Advertisement

The Role of Histone Modifications and Variants in Regulating Gene Expression in Breast Cancer

  • Mathieu Dalvai
  • Kerstin Bystricky
Article

Abstract

The role of epigenetic phenomena in cancer biology is increasingly being recognized. Here we focus on the mechanisms and enzymes involved in regulating histone methylation and acetylation, and the modulation of histone variant expression and deposition. Implications of these epigenetic marks for tumor development, progression and invasiveness are discussed with a particular emphasis on breast cancer progression.

Keywords

Breast cancer Estrogen Epigenetics Methylation Acetylation Histone variants 

Abbreviations

ER

estrogen receptor

PR

progesterone receptor

HDAC

histone deacetylase

HAT

histone acetylase

PRMT

protein arginine methyltransferase

KMT

lysine methyltransferase

Notes

Acknowledgments

MD is supported by a CNRS postdoctoral fellowship. We thank Marie Vandromme for sharing her expertise with histone modifying enzymes, team members for fruitful discussions and colleagues for their understanding that much interesting work cannot be cited due to space limitations.

References

  1. 1.
    Beatson GT. On the treatment of inoperable cases of carcinoma of the mamma: suggestions for a new method of treatment, with illustratives cases. Lancet 2. 1896;104:162–5.Google Scholar
  2. 2.
    Frasor J, Danes JM, Komm B, et al. Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology. 2003;144(10):4562–74.PubMedGoogle Scholar
  3. 3.
    Soulez M, Parker MG. Identification of novel oestrogen receptor target genes in human ZR75-1 breast cancer cells by expression profiling. J Mol Endocrinol. 2001;27(3):259–74.PubMedGoogle Scholar
  4. 4.
    Jensen EV, Desombre ER, Hurst DJ, et al. Estrogen-receptor interactions in target tissues. Arch Anat Microsc Morphol Exp. 1967;56(3):547–69.PubMedGoogle Scholar
  5. 5.
    Metivier R, Stark A, Flouriot G, et al. A dynamic structural model for estrogen receptor-alpha activation by ligands, emphasizing the role of interactions between distant A and E domains. Mol Cell. 2002;10(5):1019–32.PubMedGoogle Scholar
  6. 6.
    Chu S, Fuller PJ. Identification of a splice variant of the rat estrogen receptor beta gene. Mol Cell Endocrinol. 1997;132(1–2):195–9.PubMedGoogle Scholar
  7. 7.
    Ogawa S, Inoue S, Watanabe T, et al. Molecular cloning and characterization of human estrogen receptor betacx: a potential inhibitor ofestrogen action in human. Nucleic Acids Res. 1998;26(15):3505–12.PubMedGoogle Scholar
  8. 8.
    Zhao C, Matthews J, Tujague M, et al. Estrogen receptor beta2 negatively regulates the transactivation of estrogen receptor alpha in human breast cancer cells. Cancer Res. 2007;67(8):3955–62.PubMedGoogle Scholar
  9. 9.
    Allred DC, Harvey JM, Berardo M, et al. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol. 1998;11(2):155–68.PubMedGoogle Scholar
  10. 10.
    Thompson EW, Paik S, Brunner N, et al. Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer cell lines. J Cell Physiol. 1992;150(3):534–44.PubMedGoogle Scholar
  11. 11.
    Ottaviano YL, Issa JP, Parl FF, et al. Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res. 1994;54(10):2552–5.PubMedGoogle Scholar
  12. 12.
    Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003;100(7):3983–8.PubMedGoogle Scholar
  13. 13.
    Dontu G, Al-Hajj M, Abdallah WM, et al. Stem cells in normal breast development and breast cancer. Cell Prolif. 2003;36 Suppl 1:59–72.PubMedGoogle Scholar
  14. 14.
    Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 2003;3(12):895–902.PubMedGoogle Scholar
  15. 15.
    Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature. 2001;414(6859):105–11.PubMedGoogle Scholar
  16. 16.
    Spillane JB, Henderson MA. Cancer stem cells: a review. ANZ J Surg. 2007;77(6):464–8.PubMedGoogle Scholar
  17. 17.
    Shackleton M, Vaillant F, Simpson KJ, et al. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439(7072):84–8.PubMedGoogle Scholar
  18. 18.
    Dontu G, El-Ashry D, Wicha MS. Breast cancer, stem/progenitor cells and the estrogen receptor. Trends Endocrinol Metab. 2004;15(5):193–7.PubMedGoogle Scholar
  19. 19.
    Giamarchi C, Solanas M, Chailleux C, et al. Chromatin structure of the regulatory regions of pS2 and cathepsin D genes in hormone-dependent and -independent breast cancer cell lines. Oncogene. 1999;18(2):533–41.PubMedGoogle Scholar
  20. 20.
