Structural analysis of a dengue cross-reactive antibody complexed with envelope domain III reveals the molecular basis of cross-reactivity

Journal of Immunology

Volumn 188, Issue 10, 2012, Pages 4971-4979

  Midgley, Claire M ^a   Flanagan, Aleksandra ^b   Tran, Hai Bac ^a   Dejnirattisai, Wanwisa ^a   Chawansuntati, Kriangkrai ^a   Jumnainsong, Amonrat ^a   Wongwiwat, Wiyada ^a   Duangchinda, Thaneeya ^c   Mongkolsapaya, Juthathip ^a,d   Grimes, Jonathan M ^b,e   Screaton, Gavin R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^d MAHIDOL UNIVERSITY   (Thailand)

^e DIAMOND LIGHT SOURCE LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE DOMAIN PROTEIN III; ENVELOPE PROTEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2H12; UNCLASSIFIED DRUG;

ANTIBODY STRUCTURE; ANTIGEN BINDING; ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CROSS REACTION; CRYSTAL STRUCTURE; DENGUE; DENGUE VIRUS 2; EPITOPE MAPPING; FEMALE; MATURE VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEROTYPE; VIRION; VIRUS NEUTRALIZATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; BINDING SITES, ANTIBODY; CROSS REACTIONS; CRYSTALLOGRAPHY, X-RAY; DENGUE VIRUS; FEMALE; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PROTEIN STRUCTURE, TERTIARY; SEROTYPING; VIRAL ENVELOPE PROTEINS; VIRION;

EID: 84861117957     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200227     Document Type: Article

References (75)

