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Role of tbc1 in Drosophila embryonic salivary glands
CG4552/tbc1 was identified as a downstream target of Fork head (Fkh), the single Drosophila member of the FoxA family of transcription factors and a major player in salivary gland formation and homeostasis. Tbc1 and its orthologues have been implicated in phagocytosis, the innate immune response, bo...
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Published in: | BMC cell biology 2019-06, Vol.20 (1), p.19-19, Article 19 |
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description | CG4552/tbc1 was identified as a downstream target of Fork head (Fkh), the single Drosophila member of the FoxA family of transcription factors and a major player in salivary gland formation and homeostasis. Tbc1 and its orthologues have been implicated in phagocytosis, the innate immune response, border cell migration, cancer and an autosomal recessive form of non-degenerative Pontocerebellar hypoplasia. Recently, the mammalian Tbc1 orthologue, Tbc1d23, has been shown to bind both the conserved N-terminal domains of two Golgins (Golgin-97 and Golgin-245) and the WASH complex on endosome vesicles. Through this activity, Tbc1d23 has been proposed to link endosomally-derived vesicles to their appropriate target membrane in the trans Golgi (TGN).
In this paper, we provide an initial characterization of Drosophila orthologue, we call tbc1. We show that, like its mammalian orthologue, Tbc1 localizes to the trans Golgi. We show that it also colocalizes with a subset of Rabs associated with both early and recycling endosomes. Animals completely missing tbc1 survive, but females have fertility defects. Consistent with the human disease, loss of tbc1 reduces optic lobe size and increases response time to mechanical perturbation. Loss and overexpression of tbc1 in the embryonic salivary glands leads to secretion defects and apical membrane irregularities.
These findings support a role for tbc1 in endocytic/membrane trafficking, consistent with its activities in other systems. |
doi_str_mv | 10.1186/s12860-019-0198-z |
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In this paper, we provide an initial characterization of Drosophila orthologue, we call tbc1. We show that, like its mammalian orthologue, Tbc1 localizes to the trans Golgi. We show that it also colocalizes with a subset of Rabs associated with both early and recycling endosomes. Animals completely missing tbc1 survive, but females have fertility defects. Consistent with the human disease, loss of tbc1 reduces optic lobe size and increases response time to mechanical perturbation. Loss and overexpression of tbc1 in the embryonic salivary glands leads to secretion defects and apical membrane irregularities.
These findings support a role for tbc1 in endocytic/membrane trafficking, consistent with its activities in other systems.</description><identifier>ISSN: 2661-8850</identifier><identifier>EISSN: 2661-8850</identifier><identifier>EISSN: 1471-2121</identifier><identifier>DOI: 10.1186/s12860-019-0198-z</identifier><identifier>PMID: 31242864</identifier><language>eng</language><publisher>England: BioMed Central</publisher><subject>Alleles ; Animals ; Apical ; Cell adhesion & migration ; Cell division ; Cell migration ; Drosophila ; Drosophila melanogaster - embryology ; Drosophila melanogaster - metabolism ; Drosophila Proteins - metabolism ; Embryos ; Endosome ; Endosomes ; Endosomes - metabolism ; Fertility ; Forkhead Transcription Factors - metabolism ; Gene Expression ; Golgi ; Golgi apparatus ; GTP Phosphohydrolases - metabolism ; GTPase-Activating Proteins - genetics ; GTPase-Activating Proteins - metabolism ; Homeostasis ; Hypoplasia ; Immune response ; Innate immunity ; Insects ; Membrane trafficking ; Membrane Transport Proteins - metabolism ; Monomeric GTP-Binding Proteins - metabolism ; Morphology ; Open Reading Frames - genetics ; Optic lobe ; Optic Lobe, Nonmammalian - metabolism ; Phagocytosis ; Protein turnover ; Proteins ; rab GTP-Binding Proteins - metabolism ; Rab-GAP ; Salivary gland ; Salivary Glands - embryology ; Salivary Glands - metabolism ; trans-Golgi Network - metabolism ; Transcription factors ; Vesicles</subject><ispartof>BMC cell biology, 2019-06, Vol.20 (1), p.19-19, Article 19</ispartof><rights>2019. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s). 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c493t-446df8c0d62e556135c257b519974440472421a97c6498798d89f1ee6d10582f3</citedby><cites>FETCH-LOGICAL-c493t-446df8c0d62e556135c257b519974440472421a97c6498798d89f1ee6d10582f3</cites><orcidid>0000-0003-1051-6935</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6595604/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6595604/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,37013,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31242864$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Johnson, Dorothy M</creatorcontrib><creatorcontrib>Andrew, Deborah J</creatorcontrib><title>Role of tbc1 in Drosophila embryonic salivary glands</title><title>BMC cell biology</title><addtitle>BMC Mol Cell Biol</addtitle><description>CG4552/tbc1 was identified as a downstream target of Fork head (Fkh), the single Drosophila member of the FoxA family of transcription factors and a major player in salivary gland formation and homeostasis. Tbc1 and its orthologues have been implicated in phagocytosis, the innate immune response, border cell migration, cancer and an autosomal recessive form of non-degenerative Pontocerebellar hypoplasia. Recently, the mammalian Tbc1 orthologue, Tbc1d23, has been shown to bind both the conserved N-terminal domains of two Golgins (Golgin-97 and Golgin-245) and the WASH complex on endosome vesicles. Through this activity, Tbc1d23 has been proposed to link endosomally-derived vesicles to their appropriate target membrane in the trans Golgi (TGN).
