Human monoclonal antibodies to SARS-coronavirus inhibit infection by different mechanisms

Virology

Volumn 394, Issue 1, 2009, Pages 39-46

  Coughlin, Melissa M ^a   Babcook, John ^b   Prabhakar, Bellur S ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b Amgen British Columbia   (Canada)

Author keywords

Human monoclonal antibodies; Neutralizing antibodies; S protein; SARS CoV; Severe acute respiratory syndrome coronavirus; XenoMouse

Indexed keywords

EPITOPE; HUMAN MONOCLONAL ANTIBODY; HUMAN MONOCLONAL ANTIBODY 1B5; HUMAN MONOCLONAL ANTIBODY 3A7; HUMAN MONOCLONAL ANTIBODY 3C7; HUMAN MONOCLONAL ANTIBODY 3F3; HUMAN MONOCLONAL ANTIBODY 3H12; HUMAN MONOCLONAL ANTIBODY 4A10; HUMAN MONOCLONAL ANTIBODY 4D4; HUMAN MONOCLONAL ANTIBODY 4E2; HUMAN MONOCLONAL ANTIBODY 4G2; HUMAN MONOCLONAL ANTIBODY 5A5; HUMAN MONOCLONAL ANTIBODY 5A7; HUMAN MONOCLONAL ANTIBODY 5D3; HUMAN MONOCLONAL ANTIBODY 5D6; HUMAN MONOCLONAL ANTIBODY 5E4; HUMAN MONOCLONAL ANTIBODY 6B1; HUMAN MONOCLONAL ANTIBODY 6B5; HUMAN MONOCLONAL ANTIBODY 6B8; HUMAN MONOCLONAL ANTIBODY 6C1; HUMAN MONOCLONAL ANTIBODY 6C2; UNCLASSIFIED DRUG; VIRUS PROTEIN; VITRONECTIN;

ARTICLE; HUMAN; HUMAN CELL; IMMUNOTHERAPY; PRIORITY JOURNAL; RECEPTOR BINDING; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS ENTRY; VIRUS MUTATION; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIVIRAL AGENTS; CERCOPITHECUS AETHIOPS; HUMANS; INHIBITORY CONCENTRATION 50; MUTATION; NEUTRALIZATION TESTS; SARS VIRUS; VERO CELLS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

SARS CORONAVIRUS;

EID: 70350126946     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.07.028     Document Type: Article

References (45)

