Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus

Journal of Virology

Volumn 81, Issue 2, 2007, Pages 813-821

  McCray Jr , Paul B ^a,b   Pewe, Lecia ^b   Wohlford Lenane, Christine ^a   Hickey, Melissa ^a   Manzel, Lori ^a   Shi, Lei ^a   Netland, Jason ^b   Jia, Hong Peng ^a   Halabi, Carmen ^b   Sigmund, Curt D ^b   Meyerholz, David K ^a   Kirby, Patricia ^a   Look, Dwight C ^a   Perlman, Stanley ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOPATHOGENESIS; INFLAMMATORY INFILTRATE; LETHALITY; LUNG INFECTION; LUNG INFILTRATE; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; TRANSGENIC MOUSE; VIRUS PATHOGENESIS; VIRUS STRAIN;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; HUMANS; KERATIN-18; LUNG; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PEPTIDYL-DIPEPTIDASE A; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME;

ANIMALIA; CORONAVIRUS; MUS; MUS MUSCULUS; SARS CORONAVIRUS;

EID: 33846067199     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02012-06     Document Type: Article

References (43)

1. Ballester, M., A. Castello, E. Ibanez, A. Sanchez, and J. M. Folch. 2004. Real-time quantitative PCR-based system for determining transgene copy number in transgenic animals. BioTechniques 37:610-613.
2. Barnett, E., M. Cassell, and S. Perlman. 1993. Two neurotropic viruses, herpes simplex virus type I and mouse hepatitis virus, spread along different neural pathways from the main olfactory bulb. Neuroscience 57:1007-1025.
3. Cheung, C. Y., L. L. Poon, I. H. Ng, W. Luk, S. F. Sia, M. H. Wu, K. H. Chan, K. Y. Yuen, S. Gordon, Y. Guan, and J. S. Peiris. 2005. Cytokine responses in severe acute respiratory syndrome coronavirus-infected macrophages in vitro: possible relevance to pathogenesis. J. Virol. 79:7819-7826.
4. Chow, Y. H., H. O'Brodovich, J. Plumb, Y. Wen, K. J. Sohn, Z. Lu, F. Zhang, G. L. Lukacs, A. K. Tanswell, C. C. Hui, M. Buchwald, and J. Hu. 1997. Development of an epithelium-specific expression cassette with human DNA regulatory elements for transgene expression in lung airways. Proc. Natl. Acad. Sci. USA 94:14695-14700.
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. Drosten, C., S. Gunther, W. Preiser, S. van der Werf, H. R. Brodt, S. Becker, H. Rabenau, M. Panning, L. Kolesnikova, R. A. Fouchier, A. Berger, A. M. Burguiere, J. Cinatl, M. Eickmann, N. Escriou, K. Grywna, S. Kramme, J. C. Manuguerra, S. Muller, V. Rickerts, M. Sturmer, S. Vieth, H. D. Klenk, A. D. Osterhaus, H. Schmitz, and H. W. Doerr. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967-1976.
7. Franks, T. J., P. Y. Chong, P. Chui, J. B. 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. Gembardt, F., A. Sterner-Kock, H. Imboden, M. Spalteholz, F. Reibitz, H. P. Schultheiss, W. E. Siems, and T. Walther. 2005. Organ-specific distribution of ACE2 mRNA and correlating peptidase activity in rodents. Peptides 26:1270-1277.
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. Greenough, T. C., G. J. Babcock, A. Roberts, H. J. Hernandez, W. D. Thomas, Jr., J. A. Coccia, R. F. Graziano, M. Srinivasan, I. Lowy, R. W. Finberg, K. Subbarao, L. Vogel, M. Somasundaran, K. Luzuriaga, J. L. Sullivan, and D. M. Ambrosino. 2005. Development and characterization of a severe acute respiratory syndrome-associated coronavirus-neutralizing human monoclonal antibody that provides effective immunoprophylaxis in mice. J. Infect. Dis. 191:507-514.
11. 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.
12. Guan, Y., B. J. Zheng, Y. Q. He, X. L. Liu, Z. X. Zhuang, C. L. Cheung, S. W. Luo, P. H. Li, L. J. Zhang, Y. J. Guan, K. M. Butt, K. L. Wong, K. W. Chan, W. Lim, K. F. Shortridge, K. Y. Yuen, J. S. Peiris, and L. L. Poon. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:276-278.
13. 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.
14. Jia, H. P., D. C. Look, L. Shi, M. Hickey, L. Pewe, J. Netland, M. Farzan, C. Wohlford-Lenane, S. Perlman, and P. B. McCray, Jr. 2005. ACE2 receptor expression and severe acute respiratory syndrome coronavirus infection depend on differentiation of human airway epithelia. J. Virol. 79:14614-14621.
15. Jiang, Y., J. Xu, C. Zhou, Z. Wu, S. Zhong, J. Liu, W. Luo, T. Chen, Q. Qin, and P. Deng. 2005. Characterization of cytokine/chemokine profiles of severe acute respiratory syndrome. Am. J. Respir. Crit. Care Med. 171:850-857.
16. Koehler, D. R., Y. H. Chow, J. Plumb Y. Wen, B. Rafii, R. Belcastro, M. Haardt, G. L. Lukacs, M. Post, A. K. Tanswell, and J. Hu. 2000. A human epithelium-specific vector optimized in rat pneumocytes for lung gene therapy. Pediatr. Res. 48:184-190.
