Receptors and routes of dengue virus entry into the host cells

FEMS Microbiology Reviews

Volumn 39, Issue 2, 2015, Pages 155-170

  Cruz Oliveira, Christine ^a   Freire, João Miguel ^b   Conceição, Thaís M ^a   Higa, Luiza M ^a   Castanho, Miguel A R B ^b   Da Poian, Andrea T ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

Author keywords

Flavivirus; Genome translocation; Internalization routes; Membrane fusion; Viral structural proteins; Virus recognition

Indexed keywords

CAPSID PROTEIN; CELL RECEPTOR; CLATHRIN; ENVELOPE PROTEIN; FC RECEPTOR; VIRUS PROTEIN; PROTEIN BINDING; VIRUS RECEPTOR;

ANTIGEN ANTIBODY COMPLEX; CELL SURFACE; CELLS; CONFORMATIONAL TRANSITION; CYTOPLASM; DENGUE VIRUS; DENGUE VIRUS 1; DENGUE VIRUS 2; DENGUE VIRUS 3; DENGUE VIRUS 4; ENDOCYTOSIS; GENOME; HOST CELL; HUMAN; IMMUNOCOMPETENT CELL; MAMMAL CELL; MEMBRANE FUSION; MOSQUITO; NONHUMAN; PH; REVIEW; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENOME; VIRUS STRAIN; ANIMAL; DENGUE; HOST PATHOGEN INTERACTION; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; DENGUE; DENGUE VIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; RECEPTORS, VIRUS; VIRUS INTERNALIZATION;

EID: 84928213004     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fuu004     Document Type: Review

References (146)

