insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti
Ingestion of vertebrate blood is essential for egg maturation and transmission of disease-causing parasites by female mosquitoes. Prior studies with the yellow fever mosquito, Aedes aegypti, indicated blood feeding stimulates egg production by triggering the release of hormones from medial neurosecr...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2008-04, Vol.105 (15), p.5716-5721 |
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creator | Brown, Mark R Clark, Kevin D Gulia, Monika Zhao, Zhangwu Garczynski, Stephen F Crim, Joe W Suderman, Richard J Strand, Michael R |
description | Ingestion of vertebrate blood is essential for egg maturation and transmission of disease-causing parasites by female mosquitoes. Prior studies with the yellow fever mosquito, Aedes aegypti, indicated blood feeding stimulates egg production by triggering the release of hormones from medial neurosecretory cells in the mosquito brain. The ability of bovine insulin to stimulate a similar response further suggested this trigger is an endogenous insulin-like peptide (ILP). A. aegypti encodes eight predicted ILPs. Here, we report that synthetic ILP3 dose-dependently stimulated yolk uptake by oocytes and ecdysteroid production by the ovaries at lower concentrations than bovine insulin. ILP3 also exhibited metabolic activity by elevating carbohydrate and lipid storage. Binding studies using ovary membranes indicated that ILP3 had an IC₅₀ value of 5.9 nM that was poorly competed by bovine insulin. Autoradiography and immunoblotting studies suggested that ILP3 binds the mosquito insulin receptor (MIR), whereas loss-of-function experiments showed that ILP3 activity requires MIR expression. Overall, our results identify ILP3 as a critical regulator of egg production by A. aegypti. |
doi_str_mv | 10.1073/pnas.0800478105 |
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Prior studies with the yellow fever mosquito, Aedes aegypti, indicated blood feeding stimulates egg production by triggering the release of hormones from medial neurosecretory cells in the mosquito brain. The ability of bovine insulin to stimulate a similar response further suggested this trigger is an endogenous insulin-like peptide (ILP). A. aegypti encodes eight predicted ILPs. Here, we report that synthetic ILP3 dose-dependently stimulated yolk uptake by oocytes and ecdysteroid production by the ovaries at lower concentrations than bovine insulin. ILP3 also exhibited metabolic activity by elevating carbohydrate and lipid storage. Binding studies using ovary membranes indicated that ILP3 had an IC₅₀ value of 5.9 nM that was poorly competed by bovine insulin. Autoradiography and immunoblotting studies suggested that ILP3 binds the mosquito insulin receptor (MIR), whereas loss-of-function experiments showed that ILP3 activity requires MIR expression. Overall, our results identify ILP3 as a critical regulator of egg production by A. aegypti.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0800478105</identifier><identifier>PMID: 18391205</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Aedes - metabolism ; Aedes - physiology ; Aedes aegypti ; Animals ; binding capacity ; Biological Sciences ; biosynthesis ; Blood - metabolism ; carbohydrate metabolism ; Cattle ; Ecdysteroids ; egg yolk ; Eggs ; Female ; Female animals ; hormone receptors ; insect hormones ; Insect Hormones - physiology ; Insect Proteins ; Insect reproduction ; Insulin ; insulin-like peptides ; lipid metabolism ; Metabolism ; Molecular Sequence Data ; Mosquitoes ; Mosquitos ; Oocytes ; oogenesis ; Ovaries ; Ovum - metabolism ; Ovum - physiology ; Parasites ; Peptide Hormones - physiology ; Peptides ; Receptor, Insulin - metabolism ; Receptors ; Reproduction ; Ungulates</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2008-04, Vol.105 (15), p.5716-5721</ispartof><rights>Copyright 2008 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Apr 15, 2008</rights><rights>2008 by The National Academy of Sciences of the USA</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c583t-38171cb522ab390ca3f0f9794b30bb97d93220bd1b46ff24a16210057219936a3</citedby><cites>FETCH-LOGICAL-c583t-38171cb522ab390ca3f0f9794b30bb97d93220bd1b46ff24a16210057219936a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/105/15.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25461675$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25461675$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18391205$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Brown, Mark R</creatorcontrib><creatorcontrib>Clark, Kevin D</creatorcontrib><creatorcontrib>Gulia, Monika</creatorcontrib><creatorcontrib>Zhao, Zhangwu</creatorcontrib><creatorcontrib>Garczynski, Stephen F</creatorcontrib><creatorcontrib>Crim, Joe W</creatorcontrib><creatorcontrib>Suderman, Richard J</creatorcontrib><creatorcontrib>Strand, Michael R</creatorcontrib><title>insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Ingestion of vertebrate blood is essential for egg maturation and transmission of disease-causing parasites by female mosquitoes. Prior studies with the yellow fever mosquito, Aedes aegypti, indicated blood feeding stimulates egg production by triggering the release of hormones from medial neurosecretory cells in the mosquito brain. The ability of bovine insulin to stimulate a similar response further suggested this trigger is an endogenous insulin-like peptide (ILP). A. aegypti encodes eight predicted ILPs. Here, we report that synthetic ILP3 dose-dependently stimulated yolk uptake by oocytes and ecdysteroid production by the ovaries at lower concentrations than bovine insulin. ILP3 also exhibited metabolic activity by elevating carbohydrate and lipid storage. Binding studies using ovary membranes indicated that ILP3 had an IC₅₀ value of 5.9 nM that was poorly competed by bovine insulin. Autoradiography and immunoblotting studies suggested that ILP3 binds the mosquito insulin receptor (MIR), whereas loss-of-function experiments showed that ILP3 activity requires MIR expression. Overall, our results identify ILP3 as a critical regulator of egg production by A. aegypti.