Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Apr 25;92(9):4006–4010. doi: 10.1073/pnas.92.9.4006

Cyclin-dependent protein kinase and cyclin homologs SSN3 and SSN8 contribute to transcriptional control in yeast.

S Kuchin 1, P Yeghiayan 1, M Carlson 1
PMCID: PMC42091  PMID: 7732022

Abstract

The SSN3 and SSN8 genes of Saccharomyces cerevisiae were identified by mutations that suppress a defect in SNF1, a protein kinase required for release from glucose repression. Mutations in SSN3 and SSN8 also act synergistically with a mutation of the MIG1 repressor protein to relieve glucose repression. We have cloned the SSN3 and SSN8 genes. SSN3 encodes a cyclin-dependent protein kinase (cdk) homolog and is identical to UME5. SSN8 encodes a cyclin homolog 35% identical to human cyclin C. SSN3 and SSN8 fusion proteins interact in the two-hybrid system and coimmunoprecipitate from yeast cell extracts. Using an immune complex assay, we detected protein kinase activity that depends on both SSN3 and SSN8. Thus, the two SSN proteins are likely to function as a cdk-cyclin pair. Genetic analysis indicates that the SSN3-SSN8 complex contributes to transcriptional repression of diversely regulated genes and also affects induction of the GAL1 promoter.

