The inactive X chromosome is epigenetically unstable and transcriptionally labile in breast cancer

Genome Research

Volumn 25, Issue 4, 2015, Pages 488-503

  Chaligné, Ronan ^a,b,c   Popova, Tatiana ^a,d   Mendoza Parra, Marco Antonio ^e   Saleem, Mohamed Ashick M ^e   Gentien, David ^a   Ban, Kristen ^a,b,c   Piolot, Tristan ^a   Leroy, Olivier ^a   Mariani, Odette ^a   Gronemeyer, Hinrich ^e   Vincent Salomon, Anne ^a,c,d   Stern, Marc Henri ^a,d   Heard, Edith ^a,b,c  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c INSTITUT CURIE   (France)

^d INSERM   (France)

^e UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BREAST CANCER; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GENE ACTIVITY; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HETEROCHROMATIN; HUMAN; HUMAN CELL; PRIORITY JOURNAL; X CHROMATIN; X CHROMOSOME; BREAST TUMOR; CELL NUCLEUS; FEMALE; GENETIC EPIGENESIS; GENETICS; METABOLISM; PATHOLOGY; PROMOTER REGION; TUMOR CELL LINE; X CHROMOSOMAL INHERITANCE; X CHROMOSOME INACTIVATION;

ATRX PROTEIN, HUMAN; DNA HELICASE; HDAC8 PROTEIN, HUMAN; HISTONE; HISTONE DEACETYLASE; HISTONE DEMETHYLASE; HUWE1 PROTEIN, HUMAN; KDM5C PROTEIN, HUMAN; LONG UNTRANSLATED RNA; MAGEA6 PROTEIN, HUMAN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; TBL1X PROTEIN, HUMAN; TRANSDUCIN; TUMOR ANTIGEN; TUMOR MARKER; TUMOR PROTEIN; UBIQUITIN PROTEIN LIGASE; XIST NON-CODING RNA;

ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; CHROMOSOMES, HUMAN, X; DNA HELICASES; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENES, X-LINKED; HISTONE DEACETYLASES; HISTONE DEMETHYLASES; HISTONES; HUMANS; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; RNA, LONG NONCODING; SEX CHROMATIN; TRANSCRIPTION, GENETIC; TRANSDUCIN; UBIQUITIN-PROTEIN LIGASES; X CHROMOSOME INACTIVATION;

EID: 84927780472     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.185926.114     Document Type: Article

References (72)

