ATRX promotes gene expression by facilitating transcriptional elongation through guanine-rich coding regions

Human Molecular Genetics

Volumn 24, Issue 7, 2014, Pages 1824-1835

  Levy, Michael A ^a,b   Kernohan, Kristin D ^a,b   Jiang, Yan ^a,b   Bérubé, Nathalie G ^a,b  

^a WESTERN UNIVERSITY   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; GUANINE; GUANINE QUADRUPLEX; HISTONE H3; HISTONE H3.3; PROTEIN ATRX; RNA POLYMERASE II; TELOMERASE; UNCLASSIFIED DRUG; ATRX PROTEIN, MOUSE; CHROMATIN; DNA HELICASE; HISTONE; NUCLEAR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATRX GENE; BINDING SITE; COGNITIVE DEFECT; CONNECTOME; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; DNA STRUCTURE; EMBRYO; FOREBRAIN; GENE; GENE EXPRESSION; GENE MUTATION; HETEROCHROMATIN; HISTONE MODIFICATION; MOUSE; NEUROLIGIN 4 GENE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION ELONGATION; TRANSCRIPTION REGULATION; ALPHA THALASSEMIA; ANIMAL; CHROMATIN; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; MUTATION; OPEN READING FRAME; X LINKED MENTAL RETARDATION;

ALPHA-THALASSEMIA; ANIMALS; CHROMATIN; DNA HELICASES; DNA METHYLATION; G-QUADRUPLEXES; GENE EXPRESSION REGULATION; GUANINE; HISTONES; HUMANS; MALE; MENTAL RETARDATION, X-LINKED; MICE; MICE, KNOCKOUT; MUTATION; NUCLEAR PROTEINS; OPEN READING FRAMES; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84926480208     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu596     Document Type: Article

References (72)

