Reversal of hypermethylation and reactivation of p16INK4a, RARβ, and MGMT genes by genistein and other isoflavones from soy

Clinical Cancer Research

Volumn 11, Issue 19 I, 2005, Pages 7033-7041

  Fang, Ming Zhu ^a   Chen, Dapeng ^a   Sun, Yi ^a   Jin, Zhe ^a   Christman, Judith K ^b   Yang, Chung S ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA METHYLTRANSFERASE; EPIGALLOCATECHIN GALLATE; GENISTEIN; ISOFLAVONE; POLYPHENOL; RECOMBINANT ENZYME; SULFORAPHANE; TRICHOSTATIN A;

ARTICLE; CANCER INHIBITION; CANCER PREVENTION; CARCINOMA CELL; CELL NUCLEUS; CONTROLLED STUDY; DIETARY INTAKE; DNA HYPERMETHYLATION; DNA METHYLATION; ENZYME ASSAY; ENZYME INHIBITION; ENZYME PURIFICATION; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MGMT GENE; P16 INK4A GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSTATE CANCER; QUANTITATIVE ASSAY; RARBETA GENE; REAL TIME POLYMERASE CHAIN REACTION; SOYBEAN; SQUAMOUS CELL CARCINOMA;

ANTICARCINOGENIC AGENTS; ANTINEOPLASTIC AGENTS; AZACITIDINE; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ESOPHAGEAL NEOPLASMS; GENISTEIN; HUMANS; HYDROXAMIC ACIDS; ISOFLAVONES; O(6)-METHYLGUANINE-DNA METHYLTRANSFERASE; RECEPTORS, RETINOIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SOYBEANS; SULFITES; TEA; THIOCYANATES;

EID: 26444451123     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-05-0406     Document Type: Article

References (52)

1. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349:2042-54.
2. Egger G, Liang G, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004;429:457-63.
3. Kopelovich L, Crowell JA, Fay JR. The epigenome as a target for cancer chemoprevention. J Natl Cancer Inst 2003;95:1747-57.
4. Karpf AR, Jones DA. Reactivating the expression of methylation silenced genes in human cancer. Oncogene 2003;21:5496-503.
5. Christman JK. 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 2002;21:5483-95.
6. Fang MZ, Wang Y, Ai N, et al. Tea polyphenol (-)-epigallocatechin-3- gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res 2003;63: 7563-70.
7. Dixon RA, Ferreira D. Genistein. Phytochemistry 2002;60:205-11.
8. Cabanes A, Wang M, Olivo S, et al. Prepubertal estradiol and genistein exposures up-regulate BRCA1 mRNA and reduce mammary tumorigenesis. Carcinogenesis 2004;25:741-8.
9. Fritz WA, Coward L, Wang J, Lamartiniere CA. Dietary genistein: perinatal mammary cancer prevention, bioavailability and toxicity testing in the rat. Carcinogenesis 1998;19:2151-8.
10. Landstrom M, Zhang JX, Hallmans G, et al. Inhibitory effects of soy and rye diets on the development of Dunning R3327 prostate adenocarcinoma in rats. Prostate 1998;36:151-61.
11. Zhou JR, Gugger ET, Tanaka T, Guo Y, Blackburn GL, Clinton SK. Soybean phytochemicals inhibit the growth of transplantable human prostate carcinoma and tumor angiogenesis in mice. J Nutr 1999;129: 1628-35.
12. Mentor-Marcel R, Lamartiniere CA, Eltoum IE, Greenberg NM, Elgavish A. Genistein in the diet reduce the incidence of poorly differentiated prostatic adenocarcinoma in transgenic mice (TRAMP). Cancer Res 2001;61:6777-82.
13. Hikosaka A, Asamoto M, Hokaiwado N, et al. Inhibitory effects of soy isoflavones on rat prostate carcinogenesis induced by 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis 2004;25:381-7.
14. Li D, Yee JA, McGuire MH, Murphy PA, Van L. Soybean isoflavones reduce experimental metastasis in mice. J Nutr 1999;129:1075-8.
15. Quo JY, Li X, Browning JD, et al. Dietary soy isoflavones and estrone protect ovariectomized ERαKO and wild-type mice from carcinogen-induced colon cancer. J Nutr 2004;134:179-82.
16. Arai N, Strom A, Rafter JJ, Gustafsson JA. Estrogen receptor β mRNA in colon cancer cells: growth effects of estrogen and genistein. Biochem Biophys Res Commun 2000;270:425-31.
17. Wietrzyk J, Boratynski J, Grynkiewicz G, Ryczynski A, Radzikowski C, Opolski A. Antiangiogenic and antitumour effects in vivo of genistein applied alone or combined with cyclophosphamide. Anticancer Res 2001;21:3893-6.
18. Wietrzyk J, Opolski A, Madej J, Radzikowski C. The antitumor effect of postoperative treatment with genistein alone or combined with cyclophosphamide in mice bearing transplantable tumors. Acta Pol Pharm 2000;57 Suppl:5-8.
19. Tatsuta M, Iishi H, Baba M, Yano H, Uehara H, Nakaizumi A. Attenuation by genistein of sodium-chloride-enhanced gastric carcinogenesis induced by N-methyl-N′-nitro-N-nitrosoguanidine in Wistar rats. Int J Cancer 1999;80:396-9.
20. Zhou JR, Mukherjee P, Gugger ET, Tanaka T, Blackburn GL, Clinton SK. Inhibition of marine bladder tumorigenesis by soy isoflavones via alterations in the cell cycle, apoptosis, and angiogenesis. Cancer Res 1998;58:5231-8.
21. Dean NM, Kanemitsu M, Boynton AL. Effects of the tyrosine-kinase inhibitor genistein on DNA synthesis and phospholipid-derived second messenger generation in mouse 10T1/2 fibroblasts and rat liver T51B cells. Biochem Biophys Res Commun 1989; 165:795-801.
22. Markovits J, Linassier C, Fosse P, et al. Inhibitory effects of the tyrosine kinase inhibitor genistein on mammalian DNA topoisomerase II. Cancer Res 1989; 49:5111-7.
23. Akiyama T, Ishida J, Nakagawa S, et al. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 1987;262:5592-5.
24. Li Y, Upadhyay S, Bhuiyan M, Sarkar FH. Induction of apoptosis in breast cancer cells MDA-MB-231 by genistein. Oncogene 1999;18:3166-72.
25. Lian F, Li Y, Bhuiyan M, Sarkar FH. p53-independent apoptosis induced by genistein in lung cancer cells. Nutr Cancer 1999;33:125-31.
26. Li Y, Sarkar FH. Inhibition of nuclear factor κB activation in PCS cells by genistein is mediated via Akt signaling pathway. Clin Cancer Res 2002;8: 2369-77.
27. Shao ZM, Wu J, Shen ZZ, Barsky SH. Genistein inhibits both constitutive and EGF-stimulated invasion in ER-negative human breast carcinoma cell lines. Anticancer Res 1998;18:1435-9.
