Structural insights into the neutralization mechanism of a higher primate antibody against dengue virus

EMBO Journal

Volumn 31, Issue 3, 2012, Pages 767-779

  Cockburn, Joseph J B ^a,b   Navarro Sanchez, M Erika ^a,b   Goncalvez, Ana P ^c   Zaitseva, Elena ^d   Stura, Enrico A ^e   Kikuti, Carlos M ^a,b   Duquerroy, Stéphane ^a,b   Dussart, Philippe ^f   Chernomordik, Leonid V ^d   Lai, Ching Juh ^c   Rey, Felix A ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c National Institute of Allergy and Infectious Diseases   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^f INSTITUT PASTEUR DE LA GUYANE   (French Guiana)

Author keywords

antibody; dengue; structure

Indexed keywords

EPITOPE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 5H2; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; ARTICLE; CHIMPANZEE; CRYSTAL STRUCTURE; DENGUE VIRUS; DRUG STRUCTURE; ENDOSOME; HUMAN; IMMUNOGENICITY; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; VIRUS NEUTRALIZATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, VIRAL; DENGUE VIRUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PRIMATES; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

DENGUE VIRUS; PAN; PRIMATES;

EID: 84856503943     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.439     Document Type: Article

References (56)

1. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL, Mehlhop E, Johnson S, Diamond MS, Beatty PR, Harris E (2010) Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e1000790
2. Beltramello M, Williams KL, Simmons CP, Macagno A, Simonelli L, Quyen NT, Sukupolvi-Petty S, Navarro-Sanchez E, Young PR, de Silva AM, Rey FA, Varani L, Whitehead SS, Diamond MS, Harris E, Lanzavecchia A, Sallusto F (2010) The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8: 271-283
3. Bressanelli S, Stiasny K, Allison SL, Stura EA, Duquerroy S, Lescar J, Heinz FX, Rey FA (2004) Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J 23: 728-738 (Pubitemid 38425440)
4. Bricogne G (1993) Direct phase determination by entropy maximization and likelihood ranking: status report and perspectives. Acta Crystallogr D Biol Crystallogr 49: 37-60
5. Brien JD, Austin SK, Sukupolvi-Petty S, O'Brien KM, Johnson S, Fremont DH, Diamond MS (2010) Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J Virol 84: 10630-10643
6. Brochet X, Lefranc MP, Giudicelli V (2008) IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res 36: W503-W508
7. Broennimann C, Eikenberry EF, Henrich B, Horisberger R, Huelsen G, Pohl E, Schmitt B, Schulze-Briese C, Suzuki M, Tomizaki T, Toyokawa H, Wagner A (2006) The PILATUS 1M detector. J Synchrotron Radiat 13: 120-130
8. Cherrier MV, Kaufmann B, Nybakken GE, Lok SM, Warren JT, Chen BR, Nelson CA, Kostyuchenko VA, Holdaway HA, Chipman PR, Kuhn RJ, Diamond MS, Rossmann MG, Fremont DH (2009) Structural basis for the preferential recognition of immature flaviviruses by a fusion-loop antibody. EMBO J 28: 3269-3276
9. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763
10. Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437: 69-87
11. Crill WD, Hughes HR, Delorey MJ, Chang GJ (2009) Humoral immune responses of dengue fever patients using epitope-specific serotype-2 virus-like particle antigens. PLoS One 4: e4991
12. Crill WD, Roehrig JT (2001) 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 75: 7769-7773 (Pubitemid 32738039)
13. Dussart P, Petit L, Labeau B, Bremand L, Leduc A, Moua D, Matheus S, Baril L (2008) Evaluation of two new commercial tests for the diagnosis of acute dengue virus infection using NS1 antigen detection in human serum. PLoS Negl Trop Dis 2: e280
14. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132 (Pubitemid 41742764)
15. Evans PR (2005) Scaling and assessment of data quality. Acta Crystallogr D 62: 72-85
