Genistein and daidzein: Different molecular effects on prostate cancer

Anticancer Research

Volumn 33, Issue 1, 2013, Pages 39-44

  Adjakly, Mawussi ^a,b,c   Ngollo, Marjolaine ^a,b,c   Boiteux, Jean Paul ^c,d   Bignon, Yves Jean ^a,b,c   Guy, Laurent ^b,c,d   Bernard Gallon, Dominique ^a,b,c  

^a CENTRE JEAN PERRIN   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

^c Center for Research in Human Nutrition (CNRH)   (France)

^d SERVICE DE RHUMATOLOGIE   (France)

Author keywords

Daidzein genistein; Diet; Epigenetics; Isoflavones; Prostate cancer; Review; Soy phytoestrogens

Indexed keywords

ANGIOPOIETIN 2; CONNECTIVE TISSUE GROWTH FACTOR; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIN B; DAIDZEIN; EPHRIN B2; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GELATINASE A; GELATINASE B; GENISTEIN; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE REDUCTASE; HEAT SHOCK PROTEIN 27; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RETINOIC ACID RECEPTOR BETA; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CARDIOVASCULAR DISEASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIVISION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; DEACETYLATION; DNA METHYLATION; DOSE RESPONSE; DRUG CYTOTOXICITY; ENZYME ACTIVATION; EPIGENETICS; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HEART PROTECTION; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HISTONE UBIQUITINATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; M PHASE CELL CYCLE CHECKPOINT; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); POSTMENOPAUSE OSTEOPOROSIS; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SUMOYLATION; TUMOR MICROENVIRONMENT; UPREGULATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL SURVIVAL; EPIGENOMICS; FOOD HABITS; GENISTEIN; HUMANS; ISOFLAVONES; MALE; NF-KAPPA B; PHYTOESTROGENS; PROSTATIC NEOPLASMS; SOYBEANS;

