Transcriptomics of differential vector competence: West Nile virus infection in two populations of Culex pipiens quinquefasciatus linked to ovary development

BMC Genomics

Chelsea T Smartt¹  Carolina Acevedo¹  Ayse Civana¹  Dongyoung Shin¹ 

[1] Florida Medical Entomology Laboratory, University of Florida, 200 9th St. S.E., Vero Beach, FL 32962, USA

关键词: Vector competence;    High throughput RNA sequencing;    West Nile virus (WNV);    Culex pipiens quinquefasciatus;   

Others  :  857054
DOI  :  10.1186/1471-2164-15-513

 received in 2013-12-19, accepted in 2014-06-17,  发布年份 2014

【 摘 要 】

Background

Understanding mechanisms that contribute to viral dissemination in mosquito vectors will contribute to our ability to interfere with the transmission of viral pathogens that impact public health. The expression of genes in two Culex pipiens quinquefasciatus populations from Florida with known differences in vector competence to West Nile virus (WNV) were compared using high throughput sequencing.

Results

A total of 15,176 transcripts were combined for comparison of expression differences between the two populations and 118 transcripts were differentially expressed (p < 0.05). The fold change in expression of the differentially expressed genes ranged from -7.5 – 6.13. The more competent population for WNV (Gainesville) over expressed 77 genes and down regulated 44 genes, compared with the less competent population for WNV (Vero Beach). Also, splicing analysis identified 3 transcripts with significantly different splice forms between the two populations. The functional analysis showed that the largest proportion of transcripts was included in the catalytic activity and transporter activity groups except for those in the unknown group. Interestingly, the up- regulated gene set contained most of the catalytic activity function and the down- regulated gene set had a notable proportion of transcripts with transporter activity function. Immune response category was shown in only the down regulated gene set, although those represent a relatively small portion of the function. Several different vitellogenin genes were expressed differentially. Based on the RNAseq data analysis, ovary development was compared across the populations and following WNV infection. There were significant differences among the compared groups.

Conclusions

This study suggests that ovary development is correlated to vector competence in two Culex populations in Florida. Both populations control energy allocations to reproduction as a response to WNV. This result provides novel insight into the defense mechanism used by Culex spp. mosquitoes against WNV.

