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Chromatin Structure and ATRX Function in Mouse Oocytes

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Mouse Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 55))

Abstract

Differentiation of chromatin structure and function during oogenesis is essential to confer the mammalian oocyte with meiotic and developmental potential. Errors in chromosome segregation during female meiosis and subsequent transmission of an abnormal chromosome complement (aneuploidy) to the early conceptus are one of the leading causes of pregnancy loss in women. The chromatin remodeling protein ATRX (α-thalassemia mental retardation X-linked) has recently emerged as a critical factor involved in heterochromatin formation at mammalian centromeres during meiosis. In mammalian oocytes, ATRX binds to centromeric heterochromatin domains where it is required for accurate chromosome segregation. Loss of ATRX function induces abnormal meiotic chromosome morphology, reduces histone H3 phosphorylation, and promotes a high incidence of aneuploidy associated with severely reduced fertility. The presence of centromeric breaks during the transition to the first mitosis in the early embryo indicates that the role of ATRX in chromosome segregation is mediated through an epigenetic mechanism involving the maintenance of chromatin modifications associated with pericentric heterochromatin (PCH) formation and chromosome condensation. This is consistent with the existence of a potential molecular link between centromeric and PCH in the epigenetic control of centromere function and maintenance of chromosome stability in mammalian oocytes. Dissecting the molecular mechanisms of ATRX function during meiosis will have important clinical implications towards uncovering the epigenetic factors contributing to the onset of aneuploidy in the human oocyte.

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References

  • Aapola U, Shibuya K, Scott HS, Ollila J, Vihinen M, Heino M, Shintani A, Kawasaki K, Minoshima S, Krohn K, Antonarakis SE, Shimizu N, Kudoh J, Peterson P (2000) Isolation and initial characterization of a novel zinc finger gene, DNMT3L, on 21q22.3, related to the cytosine-5-methyltransferase 3 gene family. Genomics 65:293–298

    PubMed  CAS  Google Scholar 

  • Abe K, Inoue A, Suzuki MG, Aoki F (2010) Global gene silencing is caused by the dissociation of RNA polymerase II from DNA in mouse oocytes. J Reprod Dev 56:502–507

    PubMed  CAS  Google Scholar 

  • Adams PD (2007) Remodeling of chromatin structure in senescent cells and its potential impact on tumor suppression and aging. Gene 397:84–93

    PubMed  CAS  Google Scholar 

  • Akiyama T, Nagata M, Aoki F (2006) Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc Natl Acad Sci USA 103:7339–7344

    PubMed  CAS  Google Scholar 

  • Andreu-Vieyra CV, Chen R, Agno JE, Glaser S, Anastassiadis K, Stewart AF, Matzuk MM (2010) MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol 8:e1000453

    PubMed  Google Scholar 

  • Argentaro A, Yang J, Chapman L, Kowalczyk M, Gibbons R, Higgs D, Neuhaus D, Rhodes D (2007) Structural consequences of disease-causing mutations in the ATRX-DNMT3-DNMT3L (ADD) domain of the chromatin-associated protein ATRX. Proc Natl Acad Sci USA 104:11939–11944

    PubMed  CAS  Google Scholar 

  • Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120–124

    PubMed  CAS  Google Scholar 

  • Bassett AR, Cooper SE, Ragab A, Travers AA (2008) The chromatin remodelling factor dATRX is involved in heterochromatin formation. PLoS One 3:e2099

    PubMed  Google Scholar 

  • Baumann C, De La Fuente R (2009) ATRX marks the inactive X chromosome (Xi) in somatic cells and during imprinted X chromosome inactivation in trophoblast stem cells. Chromosoma 118:209–222

    PubMed  Google Scholar 

  • Baumann C, Schmidtmann A, Muegge K, De La Fuente R (2008) Association of ATRX with pericentric heterochromatin and the Y chromosome of neonatal mouse spermatogonia. BMC Mol Biol 9:29

    PubMed  Google Scholar 

  • Baumann C, Viveiros MM, De La Fuente R (2010) Loss of maternal ATRX results in centromere instability and aneuploidy in the mammalian oocyte and pre-implantation embryo. PLoS Genet 6:e1001137

    PubMed  Google Scholar 

  • Bernard P, Allshire R (2002) Centromeres become unstuck without heterochromatin. Trends Cell Biol 12:419–424