EID: 84873036527     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Knudsen BS and Vasioukhin V: Mechanisms of prostate cancer initiation and progression. Adv Cancer Res 109: 1-50, 2010.
2. Ferlay J, Parkin DM and Steliarova-Foucher E: Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 46: 75-781, 2010.
3. Colonna M, Danzon A, Delafosse P, Mitton N, Bara S, Bouvier AM, Ganry O, Guizard AV, Launoy G, Molinie F, Sauleau EA, Schvartz C, Velten M, Grosclaude P and Tretarre B: Cancer prevalence in France: time trend, situation in 2002 and extrapolation to 2012. Eur J Cancer 44: 115-122, 2008.
4. Kheirandish P and Chinegwundoh F: Ethnic differences in prostate cancer. Br J Cancer 105: 481-485, 2011.
5. Murthy VS, Garza MA, Almario DA, Vogel KJ, Grubs RE, Gettig EA, Wilson JW and Thomas SB: Using a family history intervention to improve cancer risk perception in a black community. J Genet Couns 20: 639-649, 2011.
6. Brawley OW: Prostate cancer epidemiology in the United States. World J Urol 30: 195-200, 2012.
7. Clapp RW, Jacobs MM and Loechler E: Environmental and occupational causes of cancer: New evidence 2005-2007. Rev Environ Health 23: 1-37, 2008.
8. Yan L and Spitznagel EL: Meta-analysis of soy food and risk of prostate cancer in men. Int J Cancer 117: 667-669, 2005.
9. Yan L and Spitznagel EL: Soy consumption and prostate cancer risk in men: A revisit of a meta-analysis. Am J Clin Nutr 89: 1155-1163, 2009.
10. Hwang YW, Kim SY, Jee SH, Kim YN and Nam CM: Soy food consumption and risk of prostate cancer: a meta-analysis of observational studies. Nutr Cancer 61: 598-606, 2009.
11. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B and Gustafsson JA: Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139: 4252-4263, 1998.
12. Birt DF, Hendrich S and Wang W: Dietary agent in cancer prevention: Flavonoids and isoflavonoids. Pharmacol Ther 90: 157-177, 2001.
13. Si H and Liu D: Phytochemical genistein in the regulation of vascular function: New insights. Curr Med Chem 14: 2581-2589, 2007.
14. Hedlund TE, Johannes WU and Miller GJ: Soy isoflavonoid equol modulates the growth of benign and malignant prostatic epithelial cells in vitro. Prostate 54: 68-78, 2003.
15. Shenouda NS, Zhou C, Browning JD, Ansell PJ, Sakla MS, Lubahn DB and Macdonald RS: Phytoestrogens in common herbs regulate prostate cancer cell growth in vitro. Nutr Cancer 49: 200-208, 2004.
16. Kobayashi T, Nakata T and Kuzumaki T: Effect of flavonoids on cell cycle progression in prostate cancer cells. Cancer Lett 176: 17-23, 2002.
17. Rabiau N, Kossai M, Braud M, Chalabi N, Satih S, Bignon YJ and Bernard-Gallon DJ: Genistein and daidzein act on a panel of genes implicated in cell cycle and angiogenesis by polymerase chain reaction arrays in human prostate cancer cell lines. Cancer Epidemiol 34: 200-206, 2010.
18. Sarkar FH and Li Y: Mechanisms of cancer chemoprevention by soy isoflavone genistein. Cancer Metastasis Rev 21: 265-280, 2002.
19. Davis JN, Singh B, Bhuiyan M and Sarkar FH: Genistein-induced up-regulation of p21WAF1, down-regulation of cyclin B, and induction of apoptosis in prostate cancer cells. Nutr Cancer 32: 123-131, 1998.
20. Shen JC, Klein RD, Wei Q, Guan Y, Contois JH, Wang TT, Chang S and Hursting SD: Low-dose genistein induces cyclin-dependent kinase inhibitors and G(1) cell-cycle arrest in human prostate cancer cells. Mol Carcinog 29: 92-102, 2000.
21. Choi YH, Lee WH, Park KY and Zhang L: p53-independent induction of p21 (WAF1/CIP1), reduction of cyclin B1 and G2/M arrest by the isoflavone genistein in human prostate carcinoma cells. Jpn J Cancer Res 91: 164-173, 2000.
22. Hedlund TE, van Bokhoven A, Johannes WU, Nordeen SK and Ogden LG: Prostatic fluid concentrations of isoflavonoids in soy consumers are sufficient to inhibit growth of benign and malignant prostatic epithelial cells in vitro. Prostate 66: 557-566, 2006.
