Pathology and pathogenesis of severe acute respiratory syndrome

American Journal of Pathology

Volumn 170, Issue 4, 2007, Pages 1136-1147

  Gu, Jiang ^a,b,c,d   Korteweg, Christine ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b Department of Pathology ^*  (China)

^c China Three Gorges Univisity   (China)

^d PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; CD209 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE; CORTICOSTEROID; CYTOKINE; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; HLA B ANTIGEN; HLA B*07; HLA B*4601; HLA DR ANTIGEN; HLA-B*07; HLA-B*4601; HLA-DRB1 ANTIGEN;

ADRENAL NECROSIS; ALANINE AMINOTRANSFERASE BLOOD LEVEL; AUTOIMMUNITY; AUTOPSY; CELL TYPE; CENTRAL NERVOUS SYSTEM INFECTION; CYTOPATHOGENIC EFFECT; DISEASE COURSE; DRUG MEGADOSE; ELECTRON MICROSCOPY; ERYTHROPHAGOCYTOSIS; HEREDITY; HISTOPATHOLOGY; HUMAN; IMMUNE DEFICIENCY; IMMUNOCOMPETENT CELL; IN SITU HYBRIDIZATION; INNATE IMMUNITY; KIDNEY NECROSIS; MYOPATHY; NEUROPATHY; ORGAN INJURY; PATHOGENESIS; PRIORITY JOURNAL; RESPIRATORY TRACT INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; SKELETAL MUSCLE; THYROID FOLLICLE CELL; VERNER MORRISON SYNDROME; BIOLOGICAL MODEL; GENETICS; IMMUNOLOGY; PATHOLOGY;

CHEMOKINES; CYTOKINES; HLA-B ANTIGENS; HLA-DR ANTIGENS; HUMANS; IMMUNITY, NATURAL; MODELS, BIOLOGICAL; SEVERE ACUTE RESPIRATORY SYNDROME;

EID: 34247853383     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.061088     Document Type: Review

References (94)

1. Drosten C, Gunther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA, Berger A, Burguiere AM, Cinatl J, Eickmann M, Escriou N, Grywna K, Kramme S, Manuguerra JC, Muller S, Rickerts V, Sturmer M, Vieth S, Klenk HD, Osterhaus AD, Schmitz H, Doerr HW: Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 2003, 348:1967-1976
2. Fouchier RA, Kuiken T, Schutten M, van Amerongen G, van Doornum GJ, van den Hoogen BG, Peiris M, Lim W, Stohr K, Osterhaus AD: Aetiology: Koch's postulates fulfilled for SARS virus. Nature 2003, 423:240
3. Marra MA, Jones SJ, Astell CR, Holt RA, Brooks-Wilson A, Butterfield YS, Khattra J, Asano JK, Barber SA, Chan SY, Cloutier A, Coughlin SM, Freeman D, Girn N, Griffith OL, Leach SR, Mayo M, McDonald H, Montgomery SB, Pandoh PK, Petrescu AS, Robertson AG, Schein JE, Siddiqui A, Smailus DE, Stott JM, Yang GS, Plummer F, Andonov A, Artsob H, Bastien N, Bernard K, Booth TF, Bowness D, Czub M, Drebot M, Fernando L, Flick R, Garbutt M, Gray M, Grolla A, Jones S, Feldmann H, Meyers A, Kabani A, Li Y, Normand S, Stroher U, Tipples GA, Tyler S, Vogrig R, Ward D, Watson B, Brunham RC, Krajden M, Petric M, Skowronski DM, Upton C, Roper RL: The genome sequence of the SARS-associated coronavirus. Science 2003, 300:1399-1404
4. Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, Cheung CL, Luo SW, Li PH, Zhang LJ, Guan YJ, Butt KM, Wong KL, Chan KW, Lim W, Shortridge KF, Yuen KY, Peiris JS, Poon LL: Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 2003, 302:276-278
5. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF: Bats are natural reservoirs of SARS-like coronavirus. Science 2005, 310:676-679
6. Peiris JS, Yuen KY, Osterhaus AD, Stohr K: The severe acute respiratory syndrome. N Engl J Med 2003, 349:2431-2441
