The C-terminus of <i>S. pombe</i> DDK subunit Dfp1 is required for meiosis-specific transcription and cohesin cleavage

Le, Anh-Huy; Mastro, Tara L.; Forsburg, Susan L.

doi:10.1242/bio.20135173

Cited by 18 publications

(35 citation statements)

References 70 publications

(141 reference statements)

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“…The eponymous DBF4 protein is an activator of the CDC7 serine/threonine kinase, which has a conserved role in DNA replication initiation from yeast to humans (Hughes et al 2012). In yeast, the dbf4/cdc7 complex was moreover linked to chromosome segregation during meiosis (Kovacikova et al 2013;Le et al 2013). Coincidently, we found that Liz expression peaks at meiosis during mouse spermatogenesis, and canonical Zdbf2 is highly transcribed in the oocyte, leading to the exciting possibility that Zdbf2 may fulfill meiotic roles in mammals.…”

Section: Discussionmentioning

confidence: 73%

The Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals

et al. 2014

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Many loci maintain parent-of-origin DNA methylation only briefly after fertilization during mammalian development: Whether this form of transient genomic imprinting can impact the early embryonic transcriptome or even have life-long consequences on genome regulation and possibly phenotypes is currently unknown. Here, we report a maternal germline differentially methylated region (DMR) at the mouse Gpr1/Zdbf2 (DBF-type zinc finger-containing protein 2) locus, which controls the paternal-specific expression of long isoforms of Zdbf2 (Liz) in the early embryo. This DMR loses parental specificity by gain of DNA methylation at implantation in the embryo but is maintained in extraembryonic tissues. As a consequence of this transient, tissue-specific maternal imprinting, Liz expression is restricted to the pluripotent embryo, extraembryonic tissues, and pluripotent male germ cells. We found that Liz potentially functions as both Zdbf2-coding RNA and cis-regulatory RNA. Importantly, Liz-mediated events allow a switch from maternal to paternal imprinted DNA methylation and from Liz to canonical Zdbf2 promoter use during embryonic differentiation, which are stably maintained through somatic life and conserved in humans. The Gpr1/Zdbf2 locus lacks classical imprinting histone modifications, but analysis of mutant embryonic stem cells reveals fine-tuned regulation of Zdbf2 dosage through DNA and H3K27 methylation interplay. Together, our work underlines the developmental and evolutionary need to ensure proper Liz/Zdbf2 dosage as a driving force for dynamic genomic imprinting at the Gpr1/Zdbf2 locus.

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Section: Discussionmentioning

confidence: 73%

The Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals

et al. 2014

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“…There is a high frequency of dyad formation [34]. A similar naturally occurring C-terminal truncation mutant of dfp1 (rad35) was previously identified and was shown to be sensitive to DNA damages.…”

Section: Regulation Of Meiotic Recombination By Hsk1/cdc7mentioning

confidence: 98%

“…In fission yeast, the localization of the monopolin complex to kinetochores is not required for mono-orientation [42]. Rec8 phosphorylation by both CK1 (casein kinase 1) and Hsk1/Cdc7 is a prerequisite for the cleavage of Rec8 by separase in budding and fission yeasts [34,43,44].…”

Section: Regulation Of Meiotic Cell Division By Hsk1/cdc7 and Relatedmentioning

confidence: 99%

“…A rad21-K1 hsk1 double mutant exhibits a severe synthetic growth defect [56,57]. hsk1-89 exhibits the premature separation of sister chromatids [56] and dfp1 (1-519), a dfp1 C-terminally truncated mutant, is defective in the phosphorylation and degradation of Rec8, the meiotic counterpart of Rad21, resulting in a failure to proceed through the MII division [34]. These results are consistent with a crucial role for hsk1 + -dfp 1 + /him1 + during M-phase through interaction with cohesin.…”

Section: Regulation Of Chromosome Partition By Hsk1/cdc7mentioning

confidence: 99%

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Regulation of chromosome dynamics by Hsk1/Cdc7 kinase

Matsumoto

Masai

2013

Biochemical Society Transactions

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Hsk1 (homologue of Cdc7 kinase 1) of the fission yeast is a member of the conserved Cdc7 (cell division cycle 7) kinase family, and promotes initiation of chromosome replication by phosphorylating Mcm (minichromosome maintenance) subunits, essential components for the replicative helicase. Recent studies, however, indicate more diverse roles for Hsk1/Cdc7 in regulation of various chromosome dynamics, including initiation of meiotic recombination, meiotic chromosome segregation, DNA repair, replication checkpoints, centromeric heterochromatin formation and so forth. Hsk1/Cdc7, with its unique target specificity, can now be regarded as an important modulator of various chromosome transactions.

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“…In yeast, 2 kinases phosphorylate Rec8 to promote the cleavage of cohesin on chromosome arms at anaphase I: Hrr25, a conserved casein kinase 1d, and the Dbf4dependent Cdc7 kinase. [21][22][23] Accordingly, inhibition of both kinases or mutations of Rec8 phospho-sites blocks Rec8 cleavage and homolog disjunction. 22 Protection of centromeric Rec8 from cleavage by separase at anaphase I depends on orthologues of the Drosophila Mei-S332 protein, known as shugoshins (Sgo).…”

Section: Introductionmentioning

confidence: 99%

APC/C-Cdc20 mediates deprotection of centromeric cohesin at meiosis II in yeast

Jonak

Zagoriy

et al. 2017

Cell Cycle

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Cells undergoing meiosis produce haploid gametes through one round of DNA replication followed by 2 rounds of chromosome segregation. This requires that cohesin complexes, which establish sister chromatid cohesion during S phase, are removed in a stepwise manner. At meiosis I, the separase protease triggers the segregation of homologous chromosomes by cleaving cohesin's Rec8 subunit on chromosome arms. Cohesin persists at centromeres because the PP2A phosphatase, recruited by the shugoshin protein, dephosphorylates Rec8 and thereby protects it from cleavage. While chromatids disjoin upon cleavage of centromeric Rec8 at meiosis II, it was unclear how and when centromeric Rec8 is liberated from its protector PP2A. One proposal is that bipolar spindle forces separate PP2A from Rec8 as cells enter metaphase II. We show here that sister centromere biorientation is not sufficient to "deprotect" Rec8 at meiosis II in yeast. Instead, our data suggest that the ubiquitin-ligase APC/C removes PP2A from centromeres by targeting for degradation the shugoshin Sgo1 and the kinase Mps1. This implies that Rec8 remains protected until entry into anaphase II when it is phosphorylated concurrently with the activation of separase. Here, we provide further support for this model and speculate on its relevance to mammalian oocytes.

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The C-terminus of S. pombe DDK subunit Dfp1 is required for meiosis-specific transcription and cohesin cleavage

Cited by 18 publications

References 70 publications

The Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals

The Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals

Regulation of chromosome dynamics by Hsk1/Cdc7 kinase

APC/C-Cdc20 mediates deprotection of centromeric cohesin at meiosis II in yeast

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