Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes

Carcinogenesis

Volumn 28, Issue 3, 2007, Pages 560-571

  Milutinovic, Snezana ^a   Detich, Nancy ^a   Szyf, Moshe ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b NONE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; GELATINASE A; GENE PRODUCT; GENOMIC DNA; HISTONE DEACETYLASE INHIBITOR; MELANOMA ANTIGEN; MELANOMA ANTIGEN B2; PROTEIN WIF1; UNCLASSIFIED DRUG; VALPROIC ACID;

ACETYLATION; ARTICLE; CANCER THERAPY; CELL STRAIN HEK293; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; GENE EXPRESSION; GENE MAPPING; GENETIC IDENTIFICATION; GENOME; HUMAN; HUMAN CELL; METASTASIS; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TUMOR GROWTH;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIGENS, NEOPLASM; CELL LINE; CHROMATIN; DNA METHYLATION; EPIGENESIS, GENETIC; HISTONE DEACETYLASES; HUMANS; KIDNEY; MATRIX METALLOPROTEINASE 2; NEOPLASM PROTEINS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VALPROIC ACID;

EID: 34047170360     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgl167     Document Type: Article

References (53)

1. Szyf,M. (2003) Targeting DNA methylation in cancer. Ageing Res. Rev., 2, 299-328.
2. Razin,A. (1998) CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J., 17, 4905-4908.
3. Jones,P.L., Veenstra,G.J., Wade,P.A., Vermaak,D., Kass,S.U., Landsberger,N., Strouboulis,J. and Wolffe,A.P. (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet., 19, 187-191.
4. Nan,X., Ng,H.H., Johnson,C.A., Laherty,C.D., Turner,B.M., Eisenman,R.N. and Bird,A. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex [see comments]. Nature, 393, 386-389.
5. Bachman,K.E., Park,B.H., Rhee,I., Rajagopalan,H., Herman,J.G., Baylin,S.B., Kinzler,K.W. and Vogelstein,B. (2003) Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell, 3, 89-95.
6. Leu,Y.W., Yan,P.S., Fan,M. et al. (2004) Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res., 64, 8184-8192.
7. Fuks,F., Hurd,P.J., Wolf,D., Nan,X., Bird,A.P. and Kouzarides,T. (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem., 278, 4035-4040.
8. Fuks,F., Hurd,P.J., Deplus,R. and Kouzarides,T. (2003) The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res., 31, 2305-2312.
9. Fuks,F., Burgers,W.A., Godin,N., Kasai,M. and Kouzarides,T. (2001) Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J., 20, 2536-2544.
10. Fuks,F., Burgers,W.A., Brehm,A., Hughes-Davies,L. and Kouzarides,T. (2000) DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat. Genet., 24, 88-91.
11. Milutinovic,S., Brown,S.E., Zhuang,Q. and Szyf,M. (2004) DNMT1 knock down induces gene expression by a mechanism independent of the two epigenetic silencing mechanisms: DNA methylation and histone deacetylation. J. Biol. Chem., 279, 27915-27927.
12. Kramer,O.H., Gottlicher,M. and Heinzel,T. (2001) Histone deacetylase as a therapeutic target. Trends Endocrinol. Metab., 12, 294-300.
13. Weidle,U.H. and Grossmann,A. (2000) Inhibition of histone deacetylases: a new strategy to target epigenetic modifications for anticancer treatment. Anticancer Res., 20, 1471-1485.
14. Costa,E., Grayson,D.R., Mitchell,C.P., Tremolizzo,L., Veldic,M. and Guidotti,A. (2003) GABAergic cortical neuron chromatin as a putative target to treat schizophrenia vulnerability. Crit. Rev. Neurobiol., 15, 121-142.
15. Cameron,E.E., Bachman,K.E., Myohanen,S., Herman,J.G. and Baylin,S.B. (1999) Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet., 21, 103-107.