    PubMed  CAS  Google Scholar 

  • Bernard P, Maure J, Partridge J, Genier S, Javerzat J, Allshire R (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542

    PubMed  CAS  Google Scholar 

  • Bérubé NG (2011) ATRX in chromatin assembly and genome architecture during development and disease. Biochem Cell Biol 89:435–444

    PubMed  Google Scholar 

  • Bérubé N, Smeenk C, Picketts D (2000) Cell cycle-dependent phosphorylation of the ATRX protein correlates with changes in nuclear matrix and chromatin association. Hum Mol Genet 9:539–547

    PubMed  Google Scholar 

  • Bérubé NG, Jagla M, Smeenk CA, De Repentigny Y, Kothary R, Picketts DJ (2002) Neurodevelopmental defects resulting from ATRX overexpression in transgenic mice. Hum Mol Genet 11:253–261

    PubMed  Google Scholar 

  • Bérubé NG, Healy J, Medina CF, Wu S, Hodgson T, Jagla M, Picketts DJ (2007) Patient mutations alter ATRX targeting to PML nuclear bodies. Eur J Hum Genet 16:192–201

    PubMed  Google Scholar 

  • Black BE, Brock MA, Bedard S, Woods VL, Cleveland DW (2007) An epigenetic mark generated by the incorporation of CENP-A into centromeric nucleosomes. Proc Natl Acad Sci USA 104:5008–5013

    PubMed  CAS  Google Scholar 

  • Black BE, Jansen LET, Foltz DR, Cleveland DW (2010) Centromere identity, function, and epigenetic propagation across cell divisions. Cold Spring Harb Symp Quant Biol 75:403–418

    PubMed  CAS  Google Scholar 

  • Cardoso C, Timsit S, Villard L, Khrestchatsy M, Fontés M, Colleaux L (1998) Specific interaction between the XNP/ATR-X gene product and the SET domain of the human EZH2 protein. Hum Mol Genet 7:679–684

    PubMed  CAS  Google Scholar 

  • Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9:33–46

    PubMed  CAS  Google Scholar 

  • Cheeseman IM, Anderson S, Jwa M, Green EM, Kang J-S, Yates Iii JR, Chan CSM, Drubin DG, Barnes G (2002) Phospho-regulation of kinetochore-microtubule attachments by the Aurora Kinase Ipl1p. Cell 111:163–172

    PubMed  CAS  Google Scholar 

  • Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20:1522–1528

    PubMed  CAS  Google Scholar 

  • De La Fuente R (2006) Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol 292:1–12

    Google Scholar 

  • De La Fuente R, Eppig JJ (2001) Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling. Dev Biol 229:224–236

    Google Scholar 

  • De La Fuente R, Viveiros M, Burns K, Adashi E, Matzuk M, Eppig J (2004a) Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev Biol 275:447–458

    Google Scholar 

  • De La Fuente R, Viveiros M, Wigglesworth K, Eppig J (2004b) ATRX, a member of the SNF2 family of helicase /ATPases, is required for chromosome alignment and meiotic spindle organization in metaphase II stage mouse oocytes. Dev Biol 272:1–14

    Google Scholar 

  • De La Fuente R, Baumann C, Viveiros MM (2011) Role of ATRX in chromatin structure and function: implications for chromosome instability and human disease. Reproduction 142:221–234

    Google Scholar 

  • Delage B, Dashwood RH (2008) Dietary manipulation of histone structure and function. Annu Rev Nutr 28:347–366

    PubMed  CAS  Google Scholar 

  • DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED (2006) Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127:969–982

    PubMed  CAS  Google Scholar 

  • Dhayalan A, Tamas R, Bock I, Tattermusch A, Dimitrova E, Kudithipudi S, Ragozin S, Jeltsch A (2011) The ATRX-ADD domain binds to H3 tail peptides and reads the combined methylation state of K4 and K9. Hum Mol Genet 20(11):2195–2203

    PubMed  CAS  Google Scholar 

  • Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24:1253–1265

    PubMed  CAS  Google Scholar 

  • Duesbery NS, Choi T, Brown KD, Wood KW, Resau J, Fukasawa K, Cleveland DW, Vande Woude GF (1997) CENP-E is an essential kinetochore motor in maturing oocytes and is masked during Mos-dependent, cell cycle arrest at metaphase II. Proc Natl Acad Sci USA 94:9165–9170

