Effect of repeat human blood feeding on Wolbachia density and dengue virus infection in Aedes aegypti

Particle and Fibre Toxicology

Elizabeth A McGraw¹  Cameron P Simmons²  Hilaria E Amuzu¹ 

[1] School of Biological Sciences, Monash University, Clayton, Melbourne, Victoria, Australia;Department of Microbiology and Immunology, University of Melbourne, Parkville, Melbourne, Victoria, Australia

关键词: Blood feeding;    Aedes aegypti;    Dengue;    Wolbachia;   

Others  :  1181782
DOI  :  10.1186/s13071-015-0853-y

 received in 2014-11-25, accepted in 2015-04-13,  发布年份 2015

【 摘 要 】

Background

The introduction of the endosymbiotic bacterium, Wolbachia into Aedes aegypti populations is a novel approach to reduce disease transmission. The presence of Wolbachia limits the ability of the mosquito to transmit dengue virus (DENV) and the strength of this effect appears to correlate with Wolbachia densities in the mosquito. There is also some evidence that Wolbachia densities may increase following the consumption of a bloodmeal. Here we have examined whether multiple blood feeds lead to increases in density or associated changes in Wolbachia-mediated blocking of DENV.

Methods

The Wolbachia infected Aedes aegypti mosquito line was used for the study. There were three treatment groups; a non-blood fed control, a second group fed once and a third group fed twice on human blood. All groups were orally infected with DENV-2 and then their midguts and salivary glands were dissected 10–11 days post infection. RNA/DNA was simultaneously extracted from each tissue and subsequently used for DENV RNA copies and Wolbachia density quantification, respectively.

Results

We found variation between replicate vector competence experiments and no clear evidence that Wolbachia numbers increased in either the salivary glands or remainder of the body with feeding and hence saw no corresponding improvements in DENV blocking.

Conclusions

Aedes aegypti are “sip” feeders returning often to obtain bloodmeals and hence it is important to assess whether repeat blood feeding improved the efficacy of Wolbachia-based DENV blocking. Our work suggests in the laboratory context when Wolbachia densities are high that repeat feeding does not improve blocking and hence this ability should likely be stable with respect to feeding cycle in the field.