1. Gubler, D. J. 2002. The global emergence/resurgence of arboviral diseases as public health problems. Arch. Med. Res. 33: 330-342. (Pubitemid 35299553)
2. Guzman, A., and R. E. Istúriz. 2010. Update on the global spread of dengue. Int. J. Antimicrob. Agents 36(Suppl. 1): S40-S42.
3. Blok, J. 1985. Genetic relationships of the dengue virus serotypes. J. Gen. Virol. 66: 1323-1325. (Pubitemid 15027199)
4. Green, S., and A. Rothman. 2006. Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr. Opin. Infect. Dis. 19: 429-436. (Pubitemid 44338101)
5. Sabin, A. B. 1952. Research on dengue during World War II. Am. J. Trop. Med. Hyg. 1: 30-50.
6. Thein, S., M. M. Aung, T. N. Shwe, M. Aye, A. Zaw, K. Aye, K. M. Aye, and J. Aaskov. 1997. Risk factors in dengue shock syndrome. Am. J. Trop. Med. Hyg. 56: 566-572. (Pubitemid 27230081)
7. Halstead, S. B., and E. J. O'Rourke. 1977. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J. Exp. Med. 146: 201-217. (Pubitemid 8139503)
8. Halstead, S. B., and E. J. O'Rourke. 1977. Antibody-enhanced dengue virus infection in primate leukocytes. Nature 265: 739-741. (Pubitemid 8039460)
9. 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.
10. Goncalvez, A. P., R. E. Engle, M. St Claire, R. H. Purcell, and C. J. Lai. 2007. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc. Natl. Acad. Sci. USA 104: 9422-9427. (Pubitemid 47185795)
11. Halstead, S. B. 1979. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J. Infect. Dis. 140: 527-533. (Pubitemid 10172725)
12. Kliks, S. C., S. Nimmanitya, A. Nisalak, and D. S. Burke. 1988. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am. J. Trop. Med. Hyg. 38: 411-419. (Pubitemid 18086128)
13. Dejnirattisai, W., A. Jumnainsong, N. Onsirisakul, P. Fitton, S. Vasanawathana, W. Limpitikul, C. Puttikhunt, C. Edwards, T. Duangchinda, S. Supasa, et al. 2010. Cross-reacting antibodies enhance dengue virus infection in humans. Science 328: 745-748.
14. Rodenhuis-Zybert, I. A., H. M. van der Schaar, J. M. da Silva Voorham, H. van der Ende-Metselaar, H. Y. Lei, J. Wilschut, and J. M. Smit. 2010. Immature dengue virus: a veiled pathogen? PLoS Pathog. 6: e1000718.
15. 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. (Pubitemid 40053904)
16. 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. (Pubitemid 28384045)
17. Thullier, P., C. Demangel, H. Bedouelle, F. Mégret, A. Jouan, V. Deubel, J. C. Mazié, 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. (Pubitemid 32707552)
18. 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. USA 100: 6986-6991. (Pubitemid 36706380)
19. Crill, W. D., and G. J. Chang. 2004. Localization and characterization of flavivirus envelope glycoprotein cross-reactive epitopes. J. Virol. 78: 13975-13986. (Pubitemid 39612794)
20. Stiasny, K., S. Kiermayr, H. Holzmann, and F. X. Heinz. 2006. Cryptic properties of a cluster of dominant flavivirus cross-reactive antigenic sites. J. Virol. 80: 9557-9568. (Pubitemid 44435631)
21. Deng, Y. Q., J. X. Dai, G. H. Ji, T. Jiang, H. J. Wang, H. O. Yang, W. L. Tan, R. Liu, M. Yu, B. X. Ge, et al. 2011. A broadly flavivirus cross-neutralizing monoclonal antibody that recognizes a novel epitope within the fusion loop of E protein. PLoS ONE 6: e16059.
22. Chin, J. F., J. J. Chu, and M. L. Ng. 2007. The envelope glycoprotein domain III of dengue virus serotypes 1 and 2 inhibit virus entry. Microbes Infect. 9: 1-6. (Pubitemid 46151756)
23. Crill, W. D., and J. T. Roehrig. 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)
24. Huerta, V., G. Chinea, N. Fleitas, M. Sarría, J. Sánchez, P. Toledo, and G. Padrón. 2008. Characterization of the interaction of domain III of the envelope protein of dengue virus with putative receptors from CHO cells. Virus Res. 137: 225-234.
25. Hung, J. J., M. T. Hsieh, M. J. Young, C. L. Kao, C. C. King, and W. Chang. 2004. An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding to mosquito but not mammalian cells. J. Virol. 78: 378-388. (Pubitemid 37549749)
26. Brien, J. D., S. K. Austin, S. Sukupolvi-Petty, K. M. O'Brien, S. Johnson, D. H. Fremont, and M. S. Diamond. 2010. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J. Virol. 84: 10630-10643.
27. 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. (Pubitemid 47398915)
