Replication cycle of chikungunya: A re-emerging arbovirus

Virology

Volumn 393, Issue 2, 2009, Pages 183-197

  Solignat, Maxime ^a   Gay, Bernard ^a   Higgs, Stephen ^b   Briant, Laurence ^a   Devaux, Christian ^a  

^a University of Montpellier I and II   (France)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Arbovirus; Chikungunya; Replicative cycle; Virus host interaction

Indexed keywords

5,5' DITHIOBIS(2 NITROBENZOIC ACID); ALPHA INTERFERON; CHLOROQUINE; DACTINOMYCIN; DECANOYL ARGINYLVALYLLYSYLARGININE CHLOROMETHYL KETONE; INTERFERON; KETONE DERIVATIVE; NEUTRALIZING ANTIBODY; NEVAQUINE; RIBAVIRIN; UNCLASSIFIED DRUG; VIRUS VACCINE;

ALPHA VIRUS; ANTIVIRAL THERAPY; ARBOVIRUS; CHIKUNGUNYA ALPHAVIRUS; CLINICAL TRIAL; EPIDEMIC; EVOLUTION; FATALITY; HUMAN; INDIA; INDIAN OCEAN; INFECTION RISK; MORTALITY; MOSQUITO; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REUNION; SCIENTIST; SEROPREVALENCE; SHORT SURVEY; VACCINATION; VIROGENESIS; VIRUS CARRIER; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTION; VIRUS REPLICATION;

ALPHAVIRUS INFECTIONS; ARBOVIRUSES; CHIKUNGUNYA VIRUS; CLATHRIN; DISEASE OUTBREAKS; ENDOCYTOSIS; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; PHYLOGENY; REUNION; SEROEPIDEMIOLOGIC STUDIES; VIRUS REPLICATION;

ARBOVIRUS; ARTHROPODA; CHIKUNGUNYA VIRUS; MOSQUITO-BORNE VIRUSES; VERTEBRATA;

EID: 70350001140     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.07.024     Document Type: Short Survey

References (146)

1. Arankalle V.A., Shrivastava S., Cherian S., Gunjikar R.S., Walimbe A.M., Jadhav S.M., Sudeep A.B., and Mishra A.C. Genetic divergence of Chikungunya viruses in India (1963-2006) with special reference to the 2005-2006 explosive epidemic. J. Gen. Virol. 88 Pt 7 (2007) 1967-1976
2. Barton D.J., Sawicki S.G., and Sawicki D.L. Solubilization and immunoprecipitation of alphavirus replication complexes. J. Virol. 65 3 (1991) 1496-1506
3. Berger S.A. GIDEON: a comprehensive Web-based resource for geographic medicine. Int. J. Health Geogr. 4 1 (2005) 10
4. Briant L., Robert-Hebmann V., Sivan V., Brunet A., Pouyssegur J., and Devaux C. Involvement of extracellular signal-regulated kinase module in HIV-mediated CD4 signals controlling activation of nuclear factor-kappa B and AP-1 transcription factors. J. Immunol. 160 4 (1998) 1875-1885
5. Brighton S.W. Chloroquine phosphate treatment of chronic chikungunya arthritis. An open pilot study. S. Afr. Med. J. 66 6 (1984) 217-218
6. Carey D.E. Chikungunya and dengue: a case of mistaken identity?. J. Hist. Med. Allied Sci. 26 3 (1971) 243-262
7. Casals J., and Brown L.V. Hemagglutination with arthropod-borne viruses. J. Exp. Med. 99 5 (1954) 429-449
8. Chambers T.J., Hahn C.S., Galler R., and Rice C.M. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 44 (1990) 649-688
9. Chanas A.C., Hubalek Z., Johnson B.K., and Simpson D.I. A comparative study of O'nyong nyong virus with Chikungunya virus and plaque variants. Arch. Virol. 59 3 (1979) 231-238
10. Charrel, R.N., Zandotti, C., and de Lamballerie, X., (2006). Complete coding sequence of chikungunya virus from La Reunion island, 2006 (human isolate). GenBank. Accession DQ443544.