In this paper, we provide an initial characterization of Drosophila orthologue, we call tbc1. We show that, like its mammalian orthologue, Tbc1 localizes to the trans Golgi. We show that it also colocalizes with a subset of Rabs associated with both early and recycling endosomes. Animals completely missing tbc1 survive, but females have fertility defects. Consistent with the human disease, loss of tbc1 reduces optic lobe size and increases response time to mechanical perturbation. Loss and overexpression of tbc1 in the embryonic salivary glands leads to secretion defects and apical membrane irregularities.
These findings support a role for tbc1 in endocytic/membrane trafficking, consistent with its activities in other systems.</description><subject>Alleles</subject><subject>Animals</subject><subject>Apical</subject><subject>Cell adhesion & migration</subject><subject>Cell division</subject><subject>Cell migration</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - embryology</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Drosophila Proteins - metabolism</subject><subject>Embryos</subject><subject>Endosome</subject><subject>Endosomes</subject><subject>Endosomes - metabolism</subject><subject>Fertility</subject><subject>Forkhead Transcription Factors - metabolism</subject><subject>Gene Expression</subject><subject>Golgi</subject><subject>Golgi apparatus</subject><subject>GTP Phosphohydrolases - metabolism</subject><subject>GTPase-Activating Proteins - genetics</subject><subject>GTPase-Activating Proteins - metabolism</subject><subject>Homeostasis</subject><subject>Hypoplasia</subject><subject>Immune response</subject><subject>Innate immunity</subject><subject>Insects</subject><subject>Membrane trafficking</subject><subject>Membrane Transport Proteins - metabolism</subject><subject>Monomeric GTP-Binding Proteins - metabolism</subject><subject>Morphology</subject><subject>Open Reading Frames - genetics</subject><subject>Optic lobe</subject><subject>Optic Lobe, Nonmammalian - metabolism</subject><subject>Phagocytosis</subject><subject>Protein turnover</subject><subject>Proteins</subject><subject>rab GTP-Binding Proteins - metabolism</subject><subject>Rab-GAP</subject><subject>Salivary gland</subject><subject>Salivary Glands - embryology</subject><subject>Salivary Glands - metabolism</subject><subject>trans-Golgi Network - metabolism</subject><subject>Transcription factors</subject><subject>Vesicles</subject><issn>2661-8850</issn><issn>2661-8850</issn><issn>1471-2121</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNpdkV1rFDEUhoMottT-AG9kwBtvRnPyeXIjSOtHoVAQvQ5JJrPNMjtZk9lC--vNurW0vTgknLzn4eR9CXkL9CMAqk8VGCraUzD7wv7uBTlmSkGPKOnLR_cjclrrmlLKgBsD7DU54sBEmxbHRPzMU-zy2C0-QJfm7rzkmrfXaXJd3Phym-cUuuqmdOPKbbea3DzUN-TV6KYaT-_PE_L729dfZz_6y6vvF2dfLvsgDF96IdQwYqCDYlFKBVwGJrWXYIwWQlCh2xbgjA5KGNQGBzQjxKgGoBLZyE_IxYE7ZLe225I2bQebXbL_GrmsrCtLClO0GLiOY2DGy9DY2jtPkeHomRDOc2iszwfWduc3cQhxXoqbnkCfvszp2q7yjVXSSEVFA3y4B5T8ZxfrYjephjg1R2LeVcuYQK45ImvS98-k67wrc7OqqRRlSku6V8FBFZrltcTxYRmgdh-xPURsW7z7QnvXZt49_sXDxP9A-V-9Hp8K</recordid><startdate>20190626</startdate><enddate>20190626</enddate><creator>Johnson, Dorothy M</creator><creator>Andrew, Deborah J</creator><general>BioMed Central</general><general>BMC</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>3V.</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-1051-6935</orcidid></search><sort><creationdate>20190626</creationdate><title>Role of tbc1 in Drosophila embryonic salivary glands</title><author>Johnson, Dorothy M ; Andrew, Deborah J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c493t-446df8c0d62e556135c257b519974440472421a97c6498798d89f1ee6d10582f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Alleles</topic><topic>Animals</topic><topic>Apical</topic><topic>Cell adhesion & migration</topic><topic>Cell division</topic><topic>Cell migration</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - embryology</topic><topic>Drosophila melanogaster - metabolism</topic><topic>Drosophila Proteins - metabolism</topic><topic>Embryos</topic><topic>Endosome</topic><topic>Endosomes</topic><topic>Endosomes - metabolism</topic><topic>Fertility</topic><topic>Forkhead Transcription Factors - metabolism</topic><topic>Gene Expression</topic><topic>Golgi</topic><topic>Golgi apparatus</topic><topic>GTP Phosphohydrolases - metabolism</topic><topic>GTPase-Activating Proteins - genetics</topic><topic>GTPase-Activating