Home LiteratureArticle Details
PMID: 12024050 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

The G(1) cyclin Cln3 promotes cell cycle entry via the transcription factor Swi6.

Molecular and cellular biology ·Vol. 22 ·No. 12 ·2002-06-00 ·Pages 4402-18

Wijnen H, Landman A, Futcher B

Abstract

In Saccharomyces cerevisiae (budding yeast), commitment to cell division in late G(1) is promoted by the G(1) cyclin Cln3 and its associated cyclin-dependent kinase, Cdc28. We show here that all known aspects of the function of Cln3 in G(1) phase, including control of cell size, pheromone sensitivity, cell cycle progress, and transcription, require the protein Swi6. Swi6 is a component of two related transcription factors, SBF and MBF, which are known to regulate many genes at the G(1)-S transition. The Cln3-Cdc28 complex somehow activates SBF and MBF, but there was no evidence for direct phosphorylation of SBF/MBF by Cln3-Cdc28 or for a stable complex between SBF/MBF and Cln3-Cdc28. The activation also does not depend on the ability of Cln3 to activate transcription when artificially recruited directly to a promoter. The amino terminus and the leucine zipper of Swi6 are important for the ability of Swi6 to respond to Cln3 but are not essential for the basal transcriptional activity of Swi6. Cln3-Cdc28 may activate SBF and MBF indirectly, perhaps by phosphorylating some intermediary protein.

