The Type-Specific Neutralizing Antibody Response Elicited by a Dengue Vaccine Candidate Is Focused on Two Amino Acids of the Envelope Protein

PLoS Pathogens

Volumn 9, Issue 12, 2013, Pages 1-14

  VanBlargan, Laura A ^a   Mukherjee, Swati ^a   Dowd, Kimberly A ^a   Durbin, Anna P ^b   Whitehead, Stephen S ^a   Pierson, Theodore C ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISERUM; DENGUE VACCINE; E126K EPITOPE; E157K EPITOPE; EPITOPE; NEUTRALIZING ANTIBODY; PLASMID VECTOR; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; AMINO ACID; VIRUS ANTIBODY;

AMINO ACID SEQUENCE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DENGUE VIRUS 1; GENE ACTIVITY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MUTAGENESIS; NONHUMAN; PATHOGENESIS; PREVALENCE; QUANTITATIVE ASSAY; VACCINATION; VIRUS CHARACTERIZATION; VIRUS NEUTRALIZATION; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; DENGUE VIRUS; EPITOPE MAPPING; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; PHASE 1 CLINICAL TRIAL (TOPIC); SITE DIRECTED MUTAGENESIS;

AMINO ACIDS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY FORMATION; ANTIBODY SPECIFICITY; CLINICAL TRIALS, PHASE I AS TOPIC; DENGUE VACCINES; DENGUE VIRUS; EPITOPE MAPPING; EPITOPES; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; VIRAL ENVELOPE PROTEINS;

EID: 84892890264     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003761     Document Type: Article

References (107)

1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, et al. (2013) The global distribution and burden of dengue. Nature 496 (7446) ():: 504-7.
2. Halstead SB, (2007) Dengue. Lancet 370: 1644-1652.
3. Srikiatkhachorn A, Rothman AL, Gibbons RV, Sittisombut N, Malasit P, et al. (2011) Dengue-how best to classify it. Clin Infect Dis 53: 563-567.
4. Guzman MG, Alvarez M, Halstead SB, (2013) Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol 158 (7) ():: 1445-59.
5. 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.
6. Kyle JL, Harris E, (2008) Global spread and persistence of dengue. Annu Rev Microbiol 62: 71-92.
7. Perera R, Kuhn RJ, (2008) Structural proteomics of dengue virus. Curr Opin Microbiol 11: 369-377.
8. Mukhopadhyay S, Kuhn RJ, Rossmann MG, (2005) A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3: 13-22.
9. Wang PG, Kudelko M, Lo J, Siu LY, Kwok KT, et al. (2009) Efficient assembly and secretion of recombinant subviral particles of the four dengue serotypes using native prM and E proteins. PLoS One 4: e8325.
10. Mackenzie JM, Westaway EG, (2001) Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. J Virol 75: 10787-10799.
11. Lorenz IC, Kartenbeck J, Mezzacasa A, Allison SL, Heinz FX, et al. (2003) Intracellular assembly and secretion of recombinant subviral particles from tick-borne encephalitis virus. J Virol 77: 4370-4382.
12. Welsch S, Miller S, Romero-Brey I, Merz A, Bleck CK, et al. (2009) Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5: 365-375.
13. Gillespie LK, Hoenen A, Morgan G, Mackenzie JM, (2010) The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J Virol 84: 10438-10447.
14. 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.
15. Zhang Y, Kaufmann B, Chipman PR, Kuhn RJ, Rossmann MG, (2007) Structure of immature West Nile virus. J Virol 81: 6141-6145.
16. Zhang Y, Corver J, Chipman PR, Zhang W, Pletnev SV, et al. (2003) Structures of immature flavivirus particles. EMBO J 22: 2604-2613.
17. Elshuber S, Allison SL, Heinz FX, Mandl CW, (2003) Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J Gen Virol 84: 183-191.
18. Stadler K, Allison SL, Schalich J, Heinz FX, (1997) Proteolytic activation of tick-borne encephalitis virus by furin. J Virol 71: 8475-8481.
19. 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.
