Novel daidzein molecules exhibited anti-prostate cancer activity through nuclear receptor ERβ modulation, in vitro and in vivo studies

References

• McPherson SJ, Hussain S, Balanathan P, Hedwards SL, Niranjan B, Grant M, et al. Estrogen receptor-beta activated apoptosis in benign hyperplasia and cancer of the prostate is androgen-independent and TNFalpha mediated. Proc Natl Acad Sci USA. 2010; 107:3123–8.
   PubMed Web of Science ®Google Scholar
• EllemSJ R. GP. Treating prostate cancer: a rationale for targeting local oestrogens. Nat Rev Cancer. 2007; 7:7621–7.
   Web of Science ®Google Scholar
• Bonkhoff H, Fixemer T, Hunsicker I, Remberger K. Estrogen receptor expression in prostate cancer and premalignant prostatic lesions. Am J Pathol. 1999; 155:641–7.
   PubMed Web of Science ®Google Scholar
• Horvath LG, Henshall SM, Lee CS, Head DR, Quinn DI, Makela S, et al. Frequent loss of estrogen receptor-beta expression in prostate cancer. Cancer Res. 2001; 155:5331–5.
   Google Scholar
• Pasquali D, Rossi V, Esposito D, Abbondanza C, Puca GA, Bellastella A, et al. Loss of estrogen receptor beta expression in malignant human prostate cells in primary cultures and in prostate cancer tissues. J Clin Endocrinol Metab. 2001; 86:2051–5.
   PubMed Web of Science ®Google Scholar
• Gangkak G, Bhattar R, Mittal A, Yadav SS, Tomar V, Yadav A, et al. Immunohistochemical analysis of estrogen receptors in prostate and clinical correlation in men with benign prostatic hyperplasia. Investig Clin Urol. 2017; 58:117–26.
   PubMed Web of Science ®Google Scholar
• Cheng J, Lee EJ, Madison LD, Lazennec G. Expression of estrogen receptor beta in prostate carcinoma cells inhibits invasion and proliferation and triggers apoptosis. FEBS Lett. 2004; 566:169–72.
   PubMed Web of Science ®Google Scholar
• Zhu X, Leav I, Leung Y-k, Wu M, Liu Q, Gao Y, McNeal JE, Ho S-M. Dynamic regulation of estrogen receptor-beta expression by DNA methylation during prostate cancer development and metastasis. Am J Pathol. 2004;164(6):2003–12.
   PubMed Web of Science ®Google Scholar
• Mahmoud AM, Al-Alem U, Ali MM, Bosland MC. Genistein increases estrogen receptor beta expression in prostate cancer via reducing its promoter methylation. J Steroid Biochem Mol Biol. 2015; 152:62–75.
   PubMed Web of Science ®Google Scholar
• Farzaneh S, Zarghi A. Estrogen receptor ligands: a review (2013-2015). SciPharm. 2016; 1384:409–27.
   Google Scholar
• Sun MY, Ye Y, Xiao L, Rahman K, Xia W, Zhang H. Daidzein: A review of pharmacological effects. Afr J Trad Compl Alt Med. 2016;13(3):117.
   Google Scholar
• Chung ST, Huang YT, Hsiung HY, Huang WH, Yao CW, Lee AR. Novel daidzein analogs and their in vitro anti-influenza activities. Chem Biodivers. 2015;12(4):685–96.
   PubMed Web of Science ®Google Scholar
• Chang C-J, Tsai T-Y. Antimelanogenic effects of the novel melanogenic inhibitors daidzein and equol, derived from soymilk fermented with Lactobacillus plantarum strain TWK10, in B16F0 mouse melanoma cells. J Funct Foods. 2016;22:211–23.
   Web of Science ®Google Scholar
• Zeng S, Tai F, Zhai P, Yuan A, Jia R, Zhang X. Effect of daidzein on anxiety, social behavior and spatial learning in male Balb/cJ mice. Pharmacol Biochem Behav. 2010;96(1):16–23.
   PubMed Web of Science ®Google Scholar
• Kang NH, Shin HC, Oh S, Lee KH, Lee YB, Choi KC. Soy milk digestion extract inhibits progression of prostate cancer cell growth via regulation of prostate cancer-specific antigen and cell cycle-regulatory genes in human LNCaP cancer cells. Mol Med Rep. 2016; 14:1809–16.
   PubMed Web of Science ®Google Scholar
• Kuiper GG, Carlsson B, Grandien K, Enmark E, Häggblad J, Nilsson S. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology. 1997; 138:863–70.
   PubMed Web of Science ®Google Scholar
• Totta P, Acconcia F, Virgili F, Cassidy A, Weinberg PD, Rimbach G, et al. Daidzein-sulfate metabolites affect transcriptional and antiproliferative activities of estrogenreceptor-beta in cultured human cancer cells. J Nutr. 2005; 135:2687–93.
   PubMed Web of Science ®Google Scholar
• Chandrasekharan S, Bhaskar B, Muthiah R, Chandrasekharan AK, Ramamurthy V. Estrogenic effect of three substituted deoxybenzoins. Steroids. 2013; 78:147–55.
   PubMed Web of Science ®Google Scholar
• Liu R, Xu X, Liang C, Chen X, Yu X, Zhong H, et al. ERβ modulates genistein’s cisplatin-enhancing activities in breast cancer MDA-MB-231 cells via P53-independent pathway. Mol Cell Biochem. 2019; 456:205–16.
   PubMed Web of Science ®Google Scholar
• Soto AM, Sonnenschein C, Chung KL, Fernandez MF, Olea N, Serrano FO. The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants. Environ. Health Perspect. 1995; 103:113–22.
   PubMed Web of Science ®Google Scholar
• Brotons JA, Olea-Serrano MF, Villalobos M, Pedraza V, Olea N. Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect. 1995; 103:608–12.
   PubMed Web of Science ®Google Scholar
• Villalobos M, Olea N, Brotons JA, Olea-Serrano MF, Ruiz de Almodovar JM, Pedraza V. PedrazaV.The E-screen assay: a comparison of different MCF7 cell stocks. Environ Health Perspect. 1995;103(9):844–50.
   PubMed Web of Science ®Google Scholar
• Sreeja S, Santhosh Kumar TR, Lakshmi BS, Sreeja S. Pomegranate extract demonstrate a selective estrogen receptor modulator profile in human tumor cell lines and in vivo models of estrogen deprivation. J Nutr Biochem. 2012;23(7):725–32.
   PubMed Web of Science ®Google Scholar
• Angelis MD, Stossi F, Waibel M, Katzenellenbogen BS, Katzenellenbogen JA. Isocoumarins as estrogen receptor beta selective ligands: Isomers of isoflavone phytoestrogens and their metabolites. Bioorg Med Chem. 2005; 13:6529–42.
   PubMed Web of Science ®Google Scholar
• Walton TJ, Li G, McCulloch TA, Seth R, Powe DG, Bishop MC, Rees RC. Quantitative RT-PCR analysis of estrogen receptor gene expression in laser microdissected prostate cancer tissue. Prostate. 2009;69(8):810–9.
   PubMed Web of Science ®Google Scholar
• Fields WR, Desiderio JG, Putnam KP, Bombick DW, Doolittle DJ. Quantification of changes in c-myc mRNA levels in normal human bronchial epithelial (NHBE) and lung adenocarcinoma (A549) cells following chemical treatment. Toxicol Sci. 2001; 63(1):107–14.
   PubMed Web of Science ®Google Scholar
• Suzuki R, Takemura K, Tsutsumi M, Nakamura S, Hamajima N, Seto M. Detection of cyclin D1 overexpression by real-time reverse-transcriptase-mediated quantitative polymerase chain reaction for the diagnosis of mantle cell lymphoma. Am J Pathol. 2001;159(2):425–9.
   PubMed Web of Science ®Google Scholar
• Křížová L, Dadáková K, Kašparovská J, Kašparovský T. Isoflavones. Molecules. 2019;24(6):1076.
   Web of Science ®Google Scholar
• Kumar R, Verma V, Jain A, Jain RK, Maikhuri JP, Gupta G. Synergistic chemoprotective mechanisms of dietary phytoestrogens in a select combination against prostate cancer. J Nutr Biochem. 2011; 22:723–31.