    Touitou I, Vignon F, Cavailles V, et al. Hormonal regulation of cathepsin D following transfection of the estrogen or progesterone receptor into three sex steroid hormone resistant cancer cell lines. J Steroid Biochem Mol Biol. 1991;40(1–3):231–7.PubMedGoogle Scholar
  21. 21.
    Yang X, Ferguson AT, Nass SJ, et al. Transcriptional activation of estrogen receptor alpha in human breast cancer cells by histone deacetylase inhibition. Cancer Res. 2000;60(24):6890–4.PubMedGoogle Scholar
  22. 22.
    Fleury L, Gerus M, Lavigne AC, et al. Eliminating epigenetic barriers induces transient hormone-regulated gene expression in estrogen receptor negative breast cancer cells. Oncogene. 2008;27(29):4075–85.PubMedGoogle Scholar
  23. 23.
    Yang X, Phillips DL, Ferguson AT, et al. Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells. Cancer Res. 2001;61(19):7025–9.PubMedGoogle Scholar
  24. 24.
    Lazennec G, Alcorn JL, Katzenellenbogen BS. Adenovirus-mediated delivery of a dominant negative estrogen receptor gene abrogates estrogen-stimulated gene expression and breast cancer cell proliferation. Mol Endocrinol. 1999;13(6):969–80.PubMedGoogle Scholar
  25. 25.
    Metivier R, Penot G, Hubner MR, et al. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell. 2003;115(6):751–63.PubMedGoogle Scholar
  26. 26.
    Wolffe AP, Matzke MA. Epigenetics: regulation through repression. Science. 1999;286(5439):481–6.PubMedGoogle Scholar
  27. 27.
    Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet. 2002;3(9):662–73.PubMedGoogle Scholar
  28. 28.
    Luger K, Mader AW, Richmond RK, et al. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389(6648):251–60.PubMedGoogle Scholar
  29. 29.
    Davey CA, Sargent DF, Luger K, et al. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol. 2002;319(5):1097–113.PubMedGoogle Scholar
  30. 30.
    Bhaumik SR, Smith E, Shilatifard A. Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol. 2007;14(11):1008–16.PubMedGoogle Scholar
  31. 31.
    Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403(6765):41–5.PubMedGoogle Scholar
  32. 32.
    Henikoff S, Ahmad K. Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol. 2005;21:133–53.PubMedGoogle Scholar
  33. 33.
    de la Cruz X, Lois S, Sanchez-Molina S, et al. Do protein motifs read the histone code? Bioessays. 2005;27(2):164–75.PubMedGoogle Scholar
  34. 34.
    Ballestar E, Esteller M. Epigenetic gene regulation in cancer. Adv Genet. 2008;61:247–67.PubMedGoogle Scholar
  35. 35.
    Feinberg AP, Ohlsson R, Henikoff S. The epigenetic progenitor origin of human cancer. Nat Rev Genet. 2006;7(1):21–33.PubMedGoogle Scholar
  36. 36.
    Deltour S, Chopin V, Leprince D. Epigenetics and cancer. Med Sci (Paris). 2005;21(4):405–11.Google Scholar
  37. 37.
    Ptashne M. On the use of the word ‘epigenetic’. Curr Biol. 2007;17(7):R233–6.PubMedGoogle Scholar
  38. 38.
    Wang GG, Allis CD, Chi P. Chromatin remodeling and cancer, part I: covalent histone modifications. Trends Mol Med. 2007;13(9):363–72.PubMedGoogle Scholar
  39. 39.
    Lee DY, Hayes JJ, Pruss D, et al. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell. 1993;72(1):73–84.PubMedGoogle Scholar
  40. 40.
    Hebbes TR, Thorne AW, Crane-Robinson C. A direct link between core histone acetylation and transcriptionally active chromatin. Embo J. 1988;7(5):1395–402.PubMedGoogle Scholar
  41. 41.
    Dhalluin C, Carlson JE, Zeng L, et al. Structure and ligand of a histone acetyltransferase bromodomain. Nature. 1999;399(6735):491–6.PubMedGoogle Scholar
  42. 42.
    Allis CD, Berger SL, Cote J, et al. New nomenclature for chromatin-modifying enzymes. Cell. 2007;131(4):633–6.PubMedGoogle Scholar
  43. 43.
    Travers AA, Thompson JM. An introduction to the mechanics of DNA. Philos Transact A Math Phys Eng Sci. 2004;362(1820):1265–79.PubMedGoogle Scholar
  44. 44.
    Khochbin S, Verdel A, Lemercier C, et al. Functional significance of histone deacetylase diversity. Curr Opin Genet Dev. 2001;11(2):162–6.PubMedGoogle Scholar
  45. 45.
    Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693–705.PubMedGoogle Scholar
  46. 46.
    Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem. 2001;70:81–120.PubMedGoogle Scholar
  47. 47.
    Martinez-Balbas MA, Bauer UM, Nielsen SJ, et al. Regulation of E2F1 activity by acetylation. Embo J. 2000;19(4):662–71.PubMedGoogle Scholar
  48. 48.
    Iyer NG, Ozdag H, Caldas C. p300/CBP and cancer. Oncogene. 2004;23(24):4225–31.PubMedGoogle Scholar
  49. 49.
