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. 1996 Jul;16(7):3264–3274. doi: 10.1128/mcb.16.7.3264

EGT2 gene transcription is induced predominantly by Swi5 in early G1.

B Kovacech 1, K Nasmyth 1, T Schuster 1
PMCID: PMC231320  PMID: 8668141

Abstract

In a screen for cell cycle-regulated genes in the yeast Saccharomyces cerevisiae, we have identified a gene, EGT2, which is involved in cell separation in the G1 stage of the cell cycle. Transcription of EGT2 is tightly regulated in a cell cycle-dependent manner. Transcriptional levels peak at the boundary of mitosis and early G1 The transcription factors responsible for EGT2 expression in early G1 are Swi5 and, to a lesser extent, Ace2. Swi5 is involved in the transcriptional activation of the HO gene during late G1 and early S phase, and Ace2 induces CTS1 transcription during early and late G1 We show that Swi5 activates EGT2 transcription as soon as it enters the nucleus at the end of mitosis in a concentration-dependent manner. Since Swi5 is unstable in the nucleus, its level drops rapidly, causing termination of EGT2 transcription before cells are committed to the next cell cycle. However, Swi5 is still able to activate transcription of HO in late G1 in conjunction with additional activators such as Swi4 and Swi6.

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Selected References

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  1. Alani E., Cao L., Kleckner N. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics. 1987 Aug;116(4):541–545. doi: 10.1534/genetics.112.541.test. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amon A., Tyers M., Futcher B., Nasmyth K. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell. 1993 Sep 24;74(6):993–1007. doi: 10.1016/0092-8674(93)90722-3. [DOI] [PubMed] [Google Scholar]
  3. Boeke J. D., LaCroute F., Fink G. R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. doi: 10.1007/BF00330984. [DOI] [PubMed] [Google Scholar]
  4. Bonneaud N., Ozier-Kalogeropoulos O., Li G. Y., Labouesse M., Minvielle-Sebastia L., Lacroute F. A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast. 1991 Aug-Sep;7(6):609–615. doi: 10.1002/yea.320070609. [DOI] [PubMed] [Google Scholar]
  5. Brazas R. M., Stillman D. J. Identification and purification of a protein that binds DNA cooperatively with the yeast SWI5 protein. Mol Cell Biol. 1993 Sep;13(9):5524–5537. doi: 10.1128/mcb.13.9.5524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brazas R. M., Stillman D. J. The Swi5 zinc-finger and Grf10 homeodomain proteins bind DNA cooperatively at the yeast HO promoter. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11237–11241. doi: 10.1073/pnas.90.23.11237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Breeden L., Nasmyth K. Cell cycle control of the yeast HO gene: cis- and trans-acting regulators. Cell. 1987 Feb 13;48(3):389–397. doi: 10.1016/0092-8674(87)90190-5. [DOI] [PubMed] [Google Scholar]
  8. Breitwieser W., Price C., Schuster T. Identification of a gene encoding a novel zinc finger protein in Saccharomyces cerevisiae. Yeast. 1993 May;9(5):551–556. doi: 10.1002/yea.320090512. [DOI] [PubMed] [Google Scholar]
  9. Butler G., Thiele D. J. ACE2, an activator of yeast metallothionein expression which is homologous to SWI5. Mol Cell Biol. 1991 Jan;11(1):476–485. doi: 10.1128/mcb.11.1.476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cross F. R., Tinkelenberg A. H. 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):875–883. doi: 10.1016/0092-8674(91)90394-e. [DOI] [PubMed] [Google Scholar]
  11. De Nobel J. G., Klis F. M., Ram A., Van Unen H., Priem J., Munnik T., Van Den Ende H. Cyclic variations in the permeability of the cell wall of Saccharomyces cerevisiae. Yeast. 1991 Aug-Sep;7(6):589–598. doi: 10.1002/yea.320070606. [DOI] [PubMed] [Google Scholar]
  12. Dirick L., Moll T., Auer H., Nasmyth K. A central role for SWI6 in modulating cell cycle Start-specific transcription in yeast. Nature. 1992 Jun 11;357(6378):508–513. doi: 10.1038/357508a0. [DOI] [PubMed] [Google Scholar]
  13. Dirick L., Nasmyth K. Positive feedback in the activation of G1 cyclins in yeast. Nature. 1991 Jun 27;351(6329):754–757. doi: 10.1038/351754a0. [DOI] [PubMed] [Google Scholar]