    PubMed  CAS  Google Scholar 

  • Durand-Dubief M, Ekwall K (2008) Heterochromatin tells CENP-A where to go. Bioessays 30:526–529

    PubMed  CAS  Google Scholar 

  • Ekwall K (2007) Epigenetic control of centromere behavior. Annu Rev Genet 41:63–81

    PubMed  CAS  Google Scholar 

  • Elsasser SJ, Allis CD, Lewis PW (2011) New epigenetic drivers of cancers. Science 331:1145–1146

    PubMed  CAS  Google Scholar 

  • Emelyanov AV, Konev AY, Vershilova E, Fyodorov DV (2010) Protein complex of Drosophila ATRX/XNP and HP1A is required for the formation of pericentric beta-heterochromatin in vivo. J Biol Chem 285:15027–15037

    PubMed  CAS  Google Scholar 

  • Eustermann S, Yang J-C, Law MJ, Amos R, Chapman LM, Jelinska C, Garrick D, Clynes D, Gibbons RJ, Rhodes D, Higgs DR, Neuhaus D (2011) Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nat Struct Mol Biol 18:777–782

    PubMed  CAS  Google Scholar 

  • Fragouli E, Bianchi V, Patrizio P, Obradors A, Huang Z, Borini A, Delhanty JDA, Wells D (2010) Transcriptomic profiling of human oocytes: association of meiotic aneuploidy and altered oocyte gene expression. Mol Hum Reprod 16:570–582

    PubMed  CAS  Google Scholar 

  • Fragouli E, Alfarawati S, Goodall N, Sanchez-Garcia 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

    Google Scholar 

  • Garrick D, Sharpe JA, Arkell R, Dobbie L, Smith AJ, Wood WG, Higgs DR, Gibbons RJ (2006) Loss of Atrx affects trophoblast development and the pattern of X-inactivation in extraembryonic tissues. PLoS Genet 2:e58

    PubMed  Google Scholar 

  • Gazdag E, Santenard A, Ziegler-Birling C, Altobelli G, Poch O, Tora L, Torres-Padilla M-E (2009) TBP2 is essential for germ cell development by regulating transcription and chromatin condensation in the oocyte. Genes Dev 23:2210–2223

    PubMed  CAS  Google Scholar 

  • Gibbons RJ, Picketts DJ, Villard L, Higgs DR (1995) Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell 80:837–845

    PubMed  CAS  Google Scholar 

  • Gibbons R, Bachoo S, Picketts D, Aftimos S, Asenbauer B, Bergoffen J, Berry S, Dahl N, Fryer A, Keppler K, Kurosawa K, Levin M, Masuno M, Neri G, Pierpont M, Slaney S, Higgs D (1997) Mutations in transcriptional regulator ATRX establish the functional significance of a PHD-like domain. Nat Genet 17:146–148

    PubMed  CAS  Google Scholar 

  • Gibbons RJ, McDowell TL, Raman S, O'Rourke DM, Garrick D, Ayyub H, Higgs DR (2000) Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat Genet 24:368–371

    PubMed  CAS  Google Scholar 

  • Gibbons RJ, Pellagatti A, Garrick D, Wood WG, Malik N, Ayyub H, Langford C, Boultwood J, Wainscoat JS, Higgs DR (2003) Identification of acquired somatic mutations in the gene encoding chromatin-remodeling factor ATRX in the [alpha]-thalassemia myelodysplasia syndrome (ATMDS). Nat Genet 34:446–449

    PubMed  CAS  Google Scholar 

  • Goldberg AD, Banaszynski LA, Noh K-M, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee Y-L, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang C, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D, Allis CD (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678–691

    PubMed  CAS  Google Scholar 

  • Gruzova MN, Parfenov VN (1993) Karyosphere in oogenesis and intranuclear morphogenesis. Int Rev Cytol 144:1–52

    PubMed  CAS  Google Scholar 

  • Guenatri M, Bailly D, Maison C, Almouzni G (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166:493–505

    PubMed  CAS  Google Scholar 

  • Hakimi M, Bochar D, Schmiesing J, Dong Y, Barak O, Speicher D, Yokomori K, Shiekhattar R (2002) A chromatin remodelling complex that loads cohesin onto human chromosomes. Nature 418:994–998