1. Acosta EG, Castilla V, Damonte EB. Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin-mediated endocytosis. J Gen Virol 2008;89:474-84.
2. Acosta EG, Castilla V, Damonte EB. Alternative infectious entry pathways for dengue virus serotypes into mammalian cells. Cell Microbiol 2009;11:1533-49.
3. Acosta EG, Castilla V, Damonte EB. Infectious dengue-1 virus entry into mosquito C6/36 cells. Virus Res 2011;160:173-9.
4. Acosta EG, Castilla V, Damonte EB. Differential requirements in endocytic trafficking for penetration of dengue virus. PLoS One 2012;7:e44835.
5. Acosta EG, Piccini LE, Talarico LB, et al. Changes in antiviral susceptibility to entry inhibitors and endocytic uptake of dengue-2 virus serially passaged in Vero or C6/36 cells. Virus Res 2014;184:39-43.
6. Alhoot MA, Wang SM, Sekaran SD. RNA interference mediated inhibition of dengue virusmultiplication and entry in HepG2 cells. PLoS One 2012;7:e34060.
7. Anez G, Men R, Eckels KH, et al. Passage of dengue virus type 4 vaccine candidates in fetal rhesus lung cells selects heparin-sensitive variants that result in loss of infectivity and immunogenicity in rhesus macaques. J Virol 2009;83:10384-94.
8. Ang F, Wong AP, Ng MM, et al. Small interference RNA profiling reveals the essential role of human membrane trafficking genes in mediating the infectious entry of dengue virus. Virol J 2010;7:24.
9. Aoki C, Hidari KI, Itonori S, et al. Identification and characterization of carbohydrate molecules in mammalian cells recognized by dengue virus type 2. J Biochem 2006;139:607-14.
10. Artpradit C, Robinson LN, Gavrilov BK, et al. Recognition of heparan sulfate by clinical strains of dengue virus serotype 1 using recombinant subviral particles. Virus Res 2013;176:69-77.
11. Beltramello M, Williams KL, Simmons CP, et al. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowedwith neutralizing and enhancing activity. Cell Host Microbe 2010;8:271-83.
12. Bryant JE, Calvert AE, Mesesan K, et al. Glycosylation of the dengue 2 virus E protein at N67 is critical for virus growth in vitro but not for growth in intrathoracically inoculated Aedes aegypti mosquitoes. Virology 2007;366:415-23.
13. Cao-Lormeau VM. Dengue viruses binding proteins from Aedes aegypti and Aedes polynesiensis salivary glands. Virol J 2009;6:35.
14. Cardosa MJ, Wang SM, Sum MS, et al. Antibodies against prM protein distinguish between previous infection with dengue and Japanese encephalitis viruses. BMC Microbiol 2002;2:9.
15. Chavez JH, Silva JR, Amarilla AA, et al. Domain III peptides from flavivirus envelope protein are useful antigens for serologic diagnosis and targets for immunization. Biologicals 2010;38:613-8.
16. Che P, Tang H, Li Q. The interaction between claudin-1 and dengue viral prM/M protein for its entry. Virology 2013;446:303-13.
17. Chen Y, Maguire T, Hileman RE, et al. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 1997;3:866-71.
18. Chen YC, Wang SY, King CC. Bacterial lipopolysaccharide inhibits dengue virus infection of primary human monocytes/macrophages by blockade of virus entry via a CD14-dependent mechanism. J Virol 1999;73:2650-7.
19. Chin JF, Chu JJ, Ng ML. The envelope glycoprotein domain III of dengue virus serotypes 1 and 2 inhibit virus entry. Microbes Infect 2007;9:1-6.
20. Costin JM, Zaitseva E, Kahle KM, et al. Mechanistic study of broadly neutralizing human monoclonal antibodies against dengue virus that target the fusion loop. J Virol 2013;87:52-66.
21. Crill WD, Roehrig JT. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are themost efficient blockers of virus adsorption to Vero cells. J Virol 2001;75:7769-73.
22. Da Poian AT, Carneiro FA, Stauffer F. Viral membrane fusion: is glycoprotein G of rhabdoviruses a representative of a new class of viral fusion proteins? Braz J Med Biol Res 2005;38:813-23.
23. Daecke J, Fackler OT, Dittmar MT, et al. Involvement of clathrinmediated endocytosis in human immunodeficiency virus type 1 entry. J Virol 2005;79:1581-94.
24. Dalrymple N, Mackow ER. Productive dengue virus infection of human endothelial cells is directed by heparan sulfate-containing proteoglycan receptors. J Virol 2011;85:9478-85.
25. de Alwis R, Beltramello M, Messer WB, et al. In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Neglect Trop D 2011;5:e1188.
26. Dejnirattisai W, Jumnainsong A, Onsirisakul N, et al. Crossreacting antibodies enhance dengue virus infection in humans. Science 2010;328:745-8.
