Chromosome Synapsis Alleviates Mek1-Dependent Suppression of Meiotic DNA Repair

PLoS Biology

Volumn 14, Issue 2, 2016, Pages

  Subramanian, Vijayalakshmi V ^a   MacQueen, Amy J ^b   Vader, Gerben ^a,e   Shinohara, Miki ^c   Sanchez, Aurore ^d   Borde, Valérie ^d   Shinohara, Akira ^c   Hochwagen, Andreas ^a  

^a NEW YORK UNIVERSITY   (United States)

^b WESLEYAN UNIVERSITY   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d CNRS   (France)

^e MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; EPITOPE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PCH2 PROTEIN; RAD54 PROTEIN; UNCLASSIFIED DRUG; DNA HELICASE; DNA LIGASE; NUCLEAR PROTEIN; PCH2 PROTEIN, S CEREVISIAE; RAD54 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; ZIP1 PROTEIN, S CEREVISIAE;

ARTICLE; CHROMOSOME ANALYSIS; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA REPAIR; DNA TEMPLATE; ENZYME ACTIVITY; ENZYME ASSAY; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN TARGETING; STRUCTURE ANALYSIS; DOUBLE STRANDED DNA BREAK; GENETICS; MEIOSIS; METABOLISM; SACCHAROMYCES CEREVISIAE;

CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPAIR; DNA REPAIR ENZYMES; MAP KINASE KINASE 1; MEIOSIS; NUCLEAR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84959560202     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002369     Document Type: Article

References (76)

1. Nagaoka SI, Hassold TJ, Hunt PA, (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet13: 493–504. doi: 10.1038/nrg324522705668
2. Zickler D, Kleckner N, (2015) Recombination, Pairing, and Synapsis of Homologs during Meiosis. Cold Spring Harb Perspect Biol7: a016626. doi: 10.1101/cshperspect.a01662625986558
3. Hollingsworth NM, (2010) Phosphorylation and the creation of interhomolog bias during meiosis in yeast. Cell Cycle9: 436–437. 20090416
4. Humphryes N, Hochwagen A, (2014) A non-sister act: Recombination template choice during meiosis. Exp Cell Res329: 53–60. doi: 10.1016/j.yexcr.2014.08.02425158281
5. Niu H, Wan L, Baumgartner B, Schaefer D, Loidl J, et al. (2005) Partner Choice during Meiosis Is Regulated by Hop1-promoted Dimerization of Mek1. Mol Biol Cell16: 5804–5818. 16221890
6. Carballo JA, Johnson AL, Sedgwick SG, Cha RS, (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell132: 758–770. doi: 10.1016/j.cell.2008.01.03518329363
7. Niu H, Li X, Job E, Park C, Moazed D, et al. (2007) Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis. Mol Cell Biol27: 5456–5467. 17526735
8. Niu H, Wan L, Busygina V, Kwon Y, Allen JA, et al. (2009) Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol Cell36: 393–404. doi: 10.1016/j.molcel.2009.09.02919917248
9. Govin J, Dorsey J, Gaucher J, Rousseaux S, Khochbin S, et al. (2010) Systematic screen reveals new functional dynamics of histones H3 and H4 during gametogenesis. Genes Dev24: 1772–1786. doi: 10.1101/gad.195491020713519
10. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, et al. (2013) Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet9: e1003978. doi: 10.1371/journal.pgen.100397824367271
11. Tsubouchi H, Roeder GS, (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev20: 1766–1775. 16818607
12. Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, et al. (2008) Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev22: 786–795. doi: 10.1101/gad.163870818347097
13. Goldfarb T, Lichten M, (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol8: e1000520. doi: 10.1371/journal.pbio.100052020976044
14. Hong S, Sung Y, Yu M, Lee M, Kleckner N, et al. (2013) The logic and mechanism of homologous recombination partner choice. Mol Cell51: 440–453. doi: 10.1016/j.molcel.2013.08.00823973374
15. Lao JP, Hunter N, (2010) Trying to avoid your sister. PLoS Biol8: e1000519. doi: 10.1371/journal.pbio.100051920976046
16. Wu HY, Ho HC, Burgess SM, (2010) Mek1 kinase governs outcomes of meiotic recombination and the checkpoint response. Curr Biol20: 1707–1716. doi: 10.1016/j.cub.2010.09.01620888230
17. Page SL, Hawley RS, (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol20: 525–558. 15473851
18. Agarwal S, Roeder GS, (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell102: 245–255. 10943844
19. Henderson KA, Keeney S, (2004) Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc Natl Acad Sci U S A101: 4519–4524. 15070750
20. Tsubouchi T, Macqueen AJ, Roeder GS, (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev22: 3217–3226. doi: 10.1101/gad.170940819056898
21. Tung KS, Roeder GS, (1998) Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics149: 817–832. 9611194
22. Sym M, Engebrecht JA, Roeder GS, (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell72: 365–378. 7916652
23. Joshi N, Barot A, Jamison C, Borner GV, (2009) Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet5: e1000557. doi: 10.1371/journal.pgen.100055719629172
24. Chen C, Jomaa A, Ortega J, Alani EE, (2014) Pch2 is a hexameric ring ATPase that remodels the chromosome axis protein Hop1. Proc Natl Acad Sci U S A111: E44–53. doi: 10.1073/pnas.131075511124367111
25. Smith AV, Roeder GS, (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol136: 957–967. 9060462
26. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, et al. (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet5: e1000702. doi: 10.1371/journal.pgen.100070219851446
27. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, et al. (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell146: 372–383. doi: 10.1016/j.cell.2011.07.00321816273
28. Carballo JA, Panizza S, Serrentino ME, Johnson AL, Geymonat M, et al. (2013) Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery. PLoS Genet9: e1003545. doi: 10.1371/journal.pgen.100354523825959
29. Maleki S, Neale MJ, Arora C, Henderson KA, Keeney S, (2007) Interactions between Mei4, Rec114, and other proteins required for meiotic DNA double-strand break formation in Saccharomyces cerevisiae. Chromosoma116: 471–486. 17558514
30. Thacker D, Mohibullah N, Zhu X, Keeney S, (2014) Homologue engagement controls meiotic DNA break number and distribution. Nature510: 241–246. doi: 10.1038/nature1312024717437
31. Allers T, Lichten M, (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell106: 47–57. 11461701
32. Xu L, Ajimura M, Padmore R, Klein C, Kleckner N, (1995) NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol Cell Biol15: 6572–6581. 8524222
33. Bailis JM, Roeder GS, (1998) Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev12: 3551–3563. 9832507
34. Cartagena-Lirola H, Guerini I, Manfrini N, Lucchini G, Longhese MP, (2008) Role of the Saccharomyces cerevisiae Rad53 checkpoint kinase in signaling double-strand breaks during the meiotic cell cycle. Mol Cell Biol28: 4480–4493. doi: 10.1128/MCB.00375-0818505828
35. Falk JE, Chan AC, Hoffmann E, Hochwagen A, (2010) A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell19: 599–611. doi: 10.1016/j.devcel.2010.09.00620951350
36. 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 Cycle5: 1549–1559. 16861895
37. Haruki H, Nishikawa J, Laemmli UK, (2008) The anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol Cell31: 925–932. doi: 10.1016/j.molcel.2008.07.02018922474
38. Subramanian VV, Hochwagen A, (2014) The meiotic checkpoint network: step-by-step through meiotic prophase. Cold Spring Harb Perspect Biol6: a016675. doi: 10.1101/cshperspect.a01667525274702
39. Tung KS, Hong EJ, Roeder GS, (2000) The pachytene checkpoint prevents accumulation and phosphorylation of the meiosis-specific transcription factor Ndt80. Proc Natl Acad Sci U S A97: 12187–12192. 11035815
