Can the combination of flaxseed and its lignans with soy and its isoflavones reduce the growth stimulatory effect of soy and its isoflavones on established breast cancer?

Molecular Nutrition and Food Research

Volumn 51, Issue 7, 2007, Pages 845-856

  Power, Krista A ^a   Thompson, Lilian U ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Breast cancer; Flaxseed; Isoflavones; Lignans; Soy

Indexed keywords

ANTINEOPLASTIC AGENT; GENISTEIN; ISOFLAVONE DERIVATIVE; LIGNAN; PHYTOESTROGEN; SOYBEAN PROTEIN;

ANIMAL; ARTICLE; BREAST TUMOR; CELL DIVISION; CHEMICALLY INDUCED DISORDER; CHEMISTRY; DIET; DRUG EFFECT; FEMALE; FLAX; HUMAN; PATHOLOGY; POSTMENOPAUSE; RANDOMIZED CONTROLLED TRIAL; SOYBEAN;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL DIVISION; DIET; FEMALE; FLAX; GENISTEIN; HUMANS; ISOFLAVONES; LIGNANS; PHYTOESTROGENS; POSTMENOPAUSE; RANDOMIZED CONTROLLED TRIALS; SOYBEAN PROTEINS; SOYBEANS;

GLYCINE MAX; MAMMALIA; MUS MUSCULUS; RODENTIA;

EID: 34547446231     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200600218     Document Type: Article

References (79)

