Resistance analysis of an antibody that selectively inhibits dengue virus serotype-1

Antiviral Research

Volumn 95, Issue 3, 2012, Pages 216-223

  Zou, Gang ^a,e   Kukkaro, Petra ^b,c   Lok, Shee Mei ^b,c   Ng, Jowin K W ^c   Tan, Grace K ^c   Hanson, Brendon J ^d   Alonso, Sylvie ^c   MacAry, Paul A ^c   Shi, Pei Yong ^a  

^a Novartis Institute for Tropical Diseases   (Singapore)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d DSO NATIONAL LABORATORIES   (Singapore)

^e INSTITUTE PASTEUR OF SHANGHAI   (China)

Author keywords

Dengue virus; Escape mutant; Flavivirus envelope protein; Neutralizing antibody; Virus entry

Indexed keywords

ANTIVIRUS AGENT; EPITOPE; HUMAN MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY HM 14C10; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ANTIVIRAL RESISTANCE; ARTICLE; DENGUE VIRUS 1; HINGE REGION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VIRUS ISOLATION; VIRUS MUTANT; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS RESISTANCE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CELL LINE; DENGUE VIRUS; DNA MUTATIONAL ANALYSIS; DRUG RESISTANCE, VIRAL; HUMANS; MICE; MICROBIAL SENSITIVITY TESTS; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN BINDING; VIRAL ENVELOPE PROTEINS;

DENGUE VIRUS; FLAVIVIRUS;

EID: 84864144309     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2012.06.010     Document Type: Article

References (37)

