ATRX contributes to epigenetic asymmetry and silencing of major satellite transcripts in the maternal genome of the mouse embryo

Development (Cambridge)

Volumn 142, Issue 10, 2015, Pages 1806-1817

  De La Fuente, Rabindranath ^a   Baumann, Claudia ^a   Viveiros, Maria M ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Centromere; Chromatin remodeling; CO FISH; Death domain associated protein (DAXX); Epigenetic modifications; Heterochromatin; Kinetochore; Meiosis

Indexed keywords

ATRX PROTEIN; AURORA B KINASE; CENP C PROTEIN; COHESIN; DAXX PROTEIN; DNA DAZ INTERACTING ZINC FINGER PROTEIN; DNA METHYLTRANSFERASE 1; HISTONE METHYL TRANSFERASE; HISTONE METHYLTRANSFERASE; METHYLTRANSFERASE; PROTEIN; SATELLITE DNA; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; ACYLTRANSFERASE; ATRX PROTEIN, MOUSE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; DNA HELICASE; ESTABLISHMENT OF COHESION 1 HOMOLOG 2, MOUSE; GLP PROTEIN, MOUSE; HETEROCHROMATIN; HISTONE LYSINE METHYLTRANSFERASE; NUCLEAR PROTEIN;

ANAPHASE; ANIMAL CELL; ARTICLE; CENTROMERE; CHROMATID; CHROMOSOMAL INSTABILITY; CHROMOSOME 16; CHROMOSOME 17; CHROMOSOME BREAKAGE; CHROMOSOME CONDENSATION; CHROMOSOME DAMAGE; CHROMOSOME SEGREGATION; DIPLOIDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; EPIGENETIC ASYMMETRY; EPIGENETICS; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE REPRESSION; GENE SILENCING; GENOME; HETEROCHROMATIN; MATERNAL GENOME; MITOSIS; MITOTIC RECOMBINATION; MOUSE; MOUSE EMBRYO; NONHUMAN; OOCYTE; PERICENTRIC HETEROCHROMATIN; PRIORITY JOURNAL; PRONUCLEUS; REAL TIME POLYMERASE CHAIN REACTION; SISTER CHROMATID EXCHANGE; SPECTRAL KARYOTYPING; UPREGULATION; WILD TYPE; X CHROMOSOME; Y CHROMOSOME; ZYGOTE; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC EPIGENESIS; GENETICS; MEIOSIS; METABOLISM; PHYSIOLOGY;

ACETYLTRANSFERASES; ANIMALS; CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA HELICASES; EPIGENESIS, GENETIC; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; KINETOCHORES; MEIOSIS; MICE; NUCLEAR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84929206958     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.118927     Document Type: Article

References (66)

1. Almouzni, G. and Probst, A. V. (2011). Heterochromatin maintenance and establishment: lessons from the mouse pericentromere. Nucleus 2, 332-338
2. Asaithamby, A., Hu, B. and Chen, D. J. (2011). Unrepaired clustered DNA lesions induce chromosome breakage in human cells. Proc. Natl. Acad. Sci. USA 108, 8293-8298
3. Banaszynski, L. A., Allis, C. D. and Lewis, P. W. (2010). Histone variants in metazoan development. Dev. Cell 19, 662-674
4. Baumann, C., Viveiros, M. M. and 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
5. Bean, C. J., Hunt, P. A., Millie, E. A. and Hassold, T. J. (2001). Analysis of a malsegregating mouse Y chromosome: evidence that the earliest cleavage divisions of the mammalian embryo are non-disjunction-prone. Hum. Mol. Genet. 10, 963-972
6. Berube, N. G. (2011). ATRX in chromatin assembly and genome architecture during development and disease. Biochem. Cell Biol. 89, 435-444
7. Bérubé, N.G., Smeenk, C.A. and Picketts, D. J. (2000). Cell cycle-dependent phosphorylation of the ATRX protein correlates with changes in nuclear matrix and chromatin association. Hum. Mol. Genet. 9, 539-547
8. Bouzinba-Segard, H., Guais, A. and Francastel, C. (2006). Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc. Natl. Acad. Sci. USA 103, 8709-8714
9. Caron, P., Aymard, F., Iacovoni, J. S., Briois, S., Canitrot, Y., Bugler, B., Massip, L., Losada, A. and Legube, G. (2012). Cohesin protects genes against gamma H2AX induced by DNA double-strand breaks. PLoS Genet. 8, e1002460
10. Casanova, M., Pasternak, M., El Marjou, F., Le Baccon, P., Probst, A. V. and Almouzni, G. (2013). Heterochromatin reorganization during early mouse development requires a single-stranded noncoding transcript. Cell Rep. 4, 1156-1167
11. Chan, F. L. and Wong, L. H. (2012). Transcription in the maintenance of centromere chromatin identity. Nucleic Acids Res. 40, 11178–11188
12. Chavez, S. L., Loewke, K. E., Han, J., Moussavi, F., Colls, P., Munne, S., Behr, B. and Reijo Pera, R. A. (2012). Dynamic blastomere behaviour reflects human embryo ploidy by the four-cell stage. Nat. Commun. 3, 1251
13. Chiolo, I., Minoda, A., Colmenares, S. U., Polyzos, A., Costes, S. V. and Karpen, G. H. (2011). Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144, 732-744
14. Chu, L., Zhu, T., Liu, X., Yu, R., Bacanamwo, M., Dou, Z., Chu, Y., Zou, H., Gibbons, G. H., Wang, D. et al. (2012). SUV39H1 orchestrates temporal dynamics of centromeric methylation essential for faithful chromosome segregation in mitosis. J. Mol. Cell Biol. 4, 331-340
15. De La Fuente, R., Viveiros, M. M., Wigglesworth, K. and Eppig, J. J. (2004). 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
16. De La Fuente, R., Baumann, C. and Viveiros, M. M. (2011). Role of ATRX in chromatin structure and function: implications for chromosome instability and human disease. Reproduction 142, 221-234
17. Drane, P., Ouararhni, K., Depaux, A., Shuaib, M. and 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
18. Durand-Dubief, M. and Ekwall, K. (2008). Heterochromatin tells CENP-A where to go. Bioessays 30, 526-529
19. Elsasser, S. J., Allis, C. D. and Lewis, P. W. (2011). New epigenetic drivers of cancers. Science 331, 1145-1146
20. Fadloun, A., Le Gras, S., Jost, B., Ziegler-Birling, C., Takahashi, H., Gorab, E., Carninci, P. and Torres-Padilla, M.-E. (2013). Chromatin signatures and retrotransposon profiling in mouse embryos reveal regulation of LINE-1 by RNA. Nat. Struct. Mol. Biol. 20, 332-338
21. Ferri, F., Bouzinba-Segard, H., Velasco, G., Hube, F. and Francastel, C. (2009). Non-coding murine centromeric transcripts associate with and potentiate Aurora B kinase. Nucleic Acids Res. 37, 5071-5080
22. Gibbons, R. J. and Higgs, D. R. (2000). Molecular-clinical spectrum of the ATR-X syndrome. Am. J. Med. Genet. 97, 204-212
23. Goldberg, A. D., Banaszynski, L. A., Noh, K.-M., Lewis, P. W., Elsaesser, S. J., Stadler, S., Dewell, S., Law, M., Guo, X., Li, X. et al. (2010). Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678-691
24. Gopalakrishnan, S., Sullivan, B. A., Trazzi, S., Della Valle, G. and Robertson, K. D. (2009). DNMT3B interacts with constitutive centromere protein CENP-C to modulate DNA methylation and the histone code at centromeric regions. Hum. Mol. Genet. 18, 3178-3193
25. Ha, K., Lee, G. E., Palii, S. S., Brown, K. D., Takeda, Y., Liu, K., Bhalla, K. N. and Robertson, K. D. (2011). Rapid and transient recruitment of DNMT1 to DNA double-strand breaks is mediated by its interaction with multiple components of the DNA damage response machinery. Hum. Mol. Genet. 20, 126-140
26. Hassold, T. and Hunt, P. (2001). To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280-291
27. Hassold, T., Hall, H. and Hunt, P. (2007). The origin of human aneuploidy: where we have been, where we are going. Hum. Mol. Genet. 16, R203-R208
28. Hayashi-Takanaka, Y., Yamagata, K., Wakayama, T., Stasevich, T. J., Kainuma, T., Tsurimoto, T., Tachibana, M., Shinkai, Y., Kurumizaka, H., Nozaki, N. et al. (2011). Tracking epigenetic histone modifications in single cells using Fab-based live endogenous modification labeling. Nucleic Acids Res. 39, 6475-6488
29. Jaco, I., Canela, A., Vera, E. and Blasco, M. A. (2008). Centromere mitotic recombination in mammalian cells. J. Cell Biol. 181, 885-892
30. Jakob, B., Splinter, J., Conrad, S., Voss, K.-O., Zink, D., Durante, M., Lobrich, M. and Taucher-Scholz, G. (2011). DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res. 39, 6489-6499
31. Jiao, Y., Shi, C., Edil, B. H., de Wilde, R. F., Klimstra, D. S., Maitra, A., Schulick, R. D., Tang, L. H., Wolfgang, C. L., Choti, M. A. et al. (2011). DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331, 1199-1203
32. Jones, M. J. K. and Jallepalli, P. V. (2012). Chromothripsis: chromosomes in crisis. Dev. Cell 23, 908-917
33. Kanellopoulou, C., Muljo, S. A., Kung, A. L., Ganesan, S., Drapkin, R., Jenuwein, T., Livingston, D. M. and Rajewsky, K. (2005). Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489-501
34. Knowlton, A. L., Lan, W. and Stukenberg, P. T. (2006). Aurora B is enriched at merotelic attachment sites, where it regulates MCAK. Curr. Biol. 16, 1705-1710
35. Kops, G. J. P. L., Weaver, B. A. A. and Cleveland, D. W. (2005). On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 5, 773-785
36. Kota, S. K. and Feil, R. (2010). Epigenetic transitions in germ cell development and meiosis. Dev. Cell 19, 675-686
37. Lewis, P. W., Elsaesser, S. J., Noh, K.-M., Stadler, S. C. and Allis, C. D. (2010). Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. USA 107, 14075-14080
38. Lin, C.-J., Conti, M. and Ramalho-Santos, M. (2013). Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development. Development 140, 3624-3634.
39. Lin, C.-J., Koh, F. M., Wong, P., Conti, M. and Ramalho-Santos, M. (2014). Hiramediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Dev. Cell 30, 268-279.
40. Losada, A. and Hirano, T. (2005). Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev. 19, 1269-1287.
41. Lovejoy, C. A., Li, W., Reisenweber, S., Thongthip, S., Bruno, J., de Lange, T., De, S., Petrini, J. H. J., Sung, P. A., Jasin, M. et al. (2012). Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLoS Genet. 8, e1002772.
42. Mayer, W., Smith, A., Fundele, R. and Haaf, T. (2000a). Spatial separation of parental genomes in preimplantation mouse embryos. J. Cell Biol. 148, 629-634.
43. Mayer, W., Niveleau, A., Walter, J., Fundele, R. and Haaf, T. (2000b).Embryogenesis: demethylation of the zygotic paternal genome. Nature 403, 501-502.
44. Milks, K. J., Moree, B. and Straight, A. F. (2009). Dissection of CENP-C–directed centromere and kinetochore assembly. Mol. Biol. Cell 20, 4246-4255.
45. Molenaar, J. J., Koster, J., Zwijnenburg, D. A., van Sluis, P., Valentijn, L. J., van der Ploeg, I., Hamdi, M., van Nes, J., Westerman, B. A., van Arkel, J. et al. (2012). Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 483, 589-593.
46. Noh, K.-M., Maze, I., Zhao, D., Xiang, B., Wenderski, W., Lewis, P. W., Shen, L., Li, H. and Allis, C. D. (2014). ATRX tolerates activity-dependent histone H3 methyl/phos switching to maintain repetitive element silencing in neurons. Proc. Natl. Acad. Sci. USA.
47. Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R., Dean, W., Reik, W. and Walter, J. (2000). Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475-478.
48. Pluta, A. F., Earnshaw, W. C. (1996). Specific interaction between human kinetochore protein CENP-C and a nucleolar transcriptional regulator. J. Biol. Chem. 271, 18767-18774.
49. Probst, A. V. and Almouzni, G. (2011). Heterochromatin establishment in the context of genome-wide epigenetic reprogramming. Trends Genet. 27, 177-185.
50. Probst, A. V., Okamoto, I., Casanova, M., El Marjou, F., Le Baccon, P. and Almouzni, G. (2010). A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev. Cell 19, 625-638.
51. Przewloka, M. R., Venkei, Z., Bolanos-Garcia, V. M., Debski, J., Dadlez, M. and Glover, D. M. (2011). CENP-C is a structural platform for kinetochore assembly. Curr. Biol. 21, 399-405.
52. Puschendorf, M., Terranova, R., Boutsma, E., Mao, X., Isono, K.-i., Brykczynska, U., Kolb, C., Otte, A. P., Koseki, H., Orkin, S. H. et al. (2008). PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 40, 411-420.
53. Ritchie, K., Seah, C., Moulin, J., Isaac, C., Dick, F. and Berube, N. G. (2008). Loss of ATRX leads to chromosome cohesion and congression defects. J. Cell Biol. 180, 315-324.
54. Robberecht, C., Vanneste, E., Pexsters, A., D’Hooghe, T., Voet, T. and Vermeesch, J. R. (2010). Somatic genomic variations in early human prenatal development. Curr. Genomics 11, 397-401.
55. Santenard, A. and Torres-Padilla, M.-E. (2009). Epigenetic reprogramming in mammalian reproduction: contribution from histone variants. Epigenetics 4, 80-84.
56. Santenard, A., Ziegler-Birling, C., Koch, M., Tora, L., Bannister, A. J. and 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.
57. Santos, F., Peters, A. H., Otte, A. P., Reik, W. and Dean, W. (2005). Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280, 225-236.
58. Thorpe, P. H., Bruno, J. and Rothstein, R. (2009). Kinetochore asymmetry defines a single yeast lineage. Proc. Natl. Acad. Sci. USA 106, 6673-6678.
59. Tomkiel, J., Cooke, C. A., Saitoh, H., Bernat, R. L. and Earnshaw, W. C. (1994). CENP-C is required for maintaining proper kinetochore size and for a timely transition to anaphase. J. Cell Biol. 125, 531-545.
60. Unal, E., Heidinger-Pauli, J. M. and Koshland, D. (2007). DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317, 245-248.
61. Urani, C., Corvi, R., Callegaro, G. and Stefanini, F. M. (2013). Objective scoring of transformed foci in BALB/c 3T3 cell transformation assay by statistical image descriptors. Toxicol. In Vitro 27, 1905-1912.
62. Vanneste, E., Voet, T., Le Caignec, C., Ampe, M., Konings, P., Melotte, C., Debrock, S., Amyere, M., Vikkula, M., Schuit, F. et al. (2009). Chromosome instability is common in human cleavage-stage embryos. Nat. Med. 15, 577-583.
63. Verdaasdonk, J. S. and Bloom, K. (2011). Centromeres: unique chromatin structures that drive chromosome segregation. Nat. Rev. Mol. Cell Biol. 12, 320-332.
64. Voet, T., Vanneste, E., Van der Aa, N., Melotte, C., Jackmaert, S., Vandendael, T., Declercq, M., Debrock, S., Fryns, J.-P., Moreau, Y. et al. (2011). Breakage– fusion–bridge cycles leading to inv dup del occur in human cleavage stage embryos. Hum. Mutat. 32, 783-793.
65. Watrin, E. and Peters, J.-M. (2009). The cohesin complex is required for the DNA damage-induced G2/M checkpoint in mammalian cells. EMBO J. 28, 2625-2635.
66. Zhou, W., Wang, X. and Rosenfeld, M. G. (2009). Histone H2A ubiquitination in transcriptional regulation and DNA damage repair. Int. J. Biochem. Cell Biol. 41, 12-15.