Proteins - metabolism</topic><topic>Homeostasis</topic><topic>Hypoplasia</topic><topic>Immune response</topic><topic>Innate immunity</topic><topic>Insects</topic><topic>Membrane trafficking</topic><topic>Membrane Transport Proteins - metabolism</topic><topic>Monomeric GTP-Binding Proteins - metabolism</topic><topic>Morphology</topic><topic>Open Reading Frames - genetics</topic><topic>Optic lobe</topic><topic>Optic Lobe, Nonmammalian - metabolism</topic><topic>Phagocytosis</topic><topic>Protein turnover</topic><topic>Proteins</topic><topic>rab GTP-Binding Proteins - metabolism</topic><topic>Rab-GAP</topic><topic>Salivary gland</topic><topic>Salivary Glands - embryology</topic><topic>Salivary Glands - metabolism</topic><topic>trans-Golgi Network - metabolism</topic><topic>Transcription factors</topic><topic>Vesicles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Johnson, Dorothy M</creatorcontrib><creatorcontrib>Andrew, Deborah J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection (Proquest)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Biological Science Database</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>BMC cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Johnson, Dorothy M</au><au>Andrew, Deborah J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Role of tbc1 in Drosophila embryonic salivary glands</atitle><jtitle>BMC cell biology</jtitle><addtitle>BMC Mol Cell Biol</addtitle><date>2019-06-26</date><risdate>2019</risdate><volume>20</volume><issue>1</issue><spage>19</spage><epage>19</epage><pages>19-19</pages><artnum>19</artnum><issn>2661-8850</issn><eissn>2661-8850</eissn><eissn>1471-2121</eissn><abstract>CG4552/tbc1 was identified as a downstream target of Fork head (Fkh), the single Drosophila member of the FoxA family of transcription factors and a major player in salivary gland formation and homeostasis. Tbc1 and its orthologues have been implicated in phagocytosis, the innate immune response, border cell migration, cancer and an autosomal recessive form of non-degenerative Pontocerebellar hypoplasia. Recently, the mammalian Tbc1 orthologue, Tbc1d23, has been shown to bind both the conserved N-terminal domains of two Golgins (Golgin-97 and Golgin-245) and the WASH complex on endosome vesicles. Through this activity, Tbc1d23 has been proposed to link endosomally-derived vesicles to their appropriate target membrane in the trans Golgi (TGN).
In this paper, we provide an initial characterization of Drosophila orthologue, we call tbc1. We show that, like its mammalian orthologue, Tbc1 localizes to the trans Golgi. We show that it also colocalizes with a subset of Rabs associated with both early and recycling endosomes. Animals completely missing tbc1 survive, but females have fertility defects. Consistent with the human disease, loss of tbc1 reduces optic lobe size and increases response time to mechanical perturbation. Loss and overexpression of tbc1 in the embryonic salivary glands leads to secretion defects and apical membrane irregularities.
These findings support a role for tbc1 in endocytic/membrane trafficking, consistent with its activities in other systems.</abstract><cop>England</cop><pub>BioMed Central</pub><pmid>31242864</pmid><doi>10.1186/s12860-019-0198-z</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-1051-6935</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alleles Animals Apical Cell adhesion & migration Cell division Cell migration Drosophila Drosophila melanogaster - embryology Drosophila melanogaster - metabolism Drosophila Proteins - metabolism Embryos Endosome Endosomes Endosomes - metabolism Fertility Forkhead Transcription Factors - metabolism Gene Expression Golgi Golgi apparatus GTP Phosphohydrolases - metabolism GTPase-Activating Proteins - genetics GTPase-Activating Proteins - metabolism Homeostasis Hypoplasia Immune response Innate immunity Insects Membrane trafficking Membrane Transport Proteins - metabolism Monomeric GTP-Binding Proteins - metabolism Morphology Open Reading Frames - genetics Optic lobe Optic Lobe, Nonmammalian - metabolism Phagocytosis Protein turnover Proteins rab GTP-Binding Proteins - metabolism Rab-GAP Salivary gland Salivary Glands - embryology Salivary Glands - metabolism trans-Golgi Network - metabolism Transcription factors Vesicles |
title | Role of tbc1 in Drosophila embryonic salivary glands |
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