Home LiteratureArticle Details
PMID: 12937340 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

ACE2 is required for daughter cell-specific G1 delay in Saccharomyces cerevisiae.

Laabs TL, Markwardt DD, Slattery MG, Newcomb LL, Stillman DJ, Heideman W

Abstract

Saccharomyces cerevisiae cells reproduce by budding to yield a mother cell and a smaller daughter cell. Although both mother and daughter begin G1 simultaneously, the mother cell progresses through G1 more rapidly. Daughter cell G1 delay has long been thought to be due to a requirement for attaining a certain critical cell size before passing the commitment point in the cell cycle known as START. We present an alternative model in which the daughter cell-specific Ace2 transcription factor delays G1 in daughter cells. Deletion of ACE2 produces daughter cells that proceed through G1 at the same rate as mother cells, whereas a mutant Ace2 protein that is not restricted to daughter cells delays G1 equally in both mothers and daughters. The differential in G1 length between mothers and daughters requires the Cln3 G1 cyclin, and CLN3-GFP reporter expression is reduced in daughters in an ACE2-dependent manner. Specific daughter delay elements in the CLN3 promoter are required for normal daughter G1 delay, and these elements bind to an unidentified 127-kDa protein. This DNA-binding activity is enhanced by deletion of ACE2. These results support a model in which daughter cell G1 delay is determined not by cell size but by an intrinsic property of the daughter cell generated by asymmetric cell division.

