Cancer epigenomics: DNA methylomes and histone-modification maps

Nature Reviews Genetics - Tập 8 Số 4 - Trang 286-298 - 2007
Manel Esteller1
1Cancer Epigenetics Laboratory, Spanish National Cancer Centre (CNIO), Melchor Fernandez Almagro 3, 28029 Madrid, Spain

Tóm tắt

Từ khóa


Tài liệu tham khảo

Herman, J. G. & Baylin, S. B. Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349, 2042–2054 (2003).

Feinberg, A. P. & Tycko, B. The history of cancer epigenetics. Nature Rev. Cancer 4, 143–153 (2004).

Egger, G., Liang, G., Aparicio, A. & Jones, P. A. Epigenetics in human disease and prospects for epigenetic therapy. Nature 429, 457–463 (2004).

Esteller, M. Aberrant DNA methylation as a cancer-inducing mechanism. Annu. Rev. Pharmacol. Toxicol. 45, 629–656 (2005).

Nguyen, C. T., Gonzales, F. A. & Jones, P. A. Altered chromatin structure associated with methylation-induced gene silencing in cancer cells: correlation of accessibility, methylation, MeCP2 binding and acetylation. Nucleic Acids Res. 29, 4598–4606 (2001).

Fahrner, J. A., Eguchi, S., Herman, J. G. & Baylin, S. B. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res. 62, 7213–7218 (2002).

Ballestar, E. et al. Methyl-CpG binding proteins identify novel sites of epigenetic inactivation in human cancer. EMBO J. 22, 6335–6345 (2003).

Fraga, M. F. et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nature Genet. 37, 391–400 (2005). The first report of a common disruption of histone- modification patterns in cancer cells.

Pruitt, K. et al. Inhibition of SIRT1 reactivates silenced cancer genes without loss of promoter DNA hypermethylation. PLoS Genet. 2, e40 (2006).

Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57–70 (2000).

Walsh, C. P., Chaillet, J. R. & Bestor, T. H. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nature Genet. 20, 116–117 (1998).

Gaudet, F. et al. Induction of tumors in mice by genomic hypomethylation. Science 300, 489–492 (2003).

Esteller, M. & Almouzni, G. How epigenetics integrates nuclear functions. Workshop on epigenetics and chromatin: transcriptional regulation and beyond. EMBO Rep. 6, 624–628 (2005).

Reik, W. & Lewis, A. Co-evolution of X-chromosome inactivation and imprinting in mammals. Nature Rev. Genet. 6, 403–410 (2005).

Bodey, B. Cancer-testis antigens: promising targets for antigen directed antineoplastic immunotherapy. Expert Opin. Biol. Ther. 2, 577–584 (2002).

Futscher, B. W. et al. Role for DNA methylation in the control of cell type specific maspin expression. Nature Genet. 31, 175–179 (2002).

Kaneda, A. & Feinberg, A. P. Loss of imprinting of IGF2: a common epigenetic modifier of intestinal tumor risk. Cancer Res. 65, 11236–11240 (2005).

Wade, P. A. Methyl CpG-binding proteins and transcriptional repression. BioEssays 23, 1131–1137 (2001).

Dobosy, J. R. & Selker, E. U. Emerging connections between DNA methylation and histone acetylation. Cell. Mol. Life Sci. 58, 721–727 (2001).

Wang, Y. et al. Beyond the double helix: writing and reading the histone code. Novartis Found. Symp. 259, 3–17 (2004).

Sanders, S. L. et al. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119, 603–614 (2004).

Espada, J. et al. Human DNA methyltransferase 1 is required for maintenance of the histone H3 modification pattern. J. Biol. Chem. 279, 37175–37184 (2004).

Seligson, D. B. et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature 435, 1262–1266 (2005). The first profile of histone modifications in cancer with prognostic relevance.

Barbacid, M. ras genes. Annu. Rev. Biochem. 56, 779–827 (1987).

Fraga, M. F. & Esteller, M. DNA methylation: a profile of methods and applications. Biotechniques 33, 632–649 (2002).

Clark, S. J., Harrison, J., Paul, C. L. & Frommer, M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22, 2990–2997 (1994).

Herman, J. G. et al. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl Acad. Sci. USA 93, 9821–9826 (1996).

Eads, C. A. et al. MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res. 28, e32 (2000).

Uhlmann, K. et al. Evaluation of a potential epigenetic biomarker by quantitative methyl-single nucleotide polymorphism analysis. Electrophoresis 23, 4072–4079 (2002).

Costello, J. F. et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nature Genet. 24, 132–138 (2000). One of the first studies to define the number of hypermethylated CpG islands in cancer cells and their distribution according to tumour type.

Zardo, G. et al. Integrated genomic and epigenomic analyses pinpoint biallelic gene inactivation in tumors. Nature Genet. 32, 453–458 (2002).

Welsh, J. & McClelland, M. Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res. 18, 7213–7218 (1990).

Gonzalgo, M. L. et al. Identification and characterization of differentially methylated regions of genomic DNA by methylation-sensitive arbitrarily primed PCR. Cancer Res. 57, 594–599 (1997).

Toyota, M. et al. Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification. Cancer Res. 59, 2307–2312 (1999).

Frigola, J., Ribas, M., Risques, R. A. & Peinado, M. A. Methylome profiling of cancer cells by amplification of inter-methylated sites (AIMS). Nucleic Acids Res. 30, e28 (2002).

Huang, T. H., Perry, M. R. & Laux, D. E. Methylation profiling of CpG islands in human breast cancer cells. Hum. Mol. Genet. 8, 459–470 (1999).

Khulan, B. et al. Comparative isoschizomer profiling of cytosine methylation: the HELP assay. Genome Res. 16, 1046–1055 (2006).

Lopez-Serra, L. et al. A profile of MBD protein occupancy of hypermethylated promoter CpG islands of tumor suppressor genes in human cancer. Cancer Res. 66, 8342–8346 (2006).

Weber, M. et al. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nature Genet. 37, 853–862 (2005). The first report of the use of methyl-DIP, a powerful epigenomic technique for identifying DNA-methylation changes in transformed cells.

Keshet, I. et al. Evidence for an instructive mechanism of de novo methylation in cancer cells. Nature Genet. 38, 149–153 (2006). This paper reports extensive mapping of DNA-methylation changes in cancer cells using methyl-DIP.

Zhang, X. et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126, 1189–1201 (2006). A ground-breaking study that combines methyl-DIP and tiling arrays, providing the first example of an almost complete DNA methylome in one organism.

Suzuki, H. et al. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nature Genet. 31, 141–149 (2002).

Yamashita, K. et al. Pharmacologic unmasking of epigenetically silenced tumor suppressor genes in esophageal squamous cell carcinoma. Cancer Cell 2, 485–495 (2002). References 42 and 43 describe pioneering studies that combine DNA-demethylating agents and expression microarrays to reveal methylation-associated silencing in cancer cells.

Fraga, M. F. et al. A mouse skin multistage carcinogenesis model reflects the aberrant DNA methylation patterns of human tumors. Cancer Res. 64, 5527–5534 (2004).

O'Neill, L. P., Vermilyea, M. D. & Turner, B. M. Epigenetic characterization of the early embryo with a chromatin immunoprecipitation protocol applicable to small cell populations. Nature Genet. 38, 835–841 (2006).

Lippman, Z. et al. Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471–476 (2004).

Kurdistani, S. K., Tavazoie, S. & Grunstein, M. Mapping global histone acetylation patterns to gene expression. Cell 117, 721–733 (2004). A pioneering study in which histone-modification changes in yeast were analysed by ChIP-on-chip.

Pokholok, D. K. et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122, 517–527 (2005).

Schubeler, D. et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18, 1263–1271 (2004).

Martens, J. H. et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800–812 (2005).

Bernstein, B. E. et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120, 169–181 (2005).

Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315–326 (2006).