11. Chevillon C., Briant L., Renaud F., and Devaux C. The chikungunya threat: an ecological and evolutionary perspective. Trends Microbiol. 16 2 (2008) 80-88
12. Choi H.K., Tong L., Minor W., Dumas P., Boege U., Rossmann M.G., and Wengler G. Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354 6348 (1991) 37-43
13. Collier N.C., Adams S.P., Weingarten H.I., and Schlesinger M.J. Inhibition of enveloped RNA virus formation by peptides corresponding to glycoproteins sequences. Antiviral Chem. Chemoter. 3 (1992) 31-36
14. Colpitts T.M., Moore A.C., Kolokoltsov A.A., and Davey R.A. Venezuelan equine encephalitis virus infection of mosquito cells requires acidification as well as mosquito homologs of the endocytic proteins Rab5 and Rab7. Virology 369 1 (2007) 78-91
15. Couderc T., Chretien F., Schilte C., Disson O., Brigitte M., Guivel-Benhassine F., Touret Y., Barau G., Cayet N., Schuffenecker I., Despres P., Arenzana-Seisdedos F., Michault A., Albert M.L., and Lecuit M. A mouse model for chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog. 4 2 (2008) e29
16. Cunningham A.L., and Fraser J.R. Ross River virus infection of human synovial cells in vitro. Aust. J. Exp. Biol. Med. Sci. 63 Pt 2 (1985) 199-204
17. Davis N.L., Willis L.V., Smith J.F., and Johnston R.E. In vitro synthesis of infectious Venezuelan equine encephalitis virus RNA from a cDNA clone: analysis of a viable deletion mutant. Virology 171 1 (1989) 189-204
18. de Curtis I., and Simons K. Dissection of Semliki Forest virus glycoprotein delivery from the trans-Golgi network to the cell surface in permeabilized BHK cells. Proc. Natl. Acad. Sci. U.S.A. 85 21 (1988) 8052-8056
19. de Lamballerie, X., and Canard, B., (2006). Communication. Meeting of the Sentinelles. France's national disease surveillance network on chikungunya. Paris, April 2006
20. De Lamballerie X., Boisson V., Reynier J.C., Enault S., Charrel R.N., Flahault A., Roques P., and Le Grand R. On chikungunya acute infection and chloroquine treatment. Vector Borne Zoonotic Dis. 8 6 (2008) 837-839
21. Doolittle R.F., Feng D.F., Tsang S., Cho G., and Little E. Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 271 5248 (1996) 470-477
22. Doxsey S.J., Brodsky F.M., Blank G.S., and Helenius A. Inhibition of endocytosis by anti-clathrin antibodies. Cell 50 3 (1987) 453-463
23. Eaton B.T., and Hapel A.J. Persistent noncytolytic togavirus infection of primary mouse muscle cells. Virology 72 1 (1976) 266-271
24. Edelman R., Tacket C.O., Wasserman S.S., Bodison S.A., Perry J.G., and Mangiafico J.A. Phase II safety and immunogenicity study of live chikungunya virus vaccine TSI-GSD-218. Am. J. Trop. Med. Hyg. 62 6 (2000) 681-685
25. Ekstrom M., Liljestrom P., and Garoff H. Membrane protein lateral interactions control Semliki Forest virus budding. EMBO J. 13 5 (1994) 1058-1064
26. Fraser J.R., and Becker G.J. Mononuclear cell types in chronic synovial effusions of Ross River virus disease. Aust. N. Z. J. Med. 14 4 (1984) 505-506
27. Fraser J.R., Ratnamohan V.M., Dowling J.P., Becker G.J., and Varigos G.A. The exanthem of Ross River virus infection: histology, location of virus antigen and nature of inflammatory infiltrate. J. Clin. Pathol. 36 11 (1983) 1256-1263
28. Fuller S.D. The T = 4 envelope of Sindbis virus is organized by interactions with a complementary T = 3 capsid. Cell 48 6 (1987) 923-934
29. Gardner C.L., Burke C.W., Tesfay M.Z., Glass P.J., Klimstra W.B., and Ryman K.D. Eastern and Venezuelan equine encephalitis viruses differ in their ability to infect dendritic cells and macrophages: impact of altered cell tropism on pathogenesis. J. Virol. 82 21 (2008) 10634-10646
30. Garoff H., Huylebroeck D., Robinson A., Tillman U., and Liljestrom P. The signal sequence of the p62 protein of Semliki Forest virus is involved in initiation but not in completing chain translocation. J. Cell Biol. 111 3 (1990) 867-876
31. Geigenmuller-Gnirke U., Nitschko H., and Schlesinger S. Deletion analysis of the capsid protein of Sindbis virus: identification of the RNA binding region. J. Virol. 67 3 (1993) 1620-1626
