Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1992 Dec;11(13):4923–4932. doi: 10.1002/j.1460-2075.1992.tb05599.x

A new cdc gene required for S phase entry of Schizosaccharomyces pombe encodes a protein similar to the cdc 10+ and SWI4 gene products.

K Tanaka 1, K Okazaki 1, N Okazaki 1, T Ueda 1, A Sugiyama 1, H Nojima 1, H Okayama 1
PMCID: PMC556970  PMID: 1464317

Abstract

We have isolated a new cell division cycle gene (res1+) required for entry into S phase, as a multicopy dual suppressor of the pat1 and cdc10 mutants of the fission yeast Schizosaccharomyces pombe. The res1+ gene specifies a 72 kDa protein with two copies of the cdc10/SWI6 motif. A disruptant of res1+ grows poorly at 30 degrees C with severe heat- and cold-sensitivities, and completely arrests in G1 at 36 degrees C and 23 degrees C. The arrested disruptant retains a full conjugation ability. In addition to the cdc10/SWI6 motif, Res1 and SWI4 proteins share a remarkable homology in their amino-terminal region, whereas Cdc10 and SWI6 do so in their carboxy-terminal region. Moreover, the amino-terminal region is essential for the function of Res1 as it is for the function of SWI4. Furthermore, analogous to the relationship of SWI4 to SWI6, the res1+ gene effectively rescues cdc10 mutants, but the cdc10+ gene cannot rescue the res1- phenotype. Thus, striking similarities exist in both structural and functional relationships between Res1 and SWI4, and between Cdc10 and SWI6. In view of the fact that SWI4 and SWI6 form a transcription factor complex and activate promoters containing the SWI4/SWI6 dependent cell-cycle box, Res1 might be a putative association partner of Cdc10 which appears to be involved at least in the activation of promoters containing a MluI cell-cycle box.

Full text

PDF
4923

Images in this article

4924Image
on p.4924
4926Image
on p.4926
4927Image
on p.4927
4928Image
on p.4928
4929Image
on p.4929
4930Image
on p.4930

