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Cooperation between Paxillin-like Protein Pxl1 and Glucan Synthase Bgs1 Is Essential for Actomyosin Ring Stability and Septum Formation in Fission Yeast
In fungal cells cytokinesis requires coordinated closure of a contractile actomyosin ring (CAR) and synthesis of a special cell wall structure known as the division septum. Many CAR proteins have been identified and characterized, but how these molecules interact with the septum synthesis enzymes to...
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Published in: | PLoS genetics 2015-07, Vol.11 (7), p.e1005358 |
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description | In fungal cells cytokinesis requires coordinated closure of a contractile actomyosin ring (CAR) and synthesis of a special cell wall structure known as the division septum. Many CAR proteins have been identified and characterized, but how these molecules interact with the septum synthesis enzymes to form the septum remains unclear. Our genetic study using fission yeast shows that cooperation between the paxillin homolog Pxl1, required for ring integrity, and Bgs1, the enzyme responsible for linear β(1,3)glucan synthesis and primary septum formation, is required for stable anchorage of the CAR to the plasma membrane before septation onset, and for cleavage furrow formation. Thus, lack of Pxl1 in combination with Bgs1 depletion, causes failure of ring contraction and lateral cell wall overgrowth towards the cell lumen without septum formation. We also describe here that Pxl1 concentration at the CAR increases during cytokinesis and that this increase depends on the SH3 domain of the F-BAR protein Cdc15. In consequence, Bgs1 depletion in cells carrying a cdc15ΔSH3 allele causes ring disassembly and septation blockage, as it does in cells lacking Pxl1. On the other hand, the absence of Pxl1 is lethal when Cdc15 function is affected, generating a large sliding of the CAR with deposition of septum wall material along the cell cortex, and suggesting additional functions for both Pxl1 and Cdc15 proteins. In conclusion, our findings indicate that CAR anchorage to the plasma membrane through Cdc15 and Pxl1, and concomitant Bgs1 activity, are necessary for CAR maintenance and septum formation in fission yeast. |
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Many CAR proteins have been identified and characterized, but how these molecules interact with the septum synthesis enzymes to form the septum remains unclear. Our genetic study using fission yeast shows that cooperation between the paxillin homolog Pxl1, required for ring integrity, and Bgs1, the enzyme responsible for linear β(1,3)glucan synthesis and primary septum formation, is required for stable anchorage of the CAR to the plasma membrane before septation onset, and for cleavage furrow formation. Thus, lack of Pxl1 in combination with Bgs1 depletion, causes failure of ring contraction and lateral cell wall overgrowth towards the cell lumen without septum formation. We also describe here that Pxl1 concentration at the CAR increases during cytokinesis and that this increase depends on the SH3 domain of the F-BAR protein Cdc15. In consequence, Bgs1 depletion in cells carrying a cdc15ΔSH3 allele causes ring disassembly and septation blockage, as it does in cells lacking Pxl1. On the other hand, the absence of Pxl1 is lethal when Cdc15 function is affected, generating a large sliding of the CAR with deposition of septum wall material along the cell cortex, and suggesting additional functions for both Pxl1 and Cdc15 proteins. In conclusion, our findings indicate that CAR anchorage to the plasma membrane through Cdc15 and Pxl1, and concomitant Bgs1 activity, are necessary for CAR maintenance and septum formation in fission yeast.