The Kin1 kinase and the calcineurin phosphatase cooperate to link actin ring assembly and septum synthesis in fission yeast
Background information The Kin1 protein kinase of fission yeast, which regulates cell surface cohesiveness during interphase cell growth, is also present at the cell division site during mitosis; however, its function in cell division has remained elusive. Results In FK506‐mediated calcineurin defic...
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creator | Cadou, Angela Couturier, Anne Le Goff, Cathy Xie, Linfeng Paulson, James R. Le Goff, Xavier |
description | Background information
The Kin1 protein kinase of fission yeast, which regulates cell surface cohesiveness during interphase cell growth, is also present at the cell division site during mitosis; however, its function in cell division has remained elusive.
Results
In FK506‐mediated calcineurin deficient cells, mitosis is extended and ring formation is transiently compromised but septation remains normal. Here, we show that Kin1 inhibition in these cells leads to polyseptation and defects in membrane closure. Actomyosin ring disassembly is prevented and ultimately the daughter cells fail to separate. We show that the Pmk1 MAP kinase pathway and the type V myosin Myo4 act downstream of the cytokinetic function of Kin1. Kin1 inhibition also promotes polyseptation in myo3Δ, a type II myosin heavy‐chain mutant defective in ring assembly. In contrast, Kin1 inactivation rescues septation in a myosin light‐chain cdc4–8 thermosensitive mutant. A structure/function analysis of the Kin1 protein sequence identified a novel motif outside the kinase domain that is important for its polarised localisation and its catalytic activity. This motif is remarkably conserved in all fungal Kin1 homologues but is absent in related kinases of metazoans.
Conclusions
We conclude that calcineurin and Kin1 activities must be tightly coordinated to link actomyosin ring assembly with septum synthesis and membrane closure and to ensure separation of the daughter cells.
In fission yeast, the function of the Kin1 protein kinase in cell division has remained elusive. In calcineurin phosphatase deficient cells, mitosis is extended and ring formation is transiently compromised but ultimately cell division is completed. Inhibition of Kin1 in these cells impinges on cytokinesis, preventing separation of the daughter cells. Thus, calcineurin and Kin1 activities must be tightly coordinated to link actin ring structure to septation at the end of the cell cycle in fission yeast. |
doi_str_mv | 10.1111/boc.201200042 |
format | Article |
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The Kin1 protein kinase of fission yeast, which regulates cell surface cohesiveness during interphase cell growth, is also present at the cell division site during mitosis; however, its function in cell division has remained elusive.
Results
In FK506‐mediated calcineurin deficient cells, mitosis is extended and ring formation is transiently compromised but septation remains normal. Here, we show that Kin1 inhibition in these cells leads to polyseptation and defects in membrane closure. Actomyosin ring disassembly is prevented and ultimately the daughter cells fail to separate. We show that the Pmk1 MAP kinase pathway and the type V myosin Myo4 act downstream of the cytokinetic function of Kin1. Kin1 inhibition also promotes polyseptation in myo3Δ, a type II myosin heavy‐chain mutant defective in ring assembly. In contrast, Kin1 inactivation rescues septation in a myosin light‐chain cdc4–8 thermosensitive mutant. A structure/function analysis of the Kin1 protein sequence identified a novel motif outside the kinase domain that is important for its polarised localisation and its catalytic activity. This motif is remarkably conserved in all fungal Kin1 homologues but is absent in related kinases of metazoans.
Conclusions
We conclude that calcineurin and Kin1 activities must be tightly coordinated to link actomyosin ring assembly with septum synthesis and membrane closure and to ensure separation of the daughter cells.
