The fission yeast S-phase cyclin Cig2 can drive mitosis.


Journal

Genetics
ISSN: 1943-2631
Titre abrégé: Genetics
Pays: United States
ID NLM: 0374636

Informations de publication

Date de publication:
03 03 2021
Historique:
received: 05 10 2020
accepted: 28 10 2020
entrez: 8 3 2021
pubmed: 9 3 2021
medline: 13 8 2021
Statut: ppublish

Résumé

Commitment to mitosis is regulated by cyclin-dependent kinase (CDK) activity. In the fission yeast Schizosaccharomyces pombe, the major B-type cyclin, Cdc13, is necessary and sufficient to drive mitotic entry. Furthermore, Cdc13 is also sufficient to drive S phase, demonstrating that a single cyclin can regulate alternating rounds of replication and mitosis, and providing the foundation of the quantitative model of CDK function. It has been assumed that Cig2, a B-type cyclin expressed only during S phase and incapable of driving mitosis in wild-type cells, was specialized for S-phase regulation. Here, we show that Cig2 is capable of driving mitosis. Cig2/CDK activity drives mitotic catastrophe-lethal mitosis in inviably small cells-in cells that lack CDK inhibition by tyrosine-phosphorylation. Moreover, Cig2/CDK can drive mitosis in the absence of Cdc13/CDK activity and constitutive expression of Cig2 can rescue loss of Cdc13 activity. These results demonstrate that in fission yeast, not only can the presumptive M-phase cyclin drive S phase, but the presumptive S-phase cyclin can drive M phase, further supporting the quantitative model of CDK function. Furthermore, these results provide an explanation, previously proposed on the basis of computational analyses, for the surprising observation that cells expressing a single-chain Cdc13-Cdc2 CDK do not require Y15 phosphorylation for viability. Their viability is due to the fact that in such cells, which lack Cig2/CDK complexes, Cdc13/CDK activity is unable to drive mitotic catastrophe.

Identifiants

pubmed: 33683349
pii: 5974038
doi: 10.1093/genetics/iyaa002
pmc: PMC8045716
doi:

Substances chimiques

Cdc13 protein, S pombe 0
Cig2 protein, S pombe 0
Cyclin B 0
Schizosaccharomyces pombe Proteins 0
Cyclin-Dependent Kinases EC 2.7.11.22

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1-12

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM134300
Pays : United States

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of Genetics Society of America. All rights reserved. For permissions, please email: journals.permissions@oup.com.