27. Dejnirattisai W, Webb AI, Chan V, et al. Lectin switching during dengue virus infection. J Infect Dis 2011;203:1775-83.
28. Duan X, Lu X, Li J, et al. Novel binding between pre-membrane protein and vacuolar ATPase is required for efficient dengue virus secretion. Biochem Bioph Res Co 2008;373:319-24.
29. Fibriansah G, Ng TS, Kostyuchenko VA, et al. Structural changes in dengue virus when exposed to a temperature of 37 degrees C. J Virol 2013;87:7585-92.
30. Fibriansah G, Tan JL, Smith SA, et al. A potent anti-dengue human antibody preferentially recognizes the conformation of E protein monomers assembled on the virus surface. EMBO Mol Med 2014;6:358-71.
31. Freire JM, Veiga AS, Conceicao TM, et al. Intracellular nucleic acid delivery by the supercharged dengue virus capsid protein. PLoS One 2013b;8:e81450.
32. Freire JM, Veiga AS, de la Torre BG, et al. Peptides as models for the structure and function of viral capsid proteins: Insights on dengue virus capsid. Biopolymers 2013a;100:325-36.
33. Freire JM, Veiga AS, Rego de Figueiredo I, et al. Nucleic acid delivery by cell penetrating peptides derived from dengue virus capsid protein: design and mechanism of action. FEBS J 2014;281:191-215.
34. Gao F, Duan X, Lu X, et al. Novel binding between pre-membrane protein and claudin-1 is required for efficient dengue virus entry. Biochem Bioph Res Co 2010;391:952-7.
35. Ge P, Zhou ZH. Chaperone fusion proteins aid entropy-driven maturation of class II viral fusion proteins. Trends Microbiol 2014;22:100-6.
36. Germi R, Crance JM, Garin D, et al. Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology 2002;292:162-8.
37. Goncalvez AP, Engle RE, StClaire M, et al. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. P Natl Acad Sci USA 2007;104:9422-7.
38. Goncalvez AP, Purcell RH, Lai CJ. 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 2004;78:12919-28.
39. Grove J, Marsh M. The cell biology of receptor-mediated virus entry. J Cell Biol 2011;195:1071-82.
40. Gubler DJ. Dengue/dengue haemorrhagic fever: history and current status. Novartis Fdn Symp 2006;277:3-16.
41. Guzman MG, Alvarez M, Halstead SB. 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 2013;158:1445-59.
42. Hacker K, White L, de Silva AM. N-linked glycans on dengue viruses grown in mammalian and insect cells. J Gen Virol 2009;90:2097-106.
43. Harris HJ, Davis C, Mullins JG, et al. Claudin association with CD81 defines hepatitis C virus entry. J Biol Chem 2010;285:21092-102.
44. Harrison SC. Viral membrane fusion. Nat Struct Mol Biol 2008;15:690-8.
45. Henchal EA, McCown JM, Burke DS, et al. Epitopic analysis of antigenic determinants on the surface of dengue-2 virions using monoclonal antibodies. Am J Trop Med Hyg 1985;34:162-9.
46. Hidari KI, Suzuki T. Dengue virus receptor. Trop Med Health 2011;39:37-43.
47. Higa LM, Curi BM, Aguiar RS, et al. Modulation of alpha-enolase post-translational modifications by dengue virus: increased secretion of the basic isoforms in infected hepatic cells. PLoS One 2014;9:e88314.
48. Huang KJ, Yang YC, Lin YS, et al. Flow cytometric determination for dengue virus-infected cells: its application for antibody-dependent enhancement study. Dengue Bulletin 2005;29:142-50.
49. Huang KJ, Yang YC, Lin YS, et al. The dual-specific binding of dengue virus and target cells for the antibodydependent enhancement of dengue virus infection. J Immunol 2006;176:2825-32.
50. Hubner W, McNerney GP, Chen P, et al. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 2009;323:1743-7.
51. Hung JJ, Hsieh MT, Young MJ, et al. An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding tomosquito but not mammalian cells. J Virol 2004;78:378-88.
52. Jemielity S, Wang JJ, Chan YK, et al. TIM-family proteins promote infection ofmultiple enveloped viruses through virion-associated phosphatidylserine. PLoS Pathog 2013;9:e1003232.
53. Jindadamrongwech S, Smith DR. Virus Overlay Protein Binding Assay (VOPBA) reveals serotype specific heterogeneity of dengue virus binding proteins on HepG2 human liver cells. Intervirology 2004;47:370-3.
54. Jindadamrongwech S, Thepparit C, Smith DR. Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2. Arch Virol 2004;149:915-27.
55. Johnson AJ, Guirakhoo F, Roehrig JT. The envelope glycoproteins of dengue 1 and dengue 2 viruses grown in mosquito cells differ in their utilization of potential glycosylation sites. Virology 1994;203:241-9.
56. Junjhon J, Edwards TJ, Utaipat U, et al. Influence of pr-M cleavage on the heterogeneity of extracellular dengue virus particles. J Virol 2010;84:8353-8.