   PubMed Web of Science ®Google Scholar
• Adjakly M, Ngollo M, Boiteux JP, Bignon YJ, Guy L, Bernard-Gallon D. Genistein and daidzein: different molecular effects on prostate cancer. Anticancer Res. 2013; 33:39–44.
   PubMed Web of Science ®Google Scholar
• Hsu A, Bray TM, Helferich WG, Doerge DR, Ho E. Differential effects of whole soy extract and soy isoflavones on apoptosis in prostate cancer cells. Exp Biol Med (Maywood). 2010;235(1):90–7.
   PubMed Web of Science ®Google Scholar
• McPherson SJ, Ellem SJ, Simpson ER, Patchev V, Fritzemeier KH, Risbridger GP. Essential role for estrogen receptor beta in stromal–epithelial regulation of prostatic hyperplasia. Endocrinology. 2007; 148:566–74.
   PubMed Web of Science ®Google Scholar
• Marik R, Allu M, Anchoori R, Stearns V, Umbricht CB, Khan S. Potent genistein derivatives as inhibitors of estrogen receptor alpha-positive breast cancer. Cancer Biol Ther. 2011; 11:883–92.
   PubMed Web of Science ®Google Scholar
• Seo H-S, DeNardo DG, Jacquot Y, Laïos I, Vidal DS, Zambrana CR, Leclercq G, Brown PH. Stimulatory effect of genistein and apigenin on the growth of breast cancer cells correlates with their ability to activate ER alpha. Breast Cancer Res Treat. 2006;99(2):121–34.
   PubMed Web of Science ®Google Scholar
• Collins-Burow BM, Burow ME, Duong BN, McLachlan JA. Estrogenic and antiestrogenic activities of flavonoid phytochemicals through estrogen receptor binding-dependent and -independent mechanisms. Nutr Cancer. 2000;38(2):229–44.
   PubMed Web of Science ®Google Scholar
• Setchell KD. Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones. Am J Clin Nutr. 1998; 68:1333–46.
   PubMed Web of Science ®Google Scholar
• Wang C, Kurzer MS. Phytoestrogen concentration determines effects on DNA synthesis in human breast cancer cells. Nutr Cancer. 1997;28(3):236–47.
   PubMed Web of Science ®Google Scholar
• Christoforou P, Christopoulos PF, Koutsilieris M. The role of estrogen receptor beta in prostate cancer. Mol Med. 2014;20:427–34.
   PubMed Web of Science ®Google Scholar
• Koh CM, Bieberich CJ, Dang CV, Nelson WG, Yegnasubramanian S, De Marzo AM. MYC and Prostate Cancer. Genes Cancer. 2010;1(6):617–28.
   PubMedGoogle Scholar
• Fiandalo MV, Kyprianou N. Caspase control: protagonists of cancer cell apoptosis. Exp Oncol. 2012;34(3):165–75.
   PubMedGoogle Scholar
• Loreto C, La Rocca G, Anzalone R, Caltabiano R, Vespasiani G, Castorina S, Ralph DJ, Cellek S, Musumeci G, Giunta S, et al. The role of intrinsic pathway in apoptosis activation and progression in Peyronie's disease. Biomed Res Int. 2014;2014:616149.
   PubMed Web of Science ®Google Scholar
• Pettaway CA, Pathak S, Greene G, Ramirez E, Wilson MR, Killion JJ, Fidler IJ. Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin Cancer Res. 1996;2(9):1627–36.
   PubMed Web of Science ®Google Scholar
• Park SI, Zhang J, Phillips KA, Araujo JC, Najjar AM. Targeting Src family kinases inhibits growth and lymph node metastases of prostate cancer in an orthotopic nude mouse model. Cancer Res. 2008;68(9):3323–33. [Internet]
   PubMed Web of Science ®Google Scholar
• Mal R, Magner A, David J, Datta J, Vallabhaneni M, Kassem M, Manouchehri J, Willingham N, Stover D, Vandeusen J, et al. Estrogen Receptor Beta (ERβ): A Ligand Activated Tumor Suppressor. Front Oncol. 2020;10:587386.
   PubMed Web of Science ®Google Scholar
• Lazennec G, Bresson D, Lucas A, Chauveau C, Vignon F. ER beta inhibits proliferation and invasion of breast cancer cells. Endocrinology. 2001;142(9):4120–30.
   PubMed Web of Science ®Google Scholar