DNMT cooperativity - The developing links between methylation, chromatin structure and cancer

BioEssays

Volumn 25, Issue 11, 2003, Pages 1071-1084

  El Osta, Assam ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER GENETICS; CANCER RISK; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CHROMATIN STRUCTURE; DNA METHYLATION; GENE DELETION; GENE DISRUPTION; GENE SILENCING; HUMAN; HUMAN CELL; REVIEW; TUMOR SUPPRESSOR GENE;

ANIMALS; CELL LINE, TUMOR; CHROMATIN; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; GENE EXPRESSION REGULATION; HISTONES; HUMANS; NEOPLASMS;

EID: 0242551379     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.10345     Document Type: Review

References (99)

1. Ponder BA. Cancer genetics. Nature 2001;411:336-341.
2. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002;3:415-428.
3. Robertson KD. DNA methylation, methyltransferases, and cancer. Oncogene 2001;20:3139-3155.
4. Bird AP, Wolffe AP. Methylation-induced repression-belts, braces, and chromatin. Cell 1999;99:451-454.
5. Baylin SB, Herman JG. DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet 2000;16:168-174.
6. El-Osta A, Wolffe AP. DNA methylation and histone deacetylation in the control of gene expression: basic biochemistry to human development and disease. Gene Expr 2000;9:63-75.
7. Ura K, Kurumizaka H, Dimitrov S, Almouzni G, Wolffe AP. Histone acetylation: influence on transcription, nucleosome mobility and positioning, and linker histone-dependent transcriptional repression. EMBO J 1997;16:2096-2107.
8. Keshet I, Lieman-Hurwitz J, Cedar H. DNA methylation affects the formation of active chromatin. Cell 1986;44:535-543.
9. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998;19:187-191.
10. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998;393:386-389.
11. Boyes J, Bird A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 1991;64:1123-1134.
12. Hendrich B, Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 1998;18:6538-6547.
13. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, Reinberg D. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 1999;13:1924-1935.
14. Ng HH, Zhang Y, Hendrich B, Johnson CA, Turner BM, Erdjument-Bromage H, Tempst P, Reinberg D, Bird A. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat Genet 1999;23:58-61.
15. Ng HH, Jeppesen P, Bird A. Active repression of methylated genes by the chromosomal protein MBD1. Mol Cell Biol 2000;20:1394-1406.
16. Cameron EE, Bachman KE, Myohanen S, Herman JG, Baylin SB. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 1999;21:103-107.
17. Coffee B, Zhang F, Warren ST, Reines D. Acetylated histones are associated with FMR1 in normal but not fragile X-syndrome cells. Nat Genet 1999;22:98-101.
18. El-Osta A, Kantharidis P, Zalcberg JR, Wolffe AP. Precipitous release of methyl-CpG binding protein 2 and histone deacetylase 1 from the methylated human multidrug resistance gene (MDR1) on activation. Mol Cell Biol 2002;22:1844-1857.
19. Suzuki H, Gabrielson E, Chen W, Anbazhagan R, van Engeland M, Weijenberg MP, Herman JG, Baylin SB. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002;31:141-149.
20. Bestor TH. The DNA methyltransferases of mammals. Hum Mol Genet 2000;9:2395-2402.
21. Chuang LS, Ian HI, Koh TW, Ng HH, Xu G, Li BF. Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 1997;277:1996-2000.
22. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 1992;69:915-926.
23. Li E, Beard C, Jaenisch R. Role for DNA methylation in genomic imprinting. Nature 1993;366:362-365.
24. Pradhan S, Bacolla A, Wells RD, Roberts RJ. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J Biol Chem 1999;274:33002-33010.
