Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T20:28:20.326Z Has data issue: false hasContentIssue false

Soya phytonutrients act on a panel of genes implicated with BRCA1and BRCA2 oncosuppressors in human breast cell lines

Published online by Cambridge University Press:  08 March 2007

Bertrand Caëtano
Affiliation:
Département d'Oncogénétique du Centre Jean PerrinINSERM UMR 484-UdA, Centre Biomédical de Recherche et de Valorisation, 28 place Henri Dunant, B.P.38, 63 001 Clermont-Ferrand Cedex 01, France
Ludovic Le Corre
Affiliation:
Département d'Oncogénétique du Centre Jean PerrinINSERM UMR 484-UdA, Centre Biomédical de Recherche et de Valorisation, 28 place Henri Dunant, B.P.38, 63 001 Clermont-Ferrand Cedex 01, France
Nassera Chalabi
Affiliation:
Département d'Oncogénétique du Centre Jean PerrinINSERM UMR 484-UdA, Centre Biomédical de Recherche et de Valorisation, 28 place Henri Dunant, B.P.38, 63 001 Clermont-Ferrand Cedex 01, France
Laetitia Delort
Affiliation:
Département d'Oncogénétique du Centre Jean PerrinINSERM UMR 484-UdA, Centre Biomédical de Recherche et de Valorisation, 28 place Henri Dunant, B.P.38, 63 001 Clermont-Ferrand Cedex 01, France
Yves-Jean Bignon*
Affiliation:
Département d'Oncogénétique du Centre Jean PerrinINSERM UMR 484-UdA, Centre Biomédical de Recherche et de Valorisation, 28 place Henri Dunant, B.P.38, 63 001 Clermont-Ferrand Cedex 01, France
Dominique J. Bernard-Gallon
Affiliation:
Département d'Oncogénétique du Centre Jean PerrinINSERM UMR 484-UdA, Centre Biomédical de Recherche et de Valorisation, 28 place Henri Dunant, B.P.38, 63 001 Clermont-Ferrand Cedex 01, France
*
*corresponding author: Professor Yves-Jean Bignon, fax +33 4 73 27 80 42, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Breast cancer is the most common cancer in women and a significant cause of death. Mutations of the oncosuppressor genes BRCA1 and BRCA2 are associated with a hereditary risk of breast cancer, and dysregulation of their expression has been observed in sporadic cases. Soya isoflavones have been shown to inhibit breast cancer in studies in vitro, but associations between the consumption of isoflavone-containing foods and breast cancer risk have varied in epidemiological studies. Soya is a unique source of the phytoestrogens daidzein (4′,7-dihydroxyisoflavone) and genistein (4′,5,7-trihydroxyisoflavone), two molecules that are able to inhibit the proliferation of human breast cancer cells in vitro. The aim of the present study was to determine the effects of genistein (5μg/ml) and daidzein (20μg/ml) on transcription in three human breast cell lines (one dystrophic, MCF10a, and two malignant, MCF-7 and MDA-MB-231) after 72h treatment. The different genes involved in the BRCA1 and BRCA2 pathways (GADD45A, BARD1, JUN, BAX, RB1, ERα, ERβ, BAP1, TNFα, p53, p21Waf1/Cip1, p300, RAD51, pS2, Ki-67) were quantified by real-time quantitative RT-PCR, using the TaqMan method and an ABI Prism 7700 Sequence Detector (Applied Biosystems). We observed that, in response to treatment, many of these genes were overexpressed in the breast cancer cell lines (MCF-7 and MDA-MB-231) but not in the dystrophic cell line (MCF10a).

