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The insulator protein Suppressor of Hairy wing is required for proper ring canal development during oogenesis in Drosophila
Chromatin insulators orchestrate gene transcription during embryo development and cell differentiation by stabilizing interactions between distant genomic sites. Mutations in genes encoding insulator proteins are generally lethal, making in vivo functional analyses of insulator proteins difficult. I...
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| Published in: | Developmental biology 2015-07, Vol.403 (1), p.57-68 |
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| creator | Hsu, Shih-Jui Plata, Maria P. Ernest, Ben Asgarifar, Saghi Labrador, Mariano |
| description | Chromatin insulators orchestrate gene transcription during embryo development and cell differentiation by stabilizing interactions between distant genomic sites. Mutations in genes encoding insulator proteins are generally lethal, making in vivo functional analyses of insulator proteins difficult. In Drosophila, however, mutations in the gene encoding the Suppressor of Hairy wing insulator protein [Su(Hw)] are viable and female sterile, providing an opportunity to study insulator function during oocyte development. Whereas previous reports suggest that the function of Su(Hw) in oogenesis is independent of its insulator activity, many aspects of the role of Su(Hw) in Drosophila oogenesis remain unexplored. Here we show that mutations in su(Hw) result in smaller ring canal lumens and smaller outer ring diameters, which likely obstruct molecular and vesicle passage from nurse cells to the oocyte. Fluorescence microscopy reveals that lack of Su(Hw) leads to excess accumulation of Kelch (Kel) and Filament-actin (F-actin) proteins in the ring canal structures of developing egg chambers. Furthermore, we found that misexpression of the Src oncogene at 64B (Src64B) may cause ring canal development defects as microarray analysis and real-time RT-PCR revealed there is a three fold decrease in Src64B expression in su(Hw) mutant ovaries. Restoration of Src64B expression in su(Hw) mutant female germ cells rescued the ring phenotype but did not restore fertility. We conclude that loss of su(Hw) affects expression of many oogenesis related genes and down-regulates Src64B, resulting in ring canal defects potentially contributing to obstruction of molecular flow and an eventual failure of egg chamber organization.
•Drosophila su (Hw) female mutants lack molecular flow from nurse cells to oocyte.•Ring canals in su(Hw) mutant egg chambers are smaller and have narrow lumens.•Ring canals in su(Hw) mutants have excess accumulation of Kelch, Hts and F-actin.•Src64B expression is reduced three-fold in su(Hw) mutant ovaries.•Restoration of Src64B expression alone rescues the ring phenotype but not fertility. |
| doi_str_mv | 10.1016/j.ydbio.2015.03.024 |
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•Drosophila su (Hw) female mutants lack molecular flow from nurse cells to oocyte.•Ring canals in su(Hw) mutant egg chambers are smaller and have narrow lumens.•Ring canals in su(Hw) mutants have excess accumulation of Kelch, Hts and F-actin.•Src64B expression is reduced three-fold in su(Hw) mutant ovaries.•Restoration of Src64B expression alone rescues the ring phenotype but not fertility.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2015.03.024</identifier><identifier>PMID: 25882370</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Actins - metabolism ; Animals ; Cell Differentiation ; Chromatin insulators ; Drosophila ; Drosophila melanogaster - embryology ; Drosophila Proteins - biosynthesis ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Female ; Gene Expression Regulation, Developmental - genetics ; Insulator Elements - genetics ; Microfilament Proteins - metabolism ; Oogenesis ; Oogenesis - genetics ; Ovary - embryology ; Protein-Tyrosine Kinases - biosynthesis ; Proto-Oncogene Proteins - biosynthesis ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; Ring canals ; Src64b ; Su(Hw) ; Suppressor of Hairy wing</subject><ispartof>Developmental biology, 2015-07, Vol.403 (1), p.57-68</ispartof><rights>2015 Elsevier Inc.</rights><rights>Copyright © 2015 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c529t-75d2eb250e654d41a3a0e0b22de5b2152ce7e847d40a3ce09ef4e895291f43823</citedby><cites>FETCH-LOGICAL-c529t-75d2eb250e654d41a3a0e0b22de5b2152ce7e847d40a3ce09ef4e895291f43823</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25882370$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hsu, Shih-Jui</creatorcontrib><creatorcontrib>Plata, Maria P.