The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1

PLoS Pathogens

Volumn 6, Issue 4, 2010, Pages 1-18

  Shrestha, Bimmi ^a   Brien, James D ^a   Sukupolvi Petty, Soila ^a   Austin, S Kyle ^a   Edeling, Melissa A ^a   Kim, Taekyung ^a   O'Brien, Katie M ^a   Nelson, Christopher A ^a   Johnson, Syd ^b   Fremont, Daved H ^a   Diamond, Michael S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MacroGenics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY DENV1 E101; MONOCLONAL ANTIBODY DENV1 E103; MONOCLONAL ANTIBODY DENV1 E104; MONOCLONAL ANTIBODY DENV1 E105; MONOCLONAL ANTIBODY DENV1 E106; MONOCLONAL ANTIBODY DENV1 E108; MONOCLONAL ANTIBODY DENV1 E111; MONOCLONAL ANTIBODY DENV1 E112; MONOCLONAL ANTIBODY DENV1 E113; MONOCLONAL ANTIBODY DENV1 E95; MONOCLONAL ANTIBODY DENV1 E99; UNCLASSIFIED DRUG; E PROTEIN TH SMAN, DENGUE VIRUS; EPITOPE; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS REACTION; CRYSTAL STRUCTURE; DENGUE; DENGUE VIRUS 1; DRUG EFFICACY; DRUG POTENCY; GENETIC VARIABILITY; GENOTYPE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOPROPHYLAXIS; MOUSE; NONHUMAN; SEROTYPE; SINGLE DRUG DOSE; VIRUS NEUTRALIZATION; VIRUS STRAIN; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CHEMISTRY; DENGUE VIRUS; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; GENETICS; HUMAN; IMMUNOLOGY; MOLECULAR GENETICS; POLYMERASE CHAIN REACTION; PROTEIN TERTIARY STRUCTURE;

DENGUE VIRUS TYPE 1; MUS; WEST NILE VIRUS;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; DENGUE VIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; EPITOPES, B-LYMPHOCYTE; GENOTYPE; HUMANS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PROTEIN STRUCTURE, TERTIARY; VIRAL ENVELOPE PROTEINS;

EID: 77954039828     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000823     Document Type: Article

References (112)

1. Burke DS, Monath TP (2001) Flaviviruses. In: Knipe DM, Howley PM, eds. Fields Virology. Fourth Edition ed. Philadelphia: Lippincott Williams &Wilkins. pp 1043-1125.
2. Rico-Hesse R (1990) Molecular evolution and distribution of dengue viruses type 1 and 2 in nature. Virology 174: 479-493.
3. Holmes EC, Twiddy SS (2003) The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol 3: 19-28.
4. Halstead SB (1988) Pathogenesis of dengue: challenges to molecular biology. Science 239: 476-481.
5. Monath TP (1994) Dengue: the risk to developed and developing countries. Proc Natl Acad Sci U S A 91: 2395-2400.
6. Chambers TJ, Hahn CS, Galler R, Rice CM (1990) Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44: 649-688.
7. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, et al. (2002) Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108: 717-725.
8. Zhang Y, Corver J, Chipman PR, Zhang W, Pletnev SV, et al. (2003) Structures of immature flavivirus particles. Embo J 22: 2604-2613.
9. Modis Y, Ogata S, Clements D, Harrison SC (2003) A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci U S A 100: 6986-6991.
10. 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.
11. Nayak V, Dessau M, Kucera K, Anthony K, Ledizet M, et al. (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.
12. Mondotte JA, Lozach PY, Amara A, Gamarnik AV (2007) Essential Role of Dengue Virus Envelope Protein N Glycosylation at Asparagine-67 during Viral Propagation. J Virol 81: 7136-7148.
13. Pokidysheva E, Zhang Y, Battisti AJ, Bator-Kelly CM, Chipman PR, et al. (2006) Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124: 485-493.
14. Tassaneetrithep B, Burgess T, Granelli-Piperno A, Trumpfheller C, Finke J, et al. (2003) DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197: 823-829.
15. Navarro-Sanchez E, Altmeyer R, Amara A, Schwartz O, Fieschi F, et al. (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.
16. Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC (1995) The envelope glycoprotein from tick-borne encephalitis virus at 2 Angstrom resolution. Nature 375: 291-298.