Full text

PDF
4006

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Carlson M., Osmond B. C., Neigeborn L., Botstein D. A suppressor of SNF1 mutations causes constitutive high-level invertase synthesis in yeast. Genetics. 1984 May;107(1):19–32. doi: 10.1093/genetics/107.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Celenza J. L., Carlson M. A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science. 1986 Sep 12;233(4769):1175–1180. doi: 10.1126/science.3526554. [DOI] [PubMed] [Google Scholar]
  4. Espinoza F. H., Ogas J., Herskowitz I., Morgan D. O. Cell cycle control by a complex of the cyclin HCS26 (PCL1) and the kinase PHO85. Science. 1994 Nov 25;266(5189):1388–1391. doi: 10.1126/science.7973730. [DOI] [PubMed] [Google Scholar]
  5. Feaver W. J., Svejstrup J. Q., Henry N. L., Kornberg R. D. Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK. Cell. 1994 Dec 16;79(6):1103–1109. doi: 10.1016/0092-8674(94)90040-x. [DOI] [PubMed] [Google Scholar]
  6. Fields S., Song O. A novel genetic system to detect protein-protein interactions. Nature. 1989 Jul 20;340(6230):245–246. doi: 10.1038/340245a0. [DOI] [PubMed] [Google Scholar]
  7. Fisher R. P., Morgan D. O. A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell. 1994 Aug 26;78(4):713–724. doi: 10.1016/0092-8674(94)90535-5. [DOI] [PubMed] [Google Scholar]
  8. Guarente L. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 1983;101:181–191. doi: 10.1016/0076-6879(83)01013-7. [DOI] [PubMed] [Google Scholar]
  9. Hanes S. D., Brent R. DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell. 1989 Jun 30;57(7):1275–1283. doi: 10.1016/0092-8674(89)90063-9. [DOI] [PubMed] [Google Scholar]
  10. Hardie D. G. Molecular physiology. Ways of coping with stress. Nature. 1994 Aug 25;370(6491):599–600. doi: 10.1038/370599a0. [DOI] [PubMed] [Google Scholar]
  11. Kaffman A., Herskowitz I., Tjian R., O'Shea E. K. Phosphorylation of the transcription factor PHO4 by a cyclin-CDK complex, PHO80-PHO85. Science. 1994 Feb 25;263(5150):1153–1156. doi: 10.1126/science.8108735. [DOI] [PubMed] [Google Scholar]
  12. Keleher C. A., Redd M. J., Schultz J., Carlson M., Johnson A. D. Ssn6-Tup1 is a general repressor of transcription in yeast. Cell. 1992 Feb 21;68(4):709–719. doi: 10.1016/0092-8674(92)90146-4. [DOI] [PubMed] [Google Scholar]
  13. Kim Y. J., Björklund S., Li Y., Sayre M. H., Kornberg R. D. A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell. 1994 May 20;77(4):599–608. doi: 10.1016/0092-8674(94)90221-6. [DOI] [PubMed] [Google Scholar]
  14. Koleske A. J., Young R. A. An RNA polymerase II holoenzyme responsive to activators. Nature. 1994 Mar 31;368(6470):466–469. doi: 10.1038/368466a0. [DOI] [PubMed] [Google Scholar]
  15. Lew D. J., Dulić V., Reed S. I. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell. 1991 Sep 20;66(6):1197–1206. doi: 10.1016/0092-8674(91)90042-w. [DOI] [PubMed] [Google Scholar]
  16. Li L., Elledge S. J., Peterson C. A., Bales E. S., Legerski R. J. Specific association between the human DNA repair proteins XPA and ERCC1. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5012–5016. doi: 10.1073/pnas.91.11.5012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Léopold P., O'Farrell P. H. An evolutionarily conserved cyclin homolog from Drosophila rescues yeast deficient in G1 cyclins. Cell. 1991 Sep 20;66(6):1207–1216. doi: 10.1016/0092-8674(91)90043-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Measday V., Moore L., Ogas J., Tyers M., Andrews B. The PCL2 (ORFD)-PHO85 cyclin-dependent kinase complex: a cell cycle regulator in yeast. Science. 1994 Nov 25;266(5189):1391–1395. doi: 10.1126/science.7973731. [DOI] [PubMed] [Google Scholar]
  19. Molz L., Beach D. Characterization of the fission yeast mcs2 cyclin and its associated protein kinase activity. EMBO J. 1993 Apr;12(4):1723–1732. doi: 10.1002/j.1460-2075.1993.tb05817.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mäkelä T. P., Tassan J. P., Nigg E. A., Frutiger S., Hughes G. J., Weinberg R. A. A cyclin associated with the CDK-activating kinase MO15. Nature. 1994 Sep 15;371(6494):254–257. doi: 10.1038/371254a0. [DOI] [PubMed] [Google Scholar]
  21. Nehlin J. O., Ronne H. Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins. EMBO J. 1990 Sep;9(9):2891–2898. doi: 10.1002/j.1460-2075.1990.tb07479.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rose M. D., Novick P., Thomas J. H., Botstein D., Fink G. R. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene. 1987;60(2-3):237–243. doi: 10.1016/0378-1119(87)90232-0. [DOI] [PubMed] [Google Scholar]
  23. Roy R., Adamczewski J. P., Seroz T., Vermeulen W., Tassan J. P., Schaeffer L., Nigg E. A., Hoeijmakers J. H., Egly J. M. The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor. Cell. 1994 Dec 16;79(6):1093–1101. doi: 10.1016/0092-8674(94)90039-6. [DOI] [PubMed] [Google Scholar]
  24. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sarokin L., Carlson M. Upstream region of the SUC2 gene confers regulated expression to a heterologous gene in Saccharomyces cerevisiae. Mol Cell Biol. 1985 Oct;5(10):2521–2526. doi: 10.1128/mcb.5.10.2521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schmitt M. E., Clayton D. A. Yeast site-specific ribonucleoprotein endoribonuclease MRP contains an RNA component homologous to mammalian RNase MRP RNA and essential for cell viability. Genes Dev. 1992 Oct;6(10):1975–1985. doi: 10.1101/gad.6.10.1975. [DOI] [PubMed] [Google Scholar]
  27. Schultz J., Carlson M. Molecular analysis of SSN6, a gene functionally related to the SNF1 protein kinase of Saccharomyces cerevisiae. Mol Cell Biol. 1987 Oct;7(10):3637–3645. doi: 10.1128/mcb.7.10.3637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schurr A., Yagil E. Regulation and characterization of acid and alkaline phosphatase in yeast. J Gen Microbiol. 1971 Mar;65(3):291–303. doi: 10.1099/00221287-65-3-291. [DOI] [PubMed] [Google Scholar]
  29. Sikorski R. S., Hieter P. 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. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Strich R., Slater M. R., Esposito R. E. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10018–10022. doi: 10.1073/pnas.86.24.10018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Surosky R. T., Strich R., Esposito R. E. The yeast UME5 gene regulates the stability of meiotic mRNAs in response to glucose. Mol Cell Biol. 1994 May;14(5):3446–3458. doi: 10.1128/mcb.14.5.3446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thompson C. M., Koleske A. J., Chao D. M., Young R. A. A multisubunit complex associated with the RNA polymerase II CTD and TATA-binding protein in yeast. Cell. 1993 Jul 2;73(7):1361–1375. doi: 10.1016/0092-8674(93)90362-t. [DOI] [PubMed] [Google Scholar]
  33. Treitel M. A., Carlson M. Repression by SSN6-TUP1 is directed by MIG1, a repressor/activator protein. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3132–3136. doi: 10.1073/pnas.92.8.3132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Valay J. G., Simon M., Faye G. The kin28 protein kinase is associated with a cyclin in Saccharomyces cerevisiae. J Mol Biol. 1993 Nov 20;234(2):307–310. doi: 10.1006/jmbi.1993.1587. [DOI] [PubMed] [Google Scholar]
  35. Vallier L. G., Carlson M. Synergistic release from glucose repression by mig1 and ssn mutations in Saccharomyces cerevisiae. Genetics. 1994 May;137(1):49–54. doi: 10.1093/genetics/137.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Xiong Y., Menninger J., Beach D., Ward D. C. Molecular cloning and chromosomal mapping of CCND genes encoding human D-type cyclins. Genomics. 1992 Jul;13(3):575–584. doi: 10.1016/0888-7543(92)90127-e. [DOI] [PubMed] [Google Scholar]
  37. Yang X., Jiang R., Carlson M. A family of proteins containing a conserved domain that mediates interaction with the yeast SNF1 protein kinase complex. EMBO J. 1994 Dec 15;13(24):5878–5886. doi: 10.1002/j.1460-2075.1994.tb06933.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Yocum R. R., Hanley S., West R., Jr, Ptashne M. Use of lacZ fusions to delimit regulatory elements of the inducible divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Oct;4(10):1985–1998. doi: 10.1128/mcb.4.10.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES