Epigenetics: The role of methylation in the mechanism of action of tumor suppressor genes

Annals of the New York Academy of Sciences

Volumn 983, Issue , 2003, Pages 71-83

  Jain, Pawan K ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Epigenetics; Histone deacetylase (HDAC); Histone methylase (HMT); Hypermethylation; Tumor suppressor genes

Indexed keywords

AZACITIDINE; DNA BINDING PROTEIN;

CANCER GROWTH; CARCINOGENESIS; CONFERENCE PAPER; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE INACTIVATION; GENE SILENCING; GENETICS; HUMAN; MITOSIS; NONHUMAN; PROMOTER REGION; TUMOR SUPPRESSOR GENE;

EID: 0037354042     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2003.tb05963.x     Document Type: Conference Paper

References (80)

1. FEINBERG, A.P. 2001. Cancer epigenetics takes center stage. Proc. Natl. Acad. Sci. USA 98: 392-394.
2. JONES, P.A. & P.W. LAIRD. 1999. Cancer epigenetics comes of age. Nat. Genet. 21: 163-167.
3. YANG, A.S., P.A. JONES & A. SHIBATA. 1996. The mutational burden of 5-methylcytosine. In Epigenetic Mechanisms of Gene Regulation. A.D. Riggs, R.A. Martienssen & V.E.A. Russo, Eds.: 77-94. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY.
4. AHLUWALIA, A., P. YAN, J.A. HURTEAU, et al. 2001. DNA methylation and ovarian cancer. I. Analysis of CpG island hypermethylation in human ovarian cancer using differential methylation hybridization. Gynecol. Oncol. 82: 261-268.
5. AKHTAR, M., Y. CHENG, R.M. MAGNO, et al. 2001. Promoter methylation regulates Helicobacter pylori-stimulated cyclooxygenase-2 expression in gastric epithelial cells. Cancer Res. 61: 2399-2403.
6. BAYLIN, S.B., J.G. HERMAN, J.R. GRAFF, et al. 1998. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv. Cancer Res. 72: 141-196.
7. ESTELLER, M., A. SPARKS, M. TOYOTA, et al. 2000. Analysis of adenomatous polyposis coil promoter hypermethylation in human cancer. Cancer Res. 60: 4366-4371.
8. TYCKO, B. 2000. Epigenetic gene silencing in cancer. J. Clin. Invest. 105: 401-407.
9. BAYLIN, S.B. & J.G. HERMAN. 2000. DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet. 16: 168-174.
10. ESTELLER, M., J.M. SILVA, G. DOMINGUEZ, et al. 2000. Promotor hypermethylation and BRCA 1 inactivation in sporadic breast and ovarian tumors. J. Natl. Cancer Inst. 92: 564-569.
11. ESTELLER M.A.E., P.G. CORN, R.A. LOTHE, et al. 2000. Epigenetic inactivation of LKB1 in primary tumors associated with the Peutz-Jeghers syndrome. Oncogene 19: 164-168.
12. EHRLICH, M., M.A. GAMA-SOSA, L.H. HUANG, et al. 1982. Amount and distribution of 5-methylcytosine in human DNA from different types of cells. Nucleic Acids Res. 10: 2709-2721.
13. YEVIN, A. & A. RAZIN. 1993. In DNA Methylation: Molecular Biology and Biological Significance. J.P. Jost & H.P. Saluz, Eds.: 523-568. Birkhauser Verlag. Basel.
14. SCARANO, E., I. IACCARINO, P. GRIPPO & E. PARISI. 1967. The heterogeneity of thymine methyl group origin in DNA pyrimidine isostichs. Proc. Natl. Acad. Sci. USA 57: 1394-1400.
15. JONES, P.A. & S.M. TAYLOR. 1980. Cellular differentiation, cytidine analogs, and DNA methylation. Cell 20: 85-93.
16. BARTOLOMEI, M.S. & S.M. TILGHMAN. 1997. Genomic imprinting in mammals. Annu. Rev. Genet. 31: 493-525.
