Quantitative comparison of the efficiency of antibodies against S1 and S2 subunit of SARS coronavirus spike protein in virus neutralization and blocking of receptor binding: Implications for the functional roles of S2 subunit

FEBS Letters

Volumn 580, Issue 24, 2006, Pages 5612-5620

  Zeng, Fanya ^a   Hon, Chung Chau ^a   Yip, Chi Wai ^a   Law, Ka Man ^a   Yeung, Yin Shan ^a   Chan, Kwok Hung ^a   Malik Peiris, Joseph S ^a   Leung, Frederick Chi Ching ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Antibodies; Cell based receptor binding assay; SARS; Spike protein; Virus neutralization

Indexed keywords

ADENOVIRUS VECTOR; CELL RECEPTOR; IMMUNOGLOBULIN G ANTIBODY; SPIKE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING ASSAY; CONTROLLED STUDY; EMBRYO; MEMBRANE BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SARS CORONAVIRUS; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, VIRAL; CELL LINE; CERCOPITHECUS AETHIOPS; CRICETINAE; EPITOPES; MEMBRANE GLYCOPROTEINS; MICE; PROTEIN BINDING; PROTEIN SUBUNITS; SARS VIRUS; VIRAL ENVELOPE PROTEINS;

SARS CORONAVIRUS;

EID: 33749382628     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2006.08.085     Document Type: Article

References (43)

