A yeast gene essential for regulation of spindle pole duplication

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.

[1]  L. Hartwell,et al.  The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. , 1988, Science.

[2]  G. Schatten,et al.  Centrosome detection in sea urchin eggs with a monoclonal antibody against Drosophila intermediate filament proteins: characterization of stages of the division cycle of centrosomes. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Michael Wigler,et al.  Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase , 1987, Cell.

[4]  M. Wigler,et al.  Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae , 1987, Molecular and cellular biology.

[5]  G. Fink,et al.  KAR1, a gene required for function of both intranuclear and extranuclear microtubules in yeast , 1987, Cell.

[6]  C. Rieder,et al.  The reproduction of centrosomes: nuclear versus cytoplasmic controls , 1986, The Journal of cell biology.

[7]  B. Byers,et al.  Yeast gene required for spindle pole body duplication: homology of its product with Ca2+-binding proteins. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. Botstein,et al.  A gene required for the separation of chromosomes on the spindle apparatus in yeast , 1986, Cell.

[9]  H. Zimmermann,et al.  Radiation induced formation of giant cells inSaccharomyces uvarum III: Effect of X-rays on nuclear division , 1986, Radiation and environmental biophysics.

[10]  S. Powers Control of the cell cycle in yeast , 1985, Nature.

[11]  R. E. Esposito,et al.  Genetic map of Saccharomyces cerevisiae, edition 9. , 1985, Microbiological reviews.

[12]  S. Reed,et al.  Protein kinase activity associated with the product of the yeast cell division cycle gene CDC28. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Olson,et al.  An electrophoretic karyotype for yeast. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[14]  L. Hartwell,et al.  Genetic analysis of the mitotic transmission of minichromosomes , 1985, Cell.

[15]  H. Ris,et al.  Centriole distribution during tripolar mitosis in Chinese hamster ovary cells , 1984, The Journal of cell biology.

[16]  S. A. Moore,et al.  Synchronous cell growth occurs upon synchronizing the two regulatory steps of the Saccharomyces cerevisiae cell cycle. , 1984, Experimental cell research.

[17]  J. Pringle,et al.  Relationship of actin and tubulin distribution to bud growth in wild- type and morphogenetic-mutant Saccharomyces cerevisiae , 1984, The Journal of cell biology.

[18]  R. Kuriyama,et al.  Microtubule-organizing centers abnormal in number, structure, and nucleating activity in x-irradiated mammalian cells , 1983, The Journal of cell biology.

[19]  J. Kilmartin,et al.  Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line , 1982, The Journal of cell biology.

[20]  K. Matsumoto,et al.  Isolation and characterization of yeast mutants deficient in adenylate cyclase and cAMP-dependent protein kinase. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[21]  G. Borisy,et al.  Centriole cycle in Chinese hamster ovary cells as determined by whole- mount electron microscopy , 1981, The Journal of cell biology.

[22]  R. Mortimer,et al.  An endomitotic effect of a cell cycle mutation of Saccharomyces cerevisiae. , 1981, Genetics.

[23]  G. Fink,et al.  Methods in yeast genetics , 1979 .

[24]  P Berg,et al.  Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. , 1977, Journal of molecular biology.

[25]  G C Johnston,et al.  Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. , 1977, Experimental cell research.

[26]  B. Byers,et al.  Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae , 1975, Journal of bacteriology.

[27]  L. Hartwell Saccharomyces cerevisiae cell cycle. , 1974, Bacteriological reviews.

[28]  B. Byers,et al.  Duplication of spindle plaques and integration of the yeast cell cycle. , 1974, Cold Spring Harbor symposia on quantitative biology.

[29]  S. Phillips,et al.  INDEPENDENCE OF CENTRIOLE FORMATION AND DNA SYNTHESIS , 1973, The Journal of cell biology.

[30]  L. Hartwell,et al.  Reversible arrest of haploid yeast cells in the initiation of DNA synthesis by a diffusible sex factor. , 1973, Experimental cell research.

[31]  L. Hartwell Synchronization of haploid yeast cell cycles, a prelude to conjugation. , 1973, Experimental cell research.

[32]  G. Simchen,et al.  Sporulation in Saccharomyces cerevisiae: premeiotic DNA synthesis, readiness and commitment. , 1972, Experimental cell research.

[33]  L. Thompson,et al.  Proliferation kinetics of x-irradiated mouse L cells studied WITH TIME-lapse photography. II. , 1969, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[34]  E. Robbins,et al.  THE CENTRIOLE CYCLE IN SYNCHRONIZED HELA CELLS , 1968, The Journal of cell biology.

[35]  L. Hartwell,et al.  Macromolecule Synthesis in Temperature-sensitive Mutants of Yeast , 1967, Journal of bacteriology.

[36]  J. Gall Centriole replication. A study of spermatogenesis in the snail Viviparus. , 1961 .

[37]  D. Mazia,et al.  The Multiplicity of the Mitotic Centers and the Time-Course of Their Duplication and Separation , 1960, The Journal of biophysical and biochemical cytology.

[38]  V. W. Burns X-ray-induced division delay of individual yeast cells. , 1956, Radiation research.

[39]  H. Roman Studies of gene mutation in Saccharomyces. , 1956, Cold Spring Harbor symposia on quantitative biology.

[40]  D. D. Perkins Biochemical Mutants in the Smut Fungus Ustilago Maydis. , 1949, Genetics.

[41]  E. B. Harvey A COMPARISON OF THE DEVELOPMENT OF NUCLEATE AND NON-NUCLEATE EGGS OF ARBACIA PUNCTULATA , 1940 .

[42]  J. Huxley,et al.  The Cell in Development and Heredity , 1925, Nature.