1. Baumann, C. and 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.
2. McDowell, T.L., Gibbons, R.J., Sutherland, H., O'Rourke, D.M., Bickmore, W.A., Pombo, A., Turley, H., Gatter, K., Picketts, D.J., Buckle, V.J. et al. (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.
3. Law, M.J., Lower, K.M., Voon, H.P., Hughes, J.R., Garrick, D., Viprakasit, V., Mitson, M., De Gobbi, M., Marra, M., Morris, A. et al. (2010) ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell, 143, 367-378.
4. Watson, L.A., Solomon, L.A., Li, J.R., Jiang, Y., Edwards, M., Shin-ya, K., Beier, F. and Berube, N.G. (2013) Atrx deficiency induces telomere dysfunction, endocrine defects, and reduced life span. J. Clin. Invest., 123, 2049-2063.
5. 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.
6. 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.
7. Wong, L.H., McGhie, J.D., Sim, M., Anderson, M.A., Ahn, S., Hannan, R.D., George, A.J., Morgan, K.A., Mann, J.R. and Choo, K.H. (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res., 20, 351-360.
8. Duquette, M.L., Handa, P., Vincent, J.A., Taylor, A.F. and Maizels, N. (2004) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev., 18, 1618-1629.
9. Biffi, G., Tannahill, D., McCafferty, J. and Balasubramanian, S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat. Chem., 5, 182-186.
10. Clynes, D. and Gibbons, R.J. (2013) ATRX and the replication of structured DNA. Curr. Opin. Genet. Dev., 23, 289-294.
11. Gibbons, R.J., Picketts, D.J., Villard, L. and Higgs, D.R. (1995) Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell, 80, 837-845.
12. Gibbons, R.J., McDowell, T.L., Raman, S., O'Rourke, D.M., Garrick, D., Ayyub, H. and 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, 368-371.
13. Heaphy, C.M., deWilde, R.F., Jiao, Y., Klein, A.P., Edil, B.H., Shi, C., Bettegowda, C., Rodriguez, F.J., Eberhart, C.G., Hebbar, S. et al. (2011) Altered telomeres in tumors with ATRX and DAXX mutations. Science, 333, 425.
14. Jiao, Y., Shi, C., Edil, B.H., deWilde, 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.
15. 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.
16. Schwartzentruber, J., Korshunov, A., Liu, X.Y., Jones, D.T., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A.M., Quang, D.A., Tonjes, M. et al. (2012) Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature, 482, 226-231.
17. Chen, X., Bahrami, A., Pappo, A., Easton, J., Dalton, J., Hedlund, E., Ellison, D., Shurtleff, S., Wu, G., Wei, L. et al. (2014) Recurrent somatic structural variations contribute to tumorigenesis in pediatric osteosarcoma. Cell Rep., 7, 104-112.
18. Qadeer, Z.A., Harcharik, S., Valle-Garcia, D., Chen, C., Birge, M. B., Vardabasso, C., Duarte, L.F. and Bernstein, E. (2014) Decreased expression of the chromatin remodeler ATRX associates with melanoma progression. J. Invest. Dermatol., 134, 1768-1772.
19. Cheung, N.K., Zhang, J., Lu, C., Parker, M., Bahrami, A., Tickoo, S.K., Heguy, A., Pappo, A.S., Federico, S., Dalton, J. et al. (2012) Association of age at diagnosis and genetic mutations in patients with neuroblastoma. JAMA, 307, 1062-1071.
20. de Wilde, R.F., Heaphy, C.M., Maitra, A., Meeker, A.K., Edil, B. H.,Wolfgang, C.L., Ellison, T.A., Schulick, R.D., Molenaar, I.Q., Valk, G.D. et al. (2012) Loss of ATRX or DAXX expression and concomitant acquisition of the alternative lengthening of telomeres phenotype are late events in a small subset of MEN-1 syndrome pancreatic neuroendocrine tumors. Mod. Pathol., 25, 1033-1039.
21. Lovejoy, C.A., Li,W., Reisenweber, S., Thongthip, S., Bruno, J., de Lange, T., De, S., Petrini, J.H., 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.
22. Gibbons, R.J. and Higgs, D.R. (2010) ATRX: taming tandem repeats. Cell Cycle, 9, 4605-4606.
23. Leung, J.W., Ghosal, G.,Wang,W., Shen, X.,Wang, J., Li, L. and Chen, J. (2013) Alpha Thalassemia/Mental Retardation Syndrome X-linked gene product ATRX is required for proper replication restart and cellular resistance to replication stress. J. Biol. Chem., 288, 6342-6350.
24. Ratnakumar, K., Duarte, L.F., LeRoy, G., Hasson, D., Smeets, D., Vardabasso, C., Bonisch, C., Zeng, T., Xiang, B., Zhang,D.Y. et al. (2012) ATRX-mediated chromatin association of histone variant macroH2A1 regulates alpha-globin expression. Genes Dev., 26, 433-438.
