Xanthine dehydrogenase‐1 silencing in Aedes aegypti mosquitoes promotes a blood feeding–induced adulticidal activity

ABSTRACT Aedes aegypti has 2 genes encoding xanthine dehydrogenase (XDH). We analyzed XDH1 and XDH2 gene expression by real‐time quantitative PCR in tissues from sugar‐ and blood‐fed females. Differential XDH1 and XDH2 gene expression was observed in tissues dissected throughout a time course. We ne...

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Veröffentlicht in:The FASEB journal 2017-06, Vol.31 (6), p.2276-2286
Hauptverfasser: Isoe, Jun, Petchampai, Natthida, Isoe, Yurika E., Co, Katrina, Mazzalupo, Stacy, Scaraffia, Patricia Y.
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container_issue 6
container_start_page 2276
container_title The FASEB journal
container_volume 31
creator Isoe, Jun
Petchampai, Natthida
Isoe, Yurika E.
Co, Katrina
Mazzalupo, Stacy
Scaraffia, Patricia Y.
description ABSTRACT Aedes aegypti has 2 genes encoding xanthine dehydrogenase (XDH). We analyzed XDH1 and XDH2 gene expression by real‐time quantitative PCR in tissues from sugar‐ and blood‐fed females. Differential XDH1 and XDH2 gene expression was observed in tissues dissected throughout a time course. We next exposed females to blood meals supplemented with allopurinol, a well‐characterized XDH inhibitor. We also tested the effects of injecting double‐stranded RNA (dsRNA) against XDH1, XDH2, or both. Disruption of XDH by allopurinol or XDH1 by RNA interference significantly affected mosquito survival, causing a disruption in blood digestion, excretion, oviposition, and reproduction. XDH1‐deficient mosquitoes showed a persistence of serine proteases in the midgut at 48 h after blood feeding and a reduction in the uptake of vitellogenin by the ovaries. Surprisingly, analysis of the fat body from dsRNA‐XDH1‐injected mosquitoes fell into 2 groups: one group was characterized by a reduction of the XDH1 transcript, whereas the other group was characterized by an up‐regulation of several transcripts, including XDH1, glutamine synthetase, alanine aminotransferase, catalase, superoxide dismutase, ornithine decarboxylase, glutamate receptor, and ammonia transporter. Our data demonstrate that XDH1 plays an essential role and that XDH1 has the potential to be used as a metabolic target for Ae. aegypti vector control.—Isoe, J., Petchampai, N., Isoe, Y. E., Co, K., Mazzalupo, S., Scaraffia, P. Y. Xanthine dehydrogenase‐1 silencing in Aedes aegypti mosquitoes promotes a blood feeding–induced adulticidal activity. FASEB J. 31, 2276–2286 (2017). www.fasebj.org
doi_str_mv 10.1096/fj.201601185R
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We analyzed XDH1 and XDH2 gene expression by real‐time quantitative PCR in tissues from sugar‐ and blood‐fed females. Differential XDH1 and XDH2 gene expression was observed in tissues dissected throughout a time course. We next exposed females to blood meals supplemented with allopurinol, a well‐characterized XDH inhibitor. We also tested the effects of injecting double‐stranded RNA (dsRNA) against XDH1, XDH2, or both. Disruption of XDH by allopurinol or XDH1 by RNA interference significantly affected mosquito survival, causing a disruption in blood digestion, excretion, oviposition, and reproduction. XDH1‐deficient mosquitoes showed a persistence of serine proteases in the midgut at 48 h after blood feeding and a reduction in the uptake of vitellogenin by the ovaries. Surprisingly, analysis of the fat body from dsRNA‐XDH1‐injected mosquitoes fell into 2 groups: one group was characterized by a reduction of the XDH1 transcript, whereas the other group was characterized by an up‐regulation of several transcripts, including XDH1, glutamine synthetase, alanine aminotransferase, catalase, superoxide dismutase, ornithine decarboxylase, glutamate receptor, and ammonia transporter. Our data demonstrate that XDH1 plays an essential role and that XDH1 has the potential to be used as a metabolic target for Ae. aegypti vector control.