Mechanisms of zoonotic severe acute respiratory syndrome coronavirus host range expansion in human airway epithelium

Journal of Virology

Volumn 82, Issue 5, 2008, Pages 2274-2285

  Sheahan, Timothy ^a   Rockx, Barry ^b   Donaldson, Eric ^a   Sims, Amy ^b   Pickles, Raymond ^a   Corti, Davide ^c   Baric, Ralph ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b IL   (United States)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; MONOCLONAL ANTIBODY; VIRUS PROTEIN; VIRUS RECEPTOR; VITRONECTIN;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGY; CELL GROWTH; CONTROLLED STUDY; EPITHELIUM CELL; EVOLUTION; FEMALE; GENE MUTATION; HOST RANGE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGENY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ENGINEERING; RESPIRATORY EPITHELIUM; SARS CORONAVIRUS; TREATMENT OUTCOME; VERO CELL; VIRUS REPLICATION; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; DNA PRIMERS; EPITHELIAL CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SARS VIRUS; TRACHEA; VERO CELLS; VIRAL ENVELOPE PROTEINS; ZOONOSES;

ANIMALIA; SARS CORONAVIRUS;

EID: 39749177748     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02041-07     Document Type: Article

References (59)

1. Cello, J., A. V. Paul, and E. Wimmer. 2002. Chemical synthesis of poliovirus cDNA: generation of infectious virus in the absence of natural template. Science 297:1016-1018.
2. Chinese SARS Molecular Epidemiology Consortium. 2004. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303:1666-1669.
3. Christian, M. D., S. M. Poutanen, M. R. Loutfy, M. P. Muller, and D. E. Low. 2004. Severe acute respiratory syndrome. Clin. Infect. Dis. 38:1420-1427.
4. de Haan, C. A. M., Z. Li, E. te Lintelo, B. J. Bosch, B. J. Haijema, and P. J. M. Rottier. 2005. Murine coronavirus with an extended host range uses heparan sulfate as an entry receptor. J. Virol. 79:14451-14456.
5. Deming, D., T. Sheahan, M. Heise, B. Yount, N. Davis, A. Sims, M. Suthar, J. Harkema, A. Whitmore, R. Pickles, A. West, E. Donaldson, K. Curtis, R. Johnston, and R. Baric. 2006. Vaccine efficacy in senescent mice challenged with recombinant SARS-CoV bearing epidemic and zoonotic spike variants. PLoS Med. 3:e525.
6. Domingo, E., and J. J. Holland. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151-178.
7. 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.
8. Fulcher, M. L., S. Gabriel, K. A. Burns, J. R. Yankaskas, and S. H. Randell. 2005. Well-differentiated human airway epithelial cell cultures. Methods Mol. Med. 107:183-206.
9. 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.
10. Haagmans, B. L., T. Kuiken, B. E. Martina, R. A. Fouchier, G. F. Rimmelzwaan, G. van Amerongen, D. van Riel, T. de Jong, S. Itamura, K. H. Chan, M. Tashiro, and A. D. Osterhaus. 2004. Pegylated interferon-alpha protects type 1 pneumocytes against SARS coronavirus infection in macaques. Nat. Med. 10:290-293.
11. Haagmans, B. L., and A. D. Osterhaus. 2006. Nonhuman primate models for SARS. PLoS Med. 3:e194.
12. 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.
13. Hsu, V. P., M. J. Hossain, U. D. Parashar, M. M. Ali, T. G. Ksiazek, I. Kuzmin, M. Niezgoda, C. Rupprecht, J. Bresee, and R. F. Breiman. 2004. Nipah virus encephalitis reemergence, Bangladesh. Emerg. Infect. Dis. 10:2082-2087.
14. Hueffer, K., J. S. L. Parker, W. S. Weichert, R. E. Geisel, J.-Y. Sgro, and C. R. Parrish. 2003. The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J. Virol. 77:1718-1726.
15. 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.
16. Kan, B., M. Wang, H. Jing, H. Xu, X. Jiang, M. Yan, W. Liang, H. Zheng, K. Wan, Q. Liu, B. Cui, Y. Xu, E. Zhang, H. Wang, J. Ye, G. Li, M. Li, Z. Cui, X. Qi, K. Chen, L. Du, K. Gao, Y.-T. Zhao, X.-Z. Zou, Y.-J. Feng, Y.-F. Gao, R. Hai, D. Yu, Y. Guan, and J. Xu. 2005. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. J. Virol. 79:11892-11900.
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. 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.
19. Lau, Y. L., and J. S. Peiris. 2005. Pathogenesis of severe acute respiratory syndrome. Curr. Opin. Immunol. 17:404-410.
