Functional characterization of heptad repeat 1 and 2 mutants of the spike protein of severe acute respiratory syndrome coronavirus

Journal of Virology

Volumn 80, Issue 7, 2006, Pages 3225-3237

  Chan, Woan Eng ^a   Chuang, Chin Kai ^b   Yeh, Shiou Hwei ^c   Chang, Mau Sun ^d   Chen, Steve S L ^a  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^b ANIMAL TECHNOLOGY INSTITUTE TAIWAN   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d MACKAY MEMORIAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; CHLORAMPHENICOL ACETYLTRANSFERASE; DIPEPTIDYL CARBOXYPEPTIDASE; HEPTAD REPEAT 1; HEPTAD REPEAT 2; ISOLEUCINE; LEUCINE; LUCIFERASE; MUTANT PROTEIN; PROLINE; RNA DIRECTED DNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS SPIKE PROTEIN;

ALPHA HELIX; ANIMAL CELL; ARTICLE; BIOSYNTHESIS; BIOTINYLATION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG TERMINAL REPEAT; MEMBRANE FUSION; MOLECULAR WEIGHT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS CELL INTERACTION;

AMINO ACID SUBSTITUTION; ANIMALS; BIOTINYLATION; CELL LINE; CERCOPITHECUS AETHIOPS; CHLORAMPHENICOL O-ACETYLTRANSFERASE; HUMANS; LUCIFERASES; MEMBRANE FUSION; MODELS, MOLECULAR; MOLECULAR WEIGHT; PRECIPITIN TESTS; PROLINE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; SARS VIRUS; VERO CELLS; VIRAL FUSION PROTEINS;

ANIMALIA; CORONAVIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; SARS CORONAVIRUS;

EID: 33645219694     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.7.3225-3237.2006     Document Type: Article

References (61)

