Altered primary chromatin structures and their implications in cancer development

Cellular Oncology

Volumn 39, Issue 3, 2016, Pages 195-210

  Ferraro, Angelo ^a,b  

^a KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^b NATIONAL TECHNICAL UNIVERSITY OF ATHENS   (Greece)

Author keywords

Cancer; Chromatin remodeling; Epigenetics; Histone modifications; Histone variants; Nucleosomes

Indexed keywords

ARGININE; BIOLOGICAL MARKER; BMI1 PROTEIN; CENTROMERE PROTEIN A; CHROMODOMAIN HELICASE DNA BINDING PROTEIN; CYCLOOXYGENASE 2; DNA; DNA BINDING PROTEIN; GLUTAMIC ACID; HELICASE LYMPHOID SPECIFIC PROTEIN; HISTONE; HISTONE H1; HISTONE H2A; HISTONE H2AX; HISTONE H2AZ; HISTONE H3; HISTONE H3T; HISTONE H3X; HISTONE H3Y; IMITATION SWITCHING DEFECTIVE PROTEIN; INOSITOL REQUIRING 80 PROTEIN; LYSINE; POLYCOMB REPRESSIVE COMPLEX 2; PROLINE; RNA POLYMERASE II; SWI SNF RELATED MATRIX ASSOCIATED ACTIN DEPENDENT REGULATOR OF CHROMATIN SUBFAMILY A CONTAINING DEAD H BOX 1 PROTEIN; SWITCHING DEFECTIVE SUCROSE NON FERMENTING PROTEIN; TATA BINDING PROTEIN; THREONINE; UNCLASSIFIED DRUG; UNTRANSLATED RNA; CHROMATIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; CANCER DIAGNOSIS; CANCER GENETICS; CANCER GROWTH; CANCER PREVENTION; CANCER STAGING; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; COLONY FORMING UNIT; CONFORMATIONAL TRANSITION; DNA BINDING; DNA REPAIR; DNA REPLICATION; DNA STRAND; DOWN REGULATION; ENHANCER REGION; EPIGENETICS; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; HETEROZYGOSITY LOSS; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE PHOSPHORYLATION; HISTONE UBIQUITINATION; ISOMERIZATION; MUTATION RATE; NUCLEOSOME; ONCOGENE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONFORMATION; REVIEW; SUMOYLATION; TRANSCRIPTION INITIATION; TRANSCRIPTION TERMINATION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; ANIMAL; CELL TRANSFORMATION; CHROMATIN; GENETIC EPIGENESIS; GENETICS; HUMAN; NEOPLASM; PATHOLOGY;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN; EPIGENESIS, GENETIC; HUMANS; NEOPLASMS;

EID: 84961784548     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-016-0276-6     Document Type: Review

References (163)

1. M.B. Dhiab, S. Ziadi, S. Mestiri, R.B. Gacem, F. Ksiaa, M. Trimeche, DNA methylation patterns in EBV-positive and EBV-negative Hodgkin lymphomas. Cell. Oncol. 38, 453–462 (2015)
2. C.B. Moelans, E.J. Vlug, C. Ercan, P. Bult, H. Buerger, G. Cserni, P.J. van Diest, P.W. Derksen, Methylation biomarkers for pleomorphic lobular breast cancer – a short report. Cell. Oncol. 38, 397–405 (2015)
3. Y. You, W. Yang, X. Qin, F. Wang, H. Li, C. Lin, W. Li, C. Gu, Y. Zhang, Y. Ran, ECRG4 acts as a tumor suppressor and as a determinant of chemotherapy resistance in human nasopharyngeal carcinoma. Cell. Oncol. 38, 205–214 (2015)
4. C. Charfi, E. Edouard, E. Rassart, Identification of GPM6A and GPM6B as potential new human lymphoid leukemia-associated oncogenes. Cell. Oncol. 37, 179–191 (2014)
5. C. Yu, M. Wang, Z. Li, J. Xiao, F. Peng, X. Guo, Y. Deng, J. Jiang, C. Sun, MicroRNA-138-5p regulates pancreatic cancer cell growth through targeting FOXC1. Cell. Oncol. 38, 173–1781 (2015)
6. A. Valouev, S.M. Johnson, S.D. Boyd, C.L. Smith, A.Z. Fire, A. Sidow, Determinants of nucleosome organization in primary human cells. Nature 474, 516–520 (2011)
7. E. Segal, J. Widom, What controls nucleosome positions? Trends Genet. 25, 335–343 (2009)
8. P.B. Becker, W. Horz, ATP-dependent nucleosome remodeling. Annu. Rev. Biochem. 71, 247–273 (2002)
9. A. Flaus, D.M. Martin, G.J. Barton, T. Owen-Hughes, Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res. 34, 2887–2905 (2006)
10. C.B. Gerhold, S.M. Gasser, INO80 and SWR complexes: relating structure to function in chromatin remodeling. Trends Cell Biol. 24, 619–631 (2014)
11. C.R. Clapier, B.R. Cairns, The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273–304 (2009)
12. D.C. Hargreaves, G.R. Crabtree, ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21, 396–420 (2011)
13. Y. Cai, J. Jin, A.J. Gottschalk, T. Yao, J.W. Conaway, R.C. Conaway, Purification and assay of the human INO80 and SRCAP chromatin remodeling complexes. Methods 40, 312–317 (2006)
14. K. Dennis, T. Fan, T. Geiman, Q. Yan, K. Muegge, Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev. 15, 2940–2944 (2001)
15. S. Awad, D. Ryan, P. Prochasson, T. Owen-Hughes, A.H. Hassan, The Snf2 homolog Fun30 acts as a homodimeric ATP-dependent chromatin-remodeling enzyme. J. Biol. Chem. 285, 9477–9484 (2010)
16. T. Costelloe, R. Louge, N. Tomimatsu, B. Mukherjee, E. Martini, B. Khadaroo, K. Dubois, W.W. Wiegant, A. Thierry, S. Burma, H. van Attikum, B. Llorente, The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489, 581–584 (2012)
17. A. Gonzalez-Perez, A. Jene-Sanz, N. Lopez-Bigas, The mutational landscape of chromatin regulatory factors across 4,623 tumor samples. Genome Biol. 14, r106 (2013)