【 授权许可】

   
2014 Shin et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Dauphin G, Zientara S, Zeller H, Murgue B: West Nile: worldwide current situation in animals and humans. Comp Immunol Microb 2004, 27:343-355.
• [2]Hayes EB, Komar N, Nasci RS, Montgomery SP, O’Leary DR, Campbell GL: Epidemiology and transmission dynamics of West Nile virus disease. Emerg Infec Dis 2005, 11:1167-1173.
• [3]Epidemic/Epizootic West Nile virus in the United States: guidelines for surveillance, Prevention, and Control [http://stacks.cdc.gov/view/cdc/7271 webcite]
• [4]West Nile virus: Statistics, surveillance, and control [http://www.cdc.gov/ncidod/dvbid/westnile/surv&controlCaseCount07_detailed.htm webcite]
• [5]Kramer LD, Ebel GD: Dynamics of flavivirus infection in mosquitoes. Adv Virus Res 2003, 60:187-232.
• [6]Gubler DJ, Nalim S, Tan R, Saipan H, Sulianti Saroso J: Variation in susceptibility to oral infection with dengue virus among geographic strains of Aedes aegypti. Am J Trop Med 1979, 28:1045-1062.
• [7]Gubler DJ, Rosen L: Variation among geographic strains of Aedes albopictus is susceptibility to infection with dengue virus. Am J Trop Med 1976, 25:318-346.
• [8]Tabachnick WJ, Wallis GP, Aitken THG, Miller BR, Amato GD, Lorenz L, Powell JR, Beaty BJ: Oral infection of Aedes aegypti with yellow fever virus: Geographic variation and genetic considerations. Am J Trop Med 1985, 34:1219-1224.
• [9]Lozano-Fuentes S, Fernandez-Salas I, de Lourdes Munoz M, Garcia-Rejon J, Olson KE, Beaty BJ, Black WC: 4th: The neovolcanic axis is a barrier to gene flow among Aedes aegypti populations in Mexico that differ in vector competence for dengue 2 virus. PLoS Neglect Trop D 2009, 3(6):e468.
• [10]Beerntsen BT, James AA, Christensen BM: Genetics of mosquito vector competence. Microbiol Mol Biol R 2000, 64:115-137.
• [11]Blackmore CG, Stark LM, Jeter WC, Oliveri RL, Brooks RG, Conti LA, Wiersma ST: Surveillance results from the first West Nile virus transmission season in Florida, 2001. Am J Trop Med 2003, 69:141-150.
• [12]Godsey MS Jr, Nasci R, Savage HM, Aspen S, King R, Powers AM, Burkhalter K, Colton L, Charnetzky D, Lasater S, Taylor V, Palmisano CT: West Nile virus-infected mosquitoes, Louisiana, 2002. Emerg Infect Dis 2005, 11:1399-1404.
• [13]Girard YA, Popov V, Wen J, Han V, Higgs S: Ultrastructural study of West Nile virus pathogenesis in Culex pipiens quinquefasciatus (Diptera: Culicidae. J Med Entomol 2005, 42:429-444.
• [14]Colton L, Nasci RS: Quantification of West Nile virus in the saliva of Culex species collected from the southern United States. J Am Mosquito Contr 2006, 22:57-63.
• [15]Romoser WS, Turell MJ, Lerdthusnee K, Neira M, Dohm D, Ludwig G, Wasieloski L: Pathogenesis of Rift Valley fever virus in mosquitoes–tracheal conduits & the basallamina as an extra-cellular barrier. Archiv Virol 2005, 19:89-100.
• [16]Mahmood F, Chiles RE, Fang Y, Green EN, Reisen WK: Effects of time after infection, mosquito genotype, and infectious viral dose on the dynamics of Culex tarsalis vector competence for western equine encephalomyelitis virus. J Am Mosquito Contr 2006, 22:272-281.
• [17]Richards SL, Mores CN, Lord CC, Tabachnick WJ: Impact of extrinsic incubation temperature and virus exposure on vector competence of Culex pipiens quinquefasciatus (Diptera: Culicidae) for West Nile virus. Vector-borne and Zoonot 2007, 7:629-636.
• [18]Richards SL, Lord CC, Pesko K, Tabachnick WJ: Environmental and biological factors influencing Culex pipiens quinquefasciatus Say (Diptera: Culicidae) vector competence for Saint Louis encephalitis virus. Am J Trop Med 2009, 81:264-272.
• [19]Anderson SL, Richards SL, Tabachnick WJ, Smartt CT: Effects of West Nile virus dose and extrinsic incubation temperature on temporal progression of vector competence in Culex pipiens quinquefasciatus. J Am Mosquito Contr 2010, 26:103-107.
• [20]Keene KM, Foy BD, Sanchez-Vargas I, Beaty BJ, Blair CD, Olsen KE: RNA interference acts as a natural antiviral response to O’nyong-nyong virus (Alphavirus:Togaviridae) infection of Anopheles gambiae. PNAS 2004, 101:17240-17245.
• [21]Sanchez-Vargas I, Travanty EA, Keene KM, Franz AW, Beaty BJ, Blair CD, Olson KE: RNA interference, arthropod-borne viruses, and mosquitoes. Virus Res 2004, 102:65-74.
• [22]Souza-Neto JA, Sim S, Dimopoulos G: An evolutionary conserved function of the JAKSTAT pathway in anti-dengue defense. PNAS 2009, 106:17841-17846.
• [23]Sanders HR, Foy BD, Evans AM, Ross LS, Beaty BJ, Olson KE, Gill SS: Sindbis virus induces transport processes and alters expression of innate immunity pathway genes in the midgut of the disease vector, Aedes aegypti. Insect Biochem Molec 2005, 35:1293-1307.
• [24]Mercado-Curiel RF, Esquinca-Aviles HA, Tovar R, Diaz-Badillo A, Camacho-Nuez M, Munoz Mde L: The four serotypes of dengue recognize the same putative receptors in Aedes aegypti midgut and Ae. albopictus cells. BMC Microbiol 2006, 6:85.
• [25]Mercado-Curiel RF, Black WC, Muñoz ML: A dengue receptor as possible genetic marker of vector competence in Aedes aegypti. BMC Microbiol 2008, 8:118.
• [26]Girard YA, Klingler KA, Higgs S: West Nile virus dissemination and tissue tropisms in orally infected Culex pipiens quinquefasciatus. Vector Borne Zoonot D 2004, 4:109-122.
• [27]TR F, Hagedorn HH: Vitellogenin synthesis in the mosquito: the role of juvenile hormone in the development of responsiveness to ecdysone. Physiol Entomol 1977, 2:173-178.
• [28]Arrese EL, Soulages JL: Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 2010, 55:207-225.
• [29]Anderson JR, Rico-Hesse R: Aedes aegypti vectorial capacity is determined by the infecting genotype of dengue virus. Am J Trop Med Hyg 2006, 75(5):886-892.
• [30]Price DP, Nagarajan V, Churbanov A, Houde P, Milligan B, Drake LL, Gustafson JE, Hansen IA: The fat body transcriptomes of the yellow fever mosquito Aedes aegypti, pre- and post- blood meal. PLoS One 2011, 6(7):e22573.
• [31]Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
• [32]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25.
• [33]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-515.
• [34]Jiang H, Wong WH: Statistical inferences for isoform expression in RNA-Seq. Bioinformatics 2009, 25:1026-1032.