Home LiteratureArticle Details
PMID: 17116692 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Novel role for Cdc14 sequestration: Cdc14 dephosphorylates factors that promote DNA replication.

Molecular and cellular biology ·Vol. 27 ·No. 3 ·2007-02-00 ·Pages 842-53

Bloom J, Cross FR

Abstract

The phosphatase Cdc14 is required for mitotic exit in budding yeast. Cdc14 promotes Cdk1 inactivation by targeting proteins that, when dephosphorylated, trigger degradation of mitotic cyclins and accumulation of the Cdk1 inhibitor, Sic1. Cdc14 is sequestered in the nucleolus during most of the cell cycle but is released into the nucleus and cytoplasm during anaphase. When Cdc14 is not properly sequestered in the nucleolus, expression of the S-phase cyclin Clb5 is required for viability, suggesting that the antagonizing activity of Clb5-dependent Cdk1 specifically is necessary when Cdc14 is delocalized. We show that delocalization of Cdc14 combined with loss of Clb5 causes defects in DNA replication. When Cdc14 is not sequestered, it efficiently dephosphorylates a subset of Cdk1 substrates including the replication factors, Sld2 and Dpb2. Mutations causing Cdc14 mislocalization interact genetically with mutations affecting the function of DNA polymerase epsilon and the S-phase checkpoint protein Mec1. Our findings suggest that Cdc14 is retained in the nucleolus to support a favorable kinase/phosphatase balance while cells are replicating their DNA, in addition to the established role of Cdc14 sequestration in coordinating nuclear segregation with mitotic exit.