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. Lassnig, C., C. M. Sanchez, M. Egerbacher, I. Walter, S. Majer, T. Kolbe, P. Pallares, L. Enjuanes, and M. Muller. 2005. Development of a transgenic mouse model susceptible to human coronavirus 229E. Proc. Natl. Acad. Sci. USA 102:8275-8280.
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. Law, H. K., C. Y. Cheung, H. Y. Ng, S. F. Sia, Y. O. Chan, W. Luk, J. M. Nicholls, J. S. Peiris, and Y. L. Lau. 2005. Chemokine upregulation in SARS coronavirus infected human monocyte derived dendritic cells. Blood 106: 2366-2376.
21. Lee, D. T., Y. K. Wing, H. C. Leung, J. J. Sung, Y. K. Ng, G. C. Yiu, R. Y. Chen, and H. F. Chiu. 2004. Factors associated with psychosis among patients with severe acute respiratory syndrome: a case-control study. Clin. Infect. Dis. 39:1247-1249.
22. Li, W., T. C. Greenough, M. J. Moore, N. Vasilieva, M. Somasundaran, J. L. Sullivan, M. Farzan, and H. Choe. 2004. Efficient replication of severe acute respiratory syndrome coronavirus in mouse cells is limited by murine angiotensin-converting enzyme 2. J. Virol. 78:11429-11433.
23. 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.
24. 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.
25. McAuliffe, J., L. Vogel, A. Roberts, G. Fahle, S. Fischer, W. J. Shieh, E. Butler, S. Zaki, M. St Claire, B. Murphy, and K. Subbarao. 2004. Replication of SARS coronavirus administered into the respiratory tract of African green, rhesus and cynomolgus monkeys. Virology 330:8-15.
26. Nicholls, J. M., J. Butany, L. L. Poon, K. H. Chan, S. L. Beh, S. Poutanen, J. S. Peiris, and M. Wong. 2006. Time course and cellular localization of SARS-CoV nucleoprotein and RNA in lungs from fatal cases of SARS. PLoS Med. 3:e27.
27. 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.
28. Peiris, J. S., Y. Guan, and K. Y. Yuen. 2004. Severe acute respiratory syndrome. Nat. Med. 10:S88-S97.
29. Peiris, J. S., S. T. Lai, L. L. Poon, Y. Guan, L. Y. Yam, W. Lim, J. Nicholls, W. K. Yee, W. W. Yan, M. T. Cheung, V. C. Cheng, K. H. Chan, D. N. Tsang, R. W. Yung, T. K. Ng, and K. Y. Yuen. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-1325.
30. Pewe, L., H. Zhou, J. Netland, C. Tangadu, H. Olivares, L. Shi, D. Look, T. M. Gallagher, and S. Perlman. 2005. A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. J. Virol. 79:11335-11342.
31. Roberts, A., W. D. Thomas, J. Guarner, E. W. Lamirande, G. J. Babcock, T. C. Greenough, L. Vogel, N. Hayes, J. L. Sullivan, S. Zaki, K. Subbarao, and D. M. Ambrosino. 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. 193:685-692.
32. Rota, P. A., M. S. Oberste, S. S. Monroe, W. A. Nix, R. Campagnoli, J. P. Icenogle, S. Penaranda, B. Bankamp, K. Maher, M. H. Chen, S. Tong, A. Tamin, L. Lowe, M. Frace, J. L. DeRisi, Q. Chen, D. Wang, D. D. Erdman, T. C. Peret, C. Burns, T. G. Ksiazek, P. E. Rollin, A. Sanchez, S. Liffick, B. Holloway, J. Limor, K. McCaustland, M. Olsen-Rasmussen, R. Fouchier, S. Gunther, A. D. Osterhaus, C. Drosten, M. A. Pallansch, L. J. Anderson, and W. J. Bellini. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399.
33. Shinya, K., A. Suto, M. Kawakami, H. Sakamoto, T. Umemura, Y. Kawaoka, N. Kasai, and T. Ito. 2005. Neurovirulence of H7N7 influenza A virus: brain stem encephalitis accompanied with aspiration pneumonia in mice. Arch. Virol. 150:1653-1660.
34. Sims, A. C., R. S. Baric, B. Yount, S. E. Burkett, P. L. Collins, and R. J. Pickles. 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. 79:15511-15524.
35. Spiegel, M., A. Pichlmair, L. Martinez-Sobrido, J. Cros, A. Garcia-Sastre, O. Haller, and F. Weber. 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. 79:2079-2086.
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. Tsang, K. W., P. L. Ho, G. C. Ooi, W. K. Yee, T. Wang, M. Chan-Yeung, W. K. Lam, W. H. Seto, L. Y. Yam, T. M. Cheung, P. C. Wong, B. Lam, M. S. Ip, J. Chan, K. Y. Yuen, and K. N. Lai. 2003. A cluster of cases of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 348:1977-1985.
40. Wang, W. K., S. Y. Chen, I. J. Liu, C. L. Kao, H. L. Chen, B. L. Chiang, J. T. Wang, W. H. Sheng, P. R. Hsueh, C. F. Yang, P. C. Yang, and S. C. Chang. 2004. Temporal relationship of viral load, libavirin, interleukin (IL)-6, IL-8, and clinical progression in patients with severe acute respiratory syndrome. Clin. Infect. Dis. 39:1071-1075.
41. 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.
42. 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.
43. Zhang, Y., J. Li, Y. Zhan, L. Wu, X. Yu, W. Zhang, L. Ye, S. Xu, R. Sun, Y. Wang, and J. Lou. 2004. Analysis of serum cytokines in patients with severe acute respiratory syndrome. Infect. Immun. 72:4410-4415.