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Tre1, a G protein-coupled receptor, directs transepithelial migration of Drosophila germ cells
In most organisms, germ cells are formed distant from the somatic part of the gonad and thus have to migrate along and through a variety of tissues to reach the gonad. Transepithelial migration through the posterior midgut (PMG) is the first active step during Drosophila germ cell migration. Here we...
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Published in: | PLoS biology 2003-12, Vol.1 (3), p.E80-E80 |
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description | In most organisms, germ cells are formed distant from the somatic part of the gonad and thus have to migrate along and through a variety of tissues to reach the gonad. Transepithelial migration through the posterior midgut (PMG) is the first active step during Drosophila germ cell migration. Here we report the identification of a novel G protein-coupled receptor (GPCR), Tre1, that is essential for this migration step. Maternal tre1 RNA is localized to germ cells, and tre1 is required cell autonomously in germ cells. In tre1 mutant embryos, most germ cells do not exit the PMG. The few germ cells that do leave the midgut early migrate normally to the gonad, suggesting that this gene is specifically required for transepithelial migration and that mutant germ cells are still able to recognize other guidance cues. Additionally, inhibiting small Rho GTPases in germ cells affects transepithelial migration, suggesting that Tre1 signals through Rho1. We propose that Tre1 acts in a manner similar to chemokine receptors required during transepithelial migration of leukocytes, implying an evolutionarily conserved mechanism of transepithelial migration. Recently, the chemokine receptor CXCR4 was shown to direct migration in vertebrate germ cells. Thus, germ cells may more generally use GPCR signaling to navigate the embryo toward their target. |
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Transepithelial migration through the posterior midgut (PMG) is the first active step during Drosophila germ cell migration. Here we report the identification of a novel G protein-coupled receptor (GPCR), Tre1, that is essential for this migration step. Maternal tre1 RNA is localized to germ cells, and tre1 is required cell autonomously in germ cells. In tre1 mutant embryos, most germ cells do not exit the PMG. The few germ cells that do leave the midgut early migrate normally to the gonad, suggesting that this gene is specifically required for transepithelial migration and that mutant germ cells are still able to recognize other guidance cues. Additionally, inhibiting small Rho GTPases in germ cells affects transepithelial migration, suggesting that Tre1 signals through Rho1. We propose that Tre1 acts in a manner similar to chemokine receptors required during transepithelial migration of leukocytes, implying an evolutionarily conserved mechanism of transepithelial migration. Recently, the chemokine receptor CXCR4 was shown to direct migration in vertebrate germ cells. Thus, germ cells may more generally use GPCR signaling to navigate the embryo toward their target.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.0000080</identifier><identifier>PMID: 14691551</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Cell Biology ; Cell Movement ; Cell Transplantation ; Cloning, Molecular ; Crosses, Genetic ; Development ; Drosophila ; Drosophila melanogaster ; Drosophila Proteins - genetics ; Drosophila Proteins - physiology ; Embryo, Nonmammalian - metabolism ; Epithelium - pathology ; Evolution, Molecular ; Female ; Gene Expression Regulation ; Genetics ; Genetics/Genomics/Gene Therapy ; Germ Cells - cytology ; Humans ; Immunohistochemistry ; Immunology ; In Situ Hybridization ; Inflammation ; Insects ; Leukocytes - cytology ; Leukocytes - metabolism ; Male ; Models, Biological ; Molecular Sequence Data ; Mutation ; Phenotype ; Phylogeny ; Proteins ; Receptors, Chemokine - metabolism ; Receptors, G-Protein-Coupled - genetics ; Receptors, G-Protein-Coupled - metabolism ; Receptors, G-Protein-Coupled - physiology ; rho GTP-Binding Proteins - metabolism ; RNA - chemistry ; RNA - metabolism ; Rodents ; Signal Transduction ; Tre1 protein ; Zebrafish</subject><ispartof>PLoS biology, 2003-12, Vol.1 (3), p.E80-E80</ispartof><rights>2003 Kunwar 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 work is properly cited. Citation: Kunwar PS, Starz-Gaiano M, Bainton RJ, Heberlein U, Lehmann R (2003) Tre1, a G Protein-Coupled Receptor, Directs Transepithelial Migration of Drosophila Germ Cells. PLoS Biol 1(3): e80. doi:10.1371/journal.pbio.0000080</rights><rights>Copyright: © 2003 Kunwar 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 work is properly cited 2003</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c618t-59fedf83c471057f69450fa414ef095f7ca71357ae3443891b0345a2853b347b3</citedby><cites>FETCH-LOGICAL-c618t-59fedf83c471057f69450fa414ef095f7ca71357ae3443891b0345a2853b347b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1291063446/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1291063446?