32. George J., and Raju R. Alphavirus RNA genome repair and evolution: molecular characterization of infectious sindbis virus isolates lacking a known conserved motif at the 3' end of the genome. J. Virol. 74 20 (2000) 9776-9785
33. Gifford G.E., and Heller E. Effect of Actinomycin D on Interferon Production by 'Active' and 'Inactive' Chikungunya Virus in Chick Cells. Nature 200 (1963) 50-51
34. Giovarelli M., Viano I., Zucca M., Valbonesi R., and Dianzani F. Effect of anti-mu-chain-specific immunosuppression on Chikungunya virus encephalitis of mice. Infect. Immun. 16 3 (1977) 849-852
35. Glass W.G., McDermott D.H., Lim J.K., Lekhong S., Yu S.F., Frank W.A., Pape J., Cheshier R.C., and Murphy P.M. CCR5 deficiency increases risk of symptomatic West Nile virus infection. J. Exp. Med. 203 1 (2006) 35-40
36. Glomb-Reinmund S., and Kielian M. The role of low pH and disulfide shuffling in the entry and fusion of Semliki Forest virus and Sindbis virus. Virology 248 2 (1998) 372-381
37. Gomatos P.J., Kaariainen L., Keranen S., Ranki M., and Sawicki D.L. Semliki Forest virus replication complex capable of synthesizing 42S and 26S nascent RNA chains. J. Gen. Virol. 49 1 (1980) 61-69
38. Gorbalenya A.E., Blinov V.M., Donchenko A.P., and Koonin E.V. An NTP-binding motif is the most conserved sequence in a highly diverged monophyletic group of proteins involved in positive strand RNA viral replication. J. Mol. Evol. 28 3 (1989) 256-268
39. Grakoui A., Levis R., Raju R., Huang H.V., and Rice C.M. A cis-acting mutation in the Sindbis virus junction region which affects subgenomic RNA synthesis. J. Virol. 63 12 (1989) 5216-5227
40. Hahn C.S., and Strauss J.H. Site-directed mutagenesis of the proposed catalytic amino acids of the Sindbis virus capsid protein autoprotease. J. Virol. 64 6 (1990) 3069-3073
41. Hahn C.S., Lustig S., Strauss E.G., and Strauss J.H. Western equine encephalitis virus is a recombinant virus. Proc. Natl. Acad. Sci. U.S.A. 85 16 (1988) 5997-6001
42. Harley D., Sleigh A., and Ritchie S. Ross River virus transmission, infection, and disease: a cross-disciplinary review. Clin. Microbiol. Rev. 14 4 (2001) 909-932 table of contents
43. Harrison R., Binn L.N., and Randall R. Comparative immunogenicities of chikungunya vaccines prepared in avian and mammalian tissues. Am. J. Trop. Med. Hyg. 16 6 (1967) 786-791
44. Harrison R., Eckels K.H., Bartelloni P.J., and Hampton C. Production and evaluation of a formalin-killed Chikungunya vaccine. J. Immunol. 107 3 (1971) 643-647
45. Harnett G.B., and Bucens M.R. Isolation of chikungunya virus in Australia. Med. J. Aust. 152 6 (1990) 328-329
46. Helenius A., Kartenbeck J., Simons K., and Fries E. On the entry of Semliki Forest virus into BHK-21 cells. J. Cell Biol. 84 2 (1980) 404-420
47. Heller E. Enhancement of Chikungunya Virus Replication and Inhibition of Interferon Production by Actinomycin D. Virology 21 (1963) 652-656
48. Higashi N., Matsumoto A., Tabata K., and Nagatomo Y. Electron microscope study of development of Chikungunya virus in green monkey kidney stable (VERO) cells. Virology 33 1 (1967) 55-69
49. Higgs S., and Beaty B.J. Natural cycles of vector-borne pathogens. In: Marquardt W.C., Kondratieff B., Moore C.G., Freier J., Hagedorn H.H., Black W.III., James A.A., Hemingway J., and Higgs S. (Eds). The Biology of Disease Vectors Chapter 14 (2004), Elsevier Academic Press 167-185
50. Hrobowski Y.M., Garry R.F., and Michael S.F. Peptide inhibitors of dengue virus and West Nile virus infectivity. Virol J 2 49 (2005)
51. Igarashi A. Isolation of a Singh's Aedes albopictus cell clone sensitive to Dengue and Chikungunya viruses. J. Gen. Virol. 40 3 (1978) 531-544
52. Ivanova L., and Schlesinger M.J. Site-directed mutations in the Sindbis virus E2 glycoprotein identify palmitoylation sites and affect virus budding. J. Virol. 67 5 (1993) 2546-2551
53. Johnson B.K. O'nyong-nyong virus disease. In: Monath T.P. (Ed). The Arboviruses: Epidemiology and Ecology vol. 3 (1988), CRC Press, Boca Raton, FL 217-223
