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. 1991 Jul;11(7):3691–3698. doi: 10.1128/mcb.11.7.3691

Protein synthesis requirements for nuclear division, cytokinesis, and cell separation in Saccharomyces cerevisiae.

D J Burke 1, D Church 1
PMCID: PMC361131  PMID: 2046672

Abstract

Protein synthesis inhibitors have often been used to identify regulatory steps in cell division. We used cell division cycle mutants of the yeast Saccharomyces cerevisiae and two chemical inhibitors of translation to investigate the requirements for protein synthesis for completing landmark events after the G1 phase of the cell cycle. We show, using cdc2, cdc6, cdc7, cdc8, cdc17 (38 degrees C), and cdc21 (also named tmp1) mutants, that cells arrested in S phase complete DNA synthesis but cannot complete nuclear division if protein synthesis is inhibited. In contrast, we show, using cdc16, cdc17 (36 degrees C), cdc20, cdc23, and nocodazole treatment, that cells that arrest in the G2 stage complete nuclear division in the absence of protein synthesis. Protein synthesis is required late in the cell cycle to complete cytokinesis and cell separation. These studies show that there are requirements for protein synthesis in the cell cycle, after G1, that are restricted to two discrete intervals.

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Selected References

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

  1. Burke D., Gasdaska P., Hartwell L. Dominant effects of tubulin overexpression in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Mar;9(3):1049–1059. doi: 10.1128/mcb.9.3.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cross S. L., Smith M. M. Comparison of the structure and cell cycle expression of mRNAs encoded by two histone H3-H4 loci in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Feb;8(2):945–954. doi: 10.1128/mcb.8.2.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dubé F. Effect of reduced protein synthesis on the cell cycle in sea urchin embryos. J Cell Physiol. 1988 Dec;137(3):545–552. doi: 10.1002/jcp.1041370321. [DOI] [PubMed] [Google Scholar]
  4. Elliott S. G., McLaughlin C. S. Synthesis and modification of proteins during the cell cycle of the yeast Saccharomyces cerevisiae. J Bacteriol. 1979 Mar;137(3):1185–1190. doi: 10.1128/jb.137.3.1185-1190.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Evans T., Rosenthal E. T., Youngblom J., Distel D., Hunt T. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell. 1983 Jun;33(2):389–396. doi: 10.1016/0092-8674(83)90420-8. [DOI] [PubMed] [Google Scholar]
  6. Fantes P. A. Dependency relations between events in mitosis in Schizosaccharomyces pombe. J Cell Sci. 1982 Jun;55:383–402. doi: 10.1242/jcs.55.1.383. [DOI] [PubMed] [Google Scholar]
  7. Hadwiger J. A., Wittenberg C., Richardson H. E., de Barros Lopes M., Reed S. I. A family of cyclin homologs that control the G1 phase in yeast. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6255–6259. doi: 10.1073/pnas.86.16.6255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hartwell L. H., Culotti J., Pringle J. R., Reid B. J. Genetic control of the cell division cycle in yeast. Science. 1974 Jan 11;183(4120):46–51. doi: 10.1126/science.183.4120.46. [DOI] [PubMed] [Google Scholar]
  9. Hartwell L. H. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res. 1971 Dec;69(2):265–276. doi: 10.1016/0014-4827(71)90223-0. [DOI] [PubMed] [Google Scholar]
  10. Hartwell L. H. Macromolecule synthesis in temperature-sensitive mutants of yeast. J Bacteriol. 1967 May;93(5):1662–1670. doi: 10.1128/jb.93.5.1662-1670.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hartwell L. H. Saccharomyces cerevisiae cell cycle. Bacteriol Rev. 1974 Jun;38(2):164–198. doi: 10.1128/br.38.2.164-198.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hartwell L. H. Sequential function of gene products relative to DNA synthesis in the yeast cell cycle. J Mol Biol. 1976 Jul 15;104(4):803–817. doi: 10.1016/0022-2836(76)90183-2. [DOI] [PubMed] [Google Scholar]
  13. Hereford L. M., Hartwell L. H. Role of protein synthesis in the replication of yeast DNA. Nat New Biol. 1973 Aug 1;244(135):129–131. doi: 10.1038/newbio244129a0. [DOI] [PubMed] [Google Scholar]
  14. Hereford L. M., Hartwell L. H. Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis. J Mol Biol. 1974 Apr 15;84(3):445–461. doi: 10.1016/0022-2836(74)90451-3. [DOI] [PubMed] [Google Scholar]
  15. Jacobs C. W., Adams A. E., Szaniszlo P. J., Pringle J. R. Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J Cell Biol. 1988 Oct;107(4):1409–1426. doi: 10.1083/jcb.107.4.1409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Johnston G. C., Pringle J. R., Hartwell L. H. Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp Cell Res. 1977 Mar 1;105(1):79–98. doi: 10.1016/0014-4827(77)90154-9. [DOI] [PubMed] [Google Scholar]