28. Shao ZM, Wu J, Shen ZZ, Barsky SH. Genistein exerts multiple suppressive effects on human breast carcinoma cells. Cancer Res 1998;58:4851-7.
29. Smirnoff P, Liel Y, GnainskyJ, Shany S, Schwartz B. The protective effect of estrogen against chemically induced murine colon carcinogenesis is associated with decreased CpG island methylation and increased mRNA and protein expression of the colonic vitamin D receptor. Oncol Res 1999;11:255-64.
30. Demirpence E, Semlali A, Oliva J, et al. An estrogen-responsive element-targeted histone deacetylase enzyme has an antiestrogen activity that differs from that of hydroxytamoxifen. Cancer Res 2002;62:6519-28.
31. Badia E, Duchesne MJ, Semlali A, et al. Long-term hydroxytamoxifen treatment of an MCF-7-derived breast cancer cell line irreversibly inhibits the expression of estrogenic genes through chromatin remodeling. Cancer Res 2000;60:4130-8.
32. Day JK, Bauer AM, DesBordes C, et al. Genistein alters methylation patterns in mice. J Nutr 2002;132: 2419-23S.
33. King EP, Nie Y, Wang LD, et al. Aberrant methylation of p16INK4a and deletion of p15INK4b are frequent events in human esophageal cancer in Linxian, China. Carcinogenesis 1999;20:77-84.
34. Wang Y, Fang MZ, Liao J, et al. Hypermethylation-associated inactivation of retinoic acid receptor β in human esophageal squamous cell carcinoma. Clin Cancer Res 2003;9:5257-63.
35. Fang MZ, Jin Z, Wang Y et al. Promoter hypermethylation and inactivation of O(6)-methylguanine-DNA methyltransferase in esophageal squamous cell carcinomas and its reactivation in cell lines. Int J Oncol 2005;26:615-22.
36. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 1996;93:9821-6.
37. Palmisano WA, Divine KK, Saccomanno G, et al. Predicting lung cancer by detecting aberrant promoter methylation in sputum. Cancer Res 2000;60: 5954-8.
38. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method. Methods 2001;25:402-8.
39. Ariani F, Mari F, Pescucci C, et al. Real-time quantitative PCR as a routine method for screening large rearrangements in Rett syndrome: report of one case of MECP2 deletion and one case of MECP2 duplication. Hum Mutat 2004;24:172-7.
40. Belinsky SA, Nikula KJ, Baylin SB, Issa JP. Increased cytosine DNA-methyltransferase activity is target-cell-specific and an early event in lung cancer. Proc Natl Acad Sci U S A 1996;93:4045-50.
41. Adams RL, Rinaldi A, Seivwright C. Microassay for DNA methyltransferase. J Biochem Biophys Methods 1991;22:19-22.
42. Brank AS, Van Bemmel DM, Christman JK. Optimization of baculovirus-mediated expression and purification of hexahistidine-tagged murine DNA (cytosine-C5)-methyltransferase-1 in Spodoptera frugiperda 9 cells. Protein Expr Purif 2002;25: 31-40.
43. Zhu B, Benjamin D, Zheng Y, et al. Overexpression of 5-methylcytosine DNA glycosylase in human embryonic kidney cells EcR293 demethylates the promoter of a hormone-regulated reporter gene. Proc Natl Acad Sci U S A 2001;98:5031-6.
44. Nguyen CT, Gonzales FA, Jones PA. Altered chromatin structure associated with methylation-induced gene silencing in cancer cells: correlation of accessibility, methylation, MeCP2 binding and acetylation. Nucleic Acids Res 2001;29:4598-606.
45. 6-methylguanine-DNA methyl-transferase (MGMT) gene expression in human cancer. Oncogene 2003;22:8835-44.
46. Myzak MC, Karplus PA, Chung FL, et al. A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Res 2004;64: 5767-74.
47. Hsieh CY, Santell RC, Haslam SZ, et al. Estrogenic effects of genistein on the growth of estrogen receptor-positive human breast cancer (MCF-7) cells in vitro and in vivo. Cancer Res 1998;58:3833-8.
48. Suzuki K, Koike H, Matsui H, et al. Genistein, a soy isoflavone, induces glutathione peroxidase in the human prostate cancer cell lines LNCaP and PC-3. Int J Cancer 2002;99:846-52.
49. Adlercreutz CH, Goldin BR, Gorbach SL, et al. Soybean phytoestrogen intake and cancer risk. J Nutr 1995;125:757-705.
50. Xu X, Harris KS, Wang HJ, et al. Bioavailability of soybean isoflavones depends upon gut microflora in women. J Nutr 1995;125:2307-15.
51. Eden A, Gaudet F, Waghmare A, et al. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003;300:455.
52. Gaudet F, Hodgson JG, Eden A, et al. Induction of tumors in mice by genomic hypomethylation. Science 2003;300:489-92.