1. Kurzer, M. S., Xu, X., Dietary phytoestrogens, Annu. Rev. Nutr. 1997, 17, 353-381.
2. Adlercreutz, H., Phytoestrogens and breast cancer, J. Steroid Biochem. Mol. Biol. 2002, 83, 113-118.
3. Adlercreutz, H., Mazur, W., Phyto-oestrogens and Western diseases, Ann. Med. 1997, 29, 95-120.
4. Thompson, L. U., Boucher, B. A., Liu, Z., Cotterchio, M., Kreiger, N., Phytoestrogen content of foods consumed in Canada, including isoflavones, lignans, and coumestan, Nutr. Cancer 2006, 54, 184-201.
5. Jacobs, E., Kulling, S. E., Metzler, M., Novel metabolites of the mammalian lignans enterolactone and enterodiol in human urine, J. Steroid Biochem. Mol. Biol. 1999, 68, 211-218.
6. Setchell, K. D., Lawson, A. M., Bordello, S. P., Harkness, R. et al., Lignan formation in man-microbial involvement and possible roles in relation to cancer, Lancet 1981, 2, 4-7.
7. Turner, N. J., Thomson, B. M., Shaw, I. C., Bioactive isoflavones in functional foods: The importance of gut microflora on bioavailability, Nutr. Rev. 2003, 61, 204-213.
8. Duffy, C., Cyr, M. J., Phytoestrogens: Potential benefits and implications for breast cancer survivors, Womens Health (Larchmt) 2003, 12, 617-631.
9. Messina, M. J., Loprinzi, C. L., Soy for breast cancer survivors: A critical review of the literature, J. Nutr. 2001, 131, 3095S-3108S.
10. Norman, H. A., Butrum, R. R., Feldman, E., Heber, D., et al., The role of dietary supplements during cancer therapy, J. Nutr. 2003, 133, 3794S-3799S.
11. Messina, M., McCaskill-Stevens, W., Lampe, J. W., Addressing the soy and breast cancer relationship: Review, commentary, and workshop proceedings, Natl. Cancer Inst. 2006, 98, 1275-1284.
12. Saarinen, N. M., Power, K., Chen, J., Thompson, L. U., Flaxseed attenuates the tumor growth stimulating effect of soy protein in ovariectomized athymic mice with MCF-7 human breast cancer xenografts, Int. J. Cancer 2006, 119, 925-931.
13. Allred, C., Allred, K., Ju, Y., Virant, S. M., Helferich, W. G., Soy diets containing varying amounts of genistein stimulate growth of estrogen-dependent (MCF-7) tumors in a dose-dependent manner, Cancer Res. 2001, 61, 5045-5050.
14. Ju, Y. H., Allred, C. D., Allred, K. F., Karko, K. L., et al., Physiological concentrations of dietary genistein dose-dependently stimulate growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in athymic nude mice, J. Nutr. 2001, 131, 2957-2962.
15. Ju, Y. H., Allred, K. F., Allred, C. D., Helferich, W. G., Genistein stimulates growth of human breast cancer cells in a novel, postmenopausal animal model, with low plasma estradiol concentrations, Carcinogenesis 2006, 27, 1292-1299.
16. Power, K. A., Saarinen, N. M., Chen, J. M., Thompson, L. U., Mammalian lignans enterolactone and enterodiol, alone and in combination with the isoflavone genistein, do not promote the growth of MCF-7 xenografts in ovariectomized athymic nude mice, Int. J. Cancer 2006, 118, 1316-1320.
17. Allred, C. D., Ju, Y. H., Allred, K. F., Chang, J., Helferich, W. G., Dietary genistin stimulates growth of estrogen-dependent breast cancer tumors similar to that observed with genistein, Carcinogenesis 2001, 22, 1667-1673.
18. Allred, C. D., Allred, K. F., Ju, Y. H., Goeppinger, T. S., et al., Dietary genistein results in larger MNU-induced, estrogen-dependent mammary tumors following ovariectomy of Sprague-Dawley rats, Carcinogenesis 2004, 25, 1649-1657.
19. Power, K. A., Thompson, L. U., in: Awad, A., Bradford, P. (Eds.), Nutrition and Cancer Prevention, CRC Press Boca Raton, FL, USA 2006, pp. 385-410.
20. Thompson, L. U., Chen, J. M., Li, T., Strasser-Weippl., K., Goss, P. E., Dietary flaxseed alters tumor biological markers in postmenopausal breast cancer, Clin. Cancer Res. 2005, 11, 3828-3835.
21. Mazur, W., Phytoestrogen content in foods, Baillieres Clin. Endocrinol. Metab. 1998, 12, 729-742.
22. Power, K. A., Thompson, L. U., Ligand-induced regulation of ERalpha and ERbeta is indicative of human breast cancer cell proliferation, Breast Cancer Res. Treat. 2003, 81, 209-221.
23. Vladusic, E. A., Hornby, A. E., Guerra-Vladusic, F. K., Lakins, J., Lupu, R., Expression and regulation of estrogen receptor beta in human breast tumors and cell lines, Oncol. Rep. 2000, 7, 157-167.
24. Macaluso, M., Montanari, M., Noto, P. B., Gregorio, V, et al., Nuclear and cytoplasmic interaction of pRb2/p130 and ER-{beta} in MCF-7 breast cancer cells, Ann. Oncol. 2006, 17, vii27-vii29.
25. Horner-Glister, E., Maleki-Dizaji, M., Guerin, C. J., Johnson, S. M. et al., Influence of oestradiol and tamoxifen on oestrogen receptors-alpha and -beta protein degradation and nongenomic signalling pathways in uterine and breast carcinoma cells, J. Mol. Endocrinol. 2005, 35, 421-432.
26. Hsieh, C. Y., Santell, R. C., Haslam, S. Z., Helferich, W. G., 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, 3833-3838.
27. Folkerd, E. J., Martin, L. A., Kendall, A., Dowsett, M., The relationship between factors affecting endogenous oestradiol levels in postmenopausal women and breast cancer, J. Steroid Biochem. Mol. Biol. 2006, in press.