23. Kung HJ: Targeting tyrosine kinases and autophagy in prostate cancer. Horm Cancer 2: 38-46, 2011.
24. Wang S, DeGroff VL and Clinton SK: Tomato and soy polyphenols reduce insulin-like growth factor-I-stimulated rat prostate cancer cell proliferation and apoptotic resistance in vitro via inhibition of intracellular signaling pathways involving tyrosine kinase J Nutr 133: 2367-2376, 2003
25. Roskoski R Jr.: ERK1/2 MAP kinases: Structure, function, and regulation. Pharmacol Res 66: 105-43, 2012.
26. Nakamura H, Wang Y, Kurita T, Adomat H, Cunha GR and Wang Y: Genistein increases epidermal growth factor receptor signaling and promotes tumor progression in advanced human prostate cancer. PLoS One 6: e20034, 2011.
27. Sithanandam G and Anderson LM: The ERBB3 receptor in cancer and cancer gene therapy. Cancer Gene Ther 15: 413-448, 2008.
28. Leung EL, Wong JC, Johlfs MG, Tsang BK and Fiscus RR: Protein kinase G type Ialpha activity in human ovarian cancer cells significantly contributes to enhanced SRC activation and DNA synthesis/cell proliferation. Mol Cancer Res 8: 578-591, 2010.
29. Takimoto CH, Glover K, Huang X, Hayes SA, Gallot L, Quinn M, Jovanovic BD, Shapiro A, Hernandez L, Goetz A, Llorens V, Lieberman R, Crowell JA, Poisson BA and Bergan RC: Phase I pharmacokinetic and pharmacodynamic analysis of unconjugated soy isoflavones administered to individuals with cancer. Cancer Epidemiol Biomarker Prev 12: 1213-1221, 2003.
30. Wang X, Clubbs EA and Bomser JA: Genistein modulates prostate epithelial cell proliferation via estrogen-and extracellular signalregulated kinase-dependent pathways. J Nutr Biochem 17: 204-210, 2006.
31. Szliszka E and Krol W: Soy isoflavones augment the effect of TRAIL-mediated apoptotic death in prostate cancer cells. Oncol Rep 26: 533-541, 2011.
32. Hsu A, Bray TM, Helferich WG, Doerge DR and Ho E: Differential effects of whole soy extract and soy isoflavones on apoptosis in prostate cancer cells. Exp Biol Med 235: 90-97, 2010.
33. Raffoul JJ, Wang Y, Kucuk O, Forman JD, Sarkar FH and Hillman GG: Genistein inhibits radiation-induced activation of NF-kappaB in prostate cancer cells promoting apoptosis and G2/M cell cycle arrest. BMC Cancer 6: 107, 2006.
34. Banerjee S, Li Y, Wang Z and Sarkar FH: Multi-targeted therapy of cancer by genistein. Cancer Lett 269: 226-242, 2008.
35. Lin A and Karin M: NF-kappaB in cancer: a marked target. Semin Cancer Biol 13: 107-114, 2003.
36. Jain G, Voogdt C, Tobias A, Spindler KD, Moller P, Cronauer MV and Marienfeld RB: IκB kinases modulate the activity of the androgen receptor in prostate carcinoma cell lines. Neoplasia 14: 178-189, 2012.
37. Jain G, Cronauer MV, Schrader M, Moller P and Marienfeld RB: NF-κB signaling in prostate cancer: A promising therapeutic target? World J Urol 30: 303-310, 2012.
38. Almasan A and Ashkenazi A: Apo2L/TRAIL: Apoptosis signaling, biology and potential for cancer therapy. Cytokine Growth Factor Rev 14: 337-348, 2003.
39. Buneker C, Mohr A and Zwacka RM: The TRAIL-receptor-1: 26. TRAIL-receptor-3 and -4 ratio is a predictor for TRAIL sensitivity of cancer cells. Oncol Rep 21: 1289-1295, 2009.
40. Kazi A, Daniel KG, Smith DM, Kumar NB and Dou QP: Inhibition of the proteasome activity, a novel mechanism associated with the tumor cell apoptosis-inducing ability of genistein. Biochem Pharmacol 66: 965-976, 2003.
41. Yanni SE, Barnett JM, Clark ML and Penn JS: The role of PGE2 receptor EP4 in pathologic ocular angiogenesis. Invest Ophtamol Vis Sci 50: 5479-5486, 2009.
42. Aragon-Ching JB and Dahut WL: The role of angiogenesis inhibitors in prostate cancer. Cancer J 14: 20-25, 2008.
43. Guo Y, Wang S, Hoot DR and Clinton SK: Suppression of VEGFmediated autocrine and paracrine interactions between prostate cancer cells and vascular endothelial cells by soy isoflavones. J Nutr Biochem 18: 408-417, 2007.
