Formation, maintenance and consequences of the imprint at the mating-type locus in fission yeast

Kaykov, Atanas; Holmes, Allyson; Arcangioli, Benoı̂t

doi:10.1038/sj.emboj.7600099

Cited by 53 publications

(55 citation statements)

References 53 publications

(76 reference statements)

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“…In this paper, we demonstrate by chromatin immunoprecipitation experiments that both Swi1p and Swi3p bind to sequences near the imprint site as well as at RTS1. Recently, the interaction of Swi1p around these regions was also observed, similar to our results in an independent investigation (23). Here, we investigated the interaction of both Swi1p and Swi3p with these regions because these proteins were identified as a multiprotein complex.…”

Section: Discussionsupporting

confidence: 56%

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Biochemical Interactions between Proteins and mat1 cis-Acting Sequences Required for Imprinting in Fission Yeast

Lee

Grewal

Klar

2004

Molecular and Cellular Biology

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DNA recombination required for mating type (mat1) switching in Schizosaccharomyces pombe is initiated by mat1 imprinting. The imprinting event is regulated by mat1 cis-acting elements and by several trans-acting factors, including swi1 (for switch), swi3, swi7, and sap1. swi1 and swi3 were previously shown to function in dictating unidirectional mat1 DNA replication by controlling replication fork movement around the mat1 region and, second, by pausing fork progression around the imprint site. With biochemical studies, we investigated whether the trans-acting factors function indirectly or directly by binding to the mat1 cis-acting sequences. First, we report the identification and DNA sequence of the swi3 gene. swi3 is not essential for viability, and, like the other factors, it exerts a stimulatory effect on imprinting. Second, we showed that only Swi1p and Swi3p interact to form a multiprotein complex and that complex formation did not require their binding to a DNA region defined by the smt-0 mutation. Third, we found that the Swi1p-Swi3p complex physically binds to a region around the imprint site where pausing of replication occurs. Fourth, the protein complex also interacted with the mat1-proximal polar terminator of replication (RTS1). These results suggest that the stimulatory effect of swi1 and swi3 on switching and imprinting occurs through interaction of the Swi1p-Swi3p complex with the mat1 regions.The fission yeast Schizosaccharomyces pombe is a haploid eukaryotic microorganism whose cells exhibit two different mating types, called P (plus) and M (minus) (18,33). The mating type is determined by the genetic information in the mat1 locus, which contains either the mat1M or the mat1P allele, each of which encodes two transcripts essential for controlling cell type (24). A copy of the mating type genetic information is also present at the mat2P and mat3M"donor" loci that are located centromere-distal to mat1 and are transcriptionally silent. The mating type switches when a copy of either the mat2P or mat3M DNA transposes and substitutes for mat1 by DNA recombination, where the transposed genetic information is expressed (6,12,26).Switching occurs spontaneously at a high frequency in "homothallic" strains (h 90 , i.e., homothallic, 90% sporulation) during mitotic growth, and it follows an interesting nonrandom pattern within a cell lineage (17,28,34). Division of an unswitchable parental cell produces two daughter cells, one of which is programmed to be switching competent and the other of which is not. After cell division of a switching-competent cell, a switched and a switching-competent daughter cell are generated. On the other hand, a switching-noncompetent cell undergoes a cell division to produce a switching-competent and a noncompetent cell. Therefore, this switching pattern in the cell lineage results in only one cell switching among four granddaughter cells after two consecutive asymmetrical cell divisions of an unswitchable cell. These rules of so-called onein-four and consecutive switching a...

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Section: Discussionsupporting

confidence: 56%

“…The imprint was characterized in previous studies as either an alkali-labile and RNasesensitive modification(s) or a single-strand break (2,13,23,42). Therefore, the chemical nature of the imprint in vivo needs to be further defined to understand how the key process of imprinting occurs.…”

Section: Discussionmentioning

confidence: 99%

Biochemical Interactions between Proteins and mat1 cis-Acting Sequences Required for Imprinting in Fission Yeast

Lee

Grewal

Klar

2004

Molecular and Cellular Biology

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“…The function of the MPS1 site is to promote site-specific RNA priming at mat1 by the primase/Polα complex at the imprint site so that the 5′ end of the stalled fork is dictated by the replication pause (37). Work from the Arcangioli laboratory suggests that the imprint is a single-stranded nick that contains unphosphorylated 3′-OH and 5′-OH termini (32,44,45). It is possible that different outcomes, such as alkali lability of the imprint, a strand-specific nick, and/or DSB, derive from inserted ribonucleotides forming the imprint.…”