Azuara, V. et al. Chromatin signatures of pluripotent cell lines. Nature Cell Biol. 8, 532–538 (2006).

Yu, L. et al. Global assessment of promoter methylation in a mouse model of cancer identifies ID4 as a putative tumor-suppressor gene in human leukemia. Nature Genet. 37, 265–274 (2005).

Esteller, M., Corn, P. G., Baylin, S. B. & Herman, J. G. A gene hypermethylation profile of human cancer. Cancer Res. 8, 3225–3229 (2001). The most comprehensive analysis of promoter CpG-island hypermethylation in human cancer using a candidate-gene approach.

Paz, M. F. et al. A systematic profile of DNA methylation in human cancer cell lines. Cancer Res. 63, 1114–1121 (2003).

Sjoblom, T. et al. The consensus coding sequences of human breast and colorectal cancers. Science 314, 268–274 (2006).

Paz, M. F. et al. Genetic unmasking of epigenetically silenced tumor suppressor genes in colon cancer cells deficient in DNA methyltransferases. Hum. Mol. Genet. 12, 2209–2219 (2003).

Saito, Y. et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9, 435–443 (2006).

Lujambio, A. et al. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 67, 1424–1429 (2007). References 59 and 60 describe the first examples of CpG-island methylation-associated silencing of microRNAs in human cancer.

Schlesinger, Y. et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nature Genet. 39, 232–236 (2006).

Widschwendter, M. et al. Epigenetic stem cell signature in cancer. Nature Genet. 39, 157–158 (2006).

Di Croce, L. et al. Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 295, 1079–1082 (2002).

Esteller, M. et al. Cancer epigenetics and methylation. Science 297, 1807–1808 (2002).

Brenner, C. et al. Myc represses transcription through recruitment of DNA methyltransferase corepressor. EMBO J. 24, 336–346 (2005).

Vire, E. et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871–874 (2006).

Richon, V. M., Sandhoff, T. W., Rifkind R. A. & Marks, P. A. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc. Natl Acad. Sci. USA 97, 10014–10019 (2000).

Esteller, M. & Herman, J. G. Generating mutations but providing chemosensitivity: the role of O6-methylguanine DNA methyltransferase in human cancer. Oncogene 23, 1–8 (2004).

Tryndyak, V. P., Kovalchuk, O. & Pogribny, I. P. Loss of DNA methylation and histone H4 lysine 20 trimethylation in human breast cancer cells is associated with aberrant expression of DNA methyltransferase 1, Suv4–20h2 histone methyltransferase and methyl-binding proteins. Cancer Biol. Ther. 5, 65–70 (2006).

Pogribny, I. P. et al. Histone H3 lysine 9 and H4 lysine 20 trimethylation and the expression of Suv4–20h2 and Suv-39h1 histone methyltransferases in hepatocarcinogenesis induced by methyl deficiency in rats. Carcinogenesis 27, 1180–1186 (2006).

Jacobsen, S. E. & Meyerowitz, E. M. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277, 1100–1103 (1997).

Mager, J. & Bartolomei, M. S. Strategies for dissecting epigenetic mechanisms in the mouse. Nature Genet. 37, 1194–1200 (2005).

Ozdag, H. et al. Differential expression of selected histone modifier genes in human solid cancers. BMC Genomics 7, 90 (2006).

Yang, X. J. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 32, 959–976 (2004).

Moore, S. D. et al. Uterine leiomyomata with t(10;17) disrupt the histone acetyltransferase MORF. Cancer Res. 64, 5570–5577 (2004).

Peters, A. H. et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323–337 (2001).

Ropero, S. et al. A truncating mutation of HDAC2 in human cancers confers resistance to histone deacetylase inhibition. Nature Genet. 38, 566–569 (2006). The first-described disruption of a histone deacetylase in human cancer provides a basis for further pharmacogenomic studies.

Varmus, H. & Stillman, B. Support for the Human Cancer Genome Project. Science 310, 1615 (2005).