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/14691551$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Geraldine Seydoux</contributor><creatorcontrib>Kunwar, Prabhat S</creatorcontrib><creatorcontrib>Starz-Gaiano, Michelle</creatorcontrib><creatorcontrib>Bainton, Roland J</creatorcontrib><creatorcontrib>Heberlein, Ulrike</creatorcontrib><creatorcontrib>Lehmann, Ruth</creatorcontrib><title>Tre1, a G protein-coupled receptor, directs transepithelial migration of Drosophila germ cells</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>In most organisms, germ cells are formed distant from the somatic part of the gonad and thus have to migrate along and through a variety of tissues to reach the gonad. Transepithelial migration through the posterior midgut (PMG) is the first active step during Drosophila germ cell migration. Here we report the identification of a novel G protein-coupled receptor (GPCR), Tre1, that is essential for this migration step. Maternal tre1 RNA is localized to germ cells, and tre1 is required cell autonomously in germ cells. In tre1 mutant embryos, most germ cells do not exit the PMG. The few germ cells that do leave the midgut early migrate normally to the gonad, suggesting that this gene is specifically required for transepithelial migration and that mutant germ cells are still able to recognize other guidance cues. Additionally, inhibiting small Rho GTPases in germ cells affects transepithelial migration, suggesting that Tre1 signals through Rho1. We propose that Tre1 acts in a manner similar to chemokine receptors required during transepithelial migration of leukocytes, implying an evolutionarily conserved mechanism of transepithelial migration. Recently, the chemokine receptor CXCR4 was shown to direct migration in vertebrate germ cells. Thus, germ cells may more generally use GPCR signaling to navigate the embryo toward their target.</description><subject>Animals</subject><subject>Cell Biology</subject><subject>Cell Movement</subject><subject>Cell Transplantation</subject><subject>Cloning, Molecular</subject><subject>Crosses, Genetic</subject><subject>Development</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - physiology</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Epithelium - pathology</subject><subject>Evolution, Molecular</subject><subject>Female</subject><subject>Gene Expression Regulation</subject><subject>Genetics</subject><subject>Genetics/Genomics/Gene Therapy</subject><subject>Germ Cells - cytology</subject><subject>Humans</subject><subject>Immunohistochemistry</subject><subject>Immunology</subject><subject>In Situ Hybridization</subject><subject>Inflammation</subject><subject>Insects</subject><subject>Leukocytes - 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genetics</topic><topic>Drosophila Proteins - physiology</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Epithelium - pathology</topic><topic>Evolution, Molecular</topic><topic>Female</topic><topic>Gene Expression Regulation</topic><topic>Genetics</topic><topic>Genetics/Genomics/Gene Therapy</topic><topic>Germ Cells - cytology</topic><topic>Humans</topic><topic>Immunohistochemistry</topic><topic>Immunology</topic><topic>In Situ Hybridization</topic><topic>Inflammation</topic><topic>Insects</topic><topic>Leukocytes - cytology</topic><topic>Leukocytes - metabolism</topic><topic>Male</topic><topic>Models, Biological</topic><topic>Molecular Sequence Data</topic><topic>Mutation</topic><topic>Phenotype</topic><topic>Phylogeny</topic><topic>Proteins</topic><topic>Receptors, Chemokine - metabolism</topic><topic>Receptors, G-Protein-Coupled - genetics</topic><topic>Receptors, G-Protein-Coupled - metabolism</topic><topic>Receptors, G-Protein-Coupled - physiology</topic><topic>rho GTP-Binding Proteins - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kunwar, Prabhat S</au><au>Starz-Gaiano, Michelle</au><au>Bainton, Roland J</au><au>Heberlein, Ulrike</au><au>Lehmann, Ruth</au><au>Geraldine Seydoux</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tre1, a G protein-coupled receptor, directs transepithelial migration of Drosophila germ cells</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2003-12-01</date><risdate>2003</risdate><volume>1</volume><issue>3</issue><spage>E80</spage><epage>E80</epage><pages>E80-E80</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>In most organisms, germ cells are formed distant from the somatic part of the gonad and thus have to migrate along and through a variety of tissues to reach the gonad. Transepithelial migration through the posterior midgut (PMG) is the first active step during Drosophila germ cell migration. Here we report the identification of a novel G protein-coupled receptor (GPCR), Tre1, that is essential for this migration step. Maternal tre1 RNA is localized to germ cells, and tre1 is required cell autonomously in germ cells. In tre1 mutant embryos, most germ cells do not exit the PMG. The few germ cells that do leave the midgut early migrate normally to the gonad, suggesting that this gene is specifically required for transepithelial migration and that mutant germ cells are still able to recognize other guidance cues. Additionally, inhibiting small Rho GTPases in germ cells affects transepithelial migration, suggesting that Tre1 signals through Rho1. We propose that Tre1 acts in a manner similar to chemokine receptors required during transepithelial migration of leukocytes, implying an evolutionarily conserved mechanism of transepithelial migration. Recently, the chemokine receptor CXCR4 was shown to direct migration in vertebrate germ cells. Thus, germ cells may more generally use GPCR signaling to navigate the embryo toward their target.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>14691551</pmid><doi>10.1371/journal.pbio.0000080</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animals Cell Biology Cell Movement Cell Transplantation Cloning, Molecular Crosses, Genetic Development Drosophila Drosophila melanogaster Drosophila Proteins - genetics Drosophila Proteins - physiology Embryo, Nonmammalian - metabolism Epithelium - pathology Evolution, Molecular Female Gene Expression Regulation Genetics Genetics/Genomics/Gene Therapy Germ Cells - cytology Humans Immunohistochemistry Immunology In Situ Hybridization Inflammation Insects Leukocytes - cytology Leukocytes - metabolism Male Models, Biological Molecular Sequence Data Mutation Phenotype Phylogeny Proteins Receptors, Chemokine - metabolism Receptors, G-Protein-Coupled - genetics Receptors, G-Protein-Coupled - metabolism Receptors, G-Protein-Coupled - physiology rho GTP-Binding Proteins - metabolism RNA - chemistry RNA - metabolism Rodents Signal Transduction Tre1 protein Zebrafish |
title | Tre1, a G protein-coupled receptor, directs transepithelial migration of Drosophila germ cells |
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