20. Leroy, E. M., B. Kumulungui, X. Pourrut, P. Rouquet, A. Hassanin, P. Yaba, A. Delicat, J. T. Paweska, J. P. Gonzalez, and R. Swanepoel. 2005. Fruit bats as reservoirs of Ebola virus. Nature 438:575-576.
21. Li, F., W. Li, M. Farzan, and S. C. Harrison. 2005. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309:1864-1868.
22. 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.
23. 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.
24. Li, W., C. Zhang, J. Sui, J. H. Kuhn, M. J. Moore, S. Luo, S. K. Wong, I. C. Huang, K. Xu, N. Vasilieva, A. Murakami, Y. He, W. A. Marasco, Y. Guan, H. Choe, and M. Farzan. 2005. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 24:1634-1643.
25. Ligon, B. L. 2006. Reemergence of an unusual disease: the chikungunya epidemic. Semin. Pediatr. Infect. Dis. 17:99-104.
26. Marra, M. A., S. J. Jones, C. R. Astell, R. A. Holt, A. Brooks-Wilson, Y. S. Butterfield, J. Khattra, J. K. Asano, S. A. Barber, S. Y. Chan, A. Cloutier, S. M. Coughlin, D. Freeman, N. Girn, O. L. Griffith, S. R. Leach, M. Mayo, H. McDonald, S. B. Montgomery, P. K. Pandoh, A. S. Petrescu, A. G. Robertson, J. E. Schein, A. Siddiqui, D. E. Smailus, J. M. Stott, G. S. Yang, F. Plummer, A. Andonov, H. Artsob, N. Bastien, K. Bernard, T. F. Booth, D. Bowness, M. Czub, M. Drebot, L. Fernando, R. Flick, M. Garbutt, M. Gray, A. Grolla, S. Jones, H. Feldmann, A. Meyers, A. Kabani, Y. Li, S. Normand, U. Stroher, G. A. Tipples, S. Tyler, R. Vogrig, D. Ward, B. Watson, R. C. Brunham, M. Krajden, M. Petric, D. M. Skowronski, C. Upton, and R. L. Roper. 2003. The Genome sequence of the SARS-associated coronavirus. Science 300:1399-1404.
27. McRoy, W. C., and R. S. Baric. 2008. Amino acid substitutions in the S2 subunit of mouse hepatitis virus variant V51 encode determinants of host range expansion. J. Virol. 82:1414-1424.
28. Morens, D. M., G. K. Folkers, and A. S. Fauci. 2004. The challenge of emerging and re-emerging infectious diseases. Nature 430:242-249.
29. Nguyen, D. C., T. M. Uyeki, S. Jadhao, T. Maines, M. Shaw, Y. Matsuoka, C. Smith, T. Rowe, X. Lu, H. Hall, X. Xu, A. Balish, A. Klimov, T. M. Tumpey, D. E. Swayne, L. P. T. Huynh, H. K. Nghiem, H. H. T. Nguyen, L. T. Hoang, N. J. Cox, and J. M. Katz. 2005. Isolation and characterization of avian influenza viruses, including highly pathogenic H5N1, from poultry in live bird markets in Hanoi, Vietnam, in 2001. J. Virol. 79:4201-4212.
30. 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.
31. Page, R. D. 1996. Tree View: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
32. Parrish, C. R., and Y. Kawaoka. 2005. The origins of new pandemic viruses: the acquisition of new host ranges by anine parvovirus and influenza A viruses. Annu. Rev. Microbiol. 59:553-586.
33. Pickles, R. J., D. McCarty, H. Matsui, P. J. Hart, S. H. Randell, and R. C. Boucher. 1998. Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer. J. Virol. 72:6014-6023.
34. Poon, L. L. M., D. K. W. Chu, K. H. Chan, O. K. Wong, T. M. Ellis, Y. H. C. Leung, S. K. P. Lau, P. C. Y. Woo, K. Y. Suen, K. Y. Yuen, Y. Guan, and J. S. M. Peiris. 2005. Identification of a novel coronavirus in bats. J. Virol. 79:2001-2009.
35. Pyrc, K., B. Berkhout, and L. van der Hoek. 2007. The novel human coronaviruses NL63 and HKUl1 J. Virol. 81:3051-3057.
36. Pyrc, K., R. Dijkman, L. Deng, M. F. Jebbink, H. A. Ross, B. Berkhout, and L. van der Hoek. 2006. Mosaic structure of human coronavirus NL63, one thousand years of evolution. J. Mol. Biol. 364:964-973.
37. Ramu, C. 2003. SIRW: a web server for the Simple Indexing and Retrieval System that combines sequence motif searches with keyword searches. Nucleic Acids Res. 31:3771-3774.
38. 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.
39. Roberts, A., and K. Subbarao. 2006. Animal models for SARS. Adv. Exp. Med. Biol. 581:463-471.
40. Rockx, B., T. Sheahan, E. Donaldson, J. Harkema, A. Sims, M. Heise, R. Pickles, M. Cameron, D. Kelvin, and R. Baric. 2007. Synthetic reconstruction of zoonotic and early human severe acute respiratory syndrome coronavirus isolates that produce fatal disease in aged mice. J. Virol. 81:7410-7423.