    Roelfsema JH, Peters DJ. Rubinstein-Taybi syndrome: clinical and molecular overview. Expert Rev Mol Med. 2007;9(23):1–16.PubMedGoogle Scholar
  50. 50.
    Avvakumov N, Cote J. The MYST family of histone acetyltransferases and their intimate links to cancer. Oncogene. 2007;26(37):5395–407.PubMedGoogle Scholar
  51. 51.
    Iizuka M, Takahashi Y, Mizzen CA, et al. Histone acetyltransferase Hbo1: catalytic activity, cellular abundance, and links to primary cancers. Gene. 2009;436(1–2):108–14.PubMedGoogle Scholar
  52. 52.
    Hyman E, Kauraniemi P, Hautaniemi S, et al. Impact of DNA amplification on gene expression patterns in breast cancer. Cancer Res. 2002;62(21):6240–5.PubMedGoogle Scholar
  53. 53.
    Pollack JR, Sorlie T, Perou CM, et al. Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proc Natl Acad Sci USA. 2002;99(20):12963–8.PubMedGoogle Scholar
  54. 54.
    Fraga MF, Ballestar E, Villar-Garea A, et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet. 2005;37(4):391–400.PubMedGoogle Scholar
  55. 55.
    Pfister S, Rea S, Taipale M, et al. The histone acetyltransferase hMOF is frequently downregulated in primary breast carcinoma and medulloblastoma and constitutes a biomarker for clinical outcome in medulloblastoma. Int J Cancer. 2008;122(6):1207–13.PubMedGoogle Scholar
  56. 56.
    Giangaspero F, Wellek S, Masuoka J, et al. Stratification of medulloblastoma on the basis of histopathological grading. Acta Neuropathol. 2006;112(1):5–12.PubMedGoogle Scholar
  57. 57.
    Elsheikh SE, Green AR, Rakha EA, et al. Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome. Cancer Res. 2009;69(9):3802–9.PubMedGoogle Scholar
  58. 58.
    Gregoretti IV, Lee YM, Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol. 2004;338(1):17–31.PubMedGoogle Scholar
  59. 59.
    de Ruijter AJ, van Gennip AH, Caron HN, et al. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J. 2003;370(Pt 3):737–49.PubMedGoogle Scholar
  60. 60.
    Spange S, Wagner T, Heinzel T, et al. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int J Biochem Cell Biol. 2009;41(1):185–98.PubMedGoogle Scholar
  61. 61.
    Suzuki J, Chen YY, Scott GK, et al. Protein acetylation and histone deacetylase expression associated with malignant breast cancer progression. Clin Cancer Res. 2009;15(9):3163–71.PubMedGoogle Scholar
  62. 62.
    Yang XJ, Gregoire S. Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol Cell Biol. 2005;25(8):2873–84.PubMedGoogle Scholar
  63. 63.
    Yang XJ, Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol. 2008;9(3):206–18.PubMedGoogle Scholar
  64. 64.
    Marks P, Rifkind RA, Richon VM, et al. Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer. 2001;1(3):194–202.PubMedGoogle Scholar
  65. 65.
    Denu JM. The Sir 2 family of protein deacetylases. Curr Opin Chem Biol. 2005;9(5):431–40.PubMedGoogle Scholar
  66. 66.
    Landry J, Sutton A, Tafrov ST, et al. The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases. Proc Natl Acad Sci USA. 2000;97(11):5807–11.PubMedGoogle Scholar
  67. 67.
    Michishita E, Park JY, Burneskis JM, et al. Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell. 2005;16(10):4623–35.PubMedGoogle Scholar
  68. 68.
    Deckert J, Struhl K. Histone acetylation at promoters is differentially affected by specific activators and repressors. Mol Cell Biol. 2001;21(8):2726–35.PubMedGoogle Scholar
  69. 69.
    Gray SG, Ekstrom TJ. The human histone deacetylase family. Exp Cell Res. 2001;262(2):75–83.PubMedGoogle Scholar
  70. 70.
    McLaughlin F, La Thangue NB. Histone deacetylase inhibitors open new doors in cancer therapy. Biochem Pharmacol. 2004;68(6):1139–44.PubMedGoogle Scholar
  71. 71.
    Robertson KD, Ait-Si-Ali S, Yokochi T, et al. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet. 2000;25(3):338–42.PubMedGoogle Scholar
  72. 72.
    Toh Y, Ohga T, Endo K, et al. Expression of the metastasis-associated MTA1 protein and its relationship to deacetylation of the histone H4 in esophageal squamous cell carcinomas. Int J Cancer. 2004;110(3):362–7.PubMedGoogle Scholar
  73. 73.
    Bai X, Wu L, Liang T, et al. Overexpression of myocyte enhancer factor 2 and histone hyperacetylation in hepatocellular carcinoma. J Cancer Res Clin Oncol. 2008;134(1):83–91.PubMedGoogle Scholar
  74. 74.
    Barlesi F, Giaccone G, Gallegos-Ruiz MI, et al. Global histone modifications predict prognosis of resected non small-cell lung cancer. J Clin Oncol. 2007;25(28):4358–64.PubMedGoogle Scholar
  75. 75.
