meiotic recombination in mammals: localization and regulation

Acquaviva L, Szkvlgyi L, Dichtl B, Dichtl BS, de La Roche Saint-Andr C, Nicolas A, Gli V 2010; Bonfils et al. 1999; Zhu et al. 2014. Within these domains, DSBs preferentially form in GC-rich chromatin loop regions rather than AT-rich axis-associated DNA (Fig. MEI4 interacts with REC114 via conserved motifs in the amino-terminal region (Kumar et al. 5, e1000648 (2009). This process initiates through breaks in genomic DNA catalyzed by the SPO11 protein. Sanchez-Moran E, Santos JL, Jones GH, Franklin FC Synaptonemal complex is found in which stage of meiosis It is speculated that requiring MRX for DSB formation facilitates rapid coordination with repair, ensuring that all breaks are efficiently processed (Borde et al. RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes. PLoS Genet. SPO11 rarely cuts in these regions in wild-type mice, but does so frequently when PRDM9 is missing (Brick et al. Baudat F1, Imai Y, de Massy B Author information Affiliations 1 author 1. 2008; Panizza et al. 2012; Sommermeyer et al. Genetic and biochemical analyses suggest the formation of a canonical PBAF and a BRG1-independent complex containing ARID2 and PBRM1 as core components, which support a model in which different PBAf complexes regulate different stages of meiosis and gametogenesis. Ski8 is involved in RNA metabolism in vegetative cells but, during meiosis, it relocalizes to the nucleus where it stabilizes the nuclear localization and chromatin association of Spo11 and, to a lesser extent, of Rec102Rec104 (Arora et al. Recombinational DNA double-strand breaks in mice precede synapsis. 2003). Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodriguez J, Jasin M, Keeney S, Bonner WM, Burgoyne PS Methylation of lysine 4 on histone H3: Intricacy of writing and reading a single epigenetic mark. Fowler KR, Sasaki M, Milman N, Keeney S, Smith GR . Marine Mammal Science 34, 113-134; M.M. Recent studies support this hypothesis (Murakami and Keeney 2014). Proc. 2013). The meiotic chromosome axis plays important roles in chromosome dynamics in mammalian meiosis, including in homologous chromosome pairing, synapsis, recombination, and segregation. 2004. Biol. Kee, K., Angeles, V. T., Flores, M., Nguyen, H. N. & Reijo Pera, R. A. TopBP1 deficiency impairs the localization of proteins involved in Download PDF: Sorry, we are unable to provide the full text but you may find it at the following location(s): https://hal.archives-ouvertes.. (external link) https . 2012). PDS5A and PDS5B in Cohesin Function and Human Disease Diagnostic of failure to make DSBs, Mei4/ spermatocytes exhibit greatly reduced H2AX; lack of RAD51, DMC1, and RPA foci; synapsis defects; and meiotic prophase arrest (Kumar et al. 2014. 2005; Arnheim et al. A prominent feature of meiosis I is recombination, comprising the formation and repair of programmed DNA double-strand breaks (DSBs). 1Louis V. Gerstner Jr. Graduate School of Biomedical Sciences, Memorial Sloan Kettering Cancer Center, New York, New York 10065, 2Molecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, 3Howard Hughes Medical Institute, Memorial Sloan Kettering Cancer Center, New York, New York 10065. Mol. 2005; Hirota et al. Mets, D. G. & Meyer, B. J. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Xu L, Ajimura M, Padmore R, Klein C, Kleckner N Tarsounas M, Morita T, Pearlman RE, Moens PB 2008. 3A) (Keeney 2007; Maleki et al. Mutagen. 2013). 2004; Kugou et al. Meiosis is a specialized cell division that generates haploid cellsspores in yeasts, gametes in multicellular organismsfrom diploid progenitors. Bustamante Jaramillo L | PDF | Mitosis | Mitosis PRDM9 has a PR/SET domain at the amino terminus with histone H3K4 trimethyltransferase activity, and multiple C2H2-type zinc-finger DNA-binding motifs at the carboxyl terminus (Hayashi et al. MRX orthologs (Rad32Rad50Nbs1) are required for repair of meiotic DSBs but not their formation (Young et al. Chen, S. Y. et al. Rec14 interacts with Mde2 (Miyoshi et al. The yeast Ski complex: Crystal structure and RNA channeling to the exosome complex, Genetics of mammalian meiosis: Regulation, dynamics and impact on fertility, A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Genet . Natl Acad. Biol. Luo G, Yao MS, Bender CF, Mills M, Bladl AR, Bradley A, Petrini JH Mandon-Pepin, B. et al. Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery. Coordination of meiotic recombination, pairing, and synapsis by PHS1. 2010; Grey et al. 06 September 2022, Scientific Reports & Koopman, P. Retinoic acid, meiosis and germ cell fate in mammals. Kassir, Y., Granot, D. & Simchen, G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Aflatoonian, B. et al. 2007. Recombination between sister. His2Av phosphorylation and MI disjunction, but not the sterility defect, can be partially rescued by X-ray-induced DSBs, suggesting that Trem has a separate role in fertility (Lake et al. Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Although all organisms must match and lock homologous chromosomes to maintain genome integrity throughout meiosis, recent results indicate that the underlying mechanisms vary in different organisms. Regulation of meiotic recombination and prophase I progression in mammals 2009; Thomas et al. 2014). Findings in recent years from studies of meiotic recombination initiation in different organisms are providing a better understanding of the mechanism of meiotic DSB formation by Spo11, particularly of the cast of players required for Spo11-mediated break formation, the spatial distribution of DSBs and how Spo11 activity is targeted to these sites, as well as regulation of DSB timing, and feedback control of DSB numbers. 