Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female
In Drosophila, the accessory gland proteins (Acps) secreted from the male accessory glands (MAGs) and transferred along with sperm into the female reproductive tract have been implicated in triggering postmating behavioral changes, including refractoriness to subsequent mating and propensity to egg...
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description | In Drosophila, the accessory gland proteins (Acps) secreted from the male accessory glands (MAGs) and transferred along with sperm into the female reproductive tract have been implicated in triggering postmating behavioral changes, including refractoriness to subsequent mating and propensity to egg laying. Recently, Acps have been found also in Anopheles, suggesting similar functions. Understanding the mechanisms underlying transcriptional regulation of Acps and their functional role in modulating Anopheles postmating behavior may lead to the identification of novel vector control strategies to reduce mosquito populations. We identified heat‐shock factor (HSF) binding sites within the Acp promoters of male Anopheles gambiae and discovered three distinct Hsf isoforms; one being significantly up‐regulated in the MAGs after mating. Through genome‐wide transcription analysis of Hsf‐silenced males, we observed significant down‐regulation in 50% of the Acp genes if compared to control males treated with a construct directed against an unrelated bacterial sequence. Treated males retained normal life span and reproductive behavior compared to control males. However, mated wild‐type females showed a ~46% reduction of egg deposition rate and a ~23% reduction of hatching rate (~58% combined reduction of progeny). Our results highlight an unsuspected role of HSF in regulating Acp transcription in A. gambiae and provide evidence that Acp down‐regulation in males leads a significant reduction of progeny, thus opening new avenues toward the development of novel vector control strategies.—Dottorini, T., Persampieri, T., Palladino, P., Baker, D. A., Spaccapelo, R., Senin, N., Crisanti, A. Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female. FASEB J. 27, 86–97 (2013). www.fasebj.org |
doi_str_mv | 10.1096/fj.12-219444 |
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Recently, Acps have been found also in Anopheles, suggesting similar functions. Understanding the mechanisms underlying transcriptional regulation of Acps and their functional role in modulating Anopheles postmating behavior may lead to the identification of novel vector control strategies to reduce mosquito populations. We identified heat‐shock factor (HSF) binding sites within the Acp promoters of male Anopheles gambiae and discovered three distinct Hsf isoforms; one being significantly up‐regulated in the MAGs after mating. Through genome‐wide transcription analysis of Hsf‐silenced males, we observed significant down‐regulation in 50% of the Acp genes if compared to control males treated with a construct directed against an unrelated bacterial sequence. Treated males retained normal life span and reproductive behavior compared to control males. However, mated wild‐type females showed a ~46% reduction of egg deposition rate and a ~23% reduction of hatching rate (~58% combined reduction of progeny). Our results highlight an unsuspected role of HSF in regulating Acp transcription in A. gambiae and provide evidence that Acp down‐regulation in males leads a significant reduction of progeny, thus opening new avenues toward the development of novel vector control strategies.—Dottorini, T., Persampieri, T., Palladino, P., Baker, D. A., Spaccapelo, R., Senin, N., Crisanti, A. Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female. 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Recently, Acps have been found also in Anopheles, suggesting similar functions. Understanding the mechanisms underlying transcriptional regulation of Acps and their functional role in modulating Anopheles postmating behavior may lead to the identification of novel vector control strategies to reduce mosquito populations. We identified heat‐shock factor (HSF) binding sites within the Acp promoters of male Anopheles gambiae and discovered three distinct Hsf isoforms; one being significantly up‐regulated in the MAGs after mating. Through genome‐wide transcription analysis of Hsf‐silenced males, we observed significant down‐regulation in 50% of the Acp genes if compared to control males treated with a construct directed against an unrelated bacterial sequence. Treated males retained normal life span and reproductive behavior compared to control males. However, mated wild‐type females showed a ~46% reduction of egg deposition rate and a ~23% reduction of hatching rate (~58% combined reduction of progeny). Our results highlight an unsuspected role of HSF in regulating Acp transcription in A. gambiae and provide evidence that Acp down‐regulation in males leads a significant reduction of progeny, thus opening new avenues toward the development of novel vector control strategies.—Dottorini, T., Persampieri, T., Palladino, P., Baker, D. A., Spaccapelo, R., Senin, N., Crisanti, A. Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female. FASEB J. 27, 86–97 (2013). www.fasebj.org</description><subject>Animals</subject><subject>Anopheles - genetics</subject><subject>Anopheles gambiae</subject><subject>Base Sequence</subject><subject>DNA Primers</subject><subject>Drosophila</subject><subject>Female</subject><subject>fertility</subject><subject>Genitalia, Male - metabolism</subject><subject>heat‐shock factor</subject><subject>malaria</subject><subject>Male</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Polymerase Chain Reaction</subject><subject>reproductive biology</subject><subject>RNA Interference</subject><subject>Sexual Behavior, Animal</subject><subject>Transcription, Genetic</subject><subject>vector control</subject><issn>0892-6638</issn><issn>1530-6860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkbtOxDAQRS0EguXRUSOXFGTxO3G5IBaQkJB41JHjjENWSRzijdD-PV4ClFBNcc8cjeYidErJnBKtLt1qTlnCqBZC7KAZlZwkKlNkF81IplmiFM8O0GEIK0IIJVTtowPGtE4ZUzNkn6AaG7OufYe9w4vO92_QQMCVaYvaAG5NA9hYCyH4YYOrxnQlrqCLSN25ZoQuRrj3Yd1GS1fhAULvuwAxxg6268doz5kmwMn3PEKvy5uX67vk4fH2_nrxkFieMpI4yQyVwljFXEFtJhwtMlkUoDkvZUoBuLOR0aU0IAqmVaq4SYuSiBKc5PwInU_efvDvI4R13tbBQhNPBj-GnEqlMqEF1_-jLOVUSqm21osJtYMPYQCX90PdmmGTU5JvG8jdKvL51EDEz77NY9FC-Qv_vDwC6QR81A1s_pTly-crRlj61Rvhn_PzknI</recordid><startdate>201301</startdate><enddate>201301</enddate><creator>Dottorini, Tania</creator><creator>Persampieri, Tania</creator><creator>Palladino, Pietro</creator><creator>Baker, Dean A.</creator><creator>Spaccapelo, Roberta</creator><creator>Senin, Nicola</creator><creator>Crisanti, Andrea</creator><general>The 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>7X8</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>201301</creationdate><title>Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female</title><author>Dottorini, Tania ; Persampieri, Tania ; Palladino, Pietro ; Baker, Dean A. ; Spaccapelo, Roberta ; Senin, Nicola ; Crisanti, Andrea</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3720-f52a154ac62fb1c84f1b85bbe933d571ee3fc52a9d5ae4b296763a7bd04def533</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Anopheles - genetics</topic><topic>Anopheles gambiae</topic><topic>Base Sequence</topic><topic>DNA Primers</topic><topic>Drosophila</topic><topic>Female</topic><topic>fertility</topic><topic>Genitalia, Male - metabolism</topic><topic>heat‐shock factor</topic><topic>malaria</topic><topic>Male</topic><topic>Oligonucleotide Array Sequence Analysis</topic><topic>Polymerase Chain Reaction</topic><topic>reproductive biology</topic><topic>RNA Interference</topic><topic>Sexual Behavior, Animal</topic><topic>Transcription, Genetic</topic><topic>vector control</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dottorini, Tania</creatorcontrib><creatorcontrib>Persampieri, Tania</creatorcontrib><creatorcontrib>Palladino, Pietro</creatorcontrib><creatorcontrib>Baker, Dean A.</creatorcontrib><creatorcontrib>Spaccapelo, Roberta</creatorcontrib><creatorcontrib>Senin, Nicola</creatorcontrib><creatorcontrib>Crisanti, Andrea</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>The FASEB journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dottorini, Tania</au><au>Persampieri, Tania</au><au>Palladino, Pietro</au><au>Baker, Dean A.</au><au>Spaccapelo, Roberta</au><au>Senin, Nicola</au><au>Crisanti, Andrea</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female</atitle><jtitle>The FASEB journal</jtitle><addtitle>FASEB J</addtitle><date>2013-01</date><risdate>2013</risdate><volume>27</volume><issue>1</issue><spage>86</spage><epage>97</epage><pages>86-97</pages><issn>0892-6638</issn><eissn>1530-6860</eissn><abstract>In Drosophila, the accessory gland proteins (Acps) secreted from the male accessory glands (MAGs) and transferred along with sperm into the female reproductive tract have been implicated in triggering postmating behavioral changes, including refractoriness to subsequent mating and propensity to egg laying. Recently, Acps have been found also in Anopheles, suggesting similar functions. Understanding the mechanisms underlying transcriptional regulation of Acps and their functional role in modulating Anopheles postmating behavior may lead to the identification of novel vector control strategies to reduce mosquito populations. We identified heat‐shock factor (HSF) binding sites within the Acp promoters of male Anopheles gambiae and discovered three distinct Hsf isoforms; one being significantly up‐regulated in the MAGs after mating. Through genome‐wide transcription analysis of Hsf‐silenced males, we observed significant down‐regulation in 50% of the Acp genes if compared to control males treated with a construct directed against an unrelated bacterial sequence. Treated males retained normal life span and reproductive behavior compared to control males. However, mated wild‐type females showed a ~46% reduction of egg deposition rate and a ~23% reduction of hatching rate (~58% combined reduction of progeny). Our results highlight an unsuspected role of HSF in regulating Acp transcription in A. gambiae and provide evidence that Acp down‐regulation in males leads a significant reduction of progeny, thus opening new avenues toward the development of novel vector control strategies.—Dottorini, T., Persampieri, T., Palladino, P., Baker, D. A., Spaccapelo, R., Senin, N., Crisanti, A. Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female. FASEB J. 27, 86–97 (2013). www.fasebj.org</abstract><cop>United States</cop><pub>The Federation of American Societies for Experimental Biology</pub><pmid>22997226</pmid><doi>10.1096/fj.12-219444</doi><tpages>12</tpages></addata></record> |
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subjects | Animals Anopheles - genetics Anopheles gambiae Base Sequence DNA Primers Drosophila Female fertility Genitalia, Male - metabolism heat‐shock factor malaria Male Oligonucleotide Array Sequence Analysis Polymerase Chain Reaction reproductive biology RNA Interference Sexual Behavior, Animal Transcription, Genetic vector control |
title | Regulation of Anopheles gambiae male accessory gland genes influences postmating response in female |
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