18. A.H. Shain, J.R. Pollack, The spectrum of SWI/SNF mutations, ubiquitous in human cancers. PLoS One 8, e55119 (2013)
19. J.A. Biegel, T.M. Busse, B.E. Weissman, SWI/SNF chromatin remodeling complexes and cancer. Am. J. Med. Genet. C: Semin. Med. Genet. 166, 350–366 (2014)
20. B.G. Wilson, X. Wang, X. Shen, E.S. McKenna, M.E. Lemieux, Y.J. Cho, E.C. Koellhoffer, S.L. Pomeroy, S.H. Orkin, C.W. Roberts, Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 18, 316–328 (2010)
21. T. Davoli, A.W. Xu, K.E. Mengwasser, L.M. Sack, J.C. Yoon, P.J. Park, S.J. Elledge, Cumulative haploinsufficiency and triplosensitivity drive aneuploidy patterns and shape the cancer genome. Cell 155, 948–962 (2013)
22. J. Clark, P.J. Rocques, A.J. Crew, S. Gill, J. Shipley, A.M. Chan, B.A. Gusterson, C.S. Cooper, Identification of novel genes, SYT and SSX, involved in the t(X;18)(p11.2;q11.2) translocation found in human synovial sarcoma. Nat. Genet. 7, 502–508 (1994)
23. M. Ladanyi, C.R. Antonescu, D.H. Leung, J.M. Woodruff, A. Kawai, J.H. Healey, M.F. Brennan, J.A. Bridge, J.R. Neff, F.G. Barr, J.D. Goldsmith, J.S. Brooks, J.R. Goldblum, S.Z. Ali, J. Shipley, C.S. Cooper, C. Fisher, B. Skytting, O. Larsson, Impact of SYT-SSX fusion type on the clinical behavior of synovial sarcoma: a multi-institutional retrospective study of 243 patients. Cancer Res. 62, 135–140 (2002)
24. Z. Jagani, E.L. Mora-Blanco, C.G. Sansam, E.S. McKenna, B. Wilson, D. Chen, J. Klekota, P. Tamayo, P.T. Nguyen, M. Tolstorukov, P.J. Park, Y.J. Cho, K. Hsiao, S. Buonamici, S.L. Pomeroy, J.P. Mesirov, H. Ruffner, T. Bouwmeester, S.J. Luchansky, J. Murtie, J.F. Kelleher, M. Warmuth, W.R. Sellers, C.W. Roberts, M. Dorsch, Loss of the tumor suppressor Snf5 leads to aberrant activation of the Hedgehog-Gli pathway. Nat. Med. 16, 1429–1433 (2010)
25. J. Caramel, F. Quignon, O. Delattre, RhoA-dependent regulation of cell migration by the tumor suppressor hSNF5/INI1. Cancer Res. 68, 6154–6161 (2008)
26. D.F. Corona, J.W. Tamkun, Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim. Biophys. Acta 1677, 113–119 (2004)
27. W. Dang, B. Bartholomew, Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol. Cell. Biol. 27, 8306–8317 (2007)
28. Y. Ye, Y. Xiao, W. Wang, Q. Wang, K. Yearsley, A.A. Wani, Q. Yan, J.X. Gao, B.S. Shetuni, S.H. Barsky, Inhibition of expression of the chromatin remodeling gene, SNF2L, selectively leads to DNA damage, growth inhibition, and cancer cell death. Mol. Cancer Res. 7, 1984–1999 (2009)
29. Q. Jin, X. Mao, B. Li, S. Guan, F. Yao, F. Jin, Overexpression of SMARCA5 correlates with cell proliferation and migration in breast cancer. Tumor Biol. 36, 1895–1902 (2015)
30. F.M. Fang, C.F. Li, H.Y. Huang, M.T. Lai, C.M. Chen, I.W. Chiu, T.L. Wang, F.J. Tsai, I.M. Shih, J.J. Sheu, Overexpression of a chromatin remodeling factor, RSF-1/HBXAP, correlates with aggressive oral squamous cell carcinoma. Am. J. Pathol. 178, 2407–2415 (2011)
31. J.J. Sheu, B. Guan, J.H. Choi, A. Lin, C.H. Lee, Y.T. Hsiao, T.L. Wang, F.J. Tsai, I.M. Shih, Rsf-1, a chromatin remodeling protein, induces DNA damage and promotes genomic instability. J. Biol. Chem. 285, 38260–38269 (2010)
32. J.J. Sheu, J.H. Choi, I. Yildiz, F.J. Tsai, Y. Shaul, T.L. Wang, I.M. Shih, The roles of human sucrose nonfermenting protein 2 homologue in the tumor-promoting functions of Rsf-1. Cancer Res. 68, 4050–4057 (2008)
33. I.M. Shih, J.J. Sheu, A. Santillan, K. Nakayama, M.J. Yen, R.E. Bristow, R. Vang, G. Parmigiani, R.J. Kurman, C.G. Trope, B. Davidson, T.L. Wang, Amplification of a chromatin remodeling gene, Rsf-1/HBXAP, in ovarian carcinoma. Proc. Natl. Acad. Sci. U. S. A. 102, 14004–14009 (2005)
34. M. Eckey, S. Kuphal, T. Straub, P. Rümmele, E. Kremmer, A.K. Bosserhoff, P.B. Becker, Nucleosome remodeler SNF2L suppresses cell proliferation and migration and attenuates Wnt signaling. Mol. Cell. Biol. 32, 2359–2371 (2012)
35. R. Kumar, R.A. Wang, R. Bagheri-Yarmand, Emerging roles of MTA family members in human cancers. Mol. Cell. Biol. 30, 30–37 (2003)
36. A. Mazumdar, R.A. Wang, S.K. Mishra, L. Adam, R. Bagheri-Yarmand, M. Mandal, R.K. Vadlamudi, R. Kumar, Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nat. Cell Biol. 3, 30–37 (2001)
37. M.D. Hofer, A. Menke, F. Genze, P. Gierschik, K. Giehl, Expression of MTA1 promotes motility and invasiveness of PANC-1 pancreatic carcinoma cells. Br. J. Cancer 90, 455–462 (2004)
38. A.E. Gururaj, R.R. Singh, S.K. Rayala, C. Holm, P. den Hollander, H. Zhang, S. Balasenthil, A.H. Talukder, G. Landberg, R. Kumar, MTA1, a transcriptional activator of breast cancer amplified sequence 3. Proc. Natl. Acad. Sci. USA 103, 6670–6675 (2006)
39. Erratum in: Proc. Natl. Acad. Sci. USA 110, 4147–4148 (2013)
40. O. Monni, M. Barlund, S. Mousses, J. Kononen, G. Sauter, M. Heiskanen, P. Paavola, K. Avela, Y. Chen, M.L. Bittner, A. Kallioniemi, Comprehensive copy number and gene expression profiling of the 17q23 amplicon in human breast cancer. Proc. Natl. Acad. Sci. U. S. A. 98, 5711–5716 (2001)
41. J. Basta, M. Rauchman, The nucleosome remodeling and deacetylase complex in development and disease. Transl. Res. 165, 36–47 (2015)
42. D. Rodríguez, G. Bretones, V. Quesada, N. Villamor, J.R. Arango, A. López-Guillermo, A.J. Ramsay, T. Baumann, P.M. Quirós, A. Navarro, C. Royo, J.I. Martín-Subero, E. Campo, C. López-Otín, Mutations in CHD2 cause defective association with active chromatin in chronic lymphocytic leukemia. Blood 126, 195–202 (2015)
43. Y. Gui, G. Guo, Y. Huang, X. Hu, A. Tang, S. Gao, R. Wu, C. Chen, X. Li, L. Zhou, M. He, Z. Li, X. Sun, W. Jia, J. Chen, S. Yang, F. Zhou, X. Zhao, S. Wan, R. Ye, C. Liang, Z. Liu, P. Huang, C. Liu, H. Jiang, Y. Wang, H. Zheng, L. Sun, X. Liu, Z. Jiang, D. Feng, J. Chen, S. Wu, J. Zou, Z. Zhang, R. Yang, J. Zhao, C. Xu, W. Yin, Z. Guan, J. Ye, H. Zhang, J. Li, K. Kristiansen, M.L. Nickerson, D. Theodorescu, Y. Li, X. Zhang, S. Li, J. Wang, H. Yang, J. Wang, Z. Cai, Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat. Genet. 43, 875–878 (2011)
44. D. Mouradov, C. Sloggett, R.N. Jorissen, C.G. Love, S. Li, A.W. Burgess, D. Arango, R.L. Strausberg, D. Buchanan, S. Wormald, L. O’Connor, J.L. Wilding, D. Bicknell, I.P. Tomlinson, W.F. Bodmer, J.M. Mariadason, O.M. Sieber, Colorectal cancer cell lines are representative models of the main molecular subtypes of primary cancer. Cancer Res. 74, 3238–3247 (2014)
45. M.S. Kim, N.G. Chung, M.R. Kang, N.J. Yoo, S.H. Lee, Genetic and expressional alterations of CHD genes in gastric and colorectal cancers. Histopathology 58, 660–668 (2011)
46. F.K. Stanley, S. Moore, A.A. Goodarzi, CHD chromatin remodelling enzymes and the DNA damage response. Mutat. Res. 750, 31–44 (2013)
47. K. Nio, T. Yamashita, H. Okada, M. Kondo, T. Hayashi, Y. Hara, Y. Nomura, S.S. Zeng, M. Yoshida, T. Hayashi, H. Sunagozaka, N. Oishi, M. Honda, S. Kaneko, Defeating EpCAM(+) liver cancer stem cells by targeting chromatin remodeling enzyme CHD4 in human hepatocellular carcinoma. J. Hepatol. 63, 1164–1172 (2015)
48. S. Guillemette, R.W. Serra, M. Peng, J.A. Hayes, P.A. Konstantinopoulos, M.R. Green, S.B. Cantor, Resistance to therapy in BRCA2 mutant cells due to loss of the nucleosome remodeling factor CHD4. Genes Dev. 29, 489–494 (2015)
49. M. Le Gallo, A.J. O’Hara, M.L. Rudd, M.E. Urick, N.F. Hansen, N.J. O’Neil, J.C. Price, S. Zhang, B.M. England, A.K. Godwin, D.C. Sgroi, NIH Intramural Sequencing Center (NISC) Comparative Sequencing Program, P. Hieter, J.C. Mullikin, M.J. Merino, D.W. Bell, Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatinremodeling and ubiquitin ligase complex genes. Nat. Genet. 44, 1310–1315 (2012)
50. G. Sawada, H. Ueo, T. Matsumura, R. Uchi, M. Ishibashi, K. Mima, J. Kurashige, Y. Takahashi, S. Akiyoshi, T. Sudo, K. Sugimachi, Y. Doki, M. Mori, K. Mimori, CHD8 is an independent prognostic indicator that regulates Wnt/β-catenin signaling and the cell cycle in gastric cancer. Oncol. Rep. 30, 1137–1142 (2013)
51. L. Wang, S. He, Y. Tu, P. Ji, J. Zong, J. Zhang, F. Feng, J. Zhao, G. Gao, Y. Zhang, Downregulation of chromatin remodeling factor CHD5 is associated with a poor prognosis in human glioma. J. Clin. Neurosci. 20, 958–963 (2013)
52. A.J. Morrison, J. Highland, N.J. Krogan, A. Arbel-Eden, J.F. Greenblatt, J.E. Haber, X. Shen, INO80 and γ-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119, 767–775 (2004)
53. H. van Attikum, O. Fritsch, S.M. Gasser, Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26, 4113–4125 (2007)
54. M. Papamichos-Chronakis, S. Watanabe, O.J. Rando, C.L. Peterson, Global regulation of H2A. Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144, 200–213 (2011)
55. H.E. Alatwi, J.A. Downs, Removal of H2A. Z by INO80 promotes homologous recombination. EMBO Rep. 16, 986–994 (2015)
56. S. Watanabe, M. Radman-Livaja, O.J. Rando, C.L. Peterson, A histone acetylation switch regulates H2A. Z deposition by the SWR-C remodeling enzyme. Science 340, 195–199 (2013)
57. A.J. Morrison, X. Shen, Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat. Rev. Mol. Cell Biol. 10, 373–384 (2009)
58. C. Kadoch, D.C. Hargreaves, C. Hodges, L. Elias, L. Ho, J. Ranish, G.R. Crabtree, Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet. 45, 592–601 (2013)
59. A. Raymond, S. Benhamouche, V. Neaud, J. Di Martino, J. Javary, J. Rosenbaum, Reptin regulates DNA double strand breaks repair in human hepatocellular carcinoma. PLoS One 10, e0123333 (2015)
60. S. Dong, J. Han, H. Chen, T. Liu, M.S. Huen, Y. Yang, C. Guo, J. Huang, The human SRCAP chromatin remodeling complex promotes DNA-end resection. Curr. Biol. 24, 2097–2110 (2014)
61. D.D. Ruhl, J. Jin, Y. Cai, S. Swanson, L. Florens, M.P. Washburn, R.C. Conaway, J.W. Conaway, J.C. Chrivia, Purification of a human SRCAP complex that remodels chromatin by incorporating the histone variant H2A. Z into nucleosomes. Biochemistry 45, 5671–5677 (2006)