    PubMed  CAS  Google Scholar 

  • Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MS (2004) Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet 13:2263–2278

    PubMed  CAS  Google Scholar 

  • Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280–291

    PubMed  CAS  Google Scholar 

  • Hassold T, Hall H, Hunt P (2007) The origin of human aneuploidy: where we have been, where we are going. Hum Mol Genet 16:203–208

    Google Scholar 

  • Heaphy CM, de Wilde RF, Jiao Y, Klein AP, Edil BH, Shi C, Bettegowda C, Rodriguez FJ, Eberhart CG, Hebbar S, Offerhaus GJ, McLendon R, Rasheed BA, He Y, Yan H, Bigner DD, Oba-Shinjo SM, Marie SKN, Riggins GJ, Kinzler KW, Vogelstein B, Hruban RH, Maitra A, Papadopoulos N, Meeker AK (2011) Altered telomeres in tumors with ATRX and DAXX mutations. Science 333:425

    PubMed  CAS  Google Scholar 

  • Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360

    PubMed  CAS  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    PubMed  CAS  Google Scholar 

  • Homer HA, McDougall A, Levasseur M, Yallop K, Murdoch AP, Herbert M (2005) Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev 19:202–207

    PubMed  CAS  Google Scholar 

  • Houlard M, Berlivet S, Probst AV, Quivy JP, Hery P, Almouzni G, Gerard M (2006) CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells. PLoS Genet 2(11):e181

    PubMed  Google Scholar 

  • Howman EV, Fowler KJ, Newson AJ, Redward S, MacDonald AC, Kalitsis P, Choo KHA (2000) Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci USA 97:1148–1153

    PubMed  CAS  Google Scholar 

  • Hunt PA, Hassold TJ (2008) Human female meiosis: what makes a good egg go bad? Trends Genet 24:86–93

    PubMed  CAS  Google Scholar 

  • Ishov AM, Vladimirova OV, Maul GG (2004) Heterochromatin and ND10 are cell-cycle regulated and phosphorylation-dependent alternate nuclear sites of the transcription repressor Daxx and SWI/SNF protein ATRX. J Cell Sci 117:3807–3820

    PubMed  CAS  Google Scholar 

  • Ivanovska I, Orr-Weaver TL (2006) Histone modifications and the chromatin scaffold for meiotic chromosome architecture. Cell Cycle 5:2064–2071

    PubMed  CAS  Google Scholar 

  • Ivanovska I, Khandan T, Ito T, Orr-Weaver TL (2005) A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Genes Dev 19:2571–2582

    PubMed  CAS  Google Scholar 

  • Iwase S, Xiang B, Ghosh S, Ren T, Lewis PW, Cochrane JC, Allis CD, Picketts DJ, Patel DJ, Li H, Shi Y (2011) ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome. Nat Struct Mol Biol 18:769–776

    PubMed  CAS  Google Scholar 

  • Jiao Y, Shi C, Edil BH, de Wilde RF, Klimstra DS, Maitra A, Schulick RD, Tang LH, Wolfgang CL, Choti MA, Velculescu VE, Diaz LA, Vogelstein B, Kinzler KW, Hruban RH, Papadopoulos N (2011) DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331:1199–1203

    PubMed  CAS  Google Scholar 

  • Karpen GH, Allshire RC (1997) The case for epigenetic effects on centromere identity and function. Trends Genet 13:489–496

    PubMed  CAS  Google Scholar 

  • Kernohan KD, Jiang Y, Tremblay DC, Bonvissuto AC, Eubanks JH, Mann MRW, Berube NG (2010) ATRX partners with cohesin and MeCP2 and contributes to developmental silencing of imprinted genes in the brain. Dev Cell 18:191–202

    PubMed  CAS  Google Scholar 

  • Kim J, Liu H, Tazaki M, Nagata M, Aoki F (2003) Changes in histone acetylation during mouse oocyte meiosis. J Cell Biol 162:37–46

    PubMed  CAS  Google Scholar 

  • Kimmins S, Sassone-Corsi P (2005) Chromatin remodelling and epigenetic features of germ cells. Nature 434:583–589

