Human chromosome segregation involves multi-layered regulation of separase by the peptidyl-prolyl-isomerase Pin1
Ring shaped cohesin keeps sister chromatids paired until cleavage of its Scc1/Rad21 subunit by separase triggers chromosome segregation in anaphase. Vertebrate separase is held inactive by mutually exclusive binding to securin or Cdk1-cyclin B1 and becomes unleashed only upon ubiquitin dependent deg...
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| Published in | Molecular cell Vol. 58; no. 3; pp. 495 - 506 |
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| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier Inc
07.05.2015
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| Abstract | Ring shaped cohesin keeps sister chromatids paired until cleavage of its Scc1/Rad21 subunit by separase triggers chromosome segregation in anaphase. Vertebrate separase is held inactive by mutually exclusive binding to securin or Cdk1-cyclin B1 and becomes unleashed only upon ubiquitin dependent degradation of these regulators. Although most separase is usually found in association with securin, this anaphase inhibitor is dispensable for murine life while Cdk1-cyclin B1 dependent control of separase is essential. Here, we show that securin independent inhibition of separase by Cdk1-cyclin B1 in early mitosis requires the phosphorylation specific peptidyl-prolyl cis/trans isomerase Pin1. Furthermore, isomerization of previously securin bound separase at the metaphase-to-anaphase transition renders it resistant to re-inhibition by residual securin. At the same time, isomerization also limits the half-life of separase's proteolytic activity, explaining how cohesin can be reloaded onto telophase chromatin in the absence of securin and cyclin B1 without being cleaved.
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•Separase is subject to native-state cis/trans isomerization by Pin1•Once liberated, separase is rendered resistant to remaining securin by Pin1•When securin is limiting, Pin1 is required for control of separase by Cdk1-cyclin B1•Isomerization limits the half-life of separase's proteolytic activity in late mitosis |
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| AbstractList | Ring shaped cohesin keeps sister chromatids paired until cleavage of its Scc1/Rad21 subunit by separase triggers chromosome segregation in anaphase. Vertebrate separase is held inactive by mutually exclusive binding to securin or Cdk1-cyclin B1 and becomes unleashed only upon ubiquitin dependent degradation of these regulators. Although most separase is usually found in association with securin, this anaphase inhibitor is dispensable for murine life while Cdk1-cyclin B1 dependent control of separase is essential. Here, we show that securin independent inhibition of separase by Cdk1-cyclin B1 in early mitosis requires the phosphorylation specific peptidyl-prolyl cis/trans isomerase Pin1. Furthermore, isomerization of previously securin bound separase at the metaphase-to-anaphase transition renders it resistant to re-inhibition by residual securin. At the same time, isomerization also limits the half-life of separase's proteolytic activity, explaining how cohesin can be reloaded onto telophase chromatin in the absence of securin and cyclin B1 without being cleaved.
[Display omitted]
•Separase is subject to native-state cis/trans isomerization by Pin1•Once liberated, separase is rendered resistant to remaining securin by Pin1•When securin is limiting, Pin1 is required for control of separase by Cdk1-cyclin B1•Isomerization limits the half-life of separase's proteolytic activity in late mitosis Ring-shaped cohesin keeps sister chromatids paired until cleavage of its Scc1/Rad21 subunit by separase triggers chromosome segregation in anaphase. Vertebrate separase is held inactive by mutually exclusive binding to securin or Cdk1-cyclin B1 and becomes unleashed only upon ubiquitin-dependent degradation of these regulators. Although most separase is usually found in association with securin, this anaphase inhibitor is dispensable for murine life while Cdk1-cyclin B1-dependent control of separase is essential. Here, we show that securin-independent inhibition of separase by Cdk1-cyclin B1 in early mitosis requires the phosphorylation-specific peptidyl-prolyl cis/trans isomerase Pin1. Furthermore, isomerization of previously securin-bound separase at the metaphase-to-anaphase transition renders it resistant to re-inhibition by residual securin. At the same time, isomerization also limits the half-life of separase's proteolytic activity, explaining how cohesin can be reloaded onto telophase chromatin in the absence of securin and cyclin B1 without being cleaved. |
| Author | Heidmann, Stefan Rata, Scott Hellmuth, Susanne Novak, Bela Brown, Andreas Stemmann, Olaf |
| Author_xml | – sequence: 1 givenname: Susanne surname: Hellmuth fullname: Hellmuth, Susanne organization: Chair of Genetics, University of Bayreuth, Universitätsstraße 30, 95440 Bayreuth, Germany – sequence: 2 givenname: Scott surname: Rata fullname: Rata, Scott organization: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK – sequence: 3 givenname: Andreas surname: Brown fullname: Brown, Andreas organization: Chair of Genetics, University of Bayreuth, Universitätsstraße 30, 95440 Bayreuth, Germany – sequence: 4 givenname: Stefan surname: Heidmann fullname: Heidmann, Stefan organization: Chair of Genetics, University of Bayreuth, Universitätsstraße 30, 95440 Bayreuth, Germany – sequence: 5 givenname: Bela surname: Novak fullname: Novak, Bela organization: Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK – sequence: 6 givenname: Olaf surname: Stemmann fullname: Stemmann, Olaf email: olaf.stemmann@uni-bayreuth.de organization: Chair of Genetics, University of Bayreuth, Universitätsstraße 30, 95440 Bayreuth, Germany |
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| Snippet | Ring shaped cohesin keeps sister chromatids paired until cleavage of its Scc1/Rad21 subunit by separase triggers chromosome segregation in anaphase. Vertebrate... Ring-shaped cohesin keeps sister chromatids paired until cleavage of its Scc1/Rad21 subunit by separase triggers chromosome segregation in anaphase. Vertebrate... |
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| SubjectTerms | anaphase Anaphase - genetics CDC2 Protein Kinase chromatids Chromatids - genetics chromatin chromosome segregation Chromosome Segregation - genetics Cyclin B1 - chemistry Cyclin B1 - genetics Cyclin B1 - metabolism Cyclin-Dependent Kinases - chemistry Cyclin-Dependent Kinases - genetics Cyclin-Dependent Kinases - metabolism cyclins enzyme inhibition Gene Expression Regulation, Enzymologic half life HEK293 Cells Humans Immunoblotting isomerases isomerization Metaphase - genetics mice Microscopy, Fluorescence mitosis Mitosis - genetics Models, Genetic Models, Molecular Mutation NIMA-Interacting Peptidylprolyl Isomerase Peptidylprolyl Isomerase - genetics Peptidylprolyl Isomerase - metabolism phosphorylation Protein Binding Protein Conformation proteolysis RNA Interference Securin - genetics Securin - metabolism separase Separase - chemistry Separase - genetics Separase - metabolism telophase ubiquitin |
| Title | Human chromosome segregation involves multi-layered regulation of separase by the peptidyl-prolyl-isomerase Pin1 |
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