62. M.M. Wong, L.K. Cox, J.C. Chrivia, The chromatin remodeling protein, SRCAP, is critical for deposition of the histone variant H2A. Z at promoters. J. Biol. Chem. 282, 26132–26139 (2007)
63. A. Slupianek, S. Yerrum, F.F. Safadi, M.A. Monroy, The chromatin remodeling factor SRCAP modulates expression of prostate specific antigen and cellular proliferation in prostate cancer cells. J. Cell. Physiol. 224, 369–375 (2010)
64. T. Bianco-Miotto, K. Chiam, G. Buchanan, S. Jindal, T.K. Day, M. Thomas, M.A. Pickering, M.A. O’Loughlin, N.K. Ryan, W.A. Raymond, L.G. Horvath, J.G. Kench, P.D. Stricker, V.R. Marshall, R.L. Sutherland, S.M. Henshall, W.L. Gerald, H.I. Scher, G.P. Risbridger, J.A. Clements, L.M. Butler, W.D. Tilley, D.J. Horsfall, C. Ricciardelli, Australian Prostate Cancer BioResource, Global levels of specific histone modifications and an epigenetic gene signature predict prostate cancer progression and development. Cancer Epidemiol. Biomarkers Prev. 19, 2611–2622 (2010)
65. V. Patil, J. Pal, K. Somasundaram, Elucidating the cancer-specific genetic alteration spectrum of glioblastoma derived cell lines from whole exome and RNA sequencing. Oncotarget 6, 43452–43471 (2015)
66. W. Martin-Doyle, D.J. Kwiatkowski, Molecular biology of bladder cancer. Hematol. Oncol. Clin. N. Am. 29, 191–203 (2015)
67. J. Burrage, A. Termanis, A. Geissner, K. Myant, K. Gordon, I. Stancheva, The SNF2 family ATPase LSH promotes phosphorylation of H2AX and efficient repair of DNA double-strand breaks in mammalian cells. J. Cell Sci. 125, 5524–5534 (2012)
68. Y. Tao, S. Xi, J. Shan, A. Maunakea, A. Che, V. Briones, E.Y. Lee, T. Geiman, J. Huang, R. Stephens, R.M. Leighty, K. Zhao, K. Muegge, Lsh, chromatin remodeling family member, modulates genome-wide cytosine methylation patterns at nonrepeat sequences. Proc. Natl. Acad. Sci. U. S. A. 108, 5626–5631 (2011)
69. J. Ren, V. Briones, S. Barbour, W. Yu, Y. Han, M. Terashima, K. Muegge, The ATP binding site of the chromatin remodeling homolog Lsh is required for nucleosome density and de novo DNA methylation at repeat sequences. Nucleic Acids Res. 43, 1444–1455 (2015)
70. D.W. Lee, K. Zhang, Z.Q. Ning, E.H. Raabe, S. Tintner, R. Wieland, B.J. Wilkins, J.M. Kim, R.I. Blough, R.J. Arceci, Proliferation-associated SNF2-like gene (PASG): a SNF2 family member altered in leukemia. Cancer Res. 60, 3612–3622 (2000)
71. M. Yano, M. Ouchida, H. Shigematsu, N. Tanaka, K. Ichimura, K. Kobayashi, Y. Inaki, S. Toyooka, K. Tsukuda, N. Shimizu, K. Shimizu, Tumor-specific exon creation of the HELLS/SMARCA6 gene in non‐small cell lung cancer. Int. J. Cancer 112, 8–13 (2004)
72. B. von Eyss, J. Maaskola, S. Memczak, K. Möllmann, A. Schuetz, C. Loddenkemper, M.D. Tanh, A. Otto, K. Muegge, U. Heinemann, N. Rajewsky, U. Ziebold, The SNF2‐like helicase HELLS mediates E2F3‐dependent transcription and cellular transformation. EMBO J. 31, 972–985 (2012)
73. C.A. Benavente, D. Finkelstein, D.A. Johnson, J.C. Marine, R. Ashery-Padan, M.A. Dyer, Chromatin remodelers HELLS and UHRF1 mediate the epigenetic deregulation of genes that drive retinoblastoma tumor progression. Oncotarget 5, 9594 (2014)
74. S.P. Rowbotham, L. Barki, A. Neves-Costa, F. Santos, W. Dean, N. Hawkes, P. Choudhary, W.R. Will, J. Webster, D. Oxley, C.M. Green, P. Varga-Weisz, J.E. Mermoud, Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol. Cell 42, 285–296 (2011)
75. C.N. Adra, J.L. Donato, R. Badovinac, F. Syed, R. Kheraj, H. Cai, C. Moran, M.T. Kolker, H. Turner, S. Weremowicz, T. Shirakawa, C.C. Morton, L.E. Schnipper, R. Drews, SMARCAD1, a novel human helicase family-defining member associated with genetic instability: cloning, expression, and mapping to 4q22–q23, a band rich in breakpoints and deletion mutants involved in several human diseases. Genomics 69, 162–173 (2000)
76. M. Berg, T.H. Ågesen, E. Thiis-Evensen, M.A. Merok, M.R. Teixeira, M.H. Vatn, A. Nesbakken, R.I. Skotheim, R.A. Lothe, Distinct high resolution genome profiles of early onset and late onset colorectal cancer integrated with gene expression data identify candidate susceptibility loci. Mol. Cancer 9, 100 (2010)
77. C.C. Chung, P.A. Kanetsky, Z. Wang, M.A. Hildebrandt, R. Koster, R.I. Skotheim, C.P. Kratz, C. Turnbull, V.K. Cortessis, A.C. Bakken, D.T. Bishop, M.B. Cook, R.L. Erickson, S.D. Fosså, K.B. Jacobs, L.A. Korde, S.M. Kraggerud, R.A. Lothe, J.T. Loud, N. Rahman, E.C. Skinner, D.C. Thomas, X. Wu, M. Yeager, F.R. Schumacher, M.H. Greene, S.M. Schwartz, K.A. McGlynn, S.J. Chanock, K.L. Nathanson, Meta-analysis identifies four new loci associated with testicular germ cell tumor. Nat. Genet. 45, 680–685 (2013)
78. E. Cetin, B. Cengiz, E. Gunduz, M. Gunduz, H. Nagatsuka, L. Bekir-Beder, K. Fukushima, D. Pehlivan, N. M.O., K. Nishizaki, K. Shimizu, N. Nagai, Author information Deletion mapping of chromosome 4q22-35 and identification of four frequently deleted regions in head and neck cancers. Neoplasma 55, 299–304 (2007)
