Chikungunya Virus and Its Mosquito Vectors

Vector-Borne and Zoonotic Diseases

Volumn 15, Issue 4, 2015, Pages 231-240

  Higgs, Stephen ^a   Vanlandingham, Dana ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Ae. albopictus; Aedes (Ae.) aegypti; Chikungunya virus; Geographic expansion; Mosquito vector interactions; RNA strategies

Indexed keywords

AEDES AEGYPTI; ARBOVIRUS; CARIBBEAN; CENTRAL AMERICA; CHIKUNGUNYA; CHIKUNGUNYA VIRUS; HUMAN; IMMUNE SYSTEM; MOLECULAR EVOLUTION; MOSQUITO; NONHUMAN; NORTH AMERICA; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; SOUTH AMERICA; VERTEBRATE; VIRAL GENETICS; VIRUS CARRIER; VIRUS TRANSMISSION; AEDES; ANIMAL; DISEASE CARRIER; EPIDEMIOLOGY; GENETICS; GEOGRAPHY; PHYSIOLOGY; TRANSMISSION; VIROLOGY;

ALPHAVIRUS; CHIKUNGUNYA VIRUS; PRIMATES;

AEDES; ANIMALS; CENTRAL AMERICA; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; GEOGRAPHY; HUMANS; INSECT VECTORS; MOSQUITO CONTROL; NORTH AMERICA; RNA INTERFERENCE; SOUTH AMERICA;

EID: 84928624265     PISSN: 15303667     EISSN: 15577759     Source Type: Journal    
DOI: 10.1089/vbz.2014.1745     Document Type: Review

References (125)

1. Agarwal A, Dash PK, Singh AK, Sharma S, et al. Evidence of experimental vertical transmission of emerging novel ECSA genotype of chikungunya virus in Aedes aegypti . PLoS Negl Trop Dis 2014; 8:e2990.
2. Alphey L. Genetic control of mosquitoes. Annu Rev Entomol 2014; 59:205-224.
3. Angelini R, Finarelli AC, Angelini P, Po C, et al. An outbreak of chikungunya fever in the province of Ravenna, Italy. Euro Surveill 2007; 12:E070906 1.
4. Belkaid Y, Butcher B, Sacks DL. Analysis of cytokine production by inflammatory mouse macrophages at the single-cell level: Selective impairment of IL-12 induction in Leishmania-infected cells. Eur J Immunol 1998; 28:1389-1400.
5. Benedict MQ, Levine RS, Hawley WA, Lounibos LP. Spread of the tiger: Global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis 2007; 7:76-85.
6. Billingsley PF, Baird J, Mitchell JA, Drakeley C. Immune interactions between mosquitoes and their hosts. Parasite Immunol 2006; 28:143-153.
7. Blagrove MS, Arias-Goeta C, Di Genua C, Failloux AB, et al. A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits Chikungunya virus. PLoS Negl Trop Dis 2013; 7:e2152.
8. Calvo E, Andersen J, Francischetti IM, Debianchi M, et al. The transcriptome of adult female Anopheles darlingi salivary glands. Insect Mol Biol 2004; 13:73-88.
9. Campbell CL, Harrison T, Hess AM, Ebel GD. MicroRNA levels are modulated in Aedes aegypti after exposure to Dengue-2. Insect Mol Biol 2014; 23:132-139.
10. Carey DE. Chikungunya and dengue: A case of mistaken identity? J Hist Med Allied Sci 1971; 26:243-262.
11. Centers for Disease Control and Prevention. Chikungunya in the Americas, 2015a. Available at www.cdc.gov/chikungunya/geo/americas.html/ Accessed January 9, 2015.
12. Centers for Disease Control and Prevention. Chikungunya virus in the United States, 2015b Available at www.cdc.gov/chikungunya/geo/united-states.html/ Accessed January 9, 2015.
13. Champagne DE, Nussenzveig RH, Ribeiro JM. Purification, partial characterization, and cloning of nitric oxide-carrying heme proteins (nitrophorins) from salivary glands of the blood-sucking insect Rhodnius prolixus. J Biol Chem 1995a; 270:8691-8695.
14. Champagne DE, Smartt CT, Ribeiro JM, James AA. The salivary gland-specific apyrase of the mosquito Aedes aegypti is a member of the 5′-nucleotidase family. Proc Natl Acad Sci USA 1995b; 92:694-698.
