Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2

Journal of Virology

Volumn 84, Issue 18, 2010, Pages 9227-9239

  Sukupolvi Petty, Soila ^a   Austin, S Kyle ^a   Engle, Michael ^a   Brien, James D ^a   Dowd, Kimberly A ^b   Williams, Katherine L ^c   Johnson, Syd ^d   Rico Hesse, Rebeca ^e   Harris, Eva ^c   Pierson, Theodore C ^b   Fremont, Daved H ^a   Diamond, Michael S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MacroGenics Inc   (United States)

^e SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DV2 104 MONOCLONAL ANTIBODY; DV2 106 MONOCLONAL ANTIBODY; DV2 16 MONOCLONAL ANTIBODY; DV2 29 MONOCLONAL ANTIBODY; DV2 30 MONOCLONAL ANTIBODY; DV2 34 MONOCLONAL ANTIBODY; DV2 36 MONOCLONAL ANTIBODY; DV2 40 MONOCLONAL ANTIBODY; DV2 44 MONOCLONAL ANTIBODY; DV2 46 MONOCLONAL ANTIBODY; DV2 47 MONOCLONAL ANTIBODY; DV2 48 MONOCLONAL ANTIBODY; DV2 51 MONOCLONAL ANTIBODY; DV2 52 MONOCLONAL ANTIBODY; DV2 53 MONOCLONAL ANTIBODY; DV2 58 MONOCLONAL ANTIBODY; DV2 67 MONOCLONAL ANTIBODY; DV2 70 MONOCLONAL ANTIBODY; DV2 73 MONOCLONAL ANTIBODY; DV2 76 MONOCLONAL ANTIBODY; DV2 77 MONOCLONAL ANTIBODY; DV2 87 MONOCLONAL ANTIBODY; DV2 96 MONOCLONAL ANTIBODY; ENVELOPE PROTEIN; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; E-GLYCOPROTEIN, DENGUE VIRUS TYPE 2; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CELL STRAIN HEK293; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 2; DRUG PROTEIN BINDING; GENOTYPE; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEROTYPE; VIRUS NEUTRALIZATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL LINE; CHEMICAL STRUCTURE; DENGUE VIRUS; DNA SEQUENCE; EPITOPE MAPPING; GENETICS; HAMSTER; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; MOLECULAR GENETICS; PROCEDURES; PROTEIN TERTIARY STRUCTURE; SERODIAGNOSIS; STRUCTURE ACTIVITY RELATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; BINDING SITES; CELL LINE; CRICETINAE; DENGUE; DENGUE VIRUS; EPITOPE MAPPING; HUMANS; IMMUNOTHERAPY; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL ENVELOPE PROTEINS;

EID: 77956031215     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01087-10     Document Type: Article

References (73)

1. Ansarah-Sobrinho, C., S. Nelson, C. A. Jost, S. S. Whitehead, and T. C. Pierson. 2008. Temperature-dependent production of pseudoinfectious dengue reporter virus particles by complementation. Virology 381:67-74.
2. Balsitis, S. J., K. L. Williams, R. Lachica, D. Flores, J. L. Kyle, E. Mehlhop, S. Johnson, M. S. Diamond, P. R. Beatty, and E. Harris. 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog. 6:e1000790.
3. Beasley, D. W., and J. G. Aaskov. 2001. Epitopes on the dengue 1 virus envelope protein recognized by neutralizing IgM monoclonal antibodies. Virology 279:447-458.
4. Beasley, D. W., and A. D. Barrett. 2002. Identification of neutralizing epitopes within structural domain III of the West Nile virus envelope protein. J. Virol. 76:13097-13100.
5. Bhardwaj, S., M. Holbrook, R. E. Shope, A. D. Barrett, and S. J. Watowich. 2001. Biophysical characterization and vector-specific antagonist activity of domain III of the tick-borne flavivirus envelope protein. J. Virol. 75:4002-4007.
6. Chen, Z., L. M. Liu, N. Gao, X. F. Xu, J. L. Zhang, J. L. Wang, and J. An. 2009. Passive protection assay of monoclonal antibodies against dengue virus in suckling mice. Curr. Microbiol. 58:326-331.