MeSH Terms
Base Sequence Cell Cycle Cell Size Cyclins/genetics,physiology DNA-Binding Proteins/physiology G1 Phase/physiology Molecular Sequence Data Promoter Regions, Genetic Saccharomyces cerevisiae/physiology Saccharomyces cerevisiae Proteins/genetics,physiology Transcription Factors/physiology
Chemicals
ACE2 protein, S cerevisiae CLN3 protein, S cerevisiae Cyclins DNA-Binding Proteins Saccharomyces cerevisiae Proteins Transcription Factors
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Laabs Tracy L
School of Pharmacy, University of Wisconsin, Madison, WI 53705, USA.
Markwardt David D
Slattery Matthew G
Newcomb Laura L
Stillman David J
Heideman Warren
References (38)
38 references, click to expand
  1. Variability in individual cell cycles of Saccharomyces cerevisiae.
    J Cell Sci. 1981 Aug;50:361-76 PMID: 7033253
  2. Coordination of growth with cell division in the yeast Saccharomyces cerevisiae.
    Exp Cell Res. 1977 Mar 1;105(1):79-98 PMID: 320023
  3. Rate of cell cycle initiation of yeast cells when cell size is not a rate-determining factor.
    J Cell Sci. 1983 Jan;59:183-201 PMID: 6345558
  4. Kinetic evidence for a critical rate of protein synthesis in the Saccharomyces cerevisiae yeast cell cycle.
    J Biol Chem. 1988 Jul 15;263(20):9674-81 PMID: 3290211
  5. DAF1, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae.
    Mol Cell Biol. 1988 Nov;8(11):4675-84 PMID: 3062366
  6. The WHI1+ gene of Saccharomyces cerevisiae tethers cell division to cell size and is a cyclin homolog.
    EMBO J. 1988 Dec 20;7(13):4335-46 PMID: 2907481
  7. Volume growth of daughter and parent cells during the cell cycle of Saccharomyces cerevisiae a/alpha as determined by image cytometry.
    J Bacteriol. 1993 May;175(10):3174-81 PMID: 8491731
  8. Far1 and Fus3 link the mating pheromone signal transduction pathway to three G1-phase Cdc28 kinase complexes.
    Mol Cell Biol. 1993 Sep;13(9):5659-69 PMID: 8395009
  9. Connections between the Ras-cyclic AMP pathway and G1 cyclin expression in the budding yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Oct;13(10):6274-82 PMID: 8413227
  10. Genes that can bypass the CLN requirement for Saccharomyces cerevisiae cell cycle START.
    Mol Cell Biol. 1994 Mar;14(3):2041-7 PMID: 8114735
  11. Activation of CLN1 and CLN2 G1 cyclin gene expression by BCK2.
    Mol Cell Biol. 1995 Apr;15(4):1835-46 PMID: 7891677
  12. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds.
    Gene. 1995 Apr 14;156(1):119-22 PMID: 7737504
  13. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells.
    Cell. 1996 Mar 8;84(5):699-709 PMID: 8625408
  14. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene.
    Cell. 1996 Mar 8;84(5):711-22 PMID: 8625409
  15. TOR controls translation initiation and early G1 progression in yeast.
    Mol Biol Cell. 1996 Jan;7(1):25-42 PMID: 8741837
  16. Saccharomyces cerevisiae G1 cyclins differ in their intrinsic functional specificities.
    Mol Cell Biol. 1996 Dec;16(12):6794-803 PMID: 8943334
  17. A novel Mcm1-dependent element in the SWI4, CLN3, CDC6, and CDC47 promoters activates M/G1-specific transcription.
    Genes Dev. 1997 May 15;11(10):1277-88 PMID: 9171372
  18. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast.
    Nature. 1997 Sep 4;389(6646):90-3 PMID: 9288973
  19. Coupling of cell division to cell growth by translational control of the G1 cyclin CLN3 in yeast.
    Genes Dev. 1997 Oct 1;11(19):2522-31 PMID: 9334317
  20. The Cln3 cyclin is down-regulated by translational repression and degradation during the G1 arrest caused by nitrogen deprivation in budding yeast.
    EMBO J. 1997 Dec 1;16(23):7196-206 PMID: 9384596
  21. Cln3-associated kinase activity in Saccharomyces cerevisiae is regulated by the mating factor pathway.
    Mol Cell Biol. 1998 Jan;18(1):433-41 PMID: 9418890
  22. Growth-independent regulation of CLN3 mRNA levels by nutrients in Saccharomyces cerevisiae.
    J Bacteriol. 1998 Jan;180(2):225-30 PMID: 9440509
  23. Regulation of the Cln3-Cdc28 kinase by cAMP in Saccharomyces cerevisiae.
    EMBO J. 1998 Aug 3;17(15):4370-8 PMID: 9687505
  24. Transcriptional regulation of CLN3 expression by glucose in Saccharomyces cerevisiae.
    J Bacteriol. 1998 Sep;180(17):4508-15 PMID: 9721289
  25. Localization of ASH1 mRNA particles in living yeast.
    Mol Cell. 1998 Oct;2(4):437-45 PMID: 9809065
  26. G1 cyclins block the Ime1 pathway to make mitosis and meiosis incompatible in budding yeast.
    EMBO J. 1999 Jan 15;18(2):320-9 PMID: 9889189
  27. Genetic analysis of the shared role of CLN3 and BCK2 at the G(1)-S transition in Saccharomyces cerevisiae.
    Genetics. 1999 Nov;153(3):1131-43 PMID: 10545447
  28. Cbk1p, a protein similar to the human myotonic dystrophy kinase, is essential for normal morphogenesis in Saccharomyces cerevisiae.
    EMBO J. 2000 Sep 1;19(17):4524-32 PMID: 10970846
  29. Osmotic stress causes a G1 cell cycle delay and downregulation of Cln3/Cdc28 activity in Saccharomyces cerevisiae.
    Mol Microbiol. 2001 Feb;39(4):1022-35 PMID: 11251821
  30. Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates.
    Cell. 2001 Dec 14;107(6):739-50 PMID: 11747810
  31. Characterization of the ECB binding complex responsible for the M/G(1)-specific transcription of CLN3 and SWI4.
    Mol Cell Biol. 2002 Jan;22(2):430-41 PMID: 11756540
  32. AZF1 is a glucose-dependent positive regulator of CLN3 transcription in Saccharomyces cerevisiae.
    Mol Cell Biol. 2002 Mar;22(5):1607-14 PMID: 11839825
  33. Systematic identification of pathways that couple cell growth and division in yeast.
    Science. 2002 Jul 19;297(5580):395-400 PMID: 12089449
  34. The Saccharomyces cerevisiae Mob2p-Cbk1p kinase complex promotes polarized growth and acts with the mitotic exit network to facilitate daughter cell-specific localization of Ace2p transcription factor.
    J Cell Biol. 2002 Sep 2;158(5):885-900 PMID: 12196508
  35. Genomic scale mutant hunt identifies cell size homeostasis genes in S. cerevisiae.
    Curr Biol. 2002 Dec 10;12(23):1992-2001 PMID: 12477387
  36. Periodic transcription: a cycle within a cycle.
    Curr Biol. 2003 Jan 8;13(1):R31-8 PMID: 12526763
  37. Glucose regulation of Saccharomyces cerevisiae cell cycle genes.
    Eukaryot Cell. 2003 Feb;2(1):143-9 PMID: 12582131
  38. Size control models of Saccharomyces cerevisiae cell proliferation.
    Mol Cell Biol. 1982 Apr;2(4):361-8 PMID: 7050671
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
2003-09-02
Epub
2003-00-22
Pages
10275-80
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC193551
Subset
IM
Grants
NIGMS NIH HHS · R01 GM048624 · United States
NIGMS NIH HHS · GM48624 · 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