17. LI, E., C. BEARD & R. JAENISCH. 1993. Role for DNA methylation in genomic imprinting. Nature 366: 362-365.
18. MONK, M. 1995. Epigenetic programming of differential gene expression in development and evolution. Dev. Genet. 17: 188-197.
19. NEUMANN, B. & D.P. BARLOW. 1996. Multiple roles for DNA methylation in gametic imprinting. Curr. Opin. Genet. Dev. 6(2):159-163.
20. BOUCHARD, J. & R.L. MOMPARLER. 1983. Incorporation of 5-Aza-29-deoxycytidine 59-triphosphate into DNA: interactions with mammalian DNA polymerase and DNA methylase. Mol. Pharmacol. 24: 109-114.
21. TUCKER, M.S. & T.H. BESTOR. 1997. Formation of methylation patterns in mammalian genome. Mutat. Res. 386: 119-130.
22. XIE, S., Z. WANG, M. OKANO, et al. 1999. Cloning, expression, and chromosome locations of the human DNMT3 gene family. Gene 236: 87-95.
23. YODER, J.A. & T.H. BESTOR. 1998. A candidate mammalian DNA methyltransferase related to pmt 1p of fission yeast. Hum. Mol. Genet. 7: 279-284.
24. OKANO, M., S. XIE & E. LI. 1998. Dnmt 2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucl. Acids Res. 26: 2536-2540.
25. BHATTACHARYA, S.K., S. RAMCHANDANI, N. CERVONI & M. SZYF. 1999. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 397: 579-583.
26. KISS, S.U., D. PRUSS & A.P. WOLFEE. 1997. How does DNA methylation repress transcription? Trends Genet. 13: 444-449.
27. IGUCHI-ARIGI, S.M.M. & W. SCHIFFNER. 1989. CpG methylation of the cAMP responsive enhancer/promoter sequence TGACGTCA abolishes specific factor binding as well as transcription activation. Genes Dev. 3: 612-619.
28. TATE, P. H. & A.P. BIRD. 1993. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr. Opin. Genet. Dev. 3: 226-231.
29. MANCINI, D.N., D.I. RODENHISER, G. AINSWORTH, et al. 1998. CpG methylation within the 59 regulatory region of BRCA1 gene is tumor specific and includes a putative CREB binding site. Oncogene 15:1161-1169.
30. HUANG, L.H., R, WANG, M.A. GAMA-SOSA, et al. 1984. A protein from human placental nuclei binds preferentially to 5-methylcytosine-rich DNA. Nature 308: 293-295.
31. JOST, J.P. & J. HOFSTEENGE. 1992. The repressor MDBP-2 is a member of the histone H1 family that binds preferentially in vitro and in vivo to methylated nonspecific DNA sequences. Proc. Natl. Acad. Sci. USA 89: 9499-9503.
32. NG, H.H., Y. ZHANG, B. HENDRICH, et al. 1999. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23: 58-61.
33. WADE, P.A., A. GEGONNE, P.L. JONES, et al. 1999. Mi-2 complex couples DNA methylation in chromatin remodelling and histone acetylation. Nat. Genet. 23: 62-66.
34. MEEHAN, R.R., J.D. LEWIS, S. MCKAY, et al. 1989. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell 58: 499-507.
35. BOYES, J. & A. BIRD. 1991. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 64: 1123-1134.
36. LEWIS, J.D., R.R. MEEHAN, W.J. HENZEL, et al. 1992. Purification, sequence and cellular localization of a novel chromosomal protein that binds to methylated. Cell 69: 905-914.
37. NAN, X., F.J. CAMPOY & A.P. BIRD. 1997. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88: 471-481.