7. Cherrier, M. V., B. Kaufmann, G. E. Nybakken, S. M. Lok, J. T. Warren, B. R. Chen, C. A. Nelson, V. A. Kostyuchenko, H. A. Holdaway, P. R. Chipman, R. J. Kuhn, M. S. Diamond, M. G. Rossmann, and D. H. Fremont. 2009. Structural basis for the preferential binding of immature flaviviruses by a fusion-loop antibody. EMBO J. 28:3269-3276.
8. Crill, W. D., and G. J. Chang. 2004. Localization and characterization of flavivirus envelope glycoprotein cross-reactive epitopes. J. Virol. 78:13975-13986.
9. Crill, W. D., N. B. Trainor, and G. J. Chang. 2007. A detailed mutagenesis study of flavivirus cross-reactive epitopes using West Nile virus-like particles. J. Gen. Virol. 88:1169-1174.
10. Diamond, M. S., B. Shrestha, A. Marri, D. Mahan, and M. Engle. 2003. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J. Virol. 77:2578-2586.
11. Durbin, A. P., and S. S. Whitehead. 2010. Dengue vaccine candidates in development. Curr. Top. Microbiol. Immunol. 338:129-143.
12. Feighny, R., J. Burrous, and R. Putnak. 1994. Dengue type-2 virus envelope protein made using recombinant baculovirus protects mice against virus challenge. Am. J. Trop. Med. Hyg. 50:322-328.
13. Gollins, S., and J. Porterfield. 1984. Flavivirus infection enhancement in macrophages: radioactive and biological studies on the effect of antibody and viral fate. J. Gen. Virol. 65:1261-1272.
14. Goncalvez, A. P., C. H. Chien, K. Tubthong, I. Gorshkova, C. Roll, O. Donau, P. Schuck, S. Yoksan, S. D. Wang, R. H. Purcell, and C. J. Lai. 2008. Humanized monoclonal antibodies derived from chimpanzee Fabs protect against Japanese encephalitis virus in vitro and in vivo. J. Virol. 82:7009-7021.
15. Goncalvez, A. P., R. H. Purcell, and C. J. Lai. 2004. Epitope determinants of a chimpanzee Fab antibody that efficiently cross-neutralizes dengue type 1 and type 2 viruses map to inside and in close proximity to fusion loop of the dengue type 2 virus envelope glycoprotein. J. Virol. 78:12919-12928.
16. Gromowski, G. D., and A. D. Barrett. 2007. Characterization of an antigenic site that contains a dominant, type-specific neutralization determinant on the envelope protein domain III (ED3) of dengue 2 virus. Virology 366:349-360.
17. Gromowski, G. D., N. D. Barrett, and A. D. Barrett. 2008. Characterization of dengue virus complex-specific neutralizing epitopes on envelope protein domain III of dengue 2 virus. J. Virol. 82:8828-8837.
18. Halstead, S. B. 1994. Antibody-dependent enhancement of infection: a mechanism for indirect virus entry into cells, p. 493-516. In E. Wimmer (ed.), Cellular receptors for animal viruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
19. Halstead, S. B. 1989. Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenetic cascade. Rev. Infect. Dis. 11(Suppl. 4): S830-S839.
20. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
21. Holmes, E. C., and S. S. Twiddy. 2003. The origin, emergence and evolutionary genetics of dengue virus. Infect. Genet. Evol. 3:19-28.
22. Hooper, D. C., T. W. Phares, M. J. Fabis, and A. Roy. 2009. The production of antibody by invading B cells is required for the clearance of rabies virus from the central nervous system. PLoS Negl. Trop. Dis. 3:e535.
23. Hung, S. L., P. L. Lee, H. W. Chen, L. K. Chen, C. L. Kao, and C. C. King. 1999. Analysis of the steps involved in dengue virus entry into host cells. Virology 257:156-167.
24. Johnson, A. J., and J. T. Roehrig. 1999. New mouse model for dengue virus vaccine testing. J. Virol. 73:783-786.
25. Kaufman, B. M., P. L. Summers, D. R. Dubois, and K. H. Eckels. 1987. Monoclonal antibodies against dengue 2 virus E-glycoprotein protect mice against lethal dengue infection. Am. J. Trop. Med. Hyg. 36:427-434.