Selected References

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

  1. Andrews B. J. Gene expression. Dialogue with the cell cycle. Nature. 1992 Jan 30;355(6359):393–394. doi: 10.1038/355393a0. [DOI] [PubMed] [Google Scholar]
  2. Andrews B. J., Herskowitz I. Identification of a DNA binding factor involved in cell-cycle control of the yeast HO gene. Cell. 1989 Apr 7;57(1):21–29. doi: 10.1016/0092-8674(89)90168-2. [DOI] [PubMed] [Google Scholar]
  3. Andrews B. J., Herskowitz I. Regulation of cell cycle-dependent gene expression in yeast. J Biol Chem. 1990 Aug 25;265(24):14057–14060. [PubMed] [Google Scholar]
  4. Andrews B. J., Herskowitz I. The yeast SWI4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle-dependent transcription. Nature. 1989 Dec 14;342(6251):830–833. doi: 10.1038/342830a0. [DOI] [PubMed] [Google Scholar]
  5. Aves S. J., Durkacz B. W., Carr A., Nurse P. Cloning, sequencing and transcriptional control of the Schizosaccharomyces pombe cdc10 'start' gene. EMBO J. 1985 Feb;4(2):457–463. doi: 10.1002/j.1460-2075.1985.tb03651.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blank V., Kourilsky P., Israël A. NF-kappa B and related proteins: Rel/dorsal homologies meet ankyrin-like repeats. Trends Biochem Sci. 1992 Apr;17(4):135–140. doi: 10.1016/0968-0004(92)90321-y. [DOI] [PubMed] [Google Scholar]
  7. Bours V., Villalobos J., Burd P. R., Kelly K., Siebenlist U. Cloning of a mitogen-inducible gene encoding a kappa B DNA-binding protein with homology to the rel oncogene and to cell-cycle motifs. Nature. 1990 Nov 1;348(6296):76–80. doi: 10.1038/348076a0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Breeden L., Nasmyth K. Similarity between cell-cycle genes of budding yeast and fission yeast and the Notch gene of Drosophila. Nature. 1987 Oct 15;329(6140):651–654. doi: 10.1038/329651a0. [DOI] [PubMed] [Google Scholar]
  10. Cross F., Roberts J., Weintraub H. Simple and complex cell cycles. Annu Rev Cell Biol. 1989;5:341–396. doi: 10.1146/annurev.cb.05.110189.002013. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Egel R., Egel-Mitani M. Premeiotic DNA synthesis in fission yeast. Exp Cell Res. 1974 Sep;88(1):127–134. doi: 10.1016/0014-4827(74)90626-0. [DOI] [PubMed] [Google Scholar]
  13. Forsburg S. L., Nurse P. Cell cycle regulation in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Annu Rev Cell Biol. 1991;7:227–256. doi: 10.1146/annurev.cb.07.110191.001303. [DOI] [PubMed] [Google Scholar]
  14. Gordon C. B., Fantes P. A. The cdc22 gene of Schizosaccharomyces pombe encodes a cell cycle-regulated transcript. EMBO J. 1986 Nov;5(11):2981–2985. doi: 10.1002/j.1460-2075.1986.tb04595.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grallert B., Sipiczki M. Common genes and pathways in the regulation of the mitotic and meiotic cell cycles of Schizosaccharomyces pombe. Curr Genet. 1991 Aug;20(3):199–204. doi: 10.1007/BF00326233. [DOI] [PubMed] [Google Scholar]
  16. Haskill S., Beg A. A., Tompkins S. M., Morris J. S., Yurochko A. D., Sampson-Johannes A., Mondal K., Ralph P., Baldwin A. S., Jr Characterization of an immediate-early gene induced in adherent monocytes that encodes I kappa B-like activity. Cell. 1991 Jun 28;65(7):1281–1289. doi: 10.1016/0092-8674(91)90022-q. [DOI] [PubMed] [Google Scholar]
  17. Igarashi M., Nagata A., Jinno S., Suto K., Okayama H. Wee1(+)-like gene in human cells. Nature. 1991 Sep 5;353(6339):80–83. doi: 10.1038/353080a0. [DOI] [PubMed] [Google Scholar]
  18. Johnston L. H., Lowndes N. F. Cell cycle control of DNA synthesis in budding yeast. Nucleic Acids Res. 1992 May 25;20(10):2403–2410. doi: 10.1093/nar/20.10.2403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kieran M., Blank V., Logeat F., Vandekerckhove J., Lottspeich F., Le Bail O., Urban M. B., Kourilsky P., Baeuerle P. A., Israël A. The DNA binding subunit of NF-kappa B is identical to factor KBF1 and homologous to the rel oncogene product. Cell. 1990 Sep 7;62(5):1007–1018. doi: 10.1016/0092-8674(90)90275-j. [DOI] [PubMed] [Google Scholar]
  20. LaMarco K., Thompson C. C., Byers B. P., Walton E. M., McKnight S. L. Identification of Ets- and notch-related subunits in GA binding protein. Science. 1991 Aug 16;253(5021):789–792. doi: 10.1126/science.1876836. [DOI] [PubMed] [Google Scholar]
