PI(3,4)P2-mediated cytokinetic abscission prevents early senescence and cataract formation
Cytokinetic membrane abscission is a spatially and temporally regulated process that requires ESCRT (endosomal sorting complexes required for transport)–dependent control of membrane remodeling at the midbody, a subcellular organelle that defines the cleavage site. Alteration of ESCRT function can l...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2021-12, Vol.374 (6573), p.eabk0410-eabk0410 |
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| creator | Gulluni, Federico Prever, Lorenzo Li, Huayi Krafcikova, Petra Corrado, Ilaria Lo, Wen-Ting Margaria, Jean Piero Chen, Anlu De Santis, Maria Chiara Cnudde, Sophie J Fogerty, Joseph Yuan, Alex Massarotti, Alberto Sarijalo, Nasrin Torabi Vadas, Oscar Williams, Roger L Thelen, Marcus Powell, David R Schueler, Markus Wiesener, Michael S Balla, Tamas Baris, Hagit N Tiosano, Dov McDermott, Jr, Brian M Perkins, Brian D Ghigo, Alessandra Martini, Miriam Haucke, Volker Boura, Evzen Merlo, Giorgio Roberto Buchner, David A Hirsch, Emilio |
| description | Cytokinetic membrane abscission is a spatially and temporally regulated process that requires ESCRT (endosomal sorting complexes required for transport)–dependent control of membrane remodeling at the midbody, a subcellular organelle that defines the cleavage site. Alteration of ESCRT function can lead to cataract, but the underlying mechanism and its relation to cytokinesis are unclear. We found a lens-specific cytokinetic process that required PI3K-C2α (phosphatidylinositol-4-phosphate 3-kinase catalytic subunit type 2α), its lipid product PI(3,4)P
(phosphatidylinositol 3,4-bisphosphate), and the PI(3,4)P
–binding ESCRT-II subunit VPS36 (vacuolar protein-sorting-associated protein 36). Loss of each of these components led to impaired cytokinesis, triggering premature senescence in the lens of fish, mice, and humans. Thus, an evolutionarily conserved pathway underlies the cell type–specific control of cytokinesis that helps to prevent early onset cataract by protecting from senescence. |
| doi_str_mv | 10.1126/science.abk0410 |
| format | Article |
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(phosphatidylinositol 3,4-bisphosphate), and the PI(3,4)P
–binding ESCRT-II subunit VPS36 (vacuolar protein-sorting-associated protein 36). Loss of each of these components led to impaired cytokinesis, triggering premature senescence in the lens of fish, mice, and humans. Thus, an evolutionarily conserved pathway underlies the cell type–specific control of cytokinesis that helps to prevent early onset cataract by protecting from senescence.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.abk0410</identifier><identifier>PMID: 34882480</identifier><language>eng</language><publisher>United States: The American Association for the Advancement of Science</publisher><subject>1-Phosphatidylinositol 3-kinase ; Abscission ; Age ; Aging ; Aging, Premature ; Animals ; Binding ; Biological Evolution ; Calcium-Binding Proteins - metabolism ; Cataract - metabolism ; Cataract - pathology ; Cataracts ; Cell Cycle Proteins - metabolism ; Cell division ; Cell Line ; Cellular Senescence ; Contractility ; Cytokinesis ; Degenerative diseases ; Endosomal Sorting Complexes Required for Transport - metabolism ; Enucleation ; Evolution ; Eye (anatomy) ; Eye lens ; Fish ; Genomic instability ; Geriatrics ; Humans ; INK4a protein ; Kinases ; Lens, Crystalline - cytology ; Lens, Crystalline - growth & development ; Lens, Crystalline - metabolism ; Lenses ; Lipid kinase ; Lipids ; Membrane fusion ; Membranes ; Mice ; Mitosis ; Mutation ; Older people ; p16 Protein ; Pathogenesis ; Phosphatidylinositol 3-Kinases - genetics ; Phosphatidylinositol 3-Kinases - metabolism ; Phosphatidylinositol 4,5-Diphosphate - metabolism ; Phosphatidylinositols - metabolism ; Protein transport ; Proteins ; Senescence ; Transcription activation ; Tubulin - metabolism ; Vertebrates ; Zebrafish ; Zebrafish Proteins - genetics ; Zebrafish Proteins - metabolism</subject><ispartof>Science (American Association for the Advancement of Science), 2021-12, Vol.374 (6573), p.eabk0410-eabk0410</ispartof><rights>Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c421t-736d090c468f31cedc4698e10fb3840e6cf09586a5e99cf6d0b411188ba600603</citedby><cites>FETCH-LOGICAL-c421t-736d090c468f31cedc4698e10fb3840e6cf09586a5e99cf6d0b411188ba600603</cites><orcidid>0000-0003-3920-4871 ; 0000-0002-4262-946X ; 0000-0002-2435-7499 ; 0000-0001-7754-4207 ; 0000-0003-0191-8035 ; 0000-0002-9073-6024 ; 0000-0002-1193-5296 ; 0000-0001-8072-388X ; 0000-0002-3443-1605 ; 0000-0001-9306-8845 ; 0000-0003-4065-7560 ; 0000-0003-2785-0665 ; 0000-0003-3121-2471 ; 0000-0001-5244-9211 ; 0000-0001-7904-6834 ; 0000-0003-3511-6479 ; 0000-0002-3363-2499 ; 0000-0001-7706-1635 ; 0000-0002-9652-4065 ; 0000-0002-9348-6542 ; 0000-0003-0151-6247 ; 0000-0003-3119-6993</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,2871,2872,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34882480$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gulluni, Federico</creatorcontrib><creatorcontrib>Prever, Lorenzo</creatorcontrib><creatorcontrib>Li, Huayi</creatorcontrib><creatorcontrib>Krafcikova, Petra</creatorcontrib><creatorcontrib>Corrado, Ilaria</creatorcontrib><creatorcontrib>Lo, Wen-Ting</creatorcontrib><creatorcontrib>Margaria, Jean Piero</creatorcontrib><creatorcontrib>Chen, Anlu</creatorcontrib><creatorcontrib>De Santis, Maria Chiara</creatorcontrib><creatorcontrib>Cnudde, Sophie J</creatorcontrib><creatorcontrib>Fogerty, Joseph</creatorcontrib><creatorcontrib>Yuan, Alex</creatorcontrib><creatorcontrib>Massarotti, Alberto</creatorcontrib><creatorcontrib>Sarijalo, Nasrin Torabi</creatorcontrib><creatorcontrib>Vadas, Oscar</creatorcontrib><creatorcontrib>Williams, Roger L</creatorcontrib><creatorcontrib>Thelen, Marcus</creatorcontrib><creatorcontrib>Powell, David R</creatorcontrib><creatorcontrib>Schueler, Markus</creatorcontrib><creatorcontrib>Wiesener, Michael S</creatorcontrib><creatorcontrib>Balla, Tamas</creatorcontrib><creatorcontrib>Baris, Hagit N</creatorcontrib><creatorcontrib>Tiosano, Dov</creatorcontrib><creatorcontrib>McDermott, Jr, Brian M</creatorcontrib><creatorcontrib>Perkins, Brian D</creatorcontrib><creatorcontrib>Ghigo, Alessandra</creatorcontrib><creatorcontrib>Martini, Miriam</creatorcontrib><creatorcontrib>Haucke, Volker</creatorcontrib><creatorcontrib>Boura, Evzen</creatorcontrib><creatorcontrib>Merlo, Giorgio Roberto</creatorcontrib><creatorcontrib>Buchner, David A</creatorcontrib><creatorcontrib>Hirsch, Emilio</creatorcontrib><title>PI(3,4)P2-mediated cytokinetic abscission prevents early senescence and cataract formation</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Cytokinetic membrane abscission is a spatially and temporally regulated process that requires ESCRT (endosomal sorting complexes required for transport)–dependent control of membrane remodeling at the midbody, a subcellular organelle that defines the cleavage site. Alteration of ESCRT function can lead to cataract, but the underlying mechanism and its relation to cytokinesis are unclear. We found a lens-specific cytokinetic process that required PI3K-C2α (phosphatidylinositol-4-phosphate 3-kinase catalytic subunit type 2α), its lipid product PI(3,4)P
(phosphatidylinositol 3,4-bisphosphate), and the PI(3,4)P
–binding ESCRT-II subunit VPS36 (vacuolar protein-sorting-associated protein 36). Loss of each of these components led to impaired cytokinesis, triggering premature senescence in the lens of fish, mice, and humans. Thus, an evolutionarily conserved pathway underlies the cell type–specific control of cytokinesis that helps to prevent early onset cataract by protecting from senescence.</description><subject>1-Phosphatidylinositol 3-kinase</subject><subject>Abscission</subject><subject>Age</subject><subject>Aging</subject><subject>Aging, Premature</subject><subject>Animals</subject><subject>Binding</subject><subject>Biological Evolution</subject><subject>Calcium-Binding Proteins - metabolism</subject><subject>Cataract - metabolism</subject><subject>Cataract - pathology</subject><subject>Cataracts</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Cell division</subject><subject>Cell Line</subject><subject>Cellular Senescence</subject><subject>Contractility</subject><subject>Cytokinesis</subject><subject>Degenerative diseases</subject><subject>Endosomal