41. 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.
42. Simmons, G., D. N. Gosalia, A. J. Rennekamp, J. D. Reeves, S. L. Diamond, and P. Bates. 2005. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad. Sci. USA 102:11876-11881.
43. 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.
44. Smith, H. O., C. A. Hutchison III, C. Pfannkoch, and J. C. Venter. 2003. Generating a synthetic genome by whole genome assembly: phiX174 bacteriophage from synthetic oligonucleotides. Proc. Natl. Acad. Sci. USA 100:15440-15445.
45. 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. Luo, 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. Nati. Acad, Sci. USA 102:2430-2435.
46. Stevens, J., O. Blixt, T. M. Tumpey, J. K. Taubenberger, J. C. Paulson, and I. A. Wilson. 2006. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312:404-410.
47. Towner, J. S., X. Pourrut, C. G. Albarino, C. N. Nkogue, B. H. Bird, G. Grard, T. G. Ksiazek, J. P. Gonzalez, S. T. Nichol, and E. M. Leroy. 2007. Marburg virus infection detected in a common African bat. PLoS ONE 2:e764.
48. Traggiai, E., S. Becker, K. Subbarao, L. Kolesnikova, Y. Uematsu, M. R. Gismondo, B. R. Murphy, R. Rappuoli, and A. Lanzavecchia. 2004. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat. Med. 10:871-875.
49. Tumpey, T. M., C. F. Basler, P. V. Aguilar, H. Zeng, A. Solorzano, D. E. Swayne, N. J. Cox, J. M. Katz, J. K. Taubenberger, P. Palese, and A. Garcia-Sastre. 2005. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77-80.
50. van der Hoek, L., K. Pyrc, M. F. Jebbink, W. Vermeulen-Oost, R. J. Berkhout, K. C. Wolthers, P. M. Wertheim-van Dillen, J. Kaandorp, J. Spaargaren, and B. Berkhout. 2004. Identification of a new human coronavirus. Nat. Med. 10:368-373.
51. Walsh, P. D., R. Biek, and L. A. Real. 2005. Wave-like spread of Ebola Zaire. PLoS Biol. 3:e371.
52. Woo, P. C. Y., S. K. P. Lau, C.-M. Chu, K.-H. Chan, H.-W. Tsoi, Y. Huang, B. H. L. Wong, R. W. S. Poon, J. J. Cai, W.-K. Luk, L. L. M. Poon, S. S. Y. Wong, Y. Guan, J. S. M. Peiris, and K.-Y. Yuen. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79:884-895.
53. Woo, P. C. Y., S. K. P. Lau, C. C. Y. Yip, Y. Huang, H.-W. Tsoi, K.-H. Chan, and K.-Y. Yuen. 2006. Comparative analysis of 22 coronavirus HKU1 genomes reveals a novel genotype and evidence of natural recombination in coronavirus HKU1. J. Virol. 80:7136-7145.
54. Yano, Y., M. Kaneniwa, M. Satomi, H. Oikawa, and S. S. Chen. 2006. Occurrence and density of Vibrio parahaemolyticus in live edible crustaceans from markets in China. J. Food Prot. 69:2742-2746.
55. Yano, Y., M. Yokoyama, M. Satomi, H. Oikawa, and S. S. Chen. 2004. Occurrence of Vibrio vulnificus in fish and shellfish available from markets in China. J. Food Prot. 67:1617-1623.
56. Yount, B., K. M. Curtis, E. A. Fritz, L. E. Hensley, P. B. Jahrling, E. Prentice, M. R. Denison, T. W. Geisbert, and R. S. Baric. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 100:12995-13000.
57. Yount, B., R. S. Roberts, L. Lindesmith, and R. S. Baric. 2006. Rewiring the severe acute respiratory syndrome coronavirus (SARS-CoV) transcription circuit: engineering a recombination-resistant genome. Proc. Natl. Acad. Sci. USA 103:12546-12551.
58. Yount, B., R. S. Roberts, A. C. Sims, D. Deming, M. B. Frieman, J. Sparks, M. R. Denison, N. Davis, and R. S. Baric. 2005. Severe acute respiratory syndrome coronavirus group-specific open reading frames encode nonessential functions for replication in cell cultures and mice. J. Virol. 79:14909-14922.
59. Zhu, Z., S. Chakraborti, Y. He, A. Roberts, T. Sheahan, X. Xiao, L. E. Hensley, P. Prabakaran, B. Rockx, I. A. Sidorov, D. Corti, L. Vogel, Y. Feng, J. O. Kim, L. F. Wang, R. Baric, A. Lanzavecchia, K. M. Curtis, G. J. Nabel, K. Subbarao, S. Jiang, and D. S. Dimitrov. 2007. Potent cross-reactive neutralization of SARS coronavirus isolates by human monoclonal antibodies. Proc. Natl. Acad. Sci. USA 104:12123-12128.