【 授权许可】

   
2015 Amuzu et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Bhatt S, Gething WP, Brady JO, Messina PJ, Farlow WA, Moyes LC. The global distribution and burden of dengue. Nature. 2013; 496:504-7.
• [2]WHO. Dengue: guidelines for diagnosis, treatment, prevention and control: New edition. Geneva: WHO press; 2009.
• [3]Thomas SJ, Endy TP. Critical issues in dengue vaccine development. Curr Opin Infect Dis. 2011; 24(5):442-50.
• [4]Zug R, Hammerstein P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One. 2012; 7(6):e38544.
• [5]Kittayapong P, Baisley KJ, Baimai V, O'Neill SL. Distribution and diversity of Wolbachia infections in Southeast Asian mosquitoes (Diptera: Culicidae). J Med Entomol. 2000; 37(3):340-5.
• [6]Xi Z, Dean JL, Khoo C, Dobson SL. Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem Mol Biol. 2005; 35(8):903-10.
• [7]McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, Wang YF et al.. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science. 2009; 323(5910):141-4.
• [8]Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ et al.. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature. 2011; 476(7361):450-3.
• [9]Serbus LR, Casper-Lindley C, Landmann F, Sullivan W. The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet. 2008; 42:683-707.
• [10]Xi Z, Khoo CC, Dobson SL. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science. 2005; 310(5746):326-8.
• [11]Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM et al.. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell. 2009; 139(7):1268-78.
• [12]Caragata EP, Rances E, Hedges LM, Gofton AW, Johnson KN, O'Neill SL et al.. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog. 2013; 9(6):e1003459.
• [13]Rances E, Ye YH, Woolfit M, McGraw EA, O'Neill SL. The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog. 2012; 8(2):e1002548.
• [14]Pan X, Zhou G, Wu J, Bian G, Lu P, Raikhel AS 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 U S A. 2012; 109(1):E23-31.
• [15]Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F et al.. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature. 2011; 476(7361):454-7.
• [16]Iturbe-Ormaetxe I, Walker T, ON SL. Wolbachia and the biological control of mosquito-borne disease. EMBO Rep. 2011; 12(6):508-18.
• [17]Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, Rousset F et al.. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Mol Biol. 1999; 29(2):153-60.
• [18]Bian G, Xu Y, Lu P, Xie Y, Xi Z. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog. 2010; 6(4):e1000833.
• [19]Frentiu FD, Robinson J, Young PR, McGraw EA, O'Neill SL. Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS One. 2010; 5(10):e13398.
• [20]Lu P, Bian G, Pan X, Xi Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis. 2012; 6(7):e1754.
• [21]Ikeda T, Ishikawa H, Sasaki T. Regulation of Wolbachia density in the Mediterranean flour moth, Ephestia kuehniella, and the almond moth, Cadra cautella. Zoolog Sci. 2003; 20(2):153-7.
• [22]Kondo N, Shimada M, Fukatsu T. Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol Lett. 2005; 1(4):488-91.
• [23]Mouton L, Henri H, Charif D, Bouletreau M, Vavre F. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol Lett. 2007; 3(2):210-3.
• [24]Dutton TJ, Sinkins SP. Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Insect Mol Biol. 2004; 13(3):317-22.
• [25]Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, van den Hurk A et al.. Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia. PLoS Negl Trop Dis. 2014; 8(2):e2688.
• [26]Black WC, Bennett KE, Gorrochotegui-Escalante N, Barillas-Mury CV, Fernandez-Salas I, de Lourdes MM et al.. Flavivirus susceptibility in Aedes aegypti. Arch Med Res. 2002; 33(4):379-88.
• [27]Warrilow D, Northill JA, Pyke A, Smith GA. Single rapid TaqMan fluorogenic probe based PCR assay that detects all four dengue serotypes. J Med Virol. 2002; 66(4):524-8.
• [28]Thellin O, Zorzi W, Lakaye B, De Borman B, Coumans B, Hennen G et al.. Housekeeping genes as internal standards: use and limits. J Biotechnol. 1999; 75(2–3):291-5.
• [29]Cook PE, Hugo LE, Iturbe-Ormaetxe I, Williams CR, Chenoweth SF, Ritchie SA et al.. The use of transcriptional profiles to predict adult mosquito age under field conditions. Proc Natl Acad Sci U S A. 2006; 103(48):18060-5.
• [30]Ye YH, Woolfit M, Rances E, O'Neill SL, McGraw EA. Wolbachia-associated bacterial protection in the mosquito Aedes aegypti. PLoS Negl Trop Dis. 2013; 7(8):e2362.
• [31]Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Strickman D et al.. Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: blood feeding frequency. J Med Entomol. 2000; 37(1):89-101.
• [32]Scott TW, Chow E, Strickman D, Kittayapong P, Wirtz RA, Lorenz LH et al.. Blood-feeding patterns of Aedes aegypti (Diptera: Culicidae) collected in a rural Thai village. J Med Entomol. 1993; 30(5):922-7.
• [33]Scott TW, Clark GG, Lorenz LH, Amerasinghe PH, Reiter P, Edman JD. Detection of multiple blood feeding in Aedes aegypti (Diptera: Culicidae) during a single gonotrophic cycle using a histologic technique. J Med Entomol. 1993; 30(1):94-9.
• [34]Koella JC, Sorense FL. Effect of adult nutrition on the melanization immune response of the malaria vector Anopheles stephensi. Med Vet Entomol. 2002; 16(3):316-20.
• [35]Chun J, Riehle M, Paskewitz SM. Effect of mosquito age and reproductive status on melanization of sephadex beads in Plasmodium-refractory and -susceptible strains of Anopheles gambiae. J Invertebr Pathol. 1995; 66(1):11-7.
• [36]Baton LA, Pacidonio EC, Goncalves DS, Moreira LA. wFlu: characterization and evaluation of a native Wolbachia from the mosquito Aedes fluviatilis as a potential vector control agent. PLoS One. 2013; 8(3):e59619.
• [37]Zouache K, Voronin D, Tran-Van V, Mousson L, Failloux AB, Mavingui P. Persistent Wolbachia and cultivable bacteria infection in the reproductive and somatic tissues of the mosquito vector Aedes albopictus. PLoS One. 2009; 4(7):e6388.
• [38]McCall K. Eggs over easy: cell death in the Drosophila ovary. Dev Biol. 2004; 274(1):3-14.
• [39]Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, Sullivan W. Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog. 2005; 1(2):e14.
• [40]Caragata EP, Rances E, O'Neill SL, McGraw EA. Competition for amino acids between Wolbachia and the mosquito host, Aedes aegypti. Microb Ecol. 2014; 67(1):205-18.
• [41]McMeniman CJ, Hughes GL, O'Neill SL. A Wolbachia symbiont in Aedes aegypti disrupts mosquito egg development to a greater extent when mosquitoes feed on nonhuman versus human blood. J Med Entomol. 2011; 48(1):76-84.