25. Bagheri-Fam, S., Argentaro, A., Svingen, T., Combes, A.N., Sinclair, A.H., Koopman, P. and 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, 2213-2224.
26. Kernohan, K.D., Jiang, Y., Tremblay, D.C., Bonvissuto, A.C., Eubanks, J.H., Mann, M.R. and Berube, N.G. (2010) ATRX partners with cohesin and MeCP2 and contributes to developmental silencing of imprinted genes in the brain. Dev. Cell, 18, 191-202.
27. Kernohan, K.D., Vernimmen, D., Gloor, G.B. and Berube, N.G. (2014) Analysis of neonatal brain lacking ATRX or MeCP2 reveals changes in nucleosome density, CTCF binding and chromatin looping. Nucleic Acids Res., 42, 8356-8368.
28. Levy, M.A., Fernandes, A.D., Tremblay, D.C., Seah, C. and Berube, N.G. (2008) The SWI/SNF protein ATRX co-regulates pseudoautosomal genes that have translocated to autosomes in the mouse genome. BMC Genomics, 9, 468.
29. Katsura, Y., Iwase, M. and Satta, Y. (2012) Evolution of genomic structures on Mammalian sex chromosomes. Curr. Genomics, 13, 115-123.
30. Gianfrancesco, F., Sanges, R., Esposito, T., Tempesta, S., Rao, E., Rappold, G., Archidiacono, N., Graves, J.A.M., Forabosco, A. and D'Urso, M. (2001) Differential divergence of three human pseudoautosomal genes and their mouse homologs:implications for sex chromosome evolution. Genome Res., 11, 2095-2100.
31. Mural, R.J., Adams, M.D., Myers, E.W., Smith, H.O., Miklos, G. L.,Wides, R., Halpern, A., Li, P.W., Sutton, G.G., Nadeau, J. et al. (2002) A comparison of whole-genome shotgun-derived mouse chromosome 16 and the human genome. Science, 296, 1661-1671.
32. Scaife, R.M. (2005) Selective and irreversible cell cycle inhibition by diphenyleneiodonium. Mol. Cancer Ther., 4, 876-884.
33. Bérubé, N.G., Mangelsdorf, M., Jagla, M., Vanderluit, J., Garrick, D., Gibbons, R.J., Higgs, D.R., Slack, R.S. and Picketts, D. J. (2005) The chromatin-remodeling protein ATRX is critical for neuronal survival during corticogenesis. J. Clin. Invest., 115, 258-267.
34. Azzalin, C.M., Reichenbach, P., Khoriauli, L., Giulotto, E. and Lingner, J. (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science, 318, 798-801.
35. Schoeftner, S. and Blasco, M.A. (2008) Developmentally regulated transcription of mammalian telomeres by DNAdependent RNA polymerase II. Nat. Cell Biol., 10, 228-236.
36. Deng, Z., Norseen, J., Wiedmer, A., Riethman, H. and Lieberman, P.M. (2009) TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell, 35, 403-413.
37. Gottschling, D.E., Aparicio, O.M., Billington, B.L. and Zakian, V.A. (1990) Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell, 63, 751-762.
38. Pedram, M., Sprung, C.N., Gao, Q., Lo, A.W., Reynolds, G.E. and Murnane, J.P. (2006) Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol. Cell. Biol., 26, 1865-1878.
39. Baur, J.A., Zou, Y., Shay, J.W. andWright,W.E. (2001) Telomere position effect in human cells. Science, 292, 2075-2077.
40. Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. (2007) Highresolution profiling of histone methylations in the human genome. Cell, 129, 823-837.
41. Wang, Z., Zang, C., Rosenfeld, J.A., Schones, D.E., Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Peng, W., Zhang, M.Q. et al. (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet., 40, 897-903.
42. Liang, G., Lin, J.C., Wei, V., Yoo, C., Cheng, J.C., Nguyen, C.T., Weisenberger, D.J., Egger, G., Takai, D., Gonzales, F.A. et al. (2004) Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc. Natl Acad. Sci. USA, 101, 7357-7362.
43. Jamain, S., Quach, H., Betancur, C., Rastam, M., Colineaux, C., Gillberg, I.C., Soderstrom, H., Giros, B., Leboyer, M., Gillberg, C. et al. (2003) Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet., 34, 27-29.
44. Laumonnier, F., Bonnet-Brilhault, F., Gomot, M., Blanc, R., David, A., Moizard, M.P., Raynaud, M., Ronce, N., Lemonnier, E., Calvas, P. et al. (2004) X-linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family. Am. J. Hum. Genet., 74, 552-557.
45. Ylisaukko-oja, T., Rehnstrom, K., Auranen, M., Vanhala, R., Alen, R., Kempas, E., Ellonen, P., Turunen, J.A., Makkonen, I., Riikonen, R. et al. (2005) Analysis of four neuroligin genes as candidates for autism. Eur. J. Hum. Genet., 13, 1285-1292.
46. Bolliger, M.F., Pei, J., Maxeiner, S., Boucard, A.A., Grishin, N.V. and Sudhof, T.C. (2008) Unusually rapid evolution of Neuroligin-4 in mice. Proc. Natl Acad. Sci. USA., 105, 6421-6426.
