The phosphoinositide phosphatase Sac1 regulates cell shape and microtubule stability in the developing Drosophila eye
Epithelial patterning in the developing eye requires the Neph1 homolog Roughest (Rst), an immunoglobulin family cell surface adhesion molecule expressed in interommatidial cells (IOCs). Here, using a novel temperature-sensitive (ts) allele, we show that the phosphoinositide phosphatase Sac1 is also...
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Veröffentlicht in: | Development (Cambridge) 2018-06, Vol.145 (11), p.dev151571-dev151571 |
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container_issue | 11 |
container_start_page | dev151571 |
container_title | Development (Cambridge) |
container_volume | 145 |
creator | Del Bel, Lauren M Griffiths, Nigel Wilk, Ronit Wei, Ho-Chun Blagoveshchenskaya, Anastasia Burgess, Jason Polevoy, Gordon Price, James V Mayinger, Peter Brill, Julie A |
description | Epithelial patterning in the developing
eye requires the Neph1 homolog Roughest (Rst), an immunoglobulin family cell surface adhesion molecule expressed in interommatidial cells (IOCs). Here, using a novel temperature-sensitive (ts) allele, we show that the phosphoinositide phosphatase Sac1 is also required for IOC patterning.
mutants have rough eyes and retinal patterning defects that resemble
mutants.
retinas exhibit elevated levels of phosphatidylinositol 4-phosphate (PI4P), consistent with the role of Sac1 as a PI4P phosphatase. Indeed, genetic rescue and interaction experiments reveal that restriction of PI4P levels by Sac1 is crucial for normal eye development. Rst is delivered to the cell surface in
mutants. However,
mutant IOCs exhibit severe defects in microtubule organization, associated with accumulation of Rst and the exocyst subunit Sec8 in enlarged intracellular vesicles upon cold fixation
Together, our data reveal a novel requirement for Sac1 in promoting microtubule stability and suggest that Rst trafficking occurs in a microtubule- and exocyst-dependent manner. |
doi_str_mv | 10.1242/dev.151571 |
format | Article |
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eye requires the Neph1 homolog Roughest (Rst), an immunoglobulin family cell surface adhesion molecule expressed in interommatidial cells (IOCs). Here, using a novel temperature-sensitive (ts) allele, we show that the phosphoinositide phosphatase Sac1 is also required for IOC patterning.
mutants have rough eyes and retinal patterning defects that resemble
mutants.
retinas exhibit elevated levels of phosphatidylinositol 4-phosphate (PI4P), consistent with the role of Sac1 as a PI4P phosphatase. Indeed, genetic rescue and interaction experiments reveal that restriction of PI4P levels by Sac1 is crucial for normal eye development. Rst is delivered to the cell surface in
mutants. However,
mutant IOCs exhibit severe defects in microtubule organization, associated with accumulation of Rst and the exocyst subunit Sec8 in enlarged intracellular vesicles upon cold fixation
Together, our data reveal a novel requirement for Sac1 in promoting microtubule stability and suggest that Rst trafficking occurs in a microtubule- and exocyst-dependent manner.