79. L. Tapak, M. Saidijam, M. Sadeghifar, J. Poorolajal, H. Mahjub, Competing risks data analysis with high-dimensional covariates: an application in bladder cancer. Genomics Proteomics Bioinformatics 13, 169–176 (2015)
80. G.G. Wang, C.D. Allis, P. Chi, Chromatin remodeling and cancer. Part I: covalent histone modifications. Trends Mol. Med. 13, 363–372 (2007)
81. M. Brehove, T. Wang, J. North, Y. Luo, S.J. Dreher, J.C. Shimko, J.J. Ottesen, K. Luger, M.G. Poirier, Histone core phosphorylation regulates DNA accessibility. J. Biol. Chem. 290, 22612–22621 (2015)
82. P. Tessarz, T. Kouzarides, Histone core modifications regulating nucleosome structure and dynamics. Nat. Rev. Mol. Cell. Biol. 15, 703–708 (2014)
83. T. Kouzarides, Chromatin modifications and their function. Cell 128, 693–705 (2007)
84. P. Filippakopoulos, S. Picaud, M. Mangos, T. Keates, J.P. Lambert, D. Barsyte-Lovejoy, Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 149, 214–231 (2012)
85. P. Filippakopoulos, S. Knapp, Targeting bromodomains: epigenetic readers of lysine acetylation. Nat. Rev. Drug Discov. 13, 337–356 (2014)
86. P. Marks, R.A. Rifkind, V.M. Richon, R. Breslow, T. Miller, W.K. Kelly, Histone deacetylases and cancer: causes and therapies. Nat. Rev. Cancer 1, 194–202 (2001)
87. V.M. Richon, J.P. O’Brien, Histone deacetylase inhibitors: a new class of potential therapeutic agents for cancer treatment. Commentary re: V. Sandor et al., Phase I trial of the histone deacetylase inhibitor, depsipeptide (FR901228, NSC 630176), in patients with refractory neoplasms. Clin. Cancer Res. 8, 718–728 (2002); Clin. Cancer Res. 8, 662–664 (2002)
88. K.C. Lakshmaiah, L.A. Jacob, S. Aparna, D. Lokanatha, S.C. Saldanha, Epigenetic therapy of cancer with histone deacetylase inhibitors. J. Cancer Res. Ther. 10, 469–478 (2014)
89. C. Cortés, S.C. Kozma, A. Tauler, S. Ambrosio, MYCN concurrence with SAHA-induced cell death in human neuroblastoma cells. Cell. Oncol. 38, 341–352 (2015)
90. K.S. Zaret, J.S. Carroll, Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25, 2227–2241 (2011)
91. P. Voigt, W.W. Tee, D. Reinberg, A double take on bivalent promoters. Genes Dev. 27, 1318–1338 (2013)
92. G.E. Zentner, S. Henikoff, Regulation of nucleosome dynamics by histone modifications. Nat. Struct. Mol. Biol. 20, 259–266 (2013)
93. M.F. Fraga, E. Ballestar, A. Villar-Garea, M. Boix-Chornet, J. Espada, G. Schotta, T. Bonaldi, C. Haydon, S. Ropero, K. Petrie, N.G. Iyer, A. Pérez-Rosado, E. Calvo, J.A. Lopez, A. Cano, M.J. Calasanz, D. Colomer, M.A. Piris, N. Ahn, A. Imhof, C. Caldas, T. Jenuwein, M. Esteller, Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 37, 391–400 (2005)
94. M.A. Hahn, A.X. Li, X. Wu, R. Yang, D.A. Drew, D.W. Rosenberg, G.P. Pfeifer, Loss of the polycomb mark from bivalent promoters leads to activation of cancer-promoting genes in colorectal tumors. Cancer Res. 74, 3617–3629 (2014)
95. S. Bhatnagar, C. Gazin, L. Chamberlain, J. Ou, X. Zhu, J.S. Tushir, C.M. Virbasius, L. Lin, L.J. Zhu, N. Wajapeyee, M.R. Green, TRIM37 is a new histone H2A ubiquitin ligase and breast cancer oncoprotein. Nature 516, 116–120 (2014)
96. A.J. Cole, R. Clifton-Bligh, D.J. Marsh, Histone H2B monoubiquitination: roles to play in human malignancy. Endocr. Relat. Cancer 22, T19–T33 (2015)
97. M.A. Hahn, K.A. Dickson, S. Jackson, A. Clarkson, A.J. Gill, D.J. Marsh, The tumor suppressor CDC73 interacts with the ring finger proteins RNF20 and RNF40 and is required for the maintenance of histone 2B monoubiquitination. Hum. Mol. Genet. 21, 559–568 (2012)
98. D.B. Seligson, S. Horvath, T. Shi, H. Yu, S. Tze, M. Grunstein, S.K. Kurdistani, Global histone modification patterns predict risk of prostate cancer recurrence. Nature 435, 1262–1266 (2005)
99. F. Barlési, G. Giaccone, M.I. Gallegos-Ruiz, A. Loundou, S.W. Span, P. Lefesvre, F.A. Kruyt, J.A. Rodriguez, Global histone modifications predict prognosis of resected non small-cell lung cancer. J. Clin. Oncol. 25, 4358–4364 (2007)
100. Y.S. Park, M.Y. Jin, Y.J. Kim, J.H. Yook, B.S. Kim, S.J. Jang, The global histone modification pattern correlates with cancer recurrence and overall survival in gastric adenocarcinoma. Ann. Surg. Oncol. 15, 1968–1976 (2008)
101. S.E. Elsheikh, A.R. Green, E.A. Rakha, D.G. Powe, R.A. Ahmed, H.M. Collins, D. Soria, J.M. Garibaldi, C.E. Paish, A.A. Ammar, M.J. Grainge, G.R. Ball, M.K. Abdelghany, L. Martinez-Pomares, D.M. Heery, I.O. Ellis, Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome. Cancer Res. 69, 3802–3809 (2009)
102. K. Zhang, L. Li, M. Zhu, G. Wang, J. Xie, Y. Zhao, E. Fan, L. Xu, E. Li, Comparative analysis of histone H3 and H4 post-translational modifications of esophageal squamous cell carcinoma with different invasive capabilities. J. Proteomics 112, 180–189 (2015)
