Literature DB >> 16698922

Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast.

Keiko Ogino1, Kouji Hirota, Seiji Matsumoto, Tadayuki Takeda, Kunihiro Ohta, Ken-ichi Arai, Hisao Masai.   

Abstract

Cdc7 kinase, conserved through evolution, is known to be essential for mitotic DNA replication. The role of Cdc7 in meiotic recombination was suggested in Saccharomyces cerevisiae, but its precise role has not been addressed. Here, we report that Hsk1, the Cdc7-related kinase in Schizosaccharomyces pombe, plays a crucial role during meiosis. In a hsk1 temperature-sensitive strain (hsk1-89), meiosis is arrested with one nucleus state before meiosis I in most of the cells and meiotic recombination frequency is reduced by one order of magnitude, whereas premeiotic DNA replication is delayed but is apparently completed. Strikingly, formation of meiotic dsDNA breaks (DSBs) are largely impaired in the mutant, and Hsk1 kinase activity is essential for these processes. Deletion of all three checkpoint kinases, namely Cds1, Chk1, and Mek1, does not restore DSB formation, meiosis, or Cdc2 activation, which is suppressed in hsk1-89, suggesting that these aberrations are not caused by known checkpoint pathways but that Hsk1 may regulate DSB formation and meiosis. Whereas transcriptional induction of some rec genes and horsetail movement are normal, chromatin remodeling at ade6-M26, a recombination hotspot, which is prerequisite for subsequent DSB formation at this locus, is not observed in hsk1-89. These results indicate unique and essential roles of Hsk1 kinase in the initiation of meiotic recombination and meiosis.

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Year:  2006        PMID: 16698922      PMCID: PMC1472441          DOI: 10.1073/pnas.0602498103

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  44 in total

1.  A fission yeast gene, him1(+)/dfp1(+), encoding a regulatory subunit for Hsk1 kinase, plays essential roles in S-phase initiation as well as in S-phase checkpoint control and recovery from DNA damage.

Authors:  T Takeda; K Ogino; E Matsui; M K Cho; H Kumagai; T Miyake; K Arai; H Masai
Journal:  Mol Cell Biol       Date:  1999-08       Impact factor: 4.272

2.  Direct coupling between meiotic DNA replication and recombination initiation.

Authors:  V Borde; A S Goldman; M Lichten
Journal:  Science       Date:  2000-10-27       Impact factor: 47.728

3.  Mitotic replication initiation proteins are not required for pre-meiotic S phase.

Authors:  S L Forsburg; J A Hodson
Journal:  Nat Genet       Date:  2000-07       Impact factor: 38.330

4.  Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast.

Authors:  H Murakami; P Nurse
Journal:  Nat Genet       Date:  2001-07       Impact factor: 38.330

5.  S. pombe mei2+ encodes an RNA-binding protein essential for premeiotic DNA synthesis and meiosis I, which cooperates with a novel RNA species meiRNA.

Authors:  Y Watanabe; M Yamamoto
Journal:  Cell       Date:  1994-08-12       Impact factor: 41.582

6.  B-type cyclins CLB5 and CLB6 control the initiation of recombination and synaptonemal complex formation in yeast meiosis.

Authors:  K N Smith; A Penkner; K Ohta; F Klein; A Nicolas
Journal:  Curr Biol       Date:  2001-01-23       Impact factor: 10.834

7.  Meiotic DNA breaks at the S. pombe recombination hot spot M26.

Authors:  Walter W Steiner; Randall W Schreckhise; Gerald R Smith
Journal:  Mol Cell       Date:  2002-04       Impact factor: 17.970

8.  A second human Dbf4/ASK-related protein, Drf1/ASKL1, is required for efficient progression of S and M phases.

Authors:  Naoko Yoshizawa-Sugata; Ai Ishii; Chika Taniyama; Etsuko Matsui; Ken-ichi Arai; Hisao Masai
Journal:  J Biol Chem       Date:  2005-01-24       Impact factor: 5.157

9.  Meiotic recombination remote from prominent DNA break sites in S. pombe.

Authors:  Jennifer A Young; Randall W Schreckhise; Walter W Steiner; Gerald R Smith
Journal:  Mol Cell       Date:  2002-02       Impact factor: 17.970

10.  Transient, meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe.

Authors:  Y Lin; G R Smith
Journal:  Genetics       Date:  1994-03       Impact factor: 4.562

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  25 in total

Review 1.  Meiotic Recombination: The Essence of Heredity.

Authors:  Neil Hunter
Journal:  Cold Spring Harb Perspect Biol       Date:  2015-10-28       Impact factor: 10.005

Review 2.  Cell cycle regulation of DNA replication.

Authors:  R A Sclafani; T M Holzen
Journal:  Annu Rev Genet       Date:  2007       Impact factor: 16.830

3.  Regulating the formation of DNA double-strand breaks in meiosis.

Authors:  Hajime Murakami; Scott Keeney
Journal:  Genes Dev       Date:  2008-02-01       Impact factor: 11.361

4.  Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis.

Authors:  Scott Keeney
Journal:  Genome Dyn Stab       Date:  2008-01-01

5.  Cdc7-Dbf4 is a gene-specific regulator of meiotic transcription in yeast.

Authors:  Hsiao-Chi Lo; Ryan C Kunz; Xiangyu Chen; Allison Marullo; Steven P Gygi; Nancy M Hollingsworth
Journal:  Mol Cell Biol       Date:  2011-11-21       Impact factor: 4.272

Review 6.  Self-organization of meiotic recombination initiation: general principles and molecular pathways.

Authors:  Scott Keeney; Julian Lange; Neeman Mohibullah
Journal:  Annu Rev Genet       Date:  2014       Impact factor: 16.830

7.  Molecular mechanism of activation of human Cdc7 kinase: bipartite interaction with Dbf4/activator of S phase kinase (ASK) activation subunit stimulates ATP binding and substrate recognition.

Authors:  Ryo Kitamura; Rino Fukatsu; Naoko Kakusho; Yong-Soon Cho; Chika Taniyama; Satoshi Yamazaki; Gaik-theng Toh; Kazuo Yanagi; Naoko Arai; Ho-Jin Chang; Hisao Masai
Journal:  J Biol Chem       Date:  2011-05-02       Impact factor: 5.157

8.  AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana.

Authors:  Arnaud De Muyt; Daniel Vezon; Ghislaine Gendrot; Jean-Luc Gallois; Rebecca Stevens; Mathilde Grelon
Journal:  EMBO J       Date:  2007-08-30       Impact factor: 11.598

9.  Multiple modes of chromatin configuration at natural meiotic recombination hot spots in fission yeast.

Authors:  Kouji Hirota; Walter W Steiner; Takehiko Shibata; Kunihiro Ohta
Journal:  Eukaryot Cell       Date:  2007-09-07

10.  Interactions between Swi1-Swi3, Mrc1 and S phase kinase, Hsk1 may regulate cellular responses to stalled replication forks in fission yeast.

Authors:  Michie Shimmoto; Seiji Matsumoto; Yukari Odagiri; Eishi Noguchi; Paul Russell; Hisao Masai
Journal:  Genes Cells       Date:  2009-04-30       Impact factor: 1.891

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