</description><identifier>ISSN: 0950-1991</identifier><identifier>ISSN: 1477-9129</identifier><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.151571</identifier><identifier>PMID: 29752385</identifier><language>eng</language><publisher>England: The Company of Biologists Ltd</publisher><subject>Animals ; Cell Adhesion Molecules, Neuronal - genetics ; Cell Differentiation - physiology ; Cell Shape - physiology ; Cell size ; Cell surface ; Drosophila ; Drosophila melanogaster - embryology ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Eye ; Eye - embryology ; Eye Proteins - genetics ; Insects ; Microtubules - metabolism ; Pattern formation ; Phosphatase ; Phosphatidylinositol 4-phosphate ; Phosphatidylinositol Phosphates - metabolism ; Phosphoinositide Phosphatases - genetics ; Phosphoinositide Phosphatases - metabolism ; Protein Transport - physiology ; Retina ; Temperature ; Vesicular Transport Proteins - metabolism</subject><ispartof>Development (Cambridge), 2018-06, Vol.145 (11), p.dev151571-dev151571</ispartof><rights>2018. Published by The Company of Biologists Ltd.</rights><rights>Copyright The Company of Biologists Ltd Jun 1, 2018</rights><rights>2018. Published by The Company of Biologists Ltd 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c370t-546db4b13ecb12865292f5c0c88f982360728488981706d1982bcd6f7090929e3</citedby><cites>FETCH-LOGICAL-c370t-546db4b13ecb12865292f5c0c88f982360728488981706d1982bcd6f7090929e3</cites><orcidid>0000-0001-7956-6303 ; 0000-0002-0982-313X ; 0000-0003-1318-3339 ; 0000-0002-6124-0273 ; 0000-0001-9068-7317 ; 0000-0002-5925-9901 ; 0000-0001-7122-0551 ; 0000-0002-0597-7406 ; 0000-0003-2909-3506</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,3678,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29752385$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Del Bel, Lauren M</creatorcontrib><creatorcontrib>Griffiths, Nigel</creatorcontrib><creatorcontrib>Wilk, Ronit</creatorcontrib><creatorcontrib>Wei, Ho-Chun</creatorcontrib><creatorcontrib>Blagoveshchenskaya, Anastasia</creatorcontrib><creatorcontrib>Burgess, Jason</creatorcontrib><creatorcontrib>Polevoy, Gordon</creatorcontrib><creatorcontrib>Price, James V</creatorcontrib><creatorcontrib>Mayinger, Peter</creatorcontrib><creatorcontrib>Brill, Julie A</creatorcontrib><title>The phosphoinositide phosphatase Sac1 regulates cell shape and microtubule stability in the developing Drosophila eye</title><title>Development (Cambridge)</title><addtitle>Development</addtitle><description>Epithelial patterning in the developing
eye requires the Neph1 homolog Roughest (Rst), an immunoglobulin family cell surface adhesion molecule expressed in interommatidial cells (IOCs). Here, using a novel temperature-sensitive (ts) allele, we show that the phosphoinositide phosphatase Sac1 is also required for IOC patterning.
mutants have rough eyes and retinal patterning defects that resemble
mutants.
retinas exhibit elevated levels of phosphatidylinositol 4-phosphate (PI4P), consistent with the role of Sac1 as a PI4P phosphatase. Indeed, genetic rescue and interaction experiments reveal that restriction of PI4P levels by Sac1 is crucial for normal eye development. Rst is delivered to the cell surface in
mutants. However,
mutant IOCs exhibit severe defects in microtubule organization, associated with accumulation of Rst and the exocyst subunit Sec8 in enlarged intracellular vesicles upon cold fixation
Together, our data reveal a novel requirement for Sac1 in promoting microtubule stability and suggest that Rst trafficking occurs in a microtubule- and exocyst-dependent manner.</description><subject>Animals</subject><subject>Cell Adhesion Molecules, Neuronal - genetics</subject><subject>Cell Differentiation - physiology</subject><subject>Cell Shape - physiology</subject><subject>Cell size</subject><subject>Cell surface</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - embryology</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Eye</subject><subject>Eye - embryology</subject><subject>Eye Proteins - genetics</subject><subject>Insects</subject><subject>Microtubules - metabolism</subject><subject>Pattern formation</subject><subject>Phosphatase</subject><subject>Phosphatidylinositol 