  14. Dohrmann P. R., Butler G., Tamai K., Dorland S., Greene J. R., Thiele D. J., Stillman D. J. Parallel pathways of gene regulation: homologous regulators SWI5 and ACE2 differentially control transcription of HO and chitinase. Genes Dev. 1992 Jan;6(1):93–104. doi: 10.1101/gad.6.1.93. [DOI] [PubMed] [Google Scholar]
  15. Elledge S. J., Davis R. W. Two genes differentially regulated in the cell cycle and by DNA-damaging agents encode alternative regulatory subunits of ribonucleotide reductase. Genes Dev. 1990 May;4(5):740–751. doi: 10.1101/gad.4.5.740. [DOI] [PubMed] [Google Scholar]
  16. Epstein C. B., Cross F. R. CLB5: a novel B cyclin from budding yeast with a role in S phase. Genes Dev. 1992 Sep;6(9):1695–1706. doi: 10.1101/gad.6.9.1695. [DOI] [PubMed] [Google Scholar]
  17. Ghiara J. B., Richardson H. E., Sugimoto K., Henze M., Lew D. J., Wittenberg C., Reed S. I. A cyclin B homolog in S. cerevisiae: chronic activation of the Cdc28 protein kinase by cyclin prevents exit from mitosis. Cell. 1991 Apr 5;65(1):163–174. doi: 10.1016/0092-8674(91)90417-w. [DOI] [PubMed] [Google Scholar]
  18. Gimeno C. J., Ljungdahl P. O., Styles C. A., Fink G. R. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell. 1992 Mar 20;68(6):1077–1090. doi: 10.1016/0092-8674(92)90079-r. [DOI] [PubMed] [Google Scholar]
  19. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Johnston L. H. Cell cycle control of gene expression in yeast. Trends Cell Biol. 1992 Dec;2(12):353–357. doi: 10.1016/0962-8924(92)90041-k. [DOI] [PubMed] [Google Scholar]
  21. Kataoka T., Powers S., McGill C., Fasano O., Strathern J., Broach J., Wigler M. Genetic analysis of yeast RAS1 and RAS2 genes. Cell. 1984 Jun;37(2):437–445. doi: 10.1016/0092-8674(84)90374-x. [DOI] [PubMed] [Google Scholar]
  22. Klis F. M. Review: cell wall assembly in yeast. Yeast. 1994 Jul;10(7):851–869. doi: 10.1002/yea.320100702. [DOI] [PubMed] [Google Scholar]
  23. Koch C., Nasmyth K. Cell cycle regulated transcription in yeast. Curr Opin Cell Biol. 1994 Jun;6(3):451–459. doi: 10.1016/0955-0674(94)90039-6. [DOI] [PubMed] [Google Scholar]
  24. Kuranda M. J., Robbins P. W. Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J Biol Chem. 1991 Oct 15;266(29):19758–19767. [PubMed] [Google Scholar]
  25. Link A. J., Olson M. V. Physical map of the Saccharomyces cerevisiae genome at 110-kilobase resolution. Genetics. 1991 Apr;127(4):681–698. doi: 10.1093/genetics/127.4.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Matsumoto K., Uno I., Ishikawa T. Initiation of meiosis in yeast mutants defective in adenylate cyclase and cyclic AMP-dependent protein kinase. Cell. 1983 Feb;32(2):417–423. doi: 10.1016/0092-8674(83)90461-0. [DOI] [PubMed] [Google Scholar]
  27. Moll T., Tebb G., Surana U., Robitsch H., Nasmyth K. The role of phosphorylation and the CDC28 protein kinase in cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SWI5. Cell. 1991 Aug 23;66(4):743–758. doi: 10.1016/0092-8674(91)90118-i. [DOI] [PubMed] [Google Scholar]
  28. Nasmyth K. A repetitive DNA sequence that confers cell-cycle START (CDC28)-dependent transcription of the HO gene in yeast. Cell. 1985 Aug;42(1):225–235. doi: 10.1016/s0092-8674(85)80118-5. [DOI] [PubMed] [Google Scholar]
  29. Nasmyth K., Adolf G., Lydall D., Seddon A. The identification of a second cell cycle control on the HO promoter in yeast: cell cycle regulation of SW15 nuclear entry. Cell. 1990 Aug 24;62(4):631–647. doi: 10.1016/0092-8674(90)90110-z. [DOI] [PubMed] [Google Scholar]
  30. Nasmyth K. Control of the yeast cell cycle by the Cdc28 protein kinase. Curr Opin Cell Biol. 1993 Apr;5(2):166–179. doi: 10.1016/0955-0674(93)90099-c. [DOI] [PubMed] [Google Scholar]
  31. Nasmyth K., Dirick L. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell. 1991 Sep 6;66(5):995–1013. doi: 10.1016/0092-8674(91)90444-4. [DOI] [PubMed] [Google Scholar]
  32. Nasmyth K., Seddon A., Ammerer G. Cell cycle regulation of SW15 is required for mother-cell-specific HO transcription in yeast. Cell. 1987 May 22;49(4):549–558. doi: 10.1016/0092-8674(87)90457-0. [DOI] [PubMed] [Google Scholar]
  33. Nasmyth K., Stillman D., Kipling D. Both positive and negative regulators of HO transcription are required for mother-cell-specific mating-type switching in yeast. Cell. 1987 Feb 27;48(4):579–587. doi: 10.1016/0092-8674(87)90236-4. [DOI] [PubMed] [Google Scholar]