Section: Swi1 Swi3 and Swi7 Factors Play Multiple Roles In Imprintingmentioning

confidence: 99%

A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review

2014

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Cells of the highly diverged Schizosaccharomyces (S.) pombe and S. japonicus fission yeasts exist in one of two sex/mating types, called P (for plus) or M (for minus), specified by which allele, M or P, resides at mat1. The fission yeasts have evolved an elegant mechanism for switching P or M information at mat1 by a programmed DNA recombination event with a copy of one of the two silent mating-type genes residing nearby in the genome. The switching process is highly cell-cycle and generation dependent such that only one of four grandchildren of a cell switches mating type. Extensive studies of fission yeast established the natural DNA strand chirality at the mat1 locus as the primary basis of asymmetric cell division. The asymmetry results from a unique site-and strand-specific epigenetic "imprint" at mat1 installed in one of the two chromatids during DNA replication. The imprint is inherited by one daughter cell, maintained for one cell cycle, and is then used for initiating recombination during mat1 replication in the following cell cycle. This mechanism of cell-type switching is considered to be unique to these two organisms, but determining the operation of such a mechanism in other organisms has not been possible for technical reasons. This review summarizes recent exciting developments in the understanding of mating-type switching in fission yeasts and extends these observations to suggest how such a DNA strand-based epigenetic mechanism of cellular differentiation could also operate in diploid organisms.

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“…In Schizosaccharomyces pombe, mating-type switching is induced by the replication fork encountering a single-strand nick at the mat1 locus, transforming this nick into a DSB, thus initiating homologous recombination with one of the two homologous mat cassettes (references 13, 14, 237, and 237a). This is a highly regulated process under the control of several proteins, including the conserved fork protection Swi1/Swi3 complex (Tim/Tipin in mammals), responsible for the temporary replication fork pausing near mat1 (200,237). The possible presence of single-strand nicks at fragile sites in vivo, during or after replication, is an open question.…”

Section: Fragile Sites and Cancermentioning

confidence: 99%

Comparative Genomics and Molecular Dynamics of DNA Repeats in Eukaryotes

Richard

Kerrest

Dujon

2008

Microbiol Mol Biol Rev

482

411

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SUMMARY Repeated elements can be widely abundant in eukaryotic genomes, composing more than 50% of the human genome, for example. It is possible to classify repeated sequences into two large families, “tandem repeats” and “dispersed repeats.” Each of these two families can be itself divided into subfamilies. Dispersed repeats contain transposons, tRNA genes, and gene paralogues, whereas tandem repeats contain gene tandems, ribosomal DNA repeat arrays, and satellite DNA, itself subdivided into satellites, minisatellites, and microsatellites. Remarkably, the molecular mechanisms that create and propagate dispersed and tandem repeats are specific to each class and usually do not overlap. In the present review, we have chosen in the first section to describe the nature and distribution of dispersed and tandem repeats in eukaryotic genomes in the light of complete (or nearly complete) available genome sequences. In the second part, we focus on the molecular mechanisms responsible for the fast evolution of two specific classes of tandem repeats: minisatellites and microsatellites. Given that a growing number of human neurological disorders involve the expansion of a particular class of microsatellites, called trinucleotide repeats, a large part of the recent experimental work on microsatellites has focused on these particular repeats, and thus we also review the current knowledge in this area. Finally, we propose a unified definition for mini- and microsatellites that takes into account their biological properties and try to point out new directions that should be explored in a near future on our road to understanding the genetics of repeated sequences.

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Formation, maintenance and consequences of the imprint at the mating-type locus in fission yeast

Cited by 53 publications

References 53 publications

Biochemical Interactions between Proteins and mat1 cis-Acting Sequences Required for Imprinting in Fission Yeast

Biochemical Interactions between Proteins and mat1 cis-Acting Sequences Required for Imprinting in Fission Yeast

A Unique DNA Recombination Mechanism of the Mating/Cell-type Switching of Fission Yeasts: a Review

Comparative Genomics and Molecular Dynamics of DNA Repeats in Eukaryotes

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