40. Cheng YH, Chuang CN, Shen HJ, Lin FM, Wang TF, (2013) Three distinct modes of Mec1/ATR and Tel1/ATM activation illustrate differential checkpoint targeting during budding yeast early meiosis. Mol Cell Biol33: 3365–3376. doi: 10.1128/MCB.00438-1323775120
41. Borner GV, Kleckner N, Hunter N, (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell117: 29–45. 15066280
42. Lynn A, Soucek R, Borner GV, (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res15: 591–605. 17674148
43. San-Segundo PA, Roeder GS, (1999) Pch2 links chromatin silencing to meiotic checkpoint control. Cell97: 313–324. 10319812
44. Borner GV, Barot A, Kleckner N, (2008) Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A105: 3327–3332. doi: 10.1073/pnas.071186410518305165
45. Mitra N, Roeder GS, (2007) A novel nonnull ZIP1 allele triggers meiotic arrest with synapsed chromosomes in Saccharomyces cerevisiae. Genetics176: 773–787. 17435220
46. Chuang CN, Cheng YH, Wang TF, (2012) Mek1 stabilizes Hop1-Thr318 phosphorylation to promote interhomolog recombination and checkpoint responses during yeast meiosis. Nucleic Acids Res40: 11416–11427. doi: 10.1093/nar/gks92023047948
47. Refolio E, Cavero S, Marcon E, Freire R, San-Segundo PA, (2011) The Ddc2/ATRIP checkpoint protein monitors meiotic recombination intermediates. J Cell Sci124: 2488–2500. doi: 10.1242/jcs.08171121693576
48. Padmore R, Cao L, Kleckner N, (1991) Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell66: 1239–1256. 1913808
49. Bishop DK, (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell79: 1081–1092. 7528104
50. Vader G, Blitzblau HG, Tame MA, Falk JE, Curtin L, et al. (2011) Protection of repetitive DNA borders from self-induced meiotic instability. Nature477: 115–119. doi: 10.1038/nature1033121822291
51. Nimonkar AV, Dombrowski CC, Siino JS, Stasiak AZ, Stasiak A, et al. (2012) Saccharomyces cerevisiae Dmc1 and Rad51 proteins preferentially function with Tid1 and Rad54 proteins, respectively, to promote DNA strand invasion during genetic recombination. J Biol Chem287: 28727–28737. doi: 10.1074/jbc.M112.37329022761450
52. Shinohara M, Sakai K, Shinohara A, Bishop DK, (2003) Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. Genetics163: 1273–1286. 12702674
53. Shah PP, Zheng X, Epshtein A, Carey JN, Bishop DK, et al. (2010) Swi2/Snf2-related translocases prevent accumulation of toxic Rad51 complexes during mitotic growth. Mol Cell39: 862–872. doi: 10.1016/j.molcel.2010.08.02820864034
54. 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. Cell69: 439–456. 1581960
55. Hunter N, Kleckner N, (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell106: 59–70. 11461702
56. Zakharyevich K, Ma Y, Tang S, Hwang PY, Boiteux S, et al. (2010) Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions. Mol Cell40: 1001–1015. doi: 10.1016/j.molcel.2010.11.03221172664
57. Bzymek M, Thayer NH, Oh SD, Kleckner N, Hunter N, (2010) Double Holliday junctions are intermediates of DNA break repair. Nature464: 937–941. doi: 10.1038/nature0886820348905
58. Callender TL, Hollingsworth NM, (2010) Mek1 suppression of meiotic double-strand break repair is specific to sister chromatids, chromosome autonomous and independent of Rec8 cohesin complexes. Genetics185: 771–782. doi: 10.1534/genetics.110.11752320421598
59. Hochwagen A, Tham WH, Brar GA, Amon A, (2005) The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell122: 861–873. 16179256
60. Wan L, de los Santos T, Zhang C, Shokat K, Hollingsworth NM, (2004) Mek1 kinase activity functions downstream of RED1 in the regulation of meiotic double strand break repair in budding yeast. Mol Biol Cell15: 11–23. 14595109
61. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell143: 924–937. doi: 10.1016/j.cell.2010.11.01521145459
62. Solinger JA, Kiianitsa K, Heyer WD, (2002) Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol Cell10: 1175–1188. 12453424
63. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet33: 603–754. 10690419
64. Tsubouchi T, Roeder GS, (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science308: 870–873. 15879219
65. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, et al. (2008) Global Analysis of the Meiotic Crossover Landscape. Dev Cell15: 401–415. doi: 10.1016/j.devcel.2008.07.00618691940
66. Henderson KA, Keeney S, (2005) Synaptonemal complex formation: where does it start?Bioessays27: 995–998. 16163735
67. Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, et al. (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev27: 873–886. doi: 10.1101/gad.213652.11323599345
68. Fukuda T, Pratto F, Schimenti JC, Turner JM, Camerini-Otero RD, et al. (2012) Phosphorylation of chromosome core components may serve as axis marks for the status of chromosomal events during mammalian meiosis. PLoS Genet8: e1002485. doi: 10.1371/journal.pgen.100248522346761
69. Pacheco S, Marcet-Ortega M, Lange J, Jasin M, Keeney S, et al. (2015) The ATM signaling cascade promotes recombination-dependent pachytene arrest in mouse spermatocytes. PLoS Genet11: e1005017. doi: 10.1371/journal.pgen.100501725768017
70. Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM, (2013) Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature502:703–706. doi: 10.1038/nature1257724107990
71. Rosu S, Libuda DE, Villeneuve AM, (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science334: 1286–1289. doi: 10.1126/science.121242422144627
72. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, et al. (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell94: 387–398. 9708740
73. Bishop DK, Zickler D, (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell117: 9–15. 15066278
74. White EJ, Cowan C, Cande WZ, Kaback DB, (2004) In vivo analysis of synaptonemal complex formation during yeast meiosis. Genetics167: 51–63. 15166136
75. Murakami H, Nicolas A, (2009) Locally, meiotic double-strand breaks targeted by Gal4BD-Spo11 occur at discrete sites with a sequence preference. Mol Cell Biol29: 3500–3516. doi: 10.1128/MCB.00088-0919380488
76. Schwacha A, Kleckner N, (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell76: 51–63. 8287479