17. Bhardwaj S, Holbrook M, Shope RE, Barrett AD, Watowich SJ (2001) Biophysical characterization and vector-specific antagonist activity of domain III of the tick-borne flavivirus envelope protein. J Virol 75: 4002-4007.
18. Volk DE, Beasley DW, Kallick DA, Holbrook MR, Barrett AD, et al. (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.
19. Yu S, Wuu A, Basu R, Holbrook MR, Barrett AD, et al. (2004) Solution structure and structural dynamics of envelope protein domain III of mosquitoand tick-borne flaviviruses. Biochemistry 43: 9168-9176.
20. Li L, Lok SM, Yu IM, Zhang Y, Kuhn RJ, et al. (2008) The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319: 1830-1834.
21. Yu IM, Zhang W, Holdaway HA, Li L, Kostyuchenko VA, et al. (2008) Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 319: 1834-1837.
22. Pierson TC, Fremont DH, Kuhn RJ, Diamond MS (2008) Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 4: 229-238.
23. Roehrig JT, Mathews JH, Trent DW (1983) Identification of epitopes on the E glycoprotein of Saint Louis encephalitis virus using monoclonal antibodies. Virology 128: 118-126.
24. Roehrig JT, Staudinger LA, Hunt AR, Mathews JH, Blair CD (2001) Antibody prophylaxis and therapy for flaviviral encephalitis infections. Ann NY Acad Sci. pp 286-297.
25. Lok SM, Kostyuchenko V, Nybakken GE, Holdaway HA, Battisti AJ, et al. (2008) Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat Struct Mol Biol 15: 312-317.
26. Sukupolvi-Petty S, Purtha WE, Austin SK, Oliphant T, Nybakken G, et al. (2007) Type- and Sub-Complex-Specific Neutralizing Antibodies Against Domain III of Dengue Virus Type-2 Envelope Protein Recognize Adjacent Epitopes. J Virol 81: 12816-12826.
27. Gromowski GD, Barrett ND, Barrett AD (2008) Characterization of dengue virus complex-specific neutralizing epitopes on envelope protein domain III of dengue 2 virus. J Virol 82: 8828-8837.
28. Diamond MS, Sitati E, Friend L, Shrestha B, Higgs S, et al. (2003) Induced IgM protects against lethal West Nile Virus infection. J Exp Med 198: 1-11.
29. Oliphant T, Engle M, Nybakken G, Doane C, Johnson S, et al. (2005) Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nature Medicine 11: 522-530.
30. Brandriss MW, Schlesinger JJ, Walsh EE, Briselli M (1986) Lethal 17D yellow fever encephalitis in mice. I. Passive protection by monoclonal antibodies to the envelope proteins of 17D yellow fever and dengue 2 viruses. J Gen Virol 67: 229-234.
31. Gould EA, Buckley A, Barrett AD, Cammack N (1986) Neutralizing (54K) and non-neutralizing (54K and 48K) monoclonal antibodies against structural and non-structural yellow fever virus proteins confer immunity in mice. J Gen Virol 67 (Pt 3): 591-595.
32. Beasley DW, Barrett AD (2002) Identification of neutralizing epitopes within structural domain III of the West Nile virus envelope protein. J Virol 76: 13097-13100.
33. 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.
34. Roehrig JT, Bolin RA, Kelly RG (1998) Monoclonal antibody mapping of the envelope glycoprotein of the dengue 2 virus, Jamaica. Virology 246: 317-328.
35. Sanchez MD, Pierson TC, McAllister D, Hanna SL, Puffer BA, et al. (2005) Characterization of neutralizing antibodies to West Nile virus. Virology 336: 70-82.
36. Cecilia D, Gould EA (1991) Nucleotide changes responsible for loss of neuroinvasiveness in Japanese encephalitis virus neutralization-resistant mutants. Virology 181: 70-77.
37. Seif SA, Morita K, Matsuo S, Hasebe F, Igarashi A (1995) Finer mapping of neutralizing epitope(s) on the C-terminal of Japanese encephalitis virus Eprotein expressed in recombinant Escherichia coli system. Vaccine 13: 1515-1521.