25. Okano M, Xie S, Li E. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res 1998;26:2536-2540.
26. Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998;19:219-220.
27. Gibbons RJ, et al. Mutations in transcriptional regulator ATRX establish the functional significance of a PHD-like domain. Nat Genet 1997;17:146-148.
28. Jeddeloh JA, Stokes TL, Richards EJ. Maintenance of genomic methylation requires a SW12/SNF2-like protein. Nat Genet 1999;22:94-97.
29. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999;99:247-257.
30. Lyko F, Ramsahoye BH, Kashevsky H, Tudor M, Mastrangelo MA, Orr-Weaver TL, Jaenisch R. Mammalian (cytosine-5) methyltransferases cause genomic DNA methylation and lethality in Drosophila. Nat Genet 1999;23:363-366.
31. Urieli-Shoval S, Gruenbaum Y, Sedat J, Razin A. The absence of detectable methylated bases in Drosophila melanogaster DNA. FEBS Lett 1982;146:148-152.
32. Lei H, Oh SP, Okano M, Juttermann R, Goss KA, Jaenisch R, Li E. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 1996;122:3195-3205.
33. Xie S, Wang Z, Okano M, Nogami M, Li Y, He WW, Okumura K, Li E. Cloning, expression and chromosome locations of the human DNMT3 gene family. Gene 1999;236:87-95.
34. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science 2001;294:2536-2539.
35. Hata K, Okano M, Lei H, Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 2002;129:1983-1993.
36. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 2000;24:88-91.
37. Rountree MR, Bachman KE, Baylin SB. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 2000;25:269-277.
38. Robertson KD, Ait-Si-Ali S, Yokochi T, Wade PA, Jones PL, Wolffe AP. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet 2000;25:338-342.
39. Tatematsu KI, Yamazaki T, Ishikawa F. MBD2-MBD3 complex binds to hemi-methylated DNA and forms a complex containing DNMT1 at the replication foci in late S phase. Genes Cells 2000;5:677-688.
40. Leonhardt H, Page AW, Weier HU, Bestor TH. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 1992;71:865-873.
41. Bachman KE, Rountree MR, Baylin SB. Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem 2001;276:32282-32287.
42. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T. Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J 2001;20:2536-2544.
43. Deplus R, Brenner C, Burgers WA, Putmans P, Kouzarides T, de Launoit Y, Fuks F. Dnmt3L is a transcriptional repressor that recruits histone deacetylase. Nucleic Acids Res 2002;30:3831-3838.
44. Aapola U, Liiv I, Peterson P. Imprinting regulator DNMT3L is a transcriptional repressor associated with histone deacetylase activity. Nucleic Acids Res 2002;30:3602-3608.
45. Gama-Sosa MA, Slagel VA, Trewyn RW, Oxenhandler R, Kuo KC, Gehrke CW, Ehrlich M. The 5-methylcytosine content of DNA from human tumors. Nucleic Acids Res 1983;11:6883-6894.
46. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983;301:89-92.
47. Goelz SE, Vogelstein B, Hamilton SR, Feinberg AP. Hypomethylation of DNA from benign and malignant human colon neoplasms. Science 1985;228:187-190.
48. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990;61:759-767.
49. Diala ES, Cheah MS, Rowitch D, Hoffman RM. Extent of DNA methylation in human tumor cells. J Natl Cancer Inst 1983;71:755-764.
50. Lengauer C, Kinzler KW, Vogelstein B. DNA methylation and genetic instability in colorectal cancer cells. Proc Natl Acad Sci USA 1997;94:2545-2550.
51. Ahuja N, Mohan AL, Li Q, Stolker JM, Herman JG, Hamilton SR, Baylin SB, Issa JP. Association between CpG island methylation and microsatellite instability in colorectal cancer. Cancer Res 1997;57:3370-3374.
