Drosophila melanogaster Cad99C, the orthologue of human Usher cadherin PCDH15, regulates the length of microvilli
Actin-based protrusions can form prominent structures on the apical surface of epithelial cells, such as microvilli. Several cytoplasmic factors have been identified that control the dynamics of actin filaments in microvilli. However, it remains unclear whether the plasma membrane participates activ...
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Veröffentlicht in: | The Journal of cell biology 2005-11, Vol.171 (3), p.549-558 |
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creator | D'Alterio, Cecilia Tran, Dao D.D Yeung, Maggie W.Y. Au Hwang, Michael S.H Li, Michelle A Arana, Claudia J Mulligan, Vikram K Kubesh, Mary Sharma, Praveer Chase, Maretta Tepass, Ulrich Godt, Dorothea |
description | Actin-based protrusions can form prominent structures on the apical surface of epithelial cells, such as microvilli. Several cytoplasmic factors have been identified that control the dynamics of actin filaments in microvilli. However, it remains unclear whether the plasma membrane participates actively in microvillus formation. In this paper, we analyze the function of Drosophila melanogaster cadherin Cad99C in the microvilli of ovarian follicle cells. Cad99C contributes to eggshell formation and female fertility and is expressed in follicle cells, which produce the eggshells. Cad99C specifically localizes to apical microvilli. Loss of Cad99C function results in shortened and disorganized microvilli, whereas overexpression of Cad99C leads to a dramatic increase of microvillus length. Cad99C that lacks most of the cytoplasmic domain, including potential PDZ domain-binding sites, still promotes excessive microvillus outgrowth, suggesting that the amount of the extracellular domain determines microvillus length. This study reveals Cad99C as a critical regulator of microvillus length, the first example of a transmembrane protein that is involved in this process. |
doi_str_mv | 10.1083/jcb.200507072 |
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Au ; Hwang, Michael S.H ; Li, Michelle A ; Arana, Claudia J ; Mulligan, Vikram K ; Kubesh, Mary ; Sharma, Praveer ; Chase, Maretta ; Tepass, Ulrich ; Godt, Dorothea</creator><creatorcontrib>D'Alterio, Cecilia ; Tran, Dao D.D ; Yeung, Maggie W.Y. Au ; Hwang, Michael S.H ; Li, Michelle A ; Arana, Claudia J ; Mulligan, Vikram K ; Kubesh, Mary ; Sharma, Praveer ; Chase, Maretta ; Tepass, Ulrich ; Godt, Dorothea</creatorcontrib><description>Actin-based protrusions can form prominent structures on the apical surface of epithelial cells, such as microvilli. Several cytoplasmic factors have been identified that control the dynamics of actin filaments in microvilli. However, it remains unclear whether the plasma membrane participates actively in microvillus formation. In this paper, we analyze the function of Drosophila melanogaster cadherin Cad99C in the microvilli of ovarian follicle cells. Cad99C contributes to eggshell formation and female fertility and is expressed in follicle cells, which produce the eggshells. Cad99C specifically localizes to apical microvilli. Loss of Cad99C function results in shortened and disorganized microvilli, whereas overexpression of Cad99C leads to a dramatic increase of microvillus length. Cad99C that lacks most of the cytoplasmic domain, including potential PDZ domain-binding sites, still promotes excessive microvillus outgrowth, suggesting that the amount of the extracellular domain determines microvillus length. This study reveals Cad99C as a critical regulator of microvillus length, the first example of a transmembrane protein that is involved in this process.