54. Journeaux S.F., Brown W.G., and Aaskov J.G. Prolonged infection of human synovial cells with Ross River virus. J. Gen. Virol. 68 Pt. 12 (1987) 3165-3169
55. Jupp P.G., and McIntosk B.M. Chikungunya virus disease. In the Arboviruses: Epidemiology and Ecology vol. 2 (1988) 137-157
56. Khan A.H., Morita K., Parquet Md Mdel C., Hasebe F., Mathenge E.G., and Igarashi A. Complete nucleotide sequence of chikungunya virus and evidence for an internal polyadenylation site. J. Gen. Virol. 83 Pt. 12 (2002) 3075-3084
57. Kitaoka M. Japanese encephalitis vaccine including a preliminary report on dengue fever and Chikungunya vaccines. Jpn. J. Med. Sci. Biol. 20 (1967) 41-56 Suppl
58. Klimstra W.B., Nangle E.M., Smith M.S., Yurochko A.D., and Ryman K.D. DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J. Virol. 77 22 (2003) 12022-12032
59. Kolokoltsov A.A., Weaver S.C., and Davey R.A. Efficient functional pseudotyping of oncoretroviral and lentiviral vectors by Venezuelan equine encephalitis virus envelope proteins. J. Virol. 79 2 (2005) 756-763
60. Kolokoltsov A.A., Fleming E.H., and Davey R.A. Venezuelan equine encephalitis virus entry mechanism requires late endosome formation and resists cell membrane cholesterol depletion. Virology 347 2 (2006) 333-342
61. Kuhn R.J., Niesters H.G., Hong Z., and Strauss J.H. Infectious RNA transcripts from Ross River virus cDNA clones and the construction and characterization of defined chimeras with Sindbis virus. Virology 182 2 (1991) 430-441
62. Kumar N.P., Joseph R., Kamaraj T., and Jambulingam P. A226V mutation in virus during the 2007 chikungunya outbreak in Kerala, India. J Gen. Virol. 89 Pt. 8 (2008) 1945-1948
63. Kwan W.H., Helt A.M., Maranon C., Barbaroux J.B., Hosmalin A., Harris E., Fridman W.H., and Mueller C.G. Dendritic cell precursors are permissive to dengue virus and human immunodeficiency virus infection. J. Virol. 79 12 (2005) 7291-7299
64. Lanciotti R.S., Ludwig M.L., Rwaguma E.B., Lutwama J.J., Kram T.M., Karabatsos N., Cropp B.C., and Miller B.R. Emergence of epidemic O'nyong-nyong fever in Uganda after a 35-year absence: genetic characterization of the virus. Virology 252 1 (1998) 258-268
65. Larke R.P., and Wheelock E.F. Stabilization of chikungunya virus infectivity by human blood platelets. J. Infect. Dis. 122 6 (1970) 523-531
66. Lee J.W., Chu J.J., and Ng M.L. Quantifying the specific binding between West Nile virus envelope domain III protein and the cellular receptor alphaVbeta3 integrin. J. Biol. Chem. 281 3 (2006) 1352-1360
67. Lee P., Knight R., Smit J.M., Wilschut J., and Griffin D.E. A single mutation in the E2 glycoprotein important for neurovirulence influences binding of sindbis virus to neuroblastoma cells. J. Virol. 76 12 (2002) 6302-6310
68. Lescar J., Roussel A., Wien M.W., Navaza J., Fuller S.D., Wengler G., and Rey F.A. The Fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105 1 (2001) 137-148
69. Levinson R.S., Strauss J.H., and Strauss E.G. Complete sequence of the genomic RNA of O'nyong-nyong virus and its use in the construction of alphavirus phylogenetic trees. Virology 175 1 (1990) 110-123
70. Levitt N.H., Ramsburg H.H., Hasty S.E., Repik P.M., Cole Jr. F.E., and Lupton H.W. Development of an attenuated strain of chikungunya virus for use in vaccine production. Vaccine 4 3 (1986) 157-162
71. Li G.P., La Starza M.W., Hardy W.R., Strauss J.H., and Rice C.M. Phosphorylation of Sindbis virus nsP3 in vivo and in vitro. Virology 179 1 (1990) 416-427
72. Linn M.A., and Suhrbier A. Persistence of Ross River virus in macrophages. Arbovirus Res. Aust. 7 (1997) 153-159
73. Linn M.L., Aaskov J.G., and Suhrbier A. Antibody-dependent enhancement and persistence in macrophages of an arbovirus associated with arthritis. J. Gen. Virol. 77 Pt 3 (1996) 407-411
74. Linn M.L., Mateo L., Gardner J., and Suhrbier A. Alphavirus-specific cytotoxic T lymphocytes recognize a cross-reactive epitope from the capsid protein and can eliminate virus from persistently infected macrophages. J. Virol. 72 6 (1998) 5146-5153