52. Almeida A, Kokalj-Vokac N, Lefrancois D, Viegas-Pequignot E, Jeanpierre M, Dutrillaux B, Malfoy B. Hypomethylation of classical satellite DNA and chromosome instability in lymphoblastoid cell lines. Hum Genet 1993;91:538-546.
53. Strand M, Prolla TA, Liskay RM, Petes TD. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 1993;365:274-276.
54. Prolla TA, et al. Tumour susceptibility and spontaneous mutation in mice deficient in Mlh1, Pros1 and Pms2 DNA mismatch repair. Nat Genet 1998;18:276-279.
55. Trinh BN, Long TI, Nickel AE, Shibata D, Laird PW. DNA methyltransferase deficiency modifies cancer susceptibility in mice lacking DNA mismatch repair. Mol Cell Biol 2002;22:2906-2917.
56. Herman JG, et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci USA 1998;95:6870-6875.
57. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, Goldman H, Jessup JM, Kolodner R. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 1997;57:808-811.
58. Esteller M, Catasus L, Matias-Guiu X, Mutter GL, Prat J, Baylin SB, Herman JG. hMLH1 promoter hypermethylation is an early event in human endometrial tumorigenesis. Am J Pathol 1999;155:1767-1772.
59. Chen RZ, Pettersson U, Beard C, Jackson-Grusby L, Jaenisch R. DNA hypomethylation leads to elevated mutation rates. Nature 1998;395:89-93.
60. Maloisel L, Rossignol JL. Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev 1998;12:1381-1389.
61. Colot V, Maloisel L, Rossignol JL. Interchromosomal transfer of epigenetic states in Ascobolus: transfer of DNA methylation is mechanistically related to homologous recombination. Cell 1996;86:855-864.
62. Sanford JP, Clark HJ, Chapman VM, Rossant J. Differences in DNA methylation during oogenesis and spermatogenesis and their persistence during early embryogenesis in the mouse. Genes Dev 1987;1:1039-1046.
63. Loeb LA. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res 1991;51:3075-3079.
64. Silverman AL, Park JG, Hamilton SR, Gazdar AF, Luk GD, Baylin SB. Abnormal methylation of the calcitonin gene in human colonic neoplasms. Cancer Res 1989;49:3468-3473.
65. Qu GZ, Grundy PE, Narayan A, Ehrlich M. Frequent hypomethylation in Wilms tumors of pericentromeric DNA in chromosomes 1 and 16. Cancer Genet Cytogenet 1999;109:34-39.
66. Qu G, Dubeau L, Narayan A, Yu MC, Ehrlich M, Satellite DNA hypomethylation vs. overall genomic hypomethylation in ovarian epithelial tumors of different malignant potential. Mutat Res 1999;423:91-101.
67. Ohtani-Fujita N, Fujita T, Aoike A, Osifchin NE, Robbins PD, Sakai T. CpG methylation inactivates the promoter activity of the human retinoblastoma tumor-suppressor gene. Oncogene 1993;8:1063-1067.
68. Merlo A, Herman JG, Mao L, Lee DJ, Gabrielson E, Burger PC, Baylin SB, Sidransky D. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat Med 1995;1:686-692.
69. Melki JR, Vincent PC, Clark SJ. Concurrent DNA hypermethylation of multiple genes in acute myeloid leukemia. Cancer Res 1999;59:3730-3740.
70. Laird PW, Jackson-Grusby L, Fazeli A, Dickinson SL, Jung WE, Li E, Weinberg RA, Jaenisch R. Suppression of intestinal neoplasia by DNA hypomethylation. Cell 1995;81:197-205.
71. Eads CA, Nickel AE, Laird PW. Complete genetic suppression of polyp formation and reduction of CpG-island hypermethylation in Apc(Min/+) Dnmtl-hypomorphic Mice. Cancer Res 2002;62:1296-1299.
72. Sakai T, Toguchida J, Ohtani N, Yandell DW, Rapaport JM, Dryja TP. Allete-specific hypermethylation of the retinoblastoma tumor-suppressor gene. Am J Hum Genet 1991;48:880-888.
73. Rice JC, Ozcelik H, Maxeiner P, Andrulis I, Futscher BW. Methylation of the BRCA1 promoter is associated with decreased BRCA1 mRNA levels in clinical breast cancer specimens. Carcinogenesis 2000;21:1761-1765.