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.200507072</identifier><identifier>PMID: 16260500</identifier><identifier>CODEN: JCLBA3</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animals ; Cadherins - genetics ; Cellular biology ; Drosophila melanogaster ; Drosophila melanogaster - genetics ; Drosophila melanogaster - metabolism ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Female ; Humans ; Insects ; Microvilli - physiology ; Microvilli - ultrastructure ; Oogenesis ; Ovarian Follicle - physiology ; Ovarian Follicle - ultrastructure ; Protein Precursors - genetics ; Protein Structure, Tertiary ; Proteins</subject><ispartof>The Journal of cell biology, 2005-11, Vol.171 (3), p.549-558</ispartof><rights>Copyright Rockefeller University Press Nov 7, 2005</rights><rights>Copyright © 2005, The Rockefeller University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c467t-7cf58ab3f47d825089d05239454e599b0691941cd201b1008ec4e825699aca803</citedby><cites>FETCH-LOGICAL-c467t-7cf58ab3f47d825089d05239454e599b0691941cd201b1008ec4e825699aca803</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16260500$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>D'Alterio, Cecilia</creatorcontrib><creatorcontrib>Tran, Dao D.D</creatorcontrib><creatorcontrib>Yeung, Maggie W.Y. Au</creatorcontrib><creatorcontrib>Hwang, Michael S.H</creatorcontrib><creatorcontrib>Li, Michelle A</creatorcontrib><creatorcontrib>Arana, Claudia J</creatorcontrib><creatorcontrib>Mulligan, Vikram K</creatorcontrib><creatorcontrib>Kubesh, Mary</creatorcontrib><creatorcontrib>Sharma, Praveer</creatorcontrib><creatorcontrib>Chase, Maretta</creatorcontrib><creatorcontrib>Tepass, Ulrich</creatorcontrib><creatorcontrib>Godt, Dorothea</creatorcontrib><title>Drosophila melanogaster Cad99C, the orthologue of human Usher cadherin PCDH15, regulates the length of microvilli</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Actin-based protrusions can form prominent structures on the apical surface of epithelial cells, such as microvilli. Several cytoplasmic factors have been identified that control the dynamics of actin filaments in microvilli. However, it remains unclear whether the plasma membrane participates actively in microvillus formation. In this paper, we analyze the function of Drosophila melanogaster cadherin Cad99C in the microvilli of ovarian follicle cells. Cad99C contributes to eggshell formation and female fertility and is expressed in follicle cells, which produce the eggshells. Cad99C specifically localizes to apical microvilli. Loss of Cad99C function results in shortened and disorganized microvilli, whereas overexpression of Cad99C leads to a dramatic increase of microvillus length. Cad99C that lacks most of the cytoplasmic domain, including potential PDZ domain-binding sites, still promotes excessive microvillus outgrowth, suggesting that the amount of the extracellular domain determines microvillus length. This study reveals Cad99C as a critical regulator of microvillus length, the first example of a transmembrane protein that is involved in this process.</description><subject>Animals</subject><subject>Cadherins - genetics</subject><subject>Cellular biology</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Female</subject><subject>Humans</subject><subject>Insects</subject><subject>Microvilli - physiology</subject><subject>Microvilli - ultrastructure</subject><subject>Oogenesis</subject><subject>Ovarian Follicle - physiology</subject><subject>Ovarian Follicle - ultrastructure</subject><subject>Protein Precursors - genetics</subject><subject>Protein Structure, Tertiary</subject><subject>Proteins</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1v1DAUxC0EotvCkStEHDg15dmxY_uChNJCkSqBBHu2HMdJvHLirZ1U4r_H7a7Kx4XTs-TfjP1mEHqF4QKDqN7vTHtBABhw4OQJ2mBGoRSYwlO0ASC4lIywE3Sa0g4AKKfVc3SCa1JnCWzQ7WUMKexH53UxWa_nMOi02Fg0upOyOS-W0RYhLmPwYVjzsS_GddJzsU1jpozu8nBz8a25vMbsvIh2WL1ebHoQejsPy3gvmpyJ4c55716gZ732yb48zjO0_XT1o7kub75-_tJ8vCkNrflSctMzoduqp7wThIGQHTBSScqoZVK2UEssKTYdAdxiAGENtRmspdRGC6jO0IeD735tJ9sZOy9Re7WPbtLxpwraqb9vZjeqIdwpgjkmdZ0N3h0NYrhdbVrU5JKxPodkw5pULTiXAvP_glhWnNdSZPDtP-AurHHOKTw8CoQSkqHyAOXAUoq2f_wyBnVfucqVq8fKM__6zz1_08eOM_DmAPQ6KD1El9T2e06tAgxVXoBWvwDj569m</recordid><startdate>20051107</startdate><enddate>20051107</enddate><creator>D'Alterio, Cecilia</creator><creator>Tran, Dao D.D</creator><creator>Yeung, Maggie W.Y. Au</creator><creator>Hwang, Michael S.H</creator><creator>Li, Michelle A</creator><creator>Arana, Claudia J</creator><creator>Mulligan, Vikram