Références

EMBO J. 2002 Jul 1;21(13):3370-6
pubmed: 12093738
J Cell Sci Suppl. 1989;12:77-97
pubmed: 2534558
Genome Biol. 2012 May 24;13(5):R36
pubmed: 22624651
J Cell Sci. 1996 Jun;109 ( Pt 6):1647-53
pubmed: 8799851
Cell. 1989 Aug 11;58(3):485-97
pubmed: 2569363
Mol Cell. 1999 Jul;4(1):11-9
pubmed: 10445023
Yeast. 2006 Feb;23(3):173-83
pubmed: 16498704
EMBO J. 1995 May 15;14(10):2166-75
pubmed: 7774574
Yeast. 1998 Jul;14(10):943-51
pubmed: 9717240
Genes Dev. 1997 Feb 15;11(4):504-11
pubmed: 9042863
Genetics. 2016 Dec;204(4):1479-1494
pubmed: 27794027
PLoS Comput Biol. 2015 Feb 06;11(2):e1004056
pubmed: 25658582
Methods Mol Biol. 2011;782:1-12
pubmed: 21870280
Nature. 1990 Apr 5;344(6266):503-8
pubmed: 2138713
Cell. 2016 Dec 15;167(7):1750-1761.e16
pubmed: 27984725
EMBO J. 1993 Sep;12(9):3427-36
pubmed: 7504624
Mol Cell. 2000 Dec;6(6):1377-87
pubmed: 11163211
J Cell Sci. 2012 Oct 15;125(Pt 20):4703-11
pubmed: 23223895
Mol Gen Genet. 1996 Jul 26;251(6):635-46
pubmed: 8757394
J Biol Chem. 1997 May 16;272(20):13320-5
pubmed: 9148953
Nature. 1999 Sep 23;401(6751):394-7
pubmed: 10517640
Nature. 1989 Nov 2;342(6245):39-45
pubmed: 2682257
Curr Biol. 2017 May 22;27(10):1491-1497.e4
pubmed: 28479325
Philos Trans R Soc Lond B Biol Sci. 2011 Dec 27;366(1584):3572-83
pubmed: 22084384
Mol Cell Biol. 1996 Apr;16(4):1527-33
pubmed: 8657126
Trends Cell Biol. 2013 Jul;23(7):345-56
pubmed: 23566594
Mol Cell Biol. 1998 Jul;18(7):3782-7
pubmed: 9632761
Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2579-84
pubmed: 10716991
Mol Biol Cell. 2019 Jan 15;30(2):169-172
pubmed: 30640587
EMBO J. 1996 Feb 15;15(4):850-60
pubmed: 8631306
Nature. 2010 Dec 23;468(7327):1074-9
pubmed: 21179163
Cell Cycle. 2015;14(24):3842-50
pubmed: 26176277
Nature. 2005 Mar 3;434(7029):104-8
pubmed: 15744308
Cell. 1989 Jul 28;58(2):361-72
pubmed: 2665944
Proc Natl Acad Sci U S A. 2005 Jun 21;102(25):8910-5
pubmed: 15956196
Nat Commun. 2017 Oct 10;8(1):816
pubmed: 29018186
Nat Commun. 2015 Apr 20;6:6871
pubmed: 25891897
Curr Biol. 2019 Apr 22;29(8):1379-1386.e4
pubmed: 30955932
Cold Spring Harb Perspect Biol. 2012 Oct 01;4(10):
pubmed: 23028116
Gene. 1993 Jan 15;123(1):131-6
pubmed: 8422997
J Biol Chem. 2004 Apr 30;279(18):18974-80
pubmed: 14970237
Trends Genet. 1996 Sep;12(9):345-50
pubmed: 8855663
Mol Cell Biol. 1993 Apr;13(4):2286-97
pubmed: 8455610
Mol Cell. 2011 Jun 10;42(5):610-23
pubmed: 21658602
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
Mol Cell Biol. 2001 Mar;21(5):1499-508
pubmed: 11238887
EMBO J. 1996 Feb 15;15(4):839-49
pubmed: 8631305
Semin Cell Biol. 1995 Apr;6(2):73-8
pubmed: 7548845
Yeast. 1996 Dec;12(16):1635-46
pubmed: 9123966
Cell. 1994 Oct 21;79(2):233-44
pubmed: 7954792
EMBO J. 1991 Dec;10(13):4301-9
pubmed: 1756737
Yeast. 2000 Jun 30;16(9):857-60
pubmed: 10861908
Cell. 1991 Mar 22;64(6):1111-22
pubmed: 1706223

Auteurs

Mary Pickering (M)

Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA 01605, USA.

Mira Magner (M)

Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA 01605, USA.

Dan Keifenheim (D)

Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA 01605, USA.

Nicholas Rhind (N)

Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA 01605, USA.

Articles similaires

Meiosis Schizosaccharomyces Schizosaccharomyces pombe Proteins Spores, Fungal
Schizosaccharomyces Meiosis Schizosaccharomyces pombe Proteins Mitosis Epigenesis, Genetic

Clr4

Hyun-Soo Kim, Benjamin Roche, Sonali Bhattacharjee et al.
1.00
Schizosaccharomyces pombe Proteins Schizosaccharomyces Heterochromatin Ubiquitination Cell Cycle Proteins
Saccharomyces cerevisiae Proteins Mitosis Saccharomyces cerevisiae Signal Transduction Spindle Pole Bodies

Classifications MeSH