3A) (Miyoshi et al. 2013). 2005. This is a preview of subscription content, access via your institution. 2005. Rad3-Cds1 mediates coupling of initiation of meiotic recombination with DNA replication. 2010), so it is possible that breaks form in the context of axial structures (as opposed to broken segments being recruited to axes after DSB formation), as has been proposed for S. cerevisiae and S. pombe (see above). Mei4 and Rec114 were identified by a phylogenomic approach through conservation of short signature sequence motifs found in their hemiascomycetal orthologs (Maleki et al. Branching out: Meiotic recombination and its regulation. 59, 871877 (1998). This review highlights the features of meiotic recombination that distinguish it from recombinational repair in somatic cells, and how the molecular processes of meiotics recombination are embedded and interdependent with the chromosome structures that characterize meiotic prophase. Current opinion in genetics & development. Purification, folding and characterization of Rec12 (Spo11) meiotic recombinase of fission yeast, Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells, Sequence non-specific double-strand breaks and interhomolog interactions prior to double-strand break formation at a meiotic recombination hot spot in yeast. 2012. 2012. Genet. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S The process is highly conserved in eukaryotes, however the recent availability of mouse models for meiotic recombination has revealed surprising regulatory differences between simple unicellular organisms and those with increasingly complex genomes. 2003), but premeiotic replication is not a prerequisite for DSB formation (Hochwagen et al. Mutations in mammalian RAD51 homologs RAD51C and XRCC3 lead to embryonic lethality. 2012). Citations: 128 Author for correspondence: F. Chris H. Franklin Tel: +44 121 4145910 Email: f.c.h.franklin@bham.ac.uk PDF Tools Share Summary Meiosis is a central feature of sexual reproduction. Furthermore, they found that hot spot usage was variable and had a genetic basis. Fukuda T, Kugou K, Sasanuma H, Shibata T, Ohta K 2010). The timing of its localization and its ability to bind chromatin suggests Pdd1p is directly involved in communicating this information to the new macronucleus. Smith KN, Penkner A, Ohta K, Klein F, Nicolas A X chromosome inactivation is a complex process that occurs in marsupial and eutherian mammals. 2004. Proc. Hiraoka, Y. PMC legacy view Deh PM, Dichtl B, Schaft D, Roguev A, Pamblanco M, Lebrun R, Rodriguez-Gil A, Mkandawire M, Landsberg K, Shevchenko A, et al. Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. These studies define epigenetic characteristics of loci that are targets for SPO11-mediated DSB formation, and provide a framework for understanding the underlying signals and mechanisms of recombination site selection. Rigorous assessment of meiotic events is crucial for the successful application of assisted reproductive technologies and efforts directed to in vitro derivation of gametes. PubMedGoogle Scholar. In many species, the homology search accompanying recombination promotes recognition and pairing of homologs (Burgess 2002; Bhalla and Dernburg 2008). Exp. Takemoto et al. For this process, recombinases must localize to DNA double-strand breaks (DSBs). S. pombe does not form synaptonemal complexes, but instead forms structures called linear elements (LinEs) similar to the axial element precursors of the synaptonemal complex in S. cerevisiae (Loidl 2006). Mol. Murakami, H. & Keeney, S. Regulating the formation of DNA double-strand breaks in meiosis. Proc. Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Characterising the binding specificities of the subunits associated with the KMT2/Set1 histone lysine methyltransferase. Cell Biol. DSB-2 chromosome localization and protein levels depend on DSB-1, and DSB-1 localization is partially dependent on DSB-2, yet the two proteins do not colocalize extensively (Rosu et al. Science 296, 11151118 (2002). Regulation of Meiotic Prophase One in Mammalian Oocytes 2012; Sommermeyer et al. Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. 5, 6980 (2009). References 32 and 33 report that recombination initiation sites (hot spots) have signature chromatin modifications H3K4me3 2014 in yeast and mice. Miyoshi T, Ito M, Kugou K, Yamada S, Furuichi M, Oda A, Yamada T, Hirota K, Masai H, Ohta K Biol. Prieler S, Penkner A, Borde V, Klein F 2010. 2004. Reprod. Mde2 expression is regulated by the Rad3Cds1 meiotic replication checkpoint (Rad3 is the homolog of S. cerevisiae Mec1 and vertebrate ATR kinases), thereby providing a potential mechanism to coordinate replication with DSB formation (Ogino and Masai 2006; Miyoshi et al. J. Smolka, M. B., Albuquerque, C. P., Chen, S. H. & Zhou, H. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. These exchanges increase genome diversity and are essential for proper chromosome segregation at the first meiotic division. Google Scholar. Coop G, Wen X, Ober C, Pritchard JK, Przeworski M Schlecht, U. et al. 2013; Yamada and Ohta 2013; Fowler et al. Mol. 2007. The role of Rec114 phosphorylation is not altogether clear, but it has been proposed to mediate a negative feedback loop to inhibit DSB formation (see Concluding Remarks) (Carballo et al. Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. 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