15. Chastel C. [Chikungunya virus: Its recent spread to the southern Indian Ocean and Reunion Island (2005-2006)]. Bull Acad Natl Med 2005; 189:1827-1835.
16. Chretien JP, Anyamba A, Bedno SA, Breiman RF, et al. Drought-associated chikungunya emergence along coastal East Africa. Am J Trop Med Hyg 2007; 76:405-407.
17. Coffey LL, Failloux A-B, Weaver SW. Chikungunya virus-vector interactions. Viruses 2014; 6:4628-4662.
18. Consigny PH, Lecuit M, Lortholary O. Chikungunya virus: A reemerging alphavirus. Med Sci (Paris) 2006; 22:444-446.
19. Dash PK, Tiwari M, Santhosh SR, Parida M, et al. RNA interference mediated inhibition of Chikungunya virus replication in mammalian cells. Biochem Biophys Res Commun 2008; 376:718-722.
20. de Lamballerie X, Leroy E, Charrel RN, Ttsetsarkin K, et al. Chikungunya virus adapts to tiger mosquito via evolutionary convergence: A sign of things to come? Virol J 2008; 5:33.
21. Edwards JF, Higgs S, Beaty BJ. Mosquito feeding-induced enhancement of Cache Valley Virus (Bunyaviridae) infection in mice. J Med Entomol 1998; 35:261-265.
22. Enserink M. Infectious diseases. Massive outbreak draws fresh attention to little-known virus. Science 2006; 311:1085.
23. Faraji, A, Egizi, A, Fonseca, DM, Unlu, I, et al. Comparative host feeding patterns of the Asian tiger mosquito, Aedes albopictus, in urban and suburban northeaster USA and implications for ddisease transmission. PLoS Negl Trop Dis 2014; 8:e3037.
24. Fragkoudis R, Chi Y, Siu RW, Barry G, et al. Semliki Forest virus strongly reduces mosquito host defence signaling. Insect Mol Biol 2008; 17:647-656.
25. Gerardin P, Barau G, Michault A, Bintner M, et al. Multi-disciplinary prospective study of mother-to-child chikungunya virus infections on the island of La Reunion. PLoS Med 2008; 5:e60.
26. Gould EA, Higgs S. Impact of climate change and other factors on emerging arbovirus diseases. Trans R Soc Trop Med Hyg 2009; 103:109-121.
27. Gould EA, Gallian P, De Lamballerie X, Charrel RN. First cases of autochthonous dengue fever and chikungunya fever in France: Fom bad dream to reality! Clin Microbiol Infect 2010; 16:1702-1704.
28. Hawman DW, Stoermer KA, Montgomery SA, Pal P, et al. Chronic joint disease caused by persistent Chikungunya virus infection is controlled by the adaptive immune response. J Virol 2013; 87:13878-13888.
29. Her Z, Teng T-S, Tan JJL, Two T-H, et al. (2014). Loss of TLR3 aggravates CHIKV replication and pathology due to an altered virus-specific neutralizing antibody response. EMBO Mol Med 2014; e201404459.
30. Higgs S. The 2005-2006 Chikungunya epidemic in the Indian Ocean. Vector Borne Zoonotic Dis 2006; 6:115-116.
31. Higgs S. Alternative approaches to control dengue and chikungunya: Transgenic mosquitoes. Public Health 2013; 24:35-42.
32. Higgs S, Vanlandingham DL. Chikungunya: Here today, where tomorrow? Int Health 2015; 7:1-3.
33. Hoarau JJ, Jaffar Bandjee MC, Krejbich Trotot P, Das T, et al. Persistent chronic inflammation and infection by Chikungunya arthritogenic alphavirus in spite of a robust host immune response. J Immunol 2010; 184:5914-5927.
34. Jain S, Rana V, Shrinet J, Sharma A, et al. Blood feeding and Plasmodium infection alters the miRNome of Anopheles stephensi. PLoS One 2014; 9:e98402.
35. James AA. Molecular and biochemical analyses of the salivary glands of vector mosquitoes. Bull Institut Pasteur 1994; 92:133-150.
36. Jupp PG, McIntosh BB. Chikungunya virus disease. In: Monath TP, ed. The Arboviruses: Epidemiology and Ecology. Boca Raton, FL: CRC Press, 1988:137-157.
37. Kamhawi S, Belkaid Y, Modi G, Rowton E, et al. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 2000a; 290:1351-1354.
38. Kamhawi S, Modi GB, Pimenta PF, Rowton E, et al. The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology 2000b; 121(Pt 1):25-33.
