Prophase I: Preparing Chromosomes for Segregation in the Develo** Oocyte

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Signaling-Mediated Control of Cell Division

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 59))

Abstract

Formation of an oocyte involves a specialized cell division termed meiosis. In meiotic prophase I (the initial stage of meiosis), chromosomes undergo elaborate events to ensure the proper segregation of their chromosomes into gametes. These events include processes leading to the formation of a crossover that, along with sister chromatid cohesion, forms the physical link between homologous chromosomes. Crossovers are formed as an outcome of recombination. This process initiates with programmed double-strand breaks that are repaired through the use of homologous chromosomes as a repair template. The accurate repair to form crossovers takes place in the context of the synaptonemal complex, a protein complex that links homologous chromosomes in meiotic prophase I. To allow proper execution of meiotic prophase I events, signaling processes connect different steps in recombination and synapsis. The events occurring in meiotic prophase I are a prerequisite for proper chromosome segregation in the meiotic divisions. When these processes go awry, chromosomes missegregate. These meiotic errors are thought to increase with aging and may contribute to the increase in aneuploidy observed in advanced maternal age female oocytes.

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References

  • Acquaviva L, Székvölgyi L, Dichtl B, Dichtl BS, de La Roche Saint-André C, Nicolas A, Géli V (2013) The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science 339:215–218

    Article  CAS  PubMed  Google Scholar 

  • Adrian AB, Comeron JM (2013) The Drosophila early ovarian transcriptome provides insight to the molecular causes of recombination rate variation across genomes. BMC Genomics 14:794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102:245–255

    Article  CAS  PubMed  Google Scholar 

  • Ajimura M, Leem SH, Ogawa H (1993) Identification of new genes required for meiotic recombination in Saccharomyces cerevisiae. Genetics 133:51–66

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson DE, Losada A, Erickson HP, Hirano T (2002) Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol 156:419–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angell RR (1991) Predivision in human oocytes at meiosis I: a mechanism for trisomy formation in man. Hum Genet 86:383–387

    Article  CAS  PubMed  Google Scholar 

  • Archambault V, Lépine G, Kachaner D (2015) Understanding the Polo Kinase machine. Oncogene 34:4799–4807

    Article  CAS  PubMed  Google Scholar 

  • Arumugam P, Gruber S, Tanaka K, Haering CH, Mechtler K, Nasmyth K (2003) ATP hydrolysis is required for cohesin’s association with chromosomes. Curr Biol 13:1941–1953

    Article  CAS  PubMed  Google Scholar 

  • Arur S, Ohmachi M, Nayak S, Hayes M, Miranda A, Hay A, Golden A, Schedl T (2009) Multiple ERK substrates execute single biological processes in Caenorhabditis elegans germ-line development. Proc Natl Acad Sci USA 106:4776–4781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badugu SB, Nabi SA, Vaidyam P, Laskar S, Bhattacharyya S, Bhattacharyya MK (2015) Identification of Plasmodium falciparum DNA repair protein Mre11 with an evolutionarily conserved nuclease function. PLoS One 10(5):e0125358. PMID: 25938776

    Google Scholar 

  • Bailly AP, Freeman A, Hall J, Déclais A-C, Alpi A, Lilley DMJ, Ahmed S, Gartner A (2010) The Caenorhabditis elegans homolog of Gen1/Yen1 resolvases links DNA damage signaling to DNA double-strand break repair. PLoS Genet 6:e1001025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, Yao X, Christie DM, Monell C, Arnheim N, Bradley A et al (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13:336–342

    Article  CAS  PubMed  Google Scholar 

  • Baker CL, Walker M, Kajita S, Petkov PM, Paigen K (2014) PRDM9 binding organizes hotspot nucleosomes and limits Holliday junction migration. Genome Res 24:724–732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, De Massy B (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327:836–840

    Article  CAS  PubMed  Google Scholar 

  • Berg IL, Neumann R, Lam K-WG, Sarbajna S, Odenthal-Hesse L, May CA, Jeffreys AJ (2010) PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet 42:859–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhuiyan H, Schmekel K (2004) Meiotic chromosome synapsis in yeast can occur without spo11-induced DNA double-strand breaks. Genetics 168:775–783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bishop DK, Zickler D (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117:9–15

    Article  CAS  PubMed  Google Scholar 

  • Bishop DK, Park D, Xu L, Kleckner N (1992) DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439–456

    Article  CAS  PubMed  Google Scholar 

  • Bisig CG, Guiraldelli MF, Kouznetsova A, Scherthan H, Hoog C, Dawson DS, Pezza RJ (2012) Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLoS Genet 8:e1002701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blat Y, Protacio RU, Hunter N, Kleckner N (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111:791–802

    Article  CAS  PubMed  Google Scholar 

  • Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-Otero RD (2013) Homologous pairing preceding SPO11-mediated double-strand breaks in mice. Dev Cell 24:196–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR 3rd, Russell P (2000) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107(4):537–548

    Article  Google Scholar 

  • Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR, Russell P (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537–548

    Article  CAS  PubMed  Google Scholar 

  • Bolcun-Filas E, Rinaldi VD, White ME, Schimenti JC (2014) Reversal of female infertility by Chk2 ablation reveals the oocyte DNA damage checkpoint pathway. Science 343:533–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Börner GV, Kleckner N, Hunter N (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:29–45

    Article  PubMed  Google Scholar 

  • Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature 485:642–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brockway H, Balukoff N, Dean M, Alleva B, Smolikove S (2014) The CSN/COP9 signalosome regulates synaptonemal complex assembly during meiotic prophase I of Caenorhabditis elegans. PLoS Genet 10:e1004757

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brown MS, Bishop DK (2015) DNA strand exchange and RecA homologs in meiosis. Cold Spring Harb Perspect Biol 7:a016659

    Article  PubMed Central  CAS  Google Scholar 

  • Brown AS, Feingold E, Broman KW, Sherman SL (2000) Genome-wide variation in recombination in female meiosis: a risk factor for non-disjunction of chromosome 21. Hum Mol Genet 9:515–523

    Article  CAS  PubMed  Google Scholar 

  • Brown MS, Grubb J, Zhang A, Rust MJ, Bishop DK (2015) Small Rad51 and Dmc1 complexes often co-occupy both ends of a meiotic DNA double strand break. PLoS Genet 11:e1005653

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bugge M, Collins A, Petersen MB, Fisher J, Brandt C, Hertz JM, Tranebjaerg L, de Lozier-Blanchet C, Nicolaides P, Brøndum-Nielsen K et al (1998) Non-disjunction of chromosome 18. Hum Mol Genet 7:661–669

    Article  CAS  PubMed  Google Scholar 

  • Bugge M, Collins A, Hertz JM, Eiberg H, Lundsteen C, Brandt CA, Bak M, Hansen C, Delozier CD, Lespinasse J et al (2007) Non-disjunction of chromosome 13. Hum Mol Genet 16:2004–2010

    Article  CAS  PubMed  Google Scholar 

  • Buonomo SB, Clyne RK, Fuchs J, Loidl J, Uhlmann F, Nasmyth K (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 103:387–398

    Article  CAS  PubMed  Google Scholar 

  • Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, Sung P (2008) Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev 22:786–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busygina V, Saro D, Williams G, Leung WK, Say AF, Sehorn MG, Sung P, Tsubouchi H (2012) Novel attributes of Hed1 affect dynamics and activity of the Rad51 presynaptic filament during meiotic recombination. J Biol Chem 287:1566–1575

    Article  CAS  PubMed  Google Scholar 

  • Cannavo E, Cejka P (2014) Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature 514:122–125

    Article  CAS  PubMed  Google Scholar 

  • Carballo JA, Johnson AL, Sedgwick SG, Cha RS (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132:758–770

    Article  CAS  PubMed  Google Scholar 

  • Carballo JA, Panizza S, Serrentino ME, Johnson AL, Geymonat M, Borde V, Klein F, Cha RS (2013) Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery. PLoS Genet 9:e1003545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carney JP, Maser RS, Olivares H, Davis EM, Le Beau M, Yates JR, Hays L, Morgan WF, Petrini JH (1998) The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93:477–486

    Article  CAS  PubMed  Google Scholar 

  • Carpenter AT (1975) Electron microscopy of meiosis in Drosophila melanogaster females. I. Structure, arrangement, and temporal change of the synaptonemal complex in wild-type. Chromosoma 51:157–182

    Article  CAS  PubMed  Google Scholar 

  • Cartagena-Lirola H, Guerini I, Viscardi V, Lucchini G, Longhese MP (2006) Budding yeast Sae2 is an in vivo target of the Mec1 and Tel1 checkpoint kinases during meiosis. Cell Cycle 5:1549–1559

    Article  CAS  PubMed  Google Scholar 

  • Challa K, Lee M-S, Shinohara M, Kim KP, Shinohara A (2016) Rad61/Wpl1 (Wapl), a cohesin regulator, controls chromosome compaction during meiosis. Nucleic Acids Res. doi:10.1093/nar/gkw034

    Google Scholar 

  • Chase D, Serafinas C, Ashcroft N, Kosinski M, Longo D, Ferris DK, Golden A (2000) The polo-like kinase PLK-1 is required for nuclear envelope breakdown and the completion of meiosis in Caenorhabditis elegans. Genesis 26:26–41

    Article  CAS  PubMed  Google Scholar 

  • Chen R, Wold MS (2014) Replication protein A: single-stranded DNA’s first responder: dynamic DNA-interactions allow replication protein A to direct single-strand DNA intermediates into different pathways for synthesis or repair. Bioessays 36:1156–1161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Suhandynata RT, Sandhu R, Rockmill B, Mohibullah N, Niu H, Liang J, Lo H-C, Miller DE, Zhou H et al (2015) Phosphorylation of the synaptonemal complex protein Zip1 regulates the crossover/noncrossover decision during yeast meiosis. Plos Biol 13:e1002329

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen Y-J, Chuang Y-C, Chuang C-N, Cheng Y-H, Chang C-R, Leng C-H, Wang T-F (2016) S. cerevisiae Mre11 recruits conjugated SUMO moieties to facilitate the assembly and function of the Mre11-Rad50-Xrs2 complex. Nucleic Acids Res. doi:10.1093/nar/gkv1523

    Google Scholar 

  • Cheng C-H, Lo Y-H, Liang S-S, Ti S-C, Lin F-M, Yeh C-H, Huang H-Y, Wang T-F (2006) SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20:2067–2081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng EY, Hunt PA, Naluai-Cecchini TA, Fligner CL, Fujimoto VY, Pasternack TL, Schwartz JM, Steinauer JE, Woodruff TJ, Cherry SM et al (2009) Meiotic recombination in human oocytes. PLoS Genet 5:e1000661

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cherry SM, Adelman CA, Theunissen JW, Hassold TJ, Hunt PA, Petrini JHJ (2007) The Mre11 complex influences DNA repair, synapsis, and crossing over in murine meiosis. Curr Biol 17:373–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chikashige Y, Ding DQ, Funabiki H, Haraguchi T, Mashiko S, Yanagida M, Hiraoka Y (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science 264:270–273

    Article  CAS  PubMed  Google Scholar 

  • Christophorou N, Rubin T, Bonnet I, Piolot T, Arnaud M, Huynh J-R (2015) Microtubule-driven nuclear rotations promote meiotic chromosome dynamics. Nat Cell Biol 17:1388–1400

    Article  CAS  PubMed  Google Scholar 

  • Church DL, Guan KL, Lambie EJ (1995) Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 121:2525–2535

    CAS  PubMed  Google Scholar 

  • Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Nasmyth K (2000) Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5:243–254

    Article  CAS  PubMed  Google Scholar 

  • Cloud V, Chan Y-L, Grubb J, Budke B, Bishop DK (2012) Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337:1222–1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colaiácovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, Villeneuve AM (2003) Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5:463–474

    Article  PubMed  Google Scholar 

  • Conrad MN, Lee C-Y, Chao G, Shinohara M, Kosaka H, Shinohara A, Conchello J-A, Dresser ME (2008) Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133:1175–1187

    Article  CAS  PubMed  Google Scholar 

  • Costelloe T, Louge R, Tomimatsu N, Mukherjee B, Martini E, Khadaroo B, Dubois K, Wiegant WW, Thierry A, Burma S et al (2012) The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489:581–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couteau F, Zetka M (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev Cell 20:353–363

    Article  CAS  PubMed  Google Scholar 

  • Crawley O, Barroso C, Testori S, Ferrandiz N, Silva N, Castellano-Pozo M, Jaso-Tamame AL, Martinez-Perez E (2016) Cohesin-interacting protein WAPL-1 regulates meiotic chromosome structure and cohesion by antagonizing specific cohesin complexes. eLife 5:563

    Article  Google Scholar 

  • Cremona CA, Sarangi P, Yang Y, Hang LE, Rahman S, Zhao X (2012) Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the mec1 checkpoint. Mol Cell 45:422–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Carvalho CE, Zaaijer S, Smolikov S, Gu Y, Schumacher JM, Colaiácovo MP (2008) LAB-1 antagonizes the Aurora B kinase in C. elegans. Genes Dev 22:2869–2885

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Vries FAT, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, Liu J-G, van Zeeland AA, Heyting C, Pastink A (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19:1376–1389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387–398

    Article  CAS  PubMed  Google Scholar 

  • Ding D-Q, Sakurai N, Katou Y, Itoh T, Shirahige K, Haraguchi T, Hiraoka Y (2006) Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast. J Cell Biol 174:499–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12:863–872

    Article  CAS  PubMed  Google Scholar 

  • Ding D-Q, Matsuda A, Okamasa K, Nagahama Y, Haraguchi T, Hiraoka Y (2016) Meiotic cohesin-based chromosome structure is essential for homologous chromosome pairing in Schizosaccharomyces pombe. Chromosoma 125(2):205–214

    Article  CAS  PubMed  Google Scholar 

  • Dodson GE, Limbo O, Nieto D, Russell P (2010) Phosphorylation-regulated binding of Ctp1 to Nbs1 is critical for repair of DNA double-strand breaks. Cell Cycle 9:1516–1522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dresser ME, Giroux CN (1988) Meiotic chromosome behavior in spread preparations of yeast. J Cell Biol 106:567–573

    Article  CAS  PubMed  Google Scholar 

  • Eichinger CS, Jentsch S (2010) Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1. Proc Natl Acad Sci USA 107:11370–11375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C (2003) Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J Cell Biol 160:657–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falck J, Forment JV, Coates J, Mistrik M, Lukas J, Bartek J, Jackson SP (2012) CDK targeting of NBS1 promotes DNA-end resection, replication restart and homologous recombination. EMBO Rep 13:561–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falk JE, Chan AC-H, Hoffmann E, Hochwagen A (2010) A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 19:599–611

    Article  CAS  PubMed  Google Scholar 

  • Fan H-Y, Sun Q-Y (2004) Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod 70:535–547

    Article  CAS  PubMed  Google Scholar 

  • Fan H-Y, Liu Z, Mullany LK, Richards JS (2012) Consequences of RAS and MAPK activation in the ovary: the good, the bad and the ugly. Mol Cell Endocrinol 356:74–79

    Article  CAS  PubMed  Google Scholar 

  • Fawcett DW (1956) The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J Biophys Biochem Cytol 2:403–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fragouli E, Alfarawati S, Goodall N-N, Sánchez-García JF, Colls P, Wells D (2011) The cytogenetics of polar bodies: insights into female meiosis and the diagnosis of aneuploidy. Mol Hum Reprod 17:286–295

    Article  PubMed  Google Scholar 

  • Fragouli E, Alfarawati S, Spath K, Jaroudi S, Sarasa J, Enciso M, Wells D (2013) The origin and impact of embryonic aneuploidy. Hum Genet 132:1001–1013

