Mechanisms of host receptor adaptation by severe acute respiratory syndrome coronavirus

Journal of Biological Chemistry

Volumn 287, Issue 12, 2012, Pages 8904-8911

  Wu, Kailang ^a   Peng, Guiqing ^a   Wilken, Matthew ^a   Geraghty, Robert J ^b   Li, Fang ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; BINDING AFFINITIES; FAVORABLE INTERACTIONS; HIGH AFFINITY; HOT SPOT; HUMAN RECEPTORS; RECEPTOR-BINDING DOMAINS; SEVERE ACUTE RESPIRATORY SYNDROME CORONAVIRUS; STRUCTURAL BASIS; STRUCTURAL MECHANISMS;

ANIMALS; BINDING ENERGY; OPTIMIZATION; VIRUSES;

DISEASES;

ANGIOTENSIN CONVERTING ENZYME 2;

ADAPTATION; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; RECEPTOR BINDING; RECEPTOR BINDING DOMAIN; SARS CORONAVIRUS; VIRUS CELL INTERACTION;

ANIMALS; CELL LINE; DISEASE RESERVOIRS; DISEASE VECTORS; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; MUTATION; PEPTIDYL-DIPEPTIDASE A; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, VIRUS; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRAL PROTEINS; VIVERRIDAE;

ANIMALIA; SARS CORONAVIRUS; VIVERRIDAE;

EID: 84858611541     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.325803     Document Type: Article

References (38)