28. 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.
29. Hiramatsu, K., M. Tadano, R. Men, and C. J. Lai. 1996. Mutational analysis of a neutralization epitope on the dengue type 2 virus (DEN2) envelope protein: monoclonal antibody resistant DEN2/DEN4 chimeras exhibit reduced mouse neurovirulence. Virology 224: 437-445. (Pubitemid 26364491)
30. 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, et al. 2008. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Biol. 15: 312-317. (Pubitemid 351654038)
31. 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.
32. 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.
33. Sukupolvi-Petty, S., S. K. Austin, M. Engle, J. D. Brien, K. A. Dowd, K. L. Williams, S. Johnson, R. Rico-Hesse, E. Harris, T. C. Pierson, et al. 2010. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J. Virol. 84: 9227-9239.
34. Sukupolvi-Petty, S., S. K. Austin, W. E. Purtha, T. Oliphant, G. E. 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. (Pubitemid 350156919)
35. 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.
36. Bernardo, L., L. Hermida, J. Martin, M. Alvarez, I. Prado, C. López, R. Martínez, R. Rodríguez-Roche, A. Zulueta, L. Lazo, et al. 2008. Anamnestic antibody response after viral challenge in monkeys immunized with dengue 2 recombinant fusion proteins. Arch. Virol. 153: 849-854.
37. Izquierdo, A., L. Bernardo, J. Martin, E. Santana, L. Hermida, G. Guillén, and M. G. Guzmán. 2008. Serotype-specificity of recombinant fusion proteins containing domain III of dengue virus. Virus Res. 138: 135-138.
38. Simmons, M., G. S. Murphy, and C. G. Hayes. 2001. Short report: Antibody responses of mice immunized with a tetravalent dengue recombinant protein subunit vaccine. Am. J. Trop. Med. Hyg. 65: 159-161. (Pubitemid 32744223)
39. Simmons, M., W. M. Nelson, S. J. Wu, and C. G. Hayes. 1998. Evaluation of the protective efficacy of a recombinant dengue envelope B domain fusion protein against dengue 2 virus infection in mice. Am. J. Trop. Med. Hyg. 58: 655-662. (Pubitemid 28237267)
40. Srivastava, A. K., J. R. Putnak, R. L. Warren, and C. H. Hoke, Jr. 1995. Mice immunized with a dengue type 2 virus E and NS1 fusion protein made in Escherichia coli are protected against lethal dengue virus infection. Vaccine 13: 1251-1258.
41. Lin, B., C. R. Parrish, J. M. Murray, and P. J. Wright. 1994. Localization of a neutralizing epitope on the envelope protein of dengue virus type 2. Virology 202: 885-890.
42. Matsui, K., G. D. Gromowski, L. Li, and A. D. Barrett. 2010. Characterization of a dengue type-specific epitope on dengue 3 virus envelope protein domain III. J. Gen. Virol. 91: 2249-2253.
43. 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.
44. Midgley, C. M., M. Bajwa-Joseph, S. Vasanawathana, W. Limpitikul, B. Wills, A. Flanagan, E. Waiyaiya, H. B. Tran, A. E. Cowper, P. Chotiyarnwong, et al. 2011. An in-depth analysis of original antigenic sin in dengue virus infection. [Published erratum appears in 2011 J. Virol. 85: 12100.] J. Virol. 85: 410-421.
45. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
46. Jirakanjanakit, N., T. Sanohsomneing, S. Yoksan, and N. Bhamarapravati. 1997. The micro-focus reduction neutralization test for determining dengue and Japanese encephalitis neutralizing antibodies in volunteers vaccinated against dengue. Trans. R. Soc. Trop. Med. Hyg. 91: 614-617. (Pubitemid 27478663)
47. Sundström, C., and K. Nilsson. 1976. Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int. J. Cancer 17: 565-577.
48. Frohman, M. A., M. K. Dush, and G. R. Martin. 1988. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85: 8998-9002. (Pubitemid 19001832)
49. Walter, T. S., J. M. Diprose, C. J. Mayo, C. Siebold, M. G. Pickford, L. Carter, G. C. Sutton, N. S. Berrow, J. Brown, I. M. Berry, et al. 2005. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr. D Biol. Crystallogr. 61: 651-657. (Pubitemid 43951502)
50. Otwinowski, Z., and W. Minor. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326 (Pubitemid 27085611)
51. Winter, G. 2010. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43: 186-190.
52. McCoy, A. J. 2007. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 63: 32-41.