38. Wu SC, Lian WC, Hsu LC, Liau MY (1997) Japanese encephalitis virus antigenic variants with characteristic differences in neutralization resistance and mouse virulence. Virus Res 51: 173-181.
39. Schlesinger JJ, Chapman S, Nestorowicz A, Rice CM, Ginocchio TE, et al. (1996) Replication of yellow fever virus in the mouse central nervous system: comparison of neuroadapted and non-neuroadapted virus and partial sequence analysis of the neuroadapted strain. J Gen Virol 77 (Pt 6): 1277-1285.
40. Lin B, Parrish CR, Murray JM, Wright PJ (1994) Localization of a neutralizing epitope on the envelope protein of dengue virus type 2. Virology 202: 885-890.
41. 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.
42. Lai CJ, Goncalvez AP, Men R, Wernly C, Donau O, et al. (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.
43. Diamond MS (2009) Progress on the development of therapeutics against West Nile virus. Antiviral Res 83: 214-227.
44. Simantini E, Banerjee K (1995) Epitope mapping of dengue 1 virus E glycoprotein using monoclonal antibodies. Arch Virol 140: 1257-1273.
45. Chen YC, Huang HN, Lin CT, Chen YF, King CC, et al. (2007) Generation and characterization of monoclonal antibodies against dengue virus type 1 for epitope mapping and serological detection by epitope-based peptide antigens. Clin Vaccine Immunol 14: 404-411.
46. Beasley DW, Aaskov JG (2001) Epitopes on the dengue 1 virus envelope protein recognized by neutralizing IgM monoclonal antibodies. Virology 279: 447-458.
47. Goncalvez AP, Escalante AA, Pujol FH, Ludert JE, Tovar D, et al. (2002) Diversity and evolution of the envelope gene of dengue virus type 1. Virology 303: 110-119.
48. Vogt MR, Moesker B, Goudsmit J, Jongeneelen M, Austin SK, et al. (2009) Human Monoclonal Antibodies Induced by Natural Infection Against West Nile Virus Neutralize at a Post-Attachment Step. J Virol 83: 6494-6507.
49. Morrey JD, Siddharthan V, Olsen AL, Roper GY, Wang H, et al. (2006) Humanized monoclonal antibody against West Nile virus E protein administered after neuronal infection protects against lethal encephalitis in hamsters. J Infect Dis 194: 1300-1308.
50. Morrey JD, Siddharthan V, Olsen AL, Wang H, Julander JG, et al. (2007) Defining limits of humanized neutralizing monoclonal antibody treatment for West Nile virus neurological infection in a hamster model. Antimicrob Agents Chemother 51: 2396-2402.
51. Zhang W, Chipman PR, Corver J, Johnson PR, Zhang Y, et al. (2003) Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat Struct Biol 10: 907-912.
52. Oliphant T, Nybakken GE, Engle M, Xu Q, Nelson CA, et al. (2006) Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J Virol 80: 12149-12159.
53. Gould LH, Sui J, Foellmer H, Oliphant T, Wang T, et al. (2005) Protective and therapeutic capacity of human single chain Fv-Fc fusion proteins against West Nile virus. J Virol 79: 14606-14613.
54. Throsby M, Geuijen C, Goudsmit J, Bakker AQ, Korimbocus J, et al. (2006) Isolation and characterization of human monoclonal antibodies from individuals infected with West Nile Virus. J Virol 80: 6982-6992.
55. Sultana H, Foellmer HG, Neelakanta G, Oliphant T, Engle M, et al. (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.
56. Johnson AJ, Roehrig JT (1999) New mouse model for dengue virus vaccine testing. J Virol 73: 783-786.
57. Goncalvez AP, Chien CH, Tubthong K, Gorshkova I, Roll C, et al. (2008) Humanized monoclonal antibodies derived from chimpanzee Fabs protect against Japanese encephalitis virus in vitro and in vivo. J Virol 82: 7009-7021.
58. Goncalvez AP, Purcell RH, Lai CJ (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.
59. Leitmeyer KC, Vaughn DW, Watts DM, Salas R, Villalobos I, et al. (1999) Dengue virus structural differences that correlate with pathogenesis. J Virol 73: 4738-4747.
60. Rico-Hesse R (2007) Dengue virus evolution and virulence models. Clin Infect Dis 44: 1462-1466.
61. Rico-Hesse R, Harrison LM, Salas RA, Tovar D, Nisalak A, et al. (1997) Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. Virology 230: 244-251.