1. Lee, N., Hui, D., Wu, A., Chan, P., Cameron, P., Joynt, G. M., Ahuja, A., Yung, M. Y., Leung, C. B., To, K. F., Lui, S. F., Szeto, C. C., Chung, S., and Sung, J. J. (2003)Amajor outbreak of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 348, 1986-1994 (Pubitemid 36569987)
2. Yu, I. T., Li, Y., Wong, T. W., Tam, W., Chan, A. T., Lee, J. H., Leung, D. Y., and Ho, T. (2004) Evidence of airborne transmission of the severe acute respiratory syndrome virus. N. Engl. J. Med. 350, 1731-1739 (Pubitemid 38528700)
3. Marra, M. A., Jones, S. J., Astell, C. R., Holt, R. A., Brooks-Wilson, A., Butterfield, Y. S., Khattra, J., Asano, J. K., Barber, S. A., Chan, S. Y., Cloutier, A., Coughlin, S. M., Freeman, D., Girn, N., Griffith, O. L., Leach, S. R., Mayo, M., McDonald, H., Montgomery, S. B., Pandoh, P. K., Petrescu, A. S., Robertson, A. G., Schein, J. E., Siddiqui, A., Smailus, D. E., Stott, J. M., Yang, G. S., Plummer, F., Andonov, A., Artsob, H., Bastien, N., Bernard, K., Booth, T. F., 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, G. A., Tyler, S., Vogrig, R., Ward, D., Watson, B., Brunham, R. C., Krajden, M., Petric, M., Skowronski, D. M., Upton, C., and Roper, R. L. (2003) The genome sequence of the SARS-associated coronavirus. Science 300, 1399-1404 (Pubitemid 36638153)
4. Peiris, J. S., Lai, S. T., Poon, L. L., Guan, Y., Yam, L. Y., Lim, W., Nicholls, J., Yee, W. K., Yan, W. W., Cheung, M. T., Cheng, V. C., Chan, K. H., Tsang, D. N., Yung, R. W., Ng, T. K., and Yuen, K. Y. (2003) Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361, 1319-1325 (Pubitemid 36514862)
5. Guan, Y., Zheng, B. J., He, Y. Q., Liu, X. L., Zhuang, Z. X., Cheung, C. L., Luo, S. W., Li, P. H., Zhang, L. J., Guan, Y. J., Butt, K. M., Wong, K. L., Chan, K. W., Lim, W., Shortridge, K. F., Yuen, K. Y., Peiris, J. S., and Poon, L. L. (2003) Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302, 276-278 (Pubitemid 37248756)
6. Liang, G., Chen, Q., Xu, J., Liu, Y., Lim, W., Peiris, J. S., Anderson, L. J., Ruan, L., Li, H., Kan, B., Di, B., Cheng, P., Chan, K. H., Erdman, D. D., Gu, S., Yan, X., Liang, W., Zhou, D., Haynes, L., Duan, S., Zhang, X., Zheng, H., Gao, Y., Tong, S., Li, D., Fang, L., Qin, P., Xu, W., and SARS Diagnosis Working Group (2004) Laboratory diagnosis of four recent sporadic cases of community-acquired SARS, Guangdong Province, China. Emerging Infectious Diseases 10, 1774-1781 (Pubitemid 39319368)
7. Song, H. D., Tu, C. C., Zhang, G. W., Wang, S. Y., Zheng, K., Lei, L. C., Chen, Q. X., Gao, Y. W., Zhou, H. Q., Xiang, H., Zheng, H. J., Chern, S. W., Cheng, F., Pan, C. M., Xuan, H., Chen, S. J., Luo, H. M., Zhou, D. H., Liu, Y. F., He, J. F., Qin, P. Z., Li, L. H., Ren, Y. Q., Liang, W. J., Yu, Y. D., Anderson, L., Wang, M., Xu, R. H., Wu, X. W., Zheng, H. Y., Chen, J. D., Liang, G., Gao, Y., Liao, M., Fang, L., Jiang, L. Y., Li, H., Chen, F., Di, B., He, L. J., Lin, J. Y., Tong, S., Kong, X., Du, L., Hao, P., Tang, H., Bernini, A., Yu, X. J., Spiga, O., Guo, Z. M., Pan, H. Y., He, W. Z., Manuguerra, J. C., Fontanet, A., Danchin, A., Niccolai, N., Li, Y. X., Wu, C. I., and Zhao, G. P. (2005) Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. U.S.A. 102, 2430-2435 (Pubitemid 40279393)
8. 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
9. Liu, L., Fang, Q., Deng, F., Wang, H., Yi, C. E., Ba, L., Yu, W., Lin, R. D., Li, T., Hu, Z., Ho, D. D., Zhang, L., and Chen, Z. (2007) Natural mutations in the receptor-binding domain of spike glycoprotein determine the reactivity of cross-neutralization between palm civet coronavirus and severe acute respiratory syndrome coronavirus. J. Virol. 81, 4694-4700 (Pubitemid 46668666)
10. Sheahan, T., Rockx, B., Donaldson, E., Sims, A., Pickles, R., Corti, D., and Baric, R. (2008) Mechanisms of zoonotic severe acute respiratory syndrome coronavirus host range expansion in human airway epithelium. J. Virol. 82, 2274-2285 (Pubitemid 351293527)
11. Li, W., Wong, S. K., Li, F., Kuhn, J. H., Huang, I. C., Choe, H., and Farzan, M. (2006) Animal origins of the severe acute respiratory syndrome coronavirus: insight from ACE2-S-protein interactions. J. Virol. 80, 4211-4219
12. Kan, B., Wang, M., Jing, H., Xu, H., Jiang, X., Yan, M., Liang, W., Zheng, H., Wan, K., Liu, Q., Cui, B., Xu, Y., Zhang, E., Wang, H., Ye, J., Li, G., Li, M., Cui, Z., Qi, X., Chen, K., Du, L., Gao, K., Zhao, Y. T., Zou, X. Z., Feng, Y. J., Gao, Y. F., Hai, R., Yu, D., Guan, Y., and Xu, J. (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 (Pubitemid 41279306)
13. Lau, S. K., Woo, P. C., Li, K. S., Huang, Y., Tsoi, H. W., Wong, B. H., Wong, S. S., Leung, S. Y., Chan, K. H., and Yuen, K. Y. (2005) Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. U.S.A. 102, 14040-14045 (Pubitemid 41377699)
14. Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J. H., Wang, H., Crameri, G., Hu, Z., Zhang, H., Zhang, J., McEachern, J., Field, H., Daszak, P., Eaton, B. T., Zhang, S., and Wang, L. F. (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310, 676-679 (Pubitemid 41528160)