39. Keene KM, Foy BD, Sanchez-Vargas I, Beaty BJ, et al. RNA interference acts as a natural antiviral response to O'nyongnyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proc Natl Acad Sci USA 2004; 101:17240-17245.
40. Kerlin RL, Hughes S. Enzymes in saliva from four parasitic arthropods. Med Vet Entomol 1992; 6:121-126.
41. Khoo CC, Piper J, Sanchez-Vargas I, Olson KE, et al. The RNA interference pathway affects midgut infection- and escape barriers for Sindbis virus in Aedes aegypti. BMC Microbiol 2010; 10:130.
42. Lam S, Chen KC, Ng MM, Chu JJ. Expression of plasmid-based shRNA against the E1 and nsP1 genes effectively silenced Chikungunya virus replication. PLoS One 2012; 7:e46396.
43. Ledermann JP, Guillaumot L, Yug L, Saweyog SC. Aedes hensilli as a potential vector of Chikungunya and Zika viruses. PLoS Negl Trop Dis 2014;8:e3188; DOI: 10.1371/journal.pntd.0003188.
44. Ligon BL. Reemergence of an unusual disease: The chikungunya epidemic. Semin Pediatr Infect Dis 2006; 17:99-104.
45. Limesand KH, Higgs S, Pearson LD, Beaty BJ. Potentiation of vesicular stomatitis New Jersey virus infection in mice by mosquito saliva. Parasite Immunol 2000; 22:461-467.
46. Limesand KH, Higgs S, Pearson LD, Beaty BJ. Effect of mosquito salivary gland treatment on vesicular stomatitis New Jersey virus replication and interferon alpha/beta expression in vitro. J Med Entomol 2003; 40:199-205.
47. Lindsey NP., Prince HE, Kosoy O., Laven J., et al. Chikungunya virus infections among travelers-United States 2010-2013. Am J Trop Med Hyg 2015; 92:82087
48. Lumsden WH. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. II. General description and epidemiology. Trans R Soc Trop Med Hyg 1955; 49:33-57.
49. Maron, DF. New type of more problematic mosquito-borne illness detected in Brazil. Available at www.scientificamerican.com/article/new-type-of-more-problematic-mosquito-borne-illness-detected-in-brazil/?WT.mc-id=SA-Twitter2014/
50. Mason PJ, Haddow AJ. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53; an additional note on Chikungunya virus isolations and serum antibodies. Trans R Soc Trop Med Hyg 1957; 51:238-240.
51. McFarlane M, Arias-Goeta C, Martin E, O'Hara Z, et al. Characterization of Aedes aegypti innate-immune pathways that limit Chikungunya virus replication. PLoS Negl Trop Dis 2014;8: e2994. DOI: 10.1371/journal.pntd.0002994
52. Miller MJ, Loaiza JR. Geographic Expansion of the Invasive Mosquito Aedes albopictus across Panama-Implications for Control of Dengue and Chikungunya Viruses. PLOS Negl Trop Dis 2015; 9:e0003383.
53. Moore DL, Reddy S, Akinkugbe FM, Lee VH, et al. An epidemic of chikungunya fever at Ibadan, Nigeria, 1969. Ann Trop Med Parasitol 1974; 68:59-68.
54. Morazzani EM, Wiley MR, Murreddu MG, Adelman ZN, et al. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog 2012; 8:e1002470.
55. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 2009; 139:1268-1278.
56. Morris RV, Shoemaker CB, David JR, Lanzaro GC, et al. Sandfly maxadilan exacerbates infection with Leishmania major and vaccinating against it protects against L. major infection. J Immunol 2001; 167:5226-5230.
57. Mourya DT, Yadav P, Mishra AC. Effect of temperature stress on immature stages and susceptibility of Aedes aegypti mosquitoes to chikungunya virus. Am J Trop Med Hyg 2004; 70:346-350.
58. Mousson L, Martin E, Zouache K, Madec Y, et al. Wolbachia modulates Chikungunya replication in Aedes albopictus. Mol Ecol 2010; 19:1953-1964.
59. Myles KM, Wiley MR, Morazzani EM, Adelman ZN. Alpha-virus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proc Natl Acad Sci USA 2008; 105:19938-19943.
60. Osorio JE, Godsey MS, Defoliart GR, Yuill TM. La Crosse viremias in white-tailed deer and chipmunks exposed by injection or mosquito bite. Am J Trop Med Hyg 1996; 54:338-342.