57. Klein DE, Choi JL, Harrison SC. Structure of a dengue virus envelope protein late-stage fusion intermediate. J Virol 2013;87:2287-93.
58. Kobayashi T, Beuchat MH, Chevallier J, et al. Separation and characterization of late endosomal membrane domains. J Biol Chem 2002;277:32157-64.
59. Krishnan MN, Sukumaran B, Pal U, et al. Rab 5 is required for the cellular entry of dengue and West Nile viruses. J Virol 2007;81:4881-5.
60. Kuadkitkan A, Wikan N, Fongsaran C, et al. Identification and characterization of prohibitin as a receptor protein mediating DENV-2 entry into insect cells. Virology 2010;406:149-61.
61. Kuhn RJ, Zhang W, Rossmann MG, et al. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 2002;108:717-25.
62. Lai CY, Tsai WY, Lin SR, et al. 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 2008;82:6631-43.
63. Lee E, Wright PJ, Davidson A, et al. Virulence attenuation of Dengue virus due to augmented glycosaminoglycan-binding affinity and restriction in extraneural dissemination. J Gen Virol 2006;87:2791-801.
64. Li L, Lok SM, Yu IM, et al. The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 2008;319:1830-4.
65. Lin YL, Lei HY, Lin YS, et al. Heparin inhibits dengue-2 virus infection of five human liver cell lines. Antivir Res 2002;56:93-6.
66. Liu S, Yang W, Shen L, et al. Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are down-regulated during infection to prevent superinfection. J Virol 2009;83:2011-4.
67. Luo YY, Feng JJ, Zhou JM, et al. Identification of a novel infection-enhancing epitope on dengue prM using a dengue cross-reacting monoclonal antibody. BMC Microbiol 2013;13:194.
68. Ma L, Jones CT, Groesch TD, et al. Solution structure of dengue virus capsid protein reveals another fold. P Natl Acad Sci USA 2004;101:3414-9.
69. McNaughton BR, Cronican JJ, Thompson DB, et al. Mammalian cell penetration, siRNA transfection, and DNA transfection by supercharged proteins. P Natl Acad Sci USA 2009;106:6111-6.
70. Marovich M, Grouard-Vogel G, Louder M, et al. Human dendritic cells as targets of dengue virus infection. J Invest Derm Symp P 2001;6:219-24.
71. Martinez-Barragan JJ, del Angel RM. Identification of a putative coreceptor on Vero cells that participates in dengue 4 virus infection. J Virol 2001;75:7818-27.
72. Martins IC, Gomes-Neto F, Faustino AF, et al. The disordered N-terminal region of dengue virus capsid protein contains a lipid-droplet-binding motif. Biochem J 2012;444:405-15.
73. Masrinoul P, Omokoko MD, Pambudi S, et al. Serotype-specific anti-Dengue virus NS1 mouse antibodies cross-react with prM and are potentially involved in virus production. Viral Immunol 2013;26:250-8.
74. Meertens L, Bertaux C, Cukierman L, et al. The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. J Virol 2008;82:3555-60.
75. Meertens L, Carnec X, Lecoin MP, et al. The TIM and TAMfamilies of phosphatidylserine receptors mediate dengue virus entry. Cell Host Microbe 2012;12:544-57.
76. Melikyan GB. HIV entry: a game of hide-and-fuse? Curr Opin Virol 2014;4:1-7.
77. Mercado-Curiel RF, Black WCt, Munoz Mde L. A dengue receptor as possible genetic marker of vector competence in Aedes aegypti. BMC Microbiol 2008;8:118.
78. Mercado-Curiel RF, Esquinca-Aviles HA, Tovar R, et al. The four serotypes of dengue recognize the same putative receptors in Aedes aegypti midgut and Ae. albopictus cells. BMC Microbiol 2006;6:85.
79. Mercer J, Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008;320:531-5.
80. Miller JL, de Wet BJ, Martinez-Pomares L, et al. The mannose receptor mediates dengue virus infection of macrophages. PLoS Pathog 2008;4:e17.
81. Miyauchi K, Kim Y, Latinovic O, et al. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 2009;137:433-44.
82. Modis Y. Relating structure to evolution in class II viral membrane fusion proteins. Curr Opin Virol 2014;5: 34-41.
83. Modis Y, Ogata S, Clements D, et al. A ligand-binding pocket in the dengue virus envelope glycoprotein. P Natl Acad Sci USA 2003;100:6986-91.
84. Modis Y, Ogata S, Clements D, et al. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004;427:313-9.
85. Modis Y, Ogata S, Clements D, et al. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J Virol 2005;79:1223-31.
86. Mondotte JA, Lozach PY, Amara A, et al. Essential role of dengue virus envelope protein N glycosylation at asparagine-67 during viral propagation. J Virol 2007;81:7136-48.
