Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human angiotensin-converting enzyme 2 virus receptor

Journal of Virology

Volumn 81, Issue 3, 2007, Pages 1162-1173

  Tseng, Chien Te K ^a,b   Huang, Cheng ^a   Newman, Patrick ^a   Wang, Nan ^a   Narayanan, Krishna ^a   Watts, Douglas M ^a,b   Makino, Shinji ^a,b   Packard, Michelle M ^c   Zaki, Sherif R ^c   Chan, Teh Sheng ^a   Peters, Clarence J ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE 2; SEVERE ACUTE RESPIRATORY SYNDROME VACCINE; UNCLASSIFIED DRUG; VIRUS RECEPTOR;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; MORTALITY; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; TRANSGENE; TRANSGENIC MOUSE; VIRUS LOAD; VIRUS PATHOGENESIS; VIRUS PNEUMONIA; VIRUS REPLICATION; WEIGHT REDUCTION;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; LUNG; MICE; MICE, TRANSGENIC; PEPTIDYL-DIPEPTIDASE A; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS REPLICATION;

ANIMALIA; MUS; MUS MUSCULUS; SARS CORONAVIRUS;

EID: 33846536739     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01702-06     Document Type: Article

References (49)

1. Arbour, N., G. Côté, C. Lachance, M. Tardieu, N. R. Cashman, and P. J. Talbot. 1999. Acute and persistent infection of human neural cell lines by human coronavirus OC43. J. Virol. 73:3338-3350.
2. Butler, N., L. Pewe, K. Trandem, and S. Perlman. 2006. Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated. Virology 347:410-421.
3. Chan, K. S., J. P. Zheng, Y. W. Mok, Y. M. Li, Y. N. Liu, C. M. Chu, and M. S. Ip. 2003. SARS: prognosis, outcome and sequelae. Respirology 8:(Suppl.) S36-S40.
4. Coley, S. E., E. Lavi, S. G. Sawicki, L. Fu, B. Schelle, N. Karl, S. G. Siddell, and V. Thiel. 2005. Recombinant mouse hepatitis virus strain A59 from cloned, full-length cDNA replicates to high titers in vitro and is fully pathogenic in vivo. J. Virol. 79:3097-3106.
5. Ding, Y., L. He, Q. Zhang, Z. Huang, X. Che, J. Hou, H. Wang, H. Shen, L. Qiu, Z. Li, J. Geng, J. Cai, H. Han, X. Li, W. Kang, D. Weng, P. Liang, and S. Jiang. 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. 203:622-630.
6. Ding, Y., H. Wang, H. Shen, Z. Li, J. Geng, H. Han, J. Cai, X. Li, W. Kang, D. Weng, Y. Lu, D. Wu, L. He, and K. Yao. 2003. The clinical pathology of severe acute respiratory syndrome (SARS): a report from China. J. Pathol. 200:282-289.
7. Franks, T. J., P. Y. Chong, P. Chui, J. R. Galvin, R. M. Lourens, A. H. Reid, E. Selbs, C. P. McEvoy, C. D. Hayden, J. Fukuoka, J. K. Taubenberger, and W. D. Travis. 2003. Lung pathology of severe acute respiratory syndrome (SARS): a study of 8 autopsy cases from Singapore. Hum. Pathol. 34:743-748.
8. Gerdts, V., J. Beyer, B. Lomniczi, and T. C. Mettenleiter. 2000. Pseudorabies virus expressing bovine herpesvirus 1 glycoprotein B exhibits altered neurotropism and increased neurovirulence. J. Virol. 74:817-827.
9. Glass, W. G., K. Subbarao, B. Murphy, and P. M. Murphy. 2004. Mechanisms of host defense following severe acute respiratory syndrome-coronavirus (SARS-CoV) pulmonary infection of mice. J. Immunol. 173:4030-4039.