44. Rosenbaum-Dekel Y, Fuchs A, Yakirevich E, Azriel A, Mazareb S, Resnick MB and Levi BZ: Nuclear localization of long-VEGF is associated with hypoxia and tumor angiogenesis. Biochem Biophys Res Commun 332: 271-278, 2005.
45. Li Y and Sarkar FH: Down-regulation of invasion and angiogenesis-related genes identified by cDNAmicroarray analysis of PC3 prostate cancer cells treated with genistein. Cancer Lett 186: 157-164, 2002.
46. Huang X, Chen S, Xu L, Liu Y, Deb DK, Platanias LC and Bergan RC: Genistein inhibits p38 map kinase activation, matrix metalloproteinase type 2, and cell invasion in human prostate epithelial cells. Cancer Res 65: 3470-3478, 2005.
47. Xu L and Bergan RC: Genistein inhibits matrix metalloproteinase type 2 activation and prostate cancer cell invasion by blocking the transforming growth factor beta-mediated activation of mitogen-activated protein kinase-activated protein kinase 2 27-kDa heat-shock protein pathway. Mol Pharmacol 70: 869-877, 2006.
48. Xu L, Chen S, and Bergan RC: MAPKAPK2 and HSP27 are downstream effectors of p38 MAP kinase-mediated matrix metalloproteinase type 2 activation and cell invasion in human prostate cancer. Oncogene 25: 2987-2998, 2006.
49. Li Y, Che M, Bhagat S, Ellis KL, Kucuk O, Doerge DR, Abrams J, Cher ML and Sarkar FH: Regulation of gene expression and inhibition of experimental prostate cancer bone metastasis by dietary genistein. Neoplasia 6: 354-363, 2004.
50. Zhou JR, Yu L, Zhong Y, Nassr RL, Franke AA, Gaston SM and Blackburn GL: Inhibition of orthotopic growth and metastasis of androgen-sensitive human prostate tumors in mice by bioactive soybean components. Prostate 53: 143-153, 2002.
51. Bostwick DG, Alexander EE, Singh R, Shan A, Qian J, Santella RM, Oberley LW, Yan T, Zhong W, Jiang X and Oberley TD: Antioxidant enzyme expression and reactive oxygen species damage in prostatic intraepithelial neoplasia and cancer. Cancer 89: 123-134, 2000.
52. Park CE, Yun H, Lee EB, Min BI, Bae H, Choe W, Kang I, Kim SS and Ha J: The antioxidant effects of genistein are associated with AMP-activated protein kinase activation and PTEN induction in prostate cancer cells. J Med Food 13: 815-820, 2010.
53. Suzuki K, Koike H, Matsui H, Ono Y, Hasumi M, Nakazato H, Okugi H, Sekine Y, Oki K, Ito K, Yamamoto T, Fukabori Y, Kurokawa K and Yamanaka H: Genistein, a soy isoflavone, induces glutathione peroxidase in the human prostate cancer cell lines LNCaP and PC-3. Int J Cancer 99: 846-852, 2002.
54. Raschke M, Rowland IR, Magee PJ and Pool-Zobel BL: Genistein protects prostate cells against hydrogen peroxide-induced DNA damage and induces expression of genes involved in the defence against oxidative stress. Carcinogenesis 27: 2322-2330, 2006.
55. Dupont C, Armant DR and Brenner CA: Epigenetics: Definition, mechanisms and clinical perspective. Semin Reprod Med 27: 351-357, 2009.
56. Dehan P, Kustermans G, Guenin S, Horion J, Boniver J and Delvenne P: DNA methylation and cancer diagnosis: New methods and applications. Expert Rev Mol Diagn 9: 651-657, 2009.
57. Long-Cheng Li, Steven T. Okino and Rajvir Dahiya: DNA methylation in prostate cancer. Biochim Biophys Acta 1704: 87-102, 2004.
58. Alumkal JJ, Zhang Z, Humphreys EB, Bennett C, Mangold LA, Carducci MA, Partin AW, Garrett-Mayer E, DeMarzo AM and Herman JG: Effect of DNA methylation on identification of aggressive prostate cancer. Urology 72: 1234-1239, 2008.
59. Mishra DK, Chen Z, Wu Y, Sarkissyan M, Koeffler HP and Vadgama JV: Global methylation pattern of genes in androgensensitive and androgen-independent prostate cancer cells. Mol Cancer Ther 9: 33-45, 2010.
60. Carvalho JR, Filipe L, Costa VL, Ribeiro FR, Martins AT, Teixeira MR, Jeronimo C and Henrique R: Detailed analysis of expression and promoter methylation status of apoptosis-related genes in prostate cancer. Apoptosis 15: 956-965, 2010.