20. Mukhopadhyay S, Kim BS, Chipman PR, Rossmann MG, Kuhn RJ, (2003) Structure of West Nile virus. Science 302: 248.
21. 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.
22. Zhang X, Sheng J, Plevka P, Kuhn RJ, Diamond MS, et al. (2013) Dengue structure differs at the temperatures of its human and mosquito hosts. Proc Natl Acad Sci U S A.
23. 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.
24. 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.
25. Pierson TC, Diamond MS, (2012) Degrees of maturity: the complex structure and biology of flaviviruses. Curr Opin Virol 2: 168-175.
26. Whitehead SS, Blaney JE, Durbin AP, Murphy BR, (2007) Prospects for a dengue virus vaccine. Nat Rev Microbiol 5: 518-528.
27. Belmusto-Worn VE, Sanchez JL, McCarthy K, Nichols R, Bautista CT, et al. (2005) Randomized, double-blind, phase III, pivotal field trial of the comparative immunogenicity, safety, and tolerability of two yellow fever 17D vaccines (Arilvax and YF-VAX) in healthy infants and children in Peru. Am J Trop Med Hyg 72: 189-197.
28. Heinz FX, Holzmann H, Essl A, Kundi M, (2007) Field effectiveness of vaccination against tick-borne encephalitis. Vaccine 25: 7559-7567.
29. Mason RA, Tauraso NM, Spertzel RO, Ginn RK, (1973) Yellow fever vaccine: direct challenge of monkeys given graded doses of 17D vaccine. Appl Microbiol 25: 539-544.
30. Monath TP, Nichols R, Archambault WT, Moore L, Marchesani R, et al. (2002) Comparative safety and immunogenicity of two yellow fever 17D vaccines (ARILVAX and YF-VAX) in a phase III multicenter, double-blind clinical trial. Am J Trop Med Hyg 66: 533-541.
31. Williams KL, Wahala WM, Orozco S, de Silva AM, Harris E, (2012) Antibodies targeting dengue virus envelope domain III are not required for serotype-specific protection or prevention of enhancement in vivo. Virology 429: 12-20.
32. Williams KL, Sukupolvi-Petty S, Beltramello M, Johnson S, Sallusto F, et al. (2013) Therapeutic Efficacy of Antibodies Lacking FcgammaR against Lethal Dengue Virus Infection Is Due to Neutralizing Potency and Blocking of Enhancing Antibodies. PLoS Pathog 9: e1003157.
33. Shrestha B, Austin SK, Dowd KA, Prasad AN, Youn S, et al. (2012) Complex phenotypes in mosquitoes and mice associated with neutralization escape of a Dengue virus type 1 monoclonal antibody. Virology 427: 127-134.
34. 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.
35. Shrestha B, Brien JD, Sukupolvi-Petty S, Austin SK, Edeling MA, et al. (2010) The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog 6: e1000823.
36. Sukupolvi-Petty S, Austin SK, Engle M, Brien JD, Dowd KA, et al. (2010) Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J Virol 84: 9227-9239.
37. Roehrig JT, (2003) Antigenic structure of flavivirus proteins. Adv Virus Res 59: 141-175.
38. Sukupolvi-Petty S, Austin SK, Purtha WE, Oliphant T, Nybakken GE, et al. (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.
39. Beltramello M, Williams KL, Simmons CP, Macagno A, Simonelli L, et al. (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.
40. Roehrig JT, Bolin RA, Kelly RG, (1998) Monoclonal antibody mapping of the envelope glycoprotein of the dengue 2 virus, Jamaica. Virology 246: 317-328.
41. 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.
42. Crill WD, Chang GJ, (2004) Localization and characterization of flavivirus envelope glycoprotein cross-reactive epitopes. J Virol 78: 13975-13986.
43. Stiasny K, Brandler S, Kossl C, Heinz FX, (2007) Probing the flavivirus membrane fusion mechanism by using monoclonal antibodies. J Virol 81: 11526-11531.