1. Agrelo R, Wutz A. 2010. ConteXt of change - X inactivation and disease. EMBO Mol Med 2: 6-15.
2. Azoulay S, Laé M, Fréneaux P, Merle S, Al Ghuzlan A, Chnecker C, Rosty C, Klijanienko J, Sigal-Zafrani B, Salmon R, et al. 2005. KIT is highly expressed in adenoid cystic carcinoma of the breast, a basal-like carcinoma associated with a favorable outcome. Mod Pathol 18: 1623-1631.
3. Barr ML, Moore KL. 1957. Chromosomes, sex chromatin, and cancer. Proc Can Cancer Conf 2: 3-16.
4. Bennett CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L, Kelly TE, Saulsbury FT, Chance PF, Ochs HD. 2001. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 27: 20-21.
5. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315-326.
6. Boggs BA, Cheung P, Heard E, Spector DL, Chinault AC, Allis CD. 2002. Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes. Nat Genet 30: 73-76.
7. Carone DM, Lawrence JB. 2013. Heterochromatin instability in cancer: from the Barr body to satellites and the nuclear periphery. Semin Cancer Biol 23: 99-108.
8. Carrel L, Willard HF. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404.
9. Chadwick BP. 2007. Variation in Xi chromatin organization and correlation of the H3K27me3 chromatin territories to transcribed sequences by microarray analysis. Chromosoma 116: 147-157.
10. Chadwick BP, Willard HF. 2004. Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome. Proc Natl Acad Sci 101: 17450-17455.
11. Chaumeil J, Okamoto I, Guggiari M, Heard E. 2002. Integrated kinetics of X chromosome inactivation in differentiating embryonic stem cells. Cytogenet Genome Res 99: 75-84.
12. Chaumeil J, Le Baccon P, Wutz A, Heard E. 2006. A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev 20: 2223-2237.
13. Chaumeil J, Augui S, Chow JC, Heard E. 2008. Combined immunofluorescence, RNA fluorescent in situ hybridization, and DNA fluorescent in situ hybridization to study chromatin changes, transcriptional activity, nuclear organization, and X-chromosome inactivation. Methods Mol Biol 463: 297-308.
14. Chow JC, Heard E. 2010. Nuclear organization and dosage compensation. Cold Spring Harb Perspect Biol 2: a000604.
15. Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N, Glass JL, Attreed M, Avner P, Wutz A, Barillot E, et al. 2010. LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141:956-969.
16. Clemson CM, Hall LL, Byron M, McNeil J, Lawrence JB. 2006. The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced nongenic sequences. Proc Natl Acad Sci 103:7688-7693.
17. Cotton AM, Ge B, Light N, Adoue V, Pastinen T, Brown CJ. 2013. Analysis of expressed SNPs identifies variable extents of expression from the human inactive X chromosome. Genome Biol 14: R122.
18. Cotton AM, Chen CY, Lam LL, Wasserman WW, Kobor MS, Brown CJ. 2014. Spread of X-chromosome inactivation into autosomal sequences: role for DNA elements, chromatin features and chromosomal domains. Hum Mol Genet 23: 1211-1223.
19. Csankovszki G, Panning B, Bates B, Pehrson JR, Jaenisch R. 1999. Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat Genet 22: 323-324.
20. Csankovszki G, Nagy A, Jaenisch R. 2001. Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation. J Cell Biol 153: 773-784.
21. De Carvalho DD, Sharma S, You JS, Su SF, Taberlay PC, Kelly TK, Yang X, Liang G, Jones PA. 2012. DNA methylation screening identifies driver epigenetic events of cancer cell survival. Cancer Cell 21: 655-667.
22. Elsheikh SE, Green AR, Rakha EA, Powe DG, Ahmed RA, Collins HM, Soria D, Garibaldi JM, Paish CE, Ammar AA, et al. 2009. Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome. Cancer Res 69: 3802-3809.
23. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
24. Filippova GN, Cheng MK, Moore JM, Truong JP, Hu YJ, Nguyen DK, Tsuchiya KD, Disteche CM. 2005. Boundaries between chromosomal domains of X inactivation and escape bind CTCF and lack CpG methylation during early development. Dev Cell 8: 31-42.
25. Ganesan S, Silver DP, Greenberg RA, Avni D, Drapkin R, Miron A, Mok SC, Randrianarison V, Brodie S, Salstrom J, et al. 2002. BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 111:393-405.
26. Gendrel AV, Tang YA, Suzuki M, Godwin J, Nesterova TB, Greally JM, Heard E, Brockdorff N. 2013. Epigenetic functions of Smchd1 repress gene clusters on the inactive X chromosome and on autosomes. Mol Cell Biol 33: 3150-3165.