26. Kuhn, R. J., W. Zhang, M. G. Rossmann, S. V. Pletnev, J. Corver, E. Lenches, C. T. Jones, S. Mukhopadhyay, P. R. Chipman, E. G. Strauss, T. S. Baker, and J. H. Strauss. 2002. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717-725.
27. Lai, C. J., A. P. Goncalvez, R. Men, C. Wernly, O. Donau, R. E. Engle, and R. H. Purcell. 2007. 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 anti-body. J. Virol. 81:12766-12774.
28. Leitmeyer, K. C., D. W. Vaughn, D. M. Watts, R. Salas, I. Villalobos de Chacon, C. Ramos, and R. Rico-Hesse. 1999. Dengue virus structural differences that correlate with pathogenesis. J. Virol. 73:4738-4747.
29. Li, L., S. M. Lok, I. M. Yu, Y. Zhang, R. J. Kuhn, J. Chen, and M. G. Rossmann. 2008. The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319:1830-1834.
30. Lisova, O., F. Hardy, V. Petit, and H. Bedouelle. 2007. Mapping to completeness and transplantation of a group-specific, discontinuous, neutralizing epitope in the envelope protein of dengue virus. J. Gen. Virol. 88:2387-2397.
31. Lok, S. M., V. Kostyuchenko, G. E. Nybakken, H. A. Holdaway, A. J. Battisti, S. Sukupolvi-Petty, D. Sedlak, D. H. Fremont, P. R. Chipman, J. T. Roehrig, M. S. Diamond, R. J. Kuhn, and M. G. Rossmann. 2008. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Biol. 15:312-317.
32. Mandl, C. W., F. Guirakhoo, H. Holzmann, F. X. Heinz, and C. Kunz. 1989. Antigenic structure of the flavivirus envelope protein E at the molecular level, using tick-borne encephalitis virus as a model. J. Virol. 63:564-571.
33. Matsui, K., G. D. Gromowski, L. Li, A. J. Schuh, J. C. Lee, and A. D. Barrett. 2009. Characterization of dengue complex-reactive epitopes on dengue 3 virus envelope protein domain III. Virology 384:16-20.
34. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2003. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 100:6986-6991.
35. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313-319.
36. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2005. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 79:1223-1231.
37. Mondotte, J. A., P. Y. Lozach, A. Amara, and A. V. Gamarnik. 2007. Essential role of dengue virus envelope protein N glycosylation at asparagine-67 during viral propagation. J. Virol. 81:7136-7148.
38. Navarro-Sanchez, E., R. Altmeyer, A. Amara, O. Schwartz, F. Fieschi, J. L. Virelizier, F. Arenzana-Seisdedos, and P. Despres. 2003. Dendritic-cell- specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep. 4:723-728. (Pubitemid 36974759)
39. Nayak, V., M. Dessau, K. Kucera, K. Anthony, M. Ledizet, and Y. Modis. 2009. Crystal structure of dengue virus type 1 envelope protein in the post-fusion conformation and its implications for membrane fusion. J. Virol. 83:4338-4344.
40. Nelson, S., C. A. Jost, Q. Xu, J. Ess, J. E. Martin, T. Oliphant, S. S. Whitehead, A. P. Durbin, B. S. Graham, M. S. Diamond, and T. C. Pierson. 2008. Maturation of West Nile virus modulates sensitivity to antibody-mediated neutralization. PLoS Pathog. 4:e1000060.
41. Noueiry, A. O., P. D. Olivo, U. Slomczynska, Y. Zhou, B. Buscher, B. Geiss, M. Engle, R. M. Roth, K. M. Chung, M. Samuel, and M. S. Diamond. 2007. Identification of novel small-molecule inhibitors of West Nile virus infection. J. Virol. 81:11992-12004.
42. Oliphant, T., M. Engle, G. Nybakken, C. Doane, S. Johnson, L. Huang, S. Gorlatov, E. Mehlhop, A. Marri, K. M. Chung, G. D. Ebel, L. D. Kramer, D. H. Fremont, and M. S. Diamond. 2005. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat. Med. 11:522-530.
43. Oliphant, T., G. E. Nybakken, M. Engle, Q. Xu, C. A. Nelson, S. Sukupolvi- Petty, A. Marri, B. E. Lachmi, U. Olshevsky, D. H. Fremont, T. C. Pierson, and M. S. Diamond. 2006. Antibody recognition and neutralization determinants on domains I and II of West Nile virus envelope protein. J. Virol. 80:12149-12159.