44. Beasley DW, Aaskov JG, (2001) Epitopes on the dengue 1 virus envelope protein recognized by neutralizing IgM monoclonal antibodies. Virology 279: 447-458.
45. Schieffelin JS, Costin JM, Nicholson CO, Orgeron NM, Fontaine KA, et al. (2010) Neutralizing and non-neutralizing monoclonal antibodies against dengue virus E protein derived from a naturally infected patient. Virol J 7: 28.
46. Vogt MR, Moesker B, Goudsmit J, Jongeneelen M, Austin SK, et al. (2009) Human monoclonal antibodies against West Nile virus induced by natural infection neutralize at a postattachment step. J Virol 83: 6494-6507.
47. Zou G, Kukkaro P, Lok SM, Ng JK, Tan GK, et al. (2012) Resistance analysis of an antibody that selectively inhibits dengue virus serotype-1. Antiviral Res 95: 216-223.
48. de Alwis R, Smith SA, Olivarez NP, Messer WB, Huynh JP, et al. (2012) Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc Natl Acad Sci U S A 109: 7439-7444.
49. de Alwis R, Beltramello M, Messer WB, Sukupolvi-Petty S, Wahala WM, et al. (2011) In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl Trop Dis 5: e1188.
50. Smith SA, de Alwis R, Kose N, Durbin AP, Whitehead SS, et al. (2013) Human monoclonal antibodies derived from memory B cells following live attenuated dengue virus vaccination or natural infection exhibit similar characteristics. J Infect Dis 207 (12) ():: 1898-908.
51. Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S, et al. (2010) Cross-reacting antibodies enhance dengue virus infection in humans. Science 328: 745-748.
52. Teoh EP, Kukkaro P, Teo EW, Lim AP, Tan TT, et al. (2012) The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci Transl Med 4: 139ra183.
53. Smith SA, Zhou Y, Olivarez NP, Broadwater AH, de Silva AM, et al. (2012) Persistence of circulating memory B cell clones with potential for dengue virus disease enhancement for decades following infection. J Virol 86: 2665-2675.
54. Mehlhop E, Nelson S, Jost CA, Gorlatov S, Johnson S, et al. (2009) Complement protein C1q reduces the stoichiometric threshold for antibody-mediated neutralization of West Nile virus. Cell Host Microbe 6: 381-391.
55. Garcia G, Arango M, Perez AB, Fonte L, Sierra B, et al. (2006) Antibodies from patients with dengue viral infection mediate cellular cytotoxicity. J Clin Virol 37: 53-57.
56. Kurane I, Hebblewaite D, Brandt WE, Ennis FA, (1984) Lysis of dengue virus-infected cells by natural cell-mediated cytotoxicity and antibody-dependent cell-mediated cytotoxicity. J Virol 52: 223-230.
57. Laoprasopwattana K, Libraty DH, Endy TP, Nisalak A, Chunsuttiwat S, et al. (2007) Antibody-dependent cellular cytotoxicity mediated by plasma obtained before secondary dengue virus infections: potential involvement in early control of viral replication. J Infect Dis 195: 1108-1116.
58. Barrett AD, Teuwen DE, (2009) Yellow fever vaccine- how does it work and why do rare cases of serious adverse events take place? Curr Opin Immunol 21: 308-313.
59. Halstead SB, Thomas SJ, (2010) Japanese encephalitis: new options for active immunization. Clin Infect Dis 50: 1155-1164.
60. Sabin AB, (1952) Research on dengue during World War II. Am J Trop Med Hyg 1: 30-50.
61. Gromowski GD, Roehrig JT, Diamond MS, Lee JC, Pitcher TJ, et al. (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.
62. Wahala WM, Donaldson EF, de Alwis R, Accavitti-Loper MA, Baric RS, et al. (2010) Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS Pathog 6: e1000821.
63. Brien JD, Austin SK, Sukupolvi-Petty S, O'Brien KM, Johnson S, et al. (2010) Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J Virol 84: 10630-10643.
64. Kliks SC, Nisalak A, Brandt WE, Wahl L, Burke DS, (1989) Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg 40: 444-451.
65. Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, et al. (1989) Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J Gen Virol 70 (Pt 1) (): 37-43.
66. De Madrid AT, Porterfield JS, (1974) The flaviviruses (group B arboviruses): a cross-neutralization study. J Gen Virol 23: 91-96.
67. Sabchareon A, Wallace D, Sirivichayakul C, Limkittikul K, Chanthavanich P, et al. (2012) Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380: 1559-1567.
68. Durbin AP, Kirkpatrick BD, Pierce KK, Schmidt AC, Whitehead SS, (2011) Development and clinical evaluation of multiple investigational monovalent DENV vaccines to identify components for inclusion in a live attenuated tetravalent DENV vaccine. Vaccine 29: 7242-7250.
69. Whitehead SS, Falgout B, Hanley KA, Blaney JE Jr, Jr, Markoff L, et al. (2003) A live, attenuated dengue virus type 1 vaccine candidate with a 30-nucleotide deletion in the 3′ untranslated region is highly attenuated and immunogenic in monkeys. J Virol 77: 1653-1657.
70. Whitehead SS, Hanley KA, Blaney JE Jr, Gilmore LE, Elkins WR, et al. (2003) Substitution of the structural genes of dengue virus type 4 with those of type 2 results in chimeric vaccine candidates which are attenuated for mosquitoes, mice, and rhesus monkeys. Vaccine 21: 4307-4316.
71. Zhang Y, Zhang W, Ogata S, Clements D, Strauss JH, et al. (2004) Conformational changes of the flavivirus E glycoprotein. Structure 12: 1607-1618.
72. Durbin AP, McArthur JH, Marron JA, Blaney JE, Thumar B, et al. (2006) rDEN2/4Delta30(ME), a live attenuated chimeric dengue serotype 2 vaccine is safe and highly immunogenic in healthy dengue-naive adults. Hum Vaccin 2: 255-260.
73. Durbin AP, McArthur J, Marron JA, Blaney JE Jr, Thumar B, et al. (2006) The live attenuated dengue serotype 1 vaccine rDEN1Delta30 is safe and highly immunogenic in healthy adult volunteers. Hum Vaccin 2: 167-173.
74. Nelson S, Jost CA, Xu Q, Ess J, Martin JE, et al. (2008) Maturation of West Nile virus modulates sensitivity to antibody-mediated neutralization. PLoS Pathog 4: e1000060.
75. Oliphant T, Nybakken GE, Austin SK, Xu Q, Bramson J, et al. (2007) Induction of epitope-specific neutralizing antibodies against West Nile virus. J Virol 81: 11828-11839.
76. 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.
77. Pierson TC, Sanchez MD, Puffer BA, Ahmed AA, Geiss BJ, et al. (2006) A rapid and quantitative assay for measuring antibody-mediated neutralization of West Nile virus infection. Virology 346: 53-65.
78. 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 Microbe 1: 135-145.
79. Klasse PJ, Sattentau QJ, (2001) Mechanisms of virus neutralization by antibody. Curr Top Microbiol Immunol 260: 87-108.
80. Andrewes CH, Elford WJ, (1933) Observations on Anti-Phage Sera. I: "The Percentage Law". British Journal of Experimental Pathology 14: 367-376.
81. Dowd KA, Jost CA, Durbin AP, Whitehead SS, Pierson TC, (2011) A dynamic landscape for antibody binding modulates antibody-mediated neutralization of West Nile virus. PLoS Pathog 7: e1002111.
82. 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.
83. Sabo MC, Luca VC, Ray SC, Bukh J, Fremont DH, et al. (2012) Hepatitis C virus epitope exposure and neutralization by antibodies is affected by time and temperature. Virology 422: 174-184.
84. Witz J, Brown F, (2001) Structural dynamics, an intrinsic property of viral capsids. Arch Virol 146: 2263-2274.
85. Lin J, Lee LY, Roivainen M, Filman DJ, Hogle JM, et al. (2012) Structure of the Fab-labeled "breathing" state of native poliovirus. J Virol 86: 5959-5962.
