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. 1988 Dec;8(12):5386–5397. doi: 10.1128/mcb.8.12.5386

A yeast gene essential for regulation of spindle pole duplication.

P Baum 1, C Yip 1, L Goetsch 1, B Byers 1
PMCID: PMC365641  PMID: 3072479

Abstract

In eucaryotic cells, duplication of spindle poles must be coordinated with other cell cycle functions. We report here the identification in Saccharomyces cerevisiae of a temperature-sensitive lethal mutation, esp1, that deregulates spindle pole duplication. Mutant cells transferred to the nonpermissive temperature became unable to continue DNA synthesis and cell division but displayed repeated duplication of their spindle pole bodies. Although entry into this state after transient challenge by the nonpermissive temperature was largely lethal, rare survivors were recovered and found to have become increased in ploidy. If the mutant cells were held in G0 or G1 during exposure to the elevated temperature, they remained viable and maintained normal numbers of spindle poles. These results suggest dual regulation of spindle pole duplication, including a mechanism that promotes duplication as cells enter the division cycle and a negative regulatory mechanism, controlled by ESP1, that limits duplication to a single occurrence in each cell division cycle. Tetrad analysis has revealed that ESP1 resides at a previously undescribed locus on the right arm of chromosome VII.

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Selected References

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

  1. Adams A. E., Pringle J. R. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol. 1984 Mar;98(3):934–945. doi: 10.1083/jcb.98.3.934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BURNS V. W. X-ray-induced division delay of individual yeast cells. Radiat Res. 1956 May;4(5):394–412. [PubMed] [Google Scholar]
  3. Baum P., Furlong C., Byers B. Yeast gene required for spindle pole body duplication: homology of its product with Ca2+-binding proteins. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5512–5516. doi: 10.1073/pnas.83.15.5512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baumstark-Khan C., Rink H., Zimmermann H. P. Radiation induced formation of giant cells in Saccharomyces uvarum. III: Effect of X-rays on nuclear division. Radiat Environ Biophys. 1986;25(1):23–30. doi: 10.1007/BF01209681. [DOI] [PubMed] [Google Scholar]
  5. Brunborg G., Williamson D. H. The relevance of the nuclear division cycle to radiosensitivity in yeast. Mol Gen Genet. 1978 Jul 4;162(3):277–286. doi: 10.1007/BF00268853. [DOI] [PubMed] [Google Scholar]
  6. Byers B., Goetsch L. Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae. J Bacteriol. 1975 Oct;124(1):511–523. doi: 10.1128/jb.124.1.511-523.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Byers B., Goetsch L. Duplication of spindle plaques and integration of the yeast cell cycle. Cold Spring Harb Symp Quant Biol. 1974;38:123–131. doi: 10.1101/sqb.1974.038.01.016. [DOI] [PubMed] [Google Scholar]
  8. Bücking-Throm E., Duntze W., Hartwell L. H., Manney T. R. Reversible arrest of haploid yeast cells in the initiation of DNA synthesis by a diffusible sex factor. Exp Cell Res. 1973 Jan;76(1):99–110. doi: 10.1016/0014-4827(73)90424-2. [DOI] [PubMed] [Google Scholar]
  9. Carle G. F., Olson M. V. An electrophoretic karyotype for yeast. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3756–3760. doi: 10.1073/pnas.82.11.3756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dawes I. W., Hardie I. D. Selective killing of vegetative cells in sporulated yeast cultures by exposure to diethyl ether. Mol Gen Genet. 1974;131(4):281–289. doi: 10.1007/BF00264859. [DOI] [PubMed] [Google Scholar]
  11. GALL J. G. Centriole replication. A study of spermatogenesis in the snail Viviparus. J Biophys Biochem Cytol. 1961 Jun;10:163–193. doi: 10.1083/jcb.10.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Hartwell L. H. Synchronization of haploid yeast cell cycles, a prelude to conjugation. Exp Cell Res. 1973 Jan;76(1):111–117. doi: 10.1016/0014-4827(73)90425-4. [DOI] [PubMed] [Google Scholar]
  15. Ikegami S., Amemiya S., Oguro M., Nagano H., Mano Y. Inhibition by aphidicolin of cell cycle progression and DNA replication in sea urchin embryos. J Cell Physiol. 1979 Sep;100(3):439–444. doi: 10.1002/jcp.1041000307. [DOI] [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. KISSANE J. M., ROBINS E. The fluorometric measurement of deoxyribonucleic acid in animal tissues with special reference to the central nervous system. J Biol Chem. 1958 Jul;233(1):184–188. [PubMed] [Google Scholar]
  18. Keryer G., Ris H., Borisy G. G. Centriole distribution during tripolar mitosis in Chinese hamster ovary cells. J Cell Biol. 1984 Jun;98(6):2222–2229. doi: 10.1083/jcb.98.6.2222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kilmartin J. V., Wright B., Milstein C. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J Cell Biol. 1982 Jun;93(3):576–582. doi: 10.1083/jcb.93.3.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Koshland D., Kent J. C., Hartwell L. H. Genetic analysis of the mitotic transmission of minichromosomes. Cell. 1985 Feb;40(2):393–403. doi: 10.1016/0092-8674(85)90153-9. [DOI] [PubMed] [Google Scholar]