In fission yeast, the function of the Kin1 protein kinase in cell division has remained elusive. In calcineurin phosphatase deficient cells, mitosis is extended and ring formation is transiently compromised but ultimately cell division is completed. Inhibition of Kin1 in these cells impinges on cytokinesis, preventing separation of the daughter cells. Thus, calcineurin and Kin1 activities must be tightly coordinated to link actin ring structure to septation at the end of the cell cycle in fission yeast.</description><identifier>ISSN: 0248-4900</identifier><identifier>EISSN: 1768-322X</identifier><identifier>DOI: 10.1111/boc.201200042</identifier><identifier>PMID: 23294323</identifier><language>eng</language><publisher>Hoboken: WILEY-VCH Verlag</publisher><subject>Actins - metabolism ; Amino Acid Motifs ; Amino Acid Sequence ; Calcineurin ; Cancer ; Cell division ; Cell Wall - drug effects ; Cytokinesis ; Cytokinesis - drug effects ; Fungi ; Genetics ; Life Sciences ; Metazoa ; Molecular Sequence Data ; Mutation - genetics ; Myosin Heavy Chains - metabolism ; Phenotype ; Phosphoric Monoester Hydrolases - antagonists & inhibitors ; Phosphoric Monoester Hydrolases - metabolism ; Protein serine/threonine kinase/phosphatase ; Protein Transport - drug effects ; Protein-Serine-Threonine Kinases - antagonists & inhibitors ; Protein-Serine-Threonine Kinases - chemistry ; Protein-Serine-Threonine Kinases - metabolism ; Pyrazoles - pharmacology ; Pyrimidines - pharmacology ; Schizosaccharomyces - cytology ; Schizosaccharomyces - drug effects ; Schizosaccharomyces - enzymology ; Schizosaccharomyces - growth & development ; Schizosaccharomyces pombe ; Schizosaccharomyces pombe Proteins - antagonists & inhibitors ; Schizosaccharomyces pombe Proteins - chemistry ; Schizosaccharomyces pombe Proteins - metabolism ; Tacrolimus - pharmacology</subject><ispartof>Biology of the cell, 2013-03, Vol.105 (3), p.129-148</ispartof><rights>Copyright © 2013 Soçiété Française des Microscopies and Soçiété de Biologie Cellulaire de France</rights><rights>Copyright © 2013 Soçiété Française des Microscopies and Soçiété de Biologie Cellulaire de France.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4492-5cdfa2dc0230872af655097f68630fe38b26e0b25b14c115268ca62d2c2943343</citedby><cites>FETCH-LOGICAL-c4492-5cdfa2dc0230872af655097f68630fe38b26e0b25b14c115268ca62d2c2943343</cites><orcidid>0000-0002-5041-0468</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fboc.201200042$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fboc.201200042$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23294323$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://inserm.hal.science/inserm-00809223$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Cadou, Angela</creatorcontrib><creatorcontrib>Couturier, Anne</creatorcontrib><creatorcontrib>Le Goff, Cathy</creatorcontrib><creatorcontrib>Xie, Linfeng</creatorcontrib><creatorcontrib>Paulson, James R.</creatorcontrib><creatorcontrib>Le Goff, Xavier</creatorcontrib><title>The Kin1 kinase and the calcineurin phosphatase cooperate to link actin ring assembly and septum synthesis in fission yeast</title><title>Biology of the cell</title><addtitle>Biology of the Cell</addtitle><description>Background information
The Kin1 protein kinase of fission yeast, which regulates cell surface cohesiveness during interphase cell growth, is also present at the cell division site during mitosis; however, its function in cell division has remained elusive.
Results
In FK506‐mediated calcineurin deficient cells, mitosis is extended and ring formation is transiently compromised but septation remains normal. Here, we show that Kin1 inhibition in these cells leads to polyseptation and defects in membrane closure. Actomyosin ring disassembly is prevented and ultimately the daughter cells fail to separate. We show that the Pmk1 MAP kinase pathway and the type V myosin Myo4 act downstream of the cytokinetic function of Kin1. Kin1 inhibition also promotes polyseptation in myo3Δ, a type II myosin heavy‐chain mutant defective in ring assembly. In contrast, Kin1 inactivation rescues septation in a myosin light‐chain cdc4–8 thermosensitive mutant. A structure/function analysis of the Kin1 protein sequence identified a novel motif outside the kinase domain that is important for its polarised localisation and its catalytic activity. This motif is remarkably conserved in all fungal Kin1 homologues but is absent in related kinases of metazoans.
Conclusions
We conclude that calcineurin and Kin1 activities must be tightly coordinated to link actomyosin ring assembly with septum synthesis and membrane closure and to ensure separation of the daughter cells.