    Yu Y, Xu F, Peng H, et al. NOEY2 (ARHI), an imprinted putative tumor suppressor gene in ovarian and breast carcinomas. Proc Natl Acad Sci USA. 1999;96(1):214–9.PubMedGoogle Scholar
  76. 76.
    Feng W, Lu Z, Luo RZ, et al. Multiple histone deacetylases repress tumor suppressor gene ARHI in breast cancer. Int J Cancer. 2007;120(8):1664–8.PubMedGoogle Scholar
  77. 77.
    Zhang Z, Yamashita H, Toyama T, et al. HDAC6 expression is correlated with better survival in breast cancer. Clin Cancer Res. 2004;10(20):6962–8.PubMedGoogle Scholar
  78. 78.
    Saji S, Kawakami M, Hayashi S, et al. Significance of HDAC6 regulation via estrogen signaling for cell motility and prognosis in estrogen receptor-positive breast cancer. Oncogene. 2005;24(28):4531–9.PubMedGoogle Scholar
  79. 79.
    Duong V, Bret C, Altucci L, et al. Specific activity of class II histone deacetylases in human breast cancer cells. Mol Cancer Res. 2008;6(12):1908–19.PubMedGoogle Scholar
  80. 80.
    Bedford MT. Arginine methylation at a glance. J Cell Sci. 2007;120(Pt 24):4243–6.PubMedGoogle Scholar
  81. 81.
    Wysocka J, Allis CD, Coonrod S. Histone arginine methylation and its dynamic regulation. Front Biosci. 2006;11:344–55.PubMedGoogle Scholar
  82. 82.
    Katz JE, Dlakic M, Clarke S. Automated identification of putative methyltransferases from genomic open reading frames. Mol Cell Proteomics. 2003;2(8):525–40.PubMedGoogle Scholar
  83. 83.
    Chang B, Chen Y, Zhao Y, et al. JMJD6 is a histone arginine demethylase. Science. 2007;318(5849):444–7.PubMedGoogle Scholar
  84. 84.
    Bedford MT, Clarke SG. Protein arginine methylation in mammals: who, what, and why. Mol Cell. 2009;33(1):1–13.PubMedGoogle Scholar
  85. 85.
    Pal S, Sif S. Interplay between chromatin remodelers and protein arginine methyltransferases. J Cell Physiol. 2007;213(2):306–15.PubMedGoogle Scholar
  86. 86.
    Lachner M, Jenuwein T. The many faces of histone lysine methylation. Curr Opin Cell Biol. 2002;14(3):286–98.PubMedGoogle Scholar
  87. 87.
    Feng Q, Wang H, Ng HH, et al. Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr Biol. 2002;12(12):1052–8.PubMedGoogle Scholar
  88. 88.
    Volkel P, Angrand PO. The control of histone lysine methylation in epigenetic regulation. Biochimie. 2007;89(1):1–20.PubMedGoogle Scholar
  89. 89.
    Vakoc CR, Sachdeva MM, Wang H, et al. Profile of histone lysine methylation across transcribed mammalian chromatin. Mol Cell Biol. 2006;26(24):9185–95.PubMedGoogle Scholar
  90. 90.
    Tachibana M, Sugimoto K, Fukushima T, et al. Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J Biol Chem. 2001;276(27):25309–17.PubMedGoogle Scholar
  91. 91.
    Sauvageau M, Sauvageau G. Polycomb group genes: keeping stem cell activity in balance. PLoS Biol. 2008;6(4):e113.PubMedGoogle Scholar
  92. 92.
    Hamamoto R, Furukawa Y, Morita M, et al. SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat Cell Biol. 2004;6(8):731–40.PubMedGoogle Scholar
  93. 93.
    Brown MA, Sims 3rd RJ, Gottlieb PD, et al. Identification and characterization of Smyd2: a split SET/MYND domain-containing histone H3 lysine 36-specific methyltransferase that interacts with the Sin3 histone deacetylase complex. Mol Cancer. 2006;5:26.PubMedGoogle Scholar
  94. 94.
    Davis CA, Haberland M, Arnold MA, et al. PRISM/PRDM6, a transcriptional repressor that promotes the proliferative gene program in smooth muscle cells. Mol Cell Biol. 2006;26(7):2626–36.PubMedGoogle Scholar
  95. 95.
    Gyory I, Wu J, Fejer G, et al. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat Immunol. 2004;5(3):299–308.PubMedGoogle Scholar
  96. 96.
    Lomberk G, Wallrath L, Urrutia R. The heterochromatin protein 1 family. Genome Biol. 2006;7(7):228.PubMedGoogle Scholar
  97. 97.
    Pena PV, Davrazou F, Shi X, et al. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature. 2006;442(7098):100–3.PubMedGoogle Scholar
  98. 98.
    Wang GG, Song J, Wang Z, et al. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature. 2009;459(7248):847–51.PubMedGoogle Scholar
  99. 99.
    Dillon N, Festenstein R. Unravelling heterochromatin: competition between positive and negative factors regulates accessibility. Trends Genet. 2002;18(5):252–8.PubMedGoogle Scholar
  100. 100.
    Shi Y, Lan F, Matson C, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 2004;119(7):941–53.PubMedGoogle Scholar
  101. 101.
    Hakimi MA, Bochar DA, Chenoweth J, et al. A core-BRAF35 complex containing histone deacetylase mediates repression of neuronal-specific genes. Proc Natl Acad Sci USA. 2002;99(11):7420–5.PubMedGoogle Scholar