10. Gu, J., E. Gong, B. Zhang, J. Zheng, Z. Gao, Y. Zhong, W. Zou, J. Zhan, S. Wang, Z. Xie, H. Zhuang, B. Wu, H. Zhong, H. Shao, W. Fang, D. Gao, F. Pei, X. Li, Z. He, D. Xu, X. Shi, V. M. Anderson, and A. S. Leong. 2005. Multiple organ infection and the pathogenesis of SARS. J. Exp. Med. 202:415-424.
11. Hamming, I., W. Timens, M. L. Bulthuis, A. T. Lely, G. J. Navis, and H. van Goor. 2004. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 203:631-637.
12. Hogan, R. J., G. Gao, T. Rowe, P. Bell, D. Flieder, J. Paragas, G. P. Kobinger, N. A. Wivel, R. G. Crystal, J. Boyer, H. Feldmann, T. G. Voss, and J. M. Wilson. 2004. Resolution of primary severe acute respiratory syndrome-associated coronavirus infection requires Stat1. J. Virol. 78:11416-11421.
13. Huang, K. J., I. J. Su, M. Theron, Y. C. Wu, S. K. Lai, C. C. Liu, and H. Y. Lei. 2005. An interferon-gamma-related cytokine storm in SARS patients. J. Med. Virol. 75:185-194.
14. Iwasaki, T., S. Itamura, H. Nishimura, Y. Sato, M. Tashiro, T. Hashikawa, and T. Kurata. 2004. Productive infection in the murine central nervous system with avian influenza virus A (H5N1) after intranasal inoculation. Acta Neuropathol. (Berlin) 108:485-492.
15. Jacomy, H., G. Fragoso, G. Almazan, W. E. Mushynski, and P. J. Talbot. 2006. Human coronavirus OC43 infection induces chronic encephalitis leading to disabilities in BALB/c mice. Virology 349:335-346.
16. Jeffers, S. A., S. M. Tusell, L. Gillim-Ross, E. M. Hemmila, J. E. Achenbach, G. J. Babcock, W. D. Thomas, Jr., L. B. Thackray, M. D. Young, R. J. Mason, D. M. Ambrosino, D. E. Wentworth, J. C. Demartini, and K. V. Holmes. 2004. CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 101:15748-15753.
17. Ksiazek, T. G., D. Erdman, C. S. Goldsmith, S. R. Zaki, T. Peret, S. Emery, S. Tong, C. Urbani, J. A. Comer, W. Lim, P. E. Rollin, S. F. Dowell, A. E. Ling, C. D. Humphrey, W. J. Shieh, J. Guarner, C. D. Paddock, P. Rota, B. Fields, J. DeRisi, J. Y. Yang, N. Cox, J. M. Hughes, J. W. LeDuc, W. J. Bellini, and L. J. Anderson. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953-1966.
18. Kuiken, T., R. A. Fouchier, M. Schutten, G. F. Rimmelzwaan, G. van Amerongen, D. van Riel, J. D. Laman, T. de Jong, G. van Doornum, W. Lim, A. E. Ling, P. K. Chan, J. S. Tam, M. C. Zambon, R. Gopal, C. Drosten, S. van der Werf, N. Escriou, J. C. Manuguerra, K. Stohr, J. S. Peiris, and A. D. Osterhaus. 2003. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263-270.
19. Lau, S. K., P. C. Woo, K. S. Li, Y. Huang, H. W. Tsoi, B. H. Wong, S. S. Wong, S. Y. Leung, K. H. Chan, and K. Y. Yuen. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. USA 102:14040-14045.
20. Li, W., M. J. Moore, N. Vasilieva, J. Sui, S. K. Wong, M. A. Berne, M. Somasundaran, J. L. Sullivan, K. Luzuriaga, T. C. Greenough, H. Choe, and M. Farzan. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454.
21. Li, W., Z. Shi, M. Yu, W. Ren, C. Smith, J. H. Epstein, H. Wang, G. Crameri, Z. Hu, H. Zhang, J. Zhang, J. McEachern, H. Field, P. Daszak, B. T. Eaton, S. Zhang, and L. F. Wang. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676-679.
22. Li, W., S.-K. Wong, F. Li, J. H. Kuhn, I.-C. Huang, H. Choe, and M. Farzan. 2006. Animal origins of the severe acute respiratory syndrome coronavirus: insight from ACE2-S-protein interactions. J. Virol. 80:4211-4219.