53. Saphire, E. O., R. L. Stanfield, M. D. Crispin, G. Morris, M. B. Zwick, R. A. Pantophlet, P. W. Parren, P. M. Rudd, R. A. Dwek, D. R. Burton, and I. A. Wilson. 2003. Crystal structure of an intact human IgG: antibody asymmetry, flexibility, and a guide for HIV-1 vaccine design. Adv. Exp. Med. Biol. 535: 55-66. (Pubitemid 38130241)
54. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50: 760-763.
55. Potterton, E., S. McNicholas, and E. Krissinel, K. Cowtan, and M. Noble. 2002. The CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 58: 1955-1957. (Pubitemid 35337294)
56. Winn, M. D., G. N. Murshudov, and M. Z. Papiz. 2003. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374: 300-321. (Pubitemid 37531815)
57. Bricogne, G., E. Blanc, M. Brandl, C. Flensburg, P. Keller, W. Paciorek, P. Roversi, A. Sharff, O. Smart, C. Vonrhein, and T. Womack. 2010. BUSTER version 2.9. Global Phasing Ltd, Cambridge, U.K.
58. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132. (Pubitemid 41742764)
59. Chen, V. B., W. B. Arendall, III, J. J. Headd, D. A. Keedy, R. M. Immormino, G. J. Kapral, L. W. Murray, J. S. Richardson, and D. C. Richardson. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66: 12-21.
60. Krissinel, E., and K. Henrick. 2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372: 774-797. (Pubitemid 47321791)
61. Jones, D. H., R. J. Looney, and C. L. Anderson. 1985. Two distinct classes of IgG Fc receptors on a human monocyte line (U937) defined by differences in binding of murine IgG subclasses at low ionic strength. J. Immunol. 135: 3348-3353. (Pubitemid 16250599)
62. Looney, R. J., G. N. Abraham, and C. L. Anderson. 1986. Human monocytes and U937 cells bear two distinct Fc receptors for IgG. J. Immunol. 136: 1641-1647. (Pubitemid 16119569)
63. Kaufmann, B., G. E. Nybakken, P. R. Chipman, W. Zhang, M. S. Diamond, D. H. Fremont, R. J. Kuhn, and M. G. Rossmann. 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)
64. Nybakken, G. E., T. Oliphant, S. Johnson, S. Burke, M. S. Diamond, and D. H. Fremont. 2005. Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 437: 764-769. (Pubitemid 41486548)
65. Cockburn, J. J., M. E. Navarro Sanchez, N. Fretes, A. Urvoas, I. Staropoli, C. M. Kikuti, L. L. Coffey, F. Arenzana Seisdedos, H. Bedouelle, and F. A. Rey. 2012. Mechanism of dengue virus broad cross-neutralization by a monoclonal antibody. Structure 20: 303-314.
66. Gromowski, G. D., J. T. Roehrig, M. S. Diamond, J. C. Lee, T. J. Pitcher, and A. D. Barrett. 2010. Mutations of an antibody binding energy hot spot on domain III of the dengue 2 envelope glycoprotein exploited for neutralization escape. Virology 407: 237-246.
67. Lewis, J. K., B. Bothner, T. J. Smith, and G. Siuzdak. 1998. Antiviral agent blocks breathing of the common cold virus. Proc. Natl. Acad. Sci. USA 95: 6774-6778. (Pubitemid 28278056)
68. Bothner, B., X. F. Dong, L. Bibbs, J. E. Johnson, and G. Siuzdak. 1998. Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry. J. Biol. Chem. 273: 673-676. (Pubitemid 28049149)
69. Mallery, D. L., W. A. McEwan, S. R. Bidgood, G. J. Towers, C. M. Johnson, and L. C. James, 2010. Antibodies mediate intracellular immunity through tripartite motif-containing 21 (TRIM21). Proc. Natl. Acad. Sci. USA 107: 19985-19990.
70. Crill, W. D., H. R. Hughes, M. J. Delorey, and G. J. Chang. 2009. Humoral immune responses of dengue fever patients using epitope-specific serotype-2 virus-like particle antigens. PLoS ONE 4: e4991.
71. Lai, C. Y., W. Y. Tsai, S. R. Lin, C. L. Kao, H. P. Hu, C. C. King, H. C. Wu, G. J. Chang, and W. K. Wang. 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.
72. Wahala, W. M., A. A. Kraus, L. B. Haymore, M. A. Accavitti-Loper, and A. M. de Silva. 2009. Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody. Virology 392: 103-113.
73. Zlatkovic, J., K. Stiasny, and F. X. Heinz. 2011. Immunodominance and functional activities of antibody responses to inactivated West Nile virus and recombinant subunit vaccines in mice. J. Virol. 85: 1994-2003.
74. Kabsch, W., and C. Sander. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
75. Rey, F. A., F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison. 1995. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375: 291-298.