1. Babcock, G. J., D. J. Esshaki, W. D. Thomas, Jr., and D. M. Ambrosino. 2004. Amino acids 270 to 510 of the severe acute respiratory syndrome coronavirus spike protein are required for interaction with receptor. J. Virol. 78:4552-4560.
2. Bisht, H., A. Roberts, L. Vogel, A. Bukreyev, P. L. Collins, B. R. Murphy, K. Subbarao, and B. Moss. 2004. Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice. Proc. Natl. Acad. Sci. USA 101:6641-6646.
3. Blacklow, S. C., M. Lu, and P. S. Kim. 1995. A trimeric subdomain of the simian immunodeficiency virus envelope glycoprotein. Biochemistry 34:14955-14962.
4. Bosch, B. J., B. E. Martina, R. Van Der Zee, J. Lepault, B. J. Haijema, C. Versluis, A. J. Heck, R. De Groot, A. D. Osterhaus, and P. J. Rottier. 2004. Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc. Natl. Acad. Sci. USA 101:8455-8460.
5. Bosch, B. J., R. van der Zee, C. A. M. de Haan, and P. J. M. Rottier. 2003. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77:8801-8811.
6. Bullough, P. A., F. M. Hughson, J. J. Skehel, and D. C. Wiley. 1994. Structure of influenza hemagglutinin at the pH of membrane fusion. Nature (London) 371:37-43.
7. Caffrey, M., M. Cai, J. Kaufman, S. J. Stahl, P. T. Wingfleld, D. G. Covell, A. M. Gronenborn, and G. M. Clore. 1998. Three-dimensional solution structure of the 44 kDa ectodomain of SIV gp41. EMBO J. 17:4572-4584.
8. Carr, C. M., and P. S. Kim. 1993. A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823-832.
9. Chan, D. C., D. Fass, J. M. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-273.
10. Chan, W.-E., Y.-L. Wang, H.-H. Lin, and S. S.-L. Chen. 2004. Effect of extension of the cytoplasmic domain of human immunodeficiency type 1 virus transmembrane protein gp41 on virus replication. J. Virol. 78:5157-5169.
11. Chan, W.-E., H.-H. Lin, and S. S.-L. Chen. 2005. Wild-type-like viral replication potential of human immunodeficiency virus type 1 envelope mutants lacking palmitoylation signals. J. Virol. 79:8374-8387.
12. Chang, M. S., Y. T. Lu, S. T. Ho, C. C. Wu, T. Y. Wei, C. J. Chen, Y. T. Hsu, P. C. Chu, C. H. Chen, J. M. Chu, Y. L. Jan, C. C. Hung, C. C. Fan, and Y. C. Yang. 2004. Antibody detection of SARS-CoV spike and nucleocapsid protein. Biochem. Biophys. Res. Commun. 314:931-936.
13. Chen, S. S.-L., A. A. Ferrante, and E. F. Terwilliger. 1996. Characterization of an envelope mutant of HIV-1 that interferes with viral infectivity. Virology 226:260-268.
14. Chen, S. S.-L., S.-F. Lee, H.-J. Hao, and C.-K. Chuang. 1998. Mutations in the leucine zipper-like heptad repeat sequence of human immunodeficiency virus type 1 gp41 dominantly interfere with wild-type virus infectivity. J. Virol. 72:4765-4774.
15. Conor, R. L., B. K. Chen, and N. R. Landau. 1995. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206:935-944.
16. Duquerroy, S., A. Vigouroux, P. J. Rottier, F. A. Rey, and B. J. Bosch. 2005. Central ions and lateral asparagine/glutamine zippers stabilize the post-fusion hairpin conformation of the SARS coronavirus spike glycoprotein. Virology 335:276-285.
17. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
18. Follis, K. E., J. York, and J. H. Nunberg. 2005. Serine-scanning mutagenesis studies of the C-terminal heptad repeats in the SARS coronavirus S glycoprotein highlight the important role of the short helical region. Virology 341:122-129.
19. Fukushi, S., T. Mizutani, M. Saijo, S. Matsuyama, N. Miyajima, F. Taguchi, S. Itamura, I. Kurane, and S. Morikawa. 2005. Vesicular stomatitis virus pseudotyped with severe acute respiratory syndrome coronavirus spike protein. J. Gen. Virol. 86:2269-2274.
20. Garoff, H., R. Hewson, and D. J. Opstelten. 1998. Virus maturation by budding. Microbiol. Mol. Biol. Rev. 62:1171-1190.
21. Giroglou, T., J. Cinatl, Jr., H. Rabenau, C. Drosten, H. Schwalbe, H. W. Doerr, and D. von Laer. 2004. Retroviral vectors pseudotyped with severe acute respiratory syndrome coronavirus S protein. J. Virol. 78:9007-9015.