61. Paganin F, Borgherini G, Staikowsky F, Arvin-Berod C, et al. Chikungunya on Reunion Island: Chronicle of an epidemic foretold. Presse Med 2006; 35:641-646.
62. Pan X, Zhou G, Wu J, Bian G, et al. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc Natl Acad Sci USA 2012; 109:E23-E31.
63. Pan American Health Organization. Chikungunya, no date. Available at www.paho.org/hq/index.php?option=com-topics&view=article&id=343&Itemid=40931/ Accessed January 7, 2015.
64. Parashar D, Paingankar MS, Kumar S, Gokhale MD, et al. Administration of E2 and NS1 siRNAs inhibit chikungunya virus replication in vitro and protects mice infected with the virus. PLoS Negl Trop Dis 2013; 7:e2405.
65. Pialoux G, Gauzere BA, Jaureguiberry S, Strobel M. Chikungunya, an epidemic arbovirosis. Lancet Infect Dis 2007; 7:319-327.
66. Powers AM, Brault AC, Tesh RB, Weaver SC. Re-emergence of Chikungunya and O'nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol 2000; 81:471-479.
67. Racioppi JV, Spielman A. Secretory proteins from the salivary glands of adult Aedes agypti mosquitoes. Insect Biochem 1987; 17:503-511.
68. Rainey SM, Shah P, Kohl A, Dietrich I. Understanding the Wolbachia-mediated inhibition of arboviruses in mosquitoes: Progress and challenges. J Gen Virol 2014; 95:517-530.
69. Reiter P, Fontenille D, Paupy C. Aedes albopictus as an epidemic vector of chikungunya virus: Another emerging problem?Lancet Infect Dis 2006; 6:463-464.
70. Ribeiro JM. Role of saliva in blood-feeding by arthropods. Annu Rev Entomol 1987; 32:463-478.
71. Ribeiro JM. Vector saliva and its role in parasite transmission. Exp Parasitol 1989; 69:104-106.
72. Ribeiro JM. Characterization of a vasodilator from the salivary glands of the yellow fever mosquito Aedes aegypti. J Exp Biol 1992; 165:61-71.
73. Ribeiro JM, Francischetti IM. Role of arthropod saliva in blood feeding: Sialome and post-sialome perspectives. Annu Rev Entomol 2003; 48:73-88.
74. Ribeiro JM, Nussenzveig RH. The salivary catechol oxidase/peroxidase activities of the mosquito Anopheles albimanus. J Exp Biol 1993; 179:273-287.
75. Ribeiro JM, Valenzuela JG. Purification and cloning of the salivary peroxidase/catechol oxidase of the mosquito Anopheles albimanus. J Exp Biol 1999; 202:809-816.
76. Ribeiro JM, Nussenzveig RH, Tortorella G. Salivary vasodilators of Aedes triseriatus and Anopheles gambiae (Diptera: Culicidae). J Med Entomol 1994; 31:747-753.
77. Ribeiro JM, Charlab R, Pham VM, Garfield M, et al. An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus. Insect Biochem Mol Biol 2004; 34:543-563.
78. Rider MA, Zou J, Vanlandingham D, Nuckols JT, et al. Quantitative proteomic analysis of the Anopheles gambiae (Diptera: Culicidae) midgut infected with o'nyong-nyong virus. J Med Entomol 2013; 50:1077-1088.
79. Rodriguez-Andres J, Rani S, Varjak M, Chase-Topping ME, et al. Phenoloxidase activity acts as a mosquito innate immune response against infection with Semliki Forest virus. PLoS Pathog 2012; 8:e1002977.
80. Rohatgi A, Corbo JC, Monte K, Higgs S, et al. Infection of myofibers contributes to increased pathogenicity during infection with an epidemic strain of chikungunya virus. J Virol 2014; 88:2414-2425.
81. Ross RW. The Newala epidemic. III. The virus: Isolation, pathogenic properties and relationship to the epidemic. J Hyg (Lond) 1956; 54:177-191.
82. Sam IC, Kummerer BM, Chan YF, Roques P, et al. Update on chikungunya epidemiology, clinical disease and diagnosis. Vector Borne Zoonotic Dis 2015; (in press).
83. Savage HM, Ledermann JP, Yug L, Burkhalter KL, et al. Incrimination of Aedes (Stegomyia) hensilli Farner as an epidemic vector of Chikungunya virus on Yap Island, Federated States of Micronesia, 2013. Am J Trop Med Hyg; 2014; [online ahead of print]: DOI: 10.4269/ajtmh.14-0374.