  102. 102.
    Hakimi MA, Dong Y, Lane WS, et al. A candidate X-linked mental retardation gene is a component of a new family of histone deacetylase-containing complexes. J Biol Chem. 2003;278(9):7234–9.PubMedGoogle Scholar
  103. 103.
    Tong JK, Hassig CA, Schnitzler GR, et al. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature. 1998;395(6705):917–21.PubMedGoogle Scholar
  104. 104.
    You A, Tong JK, Grozinger CM, et al. CoREST is an integral component of the CoREST-human histone deacetylase complex. Proc Natl Acad Sci USA. 2001;98(4):1454–8.PubMedGoogle Scholar
  105. 105.
    Metzger E, Wissmann M, Yin N, et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature. 2005;437(7057):436–9.PubMedGoogle Scholar
  106. 106.
    Klose RJ, Kallin EM, Zhang Y. JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet. 2006;7(9):715–27.PubMedGoogle Scholar
  107. 107.
    Tsukada Y, Fang J, Erdjument-Bromage H, et al. Histone demethylation by a family of JmjC domain-containing proteins. Nature. 2006;439(7078):811–6.PubMedGoogle Scholar
  108. 108.
    Yamane K, Toumazou C, Tsukada Y, et al. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell. 2006;125(3):483–95.PubMedGoogle Scholar
  109. 109.
    Cloos PA, Christensen J, Agger K, et al. The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature. 2006;442(7100):307–11.PubMedGoogle Scholar
  110. 110.
    Fodor BD, Kubicek S, Yonezawa M, et al. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev. 2006;20(12):1557–62.PubMedGoogle Scholar
  111. 111.
    Whetstine JR, Nottke A, Lan F, et al. Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell. 2006;125(3):467–81.PubMedGoogle Scholar
  112. 112.
    Huang Y, Fang J, Bedford MT, et al. Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science. 2006;312(5774):748–51.PubMedGoogle Scholar
  113. 113.
    Iwase S, Lan F, Bayliss P, et al. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell. 2007;128(6):1077–88.PubMedGoogle Scholar
  114. 114.
    Klose RJ, Yan Q, Tothova Z, et al. The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell. 2007;128(5):889–900.PubMedGoogle Scholar
  115. 115.
    Yamane K, Tateishi K, Klose RJ, et al. PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol Cell. 2007;25(6):801–12.PubMedGoogle Scholar
  116. 116.
    Agger K, Cloos PA, Christensen J, et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature. 2007;449(7163):731–4.PubMedGoogle Scholar
  117. 117.
    De Santa F, Totaro MG, Prosperini E, et al. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell. 2007;130(6):1083–94.PubMedGoogle Scholar
  118. 118.
    Hong S, Cho YW, Yu LR, et al. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci USA. 2007;104(47):18439–44.PubMedGoogle Scholar
  119. 119.
    Lan F, Bayliss PE, Rinn JL, et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature. 2007;449(7163):689–94.PubMedGoogle Scholar
  120. 120.
    Krivtsov AV, Armstrong SA. MLL translocations, histone modifications and leukaemia stem-cell development. Nat Rev Cancer. 2007;7(11):823–33.PubMedGoogle Scholar
  121. 121.
    Coles AH, Jones SN. The ING gene family in the regulation of cell growth and tumorigenesis. J Cell Physiol. 2009;218(1):45–57.PubMedGoogle Scholar
  122. 122.
    Garkavtsev I, Kazarov A, Gudkov A, et al. Suppression of the novel growth inhibitor p33ING1 promotes neoplastic transformation. Nat Genet. 1996;14(4):415–20.PubMedGoogle Scholar
  123. 123.
    Tokunaga E, Maehara Y, Oki E, et al. Diminished expression of ING1 mRNA and the correlation with p53 expression in breast cancers. Cancer Lett. 2000;152(1):15–22.PubMedGoogle Scholar
  124. 124.
    Toyama T, Iwase H, Watson P, et al. Suppression of ING1 expression in sporadic breast cancer. Oncogene. 1999;18(37):5187–93.PubMedGoogle Scholar
  125. 125.
    Buyse IM, Shao G, Huang S. The retinoblastoma protein binds to RIZ, a zinc-finger protein that shares an epitope with the adenovirus E1A protein. Proc Natl Acad Sci USA. 1995;92(10):4467–71.PubMedGoogle Scholar
  126. 126.
    Muraoka M, Konishi M, Kikuchi-Yanoshita R, et al. p300 gene alterations in colorectal and gastric carcinomas. Oncogene. 1996;12(7):1565–9.PubMedGoogle Scholar
  127. 127.
    Gibbons RJ. Histone modifying and chromatin remodelling enzymes in cancer and dysplastic syndromes. Hum Mol Genet. 2005;14(Spec No 1):R85–92.PubMedGoogle Scholar
  128. 128.