44. Pierson, T. C., and M. S. Diamond. 2008. Molecular mechanisms of anti-body- mediated neutralization of flavivirus infection. Exp. Rev. Mol. Med. 10:e12.
45. Pierson, T. C., M. Sanchez, B. A. Puffer, A. A. Ahmed, L. E. Valentine, L. Altamura, M. S. Diamond, and R. W. Doms. 2006. A rapid and quantitative assay for measuring antibody-mediated neutralization of West Nile virus. Virology 346:53-65.
46. Pokidysheva, E., Y. Zhang, A. J. Battisti, C. M. Bator-Kelly, P. R. Chipman, C. Xiao, G. G. Gregorio, W. A. Hendrickson, R. J. Kuhn, and M. G. Rossmann. 2006. Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124:485-493.
47. Rajamanonmani, R., C. Nkenfou, P. Clancy, Y. H. Yau, S. G. Shochat, S. Sukupolvi-Petty, W. Schul, M. S. Diamond, S. G. Vasudevan, and J. Lescar. 2009. On a mouse monoclonal antibody that neutralizes all four dengue virus serotypes. J. Gen. Virol. 90:799-809.
48. Rico-Hesse, R. 2003. Microevolution and virulence of dengue viruses. Adv. Virus Res. 59:315-341.
49. Rico-Hesse, R. 1990. Molecular evolution and distribution of dengue viruses type 1 and 2 in nature. Virology 174:479-493. (Pubitemid 20060152)
50. Roehrig, J. T., R. A. Bolin, and R. G. Kelly. 1998. Monoclonal antibody mapping of the envelope glycoprotein of the dengue 2 virus, Jamaica. Virology 246:317-328.
51. Sanchez, I. J., and B. H. Ruiz. 1996. A single nucleotide change in the E protein gene of dengue virus 2 Mexican strain affects neurovirulence in mice. J. Gen. Virol. 77(10):2541-2545.
52. Shresta, S., J. L. Kyle, H. M. Snider, M. Basavapatna, P. R. Beatty, and E. Harris. 2004. Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T- and B-cell-dependent immunity are less critical. J. Virol. 78:2701-2710.
53. Shrestha, B., J. D. Brien, S. Sukupolvi-Petty, S. K. Austin, M. A. Edeling, T. Kim, K. M. O'Brien, C. A. Nelson, S. Johnson, D. H. Fremont, and M. S. Diamond. 2010. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog. 6:e1000823.
54. Simmons, C. P., T. N. Chau, T. T. Thuy, N. M. Tuan, D. M. Hoang, N. T. Thien, B. Lien le, N. T. Quy, N. T. Hieu, T. T. Hien, C. McElnea, P. Young, S. Whitehead, N. T. Hung, and J. Farrar. 2007. Maternal antibody and viral factors in the pathogenesis of dengue virus in infants. J. Infect. Dis. 196: 416-424.
55. Simmons, M., K. R. Porter, C. G. Hayes, D. W. Vaughn, and R. Putnak. 2006. Characterization of antibody responses to combinations of a dengue virus type 2 DNA vaccine and two dengue virus type 2 protein vaccines in rhesus macaques. J. Virol. 80:9577-9585.
56. Stiasny, K., S. Brandler, C. Kossl, and F. X. Heinz. 2007. Probing the flavivirus membrane fusion mechanism by using monoclonal antibodies. J. Virol. 81:11526-11531.
57. Sukupolvi-Petty, S., S. K. Austin, W. E. Purtha, T. Oliphant, G. Nybakken, J. J. Schlesinger, J. T. Roehrig, G. D. Gromowski, A. D. Barrett, D. H. Fremont, and M. S. Diamond. 2007. Type- and subcomplex-specific neutralizing antibodies against domain III of dengue virus type 2 envelope protein recognize adjacent epitopes. J. Virol. 81:12816-12826.