16. Gius,D., Cui,H., Bradbury,C.M. et al. (2004) Distinct effects on gene expression of chemical and genetic manipulation of the cancer epigenome revealed by a multimodality approach. Cancer Cell, 6, 361-371.
17. Johannessen,C.U. and Johannessen,S.I. (2003) Valproate: Past, present, and future. CNS Drug Rev., 9, 199-216.
18. Spina,E. and Perugi,G. (2004) Antiepileptic drugs: Indications other than epilepsy. Epileptic Disord, 6, 57-75.
19. Phiel,C.J., Zhang,F., Huang,E.Y., Guenther,M.G., Lazar,M.A. and Klein,P.S. (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem., 276, 36734-36741.
20. Gottlicher,M., Minucci,S., Zhu,P. et al. (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J., 20, 6969-6978.
21. Yoshida,M. and Horinouchi,S. (1999) Trichostatin and leptomycin. Inhibition of histone deacetylation and signal-dependent nuclear export. Ann. N. Y. Acad. Sci., 886, 23-36.
22. Candido,E.P., Reeves,R. and Davie,J.R. (1978) Sodium butyrate inhibits histone deacetylation in cultured cells. Cell, 14, 105-113.
23. Manev,H. and Uz,T. (2002) DNA hypomethylating agents 5-aza-2′-deoxycytidine and valproate increase neuronal 5-lipoxygenase mRNA. Eur. J. Pharmacol., 445, 149-150.
24. Zhang,Z., Chen,C.Q. and Manev,H. (2004) DNA methylation as an epigenetic regulator of neural 5-lipoxygenase expression: Evidence in human NT2 and NT2-N cells. J. Neurochem., 88, 1424-1430.
25. Tremolizzo,L., Carboni,G., Ruzicka,W.B., Mitchell,C.P., Sugaya,I., Tueting,P., Sharma,R., Grayson,D.R., Costa,E. and Guidotti,A. (2002) An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability. Proc. Natl Acad. Sci. USA, 99, 17095-17100.
26. Cervoni,N. and Szyf,M. (2001) Demethylase activity is directed by histone acetylation. J. Biol. Chem., 276, 40778-40787.
27. Detich,N., Bovenzi,V. and Szyf,M. (2003) Valproate induces replication-independent active DNA demethylation. J. Biol. Chem., 278, 27586-27592.
28. Weaver,I.C., Cervoni,N., Champagne,F.A., D'Alessio,A.C., Sharma,S., Seckl,J.R., Dymov,S., Szyf,M. and Meaney,M.J. (2004) Epigenetic programming by maternal behavior. Nat. Neurosci., 7, 847-854.
29. Szyf,M., Pakneshan,P. and Rabbani,S.A. (2004) DNA demethylation and cancer: Therapeutic implications. Cancer Lett., 211, 133-143.
30. Clark,S.J., Harrison,J., Paul,C.L. and Frommer,M. (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Res., 22, 2990-2997.
31. Golub,T.R., Slonim,D.K., Tamayo,P. et al. (1999) Molecular classification of cancer: Class discovery and class prediction by gene expression monitoring. Science, 286, 531-537.
32. Meiri,K.F., Pfenninger,K.H. and Willard,M.B. (1986) Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc. Natl Acad. Sci. USA, 83, 3537-3541.
33. Kanai,Y., Okada,Y., Tanaka,Y., Harada,A., Terada,S. and Hirokawa,N. (2000) KIF5C, a novel neuronal kinesin enriched in motor neurons. J. Neurosci., 20, 6374-6384.
34. Hsu,Y.C. and Perin,M.S. (1995) Human neuronal pentraxin II (NPTX2): conservation, genomic structure, and chromosomal localization. Genomics, 28, 220-227.
35. Mazieres,J., He,B., You,L., Xu,Z., Lee,A.Y., Mikami,I., Reguart,N., Rosell,R., McCormick,F. and Jablons,D.M. (2004) Wnt inhibitory factor-1 is silenced by promoter hypermethylation in human lung cancer. Cancer Res., 64, 4717-4720.
36. Varga,A.E., Leonardos,L., Jackson,P., Marreiros,A. and Cowled,P.A. (2004) Methylation of a CpG island within the uroplakin Ib promoter: A possible mechanism for loss of uroplakin Ib expression in bladder carcinoma. Neoplasia, 6, 128-135.
