Home LiteratureArticle Details
PMID: 15956196 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Swe1 regulation and transcriptional control restrict the activity of mitotic cyclins toward replication proteins in Saccharomyces cerevisiae.

Hu F, Aparicio OM

Abstract

Cyclin-dependent kinases (CDKs) drive the cell cycle through the phosphorylation of substrates that function in genome duplication and cell division. The existence of multiple cyclin subunits and their distinct cell cycle-regulated expression suggests that cyclins impart unique specificities to CDK-substrate interactions that are critical for normal cellular function. This study shows that the combination of early cell cycle expression and deletion of the CDK inhibitor Saccharomyces Wee1 (Swe1) enables the mitotic B-type (Clb) cyclins Clb2, Clb3, and Clb4 of Saccharomyces cerevisiae to initiate S phase with similar effectiveness as the S-phase cyclin Clb5. Although in vivo analysis indicates preferential phosphorylation of a replication substrate by Clb5-Cdk1, this difference is relatively minor compared with the impact of transcriptional control and Swe1 regulation. Indeed, early expressed Clb2-Cdk1 can activate all essential Clb-Cdk substrates in a strain lacking all other Clbs and Swe1. Thus, Swe1 regulation and expression timing are key mechanisms that sequester the broad activity of Clb2-Cdk1 from critical substrates. Furthermore, the ability of Swe1 to inhibit the activity of different B-type cyclins in replication initiation correlates with the normal expression timing of those cyclins, with no apparent in vivo inhibition of Clb5 and Clb6, moderate inhibition of Clb3 and Clb4, and strong inhibition of Clb2. Hence, Swe1 appears to reinforce the temporal activity of cyclins established through transcriptional control. The conserved nature of CDK function suggests that similar mechanisms regulate CDK specificity in multicellular organisms.

MeSH Terms
Cell Cycle Proteins/genetics Cyclin-Dependent Kinases/genetics,metabolism Cyclins/genetics,metabolism Gene Expression Regulation, Enzymologic Gene Expression Regulation, Fungal Mitosis Protein-Tyrosine Kinases/genetics Saccharomyces cerevisiae/cytology,enzymology,genetics Saccharomyces cerevisiae Proteins/genetics
Chemicals
Cell Cycle Proteins Cyclins Saccharomyces cerevisiae Proteins SWE1 protein, S cerevisiae Protein-Tyrosine Kinases Cyclin-Dependent Kinases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Hu Fangfang
Molecular and Computational Biology Program, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-2910, USA.
Aparicio Oscar M
References (33)
33 references, click to expand
  1. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates.
    Nature. 2005 Mar 3;434(7029):104-8 PMID: 15744308
  2. Diminished S-phase cyclin-dependent kinase function elicits vital Rad53-dependent checkpoint responses in Saccharomyces cerevisiae.
    Mol Cell Biol. 2004 Dec;24(23):10208-22 PMID: 15542831
  3. Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae.
    Mol Biol Cell. 1992 Jul;3(7):805-18 PMID: 1387566
  4. CLB5: a novel B cyclin from budding yeast with a role in S phase.
    Genes Dev. 1992 Sep;6(9):1695-706 PMID: 1387626
  5. Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2.
    Genes Dev. 1992 Nov;6(11):2021-34 PMID: 1427070
  6. Control of the yeast cell cycle by the Cdc28 protein kinase.
    Curr Opin Cell Biol. 1993 Apr;5(2):166-79 PMID: 8507488
  7. CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae.
    Genes Dev. 1993 Jul;7(7A):1160-75 PMID: 8319908
  8. Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins.
    EMBO J. 1993 Sep;12(9):3417-26 PMID: 8253069
  9. A new pair of B-type cyclins from Saccharomyces cerevisiae that function early in the cell cycle.
    EMBO J. 1993 Sep;12(9):3437-47 PMID: 8253070
  10. A cell cycle checkpoint monitors cell morphogenesis in budding yeast.
    J Cell Biol. 1995 May;129(3):739-49 PMID: 7730408
  11. Evolution of the cell cycle.
    Philos Trans R Soc Lond B Biol Sci. 1995 Sep 29;349(1329):271-81 PMID: 8577838
  12. A single fission yeast mitotic cyclin B p34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins.
    EMBO J. 1996 Feb 15;15(4):850-60 PMID: 8631306
  13. A quantitative model for the cdc2 control of S phase and mitosis in fission yeast.
    Trends Genet. 1996 Sep;12(9):345-50 PMID: 8855663
  14. Regulatory roles of cyclin dependent kinase phosphorylation in cell cycle control.
    Curr Opin Cell Biol. 1996 Dec;8(6):795-804 PMID: 8939679
  15. The yeast mitotic cyclin Clb2 cannot substitute for S phase cyclins in replication origin firing.
    EMBO Rep. 2000 Dec;1(6):507-12 PMID: 11263495
  16. Cyclin specificity: how many wheels do you need on a unicycle?
    J Cell Sci. 2001 May;114(Pt 10):1811-20 PMID: 11329367
  17. S-Cdk-dependent phosphorylation of Sld2 essential for chromosomal DNA replication in budding yeast.
    Nature. 2002 Feb 7;415(6872):651-5 PMID: 11807498
  18. Evolution of eukaryotic cell cycle regulation: stepwise addition of regulatory kinases and late advent of the CDKs.
    Curr Biol. 2003 Jan 21;13(2):173-7 PMID: 12546794
  19. Conservation of mechanisms controlling entry into mitosis: budding yeast wee1 delays entry into mitosis and is required for cell size control.
    Curr Biol. 2003 Feb 18;13(4):264-75 PMID: 12593792
  20. Unmasking the S-phase-promoting potential of cyclin B1.
    Science. 2003 May 9;300(5621):987-90 PMID: 12738867
  21. Recycling the cell cycle: cyclins revisited.
    Cell. 2004 Jan 23;116(2):221-34 PMID: 14744433
  22. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae.
    Mol Cell Biol. 2004 Jun;24(11):4769-80 PMID: 15143171
  23. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog.
    Cell. 1987 May 22;49(4):559-67 PMID: 3032459
  24. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2.
    Cell. 1991 Mar 22;64(6):1111-22 PMID: 1706223
  25. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae.
    Cell. 1991 Apr 5;65(1):145-61 PMID: 1849457
  26. S-phase feedback control in budding yeast independent of tyrosine phosphorylation of p34cdc28.
    Nature. 1992 Jan 23;355(6358):365-8 PMID: 1731250
  27. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  28. CLB5-dependent activation of late replication origins in S. cerevisiae.
    Mol Cell. 1998 Aug;2(2):173-82 PMID: 9734354
  29. Regulation of Cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1191-243 PMID: 9841670
  30. Specialization and targeting of B-type cyclins.
    Mol Cell. 1999 Jul;4(1):11-9 PMID: 10445023
  31. Phosphorylation-independent inhibition of Cdc28p by the tyrosine kinase Swe1p in the morphogenesis checkpoint.
    Mol Cell Biol. 1999 Sep;19(9):5981-90 PMID: 10454545
  32. Evidence that a free-running oscillator drives G1 events in the budding yeast cell cycle.
    Nature. 1999 Sep 23;401(6751):394-7 PMID: 10517640
  33. Regulation of p34CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae.
    Nature. 1992 Jan 23;355(6358):368-71 PMID: 1731251
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-06-21
Epub
2005-00-14
Pages
8910-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1157011
Subset
IM
Grants
NIGMS NIH HHS · 1R01GM-CA65494 · 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: [email protected]