22. Helseth, E., M. Kowalski, D. Gabuzda, U. Olshevsky, W. Haseltine, and J. Sodroski. 1990. Rapid complementation assays measuring replicative potential of human immunodeficiency virus type 1 envelope glycoprotein mutants. J. Virol. 64:2416-2420.
23. Hernandez, L. D., L. R. Hoffman, T. G. Wolfsberg, and J. M. White. 1996. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12:627-661.
24. Hofmann, H., K. Hattermann, A. Marzi, T. Gramberg, M. Geier, M. Krumbiegel, S. Kuate, K. Uberla, M. Niedrig, and S. Pohlmann. 2004. S protein of severe acute respiratory syndrome-associated coronavirus mediates entry into hepatoma cell lines and is targeted by neutralizing antibodies in infected patients. J. Virol. 78:6134-6142.
25. Huang, L. R., C. M. Chiu, S. H. Yeh, W. H. Huang, P. R. Hsueh, W. Z. Yang, J. Y. Yang, I. J. Su, S. C. Chang, and P. J. Chen. 2004. Evaluation of antibody responses against SARS coronaviral nucleocapsid or spike proteins by immunoblotting or ELISA. J. Med. Virol. 73:338-346.
26. Ingallinella, P., E. Bianchi, M. Finotto, G. Cantoni, D. M. Eckert, V. M. Supekar, C. Bruckmann, A. Carfi, and A. Pessi. 2004. Structural characterization of the fusion-active complex of severe acute respiratory syndrome (SARS) coronavirus. Proc. Natl. Acad. Sci. USA 101:8709-8714.
27. Kos, C. H. 2004. Cre/loxP system for generating tissue-specific knockout mouse models. Nutr. Rev. 62:243-246.
28. Lai, M. M. C., and K. V. Holmes. 2001. Coronaviridae: the viruses and their replication, p. 1163-1185. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
29. Lee, S.-F., C.-Y. Ko, C.-T. Wang, and S. S.-L. Chen. 2002. Effect of point mutations in the N terminus of the lentivirus lytic peptide-1 sequence of human immunodeficiency virus type 1 transmembrane glycoprotein gp41 on Env stability. J. Biol. Chem. 277:15363-15375.
30. 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.
31. 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 (London) 426:450-454.
32. Liu, S., G. Xiao, Y. Chen, Y. He, J. Niu, C. R. Escalante, H. Xiong, J. Farmar, A. K. Debnath, P. Tien, and S. Jiang. 2004. Interaction between heptad repeat 1 and 2 regions in spike protein of SARS-associated coronavirus: implications for virus fusogenic mechanism and identification of fusion inhibitors. Lancet 363:938-947.
33. Lu, M., S. C. Blacklow, and P. S. Kim. 1995. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2:1075-1082.
34. Marra, M. A., S. J. Jones, C. R. Astell, R. A. Holt, A. Brooks-Wilson, Y. S. Butterfleld, 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.
35. Marzi, A., T. Gramberg, G. Simmons, P. Moller, A. J. Rennekamp, M. Krumbiegel, M. Geier, J. Eisemann, N. Turza, B. Saunier, A. Steinkasserer, S. Becker, P. Bates, H. Hofmann, and S. Pohlmann. 2004. DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus. J. Virol. 78:12090-12095.
36. Moore, M. J., T. Dorfman, W. Li, S. K. Wong, Y. Li, J. H. Kuhn, J. Coderre, N. Vasilieva, Z. Han, T. C. Greenough, M. Farzan, and H. Choe. 2004. Retroviruses pseudotyped with the severe acute respiratory syndrome coronavirus spike protein efficiently infect cells expressing angiotensin-converting enzyme 2. J. Virol. 78:10628-10635.
37. Murakami, T., and E. O. Freed. 2000. Genetic evidence for an interaction between human immunodeficiency virus type 1 matrix and α-helix 2 of the gp41 cytoplasmic tail. J. Virol. 74:3548-3554.
38. Opstelten, D. J., M. J. Raamsman, K. Wolfs, M. C. Horzinek, and P. J. Rottier. 1995. Envelope glycoprotein interactions in coronavirus assembly. J. Cell Biol. 131:339-349.
39. 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.
40. Salzwedel, K., J. T. West, and E. Hunter. 1999. A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J. Virol. 73:2469-2480.
41. Simmons, G., J. D. Reeves, A. J. Rennekamp, S. M. Amberg, A. J. Piefer, and P. Bates. 2004. Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. Proc. Natl. Acad. Sci. USA 101:4240-4245.
42. Skehel, J. J., and D. C. Wiley. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569.