84. Saxton-Shaw KD, Ledermann JP, Borland EM, Stovall JL et al. O'nyong nyong virus molecular determinants of unique vector specificity reside in non-structural protein 3. PLoS Negl Trop Dis 2013; 7:e1931.
85. Schaffner F, Bellini R, Petrić D, Scholte E-J, et al. Development of guidelines for the surveillance of invasive mosquitoes in Europe. Parasit Vectors 2013; 6:209.
86. Schneider BS, Soong L, Zeidner NS, Higgs S. Aedes aegypti salivary gland extracts modulate anti-viral and TH1/TH2 cytokine responses to Sindbis virus infection. Viral Immunol 2004; 17:565-573.
87. Schneider BS, Soong L, Girard YA, Campbell G, et al. Potentiation of West Nile encephalitis by mosquito feeding. Viral Immunol 2006; 19:74-82.
88. Schnettler E, Donald CL, Human S, Watson M, et al. Knockdown of piRNA pathway proteins results in enhanced Semliki Forest virus production in mosquito cells. J Gen Virol 2013; 94:1680-1689.
89. Schuffenecker I, Iteman I, Michault A, Murri S, et al. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med 2006; 3:e263.
90. Shiao SH, Higgs S, Adelman Z, Christensen BM, et al. Effect of prophenoloxidase expression knockout on the melanization of filarial worms in the mosquito, Armigeres subalbatus. Insect Mol Biol 2001; 10:315-321.
91. Sim C, Hong YS, Vanlandingham DL, Harker BW, et al. Modulation of Anopheles gambiae gene expression in response to o'nyong-nyong virus infection. Insect Mol Biol 2005; 14:475-481.
92. Sim C, Hong YS, Tsetsarkin KA, Vanlandingham DL, et al. Anopheles gambiae heat shock protein cognate 70B impedes o'nyong-nyong virus replication. BMC Genomics 2007; 8:231.
93. Siu RW, Fragkoudis R, Simmonds P, Donald CL, et al. Antiviral RNA interference responses induced by Semliki Forest virus infection of mosquito cells: characterization, origin, and frequency-dependent functions of virus-derived small interfering RNAs. J Virol 2011; 85:2907-2917.
94. Staples JE, Fischer M. Chikungunya virus in the Americas - what a vector borne pathogen can do. N Engl J Med 2014; 371:887-889.
95. Stark KR, James AA. Salivary gland anticoagulants in culicine and anopheline mosquitoes (Diptera:Culicidae). J Med Entomol 1996; 33:645-650.
96. Styer LM, Bernard KA, Kramer LD. Enhanced early West Nile virus infection in young chickens infected by mosquito bite: Effect of viral dose. Am J Trop Med Hyg 2006; 75:337-345.
97. Tchankouo-Nguetcheu S, Bourguet E, Lenormand P, Rousselle JC, et al. Infection by chikungunya virus modulates the expression of several proteins in Aedes aegypti salivary glands. Parasit Vectors 2012; 5:264.
98. Teixeira MG, Andrade A, Costa MC, Castro J, et al. Chikungunya outbreak in Brazil by African genotype. Emerg Infect Dis 2015: (In press).
99. Tesh RB, Gubler DJ, Rosen L. Variation among goegraphic strains of Aedes albopictus in susceptibility to infection with chikungunya virus. Am J Trop Med Hyg 1976; 25:326-335.
100. Thangamani S, Wikel SK. Differential expression of Aedes aegypti salivary transcriptome upon blood feeding. Parasit Vectors 2009; 2:34.
101. Thangamani S, Higgs S, Ziegler S, Vanlandingham D, et al. Host immune response to mosquito-transmitted chikungunya virus differs from that elicited by needle inoculated virus. PLoS One 2010; 5:e12137.
102. Thiberville SD, Moyen N, Dupuis-Maguiraga L, Nougairede A, et al. Chikungunya fever: Epidemiology, clinical syndrome, pathogenesis and therapy. Antiviral Res 2013; 99:345-370.
103. Trobaugh DW, Gardner CL, Sun C, Haddow AD, et al. RNA viruses can hijack vertebrate microRNAs to suppress innate immunity. Nature 2014; 506:245-248.
104. Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog 2007; 3:e201.
105. Tsetsarkin KA, McGee CE, Volk SM, Vanlandingham DL, et al. Epistatic roles of E2 glycoprotein mutations in adaption of chikungunya virus to Aedes albopictus and Ae. aegypti mosquitoes. PLoS One 2009; 4:e6835.