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005358</identifier><identifier>PMID: 26132084</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Actin Cytoskeleton - metabolism ; Actomyosin - chemistry ; Actomyosin - metabolism ; beta-Glucans - metabolism ; Cell Cycle Proteins - genetics ; Cell Cycle Proteins - metabolism ; Cell Membrane - metabolism ; Cell Surface Extensions - metabolism ; Cell Wall - metabolism ; Cooperation ; Cytokinesis - genetics ; Cytokinesis - physiology ; Cytoskeletal Proteins - genetics ; Cytoskeletal Proteins - metabolism ; Enzymes ; Glucosyltransferases - genetics ; Glucosyltransferases - metabolism ; GTP-Binding Proteins - genetics ; GTP-Binding Proteins - metabolism ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Paxillin - metabolism ; Protein Structure, Tertiary ; Proteins ; Schizosaccharomyces - genetics ; Schizosaccharomyces - metabolism ; Schizosaccharomyces pombe Proteins - genetics ; Schizosaccharomyces pombe Proteins - metabolism ; Time series ; Yeast</subject><ispartof>PLoS genetics, 2015-07, Vol.11 (7), p.e1005358</ispartof><rights>2015 G. Cortés et al 2015 G. Cortés et al</rights><rights>2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: G. Cortés JC, Pujol N, Sato M, Pinar M, Ramos M, Moreno B, et al. (2015) Cooperation between Paxillin-like Protein Pxl1 and Glucan Synthase Bgs1 Is Essential for Actomyosin Ring Stability and Septum Formation in Fission Yeast. PLoS Genet 11(7): e1005358. doi:10.1371/journal.pgen.1005358</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c531t-be3e1decdbf0e2e80310e780271a1c1e16930f5fa4f575d67fc1b4aa8aa6c4043</citedby><cites>FETCH-LOGICAL-c531t-be3e1decdbf0e2e80310e780271a1c1e16930f5fa4f575d67fc1b4aa8aa6c4043</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/PMC4489101/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4489101/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26132084$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gould, Kathleen L</contributor><creatorcontrib>Cortés, Juan C G</creatorcontrib><creatorcontrib>Pujol, Nuria</creatorcontrib><creatorcontrib>Sato, Mamiko</creatorcontrib><creatorcontrib>Pinar, Mario</creatorcontrib><creatorcontrib>Ramos, Mariona</creatorcontrib><creatorcontrib>Moreno, Belén</creatorcontrib><creatorcontrib>Osumi, Masako</creatorcontrib><creatorcontrib>Ribas, Juan Carlos</creatorcontrib><creatorcontrib>Pérez, Pilar</creatorcontrib><title>Cooperation between Paxillin-like Protein Pxl1 and Glucan Synthase Bgs1 Is Essential for Actomyosin Ring Stability and Septum Formation in Fission Yeast</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>In fungal cells cytokinesis requires coordinated closure of a contractile actomyosin ring (CAR) and synthesis of a special cell wall structure known as the division septum. Many CAR proteins have been identified and characterized, but how these molecules interact with the septum synthesis enzymes to form the septum remains unclear. Our genetic study using fission yeast shows that cooperation between the paxillin homolog Pxl1, required for ring integrity, and Bgs1, the enzyme responsible for linear β(1,3)glucan synthesis and primary septum formation, is required for stable anchorage of the CAR to the plasma membrane before septation onset, and for cleavage furrow formation. Thus, lack of Pxl1 in combination with Bgs1 depletion, causes failure of ring contraction and lateral cell wall overgrowth towards the cell lumen without septum formation. We also describe here that Pxl1 concentration at the CAR increases during cytokinesis and that this increase depends on the SH3 domain of the F-BAR protein Cdc15. In consequence, Bgs1 depletion in cells carrying a cdc15ΔSH3 allele causes ring disassembly and septation blockage, as it does in cells lacking Pxl1. On the other hand, the absence of Pxl1 is lethal when Cdc15 function is affected, generating a large sliding of the CAR with deposition of septum wall material along the cell cortex, and suggesting additional functions for both Pxl1 and Cdc15 proteins. In conclusion, our findings indicate that CAR anchorage to the plasma membrane through Cdc15 and Pxl1, and concomitant Bgs1 activity, are necessary for CAR maintenance and septum formation in fission yeast.</description><subject>Actin Cytoskeleton - metabolism</subject><subject>Actomyosin - chemistry</subject><subject>Actomyosin - metabolism</subject><subject>beta-Glucans - metabolism</subject><subject>Cell Cycle Proteins - genetics</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Cell Membrane - metabolism</subject><subject>Cell Surface Extensions - metabolism</subject><subject>Cell Wall - metabolism</subject><subject>Cooperation</subject><subject>Cytokinesis - genetics</subject><subject>Cytokinesis - physiology</subject><subject>Cytoskeletal Proteins - genetics</subject><subject>Cytoskeletal Proteins - metabolism</subject><subject>Enzymes</subject><subject>Glucosyltransferases - genetics</subject><subject>Glucosyltransferases - metabolism</subject><subject>GTP-Binding Proteins - genetics</subject><subject>GTP-Binding Proteins - metabolism</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Paxillin - metabolism</subject><subject>Protein Structure, Tertiary</subject><subject>Proteins</subject><subject>Schizosaccharomyces - genetics</subject><subject>Schizosaccharomyces - metabolism</subject><subject>Schizosaccharomyces pombe Proteins - genetics</subject><subject>Schizosaccharomyces pombe Proteins - metabolism</subject><subject>Time series</subject><subject>Yeast</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNpVUttuEzEQXSEQLYU_QOAf2GCv7b28IJWoaSNVoiLwwJM1653dOnjtyHag-RM-t5smrdonj2bOZTw6WfaR0RnjFfuy9tvgwM42A7oZo1RyWb_KTpmUPK8EFa-f1SfZuxjXlE6QpnqbnRQl4wWtxWn2f-79BgMk4x1pMf1DdOQG7oy1xuXW_EFyE3xCM3XvLCPgOnJptxocWe1cuoWI5NsQGVlGchEjumTAkt4Hcq6TH3c-Tswfxg1klaA11qTdg8YKN2k7koUP48F7gi1MjPvyN0JM77M3PdiIH47vWfZrcfFzfpVff79czs-vcy05S3mLHFmHumt7igXWlDOKVU2LigHTDFnZcNrLHkQvK9mVVa9ZKwBqgFJPl-Fn2eeD7sb6qI5HjYpVBRVlXTdsQiwPiM7DWm2CGSHslAejHho-DApCMtqiknUJVHaiEUUlRFu0wNpG9x2VUHay6Catr0e3bTtip6d7BbAvRF9OnLlVg_-rhJhWoftlxEFABx9jwP6Jy6ja5-LxC2qfC3XMxUT79Nz3ifQYBH4PS8a6Yw</recordid><startdate>201507</startdate><enddate>201507</enddate><creator>Cortés, Juan C G</creator><creator>Pujol, Nuria</creator><creator>Sato, Mamiko</creator><creator>Pinar, Mario</creator><creator>Ramos, Mariona</creator><creator>Moreno, Belén</creator><creator>Osumi, Masako</creator><creator>Ribas, Juan Carlos</creator><creator>Pérez, Pilar</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>5PM</scope><scope>DOA</scope></search><sort><creationdate>201507</creationdate><title>Cooperation between Paxillin-like Protein Pxl1 and Glucan Synthase Bgs1 Is Essential for Actomyosin Ring Stability and Septum Formation in Fission Yeast</title><author>Cortés, Juan C G ; 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Many CAR proteins have been identified and characterized, but how these molecules interact with the septum synthesis enzymes to form the septum remains unclear. Our genetic study using fission yeast shows that cooperation between the paxillin homolog Pxl1, required for ring integrity, and Bgs1, the enzyme responsible for linear β(1,3)glucan synthesis and primary septum formation, is required for stable anchorage of the CAR to the plasma membrane before septation onset, and for cleavage furrow formation. Thus, lack of Pxl1 in combination with Bgs1 depletion, causes failure of ring contraction and lateral cell wall overgrowth towards the cell lumen without septum formation. We also describe here that Pxl1 concentration at the CAR increases during cytokinesis and that this increase depends on the SH3 domain of the F-BAR protein Cdc15. In consequence, Bgs1 depletion in cells carrying a cdc15ΔSH3 allele causes ring disassembly and septation blockage, as it does in cells lacking Pxl1. On the other hand, the absence of Pxl1 is lethal when Cdc15 function is affected, generating a large sliding of the CAR with deposition of septum wall material along the cell cortex, and suggesting additional functions for both Pxl1 and Cdc15 proteins. In conclusion, our findings indicate that CAR anchorage to the plasma membrane through Cdc15 and Pxl1, and concomitant Bgs1 activity, are necessary for CAR maintenance and septum formation in fission yeast.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26132084</pmid><doi>10.1371/journal.pgen.1005358</doi><oa>free_for_read</oa></addata></record> |
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subjects | Actin Cytoskeleton - metabolism Actomyosin - chemistry Actomyosin - metabolism beta-Glucans - metabolism Cell Cycle Proteins - genetics Cell Cycle Proteins - metabolism Cell Membrane - metabolism Cell Surface Extensions - metabolism Cell Wall - metabolism Cooperation Cytokinesis - genetics Cytokinesis - physiology Cytoskeletal Proteins - genetics Cytoskeletal Proteins - metabolism Enzymes Glucosyltransferases - genetics Glucosyltransferases - metabolism GTP-Binding Proteins - genetics GTP-Binding Proteins - metabolism Membrane Proteins - genetics Membrane Proteins - metabolism Paxillin - metabolism Protein Structure, Tertiary Proteins Schizosaccharomyces - genetics Schizosaccharomyces - metabolism Schizosaccharomyces pombe Proteins - genetics Schizosaccharomyces pombe Proteins - metabolism Time series Yeast |
title | Cooperation between Paxillin-like Protein Pxl1 and Glucan Synthase Bgs1 Is Essential for Actomyosin Ring Stability and Septum Formation in Fission Yeast |
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