103. C. Müller-Tidow, H.U. Klein, A. Hascher, F. Isken, L. Tickenbrock, A. Thoennissen, S. Agrawal-Singh, P. Tschanter, C. Disselhoff, Y. Wang, A. Becker, C. Thiede, G. Ehninger, U. zur Stadt, S. Koschmieder, M. Seidl, F.U. Müller, W. Schmitz, P. Schlenke, M. McClelland, W.E. Berdel, M. Dugas, H. Serve, Study Alliance Leukemia, Profiling of histone H3 lysine 9 trimethylation levels predicts transcription factor activity and survival in acute myeloid leukemia. Blood 116, 3564–3571 (2010)
104. A. Laugesen, K. Helin, Chromatin repressive complexes in stem cells, development, and cancer. Cell Stem Cell 14, 735–751 (2014)
105. C. Bödör, V. Grossmann, N. Popov, J. Okosun, C. O’Riain, K. Tan, J. Marzec, S. Araf, J. Wang, A.M. Lee, A. Clear, S. Montoto, J. Matthews, S. Iqbal, H. Rajnai, A. Rosenwald, G. Ott, E. Campo, L.M. Rimsza, E.B. Smeland, W.C. Chan, R.M. Braziel, L.M. Staudt, G. Wright, T.A. Lister, O. Elemento, R. Hills, J.G. Gribben, C. Chelala, A. Matolcsy, A. Kohlmann, T. Haferlach, R.D. Gascoyne, J. Fitzgibbon, EZH2 mutations are frequent and represent an early event in follicular lymphoma. Blood 122, 3165–3168 (2013)
106. M. Wassef, V. Rodilla, A. Teissandier, B. Zeitouni, N. Gruel, B. Sadacca, M. Irondelle, M. Charruel, B. Ducos, A. Michaud, M. Caron, E. Marangoni, P. Chavrier, C. Le Tourneau, M. Kamal, E. Pasmant, M. Vidaud, N. Servant, F. Reyal, D. Meseure, A. Vincent-Salomon, S. Fre, R. Margueron, Impaired PRC2 activity promotes transcriptional instability and favors breast tumorigenesis. Genes Dev. 29, 2547–2562 (2015)
107. I.M. Schaefer, C.D. Fletcher, J.L. Hornick, Loss of H3K27 trimethylation distinguishes malignant peripheral nerve sheath tumors from histologic mimics. Mod. Pathol. 29, 4–13 (2015)
108. B.E. Bernstein, T.S. Mikkelsen, X. Xie, M. Kamal, D.J. Huebert, J. Cuff, B. Fry, A. Meissner, M. Wernig, K. Plath, R. Jaenisch, A. Wagschal, R. Feil, S.L. Schreiber, E.S. Lander, A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315–326 (2006)
109. A.P. Bracken, D. Kleine-Kohlbrecher, N. Dietrich, D. Pasini, G. Gargiulo, C. Beekman, K. Theilgaard-Mönch, S. Minucci, B.T. Porse, J.C. Marine, K.H. Hansen, K. Helin, The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev. 21, 525–530 (2007)
110. J.Y. Yao, L. Zhang, X. Zhang, Z.Y. He, Y. Ma, L.J. Hui, X. Wang, Y.P. Hu, H3K27 trimethylation is an early epigenetic event of p16INK4a silencing for regaining tumorigenesis in fusion reprogrammed hepatoma cells. J. Biol. Chem. 285, 18828–18837 (2010)
111. C. Vallot, A. Hérault, S. Boyle, W.A. Bickmore, F. Radvanyi, PRC2-independent chromatin compaction and transcriptional repression in cancer. Oncogene 34, 741–751 (2015)
112. P.B. Talbert, S. Henikoff, Histone variants-ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 11, 264–275 (2010)
113. M. Hondele, A.G. Ladurner, The chaperone-histone partnership: for the greater good of histone traffic and chromatin plasticity. Curr. Opin. Struct. Biol. 21, 698–708 (2011)
114. C. Bonisch, S.B. Hake, Histone H2A variants in nucleosomes and chromatin: more or less stable? Nucleic Acids Res. 40, 10719–10741 (2012)
115. H. Tachiwana, A. Osakabe, T. Shiga, Y. Miya, H. Kimura, W. Kagawa, H. Kurumizaka, Structures of human nucleosomes containing major histone H3 variants. Acta Crystallogr. 67, 578–583 (2011)
116. A. Izzo, K. Kamieniarz, R. Schneider, The histone H1 family: specific members, specific functions? Biol. Chem. 389, 333–343 (2008)
117. E. Dardenne, S. Pierredon, K. Driouch, L. Gratadou, M. Lacroix-Triki, M.P. Espinoza, E. Zonta, S. Germann, H. Mortada, J.P. Villemin, M. Dutertre, R. Lidereau, S. Vagner, D. Auboeuf, Splicing switch of an epigenetic regulator by RNA helicases promotes tumor-cell invasiveness. Nat. Struct. Mol. Biol. 19, 1139–1146 (2012)
118. C. Vardabasso, A. Gaspar-Maia, D. Hasson, S. Pünzeler, D. Valle-Garcia, T. Straub, E.C. Keilhauer, T. Strub, J. Dong, T. Panda, C.Y. Chung, J.L. Yao, R. Singh, M.F. Segura, B. Fontanals-Cirera, A. Verma, M. Mann, E. Hernando, S.B. Hake, E. Bernstein, Histone variant H2A.Z.2 mediates proliferation and drug sensitivity of malignant melanoma. Mol. Cell 59, 75–88 (2015)
119. A. Kapoor, M.S. Goldberg, L.K. Cumberland, K. Ratnakumar, M. Segura, P.O. Emanuel, S. Menendez, C. Vardabasso, G. Leroy, C.I. Vidal, D. Polsky, I. Osman, B.A. Garcia, E. Hernando, E. Bernstein, The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature 468, 1105–1109 (2010)
120. L. Novikov, J.W. Park, H. Chen, H. Klerman, A.S. Jalloh, M.J. Gamble, QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation. Mol. Cell. Biol. 31, 4244–4255 (2011)
121. A. Gaspar-Maia, Z.A. Qadeer, D. Hasson, K. Ratnakumar, N.A. Leu, G. Leroy, S. Liu, C. Costanzi, D. Valle-Garcia, C. Schaniel, I. Lemischka, B. Garcia, J.R. Pehrson, E. Bernstein, MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nat. Commun. 4, 1565 (2013)
122. B.E. Black, D.W. Cleveland, Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell 144, 471–479 (2011)
123. M.C. Barnhart, P.H. Kuich, M.E. Stellfox, J.A. Ward, E.A. Bassett, B.E. Black, D.R. Foltz, HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J. Cell Biol. 194, 229–243 (2011)
