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      The Aquaporin Gene Family of the Yellow Fever Mosquito, Aedes aegypti

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          Abstract

          Background

          The mosquito, Aedes aegypti, is the principal vector of the Dengue and yellow fever viruses. During feeding, an adult female can take up more than its own body weight in vertebrate blood. After a blood meal females excrete large amounts of urine through their excretion system, the Malpighian tubules (MT). Diuresis starts within seconds after the mosquito starts feeding. Aquaporins (AQPs) are a family of membrane transporters that regulate the flow of water, glycerol and other small molecules across cellular membranes in both prokaryotic and eukaryotic cells. Our aim was to identify aquaporins that function as water channels, mediating transcellular water transport in MTs of adult female Ae. aegypti.

          Methodology/Principal Findings

          Using a bioinformatics approach we screened genome databases and identified six putative AQPs in the genome of Ae. aegypti. Phylogenetic analysis showed that five of the six Ae. aegypti AQPs have high similarity to classical water-transporting AQPs of vertebrates. Using microarray, reverse transcription and real time PCR analysis we found that all six AQPs are expressed in distinct patterns in mosquito tissues/body parts. AaAQP1, 4, and 5 are strongly expressed in the adult female MT. RNAi-mediated knockdown of the MT-expressed mosquito AQPs resulted in significantly reduced diuresis.

          Conclusions/Significance

          Our results support the notion that AQP1, 4, and 5 function as water transporters in the MTs of adult female Ae. aegypti mosquitoes. Our results demonstrate the importance of these AQPs for mosquito diuresis after blood ingestion and highlight their potential as targets for the development of novel vector control strategies.

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          Most cited references29

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          The genome sequence of the malaria mosquito Anopheles gambiae.

          Anopheles gambiae is the principal vector of malaria, a disease that afflicts more than 500 million people and causes more than 1 million deaths each year. Tenfold shotgun sequence coverage was obtained from the PEST strain of A. gambiae and assembled into scaffolds that span 278 million base pairs. A total of 91% of the genome was organized in 303 scaffolds; the largest scaffold was 23.1 million base pairs. There was substantial genetic variation within this strain, and the apparent existence of two haplotypes of approximately equal frequency ("dual haplotypes") in a substantial fraction of the genome likely reflects the outbred nature of the PEST strain. The sequence produced a conservative inference of more than 400,000 single-nucleotide polymorphisms that showed a markedly bimodal density distribution. Analysis of the genome sequence revealed strong evidence for about 14,000 protein-encoding transcripts. Prominent expansions in specific families of proteins likely involved in cell adhesion and immunity were noted. An expressed sequence tag analysis of genes regulated by blood feeding provided insights into the physiological adaptations of a hematophagous insect.
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            An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense.

            Here, we show that the major mosquito vector for dengue virus uses the JAK-STAT pathway to control virus infection. Dengue virus infection in Aedes aegypti mosquitoes activates the JAK-STAT immune signaling pathway. The mosquito's susceptibility to dengue virus infection increases when the JAK-STAT pathway is suppressed through RNAi depletion of its receptor Domeless (Dome) and the Janus kinase (Hop), whereas mosquitoes become more resistant to the virus when the negative regulator of the JAK-STAT pathway, PIAS, is silenced. The JAK-STAT pathway exerts its anti-dengue activity presumably through one or several STAT-regulated effectors. We have identified, and partially characterized, two JAK-STAT pathway-regulated and infection-responsive dengue virus restriction factors (DVRFs) that contain putative STAT-binding sites in their promoter regions. Our data suggest that the JAK-STAT pathway is part of the A. aegypti mosquito's anti-dengue defense and may act independently of the Toll pathway and the RNAi-mediated antiviral defenses.
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              Molecules as documents of evolutionary history.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                29 December 2010
                : 5
                : 12
                : e15578
                Affiliations
                [1 ]Department of Biology, New Mexico State University, Las Cruces, New Mexico, United States of America
                [2 ]Institute of Applied Biosciences, New Mexico State University, Las Cruces, New Mexico, United States of America
                [3 ]Molecular Biology Program, New Mexico State University, Las Cruces, New Mexico, United States of America
                [4 ]Chicago Medical School, Rosalind Franklin University, North Chicago, Illinois, United States of America
                [5 ]Department of Molecular Biology and Biochemistry, University of California Irvine, Irvine, California, United States of America
                Universidade Federal do Rio de Janeiro, Brazil
                Author notes

                Conceived and designed the experiments: IAH DYB OM. Performed the experiments: LLD VKC DYB OM. Analyzed the data: IAH LLD DYB OM ALD. Contributed reagents/materials/analysis tools: DYB OM ALD IAH. Wrote the paper: LLD IAH.

                Article
                PONE-D-10-00138
                10.1371/journal.pone.0015578
                3014591
                21249121
                493d59ee-0587-48b2-95da-4bab0360e56c
                Drake et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 29 July 2010
                : 17 November 2010
                Page count
                Pages: 9
                Categories
                Research Article
                Biology
                Microbiology
                Vector Biology
                Mosquitoes
                Anatomy and Physiology
                Digestive System
                Digestive Physiology
                Medicine
                Infectious Diseases
                Vectors and Hosts
                Mosquitoes

                Uncategorized
                Uncategorized

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