4-phosphate</subject><subject>Phosphatidylinositol Phosphates - metabolism</subject><subject>Phosphoinositide Phosphatases - genetics</subject><subject>Phosphoinositide Phosphatases - metabolism</subject><subject>Protein Transport - physiology</subject><subject>Retina</subject><subject>Temperature</subject><subject>Vesicular Transport Proteins - metabolism</subject><issn>0950-1991</issn><issn>1477-9129</issn><issn>1477-9129</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU9rFTEUxYNY7Gt14weQgBsRpubPZJJshFKtLRS6sK5DJnPnTUreZEwyhfftTXltUReXCzc_DifnIPSekjPKWvZlgIczKqiQ9BXa0FbKRlOmX6MN0YI0VGt6jE5yvieE8E7KN-iYaSkYV2KD1rsJ8DLFXMfPMfvih-eDLTYD_mkdxQm2a7AFMnYQAs6TXQDbecA771Isa78GwLnY3gdf9tjPuFTdagxCXPy8xd9SzHGZfLAY9vAWHY02ZHj3tE_Rr8vvdxdXzc3tj-uL85vGcUlKI9pu6NuecnA9ZaoTTLNROOKUGrVivCOSqVYpragk3UDrrXdDN0qiiWYa-Cn6etBd1n4Hg4O5JBvMkvzOpr2J1pt_X2Y_mW18MB3hlDNaBT49CaT4e4VczM7nxwjsDHHNhhGumKRKthX9-B96H9c01-9VSrSkclpV6vOBqrHlnGB8MUOJeWzT1NDMoc0Kf_jb_gv6XB__A_YYnBU</recordid><startdate>20180601</startdate><enddate>20180601</enddate><creator>Del Bel, Lauren M</creator><creator>Griffiths, Nigel</creator><creator>Wilk, Ronit</creator><creator>Wei, Ho-Chun</creator><creator>Blagoveshchenskaya, Anastasia</creator><creator>Burgess, Jason</creator><creator>Polevoy, Gordon</creator><creator>Price, James V</creator><creator>Mayinger, Peter</creator><creator>Brill, Julie A</creator><general>The Company of Biologists Ltd</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>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7956-6303</orcidid><orcidid>https://orcid.org/0000-0002-0982-313X</orcidid><orcidid>https://orcid.org/0000-0003-1318-3339</orcidid><orcidid>https://orcid.org/0000-0002-6124-0273</orcidid><orcidid>https://orcid.org/0000-0001-9068-7317</orcidid><orcidid>https://orcid.org/0000-0002-5925-9901</orcidid><orcidid>https://orcid.org/0000-0001-7122-0551</orcidid><orcidid>https://orcid.org/0000-0002-0597-7406</orcidid><orcidid>https://orcid.org/0000-0003-2909-3506</orcidid></search><sort><creationdate>20180601</creationdate><title>The phosphoinositide phosphatase Sac1 regulates cell shape and microtubule stability in the developing Drosophila eye</title><author>Del Bel, Lauren M ; Griffiths, Nigel ; Wilk, Ronit ; Wei, Ho-Chun ; Blagoveshchenskaya, Anastasia ; Burgess, Jason ; Polevoy, Gordon ; Price, James V ; Mayinger, Peter ; Brill, Julie A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c370t-546db4b13ecb12865292f5c0c88f982360728488981706d1982bcd6f7090929e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Cell Adhesion Molecules, Neuronal - genetics</topic><topic>Cell Differentiation - physiology</topic><topic>Cell Shape - physiology</topic><topic>Cell size</topic><topic>Cell surface</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - embryology</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>Eye</topic><topic>Eye - embryology</topic><topic>Eye Proteins - genetics</topic><topic>Insects</topic><topic>Microtubules - metabolism</topic><topic>Pattern formation</topic><topic>Phosphatase</topic><topic>Phosphatidylinositol 4-phosphate</topic><topic>Phosphatidylinositol Phosphates - metabolism</topic><topic>Phosphoinositide Phosphatases - genetics</topic><topic>Phosphoinositide Phosphatases - metabolism</topic><topic>Protein Transport - physiology</topic><topic>Retina</topic><topic>Temperature</topic><topic>Vesicular Transport Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Del Bel, Lauren M</creatorcontrib><creatorcontrib>Griffiths, Nigel</creatorcontrib><creatorcontrib>Wilk, Ronit</creatorcontrib><creatorcontrib>Wei, Ho-Chun</creatorcontrib><creatorcontrib>Blagoveshchenskaya, Anastasia</creatorcontrib><creatorcontrib>Burgess, Jason</creatorcontrib><creatorcontrib>Polevoy, Gordon</creatorcontrib><creatorcontrib>Price, James