Human Molecular Genetics, 2001, Vol. 10, No. 7 687-692
© 2001 Oxford University Press
Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer
The Johns Hopkins Comprehensive Cancer Center and Johns Hopkins Medical Institutions, Baltimore, MD 21231, USA
Gene function in cancer can be disrupted either through genetic alterations, which directly mutate or delete genes, or epigenetic alterations, which alter the heritable state of gene expression. The latter events are mediated by formation of transcriptionally repressive chromatin states around gene transcription start sites and an associated gain of methylation in normally unmethylated CpG islands in these regions. The genes affected include over half of the tumor suppressor genes that cause familial cancers when mutated in the germline; the selective advantage for genetic and epigenetic dysfunction in these genes is very similar. The aberrant methylation can begin very early in tumor progression and mediate most of the important pathway abnormalities in cancer including loss of cell cycle control, altered function of transcription factors, altered receptor function, disruption of normal cell–cell and cell–substratum interaction, inactivation of signal transduction pathways, loss of apoptotic signals and genetic instability. The active role of the aberrant methylation in transcriptional silencing of genes is becoming increasingly understood and involves a synergy between the methylation and histone deacetylase (HDAC) activity. This synergy can be mediated directly by HDAC interaction with DNA methylating enzymes and by recruitment through complexes involving methyl-cytosine binding proteins. In the translational arena, the promoter hypermethylation changes hold great promise as DNA tumor markers and their potentially reversible state creates a target for cancer therapeutic strategies involving gene reactivation.
+ To whom correspondence should be addressed. Tel: +1 410 955 8506; Fax: +1 410 614 9884; Email: sbaylin@jhmi.edu
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Y. Cohen, G. Singer, O. Lavie, S. M. Dong, U. Beller, and D. Sidransky The RASSF1A Tumor Suppressor Gene Is Commonly Inactivated in Adenocarcinoma of the Uterine Cervix Clin. Cancer Res., August 1, 2003; 9(8): 2981 - 2984. [Abstract] [Full Text] [PDF]
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P.-F. Cartron, P. Juin, L. Oliver, S. Martin, K. Meflah, and F. M. Vallette Nonredundant Role of Bax and Bak in Bid-Mediated Apoptosis Mol. Cell. Biol., July 1, 2003; 23(13): 4701 - 4712. [Abstract] [Full Text] [PDF]
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N. Fujita, S. Watanabe, T. Ichimura, S. Tsuruzoe, Y. Shinkai, M. Tachibana, T. Chiba, and M. Nakao Methyl-CpG Binding Domain 1 (MBD1) Interacts with the Suv39h1-HP1 Heterochromatic Complex for DNA Methylation-based Transcriptional Repression J. Biol. Chem., June 20, 2003; 278(26): 24132 - 24138. [Abstract] [Full Text] [PDF]
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W.-G. Zhu, K. Srinivasan, Z. Dai, W. Duan, L. J. Druhan, H. Ding, L. Yee, M. A. Villalona-Calero, C. Plass, and G. A. Otterson Methylation of Adjacent CpG Sites Affects Sp1/Sp3 Binding and Activity in the p21Cip1 Promoter Mol. Cell. Biol., June 15, 2003; 23(12): 4056 - 4065. [Abstract] [Full Text] [PDF]
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H. Kimura, T. Nakamura, T. Ogawa, S. Tanaka, and K. Shiota Transcription of mouse DNA methyltransferase 1 (Dnmt1) is regulated by both E2F-Rb-HDAC-dependent and -independent pathways Nucleic Acids Res., June 15, 2003; 31(12): 3101 - 3113. [Abstract] [Full Text] [PDF]
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F. Tschentscher, J. Husing, T. Holter, E. Kruse, I. G. Dresen, K.-H. Jockel, G. Anastassiou, H. Schilling, N. Bornfeld, B. Horsthemke, et al. Tumor Classification Based on Gene Expression Profiling Shows That Uveal Melanomas with and without Monosomy 3 Represent Two Distinct Entities Cancer Res., May 15, 2003; 63(10): 2578 - 2584. [Abstract] [Full Text] [PDF]
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V. T. Mihaylova, R. S. Bindra, J. Yuan, D. Campisi, L. Narayanan, R. Jensen, F. Giordano, R. S. Johnson, S. Rockwell, and P. M. Glazer Decreased Expression of the DNA Mismatch Repair Gene Mlh1 under Hypoxic Stress in Mammalian Cells Mol. Cell. Biol., May 1, 2003; 23(9): 3265 - 3273. [Abstract] [Full Text] [PDF]
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M. Xing, H. Usadel, Y. Cohen, Y. Tokumaru, Z. Guo, W. B. Westra, B. C. Tong, G. Tallini, R. Udelsman, J. A. Califano, et al. Methylation of the Thyroid-stimulating Hormone Receptor Gene in Epithelial Thyroid Tumors: A Marker of Malignancy and a Cause of Gene Silencing Cancer Res., May 1, 2003; 63(9): 2316 - 2321. [Abstract] [Full Text] [PDF]
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K. Liu, Y. F. Wang, C. Cantemir, and M. T. Muller Endogenous Assays of DNA Methyltransferases: Evidence for Differential Activities of DNMT1, DNMT2, and DNMT3 in Mammalian Cells In Vivo Mol. Cell. Biol., April 15, 2003; 23(8): 2709 - 2719. [Abstract] [Full Text] [PDF]
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P. K. Sengupta, E. M. Smith, K. Kim, M. J. Murnane, and B. D. Smith DNA Hypermethylation Near the Transcription Start Site of Collagen {alpha}2(I) Gene Occurs in Both Cancer Cell Lines and Primary Colorectal Cancers Cancer Res., April 15, 2003; 63(8): 1789 - 1797. [Abstract] [Full Text] [PDF]
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O. Galm, H. Yoshikawa, M. Esteller, R. Osieka, and J. G. Herman SOCS-1, a negative regulator of cytokine signaling, is frequently silenced by methylation in multiple myeloma Blood, April 1, 2003; 101(7): 2784 - 2788. [Abstract] [Full Text] [PDF]
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K. Ghoshal, J. Datta, S. Majumder, S. Bai, X. Dong, M. Parthun, and S. T. Jacob Inhibitors of Histone Deacetylase and DNA Methyltransferase Synergistically Activate the Methylated Metallothionein I Promoter by Activating the Transcription Factor MTF-1 and Forming an Open Chromatin Structure Mol. Cell. Biol., December 1, 2002; 22(23): 8302 - 8319. [Abstract] [Full Text] [PDF]
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M. A. Harding, K. C. Arden, J. W. Gildea, J. J. Gildea, E. J. Perlman, C. Viars, and D. Theodorescu Functional Genomic Comparison of Lineage-related Human Bladder Cancer Cell Lines with Differing Tumorigenic and Metastatic Potentials by Spectral Karyotyping, Comparative Genomic Hybridization, and a Novel Method of Positional Expression Profiling Cancer Res., December 1, 2002; 62(23): 6981 - 6989. [Abstract] [Full Text] [PDF]
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H. Yatsuki, K. Joh, K. Higashimoto, H. Soejima, Y. Arai, Y. Wang, I. Hatada, Y. Obata, H. Morisaki, Z. Zhang, et al. Domain Regulation of Imprinting Cluster in Kip2/Lit1 Subdomain on Mouse Chromosome 7F4/F5: Large-Scale DNA Methylation Analysis Reveals That DMR-Lit1 Is a Putative Imprinting Control Region Genome Res., December 1, 2002; 12(12): 1860 - 1870. [Abstract] [Full Text] [PDF]
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M. Koslowski, O. Tureci, C. Bell, P. Krause, H.-A. Lehr, J. Brunner, G. Seitz, F. O. Nestle, C. Huber, and U. Sahin Multiple Splice Variants of Lactate Dehydrogenase C Selectively Expressed in Human Cancer , Cancer Res., November 15, 2002; 62(22): 6750 - 6755. [Abstract] [Full Text] [PDF]
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M. E. Lusher, J. C. Lindsey, F. Latif, A. D. J. Pearson, D. W. Ellison, and S. C. Clifford Biallelic Epigenetic Inactivation of the RASSF1A Tumor Suppressor Gene in Medulloblastoma Development Cancer Res., October 15, 2002; 62(20): 5906 - 5911. [Abstract] [Full Text] [PDF]
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Y. Nie, J. Liao, X. Zhao, Y. Song, G.-y. Yang, L.-D. Wang, and C. S. Yang Detection of multiple gene hypermethylation in the development of esophageal squamous cell carcinoma Carcinogenesis, October 1, 2002; 23(10): 1713 - 1720. [Abstract] [Full Text] [PDF]
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Z. Dai, D. Weichenhan, Y.-Z. Wu, J. L Hall, L. J. Rush, L. T. Smith, A. Raval, L. Yu, D. Kroll, J. Muehlisch, et al. An AscI Boundary Library for the Studies of Genetic and Epigenetic Alterations in CpG Islands Genome Res., October 1, 2002; 12(10): 1591 - 1598. [Abstract] [Full Text] [PDF]
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K. Ogi, M. Toyota, M. Ohe-Toyota, N. Tanaka, M. Noguchi, T. Sonoda, G. Kohama, and T. Tokino Aberrant Methylation of Multiple Genes and Clinicopathological Features in Oral Squamous Cell Carcinoma Clin. Cancer Res., October 1, 2002; 8(10): 3164 - 3171. [Abstract] [Full Text] [PDF]
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 S. Zochbauer-Muller, J. D. Minna, and A. F. Gazdar Aberrant DNA Methylation in Lung Cancer: Biological and Clinical Implications Oncologist, October 1, 2002; 7(5): 451 - 457. [Abstract] [Full Text] [PDF]
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M. F. Paz, S. Avila, M. F. Fraga, M. Pollan, G. Capella, M. A. Peinado, M. Sanchez-Cespedes, J. G. Herman, and M. Esteller Germ-Line Variants in Methyl-Group Metabolism Genes and Susceptibility to DNA Methylation in Normal Tissues and Human Primary Tumors Cancer Res., August 1, 2002; 62(15): 4519 - 4524. [Abstract] [Full Text] [PDF]
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Y. Saito, Y. Kanai, M. Sakamoto, H. Saito, H. Ishii, and S. Hirohashi Overexpression of a splice variant of DNA methyltransferase 3b, DNMT3b4, associated with DNA hypomethylation on pericentromeric satellite regions during human hepatocarcinogenesis PNAS, July 23, 2002; 99(15): 10060 - 10065. [Abstract] [Full Text] [PDF]
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E. Ballestar and M. Esteller The impact of chromatin in human cancer: linking DNA methylation to gene silencing Carcinogenesis, July 1, 2002; 23(7): 1103 - 1109. [Abstract] [Full Text] [PDF]
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S. H. Wei, C.-M. Chen, G. Strathdee, J. Harnsomburana, C.-R. Shyu, F. Rahmatpanah, H. Shi, S.-W. Ng, P. S. Yan, K. P. Nephew, et al. Methylation Microarray Analysis of Late-Stage Ovarian Carcinomas Distinguishes Progression-free Survival in Patients and Identifies Candidate Epigenetic Markers Clin. Cancer Res., July 1, 2002; 8(7): 2246 - 2252. [Abstract] [Full Text] [PDF]
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H. Shi, P. S. Yan, C.-M. Chen, F. Rahmatpanah, C. Lofton-Day, C. W. Caldwell, and T. H.-M. Huang Expressed CpG Island Sequence Tag Microarray for Dual Screening of DNA Hypermethylation and Gene Silencing in Cancer Cells Cancer Res., June 1, 2002; 62(11): 3214 - 3220. [Abstract] [Full Text] [PDF]
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S. Majumder, K. Ghoshal, J. Datta, S. Bai, X. Dong, N. Quan, C. Plass, and S. T. Jacob Role of de Novo DNA Methyltransferases and Methyl CpG-binding Proteins in Gene Silencing in a Rat Hepatoma J. Biol. Chem., May 3, 2002; 277(18): 16048 - 16058. [Abstract] [Full Text] [PDF]
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M. Curradi, A. Izzo, G. Badaracco, and N. Landsberger Molecular Mechanisms of Gene Silencing Mediated by DNA Methylation Mol. Cell. Biol., May 1, 2002; 22(9): 3157 - 3173. [Abstract] [Full Text] [PDF]
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C. D. Braastad, M. Leguia, and E. A. Hendrickson Ku86 autoantigen related protein-1 transcription initiates from a CpG island and is induced by p53 through a nearby p53 response element Nucleic Acids Res., April 15, 2002; 30(8): 1713 - 1724. [Abstract] [Full Text] [PDF]
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 X. Yu, Z. S. Guo, M. G. Marcu, L. Neckers, D. M. Nguyen, G. A. Chen, and D. S. Schrump Modulation of p53, ErbB1, ErbB2, and Raf-1 Expression in Lung Cancer Cells by Depsipeptide FR901228 J Natl Cancer Inst, April 3, 2002; 94(7): 504 - 513. [Abstract] [Full Text] [PDF]
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G. Liang, F. A. Gonzales, P. A. Jones, T. F. Orntoft, and T. Thykjaer Analysis of Gene Induction in Human Fibroblasts and Bladder Cancer Cells Exposed to the Methylation Inhibitor 5-Aza-2'-deoxycytidine Cancer Res., February 1, 2002; 62(4): 961 - 966. [Abstract] [Full Text] [PDF]
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M. Esteller, M. F. Fraga, M. Guo, J. Garcia-Foncillas, I. Hedenfalk, A. K. Godwin, J. Trojan, C. Vaurs-Barriere, Y.-J. Bignon, S. Ramus, et al. DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis Hum. Mol. Genet., December 1, 2001; 10(26): 3001 - 3007. [Abstract] [Full Text] [PDF]
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P. S. Yan, C.-M. Chen, H. Shi, F. Rahmatpanah, S. H. Wei, C. W. Caldwell, and T. H.-M. Huang Dissecting Complex Epigenetic Alterations in Breast Cancer Using CpG Island Microarrays Cancer Res., December 1, 2001; 61(23): 8375 - 8380. [Abstract] [Full Text] [PDF]
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