16. Glamann J, Burton DR, Parren PW, Ditzel HJ, Kent KA, Arnold C, Montefiori D, Hirsch VM (1998) Simian immunodeficiency virus (SIV) envelope-specific Fabs with high-level homologous neutralizing activity: recovery from a long-term-nonprogressor SIVinfected macaque. J Virol 72: 585-592 (Pubitemid 28048875)
17. Gromowski GD, Barrett AD (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 (Pubitemid 47398915)
18. Halstead SB (2003) Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 60: 421-467 (Pubitemid 137639381)
19. Kabsch W (1988) Automatic indexing of rotation diffraction patterns. J App Cryst 21: 67-72
20. Kanai R, Kar K, Anthony K, Gould LH, Ledizet M, Fikrig E, Marasco WA, Koski RA, Modis Y (2006) Crystal structure of West Nile virus envelope glycoprotein reveals viral surface epitopes. J Virol 80: 11000-11008 (Pubitemid 44706541)
21. Kaufmann B, Chipman PR, Holdaway HA, Johnson S, Fremont DH, Kuhn RJ, Diamond MS, Rossmann MG (2009) Capturing a flavivirus pre-fusion intermediate. PLoS Pathog 5: e1000672
22. Kaufmann B, Nybakken GE, Chipman PR, Zhang W, Diamond MS, Fremont DH, Kuhn RJ, Rossmann MG (2006) West Nile virus in complex with the Fab fragment of a neutralizing monoclonal antibody. Proc Natl Acad Sci USA 103: 12400-12404 (Pubitemid 44267271)
23. Kaufmann B, Vogt MR, Goudsmit J, Holdaway HA, Aksyuk AA, Chipman PR, Kuhn RJ, Diamond MS, Rossmann MG (2010) Neutralization of West Nile virus by cross-linking of its surface proteins with Fab fragments of the human monoclonal antibody CR4354. Proc Natl Acad Sci USA 107: 18950-18955
24. Klungthong C, Zhang C, Mammen Jr MP, Ubol S, Holmes EC (2004) The molecular epidemiology of dengue virus serotype 4 in Bangkok, Thailand. Virology 329: 168-179 (Pubitemid 39346038)
25. Kobayashi T, Beuchat MH, Chevallier J, Makino A, Mayran N, Escola JM, Lebrand C, Cosson P, Gruenberg J (2002) Separation and characterization of late endosomal membrane domains. J Biol Chem 277: 32157-32164 (Pubitemid 34969029)
26. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, Lenches E, Jones CT, Mukhopadhyay S, Chipman PR, Strauss EG, Baker TS, Strauss JH (2002) Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108: 717-725 (Pubitemid 34241430)
27. Lai CJ, Goncalvez AP, Men R, Wernly C, Donau O, Engle RE, Purcell RH (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 antibody. J Virol 81: 12766-12774 (Pubitemid 350156914)
28. Lai CY, Tsai WY, Lin SR, Kao CL, Hu HP, King CC,Wu HC, Chang GJ, Wang WK (2008) Antibodies to envelope glycoprotein of dengue virus during the natural course of infection are predominantly cross-reactive and recognize epitopes containing highly conserved residues at the fusion loop of domain II. J Virol 82: 6631-6643
29. Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV (1992) Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J Clin Microbiol 30: 545-551
30. Lawrence MC, Colman PM (1993) Shape complementarity at protein/protein interfaces. J Mol Biol 234: 946-950 (Pubitemid 24027225)
31. Liao M, Sanchez-San Martin C, Zheng A, Kielian M (2010) In vitro reconstitution reveals key intermediate states of trimer formation by the dengue virus membrane fusion protein. J Virol 84: 5730-5740
32. Lindenbach BD, Rice CM (2001) The viruses and their replication. In Fields Virology, Knipe DM, Howley PM (eds), 4th edn, pp 991-1041. Philadelphia: Lippincott Williams and Wilkins
33. Lok SM, Kostyuchenko V, Nybakken GE, Holdaway HA, Battisti AJ, Sukupolvi-Petty S, Sedlak D, Fremont DH, Chipman PR, Roehrig JT, Diamond MS, Kuhn RJ, Rossmann MG (2008) Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat Struct Mol Biol 15: 312-317 (Pubitemid 351654038)
34. Men R, Yamashiro T, Goncalvez AP, Wernly C, Schofield DJ, Emerson SU, Purcell RH, Lai CJ (2004) Identification of chimpanzee Fab fragments by repertoire cloning and production of a full-length humanized immunoglobulin G1 antibody that is highly efficient for neutralization of dengue type 4 virus. J Virol 78: 4665-4674 (Pubitemid 38501088)
35. Modis Y, Ogata S, Clements D, Harrison SC (2003) A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci USA 100: 6986-6991 (Pubitemid 36706380)
36. Modis Y, Ogata S, Clements D, Harrison SC (2004) Structure of the dengue virus envelope protein after membrane fusion. Nature 427: 313-319 (Pubitemid 38133652)
37. Modis Y, Ogata S, Clements D, Harrison SC (2005) Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J Virol 79: 1223-1231 (Pubitemid 40053904)
38. Monath TP (1994) Dengue: the risk to developed and developing countries. Proc Natl Acad Sci USA 91: 2395-2400 (Pubitemid 24139356)
39. Nayak V, Dessau M, Kucera K, Anthony K, Ledizet M, Modis Y (2009) Crystal structure of dengue virus type 1 envelope protein in the postfusion conformation and its implications for membrane fusion. J Virol 83: 4338-4344
40. Nybakken GE, Nelson CA, Chen BR, Diamond MS, Fremont DH (2006) Crystal structure of the West Nile virus envelope glycoprotein. J Virol 80: 11467-11474 (Pubitemid 44788862)
41. Nybakken GE, Oliphant T, Johnson S, Burke S, Diamond MS, Fremont DH (2005) Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 437: 764-769 (Pubitemid 41486548)
42. Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC (1995) The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375: 291-298
43. Sabin AB (1952) Research on dengue during World War II. Am J Trop Med Hyg 1: 30-50
44. Shrestha B, Brien JD, Sukupolvi-Petty S, Austin SK, Edeling MA, Kim T, O'Brien KM, Nelson CA, Johnson S, Fremont DH, Diamond MS (2010) The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog 6: e1000823
45. Stiasny K, Brandler S, Kossl C, Heinz FX (2007) Probing the flavivirus membrane fusion mechanism by using monoclonal antibodies. J Virol 81: 11526-11531 (Pubitemid 47536123)
46. Stiasny K, Kiermayr S, Holzmann H, Heinz FX (2006) Cryptic properties of a cluster of dominant flavivirus cross-reactive antigenic sites. J Virol 80: 9557-9568 (Pubitemid 44435631)
47. Sukupolvi-Petty S, Austin SK, Engle M, Brien JD, Dowd KA, Williams KL, Johnson S, Rico-Hesse R, Harris E, Pierson TC, Fremont DH, Diamond MS (2010) Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J Virol 84: 9227-9239
48. Sukupolvi-Petty S, Austin SK, Purtha WE, Oliphant T, Nybakken GE, Schlesinger JJ, Roehrig JT, Gromowski GD, Barrett AD, Fremont DH, Diamond MS (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 (Pubitemid 350156919)
49. Thompson BS, Moesker B, Smit JM, Wilschut J, Diamond MS, Fremont DH (2009) A therapeutic antibody against west nile virus neutralizes infection by blocking fusion within endosomes. PLoS Pathog 5: e1000453
50. Vagin AA, Teplyakov A (1997) MOLREP: an automated program for molecular replacement. J App Cryst 30: 1022-1025 (Pubitemid 127485985)
51. Van der Schaar HM, Rust MJ, Chen C, van der Ende-Metselaar H, Wilschut J, Zhuang X, Smit JM (2008) Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog 4: e1000244
52. Vogt MR, Moesker B, Goudsmit J, Jongeneelen M, Austin SK, Oliphant T, Nelson S, Pierson TC, Wilschut J, Throsby M, Diamond MS (2009) Human monoclonal antibodies against West Nile virus induced by natural infection neutralize at a postattachment step. J Virol 83: 6494-6507
53. Wahala WM, Donaldson EF, de Alwis R, Accavitti-Loper MA, Baric RS, de Silva AM (2010) Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS Pathog 6: e1000821
54. Wahala WM, Kraus AA, Haymore LB, Accavitti-Loper MA, de Silva AM (2009) Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody. Virology 392: 103-113
55. Zaitseva E, Yang ST, Melikov K, Pourmal S, Chernomordik LV (2010) Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog 6: e1001131
56. Zhang Y, ZhangW, Ogata S, Clements D, Strauss JH, Baker TS, Kuhn RJ, Rossmann MG (2004) Conformational changes of the flavivirus E glycoprotein. Structure 12: 1607-1618 (Pubitemid 39200514)