</creatorcontrib><creatorcontrib>Ernest, Ben</creatorcontrib><creatorcontrib>Asgarifar, Saghi</creatorcontrib><creatorcontrib>Labrador, Mariano</creatorcontrib><title>The insulator protein Suppressor of Hairy wing is required for proper ring canal development during oogenesis in Drosophila</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><description>Chromatin insulators orchestrate gene transcription during embryo development and cell differentiation by stabilizing interactions between distant genomic sites. Mutations in genes encoding insulator proteins are generally lethal, making in vivo functional analyses of insulator proteins difficult. In Drosophila, however, mutations in the gene encoding the Suppressor of Hairy wing insulator protein [Su(Hw)] are viable and female sterile, providing an opportunity to study insulator function during oocyte development. Whereas previous reports suggest that the function of Su(Hw) in oogenesis is independent of its insulator activity, many aspects of the role of Su(Hw) in Drosophila oogenesis remain unexplored. Here we show that mutations in su(Hw) result in smaller ring canal lumens and smaller outer ring diameters, which likely obstruct molecular and vesicle passage from nurse cells to the oocyte. Fluorescence microscopy reveals that lack of Su(Hw) leads to excess accumulation of Kelch (Kel) and Filament-actin (F-actin) proteins in the ring canal structures of developing egg chambers. Furthermore, we found that misexpression of the Src oncogene at 64B (Src64B) may cause ring canal development defects as microarray analysis and real-time RT-PCR revealed there is a three fold decrease in Src64B expression in su(Hw) mutant ovaries. Restoration of Src64B expression in su(Hw) mutant female germ cells rescued the ring phenotype but did not restore fertility. We conclude that loss of su(Hw) affects expression of many oogenesis related genes and down-regulates Src64B, resulting in ring canal defects potentially contributing to obstruction of molecular flow and an eventual failure of egg chamber organization.
•Drosophila su (Hw) female mutants lack molecular flow from nurse cells to oocyte.•Ring canals in su(Hw) mutant egg chambers are smaller and have narrow lumens.•Ring canals in su(Hw) mutants have excess accumulation of Kelch, Hts and F-actin.•Src64B expression is reduced three-fold in su(Hw) mutant ovaries.•Restoration of Src64B expression alone rescues the ring phenotype but not fertility.</description><subject>Actins - metabolism</subject><subject>Animals</subject><subject>Cell Differentiation</subject><subject>Chromatin insulators</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - embryology</subject><subject>Drosophila Proteins - biosynthesis</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Female</subject><subject>Gene Expression Regulation, Developmental - genetics</subject><subject>Insulator Elements - genetics</subject><subject>Microfilament Proteins - metabolism</subject><subject>Oogenesis</subject><subject>Oogenesis - genetics</subject><subject>Ovary - embryology</subject><subject>Protein-Tyrosine Kinases - biosynthesis</subject><subject>Proto-Oncogene Proteins - biosynthesis</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>Ring canals</subject><subject>Src64b</subject><subject>Su(Hw)</subject><subject>Suppressor of Hairy wing</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNp9UUtv1DAQthAVXQq_AAn5yCVh_MomB5BQaSlSpR4oEjfLsSe7XmXj1E4Wrfrn6-2WCi6cLPl7zcxHyDsGJQNWfdyUe9f6UHJgqgRRApcvyIJBowpVyV8vyQKA8YJVUJ2S1yltAEDUtXhFTrmqay6WsCD3t2ukfkhzb6YQ6RjDhH6gP-ZxjJhS_godvTI-7ulvP6yoTzTi3ewjOtodBSNGGg-YNYPpqcMd9mHc4jBRNz8CIaxwwJS12fprDCmMa9-bN-SkM33Ct0_vGfl5eXF7flVc33z7fv7lurCKN1OxVI5jyxVgpaSTzAgDCC3nDlXLmeIWl1jLpZNghEVosJNYN1nLOinynmfk89F3nNstOpsni6bXY_RbE_c6GK__RQa_1quw07KpmaxZNvjwZBDD3Yxp0lufLPa9GTDMSbOqbgTjIA5Z4ki1ec0UsXuOYaAPtemNfqxNH2rTIHSuLave_z3hs-ZPT5nw6UjAfKedx6iT9ThYdLkJO2kX_H8DHgB_b63w</recordid><startdate>20150701</startdate><enddate>20150701</enddate><creator>Hsu, Shih-Jui</creator><creator>Plata, Maria P.</creator><creator>Ernest, Ben</creator><creator>Asgarifar, Saghi</creator><creator>Labrador, Mariano</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20150701</creationdate><title>The insulator protein Suppressor of Hairy wing is required for proper ring canal development during oogenesis in Drosophila</title><author>Hsu, Shih-Jui ; Plata, Maria P. ; Ernest, Ben ; Asgarifar, Saghi ; Labrador, Mariano</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c529t-75d2eb250e654d41a3a0e0b22de5b2152ce7e847d40a3ce09ef4e895291f43823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Actins - metabolism</topic><topic>Animals</topic><topic>Cell Differentiation</topic><topic>Chromatin insulators</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - embryology</topic><topic>Drosophila