38. NAN, X., H-H. NG, C.A. JOHNSON, et al. 1998. Transcriptional repression by the methyl-CpG-binding protein McCP2 involves a histone deacetylase complex. Nature 393: 386-389.
39. BIRD, A. & A.P. WOLF. 1999. Methylation-induced repression-belts, braces, and chromatin. Cell 99: 451-454.
40. TYLER, J.K. & J.T. KADONAGA. 1999. The"dark side" of chromatin remodeling: repressive effects on transcription. Cell 99: 443-446.
41. BANNISTER, A.J., P. ZEGERMAN, J.F. PARTRIDGE, et al. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124.
42. LACHNER, M., D. O'CARROLL, S. REA, et al. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120.
43. LI, E. 1997. In Genomic Imprinting: Frontiers in Molecular Biology: 1-20. IRL Press. Oxford.
44. BESTOR, T.H. 1992. Activation of mammalian DNA methyltransferase by cleavage of a Zn binding regulatory domain. EMBO J. 11: 2611-2617.
45. LEI, H., S.P. OH, M. OKANO, et al. 1996. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 122: 3195-3205.
46. RHEE, I., K.E. BACHMAN, B.H. PARK, et al. 2002. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416: 552-556.
47. OKANO, M., D.W. BELL, D.A. HABER & E. LI. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257.
48. LAIRD, P.W., L. JACKSON-GRUSBY, A. FAZELI, et al. 1995. Suppression of intestinal neoplasia by DNA hypomethylation. Cell 81: 197-205.
49. JONES, P.L., G.J. VEENSTRA, P.A. WADE, et al. 1998. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19: 187-191.
50. CAMERON, E.E., K.E. BACHMAN, S. MYOHANEN, et al. 1999. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet. 21: 103-107.
51. HERMAN, J.G., F. LATIF, Y. WENG, et al. 1994. Silencing of the VHL tumor supressor gene by DNA methylation in renal cell carcinoma. Proc. Natl. Acad. Sci. USA 91: 9700-9704.
52. SHERR, C.J. 1996. Cancer cell cycles. Science 274: 1672-1677.
53. HERMAN, J.G., A. MERLO, L. MAO, et al. 1995. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res. 55: 4525-4530.
54. KAMB, A., N.A. GRUIS, J. WEAVER-FELDHAUS, et al. 1994. A cell cycle regulator potentially involved in genesis of many tumor types. Science 264: 436-440.
55. WOLTER, M., J. REIFENBERGER, B. BLASCHKE, et al. 2001. Oligodendroglial tumors frequently demonstrate hypermethylation of the CDKN2A (MTS1, p161NK4a), p14ARF, and CDKN2B (MTS2, p15INK4b) tumor suppressor genes. J. Neuropathol. Exp. Neurol. 60: 1170-1180.
56. BIAN, Y.S., O.M.C. FONTOLLIET, F.T. BOSMAN & J. BENHATTAR. 2002. p16 inactivation by methylation of the CDKN2A promoter occurs early during neoplastic progression in Barrett's esophagus. Gastroenterology 122: 1113-1121.
57. WANG, J.C., W. CHEN, S. NALLUSAMY, et al. 2002. Hypermethylation of the P15INK4b and P16INK4a in agnogenic myeloid metaplasia (AMM) and AMM in leukaemic transformation. Br. J. Haematol. 116: 582-586.
58. NICOLL, G., D.N. CRICHTON, H.E. McDOWELL, et al. 2001. Expression of the hypermethylated in cancer gene (HIC-1) is associated with good outcome in human breast cancer. Br. J. Cancer 85: 1878-1882.
59. FUJII, H., M.A. BIEL, W. ZHOU, et al. 1998. Methylation of the HIC-1 candidate tumor suppressor gene in human breast cancer. Oncogene 16: 2159-2164.
60. TAN, L.W., T. BIANCO & A. DOBROVIC. 2002. Variable promoter region CpG island methylation of the putative tumor suppressor gene Connexin 26 in breast cancer. Carcinogenesis 23: 231-236.