Sorting Complexes Required for Transport - metabolism</subject><subject>Enucleation</subject><subject>Evolution</subject><subject>Eye (anatomy)</subject><subject>Eye lens</subject><subject>Fish</subject><subject>Genomic instability</subject><subject>Geriatrics</subject><subject>Humans</subject><subject>INK4a protein</subject><subject>Kinases</subject><subject>Lens, Crystalline - cytology</subject><subject>Lens, Crystalline - growth & development</subject><subject>Lens, Crystalline - metabolism</subject><subject>Lenses</subject><subject>Lipid kinase</subject><subject>Lipids</subject><subject>Membrane fusion</subject><subject>Membranes</subject><subject>Mice</subject><subject>Mitosis</subject><subject>Mutation</subject><subject>Older people</subject><subject>p16 Protein</subject><subject>Pathogenesis</subject><subject>Phosphatidylinositol 3-Kinases - genetics</subject><subject>Phosphatidylinositol 3-Kinases - metabolism</subject><subject>Phosphatidylinositol 4,5-Diphosphate - metabolism</subject><subject>Phosphatidylinositols - metabolism</subject><subject>Protein transport</subject><subject>Proteins</subject><subject>Senescence</subject><subject>Transcription activation</subject><subject>Tubulin - metabolism</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><subject>Zebrafish Proteins - genetics</subject><subject>Zebrafish Proteins - 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cytokinetic abscission prevents early senescence and cataract formation</title><author>Gulluni, Federico ; Prever, Lorenzo ; Li, Huayi ; Krafcikova, Petra ; Corrado, Ilaria ; Lo, Wen-Ting ; Margaria, Jean Piero ; Chen, Anlu ; De Santis, Maria Chiara ; Cnudde, Sophie J ; Fogerty, Joseph ; Yuan, Alex ; Massarotti, Alberto ; Sarijalo, Nasrin Torabi ; Vadas, Oscar ; Williams, Roger L ; Thelen, Marcus ; Powell, David R ; Schueler, Markus ; Wiesener, Michael S ; Balla, Tamas ; Baris, Hagit N ; Tiosano, Dov ; McDermott, Jr, Brian M ; Perkins, Brian D ; Ghigo, Alessandra ; Martini, Miriam ; Haucke, Volker ; Boura, Evzen ; Merlo, Giorgio Roberto ; Buchner, David A ; Hirsch, Emilio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c421t-736d090c468f31cedc4698e10fb3840e6cf09586a5e99cf6d0b411188ba600603</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>1-Phosphatidylinositol 3-kinase</topic><topic>Abscission</topic><topic>Age</topic><topic>Aging</topic><topic>Aging, Premature</topic><topic>Animals</topic><topic>Binding</topic><topic>Biological Evolution</topic><topic>Calcium-Binding Proteins - metabolism</topic><topic>Cataract - metabolism</topic><topic>Cataract - pathology</topic><topic>Cataracts</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Cell division</topic><topic>Cell Line</topic><topic>Cellular Senescence</topic><topic>Contractility</topic><topic>Cytokinesis</topic><topic>Degenerative diseases</topic><topic>Endosomal Sorting Complexes Required for Transport - metabolism</topic><topic>Enucleation</topic><topic>Evolution</topic><topic>Eye (anatomy)</topic><topic>Eye lens</topic><topic>Fish</topic><topic>Genomic instability</topic><topic>Geriatrics</topic><topic>Humans</topic><topic>INK4a protein</topic><topic>Kinases</topic><topic>Lens, Crystalline - cytology</topic><topic>Lens, Crystalline - growth & development</topic><topic>Lens, 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gulluni, Federico</au><au>Prever, Lorenzo</au><au>Li, Huayi</au><au>Krafcikova, Petra</au><au>Corrado, Ilaria</au><au>Lo, Wen-Ting</au><au>Margaria, Jean Piero</au><au>Chen, Anlu</au><au>De Santis, Maria Chiara</au><au>Cnudde, Sophie J</au><au>Fogerty, Joseph</au><au>Yuan, Alex</au><au>Massarotti, Alberto</au><au>Sarijalo, Nasrin Torabi</au><au>Vadas, Oscar</au><au>Williams, Roger L</au><au>Thelen, Marcus</au><au>Powell, David R</au><au>Schueler, Markus</au><au>Wiesener, Michael S</au><au>Balla, Tamas</au><au>Baris, Hagit N</au><au>Tiosano, Dov</au><au>McDermott, Jr, Brian M</au><au>Perkins, Brian D</au><au>Ghigo, Alessandra</au><au>Martini, Miriam</au><au>Haucke, Volker</au><au>Boura, Evzen</au><au>Merlo, Giorgio Roberto</au><au>Buchner, David A</au><au>Hirsch, Emilio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>PI(3,4)P2-mediated cytokinetic abscission prevents early senescence