    Article  PubMed  Google Scholar 

  • Fraune J, Schramm S, Alsheimer M, Benavente R (2012) The mammalian synaptonemal complex: protein components, assembly and role in meiotic recombination. Exp Cell Res 318:1340–1346

    Article  CAS  PubMed  Google Scholar 

  • Fukuda T, Hoog C (2010) The mouse cohesin-associated protein PDS5B is expressed in testicular cells and is associated with the meiotic chromosome axes. Genes (Basel) 1:484–494

    CAS  Google Scholar 

  • Fukuda T, Pratto F, Schimenti JC, Turner JMA, Camerini-Otero RD, Hoog C (2012) Phosphorylation of chromosome core components may serve as axis marks for the status of chromosomal events during mammalian meiosis. PLoS Genet 8:e1002485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukushima K, Tanaka Y, Nabeshima K, Yoneki T, Tougan T, Tanaka S, Nojima H (2000) Dmc1 of Schizosaccharomyces pombe plays a role in meiotic recombination. Nucleic Acids Res 28:2709–2716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furuse M, Nagase Y, Tsubouchi H, Murakami-Murofushi K, Shibata T, Ohta K (1998) Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J 17:6412–6425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao J, Kim H-M, Elia AE, Elledge SJ, Colaiácovo MP (2015) NatB domain-containing CRA-1 antagonizes hydrolase ACER-1 linking acetyl-CoA metabolism to the initiation of recombination during C. elegans meiosis. PLoS Genet 11:e1005029

    Google Scholar 

  • Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ (2015) Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation. Nature 520:114–118

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Cruz R, Casanovas A, Brieno-Enriquez M, Robles P, Roig I, Pujol A, Cabero L, Durban M, Garcia Caldes M (2010) Cytogenetic analyses of human oocytes provide new data on non-disjunction mechanisms and the origin of trisomy 16. Hum Reprod 25:179–191

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Muse T, Boulton SJ (2005) Distinct modes of ATR activation after replication stress and DNA double-strand breaks in Caenorhabditis elegans. EMBO J 24:4345–4355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK (1998) Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev 12:2208–2221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gasior SL, Olivares H, Ear U, Hari DM, Weichselbaum R, Bishop DK (2001) Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis. Proc Natl Acad Sci USA 98:8411–8418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gause M, Webber HA, Misulovin Z, Haller G, Rollins RA, Eissenberg JC, Bickel SE, Dorsett D (2008) Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells. Chromosoma 117:51–66

    Article  CAS  PubMed  Google Scholar 

  • Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, Petes TD (2000) Inaugural Article: Global map** of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 97:11383–11390

    Google Scholar 

  • Getun IV, Wu ZK, Khalil AM, Bois PRJ (2010) Nucleosome occupancy landscape and dynamics at mouse recombination hotspots. EMBO Rep 11:555–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh S, Feingold E, Dey SK (2009) Etiology of Down syndrome: evidence for consistent association among altered meiotic recombination, nondisjunction, and maternal age across populations. Am J Med Genet 149A:1415–1420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goedecke W, Eijpe M, Offenberg HH, van Aalderen M, Heyting C (1999) Mre11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis. Nat Genet 23:194–198

    Article  CAS  PubMed  Google Scholar 

  • Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14:263–274

    Article  CAS  PubMed  Google Scholar 

  • Govin J, Dorsey J, Gaucher J, Rousseaux S, Khochbin S, Berger SL (2010) Systematic screen reveals new functional dynamics of histones H3 and H4 during gametogenesis. Genes Dev 24:1772–1786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guleria A, Chandna S (2016) ATM kinase: much more than a DNA damage responsive protein. DNA Repair 39:1–20

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Caballero C, Herrán Y, Sánchez-Martín M, Suja JA, Barbero JL, Llano E, Pendás AM (2011) Identification and molecular characterization of the mammalian α-kleisin RAD21L. Cell Cycle 10:1477–1487

    Article  PubMed  CAS  Google Scholar 

  • Haering CH, Löwe J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9:773–788

    Article  CAS  PubMed  Google Scholar 

  • Hall HE, Chan ER, Collins A, Judis L, Shirley S, Surti U, Hoffner L, Cockwell AE, Jacobs PA, Hassold TJ (2007a) The origin of trisomy 13. Am J Med Genet 143A:2242–2248

    Article  PubMed  Google Scholar 

  • Hall HE, Surti U, Hoffner L, Shirley S, Feingold E, Hassold T (2007b) The origin of trisomy 22: evidence for acrocentric chromosome-specific patterns of nondisjunction. Am J Med Genet 143A:2249–2255

    Article  PubMed  Google Scholar 

  • Harper L (2004) A bouquet of chromosomes. J Cell Sci 117:4025–4032

    Article  CAS  PubMed  Google Scholar 

  • Harper NC, Rillo R, Jover-Gil S, Assaf ZJ, Bhalla N, Dernburg AF (2011) Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev Cell 21:934–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey SH, Krien MJE, O’Connell MJ (2002) Structural maintenance of chromosomes (SMC) proteins, a family of conserved ATPases. Genome Biol 3:REVIEWS3003

    Google Scholar 

  • Hassold T, Chiu D (1985) Maternal age-specific rates of numerical chromosome abnormalities with special reference to trisomy. Hum Genet 70:11–17

    Article  CAS  PubMed  Google Scholar 

  • Hassold T, Merrill M, Adkins K, Freeman S, Sherman S (1995) Recombination and maternal age-dependent nondisjunction: molecular studies of trisomy 16. Am J Hum Genet 57:867–874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hayase A, Takagi M, Miyazaki T, Oshiumi H, Shinohara M, Shinohara A (2004) A protein complex containing Mei5 and Sae3 promotes the assembly of the meiosis-specific RecA homolog Dmc1. Cell 119:927–940

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K, Yoshida K, Matsui Y (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438:374–378

    Article  CAS  PubMed  Google Scholar 

  • Hayashi M, Chin GM, Villeneuve AM (2007) C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet 3:e191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heidmann D, Horn S, Heidmann S, Schleiffer A, Nasmyth K, Lehner CF (2004) The Drosophila meiotic kleisin C(2)M functions before the meiotic divisions. Chromosoma 113:177–187

    Article  CAS  PubMed  Google Scholar 

  • Herbert M, Kalleas D, Cooney D, Lamb M, Lister L (2015) Meiosis and maternal aging: insights from aneuploid oocytes and trisomy births. Cold Spring Harb Perspect Biol 7:a017970

    Article  PubMed  CAS  Google Scholar 

  • Herrán Y, Gutiérrez-Caballero C, Sánchez-Martín M, Hernández T, Viera A, Barbero JL, de Álava E, de Rooij DG, Suja JA, Llano E et al (2011) The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility. EMBO J 30:3091–3105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hill WG, Robertson A (2007) The effect of linkage on limits to artificial selection. Genet Res 89:311–336

    Article  CAS  PubMed  Google Scholar 

  • Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA (2005) SMC1β-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37:1351–1355

    Article  CAS  PubMed  Google Scholar 

  • Holloway JK, Booth J, Edelmann W, McGowan CH, Cohen PE (2008) MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLoS Genet 4:e1000186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holloway JK, Mohan S, Balmus G, Sun X, Modzelewski A, Borst PL, Freire R, Weiss RS, Cohen PE (2011) Mammalian BTBD12 (SLX4) protects against genomic instability during mammalian spermatogenesis. PLoS Genet 7:e1002094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holloway JK, Sun X, Yokoo R, Villeneuve AM, Cohen PE (2014) Mammalian CNTD1 is critical for meiotic crossover maturation and deselection of excess precrossover sites. J Cell Biol 205:633–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong S, Sung Y, Yu M, Lee M, Kleckner N, Kim KP (2013) The logic and mechanism of homologous recombination partner choice. Mol Cell 51:440–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hooker GW, Roeder GS (2006) A role for SUMO in meiotic chromosome synapsis. Curr Biol 16:1238–1243