27. Gimelbrant A, Hutchinson JN, Thompson BR, Chess A. 2007. Widespread monoallelic expression on human autosomes. Science 318: 1136-1140.
28. Grigoriadis A, Caballero OL, Hoek KS, da Silva L, Chen YT, Shin SJ, Jungbluth AA, Miller LD, Clouston D, Cebon J, et al. 2009. CT-X antigen expression in human breast cancer. Proc Natl Acad Sci 106: 13493-13498.
29. Heard E, Rougeulle C, Arnaud D, Avner P, Allis CD, Spector DL. 2001. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell 107: 727-738.
30. Huang S, Deerinck TJ, Ellisman MH, Spector DL. 1997. The dynamic organization of the perinucleolar compartment in the cell nucleus. J Cell Biol 137: 965-974.
31. Huang KC, Rao PH, Lau CC, Heard E, Ng SK, Brown C, Mok SC, Berkowitz RS, Ng SW. 2002. Relationship of XIST expression and responses of ovarian cancer to chemotherapy. Mol Cancer Ther 1: 769-776.
32. Kawakami T, Zhang C, Taniguchi T, Kim CJ, Okada Y, Sugihara H, Hattori T, Reeve AE, Ogawa O, Okamoto K. 2004. Characterization of loss-of-inactive X in Klinefelter syndrome and female-derived cancer cells. Oncogene 23: 6163-6169.
33. Keohane AM, O'Neill LP, Belyaev ND, Lavender JS, Turner BM. 1996. X-Inactivation and histone H4 acetylation in embryonic stem cells. Dev Biol 180: 618-630.
34. Kim HC, Choi KC, Choi HK, Kang HB, Kim MJ, Lee YH, Lee OH, Lee J, Kim YJ, Jun W, et al. 2010. HDAC3 selectively represses CREB3-mediated transcription and migration of metastatic breast cancer cells. Cell Mol Life Sci 67: 3499-3510.
35. Kucera KS, Reddy TE, Pauli F, Gertz J, Logan JE, Myers RM, Willard HF. 2011. Allele-specific distribution of RNA polymerase II on female X chromosomes. Hum Mol Genet 20: 3964-3973.
36. López-Soto A, Folgueras AR, Seto E, Gonzalez S. 2009. HDAC3 represses the expression of NKG2D ligands ULBPs in epithelial tumour cells: potential implications for the immunosurveillance of cancer. Oncogene 28: 2370-2382.
37. Lyon MF. 1961. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190: 372-373.
38. Maenner S, Blaud M, Fouillen L, Savoye A, Marchand V, Dubois A, Sanglier- Cianférani S, Van Dorsselaer A, Clerc P, Avner P, et al. 2010. 2-D structure of the A region of XistRNA and its implication for PRC2 association. PLoS Biol 8: e1000276.
39. Marks H, Chow JC, Denissov S, Françoijs KJ, Brockdorff N, Heard E, Stunnenberg HG. 2009. High-resolution analysis of epigenetic changes associated with X inactivation. Genome Res 19: 1361-1373.
40. Miao LJ, Huang FX, Sun ZT, Zhang RX, Huang SF, Wang J. 2014. Stat3 inhibits Beclin 1 expression through recruitment of HDAC3 in nonsmall cell lung cancer cells. Tumour Biol 35: 7097-7103.
41. Müller BM, Jana L, Kasajima A, Lehmann A, Prinzler J, Budczies J, Winzer KJ, Dietel M, Weichert W, Denkert C. 2013. Differential expression of histone deacetylases HDAC1, 2 and 3 in human breast cancer-overexpression of HDAC2 and HDAC3 is associated with clinicopathological indicators of disease progression. BMC Cancer 13: 215.
42. Nakagawa M, Oda Y, Eguchi T, Aishima S, Yao T, Hosoi F, Basaki Y, Ono M, Kuwano M, Tanaka M, et al. 2007. Expression profile of class I histone deacetylases in human cancer tissues. Oncol Rep 18: 769-774.
43. O'Donovan PJ, Livingston DM. 2010. BRCA1 and BRCA2: breast/ovarian cancer susceptibility gene products and participants in DNA double-strand break repair. Carcinogenesis 31: 961-967.
44. Oehme I, Deubzer HE, Wegener D, Pickert D, Linke JP, Hero B, Kopp- Schneider A, Westermann F, Ulrich SM, von Deimling A, et al. 2009. Histone deacetylase 8 in neuroblastoma tumorigenesis. Clin Cancer Res 15: 91-99.
45. Okamoto I, Patrat C, Thépot D, Peynot N, Fauque P, Daniel N, Diabangouaya P, Wolf JP, Renard JP, Duranthon V, et al. 2011. Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 472: 370-374.
46. Pageau GJ, Hall LL, Ganesan S, Livingston DM, Lawrence JB. 2007. The disappearing Barr body in breast and ovarian cancers. Nat Rev Cancer 7: 628-633.
47. Park SY, Jun JA, Jeong KJ, Heo HJ, Sohn JS, Lee HY, Park CG, Kang J. 2011. Histone deacetylases 1, 6 and 8 are critical for invasion in breast cancer. Oncol Rep 25: 1677-1681.
48. Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, et al. 2000. Molecular portraits of human breast tumours. Nature 406: 747-752.
49. Perry M. 1972. Evaluation of breast tumour sex chromatin (Barr body) as an index of survival and response to pituitary ablation. Br J Surg 59:731-734.
