Home LiteratureArticle Details
PMID: 15805194 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A checkpoint control linking meiotic S phase and recombination initiation in fission yeast.

Tonami Y, Murakami H, Shirahige K, Nakanishi M

Abstract

During meiosis, high levels of recombination initiated by DNA double-strand breaks (DSBs) occur only after DNA replication. However, how DSB formation is coupled to DNA replication is unknown. We examined several DNA replication proteins for a role in this coupling in Schizosaccharomyces pombe, and we show that ribonucleotide reductase, the rate-limiting enzyme of deoxyribonucleotide synthesis and the target of the DNA synthesis inhibitor hydroxyurea (HU) is indirectly required for DSB formation linked to DNA replication. However, in cells in which the function of the DNA-replication-checkpoint proteins Rad1p, Rad3p, Rad9p, Rad17p, Rad26p, Hus1p, or Cds1p was compromised, DSB formation occurred at similar frequencies in the absence or presence of HU. The DSBs in the HU-treated mutant cells occurred at normal sites and were associated with recombination. In addition, Cdc2p is apparently not involved in this process. We propose that the sequence of meiotic S phase and initiation of recombination is coordinated by DNA-replication-checkpoint proteins.

MeSH Terms
Cell Cycle Proteins/genetics,metabolism DNA Replication Genes, cdc Hydroxyurea/metabolism Meiosis/physiology Nucleic Acid Synthesis Inhibitors/metabolism Recombination, Genetic Schizosaccharomyces/cytology,physiology Schizosaccharomyces pombe Proteins/genetics,metabolism
Chemicals
Cell Cycle Proteins Nucleic Acid Synthesis Inhibitors Schizosaccharomyces pombe Proteins Hydroxyurea
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Tonami Yuko
Department of Biochemistry and Cell Biology, Graduate School of Medicine, Nagoya City University, 1 Kawasumi, Mizuho-cho, Mizuho-ku, Nagoya 467-8601, Japan.
Murakami Hiroshi
Shirahige Katsuhiko
Nakanishi Makoto
References (26)
26 references, click to expand
  1. Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast.
    Nat Genet. 2001 Jul;28(3):290-3 PMID: 11431703
  2. B-type cyclins CLB5 and CLB6 control the initiation of recombination and synaptonemal complex formation in yeast meiosis.
    Curr Biol. 2001 Jan 23;11(2):88-97 PMID: 11231124
  3. The DNA replication checkpoint response stabilizes stalled replication forks.
    Nature. 2001 Aug 2;412(6846):557-61 PMID: 11484058
  4. Meiosis: how to create a specialized cell cycle.
    Curr Opin Cell Biol. 2001 Dec;13(6):770-7 PMID: 11698195
  5. Meiotic recombination remote from prominent DNA break sites in S. pombe.
    Mol Cell. 2002 Feb;9(2):253-63 PMID: 11864600
  6. Maintenance of replication forks and the S-phase checkpoint by Cdc18p and Orp1p.
    Nat Cell Biol. 2002 May;4(5):384-8 PMID: 11988741
  7. The G1/S cyclin Cig2p during meiosis in fission yeast.
    Mol Biol Cell. 2002 Jun;13(6):2080-90 PMID: 12058071
  8. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe.
    Methods Enzymol. 1991;194:795-823 PMID: 2005825
  9. Isolation, characterisation and molecular cloning of new mutant alleles of the fission yeast p34cdc2+ protein kinase gene: identification of temperature-sensitive G2-arresting alleles.
    Mol Gen Genet. 1991 Sep;229(1):109-18 PMID: 1896017
  10. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae.
    Cell. 1991 Sep 20;66(6):1239-56 PMID: 1913808
  11. The cell cycle genes cdc22+ and suc22+ of the fission yeast Schizosaccharomyces pombe encode the large and small subunits of ribonucleotide reductase.
    Mol Gen Genet. 1993 Apr;238(1-2):241-51 PMID: 8479429
  12. Fission yeast chk1 protein kinase links the rad checkpoint pathway to cdc2.
    Nature. 1993 May 27;363(6427):368-71 PMID: 8497322
  13. A kinase from fission yeast responsible for blocking mitosis in S phase.
    Nature. 1995 Apr 27;374(6525):817-9 PMID: 7723827
  14. The role of cdc2 and other genes in meiosis in Schizosaccharomyces pombe.
    Genetics. 1995 Aug;140(4):1235-45 PMID: 7498766
  15. A single fission yeast mitotic cyclin B p34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins.
    EMBO J. 1996 Feb 15;15(4):850-60 PMID: 8631306
  16. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family.
    Cell. 1997 Feb 7;88(3):375-84 PMID: 9039264
  17. Meiotic chromosomes: it takes two to tango.
    Genes Dev. 1997 Oct 15;11(20):2600-21 PMID: 9334324
  18. CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint.
    Genes Dev. 1998 Sep 1;12(17):2698-710 PMID: 9732268
  19. Checkpoints on the road to mitosis.
    Trends Biochem Sci. 1998 Oct;23(10):399-402 PMID: 9810229
  20. Meiotic DNA replication checkpoint control in fission yeast.
    Genes Dev. 1999 Oct 1;13(19):2581-93 PMID: 10521402
  21. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway.
    Genes Dev. 1998 Sep 15;12(18):2956-70 PMID: 9744871
  22. The G2-phase DNA-damage checkpoint.
    Trends Cell Biol. 2000 Jul;10(7):296-303 PMID: 10856933
  23. Meiotic DNA breaks associated with recombination in S. pombe.
    Mol Cell. 2000 May;5(5):883-8 PMID: 10882124
  24. Direct coupling between meiotic DNA replication and recombination initiation.
    Science. 2000 Oct 27;290(5492):806-9 PMID: 11052944
  25. DNA replication and damage checkpoints and meiotic cell cycle controls in the fission and budding yeasts.
    Biochem J. 2000 Jul 1;349(Pt 1):1-12 PMID: 10861204
  26. Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8395-402 PMID: 11459981
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-04-19
Epub
2005-00-01
Pages
5797-801
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC556284
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]