Linking the epigenetic ‘language’ of covalent histone modifications to cancer

Covalent modifications of histones, such as acetylation, methylation, and phosphorylation, and other epigenetic modulations of the chromatin, such as methylation of DNA and ATP-dependent chromatin reorganisation, can play a major part in the multistep process of carcinogenesis, with far-reaching implications for human biology and human health. This review focuses on how aberrant covalent histone modifications may contribute to the development of a variety of human cancers, and discusses the recent findings with regard to potential therapies.

[1]  D. Moazed,et al.  Heterochromatin and Epigenetic Control of Gene Expression , 2003, Science.

[2]  J. Harbour,et al.  The Rb/E2F pathway: expanding roles and emerging paradigms. , 2000, Genes & development.

[3]  J. Herman,et al.  Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. , 2003, Cancer cell.

[4]  Andrew J. Bannister,et al.  Unsafe SETs: histone lysine methyltransferases and cancer. , 2002, Trends in biochemical sciences.

[5]  M. Cleary,et al.  Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. , 2003, Genes & development.

[6]  J. Gray,et al.  The genetics and genomics of cancer , 2003, Nature Genetics.

[7]  M. Yaniv,et al.  Chromatin modifiers and tumor suppression. , 2001, Biochimica et biophysica acta.

[8]  O. Rozenblatt-Rosen,et al.  The C-terminal SET domains of ALL-1 and TRITHORAX interact with the INI1 and SNR1 proteins, components of the SWI/SNF complex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Jinrong Min,et al.  Structure of the SET domain histone lysine methyltransferase Clr4 , 2002, Nature Structural Biology.

[10]  Cancer: Protective packaging for DNA , 2003, Nature.

[11]  N. Zeleznik-Le,et al.  MLL repression domain interacts with histone deacetylases, the polycomb group proteins HPC2 and BMI-1, and the corepressor C-terminal-binding protein , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  M. Diaz,et al.  Protein Interactions of the MLL PHD Fingers Modulate MLL Target Gene Regulation in Human Cells , 2001, Molecular and Cellular Biology.

[13]  A. Kimchi,et al.  Progress in differentiation induction as a treatment for acute promyelocytic leukemia and beyond. , 2002, Cancer research.

[14]  M. Yaniv,et al.  When the SWI/SNF complex remodels … the cell cycle , 2001, Oncogene.

[15]  V. Saha,et al.  Chromatin Modification, Leukaemia and Implications for Therapy , 2002, British journal of haematology.

[16]  M. Cleary,et al.  Novel SWI/SNF Chromatin-Remodeling Complexes Contain a Mixed-Lineage Leukemia Chromosomal Translocation Partner , 2003, Molecular and Cellular Biology.

[17]  B. Chait,et al.  Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement , 2003, Nature Immunology.

[18]  A. Bird,et al.  Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals , 2003, Nature Genetics.

[19]  M. Szyf,et al.  Targeting DNA methylation in cancer , 2003, Ageing Research Reviews.

[20]  A. Beaudet.  Is medical genetics neglecting epigenetics? , 2002, Genetics in Medicine.

[21]  R. Krumlauf.  Hox genes in vertebrate development , 1994, Cell.

[22]  E. Meese,et al.  The MLL fusion partner AF10 binds GAS41, a protein that interacts with the human SWI/SNF complex. , 2002, Blood.

[23]  J. Davie,et al.  Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. , 2001, Genes & development.

[24]  E. Rogakou,et al.  Histone H2A variants H2AX and H2AZ. , 2002, Current opinion in genetics & development.

[25]  J. Davie,et al.  Transcriptional Control: An Activating Role for Arginine Methylation , 2002, Current Biology.

[26]  M. Esteller.  Relevance of DNA methylation in the management of cancer. , 2003, The Lancet. Oncology.

[27]  C. Allis,et al.  Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. , 2000, Molecular cell.

[28]  T. Ried,et al.  H2AX Haploinsufficiency Modifies Genomic Stability and Tumor Susceptibility , 2003, Cell.

[29]  C. Allis,et al.  The language of covalent histone modifications , 2000, Nature.

[30]  K. Hoang-Xuan,et al.  Spectrum of hSNF5/INI1 somatic mutations in human cancer and genotype-phenotype correlations. , 1999, Human molecular genetics.

[31]  C. Allis,et al.  Histone methylation versus histone acetylation: new insights into epigenetic regulation. , 2001, Current opinion in cell biology.

[32]  A. Wolffe,et al.  The nucleosome: a powerful regulator of transcription. , 1998, Progress in nucleic acid research and molecular biology.

[33]  M. Loda,et al.  The EZH2 polycomb transcriptional repressor--a marker or mover of metastatic prostate cancer? , 2002, Cancer cell.

[34]  C. Allis,et al.  Histone and chromatin cross-talk. , 2003, Current opinion in cell biology.

[35]  D. Housman,et al.  MLL is fused to CBP, a histone acetyltransferase, in therapy-related acute myeloid leukemia with a t(11;16)(q23;p13.3). , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Youngchang Kim,et al.  Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. , 2003, Genes & development.

[37]  Thomas A Milne,et al.  MLL targets SET domain methyltransferase activity to Hox gene promoters. , 2002, Molecular cell.