    PubMed  CAS  Google Scholar 

  • Kitajima TS, Ohsugi M, Ellenberg J (2011) Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 146:568–581

    PubMed  CAS  Google Scholar 

  • Kourmouli N, Sun YM, van der Sar S, Singh PB, Brown JP (2005) Epigenetic regulation of mammalian pericentric heterochromatin in vivo by HP1. Biochem Biophys Res Commun 337:901–907

    PubMed  CAS  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    PubMed  CAS  Google Scholar 

  • Kruhlak MJ, Hendzel MJ, Fischle W, Bertos NR, Hameed S, Yang XJ, Verdin E, Bazett-Jones DP (2001) Regulation of global acetylation in mitosis through loss of histone acetyltransferases and deacetylases from chromatin. J Biol Chem 276:38307–38319

    PubMed  CAS  Google Scholar 

  • Kudo NR, Wassmann K, Anger M, Schuh M, Wirth KG, Xu H, Helmhart W, Kudo H, McKay M, Maro B, Ellenberg J, de Boer P, Nasmyth K (2006) Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 126:135–146

    PubMed  CAS  Google Scholar 

  • Kuliev A, Zlatopolsky Z, Kirillova I, Spivakova J, Cieslak J (2011) Meiosis errors in over 20,000oocytes studied in the practice of preimplantation aneuploidy testing. Reprod Biomed Online 22:2–8

    PubMed  Google Scholar 

  • Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120

    PubMed  CAS  Google Scholar 

  • Lamb NE, Sherman SL, Hassold TJ (2005) Effect of meiotic recombination on the production of aneuploid gametes in humans. Cytogenet Genome Res 111:250–255

    PubMed  CAS  Google Scholar 

  • Law MJ, Lower KM, Voon HPJ, Hughes JR, Garrick D, Viprakasit V, Mitson M, De Gobbi M, Marra M, Morris A, Abbott A, Wilder SP, Taylor S, Santos GM, Cross J, Ayyub H, Jones S, Ragoussis J, Rhodes D, Dunham I, Higgs DR, Gibbons RJ (2010) ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 143:367–378

    PubMed  CAS  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. Nat Cell Biol 10:42–52

    PubMed  CAS  Google Scholar 

  • Leland S, Nagarajan P, Polyzos A, Thomas S, Samaan G, Donnell R, Marchetti F, Venkatachalam S (2009) Heterozygosity for a Bub1 mutation causes female-specific germ cell aneuploidy in mice. Proc Natl Acad Sci USA 106:12776–12781

    PubMed  CAS  Google Scholar 

  • Levy M, Fernandes A, Tremblay D, Seah C, Berube N (2008) The SWI/SNF protein ATRX co-regulates pseudoautosomal genes that have translocated to autosomes in the mouse genome. BMC Genomics 9:468

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Llano E, Gomez R, Gutierrez-Caballero C, Herran Y, Sanchez-Martin M, Vazquez-Quinones L, Hernandez T, de Alava E, Cuadrado A, Barbero JL, Suja JA, Pendas AM (2008) Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes Dev 22:2400–2413

    PubMed  CAS  Google Scholar 

  • Luciani JJ, Depetris D, Usson Y, Metzler-Guillemain C, Mignon-Ravix C, Mitchell MJ, Megarbane A, Sarda P, Sirma H, Moncla A, Feunteun J, Mattei MG (2006) PML nuclear bodies are highly organised DNA-protein structures with a function in heterochromatin remodelling at the G2 phase. J Cell Sci 119:2518–2531

    PubMed  CAS  Google Scholar 

  • Ma W, Baumann C, Viveiros MM (2010) NEDD1 is crucial for meiotic spindle stability and accurate chromosome segregation in mammalian oocytes. Dev Biol 339:439–450

    PubMed  CAS  Google Scholar 

  • Maison C, Almouzni G (2004) HP1 and the dynamics of heterochromatin maintenance. Nat Rev Mol Cell Biol 5:296–304

    PubMed  CAS  Google Scholar 

  • Maison C, Bailly D, Peters A, Quivy J, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G (2002) Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and RNA component. Nat Genet 30:329–334

    PubMed  Google Scholar 

  • Malik HS, Henikoff S (2009) Major evolutionary transitions in centromere complexity. Cell 138:1067–1082