    Steele-Perkins G, Fang W, Yang XH, et al. Tumor formation and inactivation of RIZ1, an Rb-binding member of a nuclear protein-methyltransferase superfamily. Genes Dev. 2001;15(17):2250–62.PubMedGoogle Scholar
  129. 129.
    Lachner M, O’Carroll D, Rea S, et al. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature. 2001;410(6824):116–20.PubMedGoogle Scholar
  130. 130.
    Peters AH, O’Carroll D, Scherthan H, et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell. 2001;107(3):323–37.PubMedGoogle Scholar
  131. 131.
    Moss TJ, Wallrath LL. Connections between epigenetic gene silencing and human disease. Mutat Res. 2007;618(1–2):163–74.PubMedGoogle Scholar
  132. 132.
    Bracken AP, Pasini D, Capra M, et al. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. Embo J. 2003;22(20):5323–35.PubMedGoogle Scholar
  133. 133.
    Croonquist PA, Van Ness B. The polycomb group protein enhancer of zeste homolog 2 (EZH 2) is an oncogene that influences myeloma cell growth and the mutant ras phenotype. Oncogene. 2005;24(41):6269–80.PubMedGoogle Scholar
  134. 134.
    Kotake Y, Cao R, Viatour P, et al. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev. 2007;21(1):49–54.PubMedGoogle Scholar
  135. 135.
    Yu J, Yu J, Rhodes DR, et al. A polycomb repression signature in metastatic prostate cancer predicts cancer outcome. Cancer Res. 2007;67(22):10657–63.PubMedGoogle Scholar
  136. 136.
    Wei Y, Xia W, Zhang Z, et al. Loss of trimethylation at lysine 27 of histone H3 is a predictor of poor outcome in breast, ovarian, and pancreatic cancers. Mol Carcinog. 2008;47(9):701–6.PubMedGoogle Scholar
  137. 137.
    Mikkelsen TS, Ku M, Jaffe DB, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 2007;448(7153):553–60.PubMedGoogle Scholar
  138. 138.
    Ringrose L, Paro R. Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development. 2007;134(2):223–32.PubMedGoogle Scholar
  139. 139.
    Wen B, Wu H, Shinkai Y, et al. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet. 2009;41(2):246–50.PubMedGoogle Scholar
  140. 140.
    Lu PJ, Sundquist K, Baeckstrom D, et al. A novel gene (PLU-1) containing highly conserved putative DNA/chromatin binding motifs is specifically up-regulated in breast cancer. J Biol Chem. 1999;274(22):15633–45.PubMedGoogle Scholar
  141. 141.
    Buszczak M, Paterno S, Spradling AC. Drosophila stem cells share a common requirement for the histone H2B ubiquitin protease scrawny. Science. 2009;323(5911):248–51.PubMedGoogle Scholar
  142. 142.
    Nakanishi S, Lee JS, Gardner KE, et al. Histone H2BK123 monoubiquitination is the critical determinant for H3K4 and H3K79 trimethylation by COMPASS and Dot1. J Cell Biol. 2009;186(3):371–7.PubMedGoogle Scholar
  143. 143.
    Wu M, Wang PF, Lee JS, et al. Molecular regulation of H3K4 trimethylation by Wdr82, a component of human Set1/COMPASS. Mol Cell Biol. 2008;28(24):7337–44.PubMedGoogle Scholar
  144. 144.
    Ausio J, Abbott DW. The many tales of a tail: carboxyl-terminal tail heterogeneity specializes histone H2A variants for defined chromatin function. Biochemistry. 2002;41(19):5945–9.PubMedGoogle Scholar
  145. 145.
    Sarma K, Reinberg D. Histone variants meet their match. Nat Rev Mol Cell Biol. 2005;6(2):139–49.PubMedGoogle Scholar
  146. 146.
    Malik HS, Henikoff S. Phylogenomics of the nucleosome. Nat Struct Biol. 2003;10(11):882–91.PubMedGoogle Scholar
  147. 147.
    Redon C, Pilch D, Rogakou E, et al. Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev. 2002;12(2):162–9.PubMedGoogle Scholar
  148. 148.
    Suto RK, Clarkson MJ, Tremethick DJ, et al. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat Struct Biol. 2000;7(12):1121–4.PubMedGoogle Scholar
  149. 149.
    Svaren J, Chalkley R. The structure and assembly of active chromatin. Trends Genet. 1990;6(2):52–6.PubMedGoogle Scholar
  150. 150.
    Boulard M, Bouvet P, Kundu TK, et al. Histone variant nucleosomes: structure, function and implication in disease. Subcell Biochem. 2007;41:71–89.PubMedGoogle Scholar
  151. 151.
    Kusch T, Workman JL. Histone variants and complexes involved in their exchange. Subcell Biochem. 2007;41:91–109.PubMedGoogle Scholar
  152. 152.
    Svotelis A, Gevry N, Gaudreau L. Regulation of gene expression and cellular proliferation by histone H2A.Z. Biochem Cell Biol. 2009;87(1):179–88.PubMedGoogle Scholar
  153. 153.
    Francisco DC, Peddi P, Hair JM, et al. Induction and processing of complex DNA damage in human breast cancer cells MCF-7 and nonmalignant MCF-10A cells. Free Radic Biol Med. 2008;44(4):558–69.PubMedGoogle Scholar