50. Plath K, Talbot D, Hamer KM, Otte AP, Yang TP, Jaenisch R, Panning B. 2004. Developmentally regulated alterations in Polycomb repressive complex 1 proteins on the inactive X chromosome. J Cell Biol 167: 1025-1035.
51. Popova T, Manie E, Stoppa-Lyonnet D, Rigaill G, Barillot E, Stern MH. 2009. Genome Alteration Print (GAP): a tool to visualize and mine complex cancer genomic profiles obtained by SNP arrays. Genome Biol 10: R128.
52. Popova T, Manié E, Rieunier G, Caux-Moncoutier V, Tirapo C, Dubois T, Delattre O, Sigal-Zafrani B, Bollet M, Longy M, et al. 2012. Ploidy and large-scale genomic instability consistently identify basal-like breast carcinomas with BRCA1/2 inactivation. Cancer Res 72: 5454-5462.
53. Portela A, Esteller M. 2010. Epigenetic modifications and human disease. Nat Biotechnol 28: 1057-1068.
54. Richardson AL, Wang ZC, De Nicolo A, Lu X, Brown M, Miron A, Liao X, Iglehart JD, Livingston DM, Ganesan S. 2006. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9: 121-132.
55. Rivera MN, Kim WJ, Wells J, Driscoll DR, Brannigan BW, Han M, Kim JC, Feinberg AP, Gerald WL, Vargas SO, et al. 2007. An X chromosome gene, WTX, is commonly inactivated in Wilms tumor. Science 315: 642-645.
56. Schenk T, Chen WC, Göllner S, Howell L, Jin L, Hebestreit K, Klein HU, Popescu AC, Burnett A, Mills K, et al. 2012. Inhibition of the LSD1 (KDM1A) demethylase reactivates the all-trans-retinoic acid differentiation pathway in acute myeloid leukemia. Nat Med 18: 605-611.
57. Shah SP, Roth A, Goya R, Oloumi A, Ha G, Zhao Y, Turashvili G, Ding J, Tse K, Haffari G, et al. 2012. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 486: 395-399.
58. Shen H, Laird PW. 2013. Interplay between the cancer genome and epigenome. Cell 153: 38-55.
59. Silver DP, Dimitrov SD, Feunteun J, Gelman R, Drapkin R, Lu SD, Shestakova E, Velmurugan S, Denunzio N, Dragomir S, et al. 2007. Further evidence for BRCA1 communication with the inactive X chromosome. Cell 128: 991-1002.
60. Simon MD, Pinter SF, Fang R, Sarma K, Rutenberg-Schoenberg M, Bowman SK, Kesner BA, Maier VK, Kingston RE, Lee JT. 2013. High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature 504: 465-469.
61. Sirchia SM, Ramoscelli L, Grati FR, Barbera F, Coradini D, Rossella F, Porta G, Lesma E, Ruggeri A, Radice P, et al. 2005. Loss of the inactive X chromosome and replication of the active X in BRCA1-defective and wild-type breast cancer cells. Cancer Res 65: 2139-2146.
62. Smethurst M, Bishun NP, Fernandez D, Allen J, Burn JI, Alaghband-Zadeh J, Williams DC. 1981. Steroid hormone receptors and sex chromatin frequency in breast cancer. J Endocrinol Invest 4: 455-457.
63. Spatz A, Borg C, Feunteun J. 2004. X-chromosome genetics and human cancer. Nat Rev Cancer 4: 617-629.
64. Splinter E, de Wit E, Nora EP, Klous P, van de Werken HJ, Zhu Y, Kaaij LJ, van Ijcken W, Gribnau J, Heard E, et al. 2011. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev 25: 1371-1383.
65. Spurling CC, Godman CA, Noonan EJ, Rasmussen TP, Rosenberg DW, Giardina C. 2008. HDAC3 overexpression and colon cancer cell proliferation and differentiation. Mol Carcinog 47: 137-147.
66. Turner NC, Reis-Filho JS. 2006. Basal-like breast cancer and the BRCA1 phenotype. Oncogene 25: 5846-5853.
67. Vincent-Salomon A, Ganem-Elbaz C, Manié E, Raynal V, Sastre-Garau X, Stoppa-Lyonnet D, Stern MH, Heard E. 2007. X inactive-specific transcript RNA coating and genetic instability of the X chromosome in BRCA1 breast tumors. Cancer Res 67: 5134-5140.
68. Wutz A, Rasmussen TP, Jaenisch R. 2002. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 30: 167-174.
69. Xiao C, Sharp JA, Kawahara M, Davalos AR, Difilippantonio MJ, Hu Y, LiW, Cao L, Buetow K, Ried T, et al. 2007. The XIST noncoding RNA functions independently of BRCA1 in X inactivation. Cell 128: 977-989.
70. Yildirim E, Kirby JE, Brown DE, Mercier FE, Sadreyev RI, Scadden DT, Lee JT. 2013. Xist RNA is a potent suppressor of hematologic cancer in mice. Cell 152: 727-742.
71. Zhang J, Benavente CA, McEvoy J, Flores-Otero J, Ding L, Chen X, Ulyanov A, WuG, Wilson M, Wang J, et al. 2012. A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature 481: 329-334.
72. Zink D, Fischer AH, Nickerson JA. 2004. Nuclear structure in cancer cells. Nat Rev Cancer 4: 677-687.