62. Armstrong PM, Rico-Hesse R (2003) Efficiency of dengue serotype 2 virus strains to infect and disseminate in Aedes aegypti. Am J Trop Med Hyg 68: 539-544.
63. Rico-Hesse R (2003) Microevolution and virulence of dengue viruses. Adv Virus Res 59: 315-341.
64. Lisova O, Hardy F, Petit V, Bedouelle H (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.
65. Thullier P, Demangel C, Bedouelle H, Megret F, Jouan A, et al. (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.
66. Rajamanonmani R, Nkenfou C, Clancy P, Yau YH, Shochat SG, et al. (2009) On a mouse monoclonal antibody that neutralizes all four dengue virus serotypes. J Gen Virol 90: 799-809.
67. Matsui K, Gromowski GD, Li L, Schuh AJ, Lee JC, et al. (2009) Characterization of dengue complex-reactive epitopes on dengue 3 virus envelope protein domain III. Virology 384: 16-20.
68. Crill WD, Chang GJ (2004) Localization and characterization of flavivirus envelope glycoprotein cross-reactive epitopes. J Virol 78: 13975-13986.
69. Crill WD, Trainor NB, Chang GJ (2007) A detailed mutagenesis study of flavivirus cross-reactive epitopes using West Nile virus-like particles. J Gen Virol 88: 1169-1174.
70. Chen Z, Liu LM, Gao N, Xu XF, Zhang JL, et al. (2009) Passive protection assay of monoclonal antibodies against dengue virus in suckling mice. Curr Microbiol 58: 326-331.
71. Kaufman BM, Summers PL, Dubois DR, Eckels KH (1987) Monoclonal antibodies against dengue 2 virus E-glycoprotein protect mice against lethal dengue infection. Am J Trop Med Hyg 36: 427-434.
72. Engle M, Diamond MS (2003) Antibody prophylaxis and therapy against West Nile Virus infection in wild type and immunodeficient mice. J Virol 77: 12941-12949.
73. Ben-Nathan D, Gershoni-Yahalom O, Samina I, Khinich Y, Nur I, et al. (2009) Using high titer West Nile intravenous immunoglobulin from selected Israeli donors for treatment of West Nile virus infection. BMC Infect Dis 9: 18.
74. Ben-Nathan D, Lustig S, Tam G, Robinzon S, Segal S, et al. (2003) Prophylactic and therapeutic efficacy of human intravenous immunoglobulin in treating west nile virus infection in mice. J Infect Dis 188: 5-12.
75. Zhang MJ, Wang MJ, Jiang SZ, Ma WY (1989) Passive protection of mice, goats, and monkeys against Japanese encephalitis with monoclonal antibodies. J Med Virol 29: 133-138.
76. Kimura-Kuroda J, Yasui K (1988) Protection of mice against Japanese encephalitis virus by passive administration with monoclonal antibodies. J Immunol 141: 3606-3610.
77. Kreil TR, Eibl MM (1997) Pre- and postexposure protection by passive immunoglobulin but no enhancement of infection with a flavivirus in a mouse model. J Virol 71: 2921-2927.
78. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, et al. (2000) Dengue Viremia Titer, Antibody Response Pattern, and Virus Serotype Correlate with Disease Severity. J Infect Dis 181: 2-9.
79. Xiao SY, Guzman H, Zhang H, Travassos da Rosa AP, Tesh RB (2001) West Nile virus infection in the golden hamster (Mesocricetus auratus): a model for West Nile encephalitis. Emerg Infect Dis 7: 714-721.
80. Diamond MS, Shrestha B, Marri A, Mahan D, Engle M (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.
81. Pierson TC, Xu Q, Nelson S, Oliphant T, Nybakken GE, et al. (2007) The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host and Microbe 1: 135-145.
82. Klasse PJ (2007) Modeling how many envelope glycoprotein trimers per virion participate in human immunodeficiency virus infectivity and its neutralization by antibody. Virology 369: 245-262.
83. Gollins S, Porterfield J (1984) Flavivirus infection enhancement in macrophages: radioactive and biological studies on the effect of antibody and viral fate. J Gen Virol 65: 1261-1272.