</description><subject>Aedes - metabolism</subject><subject>Aedes - physiology</subject><subject>Aedes aegypti</subject><subject>Animals</subject><subject>binding capacity</subject><subject>Biological Sciences</subject><subject>biosynthesis</subject><subject>Blood - metabolism</subject><subject>carbohydrate metabolism</subject><subject>Cattle</subject><subject>Ecdysteroids</subject><subject>egg yolk</subject><subject>Eggs</subject><subject>Female</subject><subject>Female animals</subject><subject>hormone receptors</subject><subject>insect hormones</subject><subject>Insect Hormones - physiology</subject><subject>Insect Proteins</subject><subject>Insect reproduction</subject><subject>Insulin</subject><subject>insulin-like peptides</subject><subject>lipid metabolism</subject><subject>Metabolism</subject><subject>Molecular Sequence Data</subject><subject>Mosquitoes</subject><subject>Mosquitos</subject><subject>Oocytes</subject><subject>oogenesis</subject><subject>Ovaries</subject><subject>Ovum - metabolism</subject><subject>Ovum - physiology</subject><subject>Parasites</subject><subject>Peptide Hormones - physiology</subject><subject>Peptides</subject><subject>Receptor, Insulin - metabolism</subject><subject>Receptors</subject><subject>Reproduction</subject><subject>Ungulates</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqF0r9v1DAUB_AIgehRmJkAiwGxpH3PjmN7qVRV_JIqMUAXFstJnNRHEl9tB9H_Hp_u1CsMdPLgz_ta7_kVxUuEEwTBTjeziScgASohEfijYoWgsKwrBY-LFQAVpaxodVQ8i3ENAIpLeFocoWQKKfBV8cPNcRndXI7upyUbu0musyTYYRlNspHYYSCTSUswyfmZmLkjk02m8aOLE3EzSdeWTD7eLC55cm67XGPscJtznhdPejNG-2J_HhdXHz98v_hcXn799OXi_LJsuWSpZBIFtg2n1DRMQWtYD70SqmoYNI0SnWKUQtNhU9V9TyuDNUUALigqxWrDjouzXe5maSbbtXZOwYx6E9xkwq32xum_b2Z3rQf_S1OGyITMAe_2AcHfLDYmPbnY2nE0s_VL1LXKQ81DfhBWouaAXD0IcwNUIIoM3_4D134Jcx6XpoCMAq0wo9MdaoOPMdj-rjcEvV0DvV0DfViDXPH6_kgOfv_vGbzZg23lIY5r5JoLrLN4_3-h-2Uck_2dMn21o-uYfLizlFc11uLeY73x2gzBRX31bdsegJQ1Ssr-ACFk2M8</recordid><startdate>20080415</startdate><enddate>20080415</enddate><creator>Brown, Mark R</creator><creator>Clark, Kevin D</creator><creator>Gulia, Monika</creator><creator>Zhao, Zhangwu</creator><creator>Garczynski, Stephen F</creator><creator>Crim, Joe W</creator><creator>Suderman, Richard J</creator><creator>Strand, Michael R</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><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>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</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>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>7S9</scope><scope>L.6</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20080415</creationdate><title>insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti</title><author>Brown, Mark R ; 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Prior studies with the yellow fever mosquito, Aedes aegypti, indicated blood feeding stimulates egg production by triggering the release of hormones from medial neurosecretory cells in the mosquito brain. The ability of bovine insulin to stimulate a similar response further suggested this trigger is an endogenous insulin-like peptide (ILP). A. aegypti encodes eight predicted ILPs. Here, we report that synthetic ILP3 dose-dependently stimulated yolk uptake by oocytes and ecdysteroid production by the ovaries at lower concentrations than bovine insulin. ILP3 also exhibited metabolic activity by elevating carbohydrate and lipid storage. Binding studies using ovary membranes indicated that ILP3 had an IC₅₀ value of 5.9 nM that was poorly competed by bovine insulin. Autoradiography and immunoblotting studies suggested that ILP3 binds the mosquito insulin receptor (MIR), whereas loss-of-function experiments showed that ILP3 activity requires MIR expression. Overall, our results identify ILP3 as a critical regulator of egg production by A. aegypti.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>18391205</pmid><doi>10.1073/pnas.0800478105</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Aedes - metabolism Aedes - physiology Aedes aegypti Animals binding capacity Biological Sciences biosynthesis Blood - metabolism carbohydrate metabolism Cattle Ecdysteroids egg yolk Eggs Female Female animals hormone receptors insect hormones Insect Hormones - physiology Insect Proteins Insect reproduction Insulin insulin-like peptides lipid metabolism Metabolism Molecular Sequence Data Mosquitoes Mosquitos Oocytes oogenesis Ovaries Ovum - metabolism Ovum - physiology Parasites Peptide Hormones - physiology Peptides Receptor, Insulin - metabolism Receptors Reproduction Ungulates |
title | insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti |
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