K</creator><creator>Kubesh, Mary</creator><creator>Sharma, Praveer</creator><creator>Chase, Maretta</creator><creator>Tepass, Ulrich</creator><creator>Godt, Dorothea</creator><general>Rockefeller University Press</general><general>The Rockefeller University Press</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</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>7SS</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20051107</creationdate><title>Drosophila melanogaster Cad99C, the orthologue of human Usher cadherin PCDH15, regulates the length of microvilli</title><author>D'Alterio, Cecilia ; Tran, Dao D.D ; Yeung, Maggie W.Y. Au ; Hwang, Michael S.H ; Li, Michelle A ; Arana, Claudia J ; Mulligan, Vikram K ; Kubesh, Mary ; Sharma, Praveer ; Chase, Maretta ; Tepass, Ulrich ; Godt, Dorothea</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c467t-7cf58ab3f47d825089d05239454e599b0691941cd201b1008ec4e825699aca803</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Animals</topic><topic>Cadherins - genetics</topic><topic>Cellular biology</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila melanogaster - metabolism</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>Female</topic><topic>Humans</topic><topic>Insects</topic><topic>Microvilli - physiology</topic><topic>Microvilli - ultrastructure</topic><topic>Oogenesis</topic><topic>Ovarian Follicle - physiology</topic><topic>Ovarian Follicle - ultrastructure</topic><topic>Protein Precursors - genetics</topic><topic>Protein Structure, Tertiary</topic><topic>Proteins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>D'Alterio, Cecilia</creatorcontrib><creatorcontrib>Tran, Dao D.D</creatorcontrib><creatorcontrib>Yeung, Maggie W.Y. 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Au</au><au>Hwang, Michael S.H</au><au>Li, Michelle A</au><au>Arana, Claudia J</au><au>Mulligan, Vikram K</au><au>Kubesh, Mary</au><au>Sharma, Praveer</au><au>Chase, Maretta</au><au>Tepass, Ulrich</au><au>Godt, Dorothea</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Drosophila melanogaster Cad99C, the orthologue of human Usher cadherin PCDH15, regulates the length of microvilli</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2005-11-07</date><risdate>2005</risdate><volume>171</volume><issue>3</issue><spage>549</spage><epage>558</epage><pages>549-558</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><coden>JCLBA3</coden><abstract>Actin-based protrusions can form prominent structures on the apical surface of epithelial cells, such as microvilli. Several cytoplasmic factors have been identified that control the dynamics of actin filaments in microvilli. However, it remains unclear whether the plasma membrane participates actively in microvillus formation. In this paper, we analyze the function of Drosophila melanogaster cadherin Cad99C in the microvilli of ovarian follicle cells. Cad99C contributes to eggshell formation and female fertility and is expressed in follicle cells, which produce the eggshells. Cad99C specifically localizes to apical microvilli. Loss of Cad99C function results in shortened and disorganized microvilli, whereas overexpression of Cad99C leads to a dramatic increase of microvillus length. Cad99C that lacks most of the cytoplasmic domain, including potential PDZ domain-binding sites, still promotes excessive microvillus outgrowth, suggesting that the amount of the extracellular domain determines microvillus length. 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subjects | Animals Cadherins - genetics Cellular biology Drosophila melanogaster Drosophila melanogaster - genetics Drosophila melanogaster - metabolism Drosophila Proteins - genetics Drosophila Proteins - metabolism Female Humans Insects Microvilli - physiology Microvilli - ultrastructure Oogenesis Ovarian Follicle - physiology Ovarian Follicle - ultrastructure Protein Precursors - genetics Protein Structure, Tertiary Proteins |
title | Drosophila melanogaster Cad99C, the orthologue of human Usher cadherin PCDH15, regulates the length of microvilli |
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