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Wolbachia Reduces the Transmission Potential of Dengue-Infected Aedes aegypti.

Ye YH, Carrasco AM, Frentiu FD, Chenoweth SF, Beebe NW, van den Hurk AF, Simmons CP, O'Neill SL, McGraw EA - PLoS Negl Trop Dis (2015)

Bottom Line: We show that wMel lengthens the EIP, reduces the frequency at which the virus is expectorated and decreases the dengue copy number in mosquito saliva as compared to wild-type mosquitoes.These observations can at least be partially explained by an overall reduction in saliva produced by wMel mosquitoes.The lengthening of EIP highlights another means, in addition to the reduction of infection frequencies and DENV titers in mosquitoes, by which Wolbachia should operate to reduce DENV transmission in the field.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, Monash University, Clayton, Victoria, Australia.

ABSTRACT

Background: Dengue viruses (DENV) are the causative agents of dengue, the world's most prevalent arthropod-borne disease with around 40% of the world's population at risk of infection annually. Wolbachia pipientis, an obligate intracellular bacterium, is being developed as a biocontrol strategy against dengue because it limits replication of the virus in the mosquito. The Wolbachia strain wMel, which has been introduced into the mosquito vector, Aedes aegypti, has been shown to invade and spread to near fixation in field releases. Standard measures of Wolbachia's efficacy for blocking virus replication focus on the detection and quantification of virus in mosquito tissues. Examining the saliva provides a more accurate measure of transmission potential and can reveal the extrinsic incubation period (EIP), that is, the time it takes virus to arrive in the saliva following the consumption of DENV viremic blood. EIP is a key determinant of a mosquito's ability to transmit DENVs, as the earlier the virus appears in the saliva the more opportunities the mosquito will have to infect humans on subsequent bites.

Methodology/principal findings: We used a non-destructive assay to repeatedly quantify DENV in saliva from wMel-infected and Wolbachia-free wild-type control mosquitoes following the consumption of a DENV-infected blood meal. We show that wMel lengthens the EIP, reduces the frequency at which the virus is expectorated and decreases the dengue copy number in mosquito saliva as compared to wild-type mosquitoes. These observations can at least be partially explained by an overall reduction in saliva produced by wMel mosquitoes. More generally, we found that the concentration of DENV in a blood meal is a determinant of the length of EIP, saliva virus titer and mosquito survival.

Conclusions/significance: The saliva-based traits reported here offer more disease-relevant measures of Wolbachia's effects on the vector and the virus. The lengthening of EIP highlights another means, in addition to the reduction of infection frequencies and DENV titers in mosquitoes, by which Wolbachia should operate to reduce DENV transmission in the field.

No MeSH data available.


Related in: MedlinePlus

Survival curves of WT (grey line) and wMel.F mosquitoes (black line) orally infected with either 107 (A) or 106 (B) PFU/ml of DENV.Bars depict means ± S.E.M.
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pntd.0003894.g004: Survival curves of WT (grey line) and wMel.F mosquitoes (black line) orally infected with either 107 (A) or 106 (B) PFU/ml of DENV.Bars depict means ± S.E.M.

Mentions: The presence of wMel infection lengthened the lifespan of mosquitoes as compared to WT following DENV infection. This effect was significant for mosquitoes fed both high (P<0.001, Fig 4A) and low (P<0.0001, Fig 4B) DENV titer blood meals. The titer of DENV in the blood meal was inversely correlated with mosquito survival. WT mosquitoes infected with 107 PFU/ml of DENV died more quickly than those infected with the lower titer of 106 PFU/ml (P<0.001). This suggests that DENV infection is costly to mosquitoes and that Wolbachia is providing some protection to the host.


Wolbachia Reduces the Transmission Potential of Dengue-Infected Aedes aegypti.

Ye YH, Carrasco AM, Frentiu FD, Chenoweth SF, Beebe NW, van den Hurk AF, Simmons CP, O'Neill SL, McGraw EA - PLoS Negl Trop Dis (2015)

Survival curves of WT (grey line) and wMel.F mosquitoes (black line) orally infected with either 107 (A) or 106 (B) PFU/ml of DENV.Bars depict means ± S.E.M.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4482661&req=5

pntd.0003894.g004: Survival curves of WT (grey line) and wMel.F mosquitoes (black line) orally infected with either 107 (A) or 106 (B) PFU/ml of DENV.Bars depict means ± S.E.M.
Mentions: The presence of wMel infection lengthened the lifespan of mosquitoes as compared to WT following DENV infection. This effect was significant for mosquitoes fed both high (P<0.001, Fig 4A) and low (P<0.0001, Fig 4B) DENV titer blood meals. The titer of DENV in the blood meal was inversely correlated with mosquito survival. WT mosquitoes infected with 107 PFU/ml of DENV died more quickly than those infected with the lower titer of 106 PFU/ml (P<0.001). This suggests that DENV infection is costly to mosquitoes and that Wolbachia is providing some protection to the host.

Bottom Line: We show that wMel lengthens the EIP, reduces the frequency at which the virus is expectorated and decreases the dengue copy number in mosquito saliva as compared to wild-type mosquitoes.These observations can at least be partially explained by an overall reduction in saliva produced by wMel mosquitoes.The lengthening of EIP highlights another means, in addition to the reduction of infection frequencies and DENV titers in mosquitoes, by which Wolbachia should operate to reduce DENV transmission in the field.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, Monash University, Clayton, Victoria, Australia.

ABSTRACT

Background: Dengue viruses (DENV) are the causative agents of dengue, the world's most prevalent arthropod-borne disease with around 40% of the world's population at risk of infection annually. Wolbachia pipientis, an obligate intracellular bacterium, is being developed as a biocontrol strategy against dengue because it limits replication of the virus in the mosquito. The Wolbachia strain wMel, which has been introduced into the mosquito vector, Aedes aegypti, has been shown to invade and spread to near fixation in field releases. Standard measures of Wolbachia's efficacy for blocking virus replication focus on the detection and quantification of virus in mosquito tissues. Examining the saliva provides a more accurate measure of transmission potential and can reveal the extrinsic incubation period (EIP), that is, the time it takes virus to arrive in the saliva following the consumption of DENV viremic blood. EIP is a key determinant of a mosquito's ability to transmit DENVs, as the earlier the virus appears in the saliva the more opportunities the mosquito will have to infect humans on subsequent bites.

Methodology/principal findings: We used a non-destructive assay to repeatedly quantify DENV in saliva from wMel-infected and Wolbachia-free wild-type control mosquitoes following the consumption of a DENV-infected blood meal. We show that wMel lengthens the EIP, reduces the frequency at which the virus is expectorated and decreases the dengue copy number in mosquito saliva as compared to wild-type mosquitoes. These observations can at least be partially explained by an overall reduction in saliva produced by wMel mosquitoes. More generally, we found that the concentration of DENV in a blood meal is a determinant of the length of EIP, saliva virus titer and mosquito survival.

Conclusions/significance: The saliva-based traits reported here offer more disease-relevant measures of Wolbachia's effects on the vector and the virus. The lengthening of EIP highlights another means, in addition to the reduction of infection frequencies and DENV titers in mosquitoes, by which Wolbachia should operate to reduce DENV transmission in the field.

No MeSH data available.


Related in: MedlinePlus