124. T. Tomonaga, K. Matsushita, S. Yamaguchi, T. Oohashi, H. Shimada, T. Ochiai, K. Yoda, F. Nomura, Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res. 63, 3511–3516 (2003)
125. Q. Wu, Y.M. Qian, X.L. Zhao, S.M. Wang, X.J. Feng, X.F. Chen, S.H. Zhang, Expression and prognostic significance of centromere protein A in human lung adenocarcinoma. Lung Cancer 77, 407–414 (2012)
126. K. Biermann, L.C. Heukamp, K. Steger, H. Zhou, F.E. Franke, I. Guetgemann, V. Sonnack, R. Brehm, J. Berg, P.J. Bastian, S.C. Müller, L. Wang-Eckert, H. Schorle, R. Büttner, Gene expression profiling identifies new biological markers of neoplastic germ cells. Anticancer Res. 27, 3091–3100 (2007)
127. X.M. Gu, J. Fu, X.J. Feng, X. Huang, S.M. Wang, X.F. Chen, M.H. Zhu, S.H. Zhang, Expression and prognostic relevance of centromere protein A in primary osteosarcoma. Pathol. Res. Pract. 210, 228–233 (2014)
128. J.J. Qiu, J.J. Guo, T.J. Lv, H.Y. Jin, J.X. Ding, W.W. Feng, Y. Zhang, K.Q. Hua, Prognostic value of centromere protein-A expression in patients with epithelial ovarian cancer. Tumour Biol. 34, 2971–2975 (2013)
129. S.L. McGovern, Y. Qi, L. Pusztai, W.F. Symmans, T.A. Buchholz, Centromere protein-A, an essential centromere protein, is a prognostic marker for relapse in estrogen receptor-positive breast cancer. Breast Cancer Res. 14, R72 (2012)
130. Q. Wu, Y.F. Chen, J. Fu, Q.H. You, S.M. Wang, X. Huang, X.J. Feng, S.H. Zhang, Short hairpin RNA-mediated down-regulation of CENP-A attenuates the aggressive phenotype of lung adenocarcinoma cells. Cell. Oncol. 37, 399–407 (2014)
131. R.K. Athwal, M.P. Walkiewicz, S. Baek, S. Fu, M. Bui, J. Camps, T. Ried, M.H. Sung, Y. Dalal, CENP-A nucleosomes localize to transcription factor hotspots and subtelomeric sites in human cancer cells. Epigenetics Chromatin 8, 2 (2015)
132. J. Bieniek, C. Childress, M.D. Swatski, W. Yang, COX-2 inhibitors arrest prostate cancer cell cycle progression by down-regulation of kinetochore/centromere proteins. Prostate 74, 999–1011 (2014)
133. J. Schwartzentruber, A. Korshunov, X.Y. Liu, D.T. Jones, E. Pfaff, K. Jacob, D. Sturm, A.M. Fontebasso, D.A. Quang, M. Tönjes, V. Hovestadt, S. Albrecht, M. Kool, A. Nantel, C. Konermann, A. Lindroth, N. Jäger, T. Rausch, M. Ryzhova, J.O. Korbel, T. Hielscher, P. Hauser, M. Garami, A. Klekner, L. Bognar, M. Ebinger, M.U. Schuhmann, W. Scheurlen, A. Pekrun, M.C. Frühwald, W. Roggendorf, C. Kramm, M. Dürken, J. Atkinson, P. Lepage, A. Montpetit, M. Zakrzewska, K. Zakrzewski, P.P. Liberski, Z. Dong, P. Siegel, A.E. Kulozik, M. Zapatka, A. Guha, D. Malkin, J. Felsberg, G. Reifenberger, A. von Deimling, K. Ichimura, V.P. Collins, H. Witt, T. Milde, O. Witt, C. Zhang, P. Castelo-Branco, P. Lichter, D. Faury, U. Tabori, C. Plass, J. Majewski, S.M. Pfister, N. Jabado, Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482, 226–231 (2012)
134. G. Wu, A. Broniscer, T.A. McEachron, C. Lu, B.S. Paugh, J. Becksfort, C. Qu, L. Ding, R. Huether, M. Parker, J. Zhang, A. Gajjar, M.A. Dyer, C.G. Mullighan, R.J. Gilbertson, E.R. Mardis, R.K. Wilson, J.R. Downing, D.W. Ellison, J. Zhang, S.J. Baker, St. Jude Children’s Research Hospital–Washington University Pediatric Cancer Genome Project, Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat. Genet. 44, 251–253 (2012)
135. J. Okosun, C. Bödör, J. Wang, S. Araf, C.Y. Yang, C. Pan, S. Boller, D. Cittaro, M. Bozek, S. Iqbal, J. Matthews, D. Wrench, J. Marzec, K. Tawana, N. Popov, C. O’Riain, D. O’Shea, E. Carlotti, A. Davies, C.H. Lawrie, A. Matolcsy, M. Calaminici, A. Norton, R.J. Byers, C. Mein, E. Stupka, T.A. Lister, G. Lenz, S. Montoto, J.G. Gribben, Y. Fan, R. Grosschedl, C. Chelala, J. Fitzgibbon, Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat. Genet. 46, 176–181 (2014)
136. C. Jiang, B.F. Pugh, Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet. 10, 161–172 (2009)
137. J.L. Workman, R.E. Kingston, Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu. Rev. Biochem. 67, 545–579 (1998)
138. G.C. Yuan, Y.J. Liu, M.F. Dion, M.D. Slack, L.F. Wu, S.J. Altschuler, O.J. Rando, Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309, 626–630 (2005)
139. F. Ozsolak, J.S. Song, X.S. Liu, D.E. Fisher, High-throughput mapping of the chromatin structure of human promoters. Nat. Biotechnol. 25, 244–248 (2007)
140. W. Lee, D. Tillo, N. Bray, R.H. Morse, R.W. Davis, T.R. Hughes, C. Nislow, A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39, 1235–1244 (2007)
141. D.E. Schones, K. Cui, S. Cuddapah, T.Y. Roh, A. Barski, Z. Wang, G. Wei, K. Zhao, Dynamic regulation of nucleosome positioning in the human genome. Cell 32, 887–898 (2008)
142. S. Schwartz, E. Meshorer, G. Ast, Chromatin organization marks exon-intron structure. Nat. Struct. Mol. Biol. 16, 990–995 (2009)
143. T. Misteli, E. Soutoglou, The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat. Rev. Mol. Cell. Biol. 10, 243–254 (2009)
