ATRX in chromatin assembly and genome architecture during development and disease

Biochemistry and Cell Biology

Volumn 89, Issue 5, 2011, Pages 435-444

  Bérubé, Nathalie G ^a  

^a Victoria Research Laboratories   (Canada)

Author keywords

ATRX; Chromatin structure; Development; Gene regulation

Indexed keywords

ATRX; CHROMATIN ASSEMBLY; CHROMATIN REMODELING; CHROMATIN STRUCTURE; DEVELOPMENT; EMBRYONIC DEVELOPMENT; GENE REGULATIONS; GENOME ARCHITECTURE; HIGHER ORDER; HISTONE VARIANTS; HUMAN DISEASE;

MAMMALS;

GENES;

ATRX PROTEIN; CHROMOSOME PROTEIN; HISTONE H3; HISTONE H4; UNCLASSIFIED DRUG;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; EMBRYO DEVELOPMENT; GENE CONTROL; GENE DOSAGE; GENOME; GENOME ARCHITECTURE; HETEROCHROMATIN; HUMAN; MEIOSIS; MITOSIS; NONHUMAN; PATHOGENESIS; REVIEW;

ALPHA-THALASSEMIA; ANIMALS; CHROMATIN; DNA HELICASES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MENTAL RETARDATION, X-LINKED; MICE; NERVOUS SYSTEM DISEASES; NUCLEAR PROTEINS; RETT SYNDROME;

MAMMALIA;

EID: 80053994579     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/o11-038     Document Type: Review

References (72)

1. Aapola U. Kawasaki K. Scott H.S. Ollila J. Vihinen M. Heino M. et al. 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 (3): 293-298. 10.1006/geno.2000.6168 (Pubitemid 30332033)
2. Amitani I. Baskin R.J. Kowalczykowski S.C. 2006. Visualization of Rad54, a chromatin remodeling protein, translocating on single DNA molecules. Mol. Cell, 23 (1): 143-148. 10.1016/j.molcel.2006.05.009 (Pubitemid 43963440)
3. Argentaro A. Yang J.C. Chapman L. Kowalczyk M.S. Gibbons R.J. Higgs D.R. et al. 2007. Structural consequences of disease-causing mutations in the ATRX-DNMT3-DNMT3L (ADD) domain of the chromatin-associated protein ATRX. Proc. Natl. Acad. Sci. U.S.A. 104 (29): 11939-11944. 10.1073/pnas.0704057104 (Pubitemid 47185609)
4. Bagheri-Fam S. Argentaro A. Svingen T. Combes A.N. Sinclair A.H. Koopman P. Harley V.R. 2011. Defective survival of proliferating Sertoli cells and androgen receptor function in a mouse model of the ATR-X syndrome. Hum. Mol. Genet. 20 (11): 2213-2224. 10.1093/hmg/ddr109
5. Bassett A.R. Cooper S.E. Ragab A. Travers A.A. 2008. The chromatin remodelling factor dATRX is involved in heterochromatin formation. PLoS ONE, 3 (5): e2099. 10.1371/journal.pone.0002099 (Pubitemid 352025099)
6. 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 (2): 209-222. 10.1007/s00412-008-0189-x
7. 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 (1): 29. 10.1186/1471-2199-9-29 (Pubitemid 351455179)
8. Baumann C. Viveiros M.M. 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 (9): 6. 20885787
9. Bérubé N.G. Smeenk C.A. 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 (4): 539-547. 10.1093/hmg/9.4.539 (Pubitemid 30154012)
10. Bérubé N.G. Jagla M. Smeenk C. De Repentigny Y. Kothary R. Picketts D.J. 2002. Neurodevelopmental defects resulting from ATRX overexpression in transgenic mice. Hum. Mol. Genet. 11 (3): 253-261. 10.1093/hmg/11.3.253 (Pubitemid 34173354)
11. Bérubé N.G. Mangelsdorf M. Jagla M. Vanderluit J. Garrick D. Gibbons R.J. et al. 2005. The chromatin-remodeling protein ATRX is critical for neuronal survival during corticogenesis. J. Clin. Invest. 115: 258-267. (Pubitemid 40385468)
12. Bérubé N.G. Healy J. Medina C.F. Wu S. Hodgson T. Jagla M. Picketts D.J. 2008. Patient mutations alter ATRX targeting to PML nuclear bodies. Eur. J. Hum. Genet. 16 (2): 192-201. 10.1038/sj.ejhg.5201943
13. Boycott K.M. Parslow M.I. Ross J.L. Miller I.P. Bech-Hansen N.T. MacLeod P.M. 2003. A familial contiguous gene deletion syndrome at Xp22.3 characterized by severe learning disabilities and ADHD. Am. J. Med. Genet. A. 122A (2): 139-147. 10.1002/ajmg.a.20231 (Pubitemid 37122283)
14. Cardoso C. Timsit S. Villard L. Khrestchatisky M. Fontes 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 (4): 679-684. 10.1093/hmg/7.4.679 (Pubitemid 28152267)
15. Cardoso C. Lutz Y. Mignon C. Compe E. Depetris D. Mattei M.G. et al. 2000. ATR-X mutations cause impaired nuclear location and altered DNA binding properties of the XNP/ATR-X protein. J. Med. Genet. 37 (10): 746-751. 10.1136/jmg.37.10.746
16. Coutinho-Camillo C.M. Miracca E.C. dos Santos M.L. Salaorni S. Sarkis A.S. Nagai M.A. 2006. Identification of differentially expressed genes in prostatic epithelium in relation to androgen receptor CAG repeat length. Int. J. Biol. Markers, 21: 96-105. (Pubitemid 44210038)
17. De La Fuente R. Viveiros M.M. Wigglesworth K. 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): 1-14. 10.1016/j.ydbio.2003.12.012 (Pubitemid 38887280)
18. Dhayalan A. Tamas R. Bock I. Tattermusch A. Dimitrova E. Kudithipudi S. et al. 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. 10.1093/hmg/ddr107
19. Dorsett D. Krantz I.D. 2009. On the molecular etiology of Cornelia de Lange syndrome. Ann. N. Y. Acad. Sci. 1151 (1): 22-37. 10.1111/j.1749-6632.2008. 03450.x
20. 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 (12): 1253-1265. 10.1101/gad.566910
21. Emelyanov A.V. Konev A.Y. Vershilova E. Fyodorov D.V. 2010. Protein complex of Drosophila ATRX/XNP and HP1a is required for the formation of pericentric beta-heterochromatin in vivo. J. Biol. Chem. 285 (20): 15027-15037. 10.1074/jbc.M109.064790
22. Franco B. Meroni G. Parenti G. Levilliers J. Bernard L. Gebbia M. et al. 1995. A cluster of sulfatase genes on Xp22.3: mutations in chondrodysplasia punctata (CDPX) and implications for warfarin embryopathy. Cell, 81 (1): 15-25. 10.1016/0092-8674(95)90367-4
23. Gabory A. Jammes H. Dandolo L. 2010. The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays, 32 (6): 473-480. 10.1002/bies.200900170
24. Garrick D. Samara V. McDowell T.L. Smith A.J. Dobbie L. Higgs D.R. Gibbons R.J. 2004. A conserved truncated isoform of the ATR-X syndrome protein lacking the SWI/SNF-homology domain. Gene, 326: 23-34. 10.1016/j.gene.2003.10. 026 (Pubitemid 38068483)
25. Garrick D. Sharpe J.A. Arkell R. Dobbie L. Smith A.J. Wood W.G. et al. 2006. Loss of Atrx affects trophoblast development and the pattern of X-inactivation in extraembryonic tissues. PLoS Genet. 2 (4): e58. 10.1371/journal.pgen.0020058
26. Gibbons R.J. Higgs D.R. 2010. ATRX: Taming tandem repeats. Cell Cycle, 9 (23): 4605-4606. 10.4161/cc.9.23.14164
27. Gibbons R.J. Suthers G.K. Wilkie A.O. Buckle V.J. Higgs D.R. 1992. X-linked alpha-thalassemia/mental retardation (ATR-X) syndrome: localization to Xq12-q21.31 by X inactivation and linkage analysis. Am. J. Hum. Genet. 51: 1136-1149.
28. Gibbons R.J. Picketts D.J. Villard L. Higgs D.R. 1995. Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell, 80 (6): 837-845. 10.1016/0092- 8674(95)90287-2
29. Gibbons R.J. McDowell T.L. Raman S. O'Rourke D.M. Garrick D. Ayyub H. Higgs D.R. 2000. Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat. Genet. 24 (4): 368-371. 10.1038/74191 (Pubitemid 30187434)
30. Gibbons R.J. Pellagatti A. Garrick D. Wood W.G. Malik N. Ayyub H. et al. 2003. Identification of acquired somatic mutations in the gene encoding chromatin-remodeling factor ATRX in the alpha-thalassemia myelodysplasia syndrome (ATMDS). Nat. Genet. 34 (4): 446-449. 10.1038/ng1213 (Pubitemid 36935339)
31. Goldberg A.D. Banaszynski L.A. Noh K.M. Lewis P.W. Elsaesser S.J. Stadler S. et al. 2010. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell, 140 (5): 678-691. 10.1016/j.cell.2010.01.003
32. Grewal S.I. Jia S. 2007. Heterochromatin revisited. Nat. Rev. Genet. 8 (1): 35-46. 10.1038/nrg2008 (Pubitemid 46006048)
33. Hatton C.S. Wilkie A.O. Drysdale H.C. Wood W.G. Vickers M.A. Sharpe J. et al. 1990. Alpha-thalassemia caused by a large (62 kb) deletion upstream of the human alpha globin gene cluster. Blood, 76: 221-227. (Pubitemid 20220814)
34. Horikoshi T. Kikuchi A. Tamaru S. Ono K. Kita M. Takagi K. et al. 2010. Prenatal findings in a fetus with contiguous gene syndrome caused by deletion of Xp22.3 that includes locus for X-linked recessive type of chondrodysplasia punctata (CDPX1). J. Obstet. Gynaecol. Res. 36 (3): 671-675. 10.1111/j.1447-0756.2010.01193.x
35. Jiao Y. Shi C. Edil B.H. de Wilde R.F. Klimstra D.S. Maitra A. et al. 2011. DAxx/ATRX, MEN1, and mTOR Pathway Genes Are Frequently Altered in Pancreatic Neuroendocrine Tumors. Science, 331 (6021): 1199-1203. 10.1126/science.1200609
36. Kato H. Goto D.B. Martienssen R.A. Urano T. Furukawa K. Murakami Y. 2005. RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science, 309 (5733): 467-469. 10.1126/science.1114955 (Pubitemid 40994685)
37. Kernohan K.D. Jiang Y. Tremblay D.C. Bonvissuto A.C. Eubanks J.H. Mann M.R. Bérubé N.G. 2010. ATRX partners with cohesin and MeCP2 and contributes to developmental silencing of imprinted genes in the brain. Dev. Cell, 18 (2): 191-202. 10.1016/j.devcel.2009.12.017
38. Kourmouli N. Sun Y.M. van der Sar S. Singh P.B. Brown J.P. 2005. Epigenetic regulation of mammalian pericentric heterochromatin in vivo by HP1. Biochem. Biophys. Res. Commun. 337 (3): 901-907. 10.1016/j.bbrc.2005.09.132 (Pubitemid 41446999)
39. Kwon Y. Seong C. Chi P. Greene E.C. Klein H. Sung P. 2008. ATP-dependent chromatin remodeling by the Saccharomyces cerevisiae homologous recombination factor Rdh54. J. Biol. Chem. 283 (16): 10445-10452. 10.1074/jbc.M800082200
40. Law M.J. Lower K.M. Voon H.P. Hughes J.R. Garrick D. Viprakasit V. et al. 2010. ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell, 143 (3): 367-378. 10.1016/j.cell.2010.09.023
41. Le Douarin B. Nielsen A.L. Garnier J.M. Ichinose H. Jeanmougin F. Losson R. Chambon P. 1996. A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. EMBO J. 15: 6701-6715. (Pubitemid 26413802)
42. Lechner M.S. Schultz D.C. Negorev D. Maul G.G. Rauscher F.J. 3rd. 2005. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem. Biophys. Res. Commun. 331 (4): 929-937. 10.1016/j.bbrc.2005.04.016 (Pubitemid 40692450)
43. Lencz T. Morgan T.V. Athanasiou M. Dain B. Reed C.R. Kane J.M. et al. 2007. Converging evidence for a pseudoautosomal cytokine receptor gene locus in schizophrenia. Mol. Psychiatry, 12 (6): 572-580. 10.1038/sj.mp.4001983 (Pubitemid 46816774)
44. Levy M.A. Fernandes A.D. Tremblay D.C. Seah C. Bérubé N.G. 2008. The SWI/SNF protein ATRX co-regulates pseudoautosomal genes that have translocated to autosomes in the mouse genome. BMC Genomics, 9 (1): 468. 10.1186/1471-2164-9-468
45. Lewis P.W. Elsaesser S.J. Noh K.M. Stadler S.C. 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. U.S.A. 107 (32): 14075-14080. 10.1073/pnas.1008850107
46. Li S. Overman J.J. Katsman D. Kozlov S.V. Donnelly C.J. Twiss J.L. et al. 2010. An age-related sprouting transcriptome provides molecular control of axonal sprouting after stroke. Nat. Neurosci. 13 (12): 1496-1504. 10.1038/nn.2674
47. Loe-Mie Y. Lepagnol-Bestel A.M. Maussion G. Doron-Faigenboim A. Imbeaud S. Delacroix H. et al. 2010. SMARCA2 and other genome-wide supported schizophrenia-associated genes: regulation by REST/NRSF, network organization and primate-specific evolution. Hum. Mol. Genet. 19 (14): 2841-2857. 10.1093/hmg/ddq184
48. McDowell T.L. Gibbons R.J. Sutherland H. O'Rourke D.M. Bickmore W.A. Pombo A. et al. 1999. Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc. Natl. Acad. Sci. U.S.A. 96 (24): 13983-13988. 10.1073/pnas.96.24.13983
49. Medina C.F. Mazerolle C. Wang Y. Bérubé N.G. Coupland S. Gibbons R.J. et al. 2009. Altered visual function and interneuron survival in Atrx knockout mice: inference for the human syndrome. Hum. Mol. Genet. 18: 966-977.
50. Nagao K. Adachi Y. Yanagida M. 2004. Separase-mediated cleavage of cohesin at interphase is required for DNA repair. Nature, 430 (7003): 1044-1048. 10.1038/nature02803 (Pubitemid 39128391)
51. Nan X. Hou J. Maclean A. Nasir J. Lafuente M.J. Shu X. et al. 2007. Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc. Natl. Acad. Sci. U.S.A. 104 (8): 2709-2714. 10.1073/pnas.0608056104 (Pubitemid 46327944)
52. Nogami T. Beppu H. Tokoro T. Moriguchi S. Shioda N. Fukunaga K. et al. 2010. Reduced expression of the ATRX gene, a chromatin-remodeling factor, causes hippocampal dysfunction in mice. Hippocampus, 21 (6): 678-687. 10.1002/hipo.20782
53. Picketts D.J. Higgs D.R. Bachoo S. Blake D.J. Quarrell O.W. Gibbons R.J. 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 (12): 1899-1907. 10.1093/hmg/5.12.1899 (Pubitemid 26413632)
54. Picketts D.J. Tastan A.O. Higgs D.R. Gibbons R.J. 1998. Comparison of the human and murine ATRX gene identifies highly conserved, functionally important domains. Mamm. Genome, 9 (5): 400-403. 10.1007/s003359900781 (Pubitemid 28259217)
55. Ritchie K. Seah C. Moulin J. Isaac C. Dick F. Bérubé N.G. 2008. Loss of ATRX leads to chromosome cohesion and congression defects. J. Cell Biol. 180 (2): 315-324. 10.1083/jcb.200706083 (Pubitemid 351185918)
56. Sandhu K.S. Shi C. Sjolinder M. Zhao Z. Gondor A. Liu L. et al. 2009. Nonallelic transvection of multiple imprinted loci is organized by the H19 imprinting control region during germline development. Genes Dev. 23 (22): 2598-2603. 10.1101/gad.552109
57. Schneiderman J.I. Sakai A. Goldstein S. Ahmad K. 2009. The XNP remodeler targets dynamic chromatin in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 106 (34): 14472-14477. 10.1073/pnas.0905816106
58. Seah C. Levy M.A. Jiang Y. Mokhtarzada S. Higgs D.R. Gibbons R.J. Bérubé N.G. 2008. Neuronal death resulting from targeted disruption of the Snf2 protein ATRX is mediated by p53. J. Neurosci. 28 (47): 12570-12580. 10.1523/JNEUROSCI.4048-08.2008
59. Serrano E. Lasa A. Perea G. Carnicer M.J. Brunet S. Aventin A. et al. 2006. Acute myeloid leukemia subgroups identified by pathway-restricted gene expression signatures. Acta Haematol. 116 (2): 77-89. 10.1159/000093636 (Pubitemid 44252762)
60. Shioda N. Beppu H. Fukuda T. Li E. Kitajima I. Fukunaga K. 2011. Aberrant Calcium/Calmodulin-Dependent Protein Kinase II (CaMKII) Activity Is Associated with Abnormal Dendritic Spine Morphology in the ATRX Mutant Mouse Brain. J. Neurosci. 31 (1): 346-358. 10.1523/JNEUROSCI.4816-10.2011
61. Solomon L.A. Li J.R. Bérubé N.G. Beier F. 2009. Loss of ATRX in chondrocytes has minimal effects on skeletal development. PLoS ONE, 4 (9): e7106. 10.1371/journal.pone.0007106
62. Steensma D.P. Higgs D.R. Fisher C.A. Gibbons R.J. 2004. Acquired somatic ATRX mutations in myelodysplastic syndrome associated with alpha thalassemia (ATMDS) convey a more severe hematologic phenotype than germline ATRX mutations. Blood, 103 (6): 2019-2026. 10.1182/blood-2003-09-3360 (Pubitemid 38326215)
63. Strom L. Lindroos H.B. Shirahige K. Sjogren C. 2004. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell, 16 (6): 1003-1015. 10.1016/j.molcel.2004.11.026 (Pubitemid 40018409)
64. Sun S. Wei J. Li H. Jin S. Li P. Ju G. et al. 2009. A family-based study of the IL3RA gene on susceptibility to schizophrenia in a Chinese Han population. Brain Res. 1268: 13-16. 10.1016/j.brainres.2009.02.071
65. Tang J. Wu S. Liu H. Stratt R. Barak O.G. Shiekhattar R. et al. 2004. A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J. Biol. Chem. 279 (19): 20369-20377. 10.1074/jbc.M401321200 (Pubitemid 38623483)
66. Wan L.B. Bartolomei M.S. 2008. Regulation of imprinting in clusters: noncoding RNAs versus insulators. Adv. Genet. 61: 207-223. 10.1016/S0065- 2660(07)00007-7
67. Weatherall D.J. Higgs D.R. Bunch C. Old J.M. Hunt D.M. Pressley L. et al. 1981. Hemoglobin H disease and mental retardation: a new syndrome or a remarkable coincidence? N. Engl. J. Med. 305 (11): 607-612. 10.1056/ NEJM198109103051103 (Pubitemid 12201112)
68. Wendt K.S. Yoshida K. Itoh T. Bando M. Koch B. Schirghuber E. et al. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature, 451 (7180): 796-801. 10.1038/nature06634 (Pubitemid 351253176)
69. Wong L.H. McGhie J.D. Sim M. Anderson M.A. Ahn S. Hannan R.D. et al. 2010. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 20 (3): 351-360. 10.1101/gr.101477.109
70. Xie S. Wang Z. Okano M. Nogami M. Li Y. He W.W. et al. 1999. Cloning, expression and chromosome locations of the human DNMT3 gene family. Gene, 236 (1): 87-95. 10.1016/S0378-1119(99)00252-8 (Pubitemid 29347034)
71. Xue Y. Gibbons R. Yan Z. Yang D. McDowell T.L. Sechi S. et al. 2003. The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc. Natl. Acad. Sci. U.S.A. 100 (19): 10635-10640. 10.1073/pnas.1937626100 (Pubitemid 37140081)
72. Zhao Z. Tavoosidana G. Sjolinder M. Gondor A. Mariano P. Wang S. et al. 2006. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra-and interchromosomal interactions. Nat. Genet. 38 (11): 1341-1347. 10.1038/ng1891 (Pubitemid 44646299)