74. Hiltunen MO, Alhonen L, Koistinaho J, Myohanen S, Paakkonen M, Marin S, Kosma VM, Janne J. Hypermethylation of the APC (adenomatous polyposis coli) gene promoter region in human colorectal carcinoma. Int J Cancer 1997;70:644-648.
75. van dVPA, Metzelaar-Blok JA, Bergman W, Monique H, Hurks H, Frants RR, Gruis NA, Jager MJ. Promoter hypermethylation: a common cause of reduced p16(INK4a) expression in uveal melanoma. Cancer Res 2001;61:5303-5306.
76. Wang JC, Chen W, Nallusamy S, Chen C, Novetsky AD. Hypermethylation of the P15INK4b and P16INK4a in agnogenic myeloid metaplasia (AMM) and AMM in leukaemic transformation. Br J Haematol 2002;116:582-586.
77. Herman JG, et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci USA 1994;91:9700-9704.
78. Myohanen SK, Baylin SB, Herman JG. Hypermethylation can selectively silence individual p16ink4A alleles in neoplasia. Cancer Res 1998;58:591-593.
79. Esteller M, Corn PG, Baylin SB, Herman JG. A gene hypermethylation profile of human cancer. Cancer Res 2001;61:3225-3229.
80. Grady WM, et al. Methylation of the CDH1 promoter as the second genetic hit in hereditary diffuse gastric cancer. Nat Genet 2000;26:16-17.
81. Knudson AG, Jr. Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci USA 1971;68:820-823.
82. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, Gould KA, Dove WF. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992;256:668-670.
83. Magdinier F, Wolffe AP. Selective association of the methyl-CpG binding protein MBD2 with the silent p14/p16 locus in human neoplasia. Proc Natl Acad Sci USA 2001;98:4990-4995.
84. Rhee I, Jair KW, Yen RW, Lengauer C, Herman JG, Kinzler KW, Vogelstein B, Baylin SB, Schuebel KE. CpG methylation is maintained in human cancer cells lacking DNMT1. Nature 2000;404:1003-1007.
85. Rhee I, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 2002;416:552-556.
86. Di CL, et al. Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 2002;295:1079-1082.
87. Grignani F, et al. Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia. Nature 1998;391:815-818.
88. Dennis K, Fan T, Geiman T, Yan Q, Muegge K. Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev 2001;15:2940-2944.
89. Geiman TM, Muegge K. Lsh, an SNF2/helicase family member, is required for proliferation of mature T lymphocytes. Proc Natl Acad Sci USA 2000;97:4772-4777.
90. Vongs A, Kakutani T, Martienssen RA, Richards EJ. Arabidopsis thaliana DNA methylation mutants. Science 1993;260:1926-1928.
91. Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP. Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet 1999;23:62-66.
92. Lachner M, Jenuwein T. The many faces of histone lysine methylation. Curr Opin Cell Biol 2002;14:286-298.
93. Schneider R, Bannister AJ, Kouzarides T. Unsafe SETs: histone lysine methyltransferases and cancer. Trends Biochem Sci 2002;27:396-402.
94. Noma K, Allis CD, Grewal SI. Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 2001;293:1150-1155.
95. Rea S, et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000;406:593-599.
96. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 2003;34:75-79.
97. Bachman KE, Park BH, Rhee I, Rajagopalan H, Herman JG, Baylin SB, Kinzler KW, Vogelstein B. Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell 2003;3:89-95.
98. Fahrner JA, Eguchi S, Herman JG, Baylin SB. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res 2002;62:7213-7218.
99. Nguyen CT, Weisenberger DJ, Velicescu M, Gonzales FA, Lin JC, Liang G, Jones PA. Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′ -deoxycytidine. Cancer Res 2002;62:6456-6461.