    Article  CAS  PubMed  Google Scholar 

  • Hopfner K-P, Tainer JA (2003) Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures. Curr Opin Struct Biol 13:249–255

    Article  CAS  PubMed  Google Scholar 

  • Horn HF, Kim DI, Wright GD, Wong ESM, Stewart CL, Burke B, Roux KJ (2013) A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J Cell Biol 202:1023–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Itoh T, Mishra A, Katoh Y, Chan K-L, Upcher W, Godlee C, Roig MB, Shirahige K, Nasmyth K (2011) ATP hydrolysis is required for relocating cohesin from sites occupied by its Scc2/4 loading complex. Curr Biol 21:12–24

    Article  CAS  PubMed  Google Scholar 

  • Huang CE, Milutinovich M, Koshland D (2005) Rings, bracelet or snaps: fashionable alternatives for Smc complexes. Philos Trans R Soc Lond B Biol Sci 360:537–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Humphryes N, Leung W-K, Argunhan B, Terentyev Y, Dvorackova M, Tsubouchi H (2013) The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLoS Genet 9:e1003194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter N, Borts RH (1997) Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev 11:1573–1582

    Article  CAS  PubMed  Google Scholar 

  • Ishiguro K-I, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y (2011) A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep 12:267–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanov EL, Korolev VG, Fabre F (1992) XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics 132:651–664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanov D, Schleiffer A, Eisenhaber F, Mechtler K, Haering CH, Nasmyth K (2002) Eco1 is a novel acetyltransferase that can acetylate proteins involved in cohesion. Curr Biol 12:323–328

    Article  CAS  PubMed  Google Scholar 

  • Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24:7998–8006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeffreys CA, Burrage PS, Bickel SE (2003) A model system for increased meiotic nondisjunction in older oocytes. Curr Biol 13:498–503

    Article  CAS  PubMed  Google Scholar 

  • ** H, Guacci V, Yu H-G (2009) Pds5 is required for homologue pairing and inhibits synapsis of sister chromatids during yeast meiosis. J Cell Biol 186:713–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johzuka K, Ogawa H (1995) Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139:1521–1532

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jordan PW, Karppinen J, Handel MA (2012) Polo-like kinase is required for synaptonemal complex disassembly and phosphorylation in mouse spermatocytes. J Cell Sci 125:5061–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi N, Brown MS, Bishop DK, Börner GV (2015) Gradual implementation of the meiotic recombination program via checkpoint pathways controlled by global DSB levels. Mol Cell 57:797–811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joyce EF, Pedersen M, Tiong S, White-Brown SK, Paul A, Campbell SD, McKim KS (2011) Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair. J Cell Biol 195:359–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joyce EF, Paul A, Chen KE, Tanneti N, McKim KS (2012) Multiple barriers to nonhomologous DNA end joining during meiosis in Drosophila. Genetics 191:739–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–384

    Article  CAS  PubMed  Google Scholar 

  • Kelly KO, Dernburg AF, Stanfield GM, Villeneuve AM (2000) Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156:617–630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim Y, Kostow N, Dernburg AF (2015) The chromosome axis mediates feedback control of CHK-2 to ensure crossover formation in C. elegans. Dev Cell 35:247–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427:510–517

    Article  CAS  PubMed  Google Scholar 

  • Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98:91–103

    Article  CAS  PubMed  Google Scholar 

  • Klug H, Xaver M, Chaugule VK, Koidl S, Mittler G, Klein F, Pichler A (2013) Ubc9 sumoylation controls SUMO chain formation and meiotic synapsis in Saccharomyces cerevisiae. Mol Cell 50:625–636

    Article  CAS  PubMed  Google Scholar 

  • Koh-Stenta X, Joy J, Poulsen A, Li R, Tan Y, Shim Y, Min J-H, Wu L, Ngo A, Peng J et al (2014) Characterization of the histone methyltransferase PRDM9 using biochemical, biophysical and chemical biology techniques. Biochem J 461:323–334

    Article  CAS  PubMed  Google Scholar 

  • Kolodkin AL, Klar AJ, Stahl FW (1986) Double-strand breaks can initiate meiotic recombination in S. cerevisiae. Cell 46:733–740

    Article  CAS  PubMed  Google Scholar 

  • Koshland D, Strunnikov A (1996) Mitotic chromosome condensation. Annu Rev Cell Dev Biol 12:305–333

    Article  CAS  PubMed  Google Scholar 

  • Krishnaprasad GN, Anand MT, Lin G, Tekkedil MM, Steinmetz LM, Nishant KT (2015) Variation in crossover frequencies perturb crossover assurance without affecting meiotic chromosome segregation in Saccharomyces cerevisiae. Genetics 199:399–412

    Article  PubMed  Google Scholar 

  • Kudo NR, Wassmann K, Anger M, Schuh M, Wirth KG, Xu H, Helmhart W, Kudo H, Mckay M, Maro B et al (2006) Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 126:135–146

    Article  CAS  PubMed  Google Scholar 

  • Kuleszewicz K, Fu X, Kudo NR (2013) Cohesin loading factor Nipbl localizes to chromosome axes during mammalian meiotic prophase. Cell Div 8:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuznetsov S, Pellegrini M, Shuda K, Fernandez-Capetillo O, Liu Y, Martin BK, Burkett S, Southon E, Pati D, Tessarollo L et al (2007) RAD51C deficiency in mice results in early prophase I arrest in males and sister chromatid separation at metaphase II in females. J Cell Biol 176:581–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labella S, Woglar A, Jantsch V, Zetka M (2011) Polo kinases establish links between meiotic chromosomes and cytoskeletal forces essential for homolog pairing. Dev Cell 21:948–958

    Article  CAS  PubMed  Google Scholar 

  • Lam I, Keeney S (2015) Nonparadoxical evolutionary stability of the recombination initiation landscape in yeast. Science 350:932–937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamb NE, Freeman SB, Savage-Austin A, Pettay D, Taft L, Hersey J, Gu Y, Shen J, Saker D, May KM et al (1996) Susceptible chiasmate configurations of chromosome 21 predispose to non-disjunction in both maternal meiosis I and meiosis II. Nat Genet 14:400–405

    Article  CAS  PubMed  Google Scholar 

  • Lamb NE, Feingold E, Savage A, Avramopoulos D, Freeman S, Gu Y, Hallberg A, Hersey J, Karadima G, Pettay D et al (1997) Characterization of susceptible chiasma configurations that increase the risk for maternal nondisjunction of chromosome 21. Hum Mol Genet 6:1391–1399

    Article  CAS  PubMed  Google Scholar 

  • Lamb NE, Yu K, Shaffer J, Feingold E, Sherman SL (2005) Association between maternal age and meiotic recombination for trisomy 21. Am J Hum Genet 76:91–99

    Article  CAS  PubMed  Google Scholar 

  • Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S (2011) ATM controls meiotic double-strand-break formation. Nature 479:237–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lao JP, Cloud V, Huang C-C, Grubb J, Thacker D, Lee C-Y, Dresser ME, Hunter N, Bishop DK (2013) Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet 9:e1003978

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Latypov V, Rothenberg M, Lorenz A, Octobre G, Csutak O, Lehmann E, Loidl J, Kohli J (2010) Roles of Hop1 and Mek1 in meiotic chromosome pairing and recombination partner choice in Schizosaccharomyces pombe. Mol Cell Biol 30:1570–1581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Hirano T (2011) RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol 192:263–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee MH, Ohmachi M, Arur S, Nayak S, Francis R, Church D, Lambie E, Schedl T (2007) Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development. Genetics 177:2039–2062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, Miyake M, Watanabe Y (2008) Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nature 10:42–52