MeSH Terms
CDC2 Protein Kinase/metabolism Cell Cycle Proteins/metabolism Cyclin B/metabolism DNA Polymerase II/genetics,metabolism DNA Replication Gene Deletion Genes, Fungal Green Fluorescent Proteins/metabolism Intracellular Signaling Peptides and Proteins Mutation/genetics Nuclear Proteins/metabolism Phosphoprotein Phosphatases/metabolism Phosphorylation Protein Serine-Threonine Kinases Protein Subunits/genetics,metabolism Protein Transport Protein Tyrosine Phosphatases/metabolism Recombinant Fusion Proteins/metabolism S Phase Saccharomyces cerevisiae/cytology,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Substrate Specificity
Chemicals
CDC14 protein, S cerevisiae CLB5 protein, S cerevisiae Cell Cycle Proteins Cyclin B Intracellular Signaling Peptides and Proteins Net1 protein, S cerevisiae Nuclear Proteins Protein Subunits Recombinant Fusion Proteins Saccharomyces cerevisiae Proteins Green Fluorescent Proteins MEC1 protein, S cerevisiae Protein Serine-Threonine Kinases CDC2 Protein Kinase DNA Polymerase II Phosphoprotein Phosphatases Protein Tyrosine Phosphatases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bloom Joanna
The Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.
Cross Frederick R
References (55)
55 references, click to expand
  1. Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase.
    Science. 1997 Oct 17;278(5337):455-60 PMID: 9334303
  2. Interaction of the S-phase cyclin Clb5 with an "RXL" docking sequence in the initiator protein Orc6 provides an origin-localized replication control switch.
    Genes Dev. 2004 May 1;18(9):981-91 PMID: 15105375
  3. Mammalian G1 cyclins and cell cycle progression.
    Proc Assoc Am Physicians. 1995 Jul;107(2):181-6 PMID: 8624851
  4. At the heart of the budding yeast cell cycle.
    Trends Genet. 1996 Oct;12(10):405-12 PMID: 8909137
  5. Saccharomyces cerevisiae G1 cyclins differ in their intrinsic functional specificities.
    Mol Cell Biol. 1996 Dec;16(12):6794-803 PMID: 8943334
  6. Yeast Hct1 is a regulator of Clb2 cyclin proteolysis.
    Cell. 1997 Aug 22;90(4):683-93 PMID: 9288748
  7. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex.
    Cell. 1997 Oct 17;91(2):209-19 PMID: 9346238
  8. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p.
    Cell. 1997 Oct 17;91(2):221-30 PMID: 9346239
  9. Sld2, which interacts with Dpb11 in Saccharomyces cerevisiae, is required for chromosomal DNA replication.
    Mol Cell Biol. 1998 Oct;18(10):6102-9 PMID: 9742127
  10. A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae.
    Mol Biol Cell. 1998 Oct;9(10):2803-17 PMID: 9763445
  11. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools.
    Mol Cell. 1998 Sep;2(3):329-40 PMID: 9774971
  12. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex.
    Science. 1998 Nov 27;282(5394):1721-4 PMID: 9831566
  13. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation.
    Mol Cell. 1998 Dec;2(6):709-18 PMID: 9885559
  14. Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14.
    Curr Biol. 1999 Mar 11;9(5):227-36 PMID: 10074450
  15. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex.
    Cell. 1999 Apr 16;97(2):233-44 PMID: 10219244
  16. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus.
    Nature. 1999 Apr 29;398(6730):818-23 PMID: 10235265
  17. Specialization and targeting of B-type cyclins.
    Mol Cell. 1999 Jul;4(1):11-9 PMID: 10445023
  18. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates.
    Nature. 2005 Mar 3;434(7029):104-8 PMID: 15744308
  19. Regulation of the APC and the exit from mitosis.
    Nat Cell Biol. 1999 Jun;1(2):E47-53 PMID: 10559897
  20. APC(Cdc20) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5.
    Nature. 1999 Nov 11;402(6758):203-7 PMID: 10647015
  21. CDK inactivation is the only essential function of the APC/C and the mitotic exit network proteins for origin resetting during mitosis.
    Mol Cell. 2000 Jan;5(1):85-95 PMID: 10678171
  22. Dpb11 controls the association between DNA polymerases alpha and epsilon and the autonomously replicating sequence region of budding yeast.
    Mol Cell Biol. 2000 Apr;20(8):2809-17 PMID: 10733584
  23. Cdc14 activates cdc15 to promote mitotic exit in budding yeast.
    Curr Biol. 2000 May 18;10(10):615-8 PMID: 10837230
  24. Testing cyclin specificity in the exit from mitosis.
    Mol Cell Biol. 2000 Jul;20(13):4483-93 PMID: 10848575
  25. Conservation and function of a potential substrate-binding domain in the yeast Clb5 B-type cyclin.
    Mol Cell Biol. 2000 Jul;20(13):4782-90 PMID: 10848604
  26. A mechanism for coupling exit from mitosis to partitioning of the nucleus.
