A Checkpoint Control Linking Meiotic S Phase and Recombination Initiation in Fission Yeast

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2005 Apr 5

PMID 15805194

Citations 22

Authors

Yuko Tonami

Hiroshi Murakami

Katsuhiko Shirahige

Makoto Nakanishi

Affiliations

Soon will be listed here.

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.

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References

Murakami H, Nurse P . Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast. Nat Genet. 2001; 28(3):290-3. DOI: 10.1038/90142. View

Smith K, Penkner A, Ohta K, Klein F, Nicolas A . B-type cyclins CLB5 and CLB6 control the initiation of recombination and synaptonemal complex formation in yeast meiosis. Curr Biol. 2001; 11(2):88-97. DOI: 10.1016/s0960-9822(01)00026-4. View

Lopes M, Pellicioli A, Liberi G, Plevani P, Muzi-Falconi M, Newlon C . The DNA replication checkpoint response stabilizes stalled replication forks. Nature. 2001; 412(6846):557-61. DOI: 10.1038/35087613. View

Lee B, Amon A . Meiosis: how to create a specialized cell cycle. Curr Opin Cell Biol. 2001; 13(6):770-7. DOI: 10.1016/s0955-0674(00)00282-9. View

Young J, Schreckhise R, Steiner W, Smith G . Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol Cell. 2002; 9(2):253-63. DOI: 10.1016/s1097-2765(02)00452-5. View

Murakami H, Yanow S, Griffiths D, Nakanishi M, Nurse P . Maintenance of replication forks and the S-phase checkpoint by Cdc18p and Orp1p. Nat Cell Biol. 2002; 4(5):384-8. DOI: 10.1038/ncb789. View

Borgne A, Murakami H, Ayte J, Nurse P . The G1/S cyclin Cig2p during meiosis in fission yeast. Mol Biol Cell. 2002; 13(6):2080-90. PMC: 117626. DOI: 10.1091/mbc.01-10-0507. View

Moreno S, Klar A, Nurse P . Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991; 194:795-823. DOI: 10.1016/0076-6879(91)94059-l. View

MacNeill S, Creanor J, Nurse P . 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; 229(1):109-18. DOI: 10.1007/BF00264219. View

10.

Padmore R, Cao L, Kleckner N . Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 1991; 66(6):1239-56. DOI: 10.1016/0092-8674(91)90046-2. View

11.

Fernandez Sarabia M, McInerny C, Harris P, Gordon C, Fantes P . 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; 238(1-2):241-51. DOI: 10.1007/BF00279553. View

12.

Walworth N, Davey S, Beach D . Fission yeast chk1 protein kinase links the rad checkpoint pathway to cdc2. Nature. 1993; 363(6427):368-71. DOI: 10.1038/363368a0. View

13.

Murakami H, Okayama H . A kinase from fission yeast responsible for blocking mitosis in S phase. Nature. 1995; 374(6525):817-9. DOI: 10.1038/374817a0. View

14.

Iino Y, Hiramine Y, Yamamoto M . The role of cdc2 and other genes in meiosis in Schizosaccharomyces pombe. Genetics. 1995; 140(4):1235-45. PMC: 1206690. DOI: 10.1093/genetics/140.4.1235. View

15.

Fisher D, Nurse P . A single fission yeast mitotic cyclin B p34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins. EMBO J. 1996; 15(4):850-60. PMC: 450283. View

16.

Keeney S, Giroux C, Kleckner N . Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997; 88(3):375-84. DOI: 10.1016/s0092-8674(00)81876-0. View

17.

Roeder G . Meiotic chromosomes: it takes two to tango. Genes Dev. 1997; 11(20):2600-21. DOI: 10.1101/gad.11.20.2600. View

18.

Stuart D, Wittenberg C . CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint. Genes Dev. 1998; 12(17):2698-710. PMC: 317137. DOI: 10.1101/gad.12.17.2698. View

19.

Russell P . Checkpoints on the road to mitosis. Trends Biochem Sci. 1998; 23(10):399-402. DOI: 10.1016/s0968-0004(98)01291-2. View

20.

Murakami H, Nurse P . Meiotic DNA replication checkpoint control in fission yeast. Genes Dev. 1999; 13(19):2581-93. PMC: 317071. DOI: 10.1101/gad.13.19.2581. View