84. Halstead SB (1994) Antibody-dependent enhancement of infection: a mechanism for indirect virus entry into cells. Cellular Receptors for Animal Viruses. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. Pp 493-516.
85. Halstead SB (1979) In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 140: 527-533.
86. Goncalvez AP, Engle RE, St Claire M, Purcell RH, Lai CJ (2007) Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci U S A 104: 9422-9427.
87. Mehlhop E, Ansarah-Sobrinho C, Johnson S, Engle M, Fremont DH, et al. (2007) Complement protein C1q inhibits antibody-dependent enhancement of flavivirus infection in an IgG subclass-specific manner. Cell Host and Microbe 2: 417-426.
88. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL, et al. (2010) Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e1000790. doi:10.1371/journal.ppat.1000790.
89. Hiramatsu K, Tadano M, Men R, Lai CJ (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.
90. Serafin IL, Aaskov JG (2001) Identification of epitopes on the envelope (E) protein of dengue 2 and dengue 3 viruses using monoclonal antibodies. Arch Virol 146: 2469-2479.
91. Megret F, Hugnot JP, Falconar A, Gentry MK, Morens DM, et al. (1992) Use of recombinant fusion proteins and monoclonal antibodies to define linear and discontinuous antigenic sites on the dengue virus envelope glycoprotein. Virology 187: 480-491.
92. Trirawatanapong T, Chandran B, Putnak R, Padmanabhan R (1992) Mapping of a region of dengue virus type-2 glycoprotein required for binding by a neutralizing monoclonal antibody. Gene 116: 139-150.
93. Nybakken G, Oliphant T, Johnson S, Burke S, Diamond MS, et al. (2005) Structural basis for neutralization of a therapeutic antibody against West Nile virus. Nature 437: 764-769.
94. Cherrier MV, Kaufmann B, Nybakken GE, Lok SM, Warren JT, et al. (2009) Structural basis for the preferential binding of immature flaviviruses by a fusion-loop specific antibody. EMBO 28: 3269-3276.
95. Oliphant T, Nybakken GE, Austin SK, Xu Q, Bramson J, et al. (2007) The Induction of Epitope-Specific Neutralizing Antibodies against West Nile virus. J Virol 81: 11828-11839.
96. 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.
97. 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. doi:10.1371/journal.pone.0004991.
98. Hermida L, Bernardo L, Martin J, Alvarez M, Prado I, et al. (2006) A recombinant fusion protein containing the domain III of the dengue-2 envelope protein is immunogenic and protective in nonhuman primates. Vaccine 24: 3165-3171.
99. Chu JH, Chiang CC, Ng ML (2007) Immunization of Flavivirus West Nile Recombinant Envelope Domain III Protein Induced Specific Immune Response and Protection against West Nile Virus Infection. J Immunol 178: 2699-2705.
100. Chen S, Yu M, Jiang T, Deng Y, Qin C, et al. (2007) Induction of tetravalent protective immunity against four dengue serotypes by the tandem domain III of the envelope protein. DNA Cell Biol 26: 361-367.
101. Valdes I, Bernardo L, Gil L, Pavon A, Lazo L, et al. (2009) A novel fusion protein domain III-capsid from dengue-2, in a highly aggregated form, induces a functional immune response and protection in mice. Virology 394: 249-258.
102. Harlow E, Lane D (1988) Antibodies, A laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory. 714 p.
103. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M (2006) HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 62: 859-866.
104. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
105. Jones EY, Walker NP, Stuart DI (1991) Methodology employed for the structure determination of tumour necrosis factor, a case of high noncrystallographic symmetry. Acta Crystallogr A 47 (Pt 6): 753-770.
106. Winn MD, Murshudov GN, Papiz MZ (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol 374: 300-321.
107. Shindyalov IN, Bourne PE (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng 11: 739-747.
108. Boder ET, Wittrup KD (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat Biotechnol 15: 553-557.
109. Boder ET, Wittrup KD (1998) Optimal screening of surface-displayed polypeptide libraries. Biotechnol Prog 14: 55-62.
110. Potterton L, McNicholas S, Krissinel E, Gruber J, Cowtan K, et al. (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 60: 2288-2294.
111. Barton GJ (1993) ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng 6: 37-40.
112. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.