86. Durbin AP, Whitehead SS, Shaffer D, Elwood D, Wanionek K, et al. (2011) A single dose of the DENV-1 candidate vaccine rDEN1Delta30 is strongly immunogenic and induces resistance to a second dose in a randomized trial. PLoS Negl Trop Dis 5: e1267.
87. Lin TY, Dowd KA, Manhart CJ, Nelson S, Whitehead SS, et al. (2012) A novel approach for the rapid mutagenesis and directed evolution of the structural genes of west nile virus. J Virol 86: 3501-3512.
88. 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.
89. 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.
90. Wahala WM, Huang C, Butrapet S, White LJ, de Silva AM, (2012) Recombinant dengue type 2 viruses with altered e protein domain III epitopes are efficiently neutralized by human immune sera. J Virol 86: 4019-4023.
91. Strengell M, Ikonen N, Ziegler T, Julkunen I, (2011) Minor changes in the hemagglutinin of influenza A(H1N1)2009 virus alter its antigenic properties. PLoS One 6: e25848.
92. Walker LM, Simek MD, Priddy F, Gach JS, Wagner D, et al. (2010) A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog 6: e1001028.
93. Moore PL, Ranchobe N, Lambson BE, Gray ES, Cave E, et al. (2009) Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog 5: e1000598.
94. Murphy MK, Yue L, Pan R, Boliar S, Sethi A, et al. (2013) Viral Escape from Neutralizing Antibodies in Early Subtype A HIV-1 Infection Drives an Increase in Autologous Neutralization Breadth. PLoS Pathog 9: e1003173.
95. Resch W, Zaslavsky L, Kiryutin B, Rozanov M, Bao Y, et al. (2009) Virus variation resources at the National Center for Biotechnology Information: dengue virus. BMC Microbiol 9: 65.
96. Kaufmann B, Vogt MR, Goudsmit J, Holdaway HA, Aksyuk AA, et al. (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 U S A 107: 18950-18955.
97. Nybakken GE, Oliphant T, Johnson S, Burke S, Diamond MS, et al. (2005) Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 437: 764-769.
98. Johnson JE, (2003) Virus particle dynamics. Adv Protein Chem 64: 197-218.
99. Cockburn JJ, Navarro Sanchez ME, Fretes N, Urvoas A, Staropoli I, et al. (2012) Mechanism of dengue virus broad cross-neutralization by a monoclonal antibody. Structure 20: 303-314.
100. Austin SK, Dowd KA, Shrestha B, Nelson CA, Edeling MA, et al. (2012) Structural basis of differential neutralization of DENV-1 genotypes by an antibody that recognizes a cryptic epitope. PLoS Pathog 8: e1002930.
101. Ansarah-Sobrinho C, Nelson S, Jost CA, Whitehead SS, Pierson TC, (2008) Temperature-dependent production of pseudoinfectious dengue reporter virus particles by complementation. Virology 381: 67-74.
102. 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.
103. Huang CC, Couch GS, Pettersen EF, Ferrin TE, (1996) Chimera: An Extensible Molecular Modeling Application Constructed Using Standard Components. Pacific Symposium on Biocomputing 1.
104. Zhang X, Sheng J, Plevka P, Kuhn RJ, Diamond MS, et al. (2013) Dengue structure differs at the temperatures of its human and mosquito hosts. Proc Natl Acad Sci U S A 110: 6795-6799.
105. Fibriansah G, Ng TS, Kostyuchenko VA, Lee J, Lee S, et al. (2013) Structural changes in dengue virus when exposed to a temperature of 37 degrees C. J Virol 87: 7585-7592.
106. Mukherjee S, Lin TY, Dowd KA, Manhart CJ, Pierson TC, (2011) The infectivity of prM-containing partially mature West Nile virus does not require the activity of cellular furin-like proteases. J Virol 85: 12067-12072.
107. Obara CJ, Dowd KA, Ledgerwood JE, Pierson TC, (2013) Impact of viral attachment factor expression on antibody-mediated neutralization of flaviviruses. Virology 437: 20-27.