23. Martina, B. E., B. L. Haagmans, T. Kuiken, R. A. Fouchier, G. F. Rimmelzwaan, G. van Amerongen, J. S. Peiris, W. Lim, and A. D. Osterhaus. 2003. Virology: SARS virus infection of cats and ferrets. Nature 425:915.
24. Mossel, E. C., C. Huang, K. Narayanan, S. Makino, R. B. Tesh, and C. J. Peters. 2005. Exogenous ACE2 expression allows refractory cell lines to support severe acute respiratory syndrome coronavirus replication. J. Virol. 79:3846-3850.
25. Mulder, W., J. Pol, T. Kimman, G. Kok, J. Priem, and B. Peeters. 1996. Glycoprotein D-negative pseudorabies virus can spread transneuronally via direct neuron-to-neuron transmission in its natural host, the pig, but not after additional inactivation of gE or gI. J. Virol. 70:2191-2200.
26. Nicholls, J. M., L. L. Poon, K. C. Lee, W. F. Ng, S. T. Lai, C. Y. Leung, C. M. Chu, P. K. Hui, K. L. Mak, W. Lim, K. W. Yan, K. H. Chan, N. C. Tsang, Y. Guan, K. Y. Yuen, and J. S. Peiris. 2003. Lung pathology of fatal severe acute respiratory syndrome. Lancet 361:1773-1778.
27. Nie, Y., P. Wang, X. Shi, G. Wang, J. Chen, A. Zheng, W. Wang, Z. Wang, X. Qu, M. Luo, L. Tan, X. Song, X. Yin, J. Chen, M. Ding, and H. Deng. 2004. Highly infectious SARS-CoV pseudotyped virus reveals the cell tropism and its correlation with receptor expression. Biochem. Biophys. Res. Commun. 321:994-1000.
28. Peiris, J. S., K. Y. Yuen, A. D. Osterhaus, and K. Stohr. 2003. The severe acute respiratory syndrome. N. Engl. J. Med. 349:2431-2441.
29. Peterson, K. E., and B. Chesebro. 2006. Influence of proinflammatory cytokines and chemokines on the neuropathogenesis of oncornavirus and immunosuppressive lentivirus infections. Curr. Top. Microbiol. Immunol. 303:67-95.
30. Rempel, J. D., L. A. Quina, P. K. Blakely-Gonzales, M. J. Buchmeier, and D. L. Gruol. 2005. Viral induction of central nervous system innate immune responses. J. Virol. 79:4369-4381.
31. Roberts, A., C. Paddock, L. Vogel, E. Butler, S. Zaki, and K. Subbarao. 2005. Aged BALB/c mice as a model for increased severity of severe acute respiratory syndrome in elderly humans. J. Virol. 79:5833-5838.
32. Roberts, A., L. Vogel, J. Guarner, N. Hayes, B. Murphy, S. Zaki, and K. Subbarao. 2005. Severe acute respiratory syndrome coronavirus infection of golden Syrian hamsters. J. Virol. 79:503-511.
33. Ryzhikov, A. B., E. I. Ryabchikova, A. N. Sergeev, and N. V. Tkacheva. 1995. Spread of Venezuelan equine encephalitis virus in mice olfactory tract. Arch. Virol. 140:2243-2254.
34. Sbieh, W. J., C. H. Hsiao, C. D. Paddock, J. Guarner, C. S. Goldsmith, K. Tatti, M. Packard, L. Mueller, M. Z. Wu, P. Rollin, I. J. Su, and S. R. Zaki. 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. 36:303-309.
35. Song, H. D., C. C. Tu, G. W. Zhang, S. Y. Wang, K. Zheng, L. C. Lei, Q. X. Chen, Y. W. Gao, H. Q. Zhou, H. Xiang, H. J. Zheng, S. W. Chern, F. Cheng, C. M. Pan, H. Xuan, S. J. Chen, H. M. Luc, D. H. Zhou, Y. F. Liu, J. F. He, P. Z. Qin, L. H. Li, Y. Q. Ren, W. J. Liang, Y. D. Yu, L. Anderson, M. Wang, R. H. Xu, X. W. Wu, H. Y. Zheng, J. D. Chen, G. Liang, Y. Gao, M. Liao, L. Fang, L. Y. Jiang, H. Li, F. Chen, B. Di, L. J. He, J. Y. Lin, S. Tong, X. Kong, L. Du, P. Hao, H. Tang, A. Bernini, X. J. Yu, O. Spiga, Z. M. Guo, H. Y. Pan, W. Z. He, J. C. Manuguerra, A. Fontanet, A. Danchin, N. Niccolai, Y. X. Li, C. I. Wu, and G. P. Zhao. 2005. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. USA 102:2430-2435.