61. Rabiau N, Thiam MO, Satih S, Guy L, Kemeny JL, Boiteux JP, Fontana L, Bignon YJ and Bernard-Gallon D: Methylation analysis of BRCA1, RASSF1, GSTP1 and EPHB2 promoters in prostate biopsies according to different degrees of malignancy. In Vivo 23: 387-391, 2009.
62. Richiardi L, Fiano V, Vizzini L, De Marco L, Delsedime L, Akre O, Tos AG and Merletti F: Promoter methylation in APC, RUNX3, and GSTP1 and mortality in prostate cancer patients. J Clin Oncol 27: 3161-3168, 2009.
63. Vanaja DK, Ehrich M, Van den Boom D, Cheville JC, Karnes RJ, Tindall DJ, Cantor CR and Young CY: Hypermethylation of genes for diagnosis and risk stratification of prostate cancer. Cancer Invest 27: 549-560, 2009.
64. Payne SR, Serth J, Schostak M, Kamradt J, Strauss A, Thelen P, Model F, Day JK, Liebenberg V, Morotti A, Yamamura S, Lograsso J, Sledziewski A and Semjonow A: DNA methylation biomarkers of prostate cancer: Confirmation of candidates and evidence urine is the most sensitive body fluid for non-invasive detection. Prostate 69: 1257-1269, 2009.
65. Bastian PJ, Palapattu GS, Lin X, Yegnasubramanian S, Mangold LA, Trock B, Eisenberger MA, Partin AW and Nelson WG: Preoperative serum DNA GSTP1 CpG island hypermethylation and the risk of early prostate-specific antigen recurrence following radical prostatectomy. Clin Cancer Res 11: 4037-4043, 2005.
66. Roupret M, Hupertan V, Catto JW, Yates DR, Rehman I, Proctor LM, Phillips J, Meuth M, Cussenot O and Hamdy FC: Promoter hypermethylation in circulating blood cells identifies prostate cancer progression. Int J Cancer 122: 952-956, 2008.
67. Garcia MP and Garcia-Garcia A: Epigenome and DNA methylation in oral squamous cell carcinoma. Methods Mol Biol 863: 207-219, 2012.
68. Ling Y, Sankpal UT, Robertson AK, McNally JG, Karpova T and Robertson KD: Modification of de novo DNA methyltransferase 3a (DNMT3a) by SUMO-1 modulates its interaction with histone deacetylases (HDACs) and its capacity to repress transcription. Nucleic Acids Res 32: 598-610, 2004.
69. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, Yamochi T, Urano T, Furukawa K, Kwabi-Addo B, Gold DL, Sekido Y, Huang TH and Issa JP: Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet 40: 741-750, 2008.
70. Walton TJ, Li G, Seth R, McArdle SE, Bishop MC and Rees RC: DNA demethylation and histone deacetylation inhibition cooperate to re-express estrogen receptor beta and induce apoptosis in prostate cancer cell-lines. Prostate 68: 210-222, 2008.
71. Majid S, Kikuno N, Nelles J, Noonan E, Tanaka Y, Kawamoto K, Hirata H, Li LC, Zhao H, Okino ST, Place RF, Pookot D and Dahiya R: Genistein induces the p21WAF1/CIP1 and p16INK4A tumor suppressor genes in prostate cancer cells by epigenetic mechanisms involving active chromatin modification. Cancer Res 68: 2736-2744, 2008.
72. Majid S, Dar AA, Shahryari V, Hirata H, Ahmad A, Saini S, Tanaka Y, Dahiya AV and Dahiya R: Genistein reverses hypermethylation and induces active histone modifications in tumor suppressor gene B-Cell translocation gene 3 in prostate cancer. Cancer 116: 66-76, 2010.
73. Fang MZ, Chen D, Sun Y, Jin Z, Christman JK and Yang CS: Reversal of hypermethylation and reactivation of p16INK4A, RARbeta, and MGMT genes by genistein and other isoflavones from soy. Clin Cancer Res 11: 7033-7041, 2005.
74. Kikuno N, Shiina H, Urakami S, Kawamoto K, Hirata H, Tanaka Y, Majid S, Igawa M and Dahiya R: Genistein mediated histone acetylation and demethylation activates tumor suppressor genes in prostate cancer cells. Int J Cancer 123: 552-560, 2008.
75. Vardi A, Bosviel R, Rabiau N, Adjakly M, Satih S, Dechelotte P, Boiteux JP, Fontana L, Bignon YJ, Guy L and Bernard-Gallon DJ: Soy phytoestrogens modify DNA methylation of GSTP1, RASSF1A, EPH2 and BRCA1 promoter in prostate cancer cells. In Vivo 24: 393-400, 2010.
76. Adjakly M, Bosviel R, Rabiau N, Boiteux JP, Bignon YJ, Guy L and Bernard-Gallon D: DNA methylation and soy phytoestrogens: quantitative study in DU-145 and PC-3 human prostate cancer cell lines. Epigenomics 3: 795-803, 2001.