144. S. Sasaki, C.C. Mello, A. Shimada, Y. Nakatani, S. Hashimoto, M. Ogawa, K. Matsushima, S.G. Gu, M. Kasahara, B. Ahsan, A. Sasaki, T. Saito, Y. Suzuki, S. Sugano, Y. Kohara, H. Takeda, A. Fire, S. Morishita, Chromatin-associated periodicity in genetic variation downstream of transcriptional start sites. Science 323, 401–404 (2009)
145. K. Higasa, K. Hayashi, Periodicity of SNP distribution around transcription start sites. BMC Genomics 7, 66 (2006)
146. J.G. Prendergast, H. Campbell, N. Gilbert, M.G. Dunlop, W.A. Bickmore, C.A. Semple, Chromatin structure and evolution in the human genome. BMC Evol. Biol. 7, 72 (2007)
147. P.G. Yazdi, B.A. Pedersen, J.F. Taylor, O.S. Khattab, Y.H. Chen, Y. Chen, S.E. Jacobsen, P.H. Wang, Increasing nucleosome occupancy is correlated with an increasing mutation rate so long as DNA repair machinery is intact. PLoS One 10, e0136574 (2015)
148. P. Polak, R. Karlić, A. Koren, R. Thurman, R. Sandstrom, M.S. Lawrence, A. Reynolds, E. Rynes, K. Vlahoviček, J.A. Stamatoyannopoulos, S.R. Sunyaev, Cell-of-origin chromatin organization shapes the mutational landscape of cancer. Nature 518, 360–364 (2015)
149. P. Polak, M.S. Lawrence, E. Haugen, N. Stoletzki, P. Stojanov, R.E. Thurman, L.A. Garraway, S. Mirkin, G. Getz, J.A. Stamatoyannopoulos, S.R. Sunyaev, Reduced local mutation density in regulatory DNA of cancer genomes is linked to DNA repair. Nat. Biotechnol. 32, 71–75 (2014)
150. B. Schuster-Böckler, B. Lehner, Chromatin organization is a major influence on regional mutation rates in human cancer cells. Nature 488, 504–507 (2012)
151. A. Hodgkinson, Y. Chen, A. Eyre-Walker, The large-scale distribution of somatic mutations in cancer genomes. Hum. Mutat. 33, 136–143 (2012)
152. S. Ortiz-Cuaran, D. Cox, S. Villar, M.D. Friesen, G. Durand, A. Chabrier, T. Khuhaprema, S. Sangrajrang, S. Ognjanovic, J.D. Groopman, P. Hainaut, F. Le Calvez-Kelm, Association between TP53 R249S mutation and polymorphisms in TP53 intron 1 in hepatocellular carcinoma. Genes Chromosom. Cancer 52, 912–919 (2013)
153. L.E. Mechanic, E.D. Bowman, J.A. Welsh, M.A. Khan, N. Hagiwara, L. Enewold, P.G. Shields, L. Burdette, S. Chanock, C.C. Harris, Common genetic variation in TP53 is associated with lung cancer risk and prognosis in African Americans and somatic mutations in lung tumors. Cancer Epidemiol. Biomarkers Prev. 16, 214–222 (2007)
154. C. Lemaître, A. Grabarz, K. Tsouroula, L. Andronov, A. Furst, T. Pankotai, V. Heyer, M. Rogier, K.M. Attwood, P. Kessler, G. Dellaire, B. Klaholz, B. Reina-San-Martin, E. Soutoglou, Nuclear position dictates DNA repair pathway choice. Genes Dev. 28, 2450–2463 (2014)
155. F. Aymard, B. Bugler, C.K. Schmidt, E. Guillou, P. Caron, S. Briois, J.S. Iacovoni, V. Daburon, K.M. Miller, S.P. Jackson, G. Legube, Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nat. Struct. Mol. Biol. 21, 366–374 (2014)
156. S.X. Pfister, S. Ahrabi, L.P. Zalmas, S. Sarkar, F. Aymard, C.Z. Bachrati, T. Helleday, G. Legube, N.B. La Thangue, A.C. Porter, T.C. Humphrey, SETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell Rep. 7, 2006–2018 (2014)
157. C.L. Zheng, N.J. Wang, J. Chung, H. Moslehi, J.Z. Sanborn, J.S. Hur, E.A. Collisson, S.S. Vemula, A. Naujokas, K.E. Chiotti, J.B. Cheng, H. Fassihi, A.J. Blumberg, C.V. Bailey, G.M. Fudem, F.G. Mihm, B.B. Cunningham, I.M. Neuhaus, W. Liao, D.H. Oh, J.E. Cleaver, P.E. LeBoit, J.F. Costello, A.R. Lehmann, J.W. Gray, P.T. Spellman, S.T. Arron, N. Huh, E. Purdom, R.J. Cho, Transcription restores DNA repair to heterochromatin, determining regional mutation rates in cancer genomes. Cell Rep. 9, 1228–1234 (2014)
158. A. Kalousi, A.S. Hoffbeck, P.N. Selemenakis, J. Pinder, K.I. Savage, K.K. Khanna, L. Brino, G. Dellaire, V.G. Gorgoulis, E. Soutoglou, The nuclear oncogene SET controls DNA repair by KAP1 and HP1 retention to chromatin. Cell Rep. 11, 149–163 (2015)
159. M. Gkotzamanidou, E. Terpos, C. Bamia, S.A. Kyrtopoulos, P.P. Sfikakis, M.A. Dimopoulos, V.L. Souliotis, Progressive changes in chromatin structure and DNA damage response signals in bone marrow and peripheral blood during myelomagenesis. Leukemia 28, 1113–1121 (2014)
160. L.B. Hesson, M.A. Sloane, J.W. Wong, A.C. Nunez, S. Srivastava, B. Ng, N.J. Hawkins, M.J. Bourke, R.L. Ward, Altered promoter nucleosome positioning is an early event in gene silencing. Epigenetics 9, 1422–1430 (2014)
161. L.B. Hesson, V. Patil, M.A. Sloane, A.C. Nunez, J. Liu, J.E. Pimanda, R.L. Ward, Reassembly of nucleosomes at the MLH1 promoter initiates resilencing following decitabine exposure. PLoS Genet. 9, e1003636 (2013)
162. A.A. Alekseyenko, E.M. Walsh, X. Wang, A.R. Grayson, P.T. Hsi, P.V. Kharchenko, M.I. Kuroda, C.A. French, The oncogenic BRD4-NUT chromatin regulator drives aberrant transcription within large topological domains. Genes Dev. 29, 1507–1523 (2015)
163. S.R. James, C.D. Cedeno, A. Sharma, W. Zhang, J.L. Mohler, K. Odunsi, E.M. Wilson, A.R. Karpf, DNA methylation and nucleosome occupancy regulate the cancer germline antigen gene MAGEA11. Epigenetics 8, 849–863 (2013)