AEDES AEGYPTI VECTORIAL CAPACITY IS DETERMINED BY THE INFECTING GENOTYPE OF DENGUE VIRUS

JUSTIN R. ANDERSON Department of Virology & Immunology, Southwest Foundation for Biomedical Research, San Antonio, Texas

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REBECA RICO-HESSE Department of Virology & Immunology, Southwest Foundation for Biomedical Research, San Antonio, Texas

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Dengue viruses causing severe, hemorrhagic disease have displaced less virulent strains in the Americas during the past three decades. The American (AM) genotype of dengue serotype 2 has been endemic in the Western Hemisphere and South Pacific, causing outbreaks of dengue fever (DF), but has not been linked to dengue hemorrhagic fever (DHF). The Southeast Asian (SEA) genotype of dengue was introduced into this hemisphere in 1981, has caused outbreaks with numerous cases of DHF, and has displaced the AM genotype in several countries. We investigated the effect of viral genotype on the potential for transmission by infecting Aedes aegypti mosquitoes collected in South Texas with six viruses, representing these two genotypes. Viral replication in the midgut was significantly higher in SEA-infected mosquitoes, and virus-specific proteins could be detected in salivary glands 7 days earlier in SEA- than AM-infected mosquitoes. This much earlier appearance of dengue virus in salivary glands resulted in an estimated 2- to 65-fold increase in the vectorial capacity of these mosquitoes for the viruses that can cause DHF. This may be one of the mechanisms through which more virulent flaviviruses spread and displace others globally.

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  • 1

    Gubler DJ, 1998. Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11 :480–496.

  • 2

    Halstead SB, 2003. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 60 :421–467.

  • 3

    Rico-Hesse R, 2003. Microevolution and virulence of dengue viruses. Adv Virus Res 59 :315–341.

  • 4

    Rico-Hesse R, 1990. Molecular evolution and distribution of dengue viruses type 1 and 2 in nature. Virology 174 :479–493.

  • 5

    Rico-Hesse R, Harrison LM, Salas RA, Tovar D, Nisalak A, Ramos C, Boshell J, de Mesa MT, Nogueira RM, da Rosa AT, 1997. Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. Virology 230 :244–251.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Watts DM, Porter KR, Putvatana P, Vasquez B, Calampa C, Hayes CG, Halstead SB, 1999. Failure of secondary infection with American genotype dengue 2 to cause dengue haemorrhagic fever. Lancet 354 :1431–1434.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Kouri GP, Guzman MG, Bravo JR, Triana C, 1989. Dengue haemorrhagic fever/dengue shock syndrome: lessons from the Cuban epidemic, 1981. Bull World Health Organ 67 :375–380.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Sariol C, Pelegrino J, Martinez A, Arteaga E, Kouri G, Guzman M, 1999. Detection and genetic relationship of dengue virus sequences in seventeen-year-old paraffin-embedded samples from Cuba. Am J Trop Med Hyg 61 :994–1000.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Armstrong PM, Rico-Hesse R, 2001. Differential susceptibility of Aedes aegypti to infection by the American and Southeast Asian genotypes of dengue type 2 virus. Vector Borne Zoonotic Dis 1 :159–168.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Armstrong PM, Rico-Hesse R, 2003. Efficiency of dengue sero-type 2 virus strains to infect and disseminate in Aedes aegypti.Am J Trop Med Hyg 68 :539–544.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Cologna R, Armstrong PM, Rico-Hesse R, 2005. Selection for virulent dengue viruses occurs in humans and mosquitoes. J Virol 79 :853–859.

  • 12

    Dye C, 1986. Vectorial capacity: Must we measure all its components? Parasitol Today 2 :203–209.

  • 13

    Black WC IV, Moore CG, 1996. Population biology as a tool for studying vector-borne diseases. Beaty BJ, Marquardt WC, eds. The Biology of Disease Vectors. Niwot, CO: University Press of Colorado, 393–416.

    • PubMed
    • Export Citation
  • 14

    Bosio CF, Fulton RE, Salasek ML, Beaty BJ, Black WC IV, 2000. Quantitative trait loci that control vector competence for dengue-2 virus in the mosquito Aedes aegypti.Genetics 156 :687–698.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Besansky NJ, Hill CA, Costantini C, 2004. No accounting for taste: Host preference in malaria vectors. Trends Parasitol 20 :249–251.

  • 16

    Bates M, Roca-Garcia M, 1946. The development of the virus of yellow fever in Haemagogus mosquitoes. Am J Trop Med 26 :585–605.

  • 17

    Thu HM, Aye KM, Thein S, 1998. The effect of temperature and humidity on dengue virus propagation in Aedes aegypti mosquitos. Southeast Asian J Trop Med Public Health 29 :280–284.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Watts DM, Burke DS, Harrison BA, Whitmire RE, Nisalak A, 1987. Effect of temperature on the vector efficiency of Aedes aegypti for dengue 2 virus. Am J Trop Med Hyg 36 :143–152.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Dye C, 1992. The analysis of parasite transmission by bloodsucking insects. Annu Rev Entomol 37 :1–19.

  • 20

    Kramer LD, Ebel GD, 2003. Dynamics of flavivirus infection in mosquitoes. Adv Virus Res 60 :187–232.

  • 21

    Wang WK, Sung TL, Tsai YC, Kao CL, Chang SM, King CC, 2002. Detection of dengue virus replication in peripheral blood mononuclear cells from dengue virus type 2-infected patients by a reverse transcription-real-time PCR assay. J Clin Microbiol 40 :4472–4478.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Morlais I, Severson DW, 2001. Identification of a polymorphic mucin-like gene expressed in the midgut of the mosquito, Aedes aegypti, using an integrated bulked segregant and differential display analysis. Genetics 158 :1125–1136.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Morlais I, Mori A, Schneider JR, Severson DW, 2003. A targeted approach to the identification of candidate genes determining susceptibility to Plasmodium gallinaceum in Aedes aegypti.Mol Genet Genomics 269 :753–764.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Hornik K, 2006. The R FAQ. Available at: http://www.r-project.org/.

  • 25

    Gubler DJ, Rosen L, 1976. A simple technique for demonstrating transmission of dengue virus by mosquitoes without the use of vertebrate hosts. Am J Trop Med Hyg 25 :146–150.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Muir LE, Kay BH, 1998. Aedes aegypti survival and dispersal estimated by mark-release-recapture in northern Australia. Am J Trop Med Hyg 58 :277–282.

  • 27

    Tsuda Y, Takagi M, Wang S, Wang Z, Tang L, 2001. Movement of Aedes aegypti (Diptera: Culicidae) released in a small isolated village on Hainan Island, China. J Med Entomol 38 :93–98.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Trpis M, Hausermann W, 1986. Dispersal and other population parameters of Aedes aegypti in an African village and their possible significance in epidemiology of vector-borne diseases. Am J Trop Med Hyg 35 :1263–1279.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    McDonald PT, 1977. Population characteristics of domestic Aedes aegypti (Diptera: Culicidae) in villages on the Kenya Coast I. Adult survivorship and population size. J Med Entomol 14 :42–48.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Harrington LC, Buonaccorsi JP, Edman JD, Costero A, Kittayapong P, Clark GG, Scott TW, 2001. Analysis of survival of young and old Aedes aegypti (Diptera: Culicidac) from Puerto Rico and Thailand. J Med Entomol 38 :537–547.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Morrison AC, Costero A, Edman JD, Clark GG, Scott TW, 1999. Increased fecundity of Aedes aegypti fed human blood before release in a mark-recapture study in Puerto Rico. J Am Mosq Control Assoc 15 :98–104.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Conway GR, Trpis M, McClelland GAH, 1974. Population parameters of the mosquito Aedes aegypti (L.) estimated by mark-release-recapture in a suburban habitat in Tanzania. J Anim Ecol 43 :289–304.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Rosen L, Roseboom LE, Gubler DJ, Lien JC, Chaniotis BN, 1985. Comparative susceptibility of mosquito species and strains to oral and parenteral infection with dengue and Japanese encephalitis viruses. Am J Trop Med Hyg 34 :603–615.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Edgil D, Diamond MS, Holden KL, Paranjape SM, Harris E, 2003. Translation efficiency determines differences in cellular infection among dengue virus type 2 strains. Virology 317 :275–290.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Chiu WW, Kinney RM, Dreher TW, 2005. Control of translation by the 5′- and 3′-terminal regions of the dengue virus genome. J Virol 79 :8303–8315.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Holden KL, Harris E, 2004. Enhancement of dengue virus translation: role of the 3′ untranslated region and the terminal 3′ stem-loop domain. Virology 329 :119–133.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Cahour A, Pletnev A, Vazielle-Falcoz M, Rosen L, Lai CJ, 1995. Growth-restricted dengue virus mutants containing deletions in the 5′ noncoding region of the RNA genome. Virology 207 :68–76.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Leitmeyer KC, Vaughn DW, Watts DM, Salas R, Villalobos de C, I, Ramos C, Rico-Hesse R, 1999. Dengue virus structural differences that correlate with pathogenesis. J Virol 73 :4738–4747.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Cologna R, Rico-Hesse R, 2003. American genotype structures decrease dengue virus output from human monocytes and dendritic cells. J Virol 77 :3929–3938.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Vanlandingham DL, Schneider BS, Klingler K, Fair J, Beasley D, Huang J, Hamilton P, Higgs S, 2004. Real-time reverse transcriptase-polymerase chain reaction quantification of West Nile virus transmitted by Culex pipiens quinquefasciatus.Am J Trop Med Hyg 71 :120–123.

    • PubMed
    • Search Google Scholar
    • Export Citation
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