  21. Lowndes N. F., Johnson A. L., Breeden L., Johnston L. H. SWI6 protein is required for transcription of the periodically expressed DNA synthesis genes in budding yeast. Nature. 1992 Jun 11;357(6378):505–508. doi: 10.1038/357505a0. [DOI] [PubMed] [Google Scholar]
  22. Lowndes N. F., Johnson A. L., Johnston L. H. Coordination of expression of DNA synthesis genes in budding yeast by a cell-cycle regulated trans factor. Nature. 1991 Mar 21;350(6315):247–250. doi: 10.1038/350247a0. [DOI] [PubMed] [Google Scholar]
  23. Lowndes N. F., McInerny C. J., Johnson A. L., Fantes P. A., Johnston L. H. Control of DNA synthesis genes in fission yeast by the cell-cycle gene cdc10+. Nature. 1992 Jan 30;355(6359):449–453. doi: 10.1038/355449a0. [DOI] [PubMed] [Google Scholar]
  24. Marks J., Fankhauser C., Reymond A., Simanis V. Cytoskeletal and DNA structure abnormalities result from bypass of requirement for the cdc10 start gene in the fission yeast Schizosaccharomyces pombe. J Cell Sci. 1992 Mar;101(Pt 3):517–528. doi: 10.1242/jcs.101.3.517. [DOI] [PubMed] [Google Scholar]
  25. McLeod M., Beach D. Homology between the ran1+ gene of fission yeast and protein kinases. EMBO J. 1986 Dec 20;5(13):3665–3671. doi: 10.1002/j.1460-2075.1986.tb04697.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nagata A., Igarashi M., Jinno S., Suto K., Okayama H. An additional homolog of the fission yeast cdc25+ gene occurs in humans and is highly expressed in some cancer cells. New Biol. 1991 Oct;3(10):959–968. [PubMed] [Google Scholar]
  27. Nasmyth K. A. FAR-reaching discoveries about the regulation of START. Cell. 1990 Dec 21;63(6):1117–1120. doi: 10.1016/0092-8674(90)90404-3. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Nurse P., Bissett Y. Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature. 1981 Aug 6;292(5823):558–560. doi: 10.1038/292558a0. [DOI] [PubMed] [Google Scholar]
  30. Nurse P. Genetic control of cell size at cell division in yeast. Nature. 1975 Aug 14;256(5518):547–551. doi: 10.1038/256547a0. [DOI] [PubMed] [Google Scholar]
  31. Ogas J., Andrews B. J., Herskowitz I. Transcriptional activation of CLN1, CLN2, and a putative new G1 cyclin (HCS26) by SWI4, a positive regulator of G1-specific transcription. Cell. 1991 Sep 6;66(5):1015–1026. doi: 10.1016/0092-8674(91)90445-5. [DOI] [PubMed] [Google Scholar]
  32. Ohno H., Takimoto G., McKeithan T. W. The candidate proto-oncogene bcl-3 is related to genes implicated in cell lineage determination and cell cycle control. Cell. 1990 Mar 23;60(6):991–997. doi: 10.1016/0092-8674(90)90347-h. [DOI] [PubMed] [Google Scholar]
  33. Okazaki K., Okazaki N., Kume K., Jinno S., Tanaka K., Okayama H. High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res. 1990 Nov 25;18(22):6485–6489. doi: 10.1093/nar/18.22.6485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Okazaki N., Okazaki K., Tanaka K., Okayama H. The ste4+ gene, essential for sexual differentiation of Schizosaccharomyces pombe, encodes a protein with a leucine zipper motif. Nucleic Acids Res. 1991 Dec;19(25):7043–7047. doi: 10.1093/nar/19.25.7043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Primig M., Sockanathan S., Auer H., Nasmyth K. Anatomy of a transcription factor important for the start of the cell cycle in Saccharomyces cerevisiae. Nature. 1992 Aug 13;358(6387):593–597. doi: 10.1038/358593a0. [DOI] [PubMed] [Google Scholar]
  36. Reed S. I. G1-specific cyclins: in search of an S-phase-promoting factor. Trends Genet. 1991 Mar;7(3):95–99. doi: 10.1016/0168-9525(91)90279-Y. [DOI] [PubMed] [Google Scholar]
  37. Richardson H. E., Wittenberg C., Cross F., Reed S. I. An essential G1 function for cyclin-like proteins in yeast. Cell. 1989 Dec 22;59(6):1127–1133. doi: 10.1016/0092-8674(89)90768-x. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Stern M., Jensen R., Herskowitz I. Five SWI genes are required for expression of the HO gene in yeast. J Mol Biol. 1984 Oct 5;178(4):853–868. doi: 10.1016/0022-2836(84)90315-2. [DOI] [PubMed] [Google Scholar]
  40. Taba M. R., Muroff I., Lydall D., Tebb G., Nasmyth K. Changes in a SWI4,6-DNA-binding complex occur at the time of HO gene activation in yeast. Genes Dev. 1991 Nov;5(11):2000–2013. doi: 10.1101/gad.5.11.2000. [DOI] [PubMed] [Google Scholar]
  41. 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]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES