ATRX: The case of a peculiar chromatin remodeler

Epigenetics

Volumn 8, Issue 1, 2013, Pages 3-9

  Ratnakumar, Kajan ^a   Bernstein, Emily ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

ATRX; Histone variants; MacroH2A and H3.3; Telomeres; globin

Indexed keywords

CHAPERONE; DAXX PROTEIN; GUANINE QUADRUPLEX; HEMOGLOBIN ALPHA CHAIN; HISTONE H3; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR EZH2;

ALPHA THALASSEMIA; ARTICLE; ARTX GENE; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; DNA HISTONE INTERACTION; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; HETEROCHROMATIN; HUMAN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; TELOMERE; TRANSCRIPTION REGULATION;

EID: 84872041957     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.23271     Document Type: Article

References (57)

1. Gibbons RJ, Wilkie AO, Weatherall DJ, Higgs DR. A newly defined X linked mental retardation syndrome associated with alpha thalassaemia. J Med Genet 1991; 28:729-33; PMID:1770527; http://dx.doi. org/10.1136/jmg.28.11.729.
2. Stayton CL, Dabovic B, Gulisano M, Gecz J, Broccoli V, Giovanazzi S, et al. Cloning and characterization of a new human Xq13 gene, encoding a putative helicase. Hum Mol Genet 1994; 3:1957-64; PMID:7874112; http://dx.doi.org/10.1093/ hmg/3.11.1957.
3. Aapola U, Kawasaki K, Scott HS, Ollila J, Vihinen M, Heino M, et al. Isolation and initial characterization of a novel zinc finger gene, DNMT3L, on 21q22.3, related to the cytosine-5-methyltransferase 3 gene family. Genomics 2000; 65:293-8; PMID:10857753; http://dx.doi.org/10.1006/ geno.2000.6168.
4. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 2007; 14:1025-40; PMID:17984965; http://dx.doi.org/10.1038/ nsmb1338.
5. Baker LA, Allis CD, Wang GG. PHD fingers in human diseases: disorders arising from misinterpreting epigenetic marks. Mutat Res 2008; 647:3-12; PMID:18682256; http://dx.doi.org/10.1016/j. mrfmmm.2008.07.004.
6. Argentaro A, Yang JC, Chapman L, Kowalczyk MS, Gibbons RJ, Higgs DR, et al. Structural consequences of disease-causing mutations in the ATRXDNMT3-DNMT3L (ADD) domain of the chromatin-associated protein ATRX. Proc Natl Acad Sci U S A 2007; 104:11939-44; PMID:17609377; http:// dx.doi.org/10.1073/pnas.0704057104.
7. Gibbons RJ, McDowell TL, Raman S, O'Rourke DM, Garrick D, Ayyub H, et al. Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat Genet 2000; 24:368-71; PMID:10742099; http:// dx.doi.org/10.1038/74191.
8. Picketts DJ, Higgs DR, Bachoo S, Blake DJ, Quarrell OW, Gibbons RJ. 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 1996; 5:1899-907; PMID:8968741; http://dx.doi.org/10.1093/ hmg/5.12.1899.
9. Smith CL, Peterson CL. ATP-dependent chromatin remodeling. Curr Top Dev Biol 2005; 65:115-48; PMID:15642381; http://dx.doi.org/10.1016/S0070-2153(04)65004-6.
10. Higgs DR, Garrick D, Anguita E, De Gobbi M, Hughes J, Muers M, et al. Understanding alphaglobin gene regulation: Aiming to improve the management of thalassemia. Ann N Y Acad Sci 2005; 1054:92-102; PMID:16339655; http://dx.doi. org/10.1196/annals.1345.012.
11. Gibbons R. Alpha thalassaemia-mental retardation, X linked. Orphanet J Rare Dis 2006; 1:15; PMID:16722615; http://dx.doi.org/10.1186/1750-1172-1-15.
12. Law MJ, Lower KM, Voon HP, Hughes JR, Garrick D, Viprakasit V, et al. ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 2010; 143:367-78; PMID:21029860; http://dx.doi. org/10.1016/j.cell.2010.09.023.
13. McDowell TL, Gibbons RJ, Sutherland H, O'Rourke DM, Bickmore WA, Pombo A, et al. Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc Natl Acad Sci U S A 1999; 96:13983-8; PMID:10570185; http://dx.doi. org/10.1073/pnas.96.24.13983.
14. Wong LH, McGhie JD, Sim M, Anderson MA, Ahn S, Hannan RD, et al. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 2010; 20:351-60; PMID:20110566; http://dx.doi. org/10.1101/gr.101477.109.
15. Baumann C, De La Fuente R. ATRX marks the inactive X chromosome (Xi) in somatic cells and during imprinted X chromosome inactivation in trophoblast stem cells. Chromosoma 2009; 118:209-22; PMID:19005673; http://dx.doi.org/10.1007/ s00412-008-0189-x.
16. Lechner MS, Schultz DC, Negorev D, Maul GG, Rauscher FJ 3rd. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem Biophys Res Commun 2005; 331:929-37; PMID:15882967; http://dx.doi. org/10.1016/j.bbrc.2005.04.016.
17. Cardoso C, Timsit S, Villard L, Khrestchatisky M, Fontès M, Colleaux L. Specific interaction between the XNP/ATR-X gene product and the SET domain of the human EZH2 protein. Hum Mol Genet 1998; 7:679-84; PMID:9499421; http://dx.doi. org/10.1093/hmg/7.4.679.
18. Kernohan KD, Jiang Y, Tremblay DC, Bonvissuto AC, Eubanks JH, Mann MR, et al. ATRX partners with cohesin and MeCP2 and contributes to developmental silencing of imprinted genes in the brain. Dev Cell 2010; 18:191-202; PMID:20159591; http:// dx.doi.org/10.1016/j.devcel.2009.12.017.
19. Ratnakumar K, Duarte LF, LeRoy G, Hasson D, Smeets D, Vardabasso C, et al. ATRX-mediated chromatin association of histone variant macro-H2A1 regulates α-globin expression. Genes Dev 2012; 26:433-8; PMID:22391447; http://dx.doi. org/10.1101/gad.179416.111.
20. Nan X, Hou J, Maclean A, Nasir J, Lafuente MJ, Shu X, et al. Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc Natl Acad Sci U S A 2007; 104:2709-14; PMID:17296936; http://dx.doi.org/10.1073/pnas.0608056104.
21. Iwase S, Xiang B, Ghosh S, Ren T, Lewis PW, Cochrane JC, et al. ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome. Nat Struct Mol Biol 2011; 18:769-76; PMID:21666679; http:// dx.doi.org/10.1038/nsmb.2062.
22. Dhayalan A, Tamas R, Bock I, Tattermusch A, Dimitrova E, Kudithipudi S, et al. The ATRX-ADD domain binds to H3 tail peptides and reads the combined methylation state of K4 and K9. Hum Mol Genet 2011; 20:2195-203; PMID:21421568; http:// dx.doi.org/10.1093/hmg/ddr107.
23. Eustermann S, Yang JC, Law MJ, Amos R, Chapman LM, Jelinska C, et al. Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nat Struct Mol Biol 2011; 18:777-82; PMID:21666677; http://dx.doi. org/10.1038/nsmb.2070.
24. Wong LH, Ren H, Williams E, McGhie J, Ahn S, Sim M, et al. Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res 2009; 19:404-14; PMID:19196724; http://dx.doi. org/10.1101/gr.084947.108.
25. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010; 140:678-91; PMID:20211137; http://dx.doi.org/10.1016/j.cell.2010.01.003.
26. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004; 116:51-61; PMID:14718166; http://dx.doi.org/10.1016/S0092-8674(03)01064-X.
27. Xue Y, Gibbons R, Yan Z, Yang D, McDowell TL, Sechi S, et al. 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 2003; 100:10635-40; PMID:12953102; http://dx.doi.org/10.1073/ pnas.1937626100.
28. Tang J, Wu S, Liu H, Stratt R, Barak OG, Shiekhattar R, et al. A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J Biol Chem 2004; 279:20369-77; PMID:14990586; http://dx.doi. org/10.1074/jbc.M401321200.
29. Drané P, Ouararhni K, Depaux A, Shuaib M, Hamiche A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 2010; 24:1253-65; PMID:20504901; http://dx.doi. org/10.1101/gad.566910.
30. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD. 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 2010; 107:14075-80; PMID:20651253; http:// dx.doi.org/10.1073/pnas.1008850107.
31. Elsässer SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ. DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 2012; 491:560-5; PMID:23075851; http://dx.doi.org/10.1038/ nature11608.
32. Liu CP, Xiong C, Wang M, Yu Z, Yang N, Chen P, et al. Structure of the variant histone H3.3-H4 heterodimer in complex with its chaperone DAXX. Nat Struct Mol Biol 2012; 19:1287-92; PMID:23142979; http://dx.doi.org/10.1038/nsmb.2439.
33. Elsässer SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ. DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 2012; 491:560-5; PMID:23075851; http://dx.doi.org/10.1038/ nature11608.
34. Rafalska-Metcalf IU, Powers SL, Joo LM, LeRoy G, Janicki SM. Single cell analysis of transcriptional activation dynamics. PLoS One 2010; 5:e10272; PMID:20422051; http://dx.doi.org/10.1371/journal. pone.0010272.
35. Newhart A, Rafalska-Metcalf IU, Yang T, Negorev DG, Janicki SM. Single cell analysis of Daxx and ATRX-dependent transcriptional repression. J Cell Sci 2012; In press; PMID:22976303; http://dx.doi. org/10.1242/jcs.110148.
36. Schneiderman JI, Sakai A, Goldstein S, Ahmad K. The XNP remodeler targets dynamic chromatin in Drosophila. Proc Natl Acad Sci U S A 2009; 106:14472-7; PMID:19706533; http://dx.doi. org/10.1073/pnas.0905816106.
37. Bassett AR, Cooper SE, Ragab A, Travers AA. The chromatin remodelling factor dATRX is involved in heterochromatin formation. PLoS One 2008; 3:e2099; PMID:18461125; http://dx.doi. org/10.1371/journal.pone.0002099.
38. Bell AC, West AG, Felsenfeld G. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 1999; 98:387-96; PMID:10458613; http://dx.doi.org/10.1016/S0092-8674(00)81967-4.
39. Gerasimova TI, Corces VG. Chromatin insulators and boundaries: effects on transcription and nuclear organization. Annu Rev Genet 2001; 35:193-208; PMID:11700282; http://dx.doi.org/10.1146/ annurev.genet.35.102401.090349.
40. Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, Zhao K. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res 2009; 19:24-32; PMID:19056695; http://dx.doi.org/10.1101/gr.082800.108.
41. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, et al. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev 2006; 20:2349-54; PMID:16951251; http://dx.doi.org/10.1101/ gad.399506.
42. Gamble MJ, Frizzell KM, Yang C, Krishnakumar R, Kraus WL. The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev 2010; 24:21-32; PMID:20008927; http://dx.doi. org/10.1101/gad.1876110.
43. Li G, Fullwood MJ, Xu H, Mulawadi FH, Velkov S, Vega V, et al. ChIA-PET tool for comprehensive chromatin interaction analysis with pairedend tag sequencing. Genome Biol 2010; 11:R22; PMID:20181287; http://dx.doi.org/10.1186/gb-2010-11-2-r22.
44. Liu XY, Gerges N, Korshunov A, Sabha N, Khuong-Quang DA, Fontebasso AM, et al. Frequent ATRX mutations and loss of expression in adult diffuse astrocytic tumors carrying IDH1/IDH2 and TP53 mutations. Acta Neuropathol 2012; 124:615-25; PMID:22886134; http://dx.doi.org/10.1007/ s00401-012-1031-3.
45. Jiao Y, Shi C, Edil BH, de Wilde RF, Klimstra DS, Maitra A, et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 2011; 331:1199-203; PMID:21252315; http://dx.doi.org/10.1126/ science.1200609.
46. Steensma DP, Higgs DR, Fisher CA, Gibbons RJ. Acquired somatic ATRX mutations in myelodysplastic syndrome associated with alpha thalassemia (ATMDS) convey a more severe hematologic phenotype than germline ATRX mutations. Blood 2004; 103:2019-26; PMID:14592816; http://dx.doi. org/10.1182/blood-2003-09-3360.
47. Jiao Y, Killela PJ, Reitman ZJ, Rasheed AB, Heaphy CM, de Wilde RF, et al. Frequent ATRX, CIC, and FUBP1 mutations refine the classification of malignant gliomas. Oncotarget 2012; 3:709-22; PMID:22869205.
48. Gibbons RJ, Pellagatti A, Garrick D, Wood WG, Malik N, Ayyub H, et al. Identification of acquired somatic mutations in the gene encoding chromatinremodeling factor ATRX in the alpha-thalassemia myelodysplasia syndrome (ATMDS). Nat Genet 2003; 34:446-9; PMID:12858175; http://dx.doi. org/10.1038/ng1213.
49. Cheung NK, Zhang J, Lu C, Parker M, Bahrami A, Tickoo SK, et al.; St Jude Children's Research Hospital-Washington University Pediatric Cancer Genome Project. Association of age at diagnosis and genetic mutations in patients with neuroblastoma. JAMA 2012; 307:1062-71; PMID:22416102; http:// dx.doi.org/10.1001/jama.2012.228.
50. Schwartzentruber J, Korshunov A, Liu XY, Jones DT, Pfaff E, Jacob K, et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 2012; 482:226-31; PMID:22286061; http://dx.doi.org/10.1038/ nature10833.
51. Molenaar JJ, Koster J, Zwijnenburg DA, van Sluis P, Valentijn LJ, van der Ploeg I, et al. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 2012; 483:589-93; PMID:22367537; http://dx.doi.org/10.1038/ nature10910.
52. Gibbons RJ. α-Thalassemia, mental retardation, and myelodysplastic syndrome. Cold Spring Harb Perspect Med 2012; 2: In press; PMID:23028133.
53. Ritchie K, Seah C, Moulin J, Isaac C, Dick F, Bérubé NG. Loss of ATRX leads to chromosome cohesion and congression defects. J Cell Biol 2008; 180:315-24; PMID:18227278; http://dx.doi.org/10.1083/ jcb.200706083.
54. Heaphy CM, de Wilde RF, Jiao Y, Klein AP, Edil BH, Shi C, et al. Altered telomeres in tumors with ATRX and DAXX mutations. Science 2011; 333:425; PMID:21719641; http://dx.doi.org/10.1126/science.1207313.
55. Bérubé NG, Smeenk CA, Picketts DJ. Cell cycledependent phosphorylation of the ATRX protein correlates with changes in nuclear matrix and chromatin association. Hum Mol Genet 2000; 9:539-47; PMID:10699177; http://dx.doi.org/10.1093/ hmg/9.4.539.
56. Degner SC, Verma-Gaur J, Wong TP, Bossen C, Iverson GM, Torkamani A, et al. CCCTC-binding factor (CTCF) and cohesin influence the genomic architecture of the Igh locus and antisense transcription in pro-B cells. Proc Natl Acad Sci U S A 2011; 108:9566-71; PMID:21606361; http://dx.doi. org/10.1073/pnas.1019391108.
57. Benz EJ Jr., Murnane MJ, Tonkonow BL, Berman BW, Mazur EM, Cavallesco C, et al. Embryonicfetal erythroid characteristics of a human leukemic cell line. Proc Natl Acad Sci U S A 1980; 77:3509-13; PMID:6932034; http://dx.doi.org/10.1073/ pnas.77.6.3509.