1. Baker S.C. Coronaviruses from common colds to severe acute respiratory syndrome. Pediatr. Infect. Dis. J. 23 (2004) 1049-1050
2. Bosch B.J., Bartelink W., and Rottier P.J.M. Cathepsin L functionally cleaves the severe acute respiratory syndrome coronavirus class I fusion protein upstream of rather than adjacent to the fusion peptide. J. Virol. 82 17 (2008) 8887-8890
3. Coughlin M., Lou G., Martinez O., Masterman S.K., Olsen O.A., Moksa A.A., Farzan M., Babcook J.S., and Prabhakar B.S. Generation and characterization of human monoclonal neutralizing antibodies with distinct binding and sequence features against SARS coronavirus using XenoMouse. Virology 361 1 (2007) 93-102
4. 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 1 (2005) 186-193
5. Duffy S., Shackelton L.A., and Holmes E.C. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9 (2008) 267-276
6. Golda A., and Pyrc K. Recent antiviral strategies against human coronavirus-related respiratory illnesses. Curr. Opin. Pulm. Med. 14 3 (2008) 248-253
7. Holmes E.C.a.A.R. Viral evolution and the emergence of SARS coronavirus. Phil. Trans. R. Soc. Lond. 359 (2004) 1059-1065
8. Huang I.C., Bosch B.J., Li F., Li W., Lee K.H., Ghiran S., Vasilieva N., Dermody T.S., Harrison S.C., Dormitzer P.R., Farzan M., Rottier P.J.M., and Choe H. SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J. Biol. Chem. 281 6 (2006) 3198-3203
9. Imai M., Sugimoto K., Okazaki K., and Kida H. Fusion of influenza virus with the endosomal membrane is inhibited by monoclonal antibodies to defined epitopes on the hemagglutinin. Virus Res. 53 (1998) 129-139
10. Ingallinella P., Bianchi E., Finotto M., Cantoni G., Eckert D.M., Supekar V.M., Bruchmann C., Carfi A., and Pessi A. Structural characterization of the fusion-active complex of severe acute respiratory syndrome (SARS) coronavirus. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 8709-8714
11. 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 6 (2005) 3289-3296
12. Knudsen T., Kledal T.N., Andersen O., Eugene-Olsen J., and Kristiansen T.B. Severe acute respiratory syndrome-a new coronavirus in the Chinese dragon's lair. Scand. J. Immunol. 58 (2003) 277-284
13. Ksiazek T.G., Erdman D., Goldsmith C.S., Zaki S.R., Peret T., Emery S., Tong S., Urbani C., Comer J.A., Lim W., Rollin P.E., Dowell S.F., Ling A.E., Humphrey C.D., Shieh W.J., Guarner J., Paddock C.D., Rota P., Fields B., DeRisi J., Yang J.Y., Cox N., Hughes J.M., LeDuc J.W., Bellini W.J., and Anderson L.J. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348 20 (2003) 1953-1966
14. Ksizek T.G., Erdman D., Goldsmith C.S., Zaki S.R., Peret T., Emery S., Tong S., Urbani C., Comer J.A., Lim W., Rollin P.E., Dowell S.F., Ling A.E., Humphrey C.D., Shieh W.J., Guarner J., Paddock C.D., Rota P., Fields B., DeRisi J., Yang J.Y., Cox N., Hughes J.M., LeDuc J.W., Bellini W.J., Anderson L.J., and and the SARS Working Group. A novel coronavirus associated with severe acute respiratory syndrome. N. Eng. J. Med. 348 (2003) 1953-1966
15. Kuiken T., Fouchier R.A.M., Schutten M., Rimmelzwann G.F., van Amerongen G., van Riel D., Laman J.D., de Jong T., van Doornum G., Lim W., Ling A.E., Chan P.K.S., Tam J.S., Zambon M.C., Gopal R., Drosten C., van der Werf S., Escriou N., Manuguerra J.C., Stohr K., Malik Peiris J.S., and Osterhaus A.D.M.E. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362 9380 (2003) 263-270
16. Lai M.M.C. SARS virus: the beginning of the unraveling of a new coronavirus. J. Biomed. Sci. 10 (2003) 664-675
17. Lau S.K.P., Woo P.C.Y., Li K.S.M., Huang Y., Tsoi H., Wong B.H.L., Wong S.S.Y., Leung S., Chan K., and Yuen K. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 14040-14045
18. Li F., Li W., Farzan M., and Harrison S.C. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309 5742 (2005) 1864-1868
19. 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. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426 6965 (2003) 450-454
20. 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. Bats are the natural reservoirs of SARS-like coronaviruses. Science 310 (2005) 676-679
21. Marasco W.A.A.J.S. The growth and potential of human antiviral monoclonal antibody therapeutics. Nat. Biotechnol. 25 12 (2007) 1421-1434
22. 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. The genome sequence of the SARS-associated coronavirus. Science 300 5624 (2003) 1399-1404
23. Meulen J.t., van den Brink E.N., Poon L.L.M., Marrisen W.E., Leung C.S.W., Cox F., Cheung C.Y., Bakker A.Q., Bogaards J.A., van Deventer E., Preiser W., Doerr H.W., Chow V.T., de Kruif J., Peiris J.S.M., and Goudsmit J. Human monoclonal antibody combination against SARS coronavirus: synergy and coverage of escape mutants. PLoS. Med. 3 7 (2006) 1071-1079
24. Mitsuki Y.Y., Ohnishi K., Takagi H., Oshima M., Yamamoto T., Mizukoshi F., Terahara K., Kobayashi K., Yamamoto N., Yamaoka S., and Tsunetsugu-Yokota Y. A single amino acid substitution in the S1 and S2 Spike protein domains determines the neutralization escape phenotype of SARS-CoV. Microbes. Infect. 10 8 (2008) 908-915
25. Normile D. Researchers tie deadly SARS virus to bats. Science 309 (2005) 2154-2155
26. Osterhaus A.D.M.E. New respiratory viruses of humans. Pediatr. Infect. Dis. J. 27 10 (2008) S71-S74
27. Peiris J., Guan Y., and Yuen K.Y. Severe acute respiratory syndrome. Nat. Med. 12 (2004) S88-S97
28. Rockx B., Corti D., Donaldson E., Sheahan T., Stadler K., Lanzavecchia A., and Baric R. Structural basis for potent cross-neutralizing human monoclonal antibody protection against lethal human and zoonotic severe acute respiratory syndrome coronavirus challenge. J. Virol. 82 7 (2008) 3220-3235
29. Rockx B., Sheahan T., Donaldson E., Harkema J., Sims A., Heise M., Pickles R., Cameron M., Kelvin D., and Baric R. Synthetic reconstruction of zoonotic and early human severe acute respiratory syndrome coronavirus isolates that produce fatal disease in aged mice. J. Virol. 81 14 (2007) 7410-7423
30. Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., Penaranda S., Bankamp B., Maher K., Chen M.H., Tong S., Tamin A., Lowe L., Frace M., DeRisi J.L., Chen Q., Wang D., Erdman D.D., Peret T.C., Burns C., Ksiazek T.G., Rollin P.E., Sanchez A., Liffick S., Holloway B., Limor J., McCaustland K., Olsen-Rasmussen M., Fouchier R., Gunther S., Osterhaus A.D., Drosten C., Pallansch M.A., Anderson L.J., and Bellini W.J. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300 5624 (2003) 1394-1399
31. Simmons G., Gosalia D.N., Rennekamp A.J., Reeves J.D., Diamond S.L., and Bates A.P. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad Sci. U.S.A. 102 33 (2005) 11876-11881
32. Simmons G., Reeves J.D., Rennekamp A.J., Amberg S.M., Piefer A.J., and Bates P. Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. PNAS 101 12 (2004) 4240-4245
33. Sui J., Aird D.R., Tamin A., Murakami A., Yan M., Yammanuru A., Jing H., Kan B., Zhu Q., Yuan A.a., Adams G.P., Bellini W.J., Xu J., Anderson L.J., and Marasco W.A. Broadening of neutralization activity to directly block a dominant antibody-driven SARS-coronavirus evolution pathway. PLos. Pathogens. 4 11 (2008)
34. Sui J., Li W., Murakami A., Tamin A., Matthews L.J., Wong S.K., Moore M.J., Tallarico A.S., Olurinde M., Choe H., Anderson L.J., Bellini W.J., Farzan M., and Marasco W.A. Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc. Natl. Acad Sci. U.S.A. 101 8 (2004) 2536-2541
35. Sui J., Li W., Roberts A., Matthews L.J., Murakami A., Vogel L., Wong S.K., Subbarao K., Farzan M., and Marasco W.A. Evaluation of human monoclonal antibody 80R for immunoprophylaxis of severe acute respiratory syndrome by an animal study, epitope mapping, and analysis of spike variants. J. Virol. 79 10 (2005) 5900-5906
36. ter Meulen J., van den Brink E.N., Poon L.L., Marissen W.E., Leung C.S., Cox F., Cheung C.Y., Bakker A.Q., Bogaards J.A., van Deventer E., Preiser W., Doerr H.W., Chow V.T., de Kruif J., Peiris J.S., and Goudsmit J. Human monoclonal antibody combination against SARS coronavirus: synergy and coverage of escape mutants. PLoS. Med. 3 7 (2006) e237
37. Thompson B.S., Moesker B., Smit J.M., Wilschut J., Diamond M.S., and Fremont D.H. A therapeutic antibody against West Nile virus neutralizes infection by blocking fusion within endosomes. PLos. Pathogens. 5 5 (2009) 1-10
38. Tian Q., Liu Y.N., Xie L.X., Fan B.X., Xu H.M., and Chen W.J. Comparative study of clinical characteristics and prognosis of clinically diagnosed SARS patients with positive and negative serum SARS coronavirus-specific antibodies test. Zhonghua Yi Xue Za Zhi 84 8 (2004) 642-645
39. Tripet B., Howards M.W., Joblings M., Holmes R.K., Holmes K.V., and Hodges R.S. Structural characterization of the SARS-coronavirus spike S fusion protein core. J. Biol. Chem 279 (2004) 20836-20849
40. Wong S.K., Li W., Moore M.J., Choe H., and Farzan M. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 279 5 (2004) 3197-3201
41. Xiao X., Chakraborti S., Dimitrov A.S., Gramatikoff K., and Dimitrov D.S. The SARS-CoV S glycoprotein: expression and functional characterization. Biochem. Biophys. Res. Commun. 312 4 (2003) 1159-1164
42. Xiao X., Feng Y., Chakraorti S., and Dimitorv D.S. Oligomerization of the SARS-CoV S glycoprotein: dimerization of the N-terminus and trimerization of the ectodomain. Biochem. Biophys. Res. Commun. 322 (2004) 93-99
43. Yang Y.H., Huang Y.H., Chuang Y.H., Peng C.M., Wang L.C., Lin Y.T., and Chiang B.L. Autoantibodies against human epithelial cells and endothelial cells after severe acute respiratory syndrome (SARS)-associated coronavirus infection. J. Med. Virol. 77 1 (2005) 1-7
44. Yang Z.Y., Werner H.C., Kong W.P., Leung K., Traggiai E., Lanzavecchia A., and Nabel G.J. Evasion of antibody neutralization in emerging severe acute respiratory syndrome coronaviruses. Proc. Natl. Acad. Sci. U.S.A. 102 3 (2005) 797-801
45. Yi C.E., Ba L., Zhang L., Ho D.D., and Chen Z. Single amino acid substitutions in the severe acute respiratory syndrome coronavirus spike glycoprotein determine viral entry and immunogenicity of a major neutralizing domain. J. Virol. 79 18 (2005) 11638-11646