75. Liu L.N., Lee H., Hernandez R., and Brown D.T. Mutations in the endo domain of Sindbis virus glycoprotein E2 block phosphorylation, reorientation of the endo domain, and nucleocapsid binding. Virology 222 1 (1996) 236-246
76. Liu N., and Brown D.T. Phosphorylation and dephosphorylation events play critical roles in Sindbis virus maturation. Virology 196 2 (1993) 703-711
77. Lopez S., Yao J.S., Kuhn R.J., Strauss E.G., and Strauss J.H. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J. Virol. 68 3 (1994) 1316-1323
78. Lu Y.E., Cassese T., and Kielian M. The cholesterol requirement for Sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence. J. Virol. 73 5 (1999) 4272-4278
79. Malet H., Coutard B., Jamal S., Dutartre H., Papageorgiou N., Neuvonen M., Ahola T., Forrester N., Gould E.A., Lafitte D., Ferron F., Lescar J., Gorbalenya A.E., de Lamballerie X., and Canard B. The crystal structures of chikungunya and Venezuelan equine encephalitis virus nsP3 macro domains define a conserved adenosine binding pocket. J. Virol. 83 13 (2009) 6534-6545
80. Mantani M., Igarashi A., Tuchinda P., and Kato S. Cytoplasmic RNA synthesis and viral antigen in FL cells infected with chikungunya virus. Biken J. 10 4 (1967) 203-218
81. Mi S., Durbin R., Huang H.V., Rice C.M., and Stollar V. Association of the Sindbis virus RNA methyltransferase activity with the nonstructural protein nsP1. Virology 170 2 (1989) 385-391
82. Murphy F.A., Taylor W.P., Mims C.A., and Marshall D. Pathogenesis of Ross River virus infection in mice. II. Muscle, heart, and brown fat lesions. J. Infect. Dis. 127 2 (1973) 129-138
83. Myers R.M., and Carey D.E. Concurrent isolation from patient of two arboviruses, chikungunya and dengue type 2. Science 157 794 (1967) 1307-1308
84. Nakao E. Biological and immunological studies on chikungunya virus: a comparative observation of two strains of African and Asian origins. Kobe J. Med. Sci. 18 2 (1972) 133-141
85. Navarro-Sanchez E., Altmeyer R., Amara A., Schwartz O., Fieschi F., Virelizier J.L., Arenzana-Seisdedos F., and Despres P. 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 7 (2003) 723-728
86. Nimmo J.R. An unusual epidemics. Med. J. Aust. 1 (1928) 549-550
87. Nisole S., Stoye J.P., and Saib A. TRIM family proteins: retroviral restriction and antiviral defence. Nat. Rev. Microbiol. 3 10 (2005) 799-808
88. Ozden S., Lucas-Hourani M., Ceccaldi P.E., Basak A., Valentine M., Benjannet S., Hamelin J., Jacob Y., Mamchaoui K., Mouly V., Despres P., Gessain A., Butler-Browne G., Chretien M., Tangy F., Vidalain P.O., and Seidah N.G. Inhibition of Chikungunya virus infection in cultured human muscle cells by furin inhibitors: impairment of the maturation of the E2 surface glycoprotein. J. Biol. Chem. 283 32 (2008) 21899-21908
89. Ozden S., Huerre M., Riviere J.P., Coffey L.L., Afonso P.V., Mouly V., de Monredon J., Roger J.C., El Amrani M., Yvin J.L., Jaffar M.C., Frenkiel M.P., Sourisseau M., Schwartz O., Butler-Browne G., Despres P., Gessain A., and Ceccaldi P.E. Human muscle satellite cells as targets of chikungunya virus infection. PLoS ONE 2 6 (2007) e527
90. Pardigon N., Lenches E., and Strauss J.H. Multiple binding sites for cellular proteins in the 3′ end of Sindbis alphavirus minus-sense RNA. J. Virol. 67 8 (1993) 5003-5011
91. Parrott M.M., Sitarski S.A., Arnold R.J., Picton L.K., Hill R.B., and Mukhopadhyay S. Role of conserved cysteines in the alphavirus E3 protein. J. Virol. 83 6 (2009) 2584-2591
92. Paucker K., and Boxaca M. Cellular resistance to induction of interferon. Bacteriol. Rev. 31 2 (1967) 145-156
93. Pehrson J.R., and Fuji R.N. Evolutionary conservation of histone macroH2A subtypes and domains. Nucleic Acids Res. 26 12 (1998) 2837-2842
94. Perera R., Owen K.E., Tellinghuisen T.L., Gorbalenya A.E., and Kuhn R.J. Alphavirus nucleocapsid protein contains a putative coiled coil alpha-helix important for core assembly. J. Virol. 75 1 (2001) 1-10
