Nuclear dynamics of the Set1C subunit Spp1 prepares meiotic recombination sites for break formation

Karányi, Zsolt; Halász, László; Acquaviva, Laurent; Jonas, David; Hetey, Szabolcs; Boros-Oláh, Beáta; Peng, Feng; Chen, Doris; Klein, Franz; Géli, Vincent; Székvölgyi, Lóránt

doi:10.1083/jcb.201712122

Cited by 15 publications

(19 citation statements)

References 63 publications

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“…Set1 complex) and Spp1's interaction with Mer2 is mutually exclusive with the remainder of the COMPASS complex 14 . Furthemore, Spp1 associated with Mer2 has a longer residence time on nucleosomes when compared with Spp1 when part of COMPASS 15 residues 140-256 of Mer2 12,13 which we from now on refer to as Mer2 "core" ( Figure 1B). We measured the molecular mass of Mer2 core by size exclusion chromatography coupled to multi-angle light scattering (SEC-MALS) and concluded that the Mer2 core is a tetramer ( Figure 1D), consistent with recently published data 17 .…”

Section: Introductionmentioning

confidence: 97%

Novel mechanistic insights into the role of Mer2 as the keystone of meiotic DNA break formation

Rousová

Nivsarkar

Altmannová

et al. 2020

Preprint

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One of the defining features of sexual reproduction is the recombination events that take place during meiosis I. Recombination is both evolutionarily advantageous, but also mechanistically necessary to form the crossovers that link homologous chromosomes. Meiotic recombination is initiated through the placement of programmed double-strand DNA breaks (DSBs) mediated by the protein Spo11. The timing, number, and physical placement of DSBs are carefully controlled through a variety of protein machinery. Previous work has implicated Mer2(IHO1 in mammals) to be involved in both the placement of breaks, and their timing. In this study we use a combination of protein biochemistry and biophysics to extensively characterise various roles of the Mer2. We gain further insights into the details of Mer2 interaction with the PHD protein Spp1, reveal that Mer2 is a novel nucleosome binder, and suggest how Mer2’s interaction with the HORMA domain protein Hop1 (HORMAD1/2 in mammals) is controlled.

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Section: Introductionmentioning

confidence: 97%

Novel mechanistic insights into the role of Mer2 as the keystone of meiotic DNA break formation

Rousová

Nivsarkar

Altmannová

et al. 2020

Preprint

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“…For this reason, Spp1 can be found both around actively transcribed genes and in chromosome axial sites, with independence from Set1 [81]. Furthermore, set1∆ strains display a general reduction in most DSBs, which has been seen to correlate with H3K4me3 levels [82,83]. This particular strain has also been reported to present a synthetic defect with Rec114 of the RRM subcomplex [84].…”

Section: Int J Mol Sci 2020 21 X 6 Of 21mentioning

confidence: 94%

Sharing Marks: H3K4 Methylation and H2B Ubiquitination as Features of Meiotic Recombination and Transcription

Serrano-Quílez

Roig-Soucase

Rodrı́guez-Navarro

2020

IJMS

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Meiosis is a specialized cell division that gives raise to four haploid gametes from a single diploid cell. During meiosis, homologous recombination is crucial to ensure genetic diversity and guarantee accurate chromosome segregation. Both the formation of programmed meiotic DNA double-strand breaks (DSBs) and their repair using homologous chromosomes are essential and highly regulated pathways. Similar to other processes that take place in the context of chromatin, histone posttranslational modifications (PTMs) constitute one of the major mechanisms to regulate meiotic recombination. In this review, we focus on specific PTMs occurring in histone tails as driving forces of different molecular events, including meiotic recombination and transcription. In particular, we concentrate on the influence of H3K4me3, H2BK123ub, and their corresponding molecular machineries that write, read, and erase these histone marks. The Spp1 subunit within the Complex of Proteins Associated with Set1 (COMPASS) is a critical regulator of H3K4me3-dependent meiotic DSB formation. On the other hand, the PAF1c (RNA polymerase II associated factor 1 complex) drives the ubiquitination of H2BK123 by Rad6-Bre1. We also discuss emerging evidence obtained by cryo-electron microscopy (EM) structure determination that has provided new insights into how the “cross-talk” between these two marks is accomplished.

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“…Indeed, Spp1 protein has been identified as a molecule that mediates the association of the loops with the axis [6,8]. Spp1, although it is a component of COMPASS, binds to the meiotic chromosome axes independently of COMPASS [23,24], and tethers H3K4me-enriched loop regions to the axis through its PHD finger, a conserved binding domain for H3K4 methylation [6,8]. Importantly, Spp1 binds to Mer2 for DSB formation on the axis [6,8].…”

Section: Introductionmentioning

confidence: 99%

Genetic Interactions of Histone Modification Machinery Set1 and PAF1C with the Recombination Complex Rec114-Mer2-Mei4 in the Formation of Meiotic DNA Double-Strand Breaks

Zhang

Suzuki

et al. 2020

IJMS

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Homologous recombination is essential for chromosome segregation during meiosis I. Meiotic recombination is initiated by the introduction of double-strand breaks (DSBs) at specific genomic locations called hotspots, which are catalyzed by Spo11 and its partners. DSB hotspots during meiosis are marked with Set1-mediated histone H3K4 methylation. The Spo11 partner complex, Rec114-Mer2-Mei4, essential for the DSB formation, localizes to the chromosome axes. For efficient DSB formation, a hotspot with histone H3K4 methylation on the chromatin loops is tethered to the chromosome axis through the H3K4 methylation reader protein, Spp1, on the axes, which interacts with Mer2. In this study, we found genetic interaction of mutants in a histone modification protein complex called PAF1C with the REC114 and MER2 in the DSB formation in budding yeast Saccharomyces cerevisiae. Namely, the paf1c mutations rtf1 and cdc73 showed synthetic defects in meiotic DSB formation only when combined with a wild-type-like tagged allele of either the REC114 or MER2. The synthetic defect of the tagged REC114 allele in the DSB formation was seen also with the set1, but not with spp1 deletion. These results suggest a novel role of histone modification machinery in DSB formation during meiosis, which is independent of Spp1-mediated loop-axis tethering.

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Nuclear dynamics of the Set1C subunit Spp1 prepares meiotic recombination sites for break formation

Cited by 15 publications

References 63 publications

Novel mechanistic insights into the role of Mer2 as the keystone of meiotic DNA break formation

Novel mechanistic insights into the role of Mer2 as the keystone of meiotic DNA break formation

Sharing Marks: H3K4 Methylation and H2B Ubiquitination as Features of Meiotic Recombination and Transcription

Genetic Interactions of Histone Modification Machinery Set1 and PAF1C with the Recombination Complex Rec114-Mer2-Mei4 in the Formation of Meiotic DNA Double-Strand Breaks

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