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Alhasan, SA, Aranha, O &Sarkar, FHGenistein elicits pleiotropic molecular effects on head and neck cancer cells. Clin Cancer Res 2001 7, 41744181.Google ScholarPubMed
Aprelikova, ON, Fang, BS, Meissner, EG, Cotter, S, Campbell, M, Kuthiala, A, Bessho, M, Jensen, RA & Liu, ET (1999) BRCA1-associated growth arrest is RB-dependent. Proc Natl Acad Sci USA. 96, 11886–11871.CrossRefGoogle ScholarPubMed
Arai, Y, Watanabe, S, Kimira, M, Shimoi, K, Mochizuki, R & Kinae, NDietary intakes of flavonols, flavones and isoflavones by Japanese women and the inverse correlation between quercetin intake and plasma LDL cholesterol concentration J Nutr 2000 130, 22432250.CrossRefGoogle ScholarPubMed
Balabhadrapathruni, S, Thomas, TJ, Yurkow, EJ, Amenta, PS & Thomas, TEffects of genistein and structurally related phytoestrogens on cell cycle kinetics and apoptosis in MDA-MB-468 human breast cancer cells Oncol Rep. 2000 7, 312Google ScholarPubMed
Barnes, S & Peterson, TGBiochemical targets of the isoflavone genistein in tumor cell lines. Proc Soc Exp Biol Med 1995 208, 103108CrossRefGoogle ScholarPubMed
Bernard-Gallon, DJ, Maurizis, JC, Rio, PG & Bignon, YJInfluence of genistein and daidzein on Brca1 protein levels in human breast cell lines. J Natl Cancer Inst 1998 90, 862863.CrossRefGoogle ScholarPubMed
Bernard-Gallon, DJ, Vissac-Sabatier, C, Antoine-Vincent, D, Rio, PG,Maurizis, JC, Fustier, P& Bignon, YJDifferential effects of n-3 and n-6 polyunsaturated fatty acids on BRCA1 and BRCA2 gene expression in breast cell lines. Br J Nutr 2002 87, 281289.CrossRefGoogle ScholarPubMed
Cailleau, R, Young, R, Olive, M & Reeves, WJ JrBreast tumor cell lines from pleural effusions. J Natl Cancer Inst 1974 53, 661674.CrossRefGoogle ScholarPubMed
Chen, J, Silver, DP, Walpita, D, Cantor, SB, Gazdar, AF, Tomlinson, G, Couch, FJ, Weber, BL, Ashley, T, Livingston, DM & Scully, RStable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells Mol Cell 1998 2, 317328.CrossRefGoogle ScholarPubMed
Chen, Z, Zheng, W, Custer, LJ, Dai, Q, Shu, XO, Jin, F & Franke, AAUsual dietary consumption of soy foods and its correlation with the excretion rate of isoflavonoids in overnight urine samples among Chinese women in Shanghai Nutr Cancer 1999 33, 8287.CrossRefGoogle ScholarPubMed
Choi, YH, Zhang, L, Lee, WH & Park, KYGenistein-induced G2/M arrest is associated with the inhibition of cyclin B1 and the induction of p21 in human breast carcinoma cells. Int J Oncol 1998 13, 391396Google ScholarPubMed
Claus, EB, Risch, N & Thompson, WDGenetic analysis of breast cancer in the cancer and steroid hormone study. Am J Hum Genet 1991 48, 232242Google ScholarPubMed
Coward, L, Kirk, M, Albin, N & Barnes, SAnalysis of plasma isoflavones by reversed-phase HPLC-multiple reaction ion monitoring-mass spectrometry. Clin Chim Acta 1996 247, 121142.CrossRefGoogle ScholarPubMed
Dai, Q, Shu, XO, Jin, F, Potter, JD, Kushi, LH, Teas, J, Gao, YT & Zheng, WPopulation-based case-control study of soyfood intake and breast cancer risk in Shanghai. Br J Cancer 2001 85, 372378.CrossRefGoogle ScholarPubMed
Fan, S, Ma, YX, Wang, C et al. . Role of direct interaction in BRCA1 inhibition of estrogen receptor activity Oncogene 2001 20. 7787.CrossRefGoogle ScholarPubMed
Fan, S, Ma, YX, Wang, C et al. . p300 Modulates the BRCA1 inhibition of estrogen receptor activity. Cancer Res 2002 62, 141151.Google ScholarPubMed
Favy, DA, Lafarge, S, Rio, P, Vissac, C, Bignon, YJ & Bernard-Gallon, DReal-time PCR quantification of full-length and exon 11 spliced BRCA1 transcripts in human breast cancer cell lines. Biophys Res Commun 2000 274, 7378.CrossRefGoogle ScholarPubMed
Fink, L, Seeger, W, Ermert, W, Hanze, J, Stahl, U, Grimminger, F, Kummer, W & Bohle, RMReal-time quantitative RT-PCR after laser-assisted cell picking. Nat Med 1998 4, 13291333.CrossRefGoogle ScholarPubMed
Fioravanti, L, Cappelletti, V, Miodini, P, Ronchi, E, Brivio, M & DiFronzo, GGenistein in the control of breast cancer cell growth: insights into the mechanism of action in vitro. Cancer Lett 1998 130, 143152.CrossRefGoogle ScholarPubMed
Fotsis, T, Pepper, M, Adlercreutz, H, Fleischmann, G, Hase, T & Montesano, R, Schweigerer, LGenistein, a dietary-derived inhibitor of in vitro angiogenesis. Proc Natl Acad Sci USA 1993 90, 26902694.CrossRefGoogle ScholarPubMed
Futreal, PA, Liu, Q, Shattuck-Eidens, D et al. . BRCA1 mutations in primary breast and ovarian carcinomas. Science 1994 266, 120122.CrossRefGoogle ScholarPubMed
Grace, PB, Taylor, JI, Low, YL et al. . Phytoestrogen concentrations in serum and spot urine as biomarkers for dietary phytoestrogen intake and their relation to breast cancer risk in European prospective investigation of cancer and nutrition-norfolk. Cancer Epidemiol Biomarkers Prev 2004 13, 698708.CrossRefGoogle ScholarPubMed
Greenstein, JKushi, L, Zheng, W, Fee, R, Campbell, D, Sellers, T & Folsom, ARisk of breast cancer associated with intake of specific foods and food groups. Am J Epidemiol 1996 143, s36.Google Scholar
Hirose, K, Tajima, K, Hamajima, N, Inoue, M, Takezaki, T, Kuroishi, TYoshida, M & Tokudome, SA large-scale, hospital-based case-control study of risk factors of breast cancer according to menopausal status. Jpn J Cancer Res 1995 86, 146154.CrossRefGoogle ScholarPubMed
Hong, SJ, Kim, SI, Kwon, SM, Lee, JR & Chung, BCComparative study of concentration of isoflavones and lignans in plasma and prostatic tissues of normal control and benign prostatic hyperplasia. Yonsei Med J 2002 43, 236241.CrossRefGoogle ScholarPubMed
Horn-Ross, PL, John, EM, Lee, M, Stewart, SL, Koo, j, Sakoda, LC, Shiau, AC, Goldstein, j, Davis, p & Perez-Stable, EJPhytoestrogen consumption and breast cancer risk in a multiethnic population: the Bay Area Breast Cancer Study. Am J Epidemiol 2001 154, 434441.CrossRefGoogle Scholar
Horn-Ross, PL, Lee, M, John, EM & Koo, TSources of phytoestrogen exposure among non-Asian women in California, USA. Cancer Causes Control. 2000 11, 299302.CrossRefGoogle ScholarPubMed
Hsieh, CY, Santell, RC, Haslam, SZ & Helferich, WGEstrogenic 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, 38333838.Google ScholarPubMed
Izumi, T, Piskula, MK, Osawa, S, Obata, A, Tobe, K, Saito, M, Kataoka, S, Kubota, Y & Kikuchi, MSoy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. J Nutr 2000 130, 16951699.CrossRefGoogle ScholarPubMed
Jin, S, Tong, T, Fan, W et al. . GADD45-induced cell cycle G2-M arrest associates with altered subcellular distribution of cyclin B1 and is independent of p38 kinase activity. Oncogene 2002 21, 86968704.CrossRefGoogle ScholarPubMed
Keinan-Boker, L, Peeters, PH, Mulligan, AA et al. . Soy product consumption in 10 European countries: the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr 2002 5, 12171226.CrossRefGoogle ScholarPubMed
Kim, H, Peterson, TG & Barnes, SMechanisms of action of the soy isoflavone genistein: emerging role for its effects via transforming growth factor beta signaling pathways. Am J Clin Nutr 1998 68, 1418S1425S.Google ScholarPubMed
King, RA & Bursill, DBPlasma and urinary kinetics of the iso-flavones daidzein and genistein after a single soy meal in humans. Am J Clin Nutr 1998 67, 867872.CrossRefGoogle Scholar
Kuiper, GG, Carlsson, B, Grandien, K, Enmark, E, Haggblad, J, Nilsson, S & Gustafsson, JAComparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997 138, 863870.CrossRefGoogle ScholarPubMed
Kuiper, GG, Lemmen, JG, Carlsson, B, Corton, JC, Safe, SH, van, der, Saag, PT, van, derBurg, B & Gustafsson, JAInteraction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998 139, 42524263CrossRefGoogle ScholarPubMed
Lamartiniere, CA, Cotroneo, MS, Fritz, WA, Wang, JMentor-Marcel, R & Elgavish, AGenistein chemoprevention: timing and mechanisms of action in murine mammary and prostate. J Nutr 2002 132, 552S558S.CrossRefGoogle ScholarPubMed
Lamartiniere, CA, Moore, J, Holland, M & Barnes, SNeonatal genistein chemoprevents mammary cancer. Proc Soc Exp Biol Med 1995 208, 120123.CrossRefGoogle ScholarPubMed
Le Bail, JC, Varnat, F, Nicolas, JC & Habrioux, GEstrogenic and antiproliferative activities on MCF-7 human breast cancer cells by flavonoids. Cancer Lett 1998 130, 209216.CrossRefGoogle ScholarPubMed
Le Corre, L, Fustier, P, Chalabi, N, Bignon, YJ & Bernard-Gallon, DEffects of resveratrol on the expression of a panel of genes interacting with the BRCA1 oncosuppressor in human breast cell lines. Clin Chim Acta 2004 344, 115121.CrossRefGoogle ScholarPubMed
Lee, HP, Gourley, L, Duffy, SW, Esteve, J, Lee, J & Day, NEDietary effects on breast-cancer risk in Singapore. Lancet 1991 337, 11971200.CrossRefGoogle ScholarPubMed
Li, Y, Upadhyay, S, Bhuiyan, M & Sarkar, FHInduction of apoptosis in breast cancer cells MDA-MB-231 by genistein. Oncogene 1999 18, 31663172.CrossRefGoogle ScholarPubMed
Maggiolini, M, Bonofiglio, D, Marsico, S,Panno, ML, Cenni, B, Picard, D & Ando, SEstrogen receptor alpha mediates the proliferative but not the cytotoxic dose-dependent effects of two major phytoestrogens on human breast cancer cells. Mol Pharmacol 2001 60, 595Google Scholar
Marks, JR, Huper, G, Vaughn, JP, Davis, PL, Norris, J, McDonnell, DP, Wiseman, RW, Futreal, PA & Iglehart, JDBRCA1 expression is not directly responsive to estrogen. Oncogene 1997 14, 115121.CrossRefGoogle Scholar
Miki, Y, Swensen, J, Shattuck-Eidens, D et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 1994 266, 6671.CrossRefGoogle Scholar
Morris, SM, Chen, JJ, Domon, OE,McGarrity, LJBishop, ME, Manjanatha, MG & Casciano, DAp53, mutations, and apoptosis in genistein-exposed human lymphoblastoid cells. Mutat Res 1998 405, 4156.CrossRefGoogle ScholarPubMed
Neuteboom, ST, Karjian, PL, Boyer, CR, Beryt, M, Pegram, M, Wahl, GM & Shepard, HMInhibition of cell growth by NB1011 requires high thymidylate synthase levels and correlates with p53, p21, bax, and GADD45 induction. Mol Cancer Ther 2002 1, 377384.Google ScholarPubMed
Nomoto, S, Arao, Y, Horiguchi, H,Ikeda, K & Kayama, FOestrogen causes G2/M arrest and apoptosis in breast cancer cells MDA-MB-231. Oncol Rep 2002 9, 773776Google ScholarPubMed
Pao, GM, Janknecht, R, Ruffner, H, Hunter, T & Verma, IMCBP/p300 interact with and function as transcriptional coactivators of BRCA1 Proc Natl Acad Sci USA 2000 97, 10201025.CrossRefGoogle ScholarPubMed
Peterson, GEvaluation of the biochemical targets of genistein in tumor cells. J Nutr 1995 125, 784S789SGoogle ScholarPubMed
Sathyamoorthy, N & Wang, TTDifferential effects of dietary phyto-oestrogens daidzein and equol on human breast cancer MCF-7 cells Eur J Cancer 1997 33, 23842389.CrossRefGoogle ScholarPubMed