  17. Lörincz A. T., Miller M. J., Xuong N. H., Geiduschek E. P. Identification of proteins whose synthesis is modulated during the cell cycle of Saccharomyces cerevisiae. Mol Cell Biol. 1982 Dec;2(12):1532–1549. doi: 10.1128/mcb.2.12.1532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McCarroll R. M., Fangman W. L. Time of replication of yeast centromeres and telomeres. Cell. 1988 Aug 12;54(4):505–513. doi: 10.1016/0092-8674(88)90072-4. [DOI] [PubMed] [Google Scholar]
  19. McIntosh J. R., Koonce M. P. Mitosis. Science. 1989 Nov 3;246(4930):622–628. doi: 10.1126/science.2683078. [DOI] [PubMed] [Google Scholar]
  20. Minshull J., Blow J. J., Hunt T. Translation of cyclin mRNA is necessary for extracts of activated xenopus eggs to enter mitosis. Cell. 1989 Mar 24;56(6):947–956. doi: 10.1016/0092-8674(89)90628-4. [DOI] [PubMed] [Google Scholar]
  21. Minshull J., Pines J., Golsteyn R., Standart N., Mackie S., Colman A., Blow J., Ruderman J. V., Wu M., Hunt T. The role of cyclin synthesis, modification and destruction in the control of cell division. J Cell Sci Suppl. 1989;12:77–97. doi: 10.1242/jcs.1989.supplement_12.8. [DOI] [PubMed] [Google Scholar]
  22. Moir D., Botstein D. Determination of the order of gene function in the yeast nuclear division pathway using cs and ts mutants. Genetics. 1982 Apr;100(4):565–577. doi: 10.1093/genetics/100.4.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moreno S., Nurse P., Russell P. Regulation of mitosis by cyclic accumulation of p80cdc25 mitotic inducer in fission yeast. Nature. 1990 Apr 5;344(6266):549–552. doi: 10.1038/344549a0. [DOI] [PubMed] [Google Scholar]
  24. Murray A. W. Cyclin synthesis and degradation and the embryonic cell cycle. J Cell Sci Suppl. 1989;12:65–76. doi: 10.1242/jcs.1989.supplement_12.7. [DOI] [PubMed] [Google Scholar]
  25. Murray A. W., Kirschner M. W. Cyclin synthesis drives the early embryonic cell cycle. Nature. 1989 May 25;339(6222):275–280. doi: 10.1038/339275a0. [DOI] [PubMed] [Google Scholar]
  26. Murray A. W., Solomon M. J., Kirschner M. W. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature. 1989 May 25;339(6222):280–286. doi: 10.1038/339280a0. [DOI] [PubMed] [Google Scholar]
  27. Pardee A. B. G1 events and regulation of cell proliferation. Science. 1989 Nov 3;246(4930):603–608. doi: 10.1126/science.2683075. [DOI] [PubMed] [Google Scholar]
  28. Reed S. I., Wittenberg C. Mitotic role for the Cdc28 protein kinase of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5697–5701. doi: 10.1073/pnas.87.15.5697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Russell P., Moreno S., Reed S. I. Conservation of mitotic controls in fission and budding yeasts. Cell. 1989 Apr 21;57(2):295–303. doi: 10.1016/0092-8674(89)90967-7. [DOI] [PubMed] [Google Scholar]
  30. Sclafani R. A., Fangman W. L. Thymidine utilization by tut mutants and facile cloning of mutant alleles by plasmid conversion in S. cerevisiae. Genetics. 1986 Nov;114(3):753–767. doi: 10.1093/genetics/114.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shilo B., Riddle V. G., Pardee A. B. Protein turnover and cell-cycle initiation in yeast. Exp Cell Res. 1979 Oct 15;123(2):221–227. doi: 10.1016/0014-4827(79)90462-2. [DOI] [PubMed] [Google Scholar]
  32. Shilo B., Simchen G., Pardee A. B. Regulation of cell-cycle initiation in yeast by nutrients and protein synthesis. J Cell Physiol. 1978 Nov;97(2):177–187. doi: 10.1002/jcp.1040970207. [DOI] [PubMed] [Google Scholar]
  33. Swenson K. I., Farrell K. M., Ruderman J. V. The clam embryo protein cyclin A induces entry into M phase and the resumption of meiosis in Xenopus oocytes. Cell. 1986 Dec 26;47(6):861–870. doi: 10.1016/0092-8674(86)90801-9. [DOI] [PubMed] [Google Scholar]
  34. Unger M. W., Hartwell L. H. Control of cell division in Saccharomyces cerevisiae by methionyl-tRNA. Proc Natl Acad Sci U S A. 1976 May;73(5):1664–1668. doi: 10.1073/pnas.73.5.1664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weinert T. A., Hartwell L. H. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science. 1988 Jul 15;241(4863):317–322. doi: 10.1126/science.3291120. [DOI] [PubMed] [Google Scholar]
  36. Whitfield W. G., Gonzalez C., Maldonado-Codina G., Glover D. M. The A- and B-type cyclins of Drosophila are accumulated and destroyed in temporally distinct events that define separable phases of the G2-M transition. EMBO J. 1990 Aug;9(8):2563–2572. doi: 10.1002/j.1460-2075.1990.tb07437.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Williamson D. H., Fennell D. J. The use of fluorescent DNA-binding agent for detecting and separating yeast mitochondrial DNA. Methods Cell Biol. 1975;12:335–351. doi: 10.1016/s0091-679x(08)60963-2. [DOI] [PubMed] [Google Scholar]
  38. Williamson D. H. Replication of the nuclear genome in yeast does not require concomitant protein synthesis. Biochem Biophys Res Commun. 1973 Jun 8;52(3):731–740. doi: 10.1016/0006-291x(73)90998-4. [DOI] [PubMed] [Google Scholar]
  39. Wood J. S., Hartwell L. H. A dependent pathway of gene functions leading to chromosome segregation in Saccharomyces cerevisiae. J Cell Biol. 1982 Sep;94(3):718–726. doi: 10.1083/jcb.94.3.718. [DOI] [PMC free article] [PubMed] [Google Scholar]

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