1. Allison S.L., Schalich J., Stiasny K., Mandl C.W., Heinz F.X. Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J. Virol. 2001, 75:4268-4275.
2. Balsitis S.J., Williams K.L., Lachica R., Flores D., Kyle J.L., Mehlhop E., Johnson S., Diamond M.S., Beatty P.R., Harris E. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog. 2010, 6:e1000790.
3. Bressanelli S., Stiasny K., Allison S.L., Stura E.A., Duquerroy S., Lescar J., Heinz F.X., Rey F.A. Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J. 2004, 23:728-738.
4. Brien J.D., Austin S.K., Sukupolvi-Petty S., O'Brien K.M., Johnson S., Fremont D.H., Diamond M.S. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J. Virol. 2010, 84:10630-10643.
5. Chambers T.J., Hahn C.S., Galler R., Rice C.M. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 1990, 44:649-688.
6. Crill W.D., Roehrig J.T. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J. Virol. 2001, 75:7769-7773.
7. Dejnirattisai W., Jumnainsong A., Onsirisakul N., Fitton P., Vasanawathana S., Limpitikul W., Puttikhunt C., Edwards C., Duangchinda T., Supasa S., Chawansuntati K., Malasit P., Mongkolsapaya J., Screaton G. Cross-reacting antibodies enhance dengue virus infection in humans. Science 2010, 328:745-748.
8. Dong H., Chang D.C., Xie X., Toh Y.X., Chung K.Y., Zou G., Lescar J., Lim S.P., Shi P.Y. Biochemical and genetic characterization of dengue virus methyltransferase. Virology 2010, 405:568-578.
9. Gubler D., Kuno G., Markoff L. Flavivirus. Fields virology 2007, Lippincott William, Philadelphia, 1153-1253. fifth edition.
10. Guzman M.G., Halstead S.B., Artsob H., Buchy P., Farrar J., Gubler D.J., Hunsperger E., Kroeger A., Margolis H.S., Martinez E., Nathan M.B., Pelegrino J.L., Simmons C., Yoksan S., Peeling R.W. Dengue: a continuing global threat. Nat. Rev. Microbiol. 2010, 8:S7-S16.
11. Hsieh S.C., Zou G., Tsai W.Y., Qing M., Chang G.J., Shi P.Y., Wang W.K. The C-terminal helical domain of dengue virus precursor membrane protein is involved in virus assembly and entry. Virology 2011, 410:170-180.
12. Hurrelbrink R.J., McMinn P.C. Attenuation of Murray Valley encephalitis virus by site-directed mutagenesis of the hinge and putative receptor-binding regions of the envelope protein. J. Virol. 2001, 75:7692-7702.
13. Kuhn R., Zhang W., Rossmann M., Pletnev S., Corver J., Lenches E., Jones C., Mukhopadhyay S., Chipman P., Strauss E. Structure of dengue virus implications for flavivirus organization, maturation, and fusion. Cell 2002, 108:717-725.
14. Lai C.J., Goncalvez A.P., Men R., Wernly C., Donau O., Engle R.E., Purcell R.H. Epitope determinants of a chimpanzee dengue virus type 4 (DENV-4)-neutralizing antibody and protection against DENV-4 challenge in mice and rhesus monkeys by passively transferred humanized antibody. J. Virol. 2007, 81:12766-12774.
15. Lee E., Hall R.A., Lobigs M. Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J. Virol. 2004, 78:8271-8280.
16. Lindenbach B.D., Thiel H.J., Rice C.M. Flaviviridae: the virus and their replication. Fields virology 2007, Lippincott William, Philadelphia, 1101-1151. fifth edition.
17. Lok S.M., Kostyuchenko V., Nybakken G.E., Holdaway H.A., Battisti A.J., Sukupolvi-Petty S., Sedlak D., Fremont D.H., Chipman P.R., Roehrig J.T., Diamond M.S., Kuhn R.J., Rossmann M.G. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Biol. 2008, 15:312-317.
18. Modis Y., Ogata S., Clements D., Harrison S.C. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004, 427:313-319.
19. Modis Y., Ogata S., Clements D., Harrison S.C. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 2005, 79:1223-1231.
20. Noble C.G., Chen Y.L., Dong H., Gu F., Lim S.P., Schul W., Wang Q.Y., Shi P.Y. Strategies for development of Dengue virus inhibitors. Antiviral Res. 2010, 85:450-462.
21. Pierson T.C., Fremont D.H., Kuhn R.J., Diamond M.S. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 2008, 4:229-238.
22. Rajamanonmani R., Nkenfou C., Clancy P., Yau Y.H., Shochat S.G., Sukupolvi-Petty S., Schul W., Diamond M.S., Vasudevan S.G., Lescar J. On a mouse monoclonal antibody that neutralizes all four dengue virus serotypes. J. Gen. Virol. 2009, 90:799-809.
23. Rey F.A., Heinz F.X., Mandl C., Kunz C., Harrison S.C. The envelope glycoprotein from tick-borne encephalitis virus at 2A resolution. Nature 1995, 375:291-298.
24. Roehrig J.T., Staudinger L.A., Hunt A.R., Mathews J.H., Blair C.D. Antibody prophylaxis and therapy for flavivirus encephalitis infections. Ann. NY Acad. Sci. 2001, 951:286-297.
25. Schul W., Liu W., Xu H.Y., Flamand M., Vasudevan S.G. A dengue fever viremia model in mice shows reduction in viral replication and suppression of the inflammatory response after treatment with antiviral drugs. J. Infect. Dis. 2007, 195:665-674.
26. Shadman K.A., Wald E.R. A review of palivizumab and emerging therapies for respiratory syncytial virus. Expert Opin. Biol. Ther. 2011, 11:1455-1467.
27. Shi P.Y., Tilgner M., Lo M.K., Kent K.A., Bernard K.A. Infectious cDNA clone of the epidemic West Nile virus from New York city. J. Virol. 2002, 76:5847-5856.
28. Shrestha B., Brien J.D., Sukupolvi-Petty S., Austin S.K., Edeling M.A., Kim T., O'Brien K.M., Nelson C.A., Johnson S., Fremont D.H., Diamond M.S. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog. 2010, 6:e1000823.
29. Sukupolvi-Petty S., Austin S.K., Engle M., Brien J.D., Dowd K.A., Williams K.L., Johnson S., Rico-Hesse R., Harris E., Pierson T.C., Fremont D.H., Diamond M.S. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J. Virol. 2010, 84:9227-9239.
30. Teoh, E.P., Kukkaro, P., Teo, E.W., Lim, A.P., Tan, T.T., Yip, A., Schul, W., Aung, M., Kostyuchenko, V.A., Leo, Y.S., Chan, S.H., Smith, K.G., Chan, A.H., Zou, G., Ooi, E.E., Kemeny, M., Tan, G.K., Ng, J.K., Ng, M.L., Alonso, S., Fisher, D., Shi, P.Y., Hanson, B.J., Lok, S.M., MacAry, P.A., 2012. The Structural Basis for Serotype-Specific Neutralization of Dengue Virus by a Natural Human Antibody. Sci TM. 20, 139ra83.
31. Valdes K., Alvarez M., Pupo M., Vazquez S., Rodriguez R., Guzman M.G. Human Dengue antibodies against structural and nonstructural proteins. Clin. Diagn. Lab. Immunol. 2000, 7:856-857.
32. van den Broek M.F., Muller U., Huang S., Aguet M., Zinkernagel R.M. Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. J. Virol. 1995, 69:4792-4796.
33. Whitehead S.S., Blaney J.E., Durbin A.P., Murphy B.R. Prospects for a dengue virus vaccine. Nat. Rev. Microbiol. 2007, 5:518-528.
34. Zhang S., Vogt M.R., Oliphant T., Engle M., Bovshik E.I., Diamond M.S., Beasley D.W. Development of resistance to passive therapy with a potently neutralizing humanized monoclonal antibody against West Nile virus. J. Infect. Dis. 2009, 200:202-205.
35. Zhang Y., Zhang W., Ogata S., Clements D., Strauss J.H., Baker T.S., Kuhn R.J., Rossmann M.G. Conformational changes of the flavivirus E glycoprotein. Structure 2004, 12:1607-1618.
36. Zhou Y., Ray D., Zhao Y., Dong H., Ren S., Li Z., Guo Y., Bernard K.A., Shi P.Y., Li H. Structure and function of flavivirus NS5 methyltransferase. J. Virol. 2007, 81:3891-3903.
37. Zou G., Chen Y.L., Dong H., Lim C.C., Yap L.J., Yau Y.H., Shochat S.G., Lescar J., Shi P.Y. Functional analysis of two cavities in flavivirus NS5 polymerase. J. Biol. Chem. 2011, 286:14362-14372.