    PubMed  CAS  Google Scholar 

  • McDowell TL, Gibbons RJ, Sutherland H, O'Rourke DM, Bickmore WA, Pombo A, Turley H, Gatter K, Picketts DJ, Buckle VJ (1999) Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc Natl Acad Sci USA 96:13983–13988

    PubMed  CAS  Google Scholar 

  • McGuinness BE, Anger M, Kouznetsova A, Gil-BernabÈ AM, Helmhart W, Kudo NR, Wuensche A, Taylor S, Hoog C, Novak B, Nasmyth K (2009) Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr Biol 19:369–380

    PubMed  CAS  Google Scholar 

  • Mitson M, Kelley LA, Sternberg MJE, Higgs DR, Gibbons RJ (2011) Functional significance of mutations in the Snf2 domain of ATRX. Hum Mol Genet 20:2603–2610

    PubMed  CAS  Google Scholar 

  • Murphy TD, Karpen GH (1998) Centromeres take flight: alpha satellite and the quest for the human centromere. Cell 93:317–320

    PubMed  CAS  Google Scholar 

  • Nagaoka S, Hodges CA, Albertini DF, Hunt PA (2011) Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr Biol 21:651–657

    PubMed  CAS  Google Scholar 

  • Nan X, Hou J, Maclean A, Nasir J, Lafuente MJ, Shu X, Kriaucionis S, Bird A (2007) Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc Natl Acad Sci USA 104(8):2709–2714

    PubMed  CAS  Google Scholar 

  • Nasmyth K, Haering CH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43:525–558

    PubMed  CAS  Google Scholar 

  • Niault T, Hached K, Sotillo R, Sorger PK, Maro B, Benezra R, Wassmann K (2007) Changing Mad2 levels affects chromosome segregation and spindle assembly checkpoint control in female mouse meiosis-I. PLoS One 2:e1165

    PubMed  Google Scholar 

  • Nicklas R, Ward S (1994) Elements of error correction in mitosis: microtubule capture, release, and tension. J Cell Biol 126:1241–1253

    PubMed  CAS  Google Scholar 

  • Nicklas RB, Waters JC, Salmon ED, Ward SC (2001) Checkpoint signals in grasshopper meiosis are sensitive to microtubule attachment, but tension is still essential. J Cell Sci 114:4173–4183

    PubMed  CAS  Google Scholar 

  • Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, Grewal SI, Watanabe Y (2002) Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 4:89–93

    PubMed  CAS  Google Scholar 

  • Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA (2001) Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol 153:1209–1226

    PubMed  CAS  Google Scholar 

  • Pan H, Ma P, Zhu W, Schultz RM (2008) Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev Biol 316:397–407

    PubMed  CAS  Google Scholar 

  • Perpelescu M, Fukagawa T (2011) The ABCs of CENPs. Chromosoma 120:425–446

    PubMed  Google Scholar 

  • Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337

    PubMed  CAS  Google Scholar 

  • Petronczki M, Siomos M, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440

    PubMed  CAS  Google Scholar 

  • Picketts DJ, Higgs DR, Bachoo S, Blake DJ, Quarrell OW, Gibbons RJ (1996) ATRX encodes a novel member of the SNF2 family of proteins: mutations point to a common mechanism underlying the ATR-X syndrome. Hum Mol Genet 5:1899–1907

    PubMed  CAS  Google Scholar 

  • Picketts DJ, Tastan AO, Higgs DR, Gibbons RJ (1998) Comparison of the human and murine ATRX gene identifies highly conserved, functionally important domains. Mamm Genome 9:400–403

    PubMed  CAS  Google Scholar 

  • Pluta AF, Mackay AM, Ainsztein AM, Goldberg IG, Earnshaw WC (1995) The centromere: hub of chromosomal activities. Science 270:1591–1594

    PubMed  CAS  Google Scholar 

  • Polo SE, Almouzni G (2006) Chromatin assembly: a basic recipe with various flavours. Curr Opin Genet Dev 16:104–111

    PubMed  CAS  Google Scholar 

  • Prieto I, Tease C, Pezzi N, Buesa J, Ortega S, Kremer L, Martinez A, Martinez-A C, Hulten M, Barbero JL (2004) Cohesin component dynamics during meiotic prophase I in mammalian oocytes. Chromosome Res 12:197–213

    PubMed  CAS  Google Scholar 

  • Probst AV, Almouzni G (2011) Heterochromatin establishment in the context of genome-wide epigenetic reprogramming. Trends Genet 27:177–185

    PubMed  CAS  Google Scholar 

  • Puschendorf M, Terranova R, Boutsma E, Mao X, Isono K, Brykczynska U, Kolb C, Otte AP, Koseki H, Orkin SH, van Lohuizen M, Peters AH (2008) PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat Genet 40:411–420

    PubMed  CAS  Google Scholar 

  • Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593–599

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Revenkova E, Eijpe M, Heyting C, Hodges C, Hunt P, Liebe B, Scherthan H, Jessberger R (2004) Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6:555–562

    PubMed  CAS  Google Scholar 

  • Revenkova E, Herrmann K, Adelfalk C, Jessberger R (2010) Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol 20:1529–1533

    PubMed  CAS  Google Scholar 

  • Ritchie K, Seah C, Moulin J, Issac C, Dick F, Berube N (2008) Loss of ATRX leads to chromosome cohesion and congression defects. J Cell Biol 180:315–324

    PubMed  CAS  Google Scholar 

  • Roberts R, Iatropoulou A, Ciantar D, Stark J, Becker DL, Franks S, Hardy K (2005) Follicle-stimulating hormone affects metaphase i chromosome alignment and increases aneuploidy in mouse oocytes matured in vitro. Biol Reprod 72:107–118

    PubMed  CAS  Google Scholar 

  • Santenard A, Torres-Padilla M-E (2009) Epigenetic reprogramming in mammalian reproduction: contribution from histone variants. Epigenetics 4:80–84

    PubMed  CAS  Google Scholar 

  • Santenard A, Ziegler-Birling C, Koch M, Tora L, Bannister AJ, Torres-Padilla M-E (2010) Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat Cell Biol 12:853–862

    PubMed  CAS  Google Scholar 

  • Sarma K, Reinberg D (2005) Histone variants meet their match. Nat Rev Mol Cell Biol 6:139–149

    PubMed  CAS  Google Scholar 

  • Schneiderman JI, Sakai A, Goldstein S, Ahmad K (2009) The XNP remodeler targets dynamic chromatin in Drosophila. Proc Natl Acad Sci USA 106:14472–14477

    PubMed  CAS  Google Scholar 

  • Schober CS, Aydiner F, Booth CJ, Seli E, Reinke V (2011) The kinase VRK1 is required for normal meiotic progression in mammalian oogenesis. Mech Dev 128:178–190

    PubMed  CAS  Google Scholar 

  • Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18:1251–1262

    PubMed  CAS  Google Scholar 

  • Serrano E, Lasa A, Perea G, Carnicer M, Brunet S, Aventín A, Sierra J, Nomdedéu J (2006) Acute myeloid leukemia subgroups identified by pathway-restricted gene expression signatures. Acta Hematol 116:77–89

    CAS  Google Scholar 

  • Taddei A, Maison C, Roche D, Almouzni G (2001) Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat Cell Biol 3:114–120

    PubMed  CAS  Google Scholar 

  • Taddei A, Roche D, Bickmore WA, Almouzni G (2005) The effects of histone deacetylase inhibitors on heterochromatin: implications for anticancer therapy? EMBO Rep 6:520–524

    PubMed  CAS  Google Scholar 

  • Takada Y, Naruse C, Costa Y, Shirakawa T, Tachibana M, Sharif J, Kezuka-Shiotani F, Kakiuchi D, Masumoto H, Shinkai Y-I, Ohbo K, Peters AHFM, Turner JMA, Asano M, Koseki H (2011) HP1 gamma links histone methylation marks to meiotic synapsis in mice. Development 138:4207–4217

    PubMed  CAS  Google Scholar 

  • Talbert PB, Henikoff S (2010) Centromeres convert but don’t cross. PLoS Biol 8:e1000326

    PubMed  Google Scholar 

  • Tang J, Wu S, Liu H, Stratt R, Barak OG, Shiekhattar R, Picketts DJ, Yang X (2004) A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J Biol Chem 279:20369–20377

    PubMed  CAS  Google Scholar 

  • Torres-Padilla ME, Bannister AJ, Hurd PJ, Kouzarides T, Zernicka-Goetz M (2006) Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int J Dev Biol 50:455–461

    PubMed  CAS  Google Scholar 

  • van den Berg IM, Eleveld C, van der Hoeven M, Birnie E, Steegers EAP, Galjaard RJ, Laven JSE, van Doorninck JH (2011) Defective deacetylation of histone 4 K12 in human oocytes is associated with advanced maternal age and chromosome misalignment. Hum Reprod 26(5):1181–1190

    PubMed  Google Scholar 

  • Vialard F, Petit C, Bergere M, Gomes DM, Martel-Petit V, Lombroso R, Ville Y, Gerard H, Selva J (2006) Evidence of a high proportion of premature unbalanced separation of sister chromatids in the first polar bodies of women of advanced age. Hum Reprod 21:1172–1178

    PubMed  CAS  Google Scholar 

  • Villard L, Lossi AM, Cardoso C, Proud V, Chiaroni P, Colleaux L, Schwartz C, Fonés M (1997) Determination of the genomic structure of the XNP/ATRX gene encoding a potential zinc finger helicase. Genomics 43:149–155

    PubMed  CAS  Google Scholar 

  • Welburn JPI, Grishchuk EL, Backer CB, Wilson-Kubalek EM, Yates JR, Cheeseman IM (2009) The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev Cell 16:374–385

    PubMed  CAS  Google Scholar 

  • Welburn JPI, Vleugel M, Liu D, Yates JR, Lampson MA, Fukagawa T, Cheeseman IM (2010) Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol Cell 38:383–392

    PubMed  CAS  Google Scholar 

  • Wiens GR, Sorger PK (1998) Centromeric chromatin and epigenetic effects in kinetochore assembly. Cell 93:313–316

    PubMed  CAS  Google Scholar 

  • Wood KW, Sakowicz R, Goldstein LSB, Cleveland DW (1997) CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment. Cell 91:357–366

    PubMed  CAS  Google Scholar 

  • Wood AJ, Severson AF, Meyer BJ (2010) Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 11:391–404

    PubMed  CAS  Google Scholar 

  • Xue Y, Gibbons R, Yan Z, Yang D, McDowell TL, Sechi S, Qin J, Zhou S, Higgs D, Wang W (2003) The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc Natl Acad Sci USA 100:10635–10640

    PubMed  CAS  Google Scholar 

  • Yamagishi Y, Sakuno T, Shimura M, Watanabe Y (2008) Heterochromatin links to centromeric protection by recruiting shugoshin. Nature 455:251–255

    PubMed  CAS  Google Scholar 

  • Yang F, Baumann C, De La Fuente R (2009) Persistence of histone H2AX phosphorylation after meiotic chromosome synapsis and abnormal centromere cohesion in poly (ADP-ribose) polymerase (Parp-1) null oocytes. Dev Biol 331:326–338

    PubMed  CAS  Google Scholar 

  • Yang K-T, Li S-K, Chang C-C, Tang C-JC, Lin Y-N, Lee S-C, Tang TK (2010) Aurora-C Kinase deficiency causes cytokinesis failure in meiosis-I and production of large polyploid oocytes in mice. Mol Biol Cell 21:2371–2383

    PubMed  CAS  Google Scholar 

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Acknowledgments

Research in the author’s laboratory is supported by grants from the National Institutes of Health (NICHD): 2RO1-HDO42740 and the Georgia Cancer Coalition. We apologize to colleagues whose work could not be cited due to space limitations.

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  1. Department of Physiology and Pharmacology, College of Veterinary Medicine, University of Georgia, 501 D.W. Brooks Drive, Athens, GA, 30602, USA

    Rabindranath De La Fuente, Claudia Baumann & Maria M. Viveiros

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  1. Rabindranath De La Fuente
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  2. Claudia Baumann
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Correspondence to Rabindranath De La Fuente .

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  1. CNRS UMR 6061, Fac. Médecine, Université de Rennes 1, Rennes CX, 35043, France

    Jacek Z. Kubiak

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De La Fuente, R., Baumann, C., Viveiros, M.M. (2012). Chromatin Structure and ATRX Function in Mouse Oocytes. In: Kubiak, J. (eds) Mouse Development. Results and Problems in Cell Differentiation, vol 55. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30406-4_3

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