  154. 154.
    Kuo LJ, Yang LX. Gamma-H2AX—a novel biomarker for DNA double-strand breaks. In Vivo. 2008;22(3):305–9.PubMedGoogle Scholar
  155. 155.
    Till S, Ladurner AG. Sensing NAD metabolites through macro domains. Front Biosci. 2009;14:3246–58.PubMedGoogle Scholar
  156. 156.
    Ahel D, Horejsi Z, Wiechens N, et al. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science. 2009;325(5945):1240–3.PubMedGoogle Scholar
  157. 157.
    Gottschalk AJ, Timinszky G, Kong SE, et al. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc Natl Acad Sci USA. 2009;106(33):13770–4.PubMedGoogle Scholar
  158. 158.
    Ouararhni K, Hadj-Slimane R, Ait-Si-Ali S, et al. The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev. 2006;20(23):3324–36.PubMedGoogle Scholar
  159. 159.
    Boulikas T. Relation between carcinogenesis, chromatin structure and poly(ADP-ribosylation) (review). Anticancer Res. 1991;11(2):489–527.PubMedGoogle Scholar
  160. 160.
    Timinszky G, Till S, Hassa PO, et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat Struct Mol Biol. 2009;16(9):923–9.PubMedGoogle Scholar
  161. 161.
    Gevry N, Hardy S, Jacques PE, et al. Histone H2A.Z is essential for estrogen receptor signaling. Genes Dev. 2009.Google Scholar
  162. 162.
    Hua S, Kallen CB, Dhar R, et al. Genomic analysis of estrogen cascade reveals histone variant H2A.Z associated with breast cancer progression. Mol Syst Biol. 2008;4:188.PubMedGoogle Scholar
  163. 163.
    Altaf M, Auger A, Covic M, et al. Connection between histone H2A variants and chromatin remodeling complexes. Biochem Cell Biol. 2009;87(1):35–50.PubMedGoogle Scholar
  164. 164.
    Guillemette B, Gaudreau L. Reuniting the contrasting functions of H2A.Z. Biochem Cell Biol. 2006;84(4):528–35.PubMedGoogle Scholar
  165. 165.
    Zlatanova J, Thakar A. H2A.Z: view from the top. Structure. 2008;16(2):166–79.PubMedGoogle Scholar
  166. 166.
    Thatcher TH, Gorovsky MA. Phylogenetic analysis of the core histones H2A, H2B, H3, and H4. Nucleic Acids Res. 1994;22(2):174–9.PubMedGoogle Scholar
  167. 167.
    Iouzalen N, Moreau J, Mechali M. H2A.ZI, a new variant histone expressed during Xenopus early development exhibits several distinct features from the core histone H2A. Nucleic Acids Res. 1996;24(20):3947–52.PubMedGoogle Scholar
  168. 168.
    Jiang W, Guo X, Bhavanandan VP. Histone H2A.F/Z subfamily: the smallest member and the signature sequence. Biochem Biophys Res Commun. 1998;245(2):613–7.PubMedGoogle Scholar
  169. 169.
    Zhang H, Roberts DN, Cairns BR. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell. 2005;123(2):219–31.PubMedGoogle Scholar
  170. 170.
    van Daal A, Elgin SC. A histone variant, H2AvD, is essential in Drosophila melanogaster. Mol Biol Cell. 1992;3(6):593–602.PubMedGoogle Scholar
  171. 171.
    Ridgway P, Brown KD, Rangasamy D, et al. Unique residues on the H2A.Z containing nucleosome surface are important for Xenopus laevis development. J Biol Chem. 2004;279(42):43815–20.PubMedGoogle Scholar
  172. 172.
    Faast R, Thonglairoam V, Schulz TC, et al. Histone variant H2A.Z is required for early mammalian development. Curr Biol. 2001;11(15):1183–7.PubMedGoogle Scholar
  173. 173.
    Krogan NJ, Keogh MC, Datta N, et al. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell. 2003;12(6):1565–76.PubMedGoogle Scholar
  174. 174.
    Larochelle M, Gaudreau L. H2A.Z has a function reminiscent of an activator required for preferential binding to intergenic DNA. Embo J. 2003;22(17):4512–22.PubMedGoogle Scholar
  175. 175.
    Dhillon N, Oki M, Szyjka SJ, et al. H2A.Z functions to regulate progression through the cell cycle. Mol Cell Biol. 2006;26(2):489–501.PubMedGoogle Scholar
  176. 176.
    Rangasamy D, Greaves I, Tremethick DJ. RNA interference demonstrates a novel role for H2A.Z in chromosome segregation. Nat Struct Mol Biol. 2004;11(7):650–5.PubMedGoogle Scholar
  177. 177.
    Rangasamy D, Berven L, Ridgway P, et al. Pericentric heterochromatin becomes enriched with H2A.Z during early mammalian development. Embo J. 2003;22(7):1599–607.PubMedGoogle Scholar
  178. 178.
    Allis CD, Glover CV, Bowen JK, et al. Histone variants specific to the transcriptionally active, amitotically dividing macronucleus of the unicellular eucaryote, Tetrahymena thermophila. Cell. 1980;20(3):609–17.PubMedGoogle Scholar
  179. 179.
    Meneghini MD, Wu M, Madhani HD. Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell. 2003;112(5):725–36.PubMedGoogle Scholar