Lee, W. H. et al. Cytidine methylation of regulatory sequences near the pi-class glutathione S-transferase gene accompanies human prostatic carcinogenesis. Proc. Natl Acad. Sci. USA 91, 11733–11737 (1994).

Cairns, P. et al. Molecular detection of prostate cancer in urine by GSTP1 hypermethylation. Clin. Cancer Res. 7, 2727–2730 (2001).

Laird, P. W. The power and the promise of DNA methylation markers. Nature Rev. Cancer 3, 253–266 (2003).

Baylin, S. B. & Ohm, J. E. Epigenetic gene silencing in cancer — a mechanism for early oncogenic pathway addiction? Nature Rev. Cancer 6, 107–116 (2006).

Gallagher, W. M. et al. Multiple markers for melanoma progression regulated by DNA methylation: insights from transcriptomic studies. Carcinogenesis 26, 1856–1867 (2005).

Esteller, M. et al. DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis. Hum. Mol. Genet. 10, 3001–3007 (2001).

Alaminos, M. et al. Clustering of gene hypermethylation associated with clinical risk groups in neuroblastoma. J. Natl Cancer Inst. 96, 1208–1219 (2004).

Tsou, J. A. et al. Distinct DNA methylation profiles in malignant mesothelioma, lung adenocarcinoma, and non-tumor lung. Lung Cancer 47, 193–204 (2005).

Wei, S. H. et al. Prognostic DNA methylation biomarkers in ovarian cancer. Clin. Cancer Res. 12, 2788–2794 (2006).

Esteller, M. et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N. Engl. J. Med. 343, 1350–1354 (2000). The first translational use of a hypermethylated CpG island in the management of cancer patients.

Hegi, M. E. et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352, 997–1003 (2005).

Esteller, M. et al. Hypermethylation of the DNA repair gene O(6)-methylguanine DNA methyltransferase and survival of patients with diffuse large B-cell lymphoma. J. Natl Cancer Inst. 94, 26–32 (2002).

Glasspool, R. M., Teodoridis, J. M. & Brown, R. Epigenetics as a mechanism driving polygenic clinical drug resistance. Br. J. Cancer 94, 1087–1092 (2006).

Mack, G. S. Epigenetic cancer therapy makes headway. J. Natl Cancer Inst. 98, 1443–1444 (2006).

Thompson, C. A. Vorinostat approved for rare lymphoma. Am. J. Health Syst. Pharm. 63, 2168 (2006).

Seo, S. & Kroll, K. L. Geminin's double life: chromatin connections that regulate transcription at the transition from proliferation to differentiation. Cell Cycle 5, 374–379 (2006).

Jones, P. A. & Martienssen, R. A blueprint for a Human Epigenome Project: the AACR Human Epigenome Workshop. Cancer Res. 65, 11241–11246 (2005).

Rauscher, F. J. It is time for a Human Epigenome Project. Cancer Res. 65, 11229 (2005).

Garber, K. Momentum building for Human Epigenome Project. J. Natl Cancer Inst. 98, 84–86 (2006).

Esteller, M. The necessity of a Human Epigenome Project. Carcinogenesis 27, 1121–1125 (2006).

Zilberman, D. et al. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nature Genet. 39, 61–69 (2006). A high-resolution map of the A . thaliana DNA methylome that addresses its relationship to gene-expression patterns.

Rakian, V. K. et al. DNA methylation profiling of the human major histocompatibility complex: a pilot study for the Human Epigenome Project. PLoS Biol. 2, e405 (2004).

Fraga, M. F. et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl Acad. Sci. USA 102, 10604–10609 (2005). A comprehensive epigenomic study that demonstrates the presence of DNA methylation and histone modifications in individuals who have the same genetic background.

Frigola, J. et al. Epigenetic remodeling in colorectal cancer results in coordinate gene suppression across an entire chromosome band. Nature Genet. 38, 540–549 (2006).

Stransky, N. et al. Regional copy number-independent deregulation of transcription in cancer. Nature Genet. 38, 1386–1396 (2006).

Eckhardt, F. et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nature Genet. 38, 1378–1385 (2006).