Abstract
BackgroundDigestion of blood in the midgut of Aedes aegypti results in the release of pro-oxidant molecules that can be toxic to the mosquito. We hypothesized that after a blood meal, the antioxidant capacity of the midgut is increased to protect cells against oxidative stress. Concomitantly, pathogens present in the blood ingested by mosquitoes, such as the arboviruses Dengue and Zika, also have to overcome the same oxidative challenge, and the antioxidant program induced by the insect is likely to influence infection status of the mosquito and its vectorial competence.Methodology/Principal findingsWe found that blood-induced catalase mRNA and activity in the midgut peaked 24 h after feeding and returned to basal levels after the completion of digestion. RNAi-mediated silencing of catalase (AAEL013407-RB) reduced enzyme activity in the midgut epithelia, increased H2O2 leakage and decreased fecundity and lifespan when mosquitoes were fed H2O2. When infected with Dengue 4 and Zika virus, catalase-silenced mosquitoes showed no alteration in infection intensity (number of plaque forming units/midgut) 7 days after the infectious meal. However, catalase knockdown reduced Dengue 4, but not Zika, infection prevalence (percent of infected midguts).Conclusion/SignificanceHere, we showed that blood ingestion triggers an antioxidant response in the midgut through the induction of catalase. This protection facilitates the establishment of Dengue virus in the midgut. Importantly, this mechanism appears to be specific for Dengue because catalase silencing did not change Zika virus prevalence. In summary, our data suggest that redox balance in the midgut modulates mosquito vectorial competence to arboviral infections.
Highlights
Arthropod-borne viral diseases, such as Dengue, Chikungunya, and especially Zika, have recently occupied a central spot in the global discussions concerning infectious diseases due to the rapid spread of cases worldwide and the associated increase in syndromes such as microcephaly and Guillain–Barre, prompting the World Health Organization to declare Zika a public health emergency [1]
Mosquitoes act as important vectors of human diseases because during a blood meal they might ingest microorganism circulating in our blood, such as dengue and zika virus
The adaptive antioxidant program that protects mosquito tissues against the oxidative challenge imposed by a blood meal might influences the ability of virus to establish infection and disseminate from the midgut to the salivary glands
Summary
Arthropod-borne viral (arboviral) diseases, such as Dengue, Chikungunya, and especially Zika, have recently occupied a central spot in the global discussions concerning infectious diseases due to the rapid spread of cases worldwide and the associated increase in syndromes such as microcephaly and Guillain–Barre, prompting the World Health Organization to declare Zika a public health emergency [1]. Strategies targeting Aedes aegypti, the mosquito vector, such as utilizing the anti-viral effects of Wolbachia [4,5] and the sterile insect technique [6,7], are attractive possibilities under implementation. To stop mosquito spread of arboviral diseases, we need to further elucidate the molecular interactions between the virus and the vector. This knowledge will help to explain, for example, the observed differences in susceptibility to viral infections of mosquito strains/populations[8,9]. Pathogens present in the blood ingested by mosquitoes, such as the arboviruses Dengue and Zika, have to overcome the same oxidative challenge, and the antioxidant program induced by the insect is likely to influence infection status of the mosquito and its vectorial competence
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