7. Chan KH, Poon LL, Cheng VC, Guan Y, Hung IF, Kong J, Yam LY, Seto WH, Yuen KY, Peiris JS: Detection of SARS coronavirus in patients with suspected SARS. Emerg Infect Dis 2004, 10:294-299
8. Donnelly CA, Chani AC, Leung GM, Hedley AJ, Fraser C, Riley S, Abu-Raddad LJ, Ho LM, Thach TQ, Chau P, Chan KP, Lam TH, Tse LY, Tsang T, Liu SH, Kong JH, Lau EM, Ferguson NM, Anderson RM: Epidemiological determinants of spread of causal agent of severe acute respiratory syndrome in Hong Kong. Lancet 2003, 361:1761-1766
9. Chan HLY, Leung WK, To KF, Chan PKS, Lee N, Wu A, Tam JSL, Sung JJY: Retrospective analysis of liver function derangement in severe acute respiratory syndrome. Am J Med 2004, 116:566-567
10. He Z, Zhao C, Dong Q, Zhuang H, Song S, Peng G, Dwyer DE: Effects of severe acute respiratory syndrome (SARS) coronavirus infection on peripheral blood lymphocytes and their subsets. Int J Infect Dis 2005, 9:323-330
11. Wong RSM, Wu A, To KF, Lee N, Lam CWK, Wong CK, Chan PKS, Margaret HLN, Yu LM, Hui DS, Tam JS, Cheng G, Sung JJY: Haematological manifestations in patients with severe acute respiratory syndrome: retrospective analysis. BMJ 2003, 326:1358-1362
12. Ding YQ, Wang HJ, Shen H, Li ZG, Geng J, Han HX, Cai JJ, Li X, Kang W, Weng DS, Lu YD, Wu DH, He L, Yao KT: The clinical pathology of severe acute respiratory syndrome (SARS): a report from China. J Pathol 2003, 200:282-289
13. Lang ZW, Zhang LJ, Zhang SJ, Meng X, Li JQ, Song CZ, Sun L, Zhou YS, Dwyer DE: A clinicopathological study of three cases of severe acute respiratory syndrome (SARS). Pathology 2003, 35:526-531
14. Tse GMK, To KF, Chan PKS, Lo AWI, Ng KC, Wu A, Lee N, Wong HC, Mak SM, Chan KF, Hui DSC, Sung JJY, Ng HK: Pulmonary pathological features in coronavirus associated severe acute respiratory syndrome (SARS). J Clin Pathol 2004, 57:260-265
15. Gu J, Gong EC, Zhang B, Zheng J, Gao ZF, Zhong YF, Zou WZ, Zhan J, Wang SL, Xie ZG, Zhuang H, Wu BQ, Zhong HH, Shao HQ, Fang WG, Gao DX, Pei F, Li XW, He ZP, Xu DZ, Shi XY, Anderson VM, Leong ASY: Multiple organ infection and the pathogenesis of SARS. J Exp Med 2005, 202:415-424
16. Nicholls JM, Poon LL, Lee KC, Ng WF, Lai ST, Leung CY, Chu CM, Hui PK, Mak KL, Lim W, Yan KW, Chan KH, Tsang NC, Guan Y, Yuen KY, Peiris JS: Lung pathology of fatal severe acute respiratory syndrome. Lancet 2003, 361:1773-1778
17. Chong PY, Chui P, Ling AE, Franks TJ, Tai DY, Leo YS, Kaw GJ, Wansaicheong G, Chan KP, Ean Oon LL, Teo ES, Tan KB, Nakajima N, Sata T, Travis WD: Analysis of deaths during the severe acute respiratory syndrome (SARS) epidemic in Singapore: challenges in determining a SARS diagnosis. Arch Pathol Lab Med 2004, 128:195-204
18. Cheung OY, Chan JW, Ng CK, Koo CK: The spectrum of pathological changes in severe acute respiratory syndrome (SARS). Histopathology 2004, 45:119-124
19. Hwang DM, Chamberlain DW, Poutanen SM, Low DE, Asa SL, Butany J: Pulmonary pathology of severe acute respiratory syndrome in Toronto. Mod Pathol 2005, 18:1-10
20. Franks TJ, Chong PY, Chui P, Galvin JR, Lourens RM, Reid AH, Selbs E, McEvoy CPL, Hayden CDL, Fukuoka J, Taubenberger JK, Travis WD: Lung pathology of severe acute respiratory syndrome (SARS): a study of 8 autopsy cases from Singapore. Hum Pathol 2003, 34:743-748
