. DNA Cell Biol. 23:391-94
166. Takasuka N, Fujii H, Takahashi Y, Kasai M, Morikawa S, et al. 2004. A subcutaneously injected UV-inactivated SARS coronavirus vaccine elicits systemic humoral immunity in mice. Int. Immunol. 16:1423-30
167. Zhou J, Wang W, Zhong Q, Hou W, Yang Z, et al. 2005. Immunogenicity, safety, and protective efficacy of an inactivated SARS-associated coronavirus vaccine in rhesus monkeys. Vaccine 23:3202-9
168. Bisht H, Roberts A, Vogel L, Subbarao K, Moss B. 2005. Neutralizing antibody and protective immunity to SARS coronavirus infection of mice induced by a soluble recombinant polypeptide containing an N-terminal segment of the spike glycoprotein. Virology 334:160-65
169. Zhang H, Wang G, Li J, Nie Y, Shi X, et al. 2004. Identification of an antigenic determinant on the S2 domain of the severe acute respiratory syndrome coronavirus spike glycoprotein capable of inducing neutralizing antibodies. J. Virol. 78:6938-45
170. Gao W, Tamin A, Soloff A, D'Aiuto L, Nwanegbo E, et al. 2003. Effects of a SARS-associated coronavirus vaccine in monkeys. Lancet 362:1895-96
171. Soo YO, Cheng Y, Wong R, Hui DS, Lee CK, et al. 2004. Retrospective comparison of convalescent plasma with continuing high-dose methylprednisolone treatment in SARS patients. Clin. Microbiol. Infect. 10:676-78
172. ter Meulen J, Bakker AB, van den Brink EN, Weverling GJ, Martina BE, et al. 2004. Human monoclonal antibody as prophylaxis for SARS coronavirus infection in ferrets. Lancet 363:2139-41
173. Sui J, Li W, Murakami A, Tamin A, Matthews LJ, et al. 2004. 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 101:2536-41
174. Traggiai E, Becker S, Subbarao K, Kolesnikova L, Uematsu Y, et al. 2004. An efficient method to make human monoclonal antibodies from memory B cells:
175. Roberts A, Thomas WD, Guarner J, Lamirande EW, Babcock GJ, et al. 2006. Therapy with a severe acute respiratory syndrome-associated coronavirus- neutralizing human monoclonal antibody reduces disease severity and viral burden in golden Syrian hamsters. J. Infect. Dis. 193:685-92
176. Weingartl H, Czub M, Czub S, Neufeld J, Marszal P, 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. 78:12672-76