    CAS  Google Scholar 

  • Lee JY, Terakawa T, Qi Z, Steinfeld JB, Redding S, Kwon Y, Gaines WA, Zhao W, Sung P, Greene EC (2015) DNA recombination. Base triplet step** by the Rad51/RecA family of recombinases. Science 349:977–981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemmens BBLG, Johnson NM, Tijsterman M (2013) COM-1 promotes homologous recombination during Caenorhabditis elegans meiosis by antagonizing Ku-mediated non-homologous end joining. PLoS Genet 9:e1003276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leung W-K, Humphryes N, Afshar N, Argunhan B, Terentyev Y, Tsubouchi T, Tsubouchi H (2015) The synaptonemal complex is assembled by a polySUMOylation-driven feedback mechanism in yeast. J Cell Biol 211:785–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XC, Bolcun-Filas E, Schimenti JC (2011) Genetic evidence that synaptonemal complex axial elements govern recombination pathway choice in mice. Genetics 189:71–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM (2013) Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature 502:703–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lightfoot J, Testori S, Barroso C, Martinez-Perez E (2011) Loading of meiotic cohesin by SCC-2 is required for early processing of DSBs and for the DNA damage checkpoint. Curr Biol 21:1421–1430

    Article  CAS  PubMed  Google Scholar 

  • Lin Z, Kong H, Nei M, Ma H (2006) Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. Proc Natl Acad Sci USA 103:10328–10333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin F-M, Lai Y-J, Shen H-J, Cheng Y-H, Wang T-F (2010) Yeast axial-element protein, Red1, binds SUMO chains to promote meiotic interhomologue recombination and chromosome synapsis. EMBO J 29:586–596

    Article  CAS  PubMed  Google Scholar 

  • Lin W, ** H, Liu X, Hampton K, Yu H-G (2011) Scc2 regulates gene expression by recruiting cohesin to the chromosome as a transcriptional activator during yeast meiosis. Mol Biol Cell 22:1985–1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lipkin SM, Moens PB, Wang V, Lenzi M, Shanmugarajah D, Gilgeous A, Thomas J, Cheng J, Touchman JW, Green ED et al (2002) Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat Genet 31:385–390

    CAS  PubMed  Google Scholar 

  • Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y et al (2010) Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20:1511–1521

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Keefe DL (2008) Defective cohesin is associated with age-dependent misaligned chromosomes in oocytes. Reprod Biomed Online 16:103–112

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Tarsounas M, O’regan P, West SC (2007) Role of RAD51C and XRCC3 in genetic recombination and DNA repair. J Biol Chem 282:1973–1979

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, Heyer W-D (2011) Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 479:245–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Llano E, Herrán Y, García-Tuñón I, Gutiérrez-Caballero C, de Álava E, Barbero JL, Schimenti J, de Rooij DG, Sánchez-Martín M, Pendás AM (2012) Meiotic cohesin complexes are essential for the formation of the axial element in mice. J Cell Biol 197:877–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorenz A, Mehats A, Osman F, Whitby MC (2014) Rad51/Dmc1 paralogs and mediators oppose DNA helicases to limit hybrid DNA formation and promote crossovers during meiotic recombination. Nucleic Acids Res 42:13723–13735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lovett ST, Mortimer RK (1987) Characterization of null mutants of the RAD55 gene of Saccharomyces cerevisiae: effects of temperature, osmotic strength and mating type. Genetics 116:547–553

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lynn A, Soucek R, Börner GV (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15:591–605

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Milman N, Nambiar M, Smith GR (2015) Two separable functions of Ctp1 in the early steps of meiotic DNA double-strand break repair. Nucleic Acids Res 43:7349–7359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacQueen AJ, Villeneuve AM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15:1674–1687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacQueen AJ, Colaiácovo MP, McDonald K, Villeneuve AM (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16:2428–2442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123:1037–1050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malone RE, Haring SJ, Foreman KE, Pansegrau ML, Smith SM, Houdek DR, Carpp L, Shah B, Lee KE (2004) The signal from the initiation of meiotic recombination to the first division of meiosis. Eukaryot Cell 3:598–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manfrini N, Guerini I, Citterio A, Lucchini G, Longhese MP (2010) Processing of meiotic DNA double strand breaks requires cyclin-dependent kinase and multiple nucleases. J Biol Chem 285:11628–11637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao-Draayer Y, Galbraith AM, Pittman DL, Cool M, Malone RE (1996) Analysis of meiotic recombination pathways in the yeast Saccharomyces cerevisiae. Genetics 144:71–86

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martin RH, Ko E, Rademaker A (1991) Distribution of aneuploidy in human gametes: comparison between human sperm and oocytes. Am J Med Genet 39:321–331

    Article  CAS  PubMed  Google Scholar 

  • Martin JS, Winkelmann N, Petalcorin MIR, McIlwraith MJ, Boulton SJ (2005) RAD-51-dependent and -independent roles of a Caenorhabditis elegans BRCA2-related protein during DNA double-strand break repair. Mol Cell Biol 25:3127–3139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matos J, Blanco MG, Maslen S, Skehel JM, West SC (2011) Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell 147:158–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKim KS, Hayashi-Hagihara A (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev 12:2932–2942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, Khodosh R, Hawley RS (1998) Meiotic synapsis in the absence of recombination. Science 279:876–878

    Article  CAS  PubMed  Google Scholar 

  • Michaelis C, Ciosk R, Nasmyth K (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91:35–45

    Article  CAS  PubMed  Google Scholar 

  • Miles DC, van den Bergen JA, Sinclair AH, Western PS (2010) Regulation of the female mouse germ cell cycle during entry into meiosis. Cell Cycle 9:408–418

    Article  CAS  PubMed  Google Scholar 

  • Mimitou EP, Symington LS (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770–774

    Article  CAS  PubMed  Google Scholar 

  • Moreau S, Ferguson JR, Symington LS (1999) The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol Cell Biol 19:556–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morelli MA, Cohen PE (2005) Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130:761–781

    Article  CAS  PubMed  Google Scholar 

  • Morimoto A, Shibuya H, Zhu X, Kim J, Ishiguro K-I, Han M, Watanabe Y (2012) A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol 198:165–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moses MJ (1956) Chromosomal structures in crayfish spermatocytes. J Biophys Biochem Cytol 2:215–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moses MJ (1958) The relation between the axial complex of meiotic prophase chromosomes and chromosome pairing in a salamander (Plethodon cinereus). J Biophys Biochem Cytol 4:633–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ (2001) Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:103–118

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murayama Y, Uhlmann F (2014) Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature 505:367–371

    Article  CAS  PubMed  Google Scholar 

  • Nabeshima K, Villeneuve AM, Colaiácovo MP (2005) Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J Cell Biol 168:683–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadarajan S, Mohideen F, Tzur YB, Ferrandiz N, Crawley O, Montoya A, Faull P, Snijders AP, Cutillas PR, Jambhekar A et al (2016) The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis. eLife 5:e12039

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagaoka SI, Hassold TJ, Hunt PA (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13:493–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nairz K, Klein F (1997) mre11S--a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev 11:2272–2290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neale MJ, Pan J, Keeney S (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nešić D, Hsu Y, Stebbins CE (2004) Assembly and function of a bacterial genotoxin. Nature 429:429–433

    Article  PubMed  CAS  Google Scholar 

  • Nishant KT, Chen C, Shinohara M, Shinohara A, Alani E (2010) Genetic analysis of baker’s yeast Msh4-Msh5 reveals a threshold crossover level for meiotic viability. PLoS Genet 6:e1001083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Niu H, Li X, Job E, Park C, Moazed D, Gygi SP, Hollingsworth NM (2007) Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis. Mol Cell Biol 27:5456–5467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niwa O, Shimanuki M, Miki F (2000) Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J 19:3831–3840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Novak JE, Ross-Macdonald PB, Roeder GS (2001) The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158:1013–1025

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oh SD, Lao JP, Taylor AF, Smith GR, Hunter N (2008) RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol Cell 31:324–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver TR, Feingold E, Yu K, Cheung V, Tinker S, Yadav-Shah M, Masse N, Sherman SL (2008) New insights into human nondisjunction of chromosome 21 in oocytes. PLoS Genet 4:e1000033–e1000039