MeSH Terms
CDC28 Protein Kinase, S cerevisiae/metabolism Cell Cycle/genetics Cyclins/genetics,metabolism DNA-Binding Proteins Fungal Proteins/genetics,metabolism G1 Phase/genetics Mutation Pheromones/metabolism Phosphorylation Saccharomyces cerevisiae Proteins/genetics,metabolism Transcription Factors/genetics,metabolism Transcription, Genetic Yeasts/genetics,metabolism
Chemicals
CLN3 protein, S cerevisiae Cyclins DNA-Binding Proteins Fungal Proteins MBP1 protein, S cerevisiae Pheromones SWI4 protein, S cerevisiae SWI6 protein, S cerevisiae Saccharomyces cerevisiae Proteins Transcription Factors CDC28 Protein Kinase, S cerevisiae
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Wijnen Herman
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
Landman Allison
Futcher Bruce
References (61)
61 references, click to expand
  1. 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
  2. Roles and regulation of Cln-Cdc28 kinases at the start of the cell cycle of Saccharomyces cerevisiae.
    EMBO J. 1995 Oct 2;14(19):4803-13 PMID: 7588610
  3. Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3118-23 PMID: 10706616
  4. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF.
    Nature. 2001 Jan 25;409(6819):533-8 PMID: 11206552
  5. Cdk1 triggers association of RNA polymerase to cell cycle promoters only after recruitment of the mediator by SBF.
    Mol Cell. 2001 Jun;7(6):1213-20 PMID: 11430824
  6. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  7. Universal control mechanism regulating onset of M-phase.
    Nature. 1990 Apr 5;344(6266):503-8 PMID: 2138713
  8. G1-specific cyclins of S. cerevisiae: cell cycle periodicity, regulation by mating pheromone, and association with the p34CDC28 protein kinase.
    Cell. 1990 Jul 27;62(2):225-37 PMID: 2142620
  9. Coordination of expression of DNA synthesis genes in budding yeast by a cell-cycle regulated trans factor.
    Nature. 1991 Mar 21;350(6315):247-50 PMID: 2005980
  10. Human D-type cyclin.
    Cell. 1991 May 17;65(4):691-9 PMID: 1827756
  11. A potential positive feedback loop controlling CLN1 and CLN2 gene expression at the start of the yeast cell cycle.
    Cell. 1991 May 31;65(5):875-83 PMID: 2040016
  12. Cell cycle-specific expression of the SWI4 transcription factor is required for the cell cycle regulation of HO transcription.
    Genes Dev. 1991 Jul;5(7):1183-90 PMID: 2065973
  13. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast.
    Cell. 1991 Sep 6;66(5):995-1013 PMID: 1832338
  14. Changes in a SWI4,6-DNA-binding complex occur at the time of HO gene activation in yeast.
    Genes Dev. 1991 Nov;5(11):2000-13 PMID: 1936990
  15. FUS3 represses CLN1 and CLN2 and in concert with KSS1 promotes signal transduction.
    Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9392-6 PMID: 1946350
  16. Multifunctional yeast high-copy-number shuttle vectors.
    Gene. 1992 Jan 2;110(1):119-22 PMID: 1544568
  17. Direct induction of G1-specific transcripts following reactivation of the Cdc28 kinase in the absence of de novo protein synthesis.
    Genes Dev. 1992 Apr;6(4):557-67 PMID: 1313770
  18. CLN3, not positive feedback, determines the timing of CLN2 transcription in cycling cells.
    Genes Dev. 1995 Nov 15;9(22):2780-94 PMID: 7590253
  19. Evolution of the cell cycle.
    Philos Trans R Soc Lond B Biol Sci. 1995 Sep 29;349(1329):271-81 PMID: 8577838
  20. Start-specific transcription in yeast.
    Curr Top Microbiol Immunol. 1996;208:95-127 PMID: 8575215
  21. Switching transcription on and off during the yeast cell cycle: Cln/Cdc28 kinases activate bound transcription factor SBF (Swi4/Swi6) at start, whereas Clb/Cdc28 kinases displace it from the promoter in G2.
    Genes Dev. 1996 Jan 15;10(2):129-41 PMID: 8566747
  22. Cell cycle-regulated phosphorylation of Swi6 controls its nuclear localization.
    Mol Biol Cell. 1995 Dec;6(12):1641-58 PMID: 8590795
  23. Binding to the yeast SwI4,6-dependent cell cycle box, CACGAAA, is cell cycle regulated in vivo.
    Nucleic Acids Res. 1996 Feb 15;24(4):558-65 PMID: 8604294
  24. Saccharomyces cerevisiae G1 cyclins differ in their intrinsic functional specificities.
    Mol Cell Biol. 1996 Dec;16(12):6794-803 PMID: 8943334
  25. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast.
    Genetics. 1996 Dec;144(4):1425-36 PMID: 8978031
  26. Functional characterization of the fission yeast Start-specific transcription factor Res2.
    EMBO J. 1997 Mar 3;16(5):1023-34 PMID: 9118941
  27. Cell cycle-dependent transcription of CLN1 involves swi4 binding to MCB-like elements.
    J Biol Chem. 1997 Apr 4;272(14):9071-7 PMID: 9083033