1. 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. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361 (2003) 1319-1325
2. Cavanagh D. Severe acute respiratory syndrome vaccine development: experiences of vaccination against avian infectious bronchitis coronavirus. Avian Pathol. 32 (2003) 567-582
3. Saif L.J. Animal coronavirus vaccines: lessons for SARS. Dev. Biol. (Basel) 119 (2004) 129-140
4. Taylor D.R. Obstacles and advances in SARS vaccine development. Vaccine 24 (2006) 863-871
5. He Y., and Jiang S. Vaccine design for severe acute respiratory syndrome coronavirus. Viral Immunol. 18 (2005) 327-332
6. Dimitrov D.S. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol. 2 (2004) 109-122
7. Hofmann H., and Pohlmann S. Cellular entry of the SARS coronavirus. Trends Microbiol. 12 (2004) 466-472
8. Cavanagh D., Davis P.J., Darbyshire J.H., and Peters R.W. Coronavirus IBV: virus retaining spike glycopolypeptide S2 but not S1 is unable to induce virus-neutralizing or haemagglutination-inhibiting antibody, or induce chicken tracheal protection. J. Gen. Virol. 67 Pt 7 (1986) 1435-1442
9. Delmas B., Rasschaert D., Godet M., Gelfi J., and Laude H. Four major antigenic sites of the coronavirus transmissible gastroenteritis virus are located on the amino-terminal half of spike glycoprotein S. J. Gen. Virol. 71 Pt 6 (1990) 1313-1323
10. Godet M., Grosclaude J., Delmas B., and Laude H. Major receptor-binding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J. Virol. 68 (1994) 8008-8016
11. Vautherot J.F., Madelaine M.F., Boireau P., and Laporte J. Bovine coronavirus peplomer glycoproteins: detailed antigenic analyses of S1, S2 and HE. J. Gen. Virol. 73 Pt 7 (1992) 1725-1737
12. Keng C.T., Zhang A., Shen S., Lip K.M., Fielding B.C., Tan T.H., Chou C.F., Loh C.B., Wang S., Fu J., Yang X., Lim S.G., Hong W., and Tan Y.J. Amino acids 1055 to 1192 in the S2 region of severe acute respiratory syndrome coronavirus S protein induce neutralizing antibodies: implications for the development of vaccines and antiviral agents. J. Virol. 79 (2005) 3289-3296
13. Lai S.C., Chong P.C., Yeh C.T., Liu L.S., Jan J.T., Chi H.Y., Liu H.W., Chen A., and Wang Y.C. Characterization of neutralizing monoclonal antibodies recognizing a 15-residues epitope on the spike protein HR2 region of severe acute respiratory syndrome coronavirus (SARS-CoV). J. Biomed. Sci. 12 (2005) 711-727
14. Zhang H., Wang G., Li J., Nie Y., Shi X., Lian G., Wang W., Yin X., Zhao Y., Qu X., Ding M., and Deng H. Identification of an antigenic determinant on the S2 domain of the severe acute respiratory syndrome coronavirus spike glycoprotein capable of inducing neutralizing antibodies. J. Virol. 78 (2004) 6938-6945
15. Choy W.Y., Lin S.G., Chan P.K., Tam J.S., Lo Y.M., Chu I.M., Tsai S.N., Zhong M.Q., Fung K.P., Waye M.M., Tsui S.K., Ng K.O., Shan Z.X., Yang M., Wu Y.L., Lin Z.Y., and Ngai S.M. Synthetic peptide studies on the severe acute respiratory syndrome (SARS) coronavirus spike glycoprotein: perspective for SARS vaccine development. Clin. Chem. 50 (2004) 1036-1042
16. Hua R., Zhou Y., Wang Y., Hua Y., and Tong G. Identification of two antigenic epitopes on SARS-CoV spike protein. Biochem. Biophys. Res. Commun. 319 (2004) 929-935
17. Zhong X., Yang H., Guo Z.F., Sin W.Y., Chen W., Xu J., Fu L., Wu J., Mak C.K., Cheng C.S., Yang Y., Cao S., Wong T.Y., Lai S.T., Xie Y., and Guo Z. B-cell responses in patients who have recovered from severe acute respiratory syndrome target a dominant site in the S2 domain of the surface spike glycoprotein. J. Virol. 79 (2005) 3401-3408
18. Duan J., Yan X., Guo X., Cao W., Han W., Qi C., Feng J., Yang D., Gao G., and Jin G. A human SARS-CoV neutralizing antibody against epitope on S2 protein. Biochem. Biophys. Res. Commun. 333 (2005) 186-193
19. Wang S., Chou T.H., Sakhatskyy P.V., Huang S., Lawrence J.M., Cao H., Huang X., and Lu S. Identification of two neutralizing regions on the severe acute respiratory syndrome coronavirus spike glycoprotein produced from the mammalian expression system. J. Virol. 79 (2005) 1906-1910
20. Zeng F., Chow K.Y., Hon C.C., Law K.M., Yip C.W., Chan K.H., Peiris J.S., and Leung F.C. Characterization of humoral responses in mice immunized with plasmid DNAs encoding SARS-CoV spike gene fragments. Biochem. Biophys. Res. Commun. 315 (2004) 1134-1139
21. Earp L.J., Delos S.E., Park H.E., and White J.M. The many mechanisms of viral membrane fusion proteins. Curr. Top. Microbiol. Immunol. 285 (2005) 25-66
22. Sainz Jr. B., Rausch J.M., Gallaher W.R., Garry R.F., and Wimley W.C. Identification and characterization of the putative fusion peptide of the severe acute respiratory syndrome-associated coronavirus spike protein. J. Virol. 79 (2005) 7195-7206
23. Sainz Jr. B., Rausch J.M., Gallaher W.R., Garry R.F., and Wimley W.C. The aromatic domain of the coronavirus class I viral fusion protein induces membrane permeabilization: putative role during viral entry. Biochemistry 44 (2005) 947-958
24. Taguchi F., and Shimazaki Y.K. Functional analysis of an epitope in the S2 subunit of the murine coronavirus spike protein: involvement in fusion activity. J. Gen. Virol. 81 (2000) 2867-2871
25. Lip K.M., Shen S., Yang X., Keng C.T., Zhang A., Oh H.L., Li Z.H., Hwang L.A., Chou C.F., Fielding B.C., Tan T.H., Mayrhofer J., Falkner F.G., Fu J., Lim S.G., Hong W., and Tan Y.J. Monoclonal antibodies targeting the HR2 domain and the region immediately upstream of the HR2 of the S protein neutralize in vitro infection of severe acute respiratory syndrome coronavirus. J. Virol. 80 (2006) 941-950
26. McGaughey G.B., Barbato G., Bianchi E., Freidinger R.M., Garsky V.M., Hurni W.M., Joyce J.G., Liang X., Miller M.D., Pessi A., Shiver J.W., and Bogusky M.J. Progress towards the development of a HIV-1 gp41-directed vaccine. Curr. HIV Res. 2 (2004) 193-204
27. Zwick M.B., Jensen R., Church S., Wang M., Stiegler G., Kunert R., Katinger H., and Burton D.R. Anti-human immunodeficiency virus type 1 (HIV-1) antibodies 2F5 and 4E10 require surprisingly few crucial residues in the membrane-proximal external region of glycoprotein gp41 to neutralize HIV-1. J. Virol. 79 (2005) 1252-1261
28. Zwick M.B., Labrijn A.F., Wang M., Spenlehauer C., Saphire E.O., Binley J.M., Moore J.P., Stiegler G., Katinger H., Burton D.R., and Parren P.W. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75 (2001) 10892-10905
29. Chow K.Y., Yeung Y.S., Hon C.C., Zeng F., Law K.M., and Leung F.C. Adenovirus-mediated expression of the C-terminal domain of SARS-CoV spike protein is sufficient to induce apoptosis in Vero E6 cells. FEBS Lett. 579 (2005) 6699-6704
30. Bisht H., Roberts A., Vogel L., Bukreyev A., Collins P.L., Murphy B.R., Subbarao K., and Moss B. Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice. Proc. Natl. Acad. Sci. USA 101 (2004) 6641-6646
31. Zeng F.Y., Chan C.W., Chan M.N., Chen J.D., Chow K.Y., Hon C.C., Hui K.H., Li J., Li V.Y., Wang C.Y., Wang P.Y., Guan Y., Zheng B., Poon L.L., Chan K.H., Yuen K.Y., Peiris J.S., and Leung F.C. The complete genome sequence of severe acute respiratory syndrome coronavirus strain HKU-39849 (HK-39). Exp. Biol. Med. (Maywood) 228 (2003) 866-873
32. Chou C.F., Shen S., Tan Y.J., Fielding B.C., Tan T.H., Fu J., Xu Q., Lim S.G., and Hong W. A novel cell-based binding assay system reconstituting interaction between SARS-CoV S protein and its cellular receptor. J. Virol. Meth. 123 (2005) 41-48
33. Krokhin O., Li Y., Andonov A., Feldmann H., Flick R., Jones S., Stroeher U., Bastien N., Dasuri K.V., Cheng K., Simonsen J.N., Perreault H., Wilkins J., Ens W., Plummer F., and Standing K.G. Mass spectrometric characterization of proteins from the SARS virus: a preliminary report. Mol. Cell. Proteomics 2 (2003) 346-356
34. Burton D.R., Desrosiers R.C., Doms R.W., Koff W.C., Kwong P.D., Moore J.P., Nabel G.J., Sodroski J., Wilson I.A., and Wyatt R.T. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5 (2004) 233-236
35. Hamburger A.E., Kim S., Welch B.D., and Kay M.S. Steric accessibility of the HIV-1 gp41 N-trimer region. J. Biol. Chem. 280 (2005) 12567-12572
36. Eckert D.M., and Kim P.S. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70 (2001) 777-810
37. Zelus B.D., Schickli J.H., Blau D.M., Weiss S.R., and Holmes K.V. Conformational changes in the spike glycoprotein of murine coronavirus are induced at 37 °C either by soluble murine CEACAM1 receptors or by pH 8. J. Virol. 77 (2003) 830-840
38. Li F., Li W., Farzan M., and Harrison S.C. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309 (2005) 1864-1868
39. Chen Z., Zhang L., Qin C., Ba L., Yi C.E., Zhang F., Wei Q., He T., Yu W., Yu J., Gao H., Tu X., Gettie A., Farzan M., Yuen K.Y., and Ho D.D. Recombinant modified vaccinia virus Ankara expressing the spike glycoprotein of severe acute respiratory syndrome coronavirus induces protective neutralizing antibodies primarily targeting the receptor binding region. J. Virol. 79 (2005) 2678-2688
40. Heap C.J., Reading S.A., and Dimmock N.J. An antibody specific for the C-terminal tail of the gp41 transmembrane protein of human immunodeficiency virus type 1 mediates post-attachment neutralization, probably through inhibition of virus-cell fusion. J. Gen. Virol. 86 (2005) 1499-1507
41. 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. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302 (2003) 276-278
42. 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. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. USA 102 (2005) 14040-14045
43. 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. Bats are natural reservoirs of SARS-like coronaviruses. Science 310 (2005) 676-679