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oliver TR, Tinker SW, Allen EG, Hollis N, Locke AE, Bean LJH, Chowdhury R, Begum F, Marazita M, Cheung V et al (2012) Altered patterns of multiple recombinant events are associated with nondisjunction of chromosome 21. Hum Genet 131:1039–1046

    Article  CAS  PubMed  Google Scholar 

  • Osman F, Dixon J, Doe CL, Whitby MC (2003) Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol Cell 12:761–774

    Article  CAS  PubMed  Google Scholar 

  • Ottolini CS, Newnham LJ, Capalbo A, Natesan SA, Joshi HA, Cimadomo D, Griffin DK, Sage K, Summers MC, Thornhill AR et al (2015) Genome-wide maps of recombination and chromosome segregation in human oocytes and embryos show selection for maternal recombination rates. Nature 47:727–735

    CAS  Google Scholar 

  • Pacchierotti F, Adler ID, Eichenlaub-Ritter U, Mailhes JB (2007) Gender effects on the incidence of aneuploidy in mammalian germ cells. Environ Res 104:46–69

    Article  CAS  PubMed  Google Scholar 

  • Page SL, Hawley RS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15:3130–3143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20:525–558

    Article  CAS  PubMed  Google Scholar 

  • Parvanov ED, Petkov PM, Paigen K (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327:835

    Article  CAS  PubMed  Google Scholar 

  • Parvinen M, Söderström KO (1976) Chromosome rotation and formation of synapsis. Nature 260:534–535

    Article  CAS  PubMed  Google Scholar 

  • Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15:1349–1360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paull TT, Gellert M (1998) The 3″ to 5″ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol Cell 1:969–979

    Article  CAS  PubMed  Google Scholar 

  • Pellestor F, Andréo B, Arnal F, Humeau C, Demaille J (2003) Maternal aging and chromosomal abnormalities: new data drawn from in vitro unfertilized human oocytes. Hum Genet 112:195–203

    PubMed  Google Scholar 

  • Penedos A, Johnson AL, Strong E, Goldman AS, Carballo JA, Cha RS (2015) Essential and checkpoint functions of budding yeast ATM and ATR during meiotic prophase are facilitated by differential phosphorylation of a meiotic adaptor protein, Hop1. PLoS One 10:e0134297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T, Woglar A, Csaszar E, Pasierbek P, Ammerer G, Gruenbaum Y et al (2009) Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139:920–933

    Article  CAS  PubMed  Google Scholar 

  • Penrose LS (2009) The relative effects of paternal and maternal age in mongolism. 1933. J Genet 88:9–14

    Google Scholar 

  • Perry J, Kleckner N, Börner GV (2005) Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci USA 102:17594–17599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pezzi N, Prieto I, Kremer L, Pérez Jurado LA, Valero C, Del Mazo J, Martínez-A C, Barbero JL (2000) STAG3, a novel gene encoding a protein involved in meiotic chromosome pairing and location of STAG3-related genes flanking the Williams-Beuren syndrome deletion. FASEB J 14:581–592

    CAS  PubMed  Google Scholar 

  • Phillips CM, Dernburg AF (2006) A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell 11:817–829

    Article  CAS  PubMed  Google Scholar 

  • Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, Meneely PM, Dernburg AF (2005) HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123:1051–1063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips CM, Meng X, Zhang L, Chretien JH, Urnov FD, Dernburg AF (2009) Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat Cell Biol 11:934–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polani PE, Crolla JA (1991) A test of the production line hypothesis of mammalian oogenesis. Hum Genet 88:64–70

    Article  CAS  PubMed  Google Scholar 

  • Ponting CP (2011) What are the genomic drivers of the rapid evolution of PRDM9? Trends Genet 27:165–171

    Article  CAS  PubMed  Google Scholar 

  • Pradillo M, Knoll A, Oliver C, Varas J, Corredor E, Puchta H, Santos JL (2015) Involvement of the cohesin cofactor PDS5 (SPO76) during meiosis and DNA repair in Arabidopsis thaliana. Front Plant Sci 6:1034

    Article  PubMed  PubMed Central  Google Scholar 

  • Prieto I, Pezzi N, Buesa JM, Kremer L, Barthelemy I, Carreiro C, Roncal F, Martinez A, Gomez L, Fernandez R et al (2002) STAG2 and Rad21 mammalian mitotic cohesins are implicated in meiosis. EMBO Rep 3:543–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prinz S, Amon A, Klein F (1997) Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics 146:781–795

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi Z, Redding S, Lee JY, Gibb B, Kwon Y, Niu H, Gaines WA, Sung P, Greene EC (2015) DNA sequence alignment by microhomology sampling during homologous recombination. Cell 160:856–869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao H, Chen JK, Reynolds A, Hoog C, Paddy M, Hunter N (2012) Interplay between synaptonemal complex, homologous recombination, and centromeres during mammalian meiosis. PLoS Genet 8:e1002790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao H, Prasada Rao HBD, Yang Y, Fong JH, Cloutier JM, Deacon DC, Nagel KE, Swartz RK, Strong E, Holloway JK et al (2014) Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nature 46:194–199

    CAS  Google Scholar 

  • Radford SJ, Goley E, Baxter K, McMahan S, Sekelsky J (2005) Drosophila ERCC1 is required for a subset of MEI-9-dependent meiotic crossovers. Genetics 170:1737–1745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rakshambikai R, Srinivasan N, Nishant KT (2013) Structural insights into Saccharomyces cerevisiae Msh4-Msh5 complex function using homology modeling. PLoS One 8:e78753

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reddy KC, Villeneuve AM (2004) C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118:439–452

    Article  CAS  PubMed  Google Scholar 

  • Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 21:6984–6998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, Biswas K, Holloway JK, Baudat F, de Massy B, Wang J et al (2013) RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat Genet 45:269–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson WP, Kuchinka BD, Bernasconi F, Petersen MB, Schulze A, Brøndum-Nielsen K, Christian SL, Ledbetter DH, Schinzel AA, Horsthemke B et al (1998) Maternal meiosis I non-disjunction of chromosome 15: dependence of the maternal age effect on level of recombination. Hum Mol Genet 7:1011–1019

    Article  CAS  PubMed  Google Scholar 

  • Rodman TC (1971) Chromosomes of the first polar body in mammalian meiosis. Exp Cell Res 68:205–210

    Article  CAS  PubMed  Google Scholar 

  • Rog O, Dernburg AF (2015) Direct visualization reveals kinetics of meiotic chromosome synapsis. Cell Rep 10:1639–1645

    Article  CAS  Google Scholar 

  • Rolef Ben-Shahar T, Heeger S, Lehane C, East P, Flynn H, Skehel M, Uhlmann F (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321:563–566

    Article  PubMed  CAS  Google Scholar 

  • Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975–987

    Article  CAS  PubMed  Google Scholar 

  • Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL, Dernburg AF, Villeneuve AM (2013) The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLoS Genet 9:e1003674

    Google Scholar 

  • Rothenberg M, Kohli J, Ludin K (2009) Ctp1 and the MRN-complex are required for endonucleolytic Rec12 removal with release of a single class of oligonucleotides in fission yeast. PLoS Genet 5:e1000722

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rowsey R, Gruhn J, Broman KW, Hunt PA, Hassold T (2014) Examining variation in recombination levels in the human female: a test of the production-line hypothesis. Am J Hum Genet 95:108–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Royo H, Prosser H, Ruzankina Y, Mahadevaiah SK, Cloutier JM, Baumann M, Fukuda T, Hoog C, Tóth A, de Rooij DG et al (2013) ATR acts stage specifically to regulate multiple aspects of mammalian meiotic silencing. Genes Dev 27:1484–1494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito TT, Youds JL, Boulton SJ, Colaiácovo MP (2009) Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet 5:e1000735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saito TT, Mohideen F, Meyer K, Harper JW, Colaiácovo MP (2012) SLX-1 is required for maintaining genomic integrity and promoting meiotic noncrossovers in the Caenorhabditis elegans germline. PLoS Genet 8:e1002888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito TT, Lui DY, Kim H-M, Meyer K, Colaiácovo MP (2013) Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis. PLoS Genet 9:e1003586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salah SM, Nasmyth K (2000) Destruction of the securin Pds1p occurs at the onset of anaphase during both meiotic divisions in yeast. Chromosoma 109:27–34