87. Mosso C, Galvan-Mendoza IJ, Ludert JE, et al. Endocytic pathway followed by dengue virus to infect the mosquito cell line C6/36 HT. Virology 2008;378:193-9.
88. Mukhopadhyay S, Kuhn RJ, Rossmann MG. A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 2005;3:13-22.
89. Munoz ML, Cisneros A, Cruz J, et al. Putative dengue virus receptors from mosquito cells. FEMS Microbiol Lett 1998;168:251-8.
90. Munoz Mde L, Limon-Camacho G, Tovar R, et al. Proteomic identification of dengue virus binding proteins in Aedes aegypti mosquitoes and Aedes albopictus cells. Biomed Res Int 2013;2013:875958.
91. Murphy BR, Whitehead SS. Immune response to dengue virus and prospects for a vaccine. Annu Rev Immunol 2011;29:587-619.
92. Navarro-Sanchez E, Altmeyer R, Amara A, et al. 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 2003;4:723-8.
93. Nour AM, Li Y, Wolenski J, et al. Viral membrane fusion and nucleocapsid delivery into the cytoplasm are distinct events in some flaviviruses. PLoS Pathog 2013;9:e1003585.
94. Nour AM, Modis Y. Endosomal vesicles as vehicles for viral genomes. Trends Cell Biol 2014;24:449-54.
95. Padilla-Parra S, Marin M, Gahlaut N, et al. Fusion of mature HIV-1 particles leads to complete release of a gag-GFP-based content marker and raises the intraviral pH. PLoS One 2013;8:e71002.
96. Perera R, Kuhn RJ. Structural proteomics of dengue virus. Curr Opin Microbiol 2008;11:369-77.
97. Perera-Lecoin M, Meertens L, Carnec X, et al. Flavivirus entry receptors: an update. Viruses 2014;6:69-88.
98. Pierson TC, Kielian M. Flaviviruses: braking the entering. Curr Opin Virol 2013;3:3-12.
99. Pokidysheva E, Zhang Y, Battisti AJ, et al. Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 2006;124:485-93.
100. Prestwood TR, Prigozhin DM, Sharar KL, et al. Amouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J Virol 2008;82:8411-21.
101. Puerta-Guardo H, Mosso C, Medina F, et al. Antibody-dependent enhancement of dengue virus infection in U937 cells requires cholesterol-rich membrane microdomains. J Gen Virol 2010;91:394-403.
102. Ramos-Castaneda J, Imbert JL, Barron BL, et al. A 65-kDa trypsinsensible membrane cell protein as a possible receptor for dengue virus in cultured neuroblastoma cells. J Neurovirol 1997;3:435-40.
103. Randolph VB, Winkler G, Stollar V. Acidotropic amines inhibit proteolytic processing of flavivirus prM protein. Virology 1990;174:450-8.
104. Reyes-del Valle J, Chavez-Salinas S, Medina F, et al. Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J Virol 2005;79:4557-67.
105. Reyes-del Valle J, del Angel RM. Isolation of putative dengue virus receptor molecules by affinity chromatography using a recombinant E protein ligand. J Virol Methods 2004;116:95-102.
106. Rodenhuis-Zybert IA, van der Schaar HM, da Silva Voorham JM, et al. Immature dengue virus: a veiled pathogen? PLoS Pathog 2010;6:e1000718.
107. Rodenhuis-Zybert IA, Wilschut J, Smit JM. Dengue virus life cycle: viral and host factors modulating infectivity. Cell Mol Life Sci 2010;67:2773-86.
108. Rodenhuis-Zybert IA, Wilschut J, Smit JM. Partial maturation: an immune-evasion strategy of dengue virus? Trends Microbiol 2011;19:248-54.
109. Rothman AL. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat Rev Immunol 2011;11:532-43.
110. Sakoonwatanyoo P, Boonsanay V, Smith DR. Growth and production of the dengue virus in C6/36 cells and identification of a laminin-binding protein as a candidate serotype 3 and 4 receptor protein. Intervirology 2006;49:161-72.
111. Sakuntabhai A, Turbpaiboon C, Casademont I, et al. A variant in the CD209 promoter is associated with severity of dengue disease. Nat Genet 2005;37:507-13.
112. Salas-Benito JS, delAngel RM. Identification of two surface proteins from C6/36 cells that bind dengue type 4 virus. J Virol 1997;71:7246-52.
113. Samsa MM, Mondotte JA, Iglesias NG, et al. Dengue virus capsid protein usurps lipid droplets for viral particle formation. PLoS Pathog 2009;5:e1000632.
114. Se-Thoe SY, Ng MM, Ling AE. Retrospective study of Western blot profiles in immune sera of natural dengue virus infections. J Med Virol 1999;57:322-30.
115. Shapiro J, Sciaky N, Lee J, et al. Localization of endogenous furin in cultured cell lines. J Histochem Cytochem 1997;45:3-12.
116. Smit JM, Moesker B, Rodenhuis-Zybert I, et al. Flavivirus cell entry and membrane fusion. Viruses 2011;3:160-71.
117. Suksanpaisan L, Susantad T, Smith DR. Characterization of dengue virus entry into HepG2 cells. J Biomed Sci 2009;16:17.
