Lipid droplets maintain lipid homeostasis during anaphase for efficient cell separation in budding yeast
The neutral lipids steryl ester and triacylglycerol (TAG) are stored in the membrane-bound organelle lipid droplet (LD) in essentially all eukaryotic cells. It is unclear what physiological conditions require the mobilization or storage of these lipids. Here, we study the budding yeast mutant are1Δ...
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Veröffentlicht in: | Molecular biology of the cell 2016-08, Vol.27 (15), p.2368-2380 |
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creator | Yang, Po-Lin Hsu, Tzu-Han Wang, Chao-Wen Chen, Rey-Huei |
description | The neutral lipids steryl ester and triacylglycerol (TAG) are stored in the membrane-bound organelle lipid droplet (LD) in essentially all eukaryotic cells. It is unclear what physiological conditions require the mobilization or storage of these lipids. Here, we study the budding yeast mutant are1Δ are2Δ dga1Δ lro1Δ, which cannot synthesize the neutral lipids and therefore lacks LDs. This quadruple mutant is delayed at cell separation upon release from mitotic arrest. The cells have abnormal septa, unstable septin assembly during cytokinesis, and prolonged exocytosis at the division site at the end of cytokinesis. Lipidomic analysis shows a marked increase of diacylglycerol (DAG) and phosphatidic acid, the precursors for TAG, in the mutant during mitotic exit. The cytokinesis and separation defects are rescued by adding phospholipid precursors or inhibiting fatty acid synthesis, which both reduce DAG levels. Our results suggest that converting excess lipids to neutral lipids for storage during mitotic exit is important for proper execution of cytokinesis and efficient cell separation. |
doi_str_mv | 10.1091/mbc.E16-02-0106 |
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It is unclear what physiological conditions require the mobilization or storage of these lipids. Here, we study the budding yeast mutant are1Δ are2Δ dga1Δ lro1Δ, which cannot synthesize the neutral lipids and therefore lacks LDs. This quadruple mutant is delayed at cell separation upon release from mitotic arrest. The cells have abnormal septa, unstable septin assembly during cytokinesis, and prolonged exocytosis at the division site at the end of cytokinesis. Lipidomic analysis shows a marked increase of diacylglycerol (DAG) and phosphatidic acid, the precursors for TAG, in the mutant during mitotic exit. The cytokinesis and separation defects are rescued by adding phospholipid precursors or inhibiting fatty acid synthesis, which both reduce DAG levels. Our results suggest that converting excess lipids to neutral lipids for storage during mitotic exit is important for proper execution of cytokinesis and efficient cell separation.</description><identifier>ISSN: 1059-1524</identifier><identifier>EISSN: 1939-4586</identifier><identifier>DOI: 10.1091/mbc.E16-02-0106</identifier><identifier>PMID: 27307588</identifier><language>eng</language><publisher>United States: The American Society for Cell Biology</publisher><subject>Anaphase ; Cell Cycle ; Cell Separation ; Cytokinesis - physiology ; Diglycerides - metabolism ; Homeostasis - physiology ; Lipid Droplets - metabolism ; Lipid Droplets - physiology ; Lipid Metabolism - physiology ; Phosphatidic Acids - metabolism ; Phospholipids - metabolism ; Saccharomyces cerevisiae - metabolism ; Saccharomyces cerevisiae Proteins - metabolism ; Saccharomycetales - metabolism ; Triglycerides - metabolism</subject><ispartof>Molecular biology of the cell, 2016-08, Vol.27 (15), p.2368-2380</ispartof><rights>2016 Yang et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0).</rights><rights>2016 Yang This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License ( ). 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c505t-a8f4d301dc101d93024e9ab984ae8287b55dfb358c487140047c6286d2cd34c13</citedby><cites>FETCH-LOGICAL-c505t-a8f4d301dc101d93024e9ab984ae8287b55dfb358c487140047c6286d2cd34c13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4966979/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4966979/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27922,27923,53789,53791</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27307588$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Spang, Anne</contributor><creatorcontrib>Yang, Po-Lin</creatorcontrib><creatorcontrib>Hsu, Tzu-Han</creatorcontrib><creatorcontrib>Wang, Chao-Wen</creatorcontrib><creatorcontrib>Chen, Rey-Huei</creatorcontrib><title>Lipid droplets maintain lipid homeostasis during anaphase for efficient cell separation in budding yeast</title><title>Molecular biology of the cell</title><addtitle>Mol Biol Cell</addtitle><description>The neutral lipids steryl ester and triacylglycerol (TAG) are stored in the membrane-bound organelle lipid droplet (LD) in essentially all eukaryotic cells. It is unclear what physiological conditions require the mobilization or storage of these lipids. Here, we study the budding yeast mutant are1Δ are2Δ dga1Δ lro1Δ, which cannot synthesize the neutral lipids and therefore lacks LDs. This quadruple mutant is delayed at cell separation upon release from mitotic arrest. The cells have abnormal septa, unstable septin assembly during cytokinesis, and prolonged exocytosis at the division site at the end of cytokinesis. Lipidomic analysis shows a marked increase of diacylglycerol (DAG) and phosphatidic acid, the precursors for TAG, in the mutant during mitotic exit. The cytokinesis and separation defects are rescued by adding phospholipid precursors or inhibiting fatty acid synthesis, which both reduce DAG levels. Our results suggest that converting excess lipids to neutral lipids for storage during mitotic exit is important for proper execution of cytokinesis and efficient cell separation.