    Article  CAS  PubMed  Google Scholar 

  • Sato K-I (2015) Transmembrane signal transduction in oocyte maturation and fertilization: focusing on Xenopus laevis as a model animal. Int J Mol Sci 16:114–134

    Article  CAS  Google Scholar 

  • Scherthan H, Weich S, Schwegler H, Heyting C, Härle M, Cremer T (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134:1109–1125

    Article  CAS  PubMed  Google Scholar 

  • Schurko AM, Logsdon JM (2008) Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex. Bioessays 30:579–589

    Article  CAS  PubMed  Google Scholar 

  • Ségurel L, Leffler EM, Przeworski M (2011) The case of the fickle fingers: how the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans. Plos Biol 9:e1001211

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sehorn MG, Sigurdsson S, Bussen W, Unger VM, Sung P (2004) Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature 429:433–437

    Article  CAS  PubMed  Google Scholar 

  • Serrentino ME, Chaplais E, Sommermeyer V, Borde V (2013) Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet 9:e1003416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Severson AF, Meyer BJ (2014) Divergent kleisin subunits of cohesin specify mechanisms to tether and release meiotic chromosomes. eLife 3:e03467

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Severson AF, Ling L, van Zuylen V, Meyer BJ (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev 23:1763–1778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharan SK, Bradley A (1997) Murine Brca2: sequence, map position, and expression pattern. Genomics 40:234–241

    Article  CAS  PubMed  Google Scholar 

  • Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E, Dinh C, Sands A, Eichele G, Hasty P, Bradley A (1997) Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386:804–810

    Article  CAS  PubMed  Google Scholar 

  • Sharan SK, Pyle A, Coppola V, Babus J, Swaminathan S, Benedict J, Swing D, Martin BK, Tessarollo L, Evans JP et al (2004) BRCA2 deficiency in mice leads to meiotic impairment and infertility. Development 131:131–142

    Article  CAS  PubMed  Google Scholar 

  • Singh DK, Andreuzza S, Panoli AP, Siddiqi I (2013) AtCTF7 is required for establishment of sister chromatid cohesion and association of cohesin with chromatin during meiosis in Arabidopsis. BMC Plant Biol 13:117

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singhal S, Leffler EM, Sannareddy K, Turner I, Venn O, Hooper DM, Strand AI, Li Q, Raney B, Balakrishnan CN et al (2015) Stable recombination hotspots in birds. Science 350:928–932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skibbens RV, Corson LB, Koshland D, Hieter P (1999) Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev 13:307–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smolikov S, Eizinger A, Hurlburt A, Rogers E, Villeneuve AM, Colaiacovo MP (2007) Synapsis-defective mutants reveal a correlation between chromosome conformation and the mode of double-strand break repair during Caenorhabditis elegans meiosis. Genetics 176:2027–2033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snowden T, Acharya S, Butz C, Berardini M, Fishel R (2004) hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15:437–451

    Article  CAS  PubMed  Google Scholar 

  • Sollier J, Lin W, Soustelle C, Suhre K, Nicolas A, Géli V, de La Roche Saint-André C (2004) Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression. EMBO J 23:1957–1967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sommermeyer V, Béneut C, Chaplais E, Serrentino ME, Borde V (2013) Spp1, a member of the Set1 complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol Cell 49:43–54

    Article  CAS  PubMed  Google Scholar 

  • Sourirajan A, Lichten M (2008) Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev 22:2627–2632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, Dernburg AF (2013) Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLoS Genet 9:e1003679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stergiou L, Doukoumetzidis K, Sendoel A, Hengartner MO (2007) The nucleotide excision repair pathway is required for UV-C-induced apoptosis in Caenorhabditis elegans. Cell Death Differ 14:1129–1138

    Article  CAS  PubMed  Google Scholar 

  • Stiff T, Walker SA, Cerosaletti K, Goodarzi AA, Petermann E, Concannon P, O’Driscoll M, Jeggo PA (2006) ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J 25:5775–5782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storlazzi A, Tesse S, Ruprich-Robert G, Gargano S, Pöggeler S, Kleckner N, Zickler D (2008) Coupling meiotic chromosome axis integrity to recombination. Genes Dev 22:796–809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama T, Kowalczykowski SC (2002) Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J Biol Chem 277:31663–31672

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Treco D, Szostak JW (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell 64:1155–1161

    Article  CAS  PubMed  Google Scholar 

  • Sun F, Fujiwara Y, Reinholdt LG, Hu J, Saxl RL, Baker CL, Petkov PM, Paigen K, Handel MA (2015) Nuclear localization of PRDM9 and its role in meiotic chromatin modifications and homologous synapsis. Chromosoma 124:397–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sung P, Robberson DL (1995) DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82:453–461

    Article  CAS  PubMed  Google Scholar 

  • Sutani T, Kawaguchi T, Kanno R, Itoh T, Shirahige K (2009) Budding yeast Wpl1(Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr Biol 19:492–497

    Article  CAS  PubMed  Google Scholar 

  • Svendsen JM, Harper JW (2010) GEN1/Yen1 and the SLX4 complex: solutions to the problem of Holliday junction resolution. Genes Dev 24:521–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378

    Article  CAS  PubMed  Google Scholar 

  • Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo NR, Adams DJ, Nasmyth K (2010) Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 24:2505–2516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeo S, Lake CM, Morais-de-Sá E, Sunkel CE, Hawley RS (2011) Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr Biol 21:1845–1851

    Article  CAS  PubMed  Google Scholar 

  • Tamaki H (1965) Chromosome behaviour at meiosis in Saccharomyces cerevisiae. J Gen Microbiol 41:93–98

    Article  CAS  PubMed  Google Scholar 

  • Tanneti NS, Landy K, Joyce EF, McKim KS (2011) A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr Biol 21:1852–1857

    Article  CAS  PubMed  Google Scholar 

  • Taylor MRG, Spirek M, Chaurasiya KR, Ward JD, Carzaniga R, Yu X, Egelman EH, Collinson LM, Rueda D, Krejci L et al (2015) Rad51 paralogs remodel pre-synaptic Rad51 filaments to stimulate homologous recombination. Cell 162:271–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terasawa M, Ogawa T, Tsukamoto Y, Ogawa H (2008) Sae2p phosphorylation is crucial for cooperation with Mre11p for resection of DNA double-strand break ends during meiotic recombination in Saccharomyces cerevisiae. Genes Genet Syst 83:209–217

    Article  CAS  PubMed  Google Scholar 

  • Thomas NS, Ennis S, Sharp AJ, Durkie M, Hassold TJ, Collins AR, Jacobs PA (2001) Maternal sex chromosome non-disjunction: evidence for X chromosome-specific risk factors. Hum Mol Genet 10:243–250

    Article  CAS  PubMed  Google Scholar 

  • Toth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A, Nasmyth K (1999) Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev 13:320–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tougan T, Kasama T, Ohtaka A, Okuzaki D, Saito TT, Russell P, Nojima H (2010) The Mek1 phosphorylation cascade plays a role in meiotic recombination of Schizosaccharomyces pombe. Cell Cycle 9:4688–4702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traut H (1980) X-chromosomal nondisjunction induced by aging oocytes of Drosophila melanogaster: the special susceptibility of mature eggs. Can J Genet Cytol 22:433–437

    Article  CAS  PubMed  Google Scholar 

  • Traut H, Schröder FJ (1978) The increase in the frequency of X-chromosomal aneuploidy in Drosophila melanogaster as a consequence of suppressed oviposition. Mutat Res 49:225–232

    Article  Google Scholar 

  • Trelles-Sticken E, Dresser ME, Scherthan H (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151:95–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, Meyer BJ (2008) Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev 22:194–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsubouchi H, Roeder GS (2003) The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev Cell 5:915–925