95. Pfeffer M., Kinney R.M., and Kaaden O.R. The alphavirus 3′-nontranslated region: size heterogeneity and arrangement of repeated sequence elements. Virology 240 1 (1998) 100-108
96. Phalen T., and Kielian M. Cholesterol is required for infection by Semliki Forest virus. J. Cell. Biol. 112 4 (1991) 615-623
97. Powers A.M., Brault A.C., Shirako Y., Strauss E.G., Kang W., Strauss J.H., and Weaver S.C. Evolutionary relationships and systematics of the alphaviruses. J. Virol. 75 21 (2001) 10118-10131
98. Powers A.M., Brault A.C., Tesh R.B., and Weaver S.C. Re-emergence of Chikungunya and O'nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J. Gen. Virol. 81 Pt 2 (2000) 471-479
99. Precious S.W., Webb H.E., and Bowen E.T. Isolation and persistence of Chikungunya virus in cultures of mouse brain cells. J. Gen. Virol. 23 3 (1974) 271-279
100. Pyke A.T., Phillips D.A., Chuan T.F., and Smith G.A. Sucrose density gradient centrifugation and cross-flow filtration methods for the production of arbovirus antigens inactivated by binary ethylenimine. BMC Microbiol. 4 3 (2004)
101. Qureshi N.M., Coy D.H., Garry R.F., and Henderson L.A. Characterization of a putative cellular receptor for HIV-1 transmembrane glycoprotein using synthetic peptides. AIDS 4 6 (1990) 553-558
102. Rinaldo Jr. C.R., Overall Jr. J.C., and Glasgow L.A. Viral replication and interferon production in fetal and adult ovine leukocytes and spleen cells. Infect. Immun. 12 5 (1975) 1070-1077
103. Robinson M.C. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. I. Clinical features. Trans. R. Soc. Trop. Med. Hyg. 49 1 (1955) 28-32
104. Roggero R., Robert-Hebmann V., Harrington S., Roland J., Vergne L., Jaleco S., Devaux C., and Biard-Piechaczyk M. Binding of human immunodeficiency virus type 1 gp120 to CXCR4 induces mitochondrial transmembrane depolarization and cytochrome c-mediated apoptosis independently of Fas signaling. J. Virol. 75 16 (2001) 7637-7650
105. Ross R.W. Original isolation and characteristics of chikungunya virus. J. Hyg. 54 (1956) 192-200
106. Savarino A., Di Trani L., Donatelli I., Cauda R., and Cassone A. New insights into the antiviral effects of chloroquine. Lancet Infect. Dis. 6 2 (2006) 67-69
107. Schmid S.L., Fuchs R., Male P., and Mellman I. Two distinct subpopulations of endosomes involved in membrane recycling and transport to lysosomes. Cell 52 1 (1988) 73-83
108. Schmidt M., Schmidt M.F., and Rott R. Chemical identification of cysteine as palmitoylation site in a transmembrane protein (Semliki Forest virus E1). J. Biol. Chem. 263 35 (1988) 18635-18639
109. Schuffenecker I., Iteman I., Michault A., Murri S., Frangeul L., Vaney M.C., Lavenir R., Pardigon N., Reynes J.M., Pettinelli F., Biscornet L., Diancourt L., Michel S., Duquerroy S., Guigon G., Frenkiel M.P., Brehin A.C., Cubito N., Despres P., Kunst F., Rey F.A., Zeller H., and Brisse S. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 3 7 (2006) e263
110. Shirako Y., and Strauss J.H. Regulation of Sindbis virus RNA replication: uncleaved P123 and nsP4 function in minus-strand RNA synthesis, whereas cleaved products from P123 are required for efficient plus-strand RNA synthesis. J. Virol. 68 3 (1994) 1874-1885
111. Sieczkarski S.B., and Whittaker G.R. Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4 5 (2003) 333-343
112. Simizu B., Yamamoto K., Hashimoto K., and Ogata T. Structural proteins of chikungunya virus. J. Virol. 51 1 (1984) 254-258
113. Singh I., and Helenius A. Role of ribosomes in Semliki Forest virus nucleocapsid uncoating. J. Virol. 66 12 (1992) 7049-7058
114. Smith T.J., Cheng R.H., Olson N.H., Peterson P., Chase E., Kuhn R.J., and Baker T.S. Putative receptor binding sites on alphaviruses as visualized by cryoelectron microscopy. Proc. Natl. Acad. Sci. U.S.A. 92 23 (1995) 10648-10652
115. Solignat, M., Bernard, E., Gay, B., Chazal, N., Higgs, S., Devaux, C., Briant, L., (Submitted for publication). Involvement of clathrin pathway and early endosomal compartments during Chikungunya virus entry into mammalian cells.