36. Subbarao, K., J. McAuliffe, L. Vogel, G. Fahle, S. Fischer, K. Tatti, M. Packard, W.-J. Shieh, S. Zaki, and B. Murphy. 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. Subbarao, K., and A. Roberts. 2006. Is there an ideal animal model for SARS? Trends Microbiol. 14:299-303.
38. Tang, N. L., P. K. Chan, C. K. Wong, K. F. To, A. K. Wu, Y. M. Sung, D. S. Hui, J. J. Sung, and C. W. Lam. 2005. Early enhanced expression of interferon-inducible protein-10 (CXCL-10) and other chemokines predicts adverse outcome in severe acute respiratory syndrome. Clin. Chem. 51:2333-2340.
39. To, K. F., J. H. Tong, P. K. Chan, F. W. Au, S. S. Chim, K. C. Chan, J. L. Cheung, E. Y. Liu, G. M. Tse, A. W. Lo, Y. M. Lo, and H. K. Ng. 2004. Tissue and cellular tropism of the coronavirus associated with severe acute respiratory syndrome: an in-situ hybridization study of fatal cases. J. Pathol. 202:157-163.
40. Tseng, C. T., L. A. Perrone, H. Zhu, S. Makino, and C. J. Peters. 2005. Severe acute respiratory syndrome and the innate immune responses: modulation of effector cell function without productive infection. J. Immunol. 174:7977-7985.
41. Tseng, C.-T. K., J. Tseng, L. Perrone, M. Worthy, V. Popov, and C. J. Peters. 2005. Apical entry and release of severe acute respiratory syndrome-associated coronavirus in polarized Calu-3 lung epithelial cells. J. Virol. 79:9470-9479.
42. Tsui, S. K., S. S. Chim, and Y. M. Lo. 2003. Coronavirus genomic-sequence variations and the epidemiology of the severe acute respiratory syndrome. N. Engl. J. Med. 349:187-188.
43. Wang, T., J. A. Rumbaugh, and A. Nath. 2006. Viruses and the brain: from inflammation to dementia. Clin. Sci. (London) 110:393-407.
44. Ward, S. E., M. R. Loutfy, L. M. Blatt, K. A. Siminovitch, J. Chen, A. Hinek, B. Wolff, D. H. Pham, H. Deif, E. A. LaMere, K. C. Kain, G. A. Farcas, P. Ferguson, M. Latchford, G. Levy, L. Fung, J. W. Dennis, E. K. Lal, and E. N. Fish. 2005. Dynamic changes in clinical features and cytokine/chemokine responses in SARS patients treated with interferon alfacon-1 plus corticosteroids. Antivir. Ther. 10:263-275.
45. Whitton, J. L., C. T. Cornell, and R. Feuer. 2005. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 3:765-776.
46. Wong, C. K., C. W. Lam, A. K. Wu, W. K. Ip, N. L. Lee, I. H. Chan, L. C. Lit, D. S. Hui, M. H. Chan, S. S. Chung, and J. J. Sung. 2004. Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome. Clin. Exp. Immunol. 136:95-103.
47. Xu, J., S. Zhong, J. Liu, L. Li, Y. Li, X. Wu, Z. Li, P. Deng, J. Zhang, N. Zhong, Y. Ding, and Y. Jiang. 2005. Detection of severe acute respiratory syndrome coronavirus in the brain: potential role of the chemokine Mig in pathogenesis. Clin. Infect. Dis. 41:1089-1096.
48. Yamashita, M., M. Yamate, G. M. Li, and K. Ikuta. 2005. Susceptibility of human and rat neural cell lines to infection by SARS-coronavirus. Biochem. Biophys. Res. Commun. 334:79-85.
49. Yang, Z.-Y., Y. Huang, L. Ganesh, K. Leung, W.-P. Kong, O. Schwartz, K. Subbarao, and G. J. Nabel. 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. 78:5642-5650.