—Isoe, J., Petchampai, N., Isoe, Y. E., Co, K., Mazzalupo, S., Scaraffia, P. Y. Xanthine dehydrogenase‐1 silencing in Aedes aegypti mosquitoes promotes a blood feeding–induced adulticidal activity. 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We analyzed XDH1 and XDH2 gene expression by real‐time quantitative PCR in tissues from sugar‐ and blood‐fed females. Differential XDH1 and XDH2 gene expression was observed in tissues dissected throughout a time course. We next exposed females to blood meals supplemented with allopurinol, a well‐characterized XDH inhibitor. We also tested the effects of injecting double‐stranded RNA (dsRNA) against XDH1, XDH2, or both. Disruption of XDH by allopurinol or XDH1 by RNA interference significantly affected mosquito survival, causing a disruption in blood digestion, excretion, oviposition, and reproduction. XDH1‐deficient mosquitoes showed a persistence of serine proteases in the midgut at 48 h after blood feeding and a reduction in the uptake of vitellogenin by the ovaries. Surprisingly, analysis of the fat body from dsRNA‐XDH1‐injected mosquitoes fell into 2 groups: one group was characterized by a reduction of the XDH1 transcript, whereas the other group was characterized by an up‐regulation of several transcripts, including XDH1, glutamine synthetase, alanine aminotransferase, catalase, superoxide dismutase, ornithine decarboxylase, glutamate receptor, and ammonia transporter. Our data demonstrate that XDH1 plays an essential role and that XDH1 has the potential to be used as a metabolic target for Ae. aegypti vector control.—Isoe, J., Petchampai, N., Isoe, Y. E., Co, K., Mazzalupo, S., Scaraffia, P. Y. Xanthine dehydrogenase‐1 silencing in Aedes aegypti mosquitoes promotes a blood feeding–induced adulticidal activity. FASEB J. 31, 2276–2286 (2017). www.fasebj.org</description><subject>Aedes - enzymology</subject><subject>Aedes - genetics</subject><subject>Aedes aegypti</subject><subject>Alanine</subject><subject>Alanine transaminase</subject><subject>Allopurinol</subject><subject>Allopurinol - pharmacology</subject><subject>Ammonia</subject><subject>Animals</subject><subject>antioxidant genes</subject><subject>Aquatic insects</subject><subject>Blood</subject><subject>Blood meals</subject><subject>Catalase</subject><subject>Culicidae</subject><subject>Dehydrogenase</subject><subject>Dehydrogenases</subject><subject>Double-stranded RNA</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>Excretion</subject><subject>Fat body</subject><subject>Feeding</subject><subject>Female</subject><subject>Females</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Enzymologic - physiology</subject><subject>Gene Silencing</subject><subject>Glutamate-ammonia ligase</subject><subject>Glutamic acid receptors</subject><subject>Glutamine</subject><subject>Meals</subject><subject>metabolic target</subject><subject>Midgut</subject><subject>Mosquito Control</subject><subject>Mosquitoes</subject><subject>Nitrogen - metabolism</subject><subject>Ornithine</subject><subject>Ornithine decarboxylase</subject><subject>Ovaries</subject><subject>Oviposition</subject><subject>Oviposition - drug effects</subject><subject>Ovum</subject><subject>Reduction</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA-mediated interference</subject><subject>Sucrose</subject><subject>Sugar</subject><subject>Superoxide dismutase</subject><subject>Tissues</subject><subject>Transcription</subject><subject>Xanthine Dehydrogenase - classification</subject><subject>Xanthine Dehydrogenase - genetics</subject><subject>Xanthine Dehydrogenase - metabolism</subject><issn>0892-6638</issn><issn>1530-6860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkV1rFDEUhoModq1eeisBb7yZepLZZBIEoRbXDwpCVfAuZPOxm2Um2U5mqnPXnyD4D_tLzLK1Vi_0KnDOc56c5EXoMYEjApI_95sjCoQDIYKd3UEzwmqouOBwF81ASFpxXosD9CDnDQCQgt5HB1SQRs5pPUPfvug4rEN02Lr1ZPu0clFnd3X5neAcWhdNiCscIj521mWs3WraDgF3KZ-PYUiltO1Tl4ZdDy_blCz2ztkydHX5I0Q7GmextmM7BBOsbrE2Q7gIw_QQ3fO6ze7R9XmIPi9efzp5W51-ePPu5Pi0MgzgrGJgqeFcmFpY1oAwXpTlwWkAzxspGmq515x7aqTwNdTWLxn1zCw91R5sfYhe7r3bcdk5a1wcet2qbR863U8q6aD-7MSwVqt0odi8nnMmiuDZtaBP56PLg-pCNq5tdXRpzIpIQjiRlPH_o4JzLkFSKOjTv9BNGvtYfqIIRS2phGZ3d7WnTJ9y7p2_2ZuA2sWv_Eb9jr_wT24_9ob-lXcBXuyBryXb6d82tfj4ii7e39L_BJn4wLg</recordid><startdate>201706</startdate><enddate>201706</enddate><creator>Isoe, Jun</creator><creator>Petchampai, Natthida</creator><creator>Isoe, Yurika E.</creator><creator>Co, Katrina</creator><creator>Mazzalupo, Stacy</creator><creator>Scaraffia, Patricia Y.</creator><general>Federation of American Societies for Experimental Biology (FASEB)</general><general>Federation of American Societies for Experimental Biology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7SS</scope><scope>5PM</scope></search><sort><creationdate>201706</creationdate><title>Xanthine dehydrogenase‐1 silencing in Aedes aegypti mosquitoes promotes a blood feeding–induced adulticidal activity</title><author>Isoe, Jun ; 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We analyzed XDH1 and XDH2 gene expression by real‐time quantitative PCR in tissues from sugar‐ and blood‐fed females. Differential XDH1 and XDH2 gene expression was observed in tissues dissected throughout a time course. We next exposed females to blood meals supplemented with allopurinol, a well‐characterized XDH inhibitor. We also tested the effects of injecting double‐stranded RNA (dsRNA) against XDH1, XDH2, or both. Disruption of XDH by allopurinol or XDH1 by RNA interference significantly affected mosquito survival, causing a disruption in blood digestion, excretion, oviposition, and reproduction. XDH1‐deficient mosquitoes showed a persistence of serine proteases in the midgut at 48 h after blood feeding and a reduction in the uptake of vitellogenin by the ovaries. Surprisingly, analysis of the fat body from dsRNA‐XDH1‐injected mosquitoes fell into 2 groups: one group was characterized by a reduction of the XDH1 transcript, whereas the other group was characterized by an up‐regulation of several transcripts, including XDH1, glutamine synthetase, alanine aminotransferase, catalase, superoxide dismutase, ornithine decarboxylase, glutamate receptor, and ammonia transporter. Our data demonstrate that XDH1 plays an essential role and that XDH1 has the potential to be used as a metabolic target for Ae. aegypti vector control.—Isoe, J., Petchampai, N., Isoe, Y. E., Co, K., Mazzalupo, S., Scaraffia, P. Y. Xanthine dehydrogenase‐1 silencing in Aedes aegypti mosquitoes promotes a blood feeding–induced adulticidal activity. 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subjects Aedes - enzymology
Aedes - genetics
Aedes aegypti
Alanine
Alanine transaminase
Allopurinol
Allopurinol - pharmacology
Ammonia
Animals
antioxidant genes
Aquatic insects
Blood
Blood meals
Catalase
Culicidae
Dehydrogenase
Dehydrogenases
Double-stranded RNA
Enzyme Inhibitors - pharmacology
Excretion
Fat body
Feeding
Female
Females
Gene expression
Gene Expression Regulation, Enzymologic - physiology
Gene Silencing
Glutamate-ammonia ligase
Glutamic acid receptors
Glutamine
Meals
metabolic target
Midgut
Mosquito Control
Mosquitoes
Nitrogen - metabolism
Ornithine
Ornithine decarboxylase
Ovaries
Oviposition
Oviposition - drug effects
Ovum
Reduction
Ribonucleic acid
RNA
RNA-mediated interference
Sucrose
Sugar
Superoxide dismutase
Tissues
Transcription
Xanthine Dehydrogenase - classification
Xanthine Dehydrogenase - genetics
Xanthine Dehydrogenase - metabolism
title Xanthine dehydrogenase‐1 silencing in Aedes aegypti mosquitoes promotes a blood feeding–induced adulticidal activity
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