    Article  CAS  PubMed  Google Scholar 

  • Tsutsumi M, Fujiwara R, Nishizawa H, Ito M, Kogo H, Inagaki H, Ohye T, Kato T, Fujii T, Kurahashi H (2014) Age-related decrease of meiotic cohesins in human oocytes. PLoS One 9:e96710

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8:1095–1101

    Article  CAS  PubMed  Google Scholar 

  • Unal E, Heidinger-Pauli JM, Kim W, Guacci V, Onn I, Gygi SP, Koshland DE (2008) A molecular determinant for the establishment of sister chromatid cohesion. Science 321:566–569

    Article  PubMed  CAS  Google Scholar 

  • Urban E, Nagarkar-Jaiswal S, Lehner CF, Heidmann SK (2014) The cohesin subunit Rad21 is required for synaptonemal complex maintenance, but not sister chromatid cohesion, during Drosophila female meiosis. PLoS Genet 10:e1004540

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Usui T, Ohta T, Oshiumi H, Tomizawa J, Ogawa H, Ogawa T (1998) Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95:705–716

    Article  CAS  PubMed  Google Scholar 

  • Usui T, Ogawa H, Petrini JH (2001) A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 7:1255–1266

    Article  CAS  PubMed  Google Scholar 

  • Valencia M, Bentele M, Vaze MB, Herrmann G, Kraus E, Lee SE, Schär P, Haber JE (2001) NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae. Nature 414:666–669

    Article  CAS  PubMed  Google Scholar 

  • Vallaster M, Vallaster CD, Wu SM (2011) Epigenetic mechanisms in cardiac development and disease. Acta Biochim Biophys Sin 44:92–102

    Article  CAS  Google Scholar 

  • Vaur S, Feytout A, Vazquez S, Javerzat JP (2012) Pds5 promotes cohesin acetylation and stable cohesin-chromosome interaction. EMBO Rep 13:645–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vernì F, Gandhi R, Goldberg ML, Gatti M (2000) Genetic and molecular analysis of wings apart-like (wapl), a gene controlling heterochromatin organization in Drosophila melanogaster. Genetics 154:1693–1710

    PubMed  PubMed Central  Google Scholar 

  • Visnes T, Giordano F, Kuznetsova A, Suja JA, Lander AD, Calof AL, Ström L (2014) Localisation of the SMC loading complex Nipbl/Mau2 during mammalian meiotic prophase I. Chromosoma 123:239–252

    Article  CAS  PubMed  Google Scholar 

  • Voelkel-Meiman K, Taylor LF, Mukherjee P, Humphryes N, Tsubouchi H, MacQueen AJ (2013) SUMO localizes to the central element of synaptonemal complex and is required for the full synapsis of meiotic chromosomes in budding yeast. PLoS Genet 9:e1003837

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waizenegger IC, Hauf S, Meinke A, Peters JM (2000) Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103:399–410

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Haber JE (2004) Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. Plos Biol 2:E21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang TF, Kleckner N, Hunter N (1999) Functional specificity of MutL homologs in yeast: evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc Natl Acad Sci USA 96:13914–13919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Yoder J, Antoshechkin I, Han M (2003) Caenorhabditis elegans EVL-14/PDS-5 and SCC-3 are essential for sister chromatid cohesion in meiosis and mitosis. Mol Cell Biol 23:7698–7707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner CR, Kuervers L, Baillie DL, Yanowitz JL (2010) xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature 467(7317):839–843. PMID: 20944745

    Google Scholar 

  • Ward JO, Reinholdt LG, Motley WW, Niswander LM, Deacon DC, Griffin LB, Langlais KK, Backus VL, Schimenti KJ, O’Brien MJ et al (2007) Mutation in mouse hei10, an e3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genet 3:e139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464

    Article  CAS  PubMed  Google Scholar 

  • Woglar A, Daryabeigi A, Adamo A, Habacher C, Machacek T, La Volpe A, Jantsch V (2013) Matefin/SUN-1 phosphorylation is part of a surveillance mechanism to coordinate chromosome synapsis and recombination with meiotic progression and chromosome movement. PLoS Genet 9:e1003335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolf KW (1994) How meiotic cells deal with non-exchange chromosomes. Bioessays 16:107–114

    Article  CAS  PubMed  Google Scholar 

  • Woltering D, Baumgartner B, Bagchi S, Larkin B, Loidl J, de los Santos T, Hollingsworth NM (2000) Meiotic segregation, synapsis, and recombination checkpoint functions require physical interaction between the chromosomal proteins Red1p and Hop1p. Mol Cell Biol 20:6646–6658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Zhang X, Zhang L, Wu C-Y, Rezaeian AH, Chan C-H, Li J-M, Wang J, Gao Y, Han F et al (2012) Skp2 E3 ligase integrates ATM activation and homologous recombination repair by ubiquitinating NBS1. Mol Cell 46:351–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wyatt HDM, Sarbajna S, Matos J, West SC (2013) Coordinated actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in human cells. Mol Cell 52:234–247

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Weiner BM, Kleckner N (1997) Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev 11:106–118

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Beasley MD, Warren WD, van der Horst GTJ, McKay MJ (2005) Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 8:949–961

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto A, West RR, McIntosh JR, Hiraoka Y (1999) A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J Cell Biol 145:1233–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yildiz O, Majumder S, Kramer B, Sekelsky JJ (2002) Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol Cell 10:1503–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Smolikove S (2013) Impaired resection of meiotic double-strand breaks channels repair to nonhomologous end joining in Caenorhabditis elegans. Mol Cell Biol 33:2732–2747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Donlevy S, Smolikove S (2016) Coordination of recombination with meiotic progression in the Caenorhabditis elegans germline by KIN-18, a TAO kinase that regulates the timing of MPK-1 signaling. Genetics 202:45–59

    Article  CAS  PubMed  Google Scholar 

  • Yokobayashi S, Yamamoto M, Watanabe Y (2003) Cohesins determine the attachment manner of kinetochores to spindle microtubules at meiosis I in fission yeast. Mol Cell Biol 23:3965–3973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149:75–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zakharyevich K, Ma Y, Tang S, Hwang PY-H, Boiteux S, Hunter N (2010) Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions. Mol Cell 40:1001–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zakharyevich K, Tang S, Ma Y, Hunter N (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149:334–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zannini L, Delia D, Buscemi G (2014) CHK2 kinase in the DNA damage response and beyond. J Mol Cell Biol 6:442–457

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Ren Q, Yang H, Conrad MN, Guacci V, Kateneva A, Dresser ME (2005) Budding yeast PDS5 plays an important role in meiosis and is required for sister chromatid cohesion. Mol Microbiol 56:670–680

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Håkansson H, Kuroda M, Yuan L (2008a) Wapl localization on the synaptonemal complex, a meiosis-specific proteinaceous structure that binds homologous chromosomes, in the female mouse. Reprod Domest Anim 43:124–126

    CAS  PubMed  Google Scholar 

  • Zhang N, Kuznetsov SG, Sharan SK, Li K, Rao PH, Pati D (2008b) A handcuff model for the cohesin complex. J Cell Biol 183:1019–1031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Kim KP, Kleckner NE, Storlazzi A (2011) Meiotic double-strand breaks occur once per pair of (sister) chromatids, and via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. Proc Natl Acad Sci USA 108:20036–20041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Espagne E, De Muyt A, Zickler D, Kleckner NE (2014) Interference-mediated synaptonemal complex formation with embedded crossover designation. Proc Natl Acad Sci USA 111:E5059–E5068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Z, Chung W-H, Shim EY, Lee SE, Ira G (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981–994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Sarit Smolikove .

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Reichman, R., Alleva, B., Smolikove, S. (2017). Prophase I: Preparing Chromosomes for Segregation in the Develo** Oocyte. In: Arur, S. (eds) Signaling-Mediated Control of Cell Division . Results and Problems in Cell Differentiation, vol 59. Springer, Cham. https://doi.org/10.1007/978-3-319-44820-6_5

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