43. Song, H. C., M. Y. Seo, K. Stadler, B. J. Yoo, Q. L. Choo, S. R. Coates, Y. Uematsu, T. Harada, C. E. Greer, J. M. Polo, P. Pileri, M. Eickmann, R. Rappuoli, S. Abrignani, M. Houghton, and J. H. Han. 2004. Synthesis and characterization of a native, oligomeric form of recombinant severe acute respiratory syndrome coronavirus spike glycoprotein. J. Virol. 78:10328-10335.
44. Sui, J., W. Li, A. Murakami, A. Tamin, L. J. Matthews, S. K. Wong, M. J. Moore, A. S. Tallarico, M. Olurinde, H. Choe, L. J. Anderson, W. J. Bellini, M. Farzan, and W. A. Marasco. 2004. Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc. Natl. Acad. Sci. USA 101:2536-2541.
45. Supekar, V. M., C. Bruckmann, P. Ingallinella, E. Bianchi, A. Pessi, and A. Carfi. 2004. Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2-fusion protein. Proc. Natl. Acad. Sci. USA 101:17958-17963.
46. Tan, K., J.-H. Liu, J.-H. Wang, S. Shen, and M. Lu. 1997. Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. USA 94:12303-12308.
47. Tripet, B., M. W. Howard, M. Jobling, R. K. Holmes, K. V. Holmes, and R. S. Hodges. 2004. Structural characterization of the SARS-coronavirus spike S fusion protein core. J. Biol. Chem. 279:20836-20849.
48. Van Duyne, G. D. 2001. A structural view of Cre-loxp site-specific recombination. Annu. Rev. Biophys. Biomol. Struct. 30:87-104.
49. Vennema, H., G. J. Godeke, J. W. Rossen, W. F. Voorhout, M. C. Horzinek, D. J. Opstelten, and P. J. Rottier. 1996. Nucleocapsid-independent assembly of coronavirus-Iike particles by co-expression of viral envelope protein genes. EMBO J. 15:2020-2028.
50. Weissenhorn, W., L. Calder, A. Dessen, T. Laue, J. J. Skehel, and D. C. Wiley. 1997. Assembly of a rod-shaped chimera of a trimeric GCN4 zipper and the HIV-1 gp41 ectodomain expressed in Escherichia coli. Proc. Natl. Acad. Sci. USA 94:6065-6069.
51. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Willey. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature (London) 387:426-430.
52. Weissenhorn, W., S. A. Wharton, L. J. Calder, P. L. Earl, B. Moss, E. Aliprandis, J. J. Skehel, and D. C. Wiley. 1996. The ectodomain of HIV-1 env subunit gp41 forms a soluble, alpha-helical, rod-like oligomer in the absence of gp120 and the N-terminal fusion peptide. EMBO J. 15:1507-1514.
53. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the hemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature (London) 289:366-373.
54. Wong, S. K., W. Li, M. J. Moore, H. Choe, and M. Farzan. 2004. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 279:3197-3201.
55. Xiao, X., S. Chakraborti, A. S. Dimitrov, K. Gramatikoff, and D. S. Dimitrov. 2003. The SARS-CoV S glycoprotein: expression and functional characterization. Biochem. Biophys. Res. Commun. 312:1159-1164.
56. Xu, Y., Y. Liu, Z. Lou, L. Qin, X. Li, Z. Bai, H. Pang, P. Tien, G. F. Gao, and Z. Rao. 2004. Structural basis for coronavirus-mediated membrane fusion. Crystal structure of mouse hepatitis virus spike protein fusion core. J. Biol. Chem. 279:30514-30522.
57. Xu, Y., Z. Lou, Y. Liu, H. Pang, P. Tien, G. F. Gao, and Z. Rao. 2004. Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J. Biol. Chem. 279:49414-49419.
58. Xu, Y., J. Zhu, Y. Liu, Z. Lou, F. Yuan, Y. Liu, D. K. Cole, L. Ni, N. Su, L. Qin, X. Li, Z. Bai, J. I. Bell, H. Pang, P. Tien, G. F. Gao, and Z. Rao. 2004. Characterization of the heptad repeat regions, HR1 and HR2, and design of a fusion core structure model of the spike protein from severe acute respiratory syndrome (SARS) coronavirus. Biochemistry 43:14064-14071.
59. 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.
60. Yuan, K., L. Yi, J. Chen, X. Qu, T. Qing, X. Rao, P. Jiang, J. Hu, Z. Xiong, Y. Nie, X. Shi, W. Wang, C. Ling, X. Yin, K. Fan, L. Lai, M. Ding, and H. Deng. 2004. Suppression of SARS-CoV entry by peptides corresponding to heptad regions on spike glycoprotein. Biochem. Biophys. Res. Commun. 319:746-752.
61. Zhu, J., G. Xiao, Y. Xu, F. Yuan, C. Zheng, Y. Liu, H. Yan, D. K. Cole, J. I. Bell, Z. Rao, P. Tien, and G. F. Gao. 2004. Following the rule: formation of the 6-helix bundle of the fusion core from severe acute respiratory syndrome coronavirus spike protein and identification of potent peptide inhibitors. Biochem. Biophys. Res. Commun. 319:283-288.