V</creatorcontrib><creatorcontrib>Mayinger, Peter</creatorcontrib><creatorcontrib>Brill, Julie A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Development (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Del Bel, Lauren M</au><au>Griffiths, Nigel</au><au>Wilk, Ronit</au><au>Wei, Ho-Chun</au><au>Blagoveshchenskaya, Anastasia</au><au>Burgess, Jason</au><au>Polevoy, Gordon</au><au>Price, James V</au><au>Mayinger, Peter</au><au>Brill, Julie A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The phosphoinositide phosphatase Sac1 regulates cell shape and microtubule stability in the developing Drosophila eye</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2018-06-01</date><risdate>2018</risdate><volume>145</volume><issue>11</issue><spage>dev151571</spage><epage>dev151571</epage><pages>dev151571-dev151571</pages><issn>0950-1991</issn><issn>1477-9129</issn><eissn>1477-9129</eissn><abstract>Epithelial patterning in the developing
eye requires the Neph1 homolog Roughest (Rst), an immunoglobulin family cell surface adhesion molecule expressed in interommatidial cells (IOCs). Here, using a novel temperature-sensitive (ts) allele, we show that the phosphoinositide phosphatase Sac1 is also required for IOC patterning.
mutants have rough eyes and retinal patterning defects that resemble
mutants.
retinas exhibit elevated levels of phosphatidylinositol 4-phosphate (PI4P), consistent with the role of Sac1 as a PI4P phosphatase. Indeed, genetic rescue and interaction experiments reveal that restriction of PI4P levels by Sac1 is crucial for normal eye development. Rst is delivered to the cell surface in
mutants. However,
mutant IOCs exhibit severe defects in microtubule organization, associated with accumulation of Rst and the exocyst subunit Sec8 in enlarged intracellular vesicles upon cold fixation
Together, our data reveal a novel requirement for Sac1 in promoting microtubule stability and suggest that Rst trafficking occurs in a microtubule- and exocyst-dependent manner.</abstract><cop>England</cop><pub>The Company of Biologists Ltd</pub><pmid>29752385</pmid><doi>10.1242/dev.151571</doi><orcidid>https://orcid.org/0000-0001-7956-6303</orcidid><orcidid>https://orcid.org/0000-0002-0982-313X</orcidid><orcidid>https://orcid.org/0000-0003-1318-3339</orcidid><orcidid>https://orcid.org/0000-0002-6124-0273</orcidid><orcidid>https://orcid.org/0000-0001-9068-7317</orcidid><orcidid>https://orcid.org/0000-0002-5925-9901</orcidid><orcidid>https://orcid.org/0000-0001-7122-0551</orcidid><orcidid>https://orcid.org/0000-0002-0597-7406</orcidid><orcidid>https://orcid.org/0000-0003-2909-3506</orcidid><oa>free_for_read</oa></addata></record> |
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source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection; Company of Biologists |
subjects | Animals Cell Adhesion Molecules, Neuronal - genetics Cell Differentiation - physiology Cell Shape - physiology Cell size Cell surface Drosophila Drosophila melanogaster - embryology Drosophila Proteins - genetics Drosophila Proteins - metabolism Eye Eye - embryology Eye Proteins - genetics Insects Microtubules - metabolism Pattern formation Phosphatase Phosphatidylinositol 4-phosphate Phosphatidylinositol Phosphates - metabolism Phosphoinositide Phosphatases - genetics Phosphoinositide Phosphatases - metabolism Protein Transport - physiology Retina Temperature Vesicular Transport Proteins - metabolism |
title | The phosphoinositide phosphatase Sac1 regulates cell shape and microtubule stability in the developing Drosophila eye |
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