Shao, ZM, Alpaugh, ML, Fontana, JA & Barsky, SHGenistein inhibits proliferation similarly in estrogen receptor-positive and negative human breast carcinoma cell lines characterized by P21WAF1/CIP1 induction, G2/M arrest, and apoptosis J Cell Biochem 1998 69, 4454.3.0.CO;2-V>CrossRefGoogle Scholar
Shu, XO, Jin, F, Dai, Q, Wen, W, Potter, JD, Kushi, LH, Ruan, Z, Gao, YT & Zheng, WSoyfood intake during adolescence and subsequent risk of breast cancer among Chinese women. Cancer Epidemiol Biomarkers Prev 2001 10, 483488.Google ScholarPubMed
Soule, HDMaloney, TMWolman, SRPeterson, WD JrBrenz, RMcGrath, CMRusso, JPauley, RJJones, RF&Brooks, SCIsolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 1990 50 60756086Google ScholarPubMed
Soule, HDVazguez, JLong, AAlbert, S&Brennan, MA human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst 1973 51 14091416CrossRefGoogle ScholarPubMed
Spillman, MA&Bowcock, AMBRCA1 and BRCA2 mRNA levels are coordinately elevated in human breast cancer cells in response to estrogen. Oncogene 1996 13 16391645Google ScholarPubMed
Srivastava, SWeitzmann, MNCenci, SRoss, FPAdler, S &Pacifici, REstrogen decreases TNF gene expression by blocking JNK activity and the resulting production of c-Jun and JunD. J Clin Invest 1999 104 503513CrossRefGoogle ScholarPubMed
Takahashi, YLavigne, JAHursting, SDChandramouli, GVPerkins, SNBarrett, JC &Wang, TTUsing DNA microarray analyses to elucidate the effects of genistein in androgen-responsive prostate cancer cells: identification of novel targets. Mol Carcinog 2004 41 108119CrossRefGoogle ScholarPubMed
Thompson, MEJensen, RAObermiller, PSPage, DL & Holt, JTDecreased expression of BRCA1 accelerates growth and is often present during sporadic breast cancer progression. Nat Genet 1995 9 444450CrossRefGoogle ScholarPubMed
Vissac-Sabatier, CBignon, Y-J&Bernard-Gallon, DJEffects of the phytoestrogens genistein and daidzein on BRCA2 tumor suppress or gene expression in breast cell lines Nutr Cancer 2003 45 247255CrossRefGoogle ScholarPubMed
Welcsh, PLOwens, KN&King, MCInsights into the functions of BRCA1 and BRCA2. Trends Genet 2000 16 6974CrossRefGoogle ScholarPubMed
Witte, JSUrsin, GSiemiatycki, JThompson, WDPaganini-Hill, A&Haile, RWDiet and premenopausal bilateral breast cancer: a case-control study Breast Cancer Res Treat 1997 42 243251CrossRefGoogle ScholarPubMed
Wooster, RBignell, GLancaster, JSwift, SSeal, SMangion, JCollins, NGregory, SGumbs, C & Micklem, GIdentification of the breast cancer susceptibility gene BRCA2. Nature 1995 378 789792CrossRefGoogle ScholarPubMed
Wu, AHZiegler, RGHorn-Ross, PLNomura, AMWest, DWKolonel, LNRosenthal, JFHoover, RN &Pike, MCTofu and risk of breast cancer in Asian-Americans. Cancer Epidemiol Biomarkers Prev 1996 5 901906Google ScholarPubMed
Xu, XWang, HJMurphy, PACook, L &Hendrich, SDaidzein is a more bioavailable soymilk isoflavone than is genistein in adult women. J Nutr 1994 124 825832CrossRefGoogle ScholarPubMed
Yuan, JMWang, QSRoss, RKHenderson, BE&Yu, MCDiet and breast cancer in Shanghai and Tianjin, China Br J Cancer 1995 71 13531358CrossRefGoogle ScholarPubMed
Zava, DT&Duwe, GEstrogenic and antiproliferative properties of genistein and other flavonoids in human breast cancer cells in vitro. Nutr Cancer 1997 27 3140CrossRefGoogle ScholarPubMed
Zhang, HSomasundaram, KPeng, YTian, HBi, DWeber, BL&El-Deiry, WSBRCA1 physically associates with p53 and stimulates its transcriptional activity. Oncogene 1998 16 17131721CrossRefGoogle ScholarPubMed