In fission yeast, the function of the Kin1 protein kinase in cell division has remained elusive. In calcineurin phosphatase deficient cells, mitosis is extended and ring formation is transiently compromised but ultimately cell division is completed. Inhibition of Kin1 in these cells impinges on cytokinesis, preventing separation of the daughter cells. Thus, calcineurin and Kin1 activities must be tightly coordinated to link actin ring structure to septation at the end of the cell cycle in fission yeast.</description><subject>Actins - metabolism</subject><subject>Amino Acid Motifs</subject><subject>Amino Acid Sequence</subject><subject>Calcineurin</subject><subject>Cancer</subject><subject>Cell division</subject><subject>Cell Wall - drug effects</subject><subject>Cytokinesis</subject><subject>Cytokinesis - drug effects</subject><subject>Fungi</subject><subject>Genetics</subject><subject>Life Sciences</subject><subject>Metazoa</subject><subject>Molecular Sequence Data</subject><subject>Mutation - genetics</subject><subject>Myosin Heavy Chains - metabolism</subject><subject>Phenotype</subject><subject>Phosphoric Monoester Hydrolases - antagonists & inhibitors</subject><subject>Phosphoric Monoester Hydrolases - metabolism</subject><subject>Protein serine/threonine kinase/phosphatase</subject><subject>Protein Transport - drug effects</subject><subject>Protein-Serine-Threonine Kinases - antagonists & inhibitors</subject><subject>Protein-Serine-Threonine Kinases - chemistry</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Pyrazoles - pharmacology</subject><subject>Pyrimidines - pharmacology</subject><subject>Schizosaccharomyces - cytology</subject><subject>Schizosaccharomyces - drug effects</subject><subject>Schizosaccharomyces - enzymology</subject><subject>Schizosaccharomyces - growth & development</subject><subject>Schizosaccharomyces pombe</subject><subject>Schizosaccharomyces pombe Proteins - antagonists & inhibitors</subject><subject>Schizosaccharomyces pombe Proteins - chemistry</subject><subject>Schizosaccharomyces pombe Proteins - metabolism</subject><subject>Tacrolimus - pharmacology</subject><issn>0248-4900</issn><issn>1768-322X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqF0U2P0zAQBmALgdiycOSKfORAlvE4n8elgl2gYoVUBOJiOa5DTRM7m0mAiD-PS0vFCXyxZD9-NdbL2GMBFyKu53UwFwgCASDFO2whirxMJOKnu2wBmJZJWgGcsQdEX_ekKrP77AwlVqlEuWA_11vL3zov-M55TZZrv-FjPDO6Nc7baXCe99tA_VaP-3sTQm8HPVo-Bt46v-PajNFE94VrItvV7fw7hWw_Th2n2cc8csSjahyRC57PVtP4kN1rdEv20XE_Zx9evVwvr5PVzdXr5eUqMWlaYZKZTaNxYwAllAXqJs8yqIomL3MJjZVljbmFGrNapEaIDPPS6Bw3aPaflKk8Z88OuVvdqn5wnR5mFbRT15cr5TzZoVMAJVSI8puI_OmB90O4nSyNqnNkbNtqb8NESmQ5CFmIqvo_lSJOIEFApMmBmiEQDbY5TSJA7ZtUsUl1ajL6J8foqe7s5qT_VBdBcQDfXWvnf6epFzfLv6OPozga7Y_TSz3sVF7IIlMf313FkPRN8Vm8V2v5CxgNt5Q</recordid><startdate>201303</startdate><enddate>201303</enddate><creator>Cadou, Angela</creator><creator>Couturier, Anne</creator><creator>Le Goff, Cathy</creator><creator>Xie, Linfeng</creator><creator>Paulson, James R.</creator><creator>Le Goff, Xavier</creator><general>WILEY-VCH Verlag</general><general>WILEY‐VCH Verlag</general><general>Wiley</general><scope>BSCLL</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>7X8</scope><scope>M7N</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-5041-0468</orcidid></search><sort><creationdate>201303</creationdate><title>The Kin1 kinase and the calcineurin phosphatase cooperate to link actin ring assembly and septum synthesis in fission yeast</title><author>Cadou, Angela ; Couturier, Anne ; Le Goff, Cathy ; Xie, Linfeng ; Paulson, James R. ; Le Goff, Xavier</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4492-5cdfa2dc0230872af655097f68630fe38b26e0b25b14c115268ca62d2c2943343</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Actins - metabolism</topic><topic>Amino Acid Motifs</topic><topic>Amino Acid Sequence</topic><topic>Calcineurin</topic><topic>Cancer</topic><topic>Cell division</topic><topic>Cell Wall - drug effects</topic><topic>Cytokinesis</topic><topic>Cytokinesis - drug effects</topic><topic>Fungi</topic><topic>Genetics</topic><topic>Life Sciences</topic><topic>Metazoa</topic><topic>Molecular Sequence Data</topic><topic>Mutation - genetics</topic><topic>Myosin Heavy Chains - metabolism</topic><topic>Phenotype</topic><topic>Phosphoric Monoester Hydrolases - antagonists & inhibitors</topic><topic>Phosphoric Monoester Hydrolases - metabolism</topic><topic>Protein serine/threonine kinase/phosphatase</topic><topic>Protein Transport - drug effects</topic><topic>Protein-Serine-Threonine Kinases - antagonists & inhibitors</topic><topic>Protein-Serine-Threonine Kinases - chemistry</topic><topic>Protein-Serine-Threonine Kinases - metabolism</topic><topic>Pyrazoles - pharmacology</topic><topic>Pyrimidines - pharmacology</topic><topic>Schizosaccharomyces - cytology</topic><topic>Schizosaccharomyces - drug effects</topic><topic>Schizosaccharomyces - enzymology</topic><topic>Schizosaccharomyces - growth & development</topic><topic>Schizosaccharomyces pombe</topic><topic>Schizosaccharomyces pombe Proteins - antagonists & inhibitors</topic><topic>Schizosaccharomyces pombe Proteins - chemistry</topic><topic>Schizosaccharomyces pombe Proteins - metabolism</topic><topic>Tacrolimus - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cadou, Angela</creatorcontrib><creatorcontrib>Couturier, Anne</creatorcontrib><creatorcontrib>Le Goff, Cathy</creatorcontrib><creatorcontrib>Xie, Linfeng</creatorcontrib><creatorcontrib>Paulson, James R.