</description><subject>Anaphase</subject><subject>Cell Cycle</subject><subject>Cell Separation</subject><subject>Cytokinesis - physiology</subject><subject>Diglycerides - metabolism</subject><subject>Homeostasis - physiology</subject><subject>Lipid Droplets - metabolism</subject><subject>Lipid Droplets - physiology</subject><subject>Lipid Metabolism - physiology</subject><subject>Phosphatidic Acids - metabolism</subject><subject>Phospholipids - metabolism</subject><subject>Saccharomyces cerevisiae - metabolism</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Saccharomycetales - metabolism</subject><subject>Triglycerides - metabolism</subject><issn>1059-1524</issn><issn>1939-4586</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUUtP3DAQthAVUNozN-QjlyzjxM8LEkJAK63EhZ4tx3Z2jZI42AnS_nu8vEQP89DMN9_M6EPojMCKgCKXQ2tXt4RXUFdAgB-gE6IaVVEm-WHJgamKsJoeo585PwEQSrk4Qse1aEAwKU_Qdh2m4LBLcer9nPFgwjgXw_1bfRsHH_NscsjYLSmMG2xGM21N9riLCfuuCzb4ccbW9z3OfjLJzCGOuFC0i3P7iZ03ef6FfnSmz_73RzxF_-5uH2_-VOuH-7831-vKMmBzZWRHXQPEWVKcaqCmXplWSWq8rKVoGXNd2zBpqRSEAlBheS25q61rqCXNKbp6552WdvDOltuS6fWUwmDSTkcT9P-dMWz1Jr5oqjhXQhWCiw-CFJ8Xn2c9hLz_zow-LlkTCUIKziUU6OU71KaYc_Ld1xoCeq-PLvpoT7iGWu_1KRPn36_7wn8K0rwCdIGOzQ</recordid><startdate>20160801</startdate><enddate>20160801</enddate><creator>Yang, Po-Lin</creator><creator>Hsu, Tzu-Han</creator><creator>Wang, Chao-Wen</creator><creator>Chen, Rey-Huei</creator><general>The American Society for Cell Biology</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20160801</creationdate><title>Lipid droplets maintain lipid homeostasis during anaphase for efficient cell separation in budding yeast</title><author>Yang, Po-Lin ; Hsu, Tzu-Han ; Wang, Chao-Wen ; Chen, Rey-Huei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c505t-a8f4d301dc101d93024e9ab984ae8287b55dfb358c487140047c6286d2cd34c13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Anaphase</topic><topic>Cell Cycle</topic><topic>Cell Separation</topic><topic>Cytokinesis - physiology</topic><topic>Diglycerides - metabolism</topic><topic>Homeostasis - physiology</topic><topic>Lipid Droplets - metabolism</topic><topic>Lipid Droplets - physiology</topic><topic>Lipid Metabolism - physiology</topic><topic>Phosphatidic Acids - metabolism</topic><topic>Phospholipids - metabolism</topic><topic>Saccharomyces cerevisiae - metabolism</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Saccharomycetales - metabolism</topic><topic>Triglycerides - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Po-Lin</creatorcontrib><creatorcontrib>Hsu, Tzu-Han</creatorcontrib><creatorcontrib>Wang, Chao-Wen</creatorcontrib><creatorcontrib>Chen, Rey-Huei</creatorcontrib><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>Molecular biology of the cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Po-Lin</au><au>Hsu, Tzu-Han</au><au>Wang, Chao-Wen</au><au>Chen, Rey-Huei</au><au>Spang, Anne</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lipid droplets maintain lipid homeostasis during anaphase for efficient cell separation in budding yeast</atitle><jtitle>Molecular biology of the cell</jtitle><addtitle>Mol Biol Cell</addtitle><date>2016-08-01</date><risdate>2016</risdate><volume>27</volume><issue>15</issue><spage>2368</spage><epage>2380</epage><pages>2368-2380</pages><issn>1059-1524</issn><eissn>1939-4586</eissn><abstract>The neutral lipids steryl ester and triacylglycerol (TAG) are stored in the membrane-bound organelle lipid droplet (LD) in essentially all eukaryotic cells. It is unclear what physiological conditions require the mobilization or storage of these lipids. Here, we study the budding yeast mutant are1Δ are2Δ dga1Δ lro1Δ, which cannot synthesize the neutral lipids and therefore lacks LDs. This quadruple mutant is delayed at cell separation upon release from mitotic arrest. The cells have abnormal septa, unstable septin assembly during cytokinesis, and prolonged exocytosis at the division site at the end of cytokinesis. Lipidomic analysis shows a marked increase of diacylglycerol (DAG) and phosphatidic acid, the precursors for TAG, in the mutant during mitotic exit. The cytokinesis and separation defects are rescued by adding phospholipid precursors or inhibiting fatty acid synthesis, which both reduce DAG levels. Our results suggest that converting excess lipids to neutral lipids for storage during mitotic exit is important for proper execution of cytokinesis and efficient cell separation.</abstract><cop>United States</cop><pub>The American Society for Cell Biology</pub><pmid>27307588</pmid><doi>10.1091/mbc.E16-02-0106</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Anaphase Cell Cycle Cell Separation Cytokinesis - physiology Diglycerides - metabolism Homeostasis - physiology Lipid Droplets - metabolism Lipid Droplets - physiology Lipid Metabolism - physiology Phosphatidic Acids - metabolism Phospholipids - metabolism Saccharomyces cerevisiae - metabolism Saccharomyces cerevisiae Proteins - metabolism Saccharomycetales - metabolism Triglycerides - metabolism |
title | Lipid droplets maintain lipid homeostasis during anaphase for efficient cell separation in budding yeast |
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