and cataract formation</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2021-12-10</date><risdate>2021</risdate><volume>374</volume><issue>6573</issue><spage>eabk0410</spage><epage>eabk0410</epage><pages>eabk0410-eabk0410</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><abstract>Cytokinetic membrane abscission is a spatially and temporally regulated process that requires ESCRT (endosomal sorting complexes required for transport)–dependent control of membrane remodeling at the midbody, a subcellular organelle that defines the cleavage site. Alteration of ESCRT function can lead to cataract, but the underlying mechanism and its relation to cytokinesis are unclear. We found a lens-specific cytokinetic process that required PI3K-C2α (phosphatidylinositol-4-phosphate 3-kinase catalytic subunit type 2α), its lipid product PI(3,4)P
(phosphatidylinositol 3,4-bisphosphate), and the PI(3,4)P
–binding ESCRT-II subunit VPS36 (vacuolar protein-sorting-associated protein 36). Loss of each of these components led to impaired cytokinesis, triggering premature senescence in the lens of fish, mice, and humans. Thus, an evolutionarily conserved pathway underlies the cell type–specific control of cytokinesis that helps to prevent early onset cataract by protecting from senescence.</abstract><cop>United States</cop><pub>The American Association for the Advancement of Science</pub><pmid>34882480</pmid><doi>10.1126/science.abk0410</doi><orcidid>https://orcid.org/0000-0003-3920-4871</orcidid><orcidid>https://orcid.org/0000-0002-4262-946X</orcidid><orcidid>https://orcid.org/0000-0002-2435-7499</orcidid><orcidid>https://orcid.org/0000-0001-7754-4207</orcidid><orcidid>https://orcid.org/0000-0003-0191-8035</orcidid><orcidid>https://orcid.org/0000-0002-9073-6024</orcidid><orcidid>https://orcid.org/0000-0002-1193-5296</orcidid><orcidid>https://orcid.org/0000-0001-8072-388X</orcidid><orcidid>https://orcid.org/0000-0002-3443-1605</orcidid><orcidid>https://orcid.org/0000-0001-9306-8845</orcidid><orcidid>https://orcid.org/0000-0003-4065-7560</orcidid><orcidid>https://orcid.org/0000-0003-2785-0665</orcidid><orcidid>https://orcid.org/0000-0003-3121-2471</orcidid><orcidid>https://orcid.org/0000-0001-5244-9211</orcidid><orcidid>https://orcid.org/0000-0001-7904-6834</orcidid><orcidid>https://orcid.org/0000-0003-3511-6479</orcidid><orcidid>https://orcid.org/0000-0002-3363-2499</orcidid><orcidid>https://orcid.org/0000-0001-7706-1635</orcidid><orcidid>https://orcid.org/0000-0002-9652-4065</orcidid><orcidid>https://orcid.org/0000-0002-9348-6542</orcidid><orcidid>https://orcid.org/0000-0003-0151-6247</orcidid><orcidid>https://orcid.org/0000-0003-3119-6993</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0036-8075 |
| ispartof | Science (American Association for the Advancement of Science), 2021-12, Vol.374 (6573), p.eabk0410-eabk0410 |
| issn | 0036-8075 1095-9203 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7612254 |
| source | American Association for the Advancement of Science; MEDLINE |
| subjects | 1-Phosphatidylinositol 3-kinase Abscission Age Aging Aging, Premature Animals Binding Biological Evolution Calcium-Binding Proteins - metabolism Cataract - metabolism Cataract - pathology Cataracts Cell Cycle Proteins - metabolism Cell division Cell Line Cellular Senescence Contractility Cytokinesis Degenerative diseases Endosomal Sorting Complexes Required for Transport - metabolism Enucleation Evolution Eye (anatomy) Eye lens Fish Genomic instability Geriatrics Humans INK4a protein Kinases Lens, Crystalline - cytology Lens, Crystalline - growth & development Lens, Crystalline - metabolism Lenses Lipid kinase Lipids Membrane fusion Membranes Mice Mitosis Mutation Older people p16 Protein Pathogenesis Phosphatidylinositol 3-Kinases - genetics Phosphatidylinositol 3-Kinases - metabolism Phosphatidylinositol 4,5-Diphosphate - metabolism Phosphatidylinositols - metabolism Protein transport Proteins Senescence Transcription activation Tubulin - metabolism Vertebrates Zebrafish Zebrafish Proteins - genetics Zebrafish Proteins - metabolism |
| title | PI(3,4)P2-mediated cytokinetic abscission prevents early senescence and cataract formation |
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