</creatorcontrib><creatorcontrib>Le Goff, Xavier</creatorcontrib><collection>Istex</collection><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>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Biology of the cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cadou, Angela</au><au>Couturier, Anne</au><au>Le Goff, Cathy</au><au>Xie, Linfeng</au><au>Paulson, James R.</au><au>Le Goff, Xavier</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Kin1 kinase and the calcineurin phosphatase cooperate to link actin ring assembly and septum synthesis in fission yeast</atitle><jtitle>Biology of the cell</jtitle><addtitle>Biology of the Cell</addtitle><date>2013-03</date><risdate>2013</risdate><volume>105</volume><issue>3</issue><spage>129</spage><epage>148</epage><pages>129-148</pages><issn>0248-4900</issn><eissn>1768-322X</eissn><abstract>Background information
The Kin1 protein kinase of fission yeast, which regulates cell surface cohesiveness during interphase cell growth, is also present at the cell division site during mitosis; however, its function in cell division has remained elusive.
Results
In FK506‐mediated calcineurin deficient cells, mitosis is extended and ring formation is transiently compromised but septation remains normal. Here, we show that Kin1 inhibition in these cells leads to polyseptation and defects in membrane closure. Actomyosin ring disassembly is prevented and ultimately the daughter cells fail to separate. We show that the Pmk1 MAP kinase pathway and the type V myosin Myo4 act downstream of the cytokinetic function of Kin1. Kin1 inhibition also promotes polyseptation in myo3Δ, a type II myosin heavy‐chain mutant defective in ring assembly. In contrast, Kin1 inactivation rescues septation in a myosin light‐chain cdc4–8 thermosensitive mutant. A structure/function analysis of the Kin1 protein sequence identified a novel motif outside the kinase domain that is important for its polarised localisation and its catalytic activity. This motif is remarkably conserved in all fungal Kin1 homologues but is absent in related kinases of metazoans.
Conclusions
We conclude that calcineurin and Kin1 activities must be tightly coordinated to link actomyosin ring assembly with septum synthesis and membrane closure and to ensure separation of the daughter cells.
In fission yeast, the function of the Kin1 protein kinase in cell division has remained elusive. In calcineurin phosphatase deficient cells, mitosis is extended and ring formation is transiently compromised but ultimately cell division is completed. Inhibition of Kin1 in these cells impinges on cytokinesis, preventing separation of the daughter cells. Thus, calcineurin and Kin1 activities must be tightly coordinated to link actin ring structure to septation at the end of the cell cycle in fission yeast.</abstract><cop>Hoboken</cop><pub>WILEY-VCH Verlag</pub><pmid>23294323</pmid><doi>10.1111/boc.201200042</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0002-5041-0468</orcidid></addata></record> |
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subjects | Actins - metabolism Amino Acid Motifs Amino Acid Sequence Calcineurin Cancer Cell division Cell Wall - drug effects Cytokinesis Cytokinesis - drug effects Fungi Genetics Life Sciences Metazoa Molecular Sequence Data Mutation - genetics Myosin Heavy Chains - metabolism Phenotype Phosphoric Monoester Hydrolases - antagonists & inhibitors Phosphoric Monoester Hydrolases - metabolism Protein serine/threonine kinase/phosphatase Protein Transport - drug effects Protein-Serine-Threonine Kinases - antagonists & inhibitors Protein-Serine-Threonine Kinases - chemistry Protein-Serine-Threonine Kinases - metabolism Pyrazoles - pharmacology Pyrimidines - pharmacology Schizosaccharomyces - cytology Schizosaccharomyces - drug effects Schizosaccharomyces - enzymology Schizosaccharomyces - growth & development Schizosaccharomyces pombe Schizosaccharomyces pombe Proteins - antagonists & inhibitors Schizosaccharomyces pombe Proteins - chemistry Schizosaccharomyces pombe Proteins - metabolism Tacrolimus - pharmacology |
title | The Kin1 kinase and the calcineurin phosphatase cooperate to link actin ring assembly and septum synthesis in fission yeast |
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