58. Sultana, H., H. G. Foellmer, G. Neelakanta, T. Oliphant, M. Engle, M. Ledizet, M. N. Krishnan, N. Bonafe, K. G. Anthony, W. A. Marasco, P. Kaplan, R. R. Montgomery, M. S. Diamond, R. A. Koski, and E. Fikrig. 2009. Fusion loop peptide of the West Nile virus envelope protein is essential for pathogenesis and is recognized by a therapeutic cross-reactive human monoclonal antibody. J. Immunol. 183:650-660.
59. Tassaneetrithep, B., T. Burgess, A. Granelli-Piperno, C. Trumpfheller, J. Finke, W. Sun, M. Eller, K. Pattanapanyasat, S. Sarasombath, D. Birx, R. M. Steinman, S. Schlesinger, and M. Marovich. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197:823-829.
60. Thompson, B. S., B. Moesker, J. M. Smit, J. Wilschut, M. S. Diamond, and D. H. Fremont. 2009. A therapeutic antibody against West Nile virus neutralizes infection by blocking fusion within endosomes. PLoS Pathog. 5:e1000453.
61. Thullier, P., C. Demangel, H. Bedouelle, F. Megret, A. Jouan, V. Deubel, J. C. Mazie, and P. Lafaye. 2001. Mapping of a dengue virus neutralizing epitope critical for the infectivity of all serotypes: insight into the neutralization mechanism. J. Gen. Virol. 82:1885-1892.
62. Vasilakis, N., E. B. Fokam, C. T. Hanson, E. Weinberg, A. A. Sall, S. S. Whitehead, K. A. Hanley, and S. C. Weaver. 2008. Genetic and phenotypic characterization of sylvatic dengue virus type 2 strains. Virology 377:296-307.
63. Vogt, M. R., B. Moesker, J. Goudsmit, M. Jongeneelen, S. K. Austin, T. Oliphant, S. Nelson, T. C. Pierson, J. Wilschut, M. Throsby, and M. S. Diamond. 2009. Human monoclonal antibodies induced by natural infection against West Nile virus neutralize at a postattachment step. J. Virol. 83: 6494-6507.
64. Volk, D. E., D. W. Beasley, D. A. Kallick, M. R. Holbrook, A. D. Barrett, and D. G. Gorenstein. 2004. Solution structure and antibody binding studies of the envelope protein domain III from the New York strain of West Nile virus. J. Biol. Chem. 279:38755-38761.
65. Wahala, W. M., E. F. Donaldson, R. de Alwis, M. A. Accavitti-Loper, R. S. Baric, and A. M. de Silva. 2010. Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS Pathog. 6:e1000821.
66. Wengler, G. 1989. Cell-associated West Nile flavivirus is covered with E+pre-M protein heterodimers which are destroyed and reorganized by proteolytic cleavage during virus release. J. Virol. 63:2521-2526. (Pubitemid 19137526)
67. Whitehead, S. S., J. E. Blaney, A. P. Durbin, and B. R. Murphy. 2007. Prospects for a dengue virus vaccine. Nat. Rev. Microbiol. 5:518-528.
68. Wilder-Smith, A., and D. J. Gubler. 2008. Geographic expansion of dengue: the impact of international travel. Med. Clin. North Am. 92:1377-1390, x.
69. Yu, I. M., H. A. Holdaway, P. R. Chipman, R. J. Kuhn, M. G. Rossmann, and J. Chen. 2009. Association of the pr peptides with dengue virus at acidic pH blocks membrane fusion. J. Virol. 83:12101-12107.
70. Yu, I. M., W. Zhang, H. A. Holdaway, L. Li, V. A. Kostyuchenko, P. R. Chipman, R. J. Kuhn, M. G. Rossmann, and J. Chen. 2008. Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 319:1834-1837.
71. Yu, S., A. Wuu, R. Basu, M. R. Holbrook, A. D. Barrett, and J. C. Lee. 2004. Solution structure and structural dynamics of envelope protein domain III of mosquito- and tick-borne flaviviruses. Biochemistry 43:9168-9176.
72. Zellweger, R. M., T. R. Prestwood, and S. Shresta. 2010. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 7:128-139.
73. Zhang, Y., J. Corver, P. R. Chipman, W. Zhang, S. V. Pletnev, D. Sedlak, T. S. Baker, J. H. Strauss, R. J. Kuhn, and M. G. Rossmann. 2003. Structures of immature flavivirus particles. EMBO J. 22:2604-2613.