15. Ren, W., Qu, X., Li, W., Han, Z., Yu, M., Zhou, P., Zhang, S. Y., Wang, L. F., Deng, H., and Shi, Z. (2008) Difference in receptor usage between severe acute respiratory syndrome (SARS) coronavirus and SARS-like coronavirus of bat origin. J. Virol. 82, 1899-1907 (Pubitemid 351206936)
16. Li, W., Moore, M. J., Vasilieva, N., Sui, J., Wong, S. K., Berne, M. A., Somasundaran, M., Sullivan, J. L., Luzuriaga, K., Greenough, T. C., Choe, H., and Farzan, M. (2003) Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426, 450-454 (Pubitemid 37490132)
17. Li, F., Berardi, M., Li, W., Farzan, M., Dormitzer, P. R., and Harrison, S. C. (2006) Conformational states of the severe acute respiratory syndrome coronavirus spike protein ectodomain. J. Virol. 80, 6794-6800 (Pubitemid 44025179)
18. Lai, M. M., and Holmes, K. V. (2001) in Fields Virology (Knipe, D. M., and Howley, P. M., eds) pp. 1163-1186, Lippincott Williams & Wilkins, Philadelphia, PA
19. Xu, Y., Lou, Z., Liu, Y., Pang, H., Tien, P., Gao, G. F., and Rao, Z. (2004) Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J. Biol. Chem. 279, 49414-49419 (Pubitemid 39625827)
20. Babcock, G. J., Esshaki, D. J., Thomas, W. D., Jr., and Ambrosino, D. M. (2004) Amino acids 270-510 of the severe acute respiratory syndrome coronavirus spike protein are required for interaction with receptor. J. Virol. 78, 4552-4560 (Pubitemid 38501075)
21. Wong, S. K., Li, W., Moore, M. J., Choe, H., and Farzan, M. (2004) A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 279, 3197-3201 (Pubitemid 38140552)
22. Xiao, X., Chakraborti, S., Dimitrov, A. S., Gramatikoff, K., and Dimitrov, D. S. (2003) The SARS-CoV S glycoprotein: expression and functional characterization. Biochem. Biophys. Res. Commun. 312, 1159-1164 (Pubitemid 37490937)
23. Li, W., Greenough, T. C., Moore, M. J., Vasilieva, N., Somasundaran, M., Sullivan, J. L., Farzan, M., and Choe, H. (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 (Pubitemid 39299688)
24. Li, W., Zhang, C., Sui, J., Kuhn, J. H., Moore, M. J., Luo, S., Wong, S. K., Huang, I. C., Xu, K., Vasilieva, N., Murakami, A., He, Y., Marasco, W. A., Guan, Y., Choe, H., and Farzan, M. (2005) Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 24, 1634-1643 (Pubitemid 40646452)
25. McCray, P. B., Jr., Pewe, L., Wohlford-Lenane, C., Hickey, M., Manzel, L., Shi, L., Netland, J., Jia, H. P., Halabi, C., Sigmund, C. D., Meyerholz, D. K., Kirby, P., Look, D. C., and Perlman, S. (2007) Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J. Virol. 81, 813-821 (Pubitemid 46067907)
26. Li, F., Li, W., Farzan, M., and Harrison, S. C. (2005) Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309, 1864-1868 (Pubitemid 41325098)
27. Li, F. (2008) Structural analysis of major species barriers between humans and palm civets for severe acute respiratory syndrome coronavirus infections. J. Virol. 82, 6984-6991
28. Qu, X. X., Hao, P., Song, X. J., Jiang, S. M., Liu, Y. X., Wang, P. G., Rao, X., Song, H. D., Wang, S. Y., Zuo, Y., Zheng, A. H., Luo, M., Wang, H. L., Deng, F., Wang, H. Z., Hu, Z. H., Ding, M. X., Zhao, G. P., and Deng, H. K. (2005) Identification of two critical amino acid residues of the severe acute respiratory syndrome coronavirus spike protein for its variation in zoonotic tropism transition via a double substitution strategy. J. Biol. Chem. 280, 29588-29595 (Pubitemid 41177034)
29. Wu, K., Chen, L., Peng, G., Zhou, W., Pennell, C. A., Mansky, L. M., Geraghty, R. J., and Li, F. (2011) A virus-binding hot spot on human angiotensin-converting enzyme 2 is critical for binding of two different coronaviruses. J. Virol. 85, 5331-5337
30. Wu, K., Li, W., Peng, G., and Li, F. (2009) Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor. Proc. Natl. Acad. Sci. U.S.A. 106, 19970-19974
31. Price, J., Turner, D., and Cepko, C. (1987) Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc. Natl. Acad. Sci. U.S.A. 84, 156-160 (Pubitemid 17013593)
32. Peng, G., Sun, D., Rajashankar, K. R., Qian, Z., Holmes, K. V., and Li, F. (2011) Crystal structure of mouse coronavirus receptor-binding domain complexed with its murine receptor. Proc. Natl. Acad. Sci. U.S.A. 108, 10696-10701
33. Towler, P., Staker, B., Prasad, S. G., Menon, S., Tang, J., Parsons, T., Ryan, D., Fisher, M., Williams, D., Dales, N. A., Patane, M. A., and Pantoliano, M. W. (2004) ACE2 X-ray structures reveal a large hinge-bending motion important for inhibitor binding and catalysis. J. Biol. Chem. 279, 17996-18007 (Pubitemid 38560569)
34. Hou, Y., Peng, C., Yu, M., Li, Y., Han, Z., Li, F., Wang, L. F., and Shi, Z. (2010) Angiotensin-converting enzyme 2 (ACE2) proteins of different bat species confer variable susceptibility to SARS-CoV entry. Arch. Virol. 155, 1563-1569
35. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
36. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography &NMRsystem: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
37. Murshudov, G. N., Vagin, A. A., Lebedev, A., Wilson, K. S., and Dodson, E. J. (1999) Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D Biol. Crystallogr. 55, 247-255 (Pubitemid 29053823)
38. Fenn, T. D., Ringe, D., and Petsko, G. A. (2003) POVScript+: a program for model and data visualization using persistence of vision ray-tracing. J. Appl. Crystallogr. 36, 944-947