    Cell. 2000 Jul 7;102(1):21-31 PMID: 10929710
  27. A chemical switch for inhibitor-sensitive alleles of any protein kinase.
    Nature. 2000 Sep 21;407(6802):395-401 PMID: 11014197
  28. Cyclin specificity: how many wheels do you need on a unicycle?
    J Cell Sci. 2001 May;114(Pt 10):1811-20 PMID: 11329367
  29. Characterization of the Net1 cell cycle-dependent regulator of the Cdc14 phosphatase from budding yeast.
    J Biol Chem. 2001 Jun 15;276(24):21924-31 PMID: 11274204
  30. Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms.
    Nature. 2001 Jun 28;411(6841):1068-73 PMID: 11429609
  31. Net1 stimulates RNA polymerase I transcription and regulates nucleolar structure independently of controlling mitotic exit.
    Mol Cell. 2001 Jul;8(1):45-55 PMID: 11511359
  32. Mrc1 transduces signals of DNA replication stress to activate Rad53.
    Nat Cell Biol. 2001 Nov;3(11):958-65 PMID: 11715016
  33. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1.
    Nat Cell Biol. 2001 Nov;3(11):966-72 PMID: 11715017
  34. Testing a mathematical model of the yeast cell cycle.
    Mol Biol Cell. 2002 Jan;13(1):52-70 PMID: 11809822
  35. Separase, polo kinase, the kinetochore protein Slk19, and Spo12 function in a network that controls Cdc14 localization during early anaphase.
    Cell. 2002 Jan 25;108(2):207-20 PMID: 11832211
  36. S-Cdk-dependent phosphorylation of Sld2 essential for chromosomal DNA replication in budding yeast.
    Nature. 2002 Feb 7;415(6872):651-5 PMID: 11807498
  37. Budding yeast Cdc5 phosphorylates Net1 and assists Cdc14 release from the nucleolus.
    Biochem Biophys Res Commun. 2002 Jun 14;294(3):687-91 PMID: 12056824
  38. MEN, destruction and separation: mechanistic links between mitotic exit and cytokinesis in budding yeast.
    Bioessays. 2002 Jul;24(7):659-66 PMID: 12111726
  39. Systematic identification of pathways that couple cell growth and division in yeast.
    Science. 2002 Jul 19;297(5580):395-400 PMID: 12089449
  40. APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit.
    Nature. 2002 Aug 1;418(6897):556-62 PMID: 12152084
  41. A non-proteolytic function of separase links the onset of anaphase to mitotic exit.
    Nat Cell Biol. 2003 Mar;5(3):249-54 PMID: 12598903
  42. The structure of the cell cycle protein Cdc14 reveals a proline-directed protein phosphatase.
    EMBO J. 2003 Jul 15;22(14):3524-35 PMID: 12853468
  43. Genetic and biochemical evaluation of the importance of Cdc6 in regulating mitotic exit.
    Mol Biol Cell. 2003 Nov;14(11):4592-604 PMID: 12960422
  44. The spindle assembly and spindle position checkpoints.
    Annu Rev Genet. 2003;37:251-82 PMID: 14616062
  45. Enigmatic variations: divergent modes of regulating eukaryotic DNA replication.
    Mol Cell. 2003 Nov;12(5):1067-75 PMID: 14636567
  46. Clb6/Cdc28 and Cdc14 regulate phosphorylation status and cellular localization of Swi6.
    Mol Cell Biol. 2004 Mar;24(6):2277-85 PMID: 14993267
  47. Cell cycle-dependent phosphorylation of the DNA polymerase epsilon subunit, Dpb2, by the Cdc28 cyclin-dependent protein kinase.
    J Biol Chem. 2004 Apr 2;279(14):14245-55 PMID: 14747467
  48. CLB5: a novel B cyclin from budding yeast with a role in S phase.
    Genes Dev. 1992 Sep;6(9):1695-706 PMID: 1387626
  49. DNA polymerases delta and epsilon are required for chromosomal replication in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Jan;13(1):496-505 PMID: 8417347
  50. The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae.
    Cell. 1994 Oct 21;79(2):233-44 PMID: 7954792
  51. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression.
    Nucleic Acids Res. 1994 Dec 25;22(25):5767-8 PMID: 7838736
  52. Principles of CDK regulation.
    Nature. 1995 Mar 9;374(6518):131-4 PMID: 7877684
  53. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage.
    Cell. 1995 Sep 8;82(5):841-7 PMID: 7671311
  54. Dpb11, which interacts with DNA polymerase II(epsilon) in Saccharomyces cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint.
    Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11791-5 PMID: 8524850
  55. CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis.
    Science. 1997 Oct 17;278(5337):460-3 PMID: 9334304
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2007-02-00
Epub
2006-00-20
Pages
842-53
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1800703
Subset
IM
Grants
NIGMS NIH HHS · R01 GM047238 · United States
NCI NIH HHS · T32 CA009673 · United States
NIGMS NIH HHS · GM 047238 · United States
NCI NIH HHS · T32 CA 009673-29 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com