106. Tsetsarkin KA, Weaver SC. Sequential adaptive mutations enhance efficient vector switching by Chikungunya virus and its epidemic emergence. PLoS Pathog 2011; 7:e1002412.
107. Tsetsarkin KA, Chen R, Leal G, Forrester N, et al. Chikungunya virus emergence is constrained in Asia by lineage-specific adaptive landscapes. Proc Natl Acad Sci USA 2011a; 108:7872-7877.
108. Tsetsarkin KA, McGee CE, Higgs S. Chikungunya virus adaptation to Aedes albopictus mosquitoes does not correlate with acquisition of cholesterol dependence or decreased pH threshold for fusion reaction. Virol J 2011b; 8:376.
109. Tsetsarkin KA, Chen R, Yun R, Rossi SL, et al. Multi-peaked adaptive landscape for chikungunya virus evolution predicts continued fitness optimization in Aedes albopictus mosquitoes. Nat Commun 2014; 5:4084.
110. Turell MJ, Spielman A. Nonvascular delivery of Rift Valley fever virus by infected mosquitoes. Am J Trop Med Hyg 1992; 47:190-194.
111. Turell MJ, Beaman JR, Tammariello RF. Susceptibility of selected strains of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) to chikungunya virus. J Med Entomol 1992; 29:49-53.
112. Turell MJ, Tammariello RF, Spielman A. Nonvascular delivery of St. Louis encephalitis and Venezuelan equine encephalitis viruses by infected mosquitoes (Diptera: Culicidae) feeding on a vertebrate host. J Med Entomol 1995; 32:563-568.
113. Valenzuela JG. High-throughput approaches to study salivary proteins and genes from vectors of disease. Insect Biochem Mol Biol 2002; 32:1199-1209.
114. Valenzuela JG, Charlab R, Gonzalez EC, de Miranda-Santos IK, et al. The D7 family of salivary proteins in blood sucking diptera. Insect Mol Biol 2002; 11:149-155.
115. Van Bortel W, Dorleans F, Rosine J, Blateau A, et al. Chikungunya outbreak in the Caribbean region, December 2013 to March 2014, and the significance for Europe. Euro Surveill 2014; 19.
116. van den Hurk AF, Hall-Mendelin S, Pyke AT, Frentiu FD, et al. Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis 2012; 6:e1892.
117. Vanlandingham DL, Hong C, Klingler K, Tsetsarkin K, et al. Differential infectivities of o'nyong-nyong and chikungunya virus isolates in Anopheles gambiae and Aedes aegypti mosquitoes. Am J Trop Med Hyg 2005; 72:616-621.
118. Vanlandingham DL, Tsetsarkin K, Klingler KA, Hong C, et al. Determinants of vector specificity of o'nyong nyong and chikungunya viruses in Anopheles and Aedes mosquitoes. Am J Trop Med Hyg 2006; 74:663-669.
119. Vega-Rua A, Zouache K, Girod R, Failloux AB, et al. High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of Chikungunya virus. J Virol 2014; 88:6294-6306.
120. Volk SM, Chen R, Tsetsarkin KA, Adams AP, et al. Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J Virol 2010; 84:6497-6504.
121. Wanasen N, Nussenzveig RH, Champagne DE, Soong L, et al. Differential modulation of murine host immune response by salivary gland extracts from the mosquitoes Aedes aegypti and Culex quinquefasciatus . Med Vet Entomol 2004; 18:191-199.
122. Wasserman HA, Singh S, Champagne DE. Saliva of the Yellow Fever mosquito, Aedes aegypti, modulates murine lymphocyte function. Parasite Immunol 2004; 26:295-306.
123. Zeidner N, Mbow ML, Dolan M, Massung R, et al. Effects of Ixodes scapularis and Borrelia burgdorferi on modulation of the host immune response: Induction of a TH2 cytokine response in Lyme disease-susceptible (C3H/HeJ) mice but not in disease-resistant (BALB/c) mice. Infect Immun 1997; 65:3100-3106.
124. Zouache K, Fontaine A, Vega-Rua A, Mousson L, et al. Three-way interactions between mosquito population, viral strain and temperature underlying chikungunya virus transmission potential. Proc R Soc B 2014; 281:20141078
125. Zuchi N, da Silva Heinen LB, dos Santos MAM, Pereira FC, et al. Molecular detection of Mayaro virus during a dengue outbreak in the state of Mato Grosso, Central-West Brazil. Mem Inst Oswaldo Cruz 2014: 109:820-823.