Proteins - biosynthesis</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>Female</topic><topic>Gene Expression Regulation, Developmental - genetics</topic><topic>Insulator Elements - genetics</topic><topic>Microfilament Proteins - metabolism</topic><topic>Oogenesis</topic><topic>Oogenesis - genetics</topic><topic>Ovary - embryology</topic><topic>Protein-Tyrosine Kinases - biosynthesis</topic><topic>Proto-Oncogene Proteins - biosynthesis</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>Ring canals</topic><topic>Src64b</topic><topic>Su(Hw)</topic><topic>Suppressor of Hairy wing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hsu, Shih-Jui</creatorcontrib><creatorcontrib>Plata, Maria P.</creatorcontrib><creatorcontrib>Ernest, Ben</creatorcontrib><creatorcontrib>Asgarifar, Saghi</creatorcontrib><creatorcontrib>Labrador, Mariano</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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>PubMed Central (Full Participant titles)</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hsu, Shih-Jui</au><au>Plata, Maria P.</au><au>Ernest, Ben</au><au>Asgarifar, Saghi</au><au>Labrador, Mariano</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The insulator protein Suppressor of Hairy wing is required for proper ring canal development during oogenesis in Drosophila</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2015-07-01</date><risdate>2015</risdate><volume>403</volume><issue>1</issue><spage>57</spage><epage>68</epage><pages>57-68</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Present address: Department of Cancer biology, University of Cincinnati, Cincinnati, OH 45267</notes><abstract>Chromatin insulators orchestrate gene transcription during embryo development and cell differentiation by stabilizing interactions between distant genomic sites. Mutations in genes encoding insulator proteins are generally lethal, making in vivo functional analyses of insulator proteins difficult. In Drosophila, however, mutations in the gene encoding the Suppressor of Hairy wing insulator protein [Su(Hw)] are viable and female sterile, providing an opportunity to study insulator function during oocyte development. Whereas previous reports suggest that the function of Su(Hw) in oogenesis is independent of its insulator activity, many aspects of the role of Su(Hw) in Drosophila oogenesis remain unexplored. Here we show that mutations in su(Hw) result in smaller ring canal lumens and smaller outer ring diameters, which likely obstruct molecular and vesicle passage from nurse cells to the oocyte. Fluorescence microscopy reveals that lack of Su(Hw) leads to excess accumulation of Kelch (Kel) and Filament-actin (F-actin) proteins in the ring canal structures of developing egg chambers. Furthermore, we found that misexpression of the Src oncogene at 64B (Src64B) may cause ring canal development defects as microarray analysis and real-time RT-PCR revealed there is a three fold decrease in Src64B expression in su(Hw) mutant ovaries. Restoration of Src64B expression in su(Hw) mutant female germ cells rescued the ring phenotype but did not restore fertility. We conclude that loss of su(Hw) affects expression of many oogenesis related genes and down-regulates Src64B, resulting in ring canal defects potentially contributing to obstruction of molecular flow and an eventual failure of egg chamber organization.
•Drosophila su (Hw) female mutants lack molecular flow from nurse cells to oocyte.•Ring canals in su(Hw) mutant egg chambers are smaller and have narrow lumens.•Ring canals in su(Hw) mutants have excess accumulation of Kelch, Hts and F-actin.•Src64B expression is reduced three-fold in su(Hw) mutant ovaries.•Restoration of Src64B expression alone rescues the ring phenotype but not fertility.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25882370</pmid><doi>10.1016/j.ydbio.2015.03.024</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Actins - metabolism Animals Cell Differentiation Chromatin insulators Drosophila Drosophila melanogaster - embryology Drosophila Proteins - biosynthesis Drosophila Proteins - genetics Drosophila Proteins - metabolism Female Gene Expression Regulation, Developmental - genetics Insulator Elements - genetics Microfilament Proteins - metabolism Oogenesis Oogenesis - genetics Ovary - embryology Protein-Tyrosine Kinases - biosynthesis Proto-Oncogene Proteins - biosynthesis Repressor Proteins - genetics Repressor Proteins - metabolism Ring canals Src64b Su(Hw) Suppressor of Hairy wing |
| title | The insulator protein Suppressor of Hairy wing is required for proper ring canal development during oogenesis in Drosophila |
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