  28. 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
  29. 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
  30. A genome-wide transcriptional analysis of the mitotic cell cycle.
    Mol Cell. 1998 Jul;2(1):65-73 PMID: 9702192
  31. Structural and functional architecture of the yeast cell-cycle transcription factor swi6.
    J Mol Biol. 1998 Sep 4;281(5):763-75 PMID: 9719633
  32. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization.
    Mol Biol Cell. 1998 Dec;9(12):3273-97 PMID: 9843569
  33. Role of the retinoblastoma protein family, pRB, p107 and p130 in the negative control of cell growth.
    Oncogene. 1998 Dec 24;17(25):3365-83 PMID: 9916999
  34. A role for Ctr9p and Paf1p in the regulation G1 cyclin expression in yeast.
    Nucleic Acids Res. 1999 May 15;27(10):2126-34 PMID: 10219085
  35. Mechanisms controlling subcellular localization of the G(1) cyclins Cln2p and Cln3p in budding yeast.
    Mol Cell Biol. 2001 Sep;21(18):6292-311 PMID: 11509671
  36. Serial regulation of transcriptional regulators in the yeast cell cycle.
    Cell. 2001 Sep 21;106(6):697-708 PMID: 11572776
  37. Relationship between the function and the location of G1 cyclins in S. cerevisiae.
    J Cell Sci. 2001 Dec;114(Pt 24):4599-611 PMID: 11792824
  38. Animal cell cycle.
    Annu Rev Biochem. 1978;47:715-50 PMID: 354504
  39. Sterile host yeasts (SHY): a eukaryotic system of biological containment for recombinant DNA experiments.
    Gene. 1979 Dec;8(1):17-24 PMID: 395030
  40. A repetitive DNA sequence that confers cell-cycle START (CDC28)-dependent transcription of the HO gene in yeast.
    Cell. 1985 Aug;42(1):225-35 PMID: 3893742
  41. Plasmid construction by homologous recombination in yeast.
    Gene. 1987;58(2-3):201-16 PMID: 2828185
  42. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector.
    Gene. 1987;60(2-3):237-43 PMID: 3327750
  43. 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
  44. Yeast/E. coli shuttle vectors with multiple unique restriction sites.
    Yeast. 1986 Sep;2(3):163-7 PMID: 3333305
  45. Identification of a DNA binding factor involved in cell-cycle control of the yeast HO gene.
    Cell. 1989 Apr 7;57(1):21-9 PMID: 2649246
  46. 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
  47. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.
    Gene. 1988 Dec 30;74(2):527-34 PMID: 3073106
  48. The Cln3-Cdc28 kinase complex of S. cerevisiae is regulated by proteolysis and phosphorylation.
    EMBO J. 1992 May;11(5):1773-84 PMID: 1316273
  49. Cell cycle control of DNA synthesis in budding yeast.
    Nucleic Acids Res. 1992 May 25;20(10):2403-10 PMID: 1598198
  50. SWI6 protein is required for transcription of the periodically expressed DNA synthesis genes in budding yeast.
    Nature. 1992 Jun 11;357(6378):505-8 PMID: 1608450
  51. A central role for SWI6 in modulating cell cycle Start-specific transcription in yeast.
    Nature. 1992 Jun 11;357(6378):508-13 PMID: 1608451
  52. Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun.
    Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5789-93 PMID: 1631061
  53. SIT4 protein phosphatase is required for the normal accumulation of SWI4, CLN1, CLN2, and HCS26 RNAs during late G1.
    Genes Dev. 1992 Dec;6(12A):2417-28 PMID: 1334024
  54. FAR1 is required for posttranscriptional regulation of CLN2 gene expression in response to mating pheromone.
    Mol Cell Biol. 1993 Feb;13(2):1013-22 PMID: 8423774
  55. Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins.
    EMBO J. 1993 May;12(5):1955-68 PMID: 8387915
  56. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase.
    Science. 1993 Sep 17;261(5128):1551-7 PMID: 8372350
  57. Genes that can bypass the CLN requirement for Saccharomyces cerevisiae cell cycle START.
    Mol Cell Biol. 1994 Mar;14(3):2041-7 PMID: 8114735
  58. Direct inhibition of the yeast cyclin-dependent kinase Cdc28-Cln by Far1.
    Science. 1994 Aug 26;265(5176):1228-31 PMID: 8066461
  59. Activation of CLN1 and CLN2 G1 cyclin gene expression by BCK2.
    Mol Cell Biol. 1995 Apr;15(4):1835-46 PMID: 7891677
  60. D-type cyclins.
    Trends Biochem Sci. 1995 May;20(5):187-90 PMID: 7610482
  61. Distinct subcellular localization patterns contribute to functional specificity of the Cln2 and Cln3 cyclins of Saccharomyces cerevisiae.
    Mol Cell Biol. 2000 Jan;20(2):542-55 PMID: 10611233
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2002-06-00
Pages
4402-18
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC133883
Subset
IM
Grants
NIGMS NIH HHS · R01 GM039978 · United States
NIGMS NIH HHS · R01 GM39978 · 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