  34. Nugroho T. T., Mendenhall M. D. An inhibitor of yeast cyclin-dependent protein kinase plays an important role in ensuring the genomic integrity of daughter cells. Mol Cell Biol. 1994 May;14(5):3320–3328. doi: 10.1128/mcb.14.5.3320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Olson M. V., Dutchik J. E., Graham M. Y., Brodeur G. M., Helms C., Frank M., MacCollin M., Scheinman R., Frank T. Random-clone strategy for genomic restriction mapping in yeast. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7826–7830. doi: 10.1073/pnas.83.20.7826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Piatti S., Lengauer C., Nasmyth K. Cdc6 is an unstable protein whose de novo synthesis in G1 is important for the onset of S phase and for preventing a 'reductional' anaphase in the budding yeast Saccharomyces cerevisiae. EMBO J. 1995 Aug 1;14(15):3788–3799. doi: 10.1002/j.1460-2075.1995.tb00048.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Price C., Nasmyth K., Schuster T. A general approach to the isolation of cell cycle-regulated genes in the budding yeast, Saccharomyces cerevisiae. J Mol Biol. 1991 Apr 5;218(3):543–556. doi: 10.1016/0022-2836(91)90700-g. [DOI] [PubMed] [Google Scholar]
  38. Pringle J. R. Staining of bud scars and other cell wall chitin with calcofluor. Methods Enzymol. 1991;194:732–735. doi: 10.1016/0076-6879(91)94055-h. [DOI] [PubMed] [Google Scholar]
  39. Richardson H., Lew D. J., Henze M., Sugimoto K., Reed S. I. Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2. Genes Dev. 1992 Nov;6(11):2021–2034. doi: 10.1101/gad.6.11.2021. [DOI] [PubMed] [Google Scholar]
  40. Rigaud G., Roux J., Pictet R., Grange T. In vivo footprinting of rat TAT gene: dynamic interplay between the glucocorticoid receptor and a liver-specific factor. Cell. 1991 Nov 29;67(5):977–986. doi: 10.1016/0092-8674(91)90370-e. [DOI] [PubMed] [Google Scholar]
  41. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  42. Schwob E., Böhm T., Mendenhall M. D., Nasmyth K. The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell. 1994 Oct 21;79(2):233–244. doi: 10.1016/0092-8674(94)90193-7. [DOI] [PubMed] [Google Scholar]
  43. Schwob E., Nasmyth K. CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev. 1993 Jul;7(7A):1160–1175. doi: 10.1101/gad.7.7a.1160. [DOI] [PubMed] [Google Scholar]
  44. Scott J. H., Schekman R. Lyticase: endoglucanase and protease activities that act together in yeast cell lysis. J Bacteriol. 1980 May;142(2):414–423. doi: 10.1128/jb.142.2.414-423.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sloat B. F., Pringle J. R. A mutant of yeast defective in cellular morphogenesis. Science. 1978 Jun 9;200(4346):1171–1173. doi: 10.1126/science.349694. [DOI] [PubMed] [Google Scholar]
  46. Smith D. H., Brutlag D., Friedland P., Kedes L. H. BIONET: national computer resource for molecular biology. Nucleic Acids Res. 1986 Jan 10;14(1):17–20. doi: 10.1093/nar/14.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Surana U., Robitsch H., Price C., Schuster T., Fitch I., Futcher A. B., Nasmyth K. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell. 1991 Apr 5;65(1):145–161. doi: 10.1016/0092-8674(91)90416-v. [DOI] [PubMed] [Google Scholar]
  48. Tebb G., Moll T., Dowzer C., Nasmyth K. SWI5 instability may be necessary but is not sufficient for asymmetric HO expression in yeast. Genes Dev. 1993 Mar;7(3):517–528. doi: 10.1101/gad.7.3.517. [DOI] [PubMed] [Google Scholar]
  49. Toda T., Uno I., Ishikawa T., Powers S., Kataoka T., Broek D., Cameron S., Broach J., Matsumoto K., Wigler M. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell. 1985 Jan;40(1):27–36. doi: 10.1016/0092-8674(85)90305-8. [DOI] [PubMed] [Google Scholar]
  50. Vazquez de Aldana C. R., Correa J., San Segundo P., Bueno A., Nebreda A. R., Mendez E., del Rey F. Nucleotide sequence of the exo-1,3-beta-glucanase-encoding gene, EXG1, of the yeast Saccharomyces cerevisiae. Gene. 1991 Jan 15;97(2):173–182. doi: 10.1016/0378-1119(91)90049-h. [DOI] [PubMed] [Google Scholar]
  51. Wittenberg C., Sugimoto K., Reed S. I. 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):225–237. doi: 10.1016/0092-8674(90)90361-h. [DOI] [PubMed] [Google Scholar]

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