116. Sourisseau M., Schilte C., Casartelli N., Trouillet C., Guivel-Benhassine F., Rudnicka D., Sol-Foulon N., Le Roux K., Prevost M.C., Fsihi H., Frenkiel M.P., Blanchet F., Afonso P.V., Ceccaldi P.E., Ozden S., Gessain A., Schuffenecker I., Verhasselt B., Zamborlini A., Saib A., Rey F.A., Arenzana-Seisdedos F., Despres P., Michault A., Albert M.L., and Schwartz O. Characterization of reemerging chikungunya virus. PLoS Pathog. 3 6 (2007) e89
117. Stim T.B., and Henderson J.R. Arbovirus plaquing in a clonal line (PS Y-15) of porcine kidney. Appl. Microbiol. 17 2 (1969) 246-249
118. Strauss E.G., Levinson R., Rice C.M., Dalrymple J., and Strauss J.H. Nonstructural proteins nsP3 and nsP4 of Ross River and O'Nyong-nyong viruses: sequence and comparison with those of other alphaviruses. Virology 164 1 (1988) 265-274
119. Strauss E.G., Stec D.S., Schmaljohn A.L., and Strauss J.H. Identification of antigenically important domains in the glycoproteins of Sindbis virus by analysis of antibody escape variants. J. Virol. 65 9 (1991) 4654-4664
120. Strauss J.H., and Strauss E.G. Alphavirus proteinases. Sem. Virol. 1 (1990) 347-356
121. Strauss J.H., and Strauss E.G. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58 3 (1994) 491-562
122. Suomalainen M., Liljestrom P., and Garoff H. Spike protein-nucleocapsid interactions drive the budding of alphaviruses. J. Virol. 66 8 (1992) 4737-4747
123. Tan K.B., and Sokol F. Virion-bound protein kinase in Semliki Forest and Sindbis viruses. J. Virol. 13 6 (1974) 1245-1253
124. Tassaneetrithep B., Burgess T.H., Granelli-Piperno A., Trumpfheller C., Finke J., Sun W., Eller M.A., Pattanapanyasat K., Sarasombath S., Birx D.L., Steinman R.M., Schlesinger S., and Marovich M.A. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197 7 (2003) 823-829
125. Tishkoff S.A., Pakstis A.J., Stoneking M., Kidd J.R., Destro-Bisol G., Sanjantila A., Lu R.B., Deinard A.S., Sirugo G., Jenkins T., Kidd K.K., and Clark A.G. Short tandem-repeat polymorphism/alu haplotype variation at the PLAT locus: implications for modern human origins. Am. J. Hum. Genet. 67 4 (2000) 901-925
126. Tsetsarkin K., Higgs S., McGee C.E., De Lamballerie X., Charrel R.N., and Vanlandingham D.L. Infectious clones of chikungunya virus (La Reunion isolate) for vector competence studies. Vector Borne Zoonotic Dis. 6 4 (2006) 325-337
127. Tsetsarkin K.A., Vanlandingham D.L., McGee C.E., and Higgs S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 3 12 (2007) e201
128. Vanlandingham D.L., Hong C., Klingler K., Tsetsarkin K., McElroy K.L., Powers A.M., Lehane M.J., and Higgs S. Differential infectivities of o'nyong-nyong and chikungunya virus isolates in Anopheles gambiae and Aedes aegypti mosquitoes. Am. J. Trop. Med. Hyg. 72 5 (2005) 616-621
129. Vanlandingham D.L., Tsetsarkin K., Hong C., Klingler K., McElroy K.L., Lehane M.J., and Higgs S. Development and characterization of a double subgenomic chikungunya virus infectious clone to express heterologous genes in Aedes aegypti mosquitoes. Insect Biochem. Mol. Biol. 35 10 (2005) 1162-1170
130. Vashishtha M., Phalen T., Marquardt M.T., Ryu J.S., Ng A.C., and Kielian M. A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit. J. Cell Biol. 140 1 (1998) 91-99
131. Vidalain, P.O., Tangy, F., Jacob, Y., and Lucas-Hourani, M., (2007). A mammalian cell-based screening assay to identify inhibitors of alphaviruses. Patent Application Number EP07291429.4; November 30, 2007.
132. Vrati S., Fernon C.A., Dalgarno L., and Weir R.C. Location of a major antigenic site involved in Ross River virus neutralization. Virology 162 2 (1988) 346-353
133. Waarts B.L., Bittman R., and Wilschut J. Sphingolipid and cholesterol dependence of alphavirus membrane fusion. Lack of correlation with lipid raft formation in target liposomes. J. Biol. Chem. 277 41 (2002) 38141-38147
134. Wang K.S., Kuhn R.J., Strauss E.G., Ou S., and Strauss J.H. High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J. Virol. 66 8 (1992) 4992-5001
135. Waite M.R., Lubin M., Jones K.J., and Bose H.R. Phosphorylated proteins of Sindbis virus. J. Virol. 13 1 (1974) 244-246
136. Weaver S.C., Hagenbaugh A., Bellew L.A., Gousset L., Mallampalli V., Holland J.J., and Scott T.W. Evolution of alphaviruses in the eastern equine encephalomyelitis complex. J. Virol. 68 1 (1994) 158-169
137. Weaver S.C., Hagenbaugh A., Bellew L.A., Netesov S.V., Volchkov V.E., Chang G.J., Clarke D.K., Gousset L., Scott T.W., Trent D.W., et al. A comparison of the nucleotide sequences of eastern and western equine encephalomyelitis viruses with those of other alphaviruses and related RNA viruses. Virology 197 1 (1993) 375-390
138. Weaver S.C., Kang W., Shirako Y., Rumenapf T., Strauss E.G., and Strauss J.H. Recombinational history and molecular evolution of western equine encephalomyelitis complex alphaviruses. J. Virol. 71 1 (1997) 613-623
139. Weber F.C., Oppel T.W., and Raymon R.W. A mild exanthematous disease seen in the Schouten Islands. Am. J. Trop. Med. 26 (1946) 489-492
140. Weiss B., Nitschko H., Ghattas I., Wright R., and Schlesinger S. Evidence for specificity in the encapsidation of Sindbis virus RNAs. J. Virol. 63 12 (1989) 5310-5318
141. Wengler G., and Wurkner D. Identification of a sequence element in the alphavirus core protein which mediates interaction of cores with ribosomes and the disassembly of cores. Virology 191 2 (1992) 880-888
142. Westaway E.G., Brinton M.A., Gaidamovich S., Horzinek M.C., Igarashi A., Kaariainen L., Lvov D.K., Porterfield J.S., Russell P.K., and Trent D.W. Togaviridae. Intervirology 24 3 (1985) 125-139
143. White A., Berman S., and Lowenthal J.P. Comparative immunogenicities of Chikungunya vaccines propagated in monkey kidney monolayers and chick embryo suspension cultures. Appl. Microbiol. 23 5 (1972) 951-952
144. Yadav P., Shouche Y.S., Munot H.P., Mishra A.C., and Mourya D.T. Genotyping of chikungunya virus isolates from India during 1963-2000 by reverse transcription-polymerase chain reaction. Acta Virol. 47 2 (2003) 125-127
145. Zhao H., Lindqvist B., Garoff H., von Bonsdorff C.H., and Liljestrom P. A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential for budding. EMBO J. 13 18 (1994) 4204-4211
146. Zheng Y.H., and Peterlin B.M. Intracellular immunity to HIV-1: newly defined retroviral battles inside infected cells. Retrovirology 2 25 (2005)