Skip to main content
Log in

DNA polymerase δ is required for the replication feedback control of cell cycle progression in Schizosaccharomyces pombe

  • Original Paper
  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Abstract

DNA replication and DNA repair are essential cell cycle steps ensuring correct transmission of the genome. The feedback replication control system links mitosis to completion of DNA replication and partially overlaps the radiation checkpoint control. Deletion of the chkl/rad27 gene abolishes the radiation but not the replication feedback control. Thermosensitive mutations in the DNA polymerase λ, cdc18 or cdc20 genes lead cells to arrest in the S phase of the cell cycle. We show that strains carrying any of these mutations enter lethal mitosis in the absence of the radiation checkpoint chk1/rad27. We interpret these data as an indication that an assembled replisome is essential for replication dependent control of mitosis and we propose that the arrest of the cell cycle in the thermosensitive mutants is due to the chk1 +/rad27 + pathway, which monitors directly DNA for signs of damage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Al-Khodairy F, Carr AM (1992) DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe. EMBO J 11:1343–1350

    Google Scholar 

  • Al-Khodairy F, Fotou E, Sheldrick KS, Griffith DJF, Lehmann AR, Carr AM (1994) Identification and characterization of new elements involved in checkpoint and feedback controls in fission yeast. Mol Biol Cell 5: 147–160

    Google Scholar 

  • Beach D, Rodgers L, Gould J (1985) RAN1+ controls the transition from mitotic division to meiosis in fission yeast. Curr Genet 10:297–311

    Google Scholar 

  • Boulet A, Simon M, Faye G, Bauer GA, Burgers PMJ (1989) Structure and function of the Saccharomyces cerevisiae CDC2 gene encoding the large subunit of DNA polymerase III. EMBO J 8:1849–1854

    Google Scholar 

  • Damagnez V, Tillit J, De Recondo A-M, Baldacci G (1991) The POL1 gene from the fission yeast, Schizosaccharomyces pombe, shows conserved amino acid blocks specific for eukaryotic DNA polymerases alpha. Mol Gen Genet 226:182–189

    Google Scholar 

  • Enoch T, Nurse P (1990) Mutation of fission yeast cell cycle control genes abolishes dependence of mitosis on DNA replication. Cell 60:665–673

    Google Scholar 

  • Enoch T, Carr AM, Nurse P (1992) Fission yeast genes involved in coupling mitosis to completion of DNA replication. Genes Dev 6:2035–2046

    Google Scholar 

  • Falconi MM, Piseri A, Ferrari M, Lucchini G, Plevani P, Foiani M (1994) De novo synthesis of budding yeast DNA polymerase alpha and transcription at the G1/S boundary are not required for entrance into S phase. Proc Natl Acad Sci USA 91:1598–1602

    Google Scholar 

  • Francesconi S, Park H, Wang TSF (1993) Fission yeast with DNA polymerase delta temperature-sensitive alleles exhibits cell division cycle phenotype. Nucleic Acids Res 21: 3821–3828

    Google Scholar 

  • Gutz H, Heslot H, Leupold U, Loprieno M (1974) Schizosaccharomyces pombe. In: King RC (ed) Handbook of Genetics. Plenum Press, New York, pp 395–446

    Google Scholar 

  • Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246: 629–634

    Google Scholar 

  • Hofmann JFX, Beach D (1994) cdt1 is an essential target of the Cdc10/Sctl transcription factor: requirement for DNA replication and inhibition of mitosis. EMBO J 13:425–434

    Google Scholar 

  • Johnson LM, Synder M, Chang LMS, Davis RW Campbell JL (1985) Isolation of the gene encoding yeast DNA polymerase I. Cell 43: 369–377

    Google Scholar 

  • Kelly TJ, Martin GS, Forsburg SL, Stephen RJ, Russo A, Nurse P (1993) The fission yeast cdc18 + gene product couples S-phase to START and mitosis. Cell 74:371–382

    Google Scholar 

  • Li JJ, Deshaies RJ (1993) Exercising self-restraint: discouraging illicit acts of S and M in eukaryotes. Cell 74: 223–226

    Google Scholar 

  • Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. In: Guthrie C, Fink GR (eds) Guide to yeast genetics and molecular biology. Academic Press, New York, pp 795–823

    Google Scholar 

  • Morrison A, Hiroyuki A, Clark AB, Hamatake RK, Sugino A (1990) A third essential DNA polymerase in S. cerevisiae. Cell 62:1143–1151

    Google Scholar 

  • Nasmyth K, Nurse P (1981) Cell division cycle mutants altered in DNA replication and mitosis in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 182:119–124

    Google Scholar 

  • Pignede G, Bouvier D, De Recondo A-M, Baldacci G (1991) Characterization of the POL3 gene product from Schizosaccharomyces pombe indicates inter-species conservation of the catalytic subunit of DNA polymerase delta. J Mol Biol 222:209–218

    Google Scholar 

  • Pizzagalli A, Valsasnini P, Plevani P, Lucchini G (1988) DNA polymerase I gene of Saccharomyces cerevisiae: Nucleotide sequence, mapping of a temperature-sensitive mutation, and protein homology with other DNA polymerases. Proc Natl Acad Sci USA 85: 3772–3776

    Google Scholar 

  • Rowley R (1992) Radiation-induced mitotic delay: a genetic characterization in the fission yeast. Radiat Res 132: 144–152

    Google Scholar 

  • Saka Y, Yanagida M (1993) Fission yeast cut5 +, required for S phase onset and M phase restraint, is identical to the radiation-damage repair gene rad4 +. Cell 74:383–393

    Google Scholar 

  • Sheldrick KS, Carr AM (1993) Feedback controls and G2 checkpoints: fission yeast as a model system. BioEssays 15:775–782

    Google Scholar 

  • Sitney KC, Budd ME, Campbell JL (1989) DNA polymerase III, a second essential DNA polymerase is encoded by the S. cerevisiae CDC2 gene. Cell 56:599–605

    Google Scholar 

  • Waga S, Stillman B (1994) Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 369: 207–212

    Google Scholar 

  • Walworth N, Davey S, Beach D (1993) Fission yeast chkl-protein kinase links the rad checkpoint pathway to cdc2. Nature 363:368–371

    Google Scholar 

  • Waseem NH, Labib K, Nurse P, Lane DP (1992) Isolation and analysis of the fission yeast gene encoding polymerase δ accessory protein PCNA. EMBO J 11: 5111–5120

    Google Scholar 

  • Weinert TA (1992) Dual cell cycle checkpoints sensitive to chromosome replication and DNA damage in the budding yeast Saccharomyces cerevisiae. Radiat Res 132: 141–143

    Google Scholar 

  • Weinert TA, Hartwell HL (1988) The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241:317–322

    Google Scholar 

  • Weinert TA, Kiser GL, Hartwell HL (1994) Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev 8: 652–665

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by R. Devoret

Rights and permissions

Reprints and permissions

About this article

Cite this article

Francesconi, S., De Recondo, AM. & Baldacci, G. DNA polymerase δ is required for the replication feedback control of cell cycle progression in Schizosaccharomyces pombe . Molec. Gen. Genet. 246, 561–569 (1995). https://doi.org/10.1007/BF00298962

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00298962

Key words

Navigation