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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

Comparison of saliva volume of WT (white) and wMel.F mosquitoes (grey) of different ages.Saliva volume is measure through the sphere volume of saliva droplets using mineral oil. Bars depict means ±S.E.M. Number of replicates range from 33 to 80 with a mean of 62 individuals for WT mosquitoes and 34 to 85 with a mean of 64 for wMel.F mosquitoes. 86.8% of all the mosquitoes produced saliva during the assay.
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pntd.0003894.g006: Comparison of saliva volume of WT (white) and wMel.F mosquitoes (grey) of different ages.Saliva volume is measure through the sphere volume of saliva droplets using mineral oil. Bars depict means ±S.E.M. Number of replicates range from 33 to 80 with a mean of 62 individuals for WT mosquitoes and 34 to 85 with a mean of 64 for wMel.F mosquitoes. 86.8% of all the mosquitoes produced saliva during the assay.

Mentions: To determine if the dynamics in saliva DENV titer and infectivity can be explained by mosquito saliva production we compared the saliva volume of the two mosquito populations over time in their natural DENV uninfected state (Fig 6). wMel.F mosquitoes produced less saliva as compared to WT mosquitoes (df = 1, F = 55.3, P<0.0001). The age of the mosquitoes was also a determinant of saliva volume (df = 1, F = 17.5, P<0.0001). In WT mosquitoes, saliva volume increased as mosquitoes aged until 17 days of age and then declined. In wMel.F mosquitoes saliva volume remained low throughout the lifespan of the mosquitoes. The saliva volume also varied hugely between individuals especially on day 17 (ranged 0.11–23.63nL) in WT mosquitoes. The dynamics of expectorated saliva volume mirror that of DENV titer and the dynamics of the infective mosquitoes, all peaking between 5 and 11 DPI. Together, the results suggest that wMel.F mosquitoes expectorate less DENV, which can at least be partly explained by producing less saliva and older mosquitoes are less likely to expectorate detectable DENV as their saliva volume deceases with age.


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)

Comparison of saliva volume of WT (white) and wMel.F mosquitoes (grey) of different ages.Saliva volume is measure through the sphere volume of saliva droplets using mineral oil. Bars depict means ±S.E.M. Number of replicates range from 33 to 80 with a mean of 62 individuals for WT mosquitoes and 34 to 85 with a mean of 64 for wMel.F mosquitoes. 86.8% of all the mosquitoes produced saliva during the assay.
© Copyright Policy
Related In: Results  -  Collection

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

pntd.0003894.g006: Comparison of saliva volume of WT (white) and wMel.F mosquitoes (grey) of different ages.Saliva volume is measure through the sphere volume of saliva droplets using mineral oil. Bars depict means ±S.E.M. Number of replicates range from 33 to 80 with a mean of 62 individuals for WT mosquitoes and 34 to 85 with a mean of 64 for wMel.F mosquitoes. 86.8% of all the mosquitoes produced saliva during the assay.
Mentions: To determine if the dynamics in saliva DENV titer and infectivity can be explained by mosquito saliva production we compared the saliva volume of the two mosquito populations over time in their natural DENV uninfected state (Fig 6). wMel.F mosquitoes produced less saliva as compared to WT mosquitoes (df = 1, F = 55.3, P<0.0001). The age of the mosquitoes was also a determinant of saliva volume (df = 1, F = 17.5, P<0.0001). In WT mosquitoes, saliva volume increased as mosquitoes aged until 17 days of age and then declined. In wMel.F mosquitoes saliva volume remained low throughout the lifespan of the mosquitoes. The saliva volume also varied hugely between individuals especially on day 17 (ranged 0.11–23.63nL) in WT mosquitoes. The dynamics of expectorated saliva volume mirror that of DENV titer and the dynamics of the infective mosquitoes, all peaking between 5 and 11 DPI. Together, the results suggest that wMel.F mosquitoes expectorate less DENV, which can at least be partly explained by producing less saliva and older mosquitoes are less likely to expectorate detectable DENV as their saliva volume deceases with age.

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