  180. 180.
    Li B, Pattenden SG, Lee D, et al. Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling. Proc Natl Acad Sci USA. 2005;102(51):18385–90.PubMedGoogle Scholar
  181. 181.
    Park YJ, Dyer PN, Tremethick DJ, et al. A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. J Biol Chem. 2004;279(23):24274–82.PubMedGoogle Scholar
  182. 182.
    Abbott DW, Ivanova VS, Wang X, et al. Characterization of the stability and folding of H2A.Z chromatin particles: implications for transcriptional activation. J Biol Chem. 2001;276(45):41945–9.PubMedGoogle Scholar
  183. 183.
    Millar CB, Xu F, Zhang K, et al. Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev. 2006;20(6):711–22.PubMedGoogle Scholar
  184. 184.
    Raisner RM, Hartley PD, Meneghini MD, et al. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell. 2005;123(2):233–48.PubMedGoogle Scholar
  185. 185.
    Guillemette B, Bataille AR, Gevry N, et al. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 2005;3(12):e384.PubMedGoogle Scholar
  186. 186.
    Adam M, Robert F, Larochelle M, et al. H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol Cell Biol. 2001;21(18):6270–9.PubMedGoogle Scholar
  187. 187.
    Farris SD, Rubio ED, Moon JJ, et al. Transcription-induced chromatin remodeling at the c-myc gene involves the local exchange of histone H2A.Z. J Biol Chem. 2005;280(26):25298–303.PubMedGoogle Scholar
  188. 188.
    Fan JY, Rangasamy D, Luger K, et al. H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol Cell. 2004;16(4):655–61.PubMedGoogle Scholar
  189. 189.
    Swaminathan J, Baxter EM, Corces VG. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev. 2005;19(1):65–76.PubMedGoogle Scholar
  190. 190.
    Sarcinella E, Zuzarte PC, Lau PN, et al. Monoubiquitylation of H2A.Z distinguishes its association with euchromatin or facultative heterochromatin. Mol Cell Biol. 2007;27(18):6457–68.PubMedGoogle Scholar
  191. 191.
    Dunican DS, McWilliam P, Tighe O, et al. Gene expression differences between the microsatellite instability (MIN) and chromosomal instability (CIN) phenotypes in colorectal cancer revealed by high-density cDNA array hybridization. Oncogene. 2002;21(20):3253–7.PubMedGoogle Scholar
  192. 192.
    Zucchi I, Mento E, Kuznetsov VA, et al. Gene expression profiles of epithelial cells microscopically isolated from a breast-invasive ductal carcinoma and a nodal metastasis. Proc Natl Acad Sci USA. 2004;101(52):18147–52.PubMedGoogle Scholar
  193. 193.
    Rhodes DR, Yu J, Shanker K, et al. Large-scale meta-analysis of cancer microarray data identifies common transcriptional profiles of neoplastic transformation and progression. Proc Natl Acad Sci USA. 2004;101(25):9309–14.PubMedGoogle Scholar
  194. 194.
    Dubik D, Shiu RP. Mechanism of estrogen activation of c-myc oncogene expression. Oncogene. 1992;7(8):1587–94.PubMedGoogle Scholar
  195. 195.
    Cheng AS, Jin VX, Fan M, et al. Combinatorial analysis of transcription factor partners reveals recruitment of c-MYC to estrogen receptor-alpha responsive promoters. Mol Cell. 2006;21(3):393–404.PubMedGoogle Scholar
  196. 196.
    Santisteban MS, Kalashnikova T, Smith MM. Histone H2A.Z regulats transcription and is partially redundant with nucleosome remodeling complexes. Cell. 2000;103(3):411–22.PubMedGoogle Scholar
  197. 197.
    Duong V, Licznar A, Margueron R, et al. ERalpha and ERbeta expression and transcriptional activity are differentially regulated by HDAC inhibitors. Oncogene. 2006;25(12):1799–806.PubMedGoogle Scholar
  198. 198.
    Margueron R, Licznar A, Lazennec G, et al. Oestrogen receptor alpha increases p21(WAF1/CIP1) gene expression and the antiproliferative activity of histone deacetylase inhibitors in human breast cancer cells. J Endocrinol. 2003;179(1):41–53.PubMedGoogle Scholar
  199. 199.
    Yi X, Wei W, Wang SY, et al. Histone deacetylase inhibitor SAHA induces ERalpha degradation in breast cancer MCF-7 cells by CHIP-mediated ubiquitin pathway and inhibits survival signaling. Biochem Pharmacol. 2008;75(9):1697–705.PubMedGoogle Scholar
  200. 200.
    Alao JP, Lam EW, Ali S, et al. Histone deacetylase inhibitor trichostatin A represses estrogen receptor alpha-dependent transcription and promotes proteasomal degradation of cyclin D1 in human breast carcinoma cell lines. Clin Cancer Res. 2004;10(23):8094–104.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Université de Toulouse, LBMEToulouseFrance
  2. 2.CNRSToulouseFrance

Personalised recommendations