[38]  Wei-Hua Wu,et al.  ATP-Driven Exchange of Histone H2AZ Variant Catalyzed by SWR1 Chromatin Remodeling Complex , 2004, Science.

[39]  Shi Huang.  Histone methyltransferases, diet nutrients and tumour suppressors , 2002, Nature Reviews Cancer.

[40]  S. Henikoff,et al.  Histone H3 variants specify modes of chromatin assembly , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[41]  M. Lachner.  Epigenetics: SUPERMAN Dresses Up , 2002, Current Biology.

[42]  M. Cleary,et al.  Dimerization contributes to oncogenic activation of MLL chimeras in acute leukemias. , 2003, Cancer cell.

[43]  Michel C. Nussenzweig,et al.  Genomic Instability in Mice Lacking Histone H2AX , 2002, Science.

[44]  M. Groudine,et al.  Controlling the double helix , 2003, Nature.

[45]  Samantha G. Zeitlin,et al.  CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis , 2001, The Journal of cell biology.

[46]  B R Das,et al.  Increased ADP-ribosylation of histones in oral cancer. , 1993, Cancer letters.

[47]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[48]  V. Yamazaki,et al.  A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage , 2000, Current Biology.

[49]  B M Turner,et al.  Histone acetylation and an epigenetic code. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[50]  G. Maul,et al.  Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. , 2003, Genes & development.

[51]  C. Pabo,et al.  Gene-Specific Targeting of H3K9 Methylation Is Sufficient for Initiating Repression In Vivo , 2002, Current Biology.

[52]  J. Hess,et al.  Dimerization of MLL fusion proteins immortalizes hematopoietic cells. , 2003, Cancer cell.

[53]  Andrew J. Bannister,et al.  Histone Methylation Dynamic or Static? , 2002, Cell.

[54]  M. Stallcup,et al.  Role of protein methylation in chromatin remodeling and transcriptional regulation , 2001, Oncogene.

[55]  Robert Brown,et al.  Epigenomics and epigenetic therapy of cancer. , 2002, Trends in molecular medicine.

[56]  T. Tomonaga,et al.  Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. , 2003, Cancer research.

[57]  John M. Maris,et al.  Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia , 1999, Nature Genetics.

[58]  M. Cleary,et al.  Molecular mechanisms of leukemogenesis mediated by MLL fusion proteins , 2001, Oncogene.

[59]  S. Gonzalo,et al.  Linking the Rb and polycomb pathways. , 2001, Molecular cell.

[60]  B. Dunn.  Hypomethylation: One Side of a Larger Picture , 2003, Annals of the New York Academy of Sciences.

[61]  P. Laird.  Early detection: The power and the promise of DNA methylation markers , 2003, Nature Reviews Cancer.

[62]  Michael Grunstein,et al.  Histone acetylation and deacetylation in yeast , 2003, Nature Reviews Molecular Cell Biology.

[63]  Andrew J. Bannister,et al.  Rb targets histone H3 methylation and HP1 to promoters , 2001, Nature.

[64]  D. Gottschling,et al.  The Histone Minority Report the Variant Shall Not Be Silenced , 2003, Cell.

[65]  M. Yaniv,et al.  ATP-dependent chromatin remodelling: SWI/SNF and Co. are on the job. , 1999, Journal of molecular biology.

[66]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[67]  F. Alt,et al.  Histone H2AX A Dosage-Dependent Suppressor of Oncogenic Translocations and Tumors , 2003, Cell.

[68]  S. Schreiber,et al.  Signaling Network Model of Chromatin , 2002, Cell.

[69]  S. Dhanasekaran,et al.  The polycomb group protein EZH2 is involved in progression of prostate cancer , 2002, Nature.

[70]  En Li,et al.  Suv 39 h-Mediated Histone H 3 Lysine 9 Methylation Directs DNA Methylation to Major Satellite Repeats at Pericentric Heterochromatin , 2003 .

[71]  S. Knuutila,et al.  11q Deletions in Hematological Malignancies , 2001, Leukemia & lymphoma.

[72]  D. Reinberg,et al.  Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. , 2001, Genes & development.

[73]  S. Korsmeyer,et al.  The role of MLL in hematopoiesis and leukemia , 2002, Current opinion in hematology.

[74]  G. Nucifora,et al.  Genetic lesions and perturbation of chromatin architecture: A road to cell transformation , 2001, Journal of cellular biochemistry.

[75]  T. Hashimshony,et al.  The role of DNA methylation in setting up chromatin structure during development , 2003, Nature Genetics.

[76]  Wolfgang Fischle,et al.  Binary switches and modification cassettes in histone biology and beyond , 2003, Nature.

[77]  M. Osborne,et al.  Groucho/TLE/R-esp proteins associate with the nuclear matrix and repress RUNX (CBF(alpha)/AML/PEBP2(alpha)) dependent activation of tissue-specific gene transcription. , 2000, Journal of cell science.

[78]  R. Kingston,et al.  Stabilization of Chromatin Structure by PRC1, a Polycomb Complex , 1999, Cell.

[79]  C. Allis,et al.  Translating the Histone Code , 2001, Science.