  21. Kuriyama R., Borisy G. G. Centriole cycle in Chinese hamster ovary cells as determined by whole-mount electron microscopy. J Cell Biol. 1981 Dec;91(3 Pt 1):814–821. doi: 10.1083/jcb.91.3.814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Matsumoto K., Uno I., Oshima Y., Ishikawa T. Isolation and characterization of yeast mutants deficient in adenylate cyclase and cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2355–2359. doi: 10.1073/pnas.79.7.2355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moens P. B., Rapport E. Spindles, spindle plaques, and meiosis in the yeast Saccharomyces cerevisiae (Hansen). J Cell Biol. 1971 Aug;50(2):344–361. doi: 10.1083/jcb.50.2.344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Moore S. A. Synchronous cell growth occurs upon synchronizing the two regulatory steps of the Saccharomyces cerevisiae cell cycle. Exp Cell Res. 1984 Apr;151(2):542–556. doi: 10.1016/0014-4827(84)90402-6. [DOI] [PubMed] [Google Scholar]
  25. Mortimer R. K., Schild D. Genetic map of Saccharomyces cerevisiae, edition 9. Microbiol Rev. 1985 Sep;49(3):181–213. doi: 10.1128/mr.49.3.181-213.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nishioka D., Balczon R., Schatten G. Relationships between DNA synthesis and mitotic events in fertilized sea urchin eggs: aphidicolin inhibits DNA synthesis, nuclear breakdown and proliferation of microtubule organizing centers, but not cycles of microtubule assembly. Cell Biol Int Rep. 1984 Apr;8(4):337–346. doi: 10.1016/0309-1651(84)90161-9. [DOI] [PubMed] [Google Scholar]
  27. Perkins D. D. Biochemical Mutants in the Smut Fungus Ustilago Maydis. Genetics. 1949 Sep;34(5):607–626. doi: 10.1093/genetics/34.5.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. ROMAN H. Studies of gene mutation in Saccharomyces. Cold Spring Harb Symp Quant Biol. 1956;21:175–185. doi: 10.1101/sqb.1956.021.01.015. [DOI] [PubMed] [Google Scholar]
  29. Rattner J. B., Phillips S. G. Independence of centriole formation and DNA synthesis. J Cell Biol. 1973 May;57(2):359–372. doi: 10.1083/jcb.57.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Reed S. I., Hadwiger J. A., Lörincz A. T. Protein kinase activity associated with the product of the yeast cell division cycle gene CDC28. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4055–4059. doi: 10.1073/pnas.82.12.4055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  32. Robbins E., Jentzsch G., Micali A. The centriole cycle in synchronized HeLa cells. J Cell Biol. 1968 Feb;36(2):329–339. doi: 10.1083/jcb.36.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rose M. D., Fink G. R. KAR1, a gene required for function of both intranuclear and extranuclear microtubules in yeast. Cell. 1987 Mar 27;48(6):1047–1060. doi: 10.1016/0092-8674(87)90712-4. [DOI] [PubMed] [Google Scholar]
  34. Sato C., Kuriyama R., Nishizawa K. Microtubule-organizing centers abnormal in number, structure, and nucleating activity in x-irradiated mammalian cells. J Cell Biol. 1983 Mar;96(3):776–782. doi: 10.1083/jcb.96.3.776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schatten H., Walter M., Mazia D., Biessmann H., Paweletz N., Coffe G., Schatten G. Centrosome detection in sea urchin eggs with a monoclonal antibody against Drosophila intermediate filament proteins: characterization of stages of the division cycle of centrosomes. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8488–8492. doi: 10.1073/pnas.84.23.8488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schild D., Ananthaswamy H. N., Mortimer R. K. An endomitotic effect of a cell cycle mutation of Saccharomyces cerevisiae. Genetics. 1981 Mar-Apr;97(3-4):551–562. doi: 10.1093/genetics/97.3-4.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Simchen G., Piñon R., Salts Y. Sporulation in Saccharomyces cerevisiae: premeiotic DNA synthesis, readiness and commitment. Exp Cell Res. 1972 Nov;75(1):207–218. doi: 10.1016/0014-4827(72)90538-1. [DOI] [PubMed] [Google Scholar]
  38. Sluder G., Miller F. J., Rieder C. L. The reproduction of centrosomes: nuclear versus cytoplasmic controls. J Cell Biol. 1986 Nov;103(5):1873–1881. doi: 10.1083/jcb.103.5.1873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Thomas J. H., Botstein D. A gene required for the separation of chromosomes on the spindle apparatus in yeast. Cell. 1986 Jan 17;44(1):65–76. doi: 10.1016/0092-8674(86)90485-x. [DOI] [PubMed] [Google Scholar]
  40. Thompson L. H., Suit H. D. Proliferation kinetics of x-irradiated mouse L cells studied WITH TIME-lapse photography. II. Int J Radiat Biol Relat Stud Phys Chem Med. 1969;15(4):347–362. doi: 10.1080/09553006914550571. [DOI] [PubMed] [Google Scholar]
  41. Toda T., Cameron S., Sass P., Zoller M., Scott J. D., McMullen B., Hurwitz M., Krebs E. G., Wigler M. Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Apr;7(4):1371–1377. doi: 10.1128/mcb.7.4.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Toda T., Cameron S., Sass P., Zoller M., Wigler M. Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell. 1987 Jul 17;50(2):277–287. doi: 10.1016/0092-8674(87)90223-6. [DOI] [PubMed] [Google Scholar]
  43. Vorobjev I. A., Chentsov YuS Centrioles in the cell cycle. I. Epithelial cells. J Cell Biol. 1982 Jun;93(3):938–949. doi: 10.1083/jcb.93.3.938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]

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