21. Hsiao CH, Wu MZ, Chen CL, Hsueh PR, Hsieh SW, Yang PC, Su IJ: Evolution of pulmonary pathology in severe acute respiratory syndrome. J Formos Med Assoc 2005, 104:75-81
22. Nakajima N, Asahi-Ozaki Y, Nagata N, Yko S, Dizon F, Paladin FJ, Olveda RM, Odagiri T, Masato T, Sata T: SARS coronavirus-infected cells in lung detected by new in situ hybridization technique. Jpn J Infect Dis 2003, 56:139-141
23. He L, Ding Y, Zhang Q, Che X, He Y, Shen H, Wang H, Li Z, Zhao L, Geng J, Deng Y, Yang L, Li J, Cai J, Qiu L, Wen K, Xu X, Jiang S: Expression of elevated levels of pro-inflammatory cytokines in SARS-CoV-infected ACE2(+) cells in SARS patients: relation to the acute lung injury and pathogenesis of SARS. J Pathol 2006, 210:288-297
24. Shieh WJ, Hsiao CH, Paddock CD, Guarner J, Goldsmith CS, Tatti K, Packard M, Mueller L, Wu MZ, Rollin P, Su IJ, Zaki SR: 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 2005, 36:203-209
25. Hsueh PR, Chen PJ, Hsiao CH, Yeh SH, Cheng WC, Wang JL, Chiang BL, Chang SC, Chang FY, Wong WW, Kao CL, Yang PC: SARS Research Group of National Taiwan University College of Medicine and National Taiwan University Hospital: Patient data, early SARS epidemic, Taiwan. Emerg Infect Dis 2004, 10:489-493
26. Yen YT, Liao F, Hsiao CH, Kao CL, Chen YC, Wu-Hsieh BA: Modeling the early events of severe acute respiratory syndrome coronavirus infection in vitro. J Virol 2006, 80:2684-2693
27. Zhan J, Deng R, Tang J, Zhang B, Tang Y, Wang JK, Li F, Anderson VM, McNutt MA, Gu J: The spleen as a target in severe acute respiratory syndrome. FASEB J 2006, 20:2321-2328
28. Nicholls JM, Butany J, Poon LL, Chan KH, Beh SL, Poutanen S, Peiris JS, Wong M: Time course and cellular localization of SARS-CoV nucleoprotein and RNA in lungs from fatal cases of SARS. PLoS Med 2006, 3:0222-0229
29. Chan WS, Wu C, Chow SC, Cheung T, To KF, Leung WK, Chan PK, Lee KC, Ng HK, Au DM, Lo AW: Coronaviral hypothetical and structural proteins were found in the intestinal surface enterocytes and pneumocytes of severe acute respiratory syndrome (SARS). Mod Pathol 2005, 18:1432-1439
30. Ding YQ, He L, Zhang QL, Huang ZX, Che XY, Hou JL, Wang HJ, Shen H, Qiu LW, Li ZG, Geng J, Cai JJ, Han HX, Li X, Kang W, Weng DS, Liang P, Jiang SB: Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J Pathol 2004, 203:622-630
31. To KF, Tong JH, Chan PK, Au FW, Chim SS, Chan KC, Cheung JL, Liu EY, Tse GM, Lo AW, Lo YM, Ng HK: Tissue and cellular tropism of the coronavirus associated with severe acute respiratory syndrome: an in-situ hybridization study of fatal cases. J Pathol 2004, 202:157-163
32. Chow KC, Hsiao CH, Lin TY, Chen CL, Chiou SH: Detection of severe acute respiratory syndrome-associated coronavirus in pneumocytes of the lung. Am J Clin Pathol 2004, 121:574-580
33. Ye J, Zhang B, Xu J, Chang Q, McNutt MA, Korteweg C, Gong E, Gu J: Molecular pathology in the lungs of severe acute respiratory syndrome patients. Am J Pathol 2007, 170:538-545
34. Jiang Y, Xu J, Zhou C, Wu Z, Zhong S, Liu J, Luo W, Chen T, Qin Q, Deng P: Characterization of cytokine/chemokine profiles of severe acute respiratory syndrome. Am J Respir Crit Care Med 2005, 171:850-857
35. Tang NL, Chan PK, Wong CK, To KF, Wu AK, Sung YM, Hui DS, Sung JJ, Lam CW: Early enhanced expression of interferon-inducible protein-10 (CXCL-10) and other chemokines predicts adverse outcome in severe acute respiratory syndrome. Clin Chem 2005, 51:2333-2340
36. Goldsmith CS, Tatti KM, Ksiazek TG, Rollin PE, Comer JA, Lee WW, Rota PA, Bankamp B, Bellini WJ, Zaki SR: Ultrastructural characterization of SARS coronavirus. Emerg Infect Dis 2004, 10:320-326
37. Farcas GA, Poutanen SM, Mazzulli T, Willey BM, Butany J, Asa SL, Faure P, Akhavan P, Low DE, Kain KC: Fatal severe acute respiratory syndrome is associated with multiorgan involvement by coronavirus. J Infect Dis 2005, 191:193-197
38. Ng WF, To KF, Lam WW, Ng TK, Lee KC: The comparative pathology of severe acute respiratory syndrome and avian influenza A subtype H5N1 - a review. Hum Pathol 2006, 37:381-390
39. Shi X, Gong E, Gao D, Zhang B, Zheng J, Gao Z, Zhong Y, Zou W, Wu B, Fang W, Liao S, Wang S, Xie Z, Lu M, Hou L, Zhong H, Shao H, Li N, Liu C, Pei F, Yang J, Wang Y, Han Z, Shi X, Zhang Q, You J, Zhu X, Gu J: Severe acute respiratory syndrome associated coronavirus is detected in intestinal tissues of fatal cases. Am J Gastroenterol 2005, 100:169-176
40. Hung EC, Chim SS, Chan PK, Chan PK, Tong YK, Ng EK, Chiu RW, Leung CB, Sung JJ, Tam JS, Lo YM: Detection of SARS coronavirus RNA in the cerebrospinal fluid of a patient with severe acute respiratory syndrome. Clin Chem 2003, 49:2108-2109
41. Lau KK, Yu WC, Chu CM, Lau ST, Sheng B, Yuen KY: Possible central nervous system infection by SARS coronavirus. Emerg Infect Dis 2004, 10:342-344
42. Xu J, Zhong S, Liu J, Li L, Li Y, Wu X, Li Z, Deng P, Zhang J, Zhong N, Ding Y, Jiang Y: Detection of severe acute respiratory syndrome coronavirus in the brain: potential role of the chemokine mig in pathogenesis. Clin Infect Dis 2005, 41:1089-1096
43. Chu KH, Tsang WK, Tang CS, Lam MF, Lai FM, To KF, Fung KS, Tang HL, Yan WW, Chan HW, Lai TS, Tong KL, Lai KN: Acute renal impairment in coronavirus-associated severe acute respiratory syndrome. Kidney Int 2005, 67:698-705
44. Wu VC, Hsueh PR, Lin WC, Huang JW, Tsai HB, Chen YM, Wu KD, and the SARS Research Group of the National Taiwan: Acute renal failure in SARS patients: more than rhabdomyolysis. Nephrol Dial Transplant 2004, 19:3180-3182
45. Xu J, Qi L, Chi X, Yang J, Wei X, Gong E, Peh S, Gu J: Orchitis: a complication of severe acute respiratory syndrome (SARS). Biol Reprod 2006, 74:410-416
46. Leung WK, To KF, Chan PK, Chan HL, Wu AK, Lee N, Yuen KY, Sung JJ: Enteric involvement of severe acute respiratory syndrome-associated coronavirus infection. Gastroenterology 2003, 125:1011-1017
47. Chan HL, Kwan AC, To KF, Lai ST, Chan PK, Leung WK, Lee N, Wu A, Sung JJ: Clinical significance of hepatic derangement in severe acute respiratory syndrome. World J Gastroenterol 2005, 11:2148-2153
48. Chau TN, Lee KC, Yao H, Tsang TY, Chow TC, Yeung YC, Choi KW, Tso YK, Lau T, Lai ST, Lai CL: SARS-associated viral hepatitis caused by a novel coronavirus: report of three cases. Hepatology 2004, 39:302-310
49. Wei L, Sun S, Xu CH, Zhang J, Xu Y, Zhu H, Peh SC, Korteweg C, McNutt MA, Gu J: Pathology of the thyroid in severe acute respiratory syndrome. Hum Pathol 2007, 38:95-102
50. Leung TW, Wong KS, Hui AC, To KF, Lai ST, Ng WF, Ng HK: Myopathic changes associated with severe acute respiratory syndrome: a postmortem case series. Arch Neurol 2005, 62:1113-1117
51. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M: Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 2003, 426:450-454
52. Sims AC, Baric RS, Yount B, Burkett SE, Collins PL, Pickles RJ: 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 2005, 79:15511-15524
53. Hamming I, Timens W, Bulthuis MLC, Lely AT, Navis GJ, Goor HV: Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus - a first step in understanding SARS pathogenesis. J Pathol 2004, 203:631-637
54. Ren X, Glende J, Al-Falah M, de Vries V, Schwegmann-Wessels C, Qu X, Tan L, Tschernig T, Deng H, Naim HY, Herrler G: Analysis of ACE2 in polarized epithelial cells: surface expression and function as receptor for severe acute respiratory syndrome-associated coronavirus. J Gen Virol 2006, 87:1691-1695
55. Chan PK, To KF, Lo AW, Cheung JL, Chu I, Au FW, Tong JH, Tam JS, Sung JJ, Ng HK: Persistent infection of SARS coronavirus in colonic cells in vitro. J Med Virol 2004, 74:1-7
56. Jia HP, Look DC, Shi L, Hickey M, Pewe L, Netland J, Farzan M, Wohlford-Lenane C, Perlman S, McCray PB: ACE2 receptor expression and severe acute respiratory syndrome coronavirus infection depend on differentiation of human airway epithelia. J Virol 2005, 79:14616-14621
57. Huang IC, Bosch BJ, Li F, Li W, Lee KH, Ghiran S, Vasilieva N, Dermody TS, Harrison SC, Dormitzer PR, Farzan M, Rottier PJ, Choe H: SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J Biol Chem 2006, 281:3198-3203
58. Simmons G, Gosalia DN, Rennekamp AJ, Reeves JD, Diamond SL, Bates P: Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc Natl Acad Sci USA 2005, 102:11876-11881
59. Jeffers SA, Tusell SM, Gillim-Ross L, Hemmila EM, Achenbach JE, Babcock GJ, Thomas Jr WD, Thackray LB, Young MD, Mason RJ, Ambrosino DM, Wentworth DE, Demartini JC, Holmes KV: CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci USA 2004, 101:15748-15753
60. Marzi A, Gramberg T, Simmons G, Moller P, Rennekamp AJ, Krumbiegel M, Geier M, Eisemann J, Turza N, Saunier B, Steinkasserer A, Becker S, Bates P, Hofmann H, Pohlmann S: DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus. J Virol 2004, 78:12090-12095
61. Bashirova AA, Geijtenbeek TB, van Duijnhoven GC, van Vliet SJ, Eilering JB, Martin MP, Wu L, Martin TD, Viebig N, Knolle PA, Kewal-Ramani VN, van Kooyk Y, Carrington M: 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 2001, 193:671-678
62. Soilleux EJ, Morris LS, Leslie G, Chehimi J, Luo Q, Levroney E, Trowsdale J, Montaner LJ, Doms RW, Weissman D, Coleman N, Lee B: Constitutive and induced expression of DC-SIGN on dendritic cell and macrophage subpopulations in situ and in vitro. J Leukoc Biol 2002, 71:445-457
63. Yang ZY, Huang Y, Ganesh L, Leung K, Kong WP, Schwartz O, Subbarao K, Nabel GJ: 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 2004, 78:5642-5650
64. Imai Y, Kuba K, Rao S, Huan Y, Guo F, Guan B, Yang P, Sarao R, Wada T, Leong-Poi H, Crackower MA, Fukamizu A, Hui CC, Hein L, Uhlig S, Slutsky AS, Jiang C, Penninger JM: Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 2005, 436:112-116
65. Kuba K, Imai Y, Rao S, Gao H, Guo F, Guan B, Huan Y, Yang P, Zhang Y, Deng W, Bao L, Zhang B, Liu G, Wang Z, Chappell M, Liu Y, Zheng D, Leibbrandt A, Wada T, Slutsky AS, Liu D, Qin C, Jiang C, Penninger JM: A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat Med 2005, 11:875-879
66. Yan H, Xiao G, Zhang J, Hu Y, Yuan F, Cole DK, Zheng C, Gao GF: SARS coronavirus induces apoptosis in Vero E6 cells. J Med Virol 2004, 73:323-331
67. Tan YJ, Fielding BC, Goh PY, Shen S, Tan TH, Lim SG, Hong W: Overexpression of 7a, a protein specifically encoded by the severe acute respiratory syndrome coronavirus, induces apoptosis via a caspase-dependent pathway. J Virol 2004, 78:14043-14047
68. Law PT, Wong CH, Au TC, Chuck CP, Kong SK, Chan PK, To KF, Lo AW, Chan JY, Suen YK, Chan HY, Fung KP, Waye MM, Sung JJ, Lo YM, Tsui SK: The 3a protein of severe acute respiratory syndrome-associated coronavirus induces apoptosis in Vero E6 cells. J Gen Virol 2005, 86:1921-1930
69. Yang Y, Xiong Z, Zhang S, Yan Y, Nguyen J, Ng B, Lu H, Brendese J, Yang F, Wang H, Yang XF: Bcl-xL inhibits T-cell apoptosis induced by expression of SARS coronavirus E protein in the absence of growth factors. Biochem J 2005, 392:135-143
70. Ng LF, Hibberd ML, Ooi EE, Tang KF, Neo SY, Tan J, Murthy KR, Vega VB, Chia JM, Liu ET, Ren EC: A human in vitro model system for investigating genome-wide host responses to SARS coronavirus infection. BMC Infect Dis 2004, 4:34
71. Law HK, Cheung CY, Ng HY, Sia SF, Chan YO, Luk W, Nicholls JM, Peiris JS, Lau YL: Chemokine up-regulation in SARS-coronavirus-infected, monocyte-derived human dendritic cells. Blood 2005, 106:2366-2374
72. Cheung CY, Poon LL, Ng IH, Luk W, Sia SF, Wu MH, Chan KH, Yuen KY, Gordon S, Guan Y, Peiris JS: Cytokine responses in severe acute respiratory syndrome coronavirus-infected macrophages in vitro: possible relevance to pathogenesis. J Virol 2005, 79:7819-7826
73. Li L, Wo J, Shao J, Zhu H, Wu N, Li M, Yao H, Hu M, Dennin RH: SARS-coronavirus replicates in mononuclear cells of peripheral blood (PBMCs) from SARS patients. J Clin Virol 2003, 28:239-244
74. Schneider-Schaulies S, Niewiesk S, Schneider-Schaulies J, ter Meulen V: Measles virus induced immunosuppression: targets and effector mechanisms. Curr Mol Med 2001, 1:163-181
75. Geisbert TW, Jahrling PB: Exotic emerging viral diseases: progress and challenges. Nat Med 2004, 10(12 Suppl):110-121
76. Openshaw PJ: Potential therapeutic implications of new insights into respiratory syncytial virus disease. Respir Res 2002, 3(Suppl 1):S15-S20
77. Lee CH, Chen RF, Liu JW, Yeh WT, Chang JC, Liu PM, Eng HL, Lin MC, Yang KD: Altered p38 mitogen-activated protein kinase expression in different leukocytes with increment of immunosuppressive mediators in patients with severe acute respiratory syndrome. J Immunol 2004, 172:7841-7847
78. Huang KJ, Su IJ, Theron M, Wu YC, Lai SK, Liu CC, Lei HY: An interferon-γ-related cytokine storm in SARS patients. J Med Virol 2005, 75:185-194
79. Wong CK, Lam CW, Wu AK, Ip WK, Lee NL, Chan IH, Lit LC, Hui DS, Chan MH, Chung SS, Sung JJ: Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome. Clin Exp Immunol 2004, 136:95-103
80. Spiegel M, Pichlmair A, Martinez-Sobrido L, Cros J, Garcia-Sastre, A, Haller O, Weber F: Inhibition of beta interferon induction by severe acute respiratory syndrome coronavirus suggests a two-step model for activation of interferon regulatory factor 3. J Med Virol2005, 79:2079-2086
81. Tseng CT, Perrone LA, Zhu H, Makino S, Peters CJ: Severe acute respiratory syndrome and the innate immune responses: modulation of effector cell function without productive infection. J Immunol 2005, 174:7977-7985
82. Medzhitov R, Janeway Jr C: Innate immunity. N Engl J Med 2000, 343:338-344
83. Ip WK, Chan KH, Law HK, Tso GH, Kong EK, Wong WH, To YF, Yung RW, Chow EY, Au KL, Chan EY, Lim W, Jensenius JC, Turner MW, Peiris JS, Lau YL: Mannose-binding lectin in severe acute respiratory syndrome coronavirus infection. J Infect Dis 2005, 191:1697-1704
84. Lin YS, Lin CF, Fang YT, Kuo YM, Liao PC, Yeh TM, Hwa KY, Shieh CC, Yen JH, Wang HJ, Su IJ, Lei HY: Antibody to severe acute respiratory syndrome (SARS)-associated coronavirus spike protein domain 2 cross-reacts with lung epithelial cells and causes cytotoxicity. Clin Exp Immunol 2005, 141:500-508
85. Yang YH, Huang YH, Chuang YH, Peng CM, Wang LC, Lin YT, Chiang BL: Autoantibodies against human epithelial cells and endothelial cells after severe acute respiratory syndrome (SARS)-associated coronavirus infection. J Med Virol 2005, 77:1-7
86. Leung GM, Hedley AJ, Ho LM, Chau P, Wong IO, Thach TQ, Ghani AC, Donnelly CA, Fraser C, Riley S, Ferguson NM, Anderson RM, Tsang T, Leung PY, Wong V, Chan JC, Tsui E, Lo SV, Lam TH: The epidemiology of severe acute respiratory syndrome in the 2003 Hong Kong epidemic: an analysis of all 1755 patients. Ann Intern Med 2004, 141:662-673
87. Booth CM, Matukas LM, Tomlinson GA, Rachlis AR, Rose DB, Dwosh HA, Walmsley SL, Mazzulli T, Avendano M, Derkach P, Ephtimios IE, Kitai I, Mederski BD, Shadowitz SB, Gold WL, Hawryluck LA, Rea E, Chenkin JS, Cescon DW, Poutanen SM, Detsky AS: Clinical features and short-term outcomes of 144 patients with SARS in the greater Toronto area. JAMA 2003, 289:2801-2809
88. Zou Z, Yang Y, Chen J, Xin S, Zhang W, Zhou X, Mao Y, Hu L, Liu D, Chang B, Chang W, Liu Y, Ma X, Wang Y, Liu X: Prognostic factors for severe acute respiratory syndrome: a clinical analysis of 165 cases. Clin Infect Dis 2004, 38:483-489
89. Chan JW, Ng CK, Chan YH, Mok TY, Lee S, Chu SY, Law WL, Lee MP, Li PC: Short term outcome and risk factors for adverse clinical outcomes in adults with severe acute respiratory syndrome (SARS). Thorax 2003, 58:686-689
90. Peiris JS, Chu CM, Cheng VC, Chan KS, Hung IF, Poon LL, Law KI, Tang BS, Hon TY, Chan CS, Chan KH, Ng JS, Zheng BJ, Ng WL, Lai RW, Guan Y, Yuen KY; HKU/UCH SARS Study Group: Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 2003, 361:1767-1772
91. Lin M, Tseng HK, Trejaut JA, Lee HL, Loo JH, Chu CC, Chen PJ, Su YW, Lim KH, Tsai ZU, Lin RY, Lin RS, Huang CH: Association of HLA class I with severe acute respiratory syndrome coronavirus infection. BMC Med Genet 2003, 4:9
92. Ng MH, Lau KM, Li L, Cheng SH, Chan WY, Hui PK, Zee B, Leung CB, Sung JJ: 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 2004, 190:515-518
93. Chan VS, Chan KY, Chen Y, Poon LL, Cheung AN, Zheng B, Chan KH, Mak W, Ngan HY, Xu X, Screaton G, Tam PK, Austyn JM, Chan LC, Yip SP, Peiris M, Khoo US, Lin CL: Homozygous L-SIGN (CLEC4M) plays a protective role in SARS coronavirus infection Nat Genet 2006, 38:38-46
94. Gu J, Taylor RC: The pathogenesis of SARS Appl Immunohistochem Mol Morphol 2003, 11:281-282