全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Dot1-Dependent Histone H3K79 Methylation Promotes the Formation of Meiotic Double-Strand Breaks in the Absence of Histone H3K4 Methylation in Budding Yeast

DOI: 10.1371/journal.pone.0096648

Full-Text   Cite this paper   Add to My Lib

Abstract:

Epigenetic marks such as histone modifications play roles in various chromosome dynamics in mitosis and meiosis. Methylation of histones H3 at positions K4 and K79 is involved in the initiation of recombination and the recombination checkpoint, respectively, during meiosis in the budding yeast. Set1 promotes H3K4 methylation while Dot1 promotes H3K79 methylation. In this study, we carried out detailed analyses of meiosis in mutants of the SET1 and DOT1 genes as well as methylation-defective mutants of histone H3. We confirmed the role of Set1-dependent H3K4 methylation in the formation of double-strand breaks (DSBs) in meiosis for the initiation of meiotic recombination, and we showed the involvement of Dot1 (H3K79 methylation) in DSB formation in the absence of Set1-dependent H3K4 methylation. In addition, we showed that the histone H3K4 methylation-defective mutants are defective in SC elongation, although they seem to have moderate reduction of DSBs. This suggests that high levels of DSBs mediated by histone H3K4 methylation promote SC elongation.

References

[1]  Petronczki M, Siomos MF, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112: 423–440. doi: 10.1016/s0092-8674(03)00083-7
[2]  Kleckner N (2006) Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115: 175–194. doi: 10.1007/s00412-006-0055-7
[3]  Borde V, de Massy B (2013) Programmed induction of DNA double strand breaks during meiosis: setting up communication between DNA and the chromosome structure. Curr Opin Genet Dev 23: 147–155. doi: 10.1016/j.gde.2012.12.002
[4]  Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52: 1–53. doi: 10.1016/s0070-2153(01)52008-6
[5]  Lichten M, de Massy B (2011) The impressionistic landscape of meiotic recombination. Cell 147: 267–270. doi: 10.1016/j.cell.2011.09.038
[6]  Yamada T, Ohta K (2013) Initiation of meiotic recombination in chromatin structure. J Biochem.
[7]  Borde V, Robine N, Lin W, Bonfils S, Geli V, et al. (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28: 99–111. doi: 10.1038/emboj.2008.257
[8]  Buard J, Barthes P, Grey C, de Massy B (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 28: 2616–2624. doi: 10.1038/emboj.2009.207
[9]  Yamada S, Ohta K, Yamada T (2013) Acetylated Histone H3K9 is associated with meiotic recombination hotspots, and plays a role in recombination redundantly with other factors including the H3K4 methylase Set1 in fission yeast. Nucleic Acids Res 41: 3504–3517. doi: 10.1093/nar/gkt049
[10]  Sollier J, Lin W, Soustelle C, Suhre K, Nicolas A, et al. (2004) Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression. EMBO J 23: 1957–1967. doi: 10.1038/sj.emboj.7600204
[11]  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. doi: 10.1038/nature11089
[12]  Sommermeyer V, Beneut 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. doi: 10.1016/j.molcel.2012.11.008
[13]  Acquaviva L, Szekvolgyi L, Dichtl B, Dichtl BS, de La Roche Saint Andre C, et al. (2013) The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science 339: 215–218. doi: 10.1126/science.1225739
[14]  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. Cell 106: 59–70. doi: 10.1016/s0092-8674(01)00430-5
[15]  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. doi: 10.1016/0092-8674(92)90446-j
[16]  Cloud V, Chan YL, Grubb J, Budke B, Bishop DK (2012) Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337: 1222–1225. doi: 10.1126/science.1219379
[17]  Shinohara A, Ogawa H, Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69: 457–470. doi: 10.1016/0092-8674(92)90447-k
[18]  Schwacha A, Kleckner N (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51–63. doi: 10.1016/0092-8674(94)90172-4
[19]  Allers T, Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47–57. doi: 10.1016/s0092-8674(01)00416-0
[20]  Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603–754. doi: 10.1146/annurev.genet.33.1.603
[21]  Borner 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. doi: 10.1016/s0092-8674(04)00292-2
[22]  Hochwagen A, Amon A (2006) Checking your breaks: surveillance mechanisms of meiotic recombination. Curr Biol 16: R217–228. doi: 10.1016/j.cub.2006.03.009
[23]  Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365–378. doi: 10.1016/0092-8674(93)90114-6
[24]  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 Biol 15: 6572–6581.
[25]  Chu S, Herskowitz I (1998) Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol Cell 1: 685–696. doi: 10.1016/s1097-2765(00)80068-4
[26]  Clyne RK, Katis VL, Jessop L, Benjamin KR, Herskowitz I, et al. (2003) Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 5: 480–485. doi: 10.1038/ncb977
[27]  Sourirajan A, Lichten M (2008) Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev 22: 2627–2632. doi: 10.1101/gad.1711408
[28]  San-Segundo PA, Roeder GS (1999) Pch2 links chromatin silencing to meiotic checkpoint control. Cell 97: 313–324. doi: 10.1016/s0092-8674(00)80741-2
[29]  San-Segundo PA, Roeder GS (2000) Role for the silencing protein Dot1 in meiotic checkpoint control. Mol Biol Cell 11: 3601–3615. doi: 10.1091/mbc.11.10.3601
[30]  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 A 105: 3327–3332. doi: 10.1073/pnas.0711864105
[31]  Ho HC, Burgess SM (2011) Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet 7: e1002351. doi: 10.1371/journal.pgen.1002351
[32]  Conde F, Ontoso D, Acosta I, Gallego-Sanchez A, Bueno A, et al. (2010) Regulation of tolerance to DNA alkylating damage by Dot1 and Rad53 in Saccharomyces cerevisiae. DNA Repair (Amst) 9: 1038–1049. doi: 10.1016/j.dnarep.2010.07.003
[33]  Conde F, Refolio E, Cordon-Preciado V, Cortes-Ledesma F, Aragon L, et al. (2009) The Dot1 histone methyltransferase and the Rad9 checkpoint adaptor contribute to cohesin-dependent double-strand break repair by sister chromatid recombination in Saccharomyces cerevisiae. Genetics 182: 437–446. doi: 10.1534/genetics.109.101899
[34]  Conde F, San-Segundo PA (2008) Role of Dot1 in the response to alkylating DNA damage in Saccharomyces cerevisiae: regulation of DNA damage tolerance by the error-prone polymerases Polzeta/Rev1. Genetics 179: 1197–1210. doi: 10.1534/genetics.108.089003
[35]  Levesque N, Leung GP, Fok AK, Schmidt TI, Kobor MS (2010) Loss of H3 K79 trimethylation leads to suppression of Rtt107-dependent DNA damage sensitivity through the translesion synthesis pathway. J Biol Chem 285: 35113–35122. doi: 10.1074/jbc.m110.116855
[36]  Tatum D, Li S (2011) Evidence that the histone methyltransferase Dot1 mediates global genomic repair by methylating histone H3 on lysine 79. J Biol Chem 286: 17530–17535. doi: 10.1074/jbc.m111.241570
[37]  Nguyen AT, Zhang Y (2011) The diverse functions of Dot1 and H3K79 methylation. Genes Dev 25: 1345–1358. doi: 10.1101/gad.2057811
[38]  Shilatifard A (2012) The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem 81: 65–95. doi: 10.1146/annurev-biochem-051710-134100
[39]  Yamashita K, Shinohara M, Shinohara A (2004) Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis. Proc Natl Acad Sci U S A 101: 11380–11385. doi: 10.1073/pnas.0400078101
[40]  Shinohara M, Gasior SL, Bishop DK, Shinohara A (2000) Tid1/Rdh54 promotes colocalization of Rad51 and Dmc1 during meiotic recombination. Proc Natl Acad Sci U S A 97: 10814–10819. doi: 10.1073/pnas.97.20.10814
[41]  Farmer S, Leung WK, Tsubouchi H (2011) Characterization of meiotic recombination initiation sites using pulsed-field gel electrophoresis. Methods Mol Biol 745: 33–45. doi: 10.1007/978-1-61779-129-1_3
[42]  Shinohara M, Sakai K, Ogawa T, Shinohara A (2003) The mitotic DNA damage checkpoint proteins Rad17 and Rad24 are required for repair of double-strand breaks during meiosis in yeast. Genetics 164: 855–865.
[43]  Storlazzi A, Xu L, Cao L, Kleckner N (1995) Crossover and noncrossover recombination during meiosis: timing and pathway relationships. Proc Natl Acad Sci U S A 92: 8512–8516. doi: 10.1073/pnas.92.18.8512
[44]  Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61: 1089–1101. doi: 10.1016/0092-8674(90)90072-m
[45]  Schwacha A, Kleckner N (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123–1135. doi: 10.1016/s0092-8674(00)80378-5
[46]  Shinohara A, Gasior S, Ogawa T, Kleckner N, Bishop DK (1997) Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2: 615–629. doi: 10.1046/j.1365-2443.1997.1480347.x
[47]  Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79: 1081–1092. doi: 10.1016/0092-8674(94)90038-8
[48]  Miyazaki T, Bressan DA, Shinohara M, Haber JE, Shinohara A (2004) In vivo assembly and disassembly of Rad51 and Rad52 complexes during double-strand break repair. Embo J 23: 939–949. doi: 10.1038/sj.emboj.7600091
[49]  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 Genet 9: e1003545. doi: 10.1371/journal.pgen.1003545
[50]  Argunhan B, Farmer S, Leung WK, Terentyev Y, Humphryes N, et al. (2013) Direct and indirect control of the initiation of meiotic recombination by DNA damage checkpoint mechanisms in budding yeast. PLoS One 8: e65875. doi: 10.1371/journal.pone.0065875
[51]  Trelles-Sticken E, Bonfils S, Sollier J, Geli V, Scherthan H, et al. (2005) Set1- and Clb5-deficiencies disclose the differential regulation of centromere and telomere dynamics in Saccharomyces cerevisiae meiosis. J Cell Sci 118: 4985–4994. doi: 10.1242/jcs.02612
[52]  Hollingsworth NM, Goetsch L, Byers B (1990) The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61: 73–84. doi: 10.1016/0092-8674(90)90216-2
[53]  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 Genet 5: e1000702. doi: 10.1371/journal.pgen.1000702
[54]  Armstrong SJ, Caryl AP, Jones GH, Franklin FC (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: 3645–3655. doi: 10.1242/jcs.00048
[55]  Rockmill B, Roeder GS (1988) RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis. Proc Natl Acad Sci U S A 85: 6057–6061. doi: 10.1073/pnas.85.16.6057
[56]  Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, et al. (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98: 91–103. doi: 10.1016/s0092-8674(00)80609-1
[57]  Hollingsworth NM, Ponte L (1997) Genetic interactions between HOP1, RED1 and MEK1 suggest that MEK1 regulates assembly of axial element components during meiosis in the yeast Saccharomyces cerevisiae. Genetics 147: 33–42. doi: 10.1007/springerreference_17039
[58]  Leem SH, Ogawa H (1992) The MRE4 gene encodes a novel protein kinase homologue required for meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res 20: 449–457. doi: 10.1093/nar/20.3.449
[59]  Smith AV, Roeder GS (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136: 957–967. doi: 10.1083/jcb.136.5.957
[60]  Choi K, Zhao X, Kelly KA, Venn O, Higgins JD, et al. (2013) Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat Genet 45: 1327–1336. doi: 10.1038/ng.2766
[61]  Grenon M, Costelloe T, Jimeno S, O'Shaughnessy A, Fitzgerald J, et al. (2007) Docking onto chromatin via the Saccharomyces cerevisiae Rad9 Tudor domain. Yeast 24: 105–119.
[62]  Lydall D, Nikolsky Y, Bishop DK, Weinert T (1996) A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383: 840–843. doi: 10.1038/383840a0
[63]  Ontoso D, Acosta I, van Leeuwen F, Freire R, San-Segundo PA (2013) Dot1-dependent histone H3K79 methylation promotes activation of the Mek1 meiotic checkpoint effector kinase by regulating the Hop1 adaptor. PLoS Genet 9: e1003262. doi: 10.1371/journal.pgen.1003262
[64]  Gray S, Allison RM, Garcia V, Goldman AS, Neale MJ (2013) Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR). Open Biol 3: 130019. doi: 10.1098/rsob.130019
[65]  Zhang L, Ma H, Pugh BF (2011) Stable and dynamic nucleosome states during a meiotic developmental process. Genome Res 21: 875–884. doi: 10.1101/gr.117465.110
[66]  Stahl FW, Foss HM, Young LS, Borts RH, Abdullah MF, et al. (2004) Does crossover interference count in Saccharomyces cerevisiae? Genetics 168: 35–48.
[67]  Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM (1999) Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153: 1271–1283.
[68]  Martini E, Diaz RL, Hunter N, Keeney S (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285–295. doi: 10.1016/j.cell.2006.05.044

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133