61. YUAN, Y., R. MENDEZ, A. SAHIN & J.L. DAI. 2001. Hypermethylation leads to silencing of the SYK gene in human breast cancer. Cancer Res. 61: 5558-5561.
62. 2 and cyclooxygenase gene expression in human preimplantation embryos. J. Clin. Endocrinol. Metab. 87: 2629-2634.
63. KIKUCHI, T., F. ITOH, M. TOYOTA, et al. 2002. Aberrant methylation and histone deacetylation of cyclooxygenase 2 in gastric cancer. Int. J. Cancer 97: 272-277.
64. TAMURA, G. 2002. Genetic and epigenetic alterations of tumor suppressor and tumor-related genes in gastric cancer. Histol. Histopathol. 17: 323-329.
65. GRAFF, J.R., J.G. HERMAN, R.G. LAPIDUS, et al. 1995. E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res. 55: 5195-5199.
66. KANAI, Y., S. USHIJIMA, A.M. HUI, et al. 1997. The E-cadherin gene is silenced by CpG methylation in human hepatocellular carcinomas. Int. J. Cancer 71: 355-359.
67. MIZUNO, K., H. OSADA, H. KONISHI, et al. 2002. Aberrant hypermethylation of the CHFR prophase checkpoint gene in human lung cancers. Oncogene 21: 2328-2333.
68. LIANG, G., K.D. ROBERTSON, C. TALMADGE, et al. 2000. The gene for a novel transmembrane protein containing epidermal growth factor and follistatin domains is frequently hypermethylated in human tumor cells. Cancer Res. 60: 4907-4912.
69. MOINOVA, H.R., W.D. CHEN, L. SHEN, et al. 2002. HLTF gene silencing in human colon cancer. Proc. Natl. Acad. Sci. USA 99: 4562-4567.
70. LO, K.F., Y.S. TSANG, J. KWONG, et al. 2002. Promoter hypermethylation of the EDNRB gene in nasopharyngeal carcinoma. Int. J. Cancer 98: 651-655.
71. KWONG, J., K.W. LO, K.F. TO, et al. 2002. Promoter hypermethylation of multiple genes in nasopharyngeal carcinoma. Clin. Cancer Res. 8: 131-137.
72. ASTUTI, D., A. AGATHANGGELOU, S. HONORIO, et al. 2001. RASSF1A promotor region CpG island hypermethylation in phaeochromocytomas and neuroblastoma tumors. Oncogene 20: 7573-7577.
73. KIKUCHI, T., M. TOYOTA, F. ITOH, et al. 2002. Inactivation of p57KIP2 by regional promoter hypermethylation and histone deacetylation in human tumors. Oncogene 21: 2741-2749.
74. ESTELLER, M., G. GAIDANO, S.N. GOODMAN, et al. 2002. 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.
75. SOENGAS, M.S., P. CAPODIECI, D. POLSKY, et al. 200l. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature 409: 207-211.
76. PALMISANO, W.A., K.K. DIVINE, G. SACCOMANNO, et al. 2000. Predicting lung cancer by detecting aberrant promoter methylation in sputum. Cancer Res. 60: 5954-5958.
77. GITAN, R.S., H. SHI, C.M. CHEN, et al. 2002. Methylation-specific oligonucleotide microarray: a new potential for high-throughput methylation analysis. Genome Res. 12: 158-164.
78. SUZUKI, H., E. GABRIELSON, W. CHEN, et al. 2002. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat. Genet. 31: 141-149.
79. NARAYAN, A., W. JI, X.Y. ZHANG, et al. 1998. Hypomethylation of pericentromeric DNA in breast adenocarcinomas. Int. J. Cancer 77: 838-838.
80. GAMA-SOSA, M.A., V.A. SLAGEL, R.W. TREWYN, et al. 1983. The 5-methylcytosine content of DNA from human tumors. Nucleic Acids Res. 11: 6883-6894.