118. Suomalainen M, Greber UF. Uncoating of non-enveloped viruses. Curr Opin Virol 2013;3:27-33.
119. Tassaneetrithep B, Burgess TH, Granelli-Piperno A, et al. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 2003;197:823-9.
120. Thepparit C, Phoolcharoen W, Suksanpaisan L, et al. Internalization and propagation of the dengue virus in human hepatoma (HepG2) cells. Intervirology 2004;47:78-86.
121. Thepparit C, Smith DR. Serotype-specific entry of dengue virus into liver cells: identification of the 37-kilodalton/67-kilodalton high-affinity laminin receptor as a dengue virus serotype 1 receptor. J Virol 2004;78:12647-56.
122. Thompson DB, Cronican JJ, Liu DR. Engineering and identifying supercharged proteins for macromolecule delivery into mammalian cells. Methods Enzymol 2012;503:293-319.
123. Upanan S, Kuadkitkan A, Smith DR. Identification of dengue virus binding proteins using affinity chromatography. J Virol Methods 2008;151:325-8.
124. Usme-Ciro JA, Campillo-Pedroza N, Almazan F, et al. Cytoplasmic RNA viruses as potential vehicles for the delivery of therapeutic small RNAs. Virol J 2013;10:185.
125. van der Schaar HM, Rust MJ, Chen C, et al. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog 2008;4:e1000244.
126. van der Schaar HM, Rust MJ, Waarts BL, et al. Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J Virol 2007;81:12019-28.
127. van Meer G, Voelker DR, Feigenson GW. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 2008;9:112-24.
128. Vancini R, Kramer LD, Ribeiro M, et al. Flavivirus infection from mosquitoes in vitro reveals cell entry at the plasma membrane. Virology 2013;435:406-14.
129. Vaughan K, Greenbaum J, Blythe M, et al. Meta-analysis of all immune epitope data in the Flavivirus genus: inventory of current immune epitope data status in the context of virus immunity and immunopathology. Viral Immunol 2010;23:259-84.
130. Watterson D, Kobe B, Young PR. Residues in domain III of the dengue virus envelope glycoprotein involved in cell-surface glycosaminoglycan binding. J Gen Virol 2012;93:72-82.
131. Wei HY, Jiang LF, Fang DY, et al. Dengue virus type 2 infects human endothelial cells through binding of the viral envelope glycoprotein to cell surface polypeptides. J Gen Virol 2003;84:3095-8.
132. WHO. WHO Report on Global Surveillance of Epidemic-prone Infectious Diseases - Dengue and Dengue Haemorrhagic Fever. 2014. http://www.who.int/csr/resources/publications/dengue/CSR?ISR?2000?1/en/. Last accessed in April 15th, 2014.
133. Wichit S, Jittmittraphap A, Hidari KI, et al. Dengue virus type 2 recognizes the carbohydrate moiety of neutral glycosphingolipids in mammalian and mosquito cells. Microbiol Immunol 2011;55:135-40.
134. Wu SJ, Grouard-Vogel G, Sun W, et al. Human skin Langerhans cells are targets of dengue virus infection. Nat Med 2000;6:816-20.
135. Yazi Mendoza M, Salas-Benito JS, Lanz-Mendoza H, et al. A putative receptor for dengue virus in mosquito tissues: localization of a 45-kDa glycoprotein. Am J Trop Med Hyg 2002;67:76-84.
136. Yu IM, Holdaway HA, Chipman PR, et al. Association of the pr peptides with dengue virus at acidic pH blocks membrane fusion. J Virol 2009;83:12101-7.
137. Yu IM, Zhang W, Holdaway HA, et al. Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 2008;319:1834-7.
138. Zaitseva E, Yang ST, Melikov K, et al. Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog 2010;6:e1001131.
139. Zhang W, Chipman PR, Corver J, et al. Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat Struct Biol 2003a;10:907-12.
140. Zhang X, Ge P, Yu X, et al. Cryo-EM structure of the mature dengue virus at 3.5-A resolution. Nat Struct Mol Biol 2013a;20:105-10.
141. Zhang X, Sheng J, Plevka P, et al. Dengue structure differs at the temperatures of its human and mosquito hosts. P Natl Acad Sci USA 2013b;110:6795-9.
142. Zhang Y, Corver J, Chipman PR, et al. Structures of immature flavivirus particles. EMBO J 2003b;22:2604-13.
143. Zhang Y, Zhang W, Ogata S, et al. Conformational changes of the flavivirus E glycoprotein. Structure 2004;12:1607-18.
144. Zheng A, Umashankar M, Kielian M. In vitro and in vivo studies identify important features of dengue virus pr-E protein interactions. PLoS Pathog 2010;6:e1001157.
145. Zhong P, Agosto LM, Munro JB, et al. Cell-to-cell transmission of viruses. Curr Opin Virol 2013;3:44-50.
146. Zybert IA, van der Ende-Metselaar H, Wilschut J, et al. Functional importance of dengue virus maturation: infectious properties of immature virions. J Gen Virol 2008;89:3047-51.