47. Ivanauskiene, K., Delbarre, E., McGhie, J.D., Kuntziger, T., Wong, L.H. and Collas, P. (2014) The PML-associated protein DEK regulates the balance of H3.3 loading on chromatin and is important for telomere integrity. Genome Res., 24, 1584-1594.
48. Garrick, D., Sharpe, J.A., Arkell, R., Dobbie, L., Smith, A.J., Wood, W.G., Higgs, D.R. and Gibbons, R.J. (2006) Loss of Atrx affects trophoblast development and the pattern of X-inactivation in extraembryonic tissues. PLoS Genet., 2, e58.
49. Ahmad, K. and Henikoff, S. (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell, 9, 1191-1200.
50. Schwartz, B.E. and Ahmad, K. (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev., 19, 804-814.
51. Henikoff, S. (2008) Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. Genet., 9, 15-26.
52. Siddiqui-Jain, A., Grand, C.L., Bearss, D.J. and Hurley, L.H. (2002) Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc. Natl Acad. Sci. USA, 99, 11593-11598.
53. Eddy, J., Vallur, A.C., Varma, S., Liu, H., Reinhold, W.C., Pommier, Y. and Maizels, N. (2011) G4 motifs correlate with promoter-proximal transcriptional pausing in human genes. Nucleic Acids Res., 39, 4975-4983.
54. Skourti-Stathaki, K., Proudfoot, N.J. and Gromak, N. (2011) Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol. Cell, 42, 794-805.
55. Perrone, R., Nadai, M., Poe, J.A., Frasson, I., Palumbo, M., Palu, G., Smithgall, T.E. and Richter, S.N. (2013) Formation of a unique cluster of G-quadruplex structures in the HIV-1 Nef coding region: implications for antiviral activity. PLoS ONE, 8, e73121.
56. Broxson, C., Beckett, J. and Tornaletti, S. (2011) Transcription arrest by a G quadruplex forming-trinucleotide repeat sequence from the human c-myb gene. Biochemistry, 50, 4162-4172.
57. Clynes, D., Jelinska, C., Xella, B., Ayyub, H., Taylor, S., Mitson, M., Bachrati, C.Z., Higgs, D.R. and Gibbons, R.J. (2014) ATRX dysfunction induces replication defects in primary mouse cells. PLoS ONE, 9, e92915.
58. Ellison, J., Franckle, L.U. and LJ, S. (1996) Rapid evolution of human pseudoautosomal genes and their mouse homologs. Mamm. Genome, 7, 25-30.
59. Perry, J., Palmer, S., Gabriel, A. and Ashworth, A. (2001) Ashort pseudoautosomal region in laboratory mice. Genome Res., 11, 1826-1832.
60. Hoon, M., Soykan, T., Falkenburger, B., Hammer, M., Patrizi, A., Schmidt, K.F., Sassoe-Pognetto, M., Lowel, S., Moser, T., Taschenberger, H. et al. (2011) Neuroligin-4 is localized to glycinergic postsynapses and regulates inhibition in the retina. Proc. Natl Acad. Sci. USA, 108, 3053-3058.
61. Jamain, S., Radyushkin, K., Hammerschmidt, K., Granon, S., Boretius, S., Varoqueaux, F., Ramanantsoa, N., Gallego, J., Ronnenberg, A., Winter, D. et al. (2008) Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc. Natl Acad. Sci. USA, 105, 1710-1715.
62. Chih, B., Afridi, S.K., Clark, L. and Scheiffele, P. (2004) Disorder-associated mutations lead to functional inactivation of neuroligins. Hum. Mol. Genet., 13, 1471-1477.
63. 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.
64. Seah, C., Levy, M.A., Jiang, Y., Mokhtarzada, S., Higgs, D.R., Gibbons, R.J. and Berube, N.G. (2008) Neuronal death resulting from targeted disruption of the Snf2 protein ATRX is mediated by p53. J. Neurosci., 28, 12570-12580.
65. Zhang, L.F., Ogawa, Y., Ahn, J.Y., Namekawa, S.H., Silva, S.S. and Lee, J.T. (2009) Telomeric RNAs mark sex chromosomes in stem cells. Genetics, 182, 685-698.
66. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 9, 671-675.
67. Market-Velker, B.A., Zhang, L., Magri, L.S., Bonvissuto, A.C. and Mann, M.R. (2010) Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dosedependent manner. Hum. Mol. Genet., 19, 36-51.
68. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
69. Kent,W.J., Sugnet, C.W., Furey, T.S., Roskin, K.M., Pringle, T.H., Zahler, A.M. and Haussler, D. (2002) The human genome browser at UCSC. Genome Res., 12, 996-1006.
70. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W. et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, R137.
71. Day, D.S., Luquette, L.J., Park, P.J. and Kharchenko, P.V. (2010) Estimating enrichment of repetitive elements from highthroughput sequence data. Genome Biol., 11, R69.
72. Scaria, V., Hariharan, M., Arora, A. and Maiti, S. (2006) Quadfinder:server for identification and analysis of quadruplexforming motifs in nucleotide sequences. Nucleic Acids Res., 34, W683-W685.