37. Sato,N., Fukushima,N., Maitra,A., Matsubayashi,H., Yeo,C.J., Cameron,J.L., Hruban,R.H. and Goggins,M. (2003) Discovery of novel targets for aberrant methylation in pancreatic carcinoma using high-throughput microarrays. Cancer Res., 63, 3735-3742.
38. Vihinen,P. and Kahari,V.M. (2002) Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets. Int. J. Cancer, 99, 157-166.
39. Li,H.C., Cao,D.C., Liu,Y. et al. (2004) Prognostic value of matrix metalloproteinases (MMP-2 and MMP-9) in patients with lymph node-negative breast carcinoma. Breast Cancer Res. Treat., 88, 75-85.
40. Raouf,A., Ganss,B., McMahon,C., Vary,C., Roughley,P.J. and Seth,A. (2002) Lumican is a major proteoglycan component of the bone matrix. Matrix Biol., 21, 361-367.
41. Lurquin,C., De Smet,C., Brasseur,F., Muscatelli,F., Martelange,V., De Plaen,E., Brasseur,R., Monaco,A.P. and Boon,T. (1997) Two members of the human MAGE-B gene family located in Xp21.3 are expressed in tumors of various histological origins. Genomics, 46, 397-408.
42. De Smet,C., De Backer,O., Faraoni,I., Lurquin,C., Brasseur,F. and Boon,T. (1996) The activation of human gene MAGE-1 in tumor cells is correlated with genome-wide demethylation. Proc. Natl Acad. Sci. USA, 93, 7149-7153.
43. De Smet,C., Lurquin,C., Lethe,B., Martelange,V. and Boon,T. (1999) DNA methylation is the primary silencing mechanism for a set of germ line- and tumor-specific genes with a CpG-rich promoter. Mol. Cell. Biol., 19, 7327-7335.
44. Nagashima,H., Sadanaga,N., Mashino,K., Yamashita,K., Inoue,H., Mori,M. and Sugimachi,K. (2001) Expression of MAGE-B genes in esophageal squamous cell carcinoma. Jpn. J. Cancer Res., 92, 167-173.
45. Milutinovic,S., Zhuang,Q., Niveleau,A. and Szyf,M. (2003) Epigenomic stress response. Knockdown of DNA methyltransferase 1 triggers an intra-S-phase arrest of DNA replication and induction of stress response genes. J. Biol. Chem., 278, 14985-14995.
46. Yoshizaki,T., Sato,H. and Furukawa,M. (2002) Recent advances in the regulation of matrix metalloproteinase 2 activation: From basic research to clinical implication (Review). Oncol. Rep., 9, 607-611.
47. Cervoni,N., Detich,N., Seo,S.B., Chakravarti,D. and Szyf,M. (2002) The oncoprotein Set/TAF-1beta, an inhibitor of histone acetyltransferase, inhibits active demethylation of DNA, integrating DNA methylation and transcriptional silencing. J. Biol. Chem., 277, 25026-25031.
48. Guo,Y., Pakneshan,P., Gladu,J., Slack,A., Szyf,M. and Rabbani,S.A. (2002) Regulation of DNA methylation in human breast cancer. Effect on the urokinase-type plasminogen activator gene production and tumor invasion. J. Biol. Chem., 277, 41571-41579.
49. Pakneshan,P., Szyf,M. and Rabbani,S.A. (2004) Methylation and inhibition of uPA expression by RAS oncogene: Divergence of growth control and invasion in breast cancer cells. Carcinogenesis, 26, 557-564.
50. Pakneshan,P., Xing,R.H. and Rabbani,S.A. (2003) Methylation status of uPA promoter as a molecular mechanism regulating prostate cancer invasion and growth in vitro and in vivo. FASEB J., 17, 1081-1088.
51. Szyf,M., Pakneshan,P. and Rabbani,S.A. (2004) DNA methylation and breast cancer. Biochem. Pharmacol., 68, 1187-1197.
52. Baylin,S.B., Esteller,M., Rountree,M.R., Bachman,K.E., Schuebel,K. and Herman,J.G. (2001) Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet., 10, 687-692.
53. Seo,S.B., McNamara,P., Heo,S., Turner,A., Lane,W.S. and Chakravarti,D. (2001) Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the set oncoprotein. Cell, 104, 119-130.