Abstract
Despite the devastating impact of mosquito-borne illnesses on human health, surprisingly little is known about mosquito developmental biology, including development of the olfactory system, a tissue of vector importance. Analysis of mosquito olfactory developmental genetics has been hindered by a lack of means to target specific genes during the development of this sensory system. In this investigation, chitosan/siRNA nanoparticles were used to target semaphorin-1a (sema1a) during olfactory system development in the dengue and yellow fever vector mosquito Aedes aegypti. Immunohistochemical analyses and anterograde tracing of antennal sensory neurons, which were used to track the progression of olfactory development in this species, revealed antennal lobe defects in sema1a knockdown fourth instar larvae. These findings, which correlated with a larval odorant tracking behavioral phenotype, identified previously unreported roles for Sema1a in the developing insect larval olfactory system. Analysis of sema1a knockdown pupae also revealed a number of olfactory phenotypes, including olfactory receptor neuron targeting and projection neuron defects coincident with a collapse in the structure and shape of the antennal lobe and individual glomeruli. This study, which is to our knowledge the first functional genetic analysis of insect olfactory development outside of D. melanogaster, identified critical roles for Sema1a during Ae. aegypti larval and pupal olfactory development and advocates the use of chitosan/siRNA nanoparticles as an effective means of targeting genes during post-embryonic Ae. aegypti development. Use of siRNA nanoparticle methodology to understand sensory developmental genetics in mosquitoes will provide insight into the evolutionary conservation and divergence of key developmental genes which could be exploited in the development of both common and species-specific means for intervention.
Highlights
A lack of functional genetic analyses in vector mosquitoes has prevented us from gaining insight into how the process of development is regulated in these insect vectors of human disease
We analyze development of the Aedes aegypti olfactory system, a tissue of vector importance which is critical for recognition of human blood meal hosts and many other essential behaviors
We used small interfering RNAs, which were delivered through chitosan nanoparticle feedings to larvae, to target the axon guidance gene semaphorin-1a
Summary
A lack of functional genetic analyses in vector mosquitoes has prevented us from gaining insight into how the process of development is regulated in these insect vectors of human disease. To address this problem, we have begun to functionally characterize the development of the dengue and yellow fever vector mosquito Aedes aegypti [1]. D. melanogaster Sema1a, a transmembrane member of this family initially studied in the context of the embryonic ventral nerve cord, is required for proper development of the Drosophila pupal olfactory system [12,13,14,15]. Graded Sema1a expression in the antennal lobe is required for the proper targeting of projection neuron dendrites
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