28. Head, K., Isoflavones and other soy constituents in human health and disease, Alt. Med. Rev. 1997, 2, 433-450.
29. Erdman, J. W., Jr., Badger, T. M., Lampe, J. W., Setchell, K. D., Messina, M., Not all soy products are created equal: Caution needed in interpretation of research results, J. Nutr. 2004, 134, 1229S-1233S.
30. Gallo, D., Ferlini, C., Fabrizi, M., Prislei, S., Scambia, G., Lack of stimulatory activity of a Phytoestrogen-containing soy extract on the growth of breast cancer tumors in mice, Carcinogenesis 2006, 27, 1404-1409.
31. Penalvo, J. L., Heinonen, S. M., Nurmi, T., Deyama, T., et al., Plant lignans in soy-based health supplements, J. Agric. Food Chem. 2004, 52, 4133-4138.
32. Nurmi, T., Mazur, W., Heinonen, S., Kokkonen, J., Adlercreutz, H., Isoflavone content of the soy based supplements, J. Pharm. Biomed. Anal. 2002, 28, 1-11.
33. Ju, Y. H., Fultz, J., Allred, K. F., Doerge, D. R., Helferich, W. G., Effects of dietary daidzein and its metabolite, equol, at physiological concentrations on the growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in ovariectomized athymic mice, Carcinogenesis 2006, 27, 856-863.
34. Ju, Y. H., Doerge, D. R., Allred, K. F., Allred, C. D., Helferich, W. G., Dietary genistein negates the inhibitory effect of tamoxifen on growth of estrogen-dependent human breast cancer (MCF-7) cells implanted in athymic mice, Cancer Res. 2002, 62, 2474-2477.
35. Liu, B., Edgerton, S., Yang, X., Kim, A., et al., Low-dose dietary phytoestrogen abrogates tamoxifen-associated mammary tumor prevention, Cancer Res. 2005, 65, 879-886.
36. Santell, R. C., Kieu, N., Helferich, W. G., Genistein inhibits growth of estrogen-independent human breast cancer cells in culture but not in athymic mice, J. Nutr. 2000, 130, 1665-1669.
37. Shao, Z. M., Wu, J., Shen, Z. Z., Barsky, S. H., Genistein exerts multiple suppressive effects on human breast carcinoma cells, Cancer Res. 1998, 58, 4851-4857.
38. Ueda, M., Niho, N., Imai, T., Shibutani, M., et al., Lack of significant effects of genistein on the progression of 7,12-dimethylbenz(a) anthracene-induced mammary tumors in ovariectomized Sprague-Dawley rats, Nutr. Cancer 2003, 47, 141-147.
39. Allred, C. D., Allred, K. E, Ju, Y. H., Clausen, L. M., et al., Dietary genistein results in larger MNU-induced, estrogen-dependent mammary tumors following ovariectomy of Sprague-Dawley rats, Carcinogenesis 2004, 25, 111-218.
40. Watanabe, S., Yamaguchi, M., Sobue, T., Takahashi, T., et al., Pharmacokinetics of soybean isoflavones in plasma, urine and feces of men after ingestion of 60 g baked soybean powder (kinako), J. Nutr. 1998, 128, 1710-1715.
41. King, R. A., Bursill, D. B., Plasma and urinary kinetics of the isoflavones daidzein and genistein after a single soy meal in humans, Am. J. Clin. Nutr. 1998, 67, 867-872.
42. Setchell, K. D., Brown, N. M., Desai, P. B., Zimmer-Nechimias, L. et al., Evidence for lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability, J. Nutr. 2003, 133, 1027-1035.
43. Petrakis, N. L., Barnes, S., King, E. B., Lowenstein, J., Stimulatory influence of soy protein isolate on breast secretion in pre- and postmenopausal women, Cancer Epidemiol. Biomarkers Prev. 1996, 5, 785-794.
44. McMichael-Phillips, D. F., Harding, C., Morton, M., Roberts, S. A. et al., Effects of soy-protein supplementation on epithelial proliferation in the histologically normal human breast, Am. J. Clin. Nutr. 1998, 68, 1431S-1435S.
45. Hargreaves, D. F., Potten, C. S., Harding, C., Shaw, L. E., Two-week dietary soy supplementation has an estrogenic effect on normal premenopausal breast, J. Clin. Endocrinol. Metab. 1999, 84, 4017-4024.
46. Maskarinec, G., Franke, A. A., Williams, A. E., Hebshi, S., et al., Effects of a 2-year randomized soy intervention on sex hormone levels in premenopausal women, Cancer Epidemiol. Biomarkers Prev. 2004, 13, 1736-1744.
47. Maskarinec, G., Takata, Y., Franke, A., Williams, A., Murphy, S., A 2-year soy intervention in premenopausal women does not change mammographic densities, J. Nutr. 2004, 134, 3089-3094.
48. Sartippour, M. R., Rao, J. Y., Apple, S., Wu, D. et al., A pilot clinical study of short-term isoflavone supplements in breast cancer patients, Nutr. Cancer 2004, 49, 59-65.
49. Chen, J., Hui, E., Ip, T., Thompson, L. U., Dietary flaxseed enhances the inhibitory effect of tamoxifen on the growth of estrogen-dependent human breast cancer (MCF-7) in nude mice, Clin. Cancer Res. 2004, 10, 7703-7711.
50. Chen, J., Power, K. A., Mann, J., Cheng, A., Thompson, L. U., Dietary flaxseed dose dependently inhibits tumor re-growth induced by tamoxifen in nude mice with MCF-7 xenografts by down-regulating the expression of estrogen related genes and signal transduction pathways, Nutr. Cancer, in press.
51. Chen, J., Stavro, P., Thompson, L. U., Dietary flaxseed inhibits human breast cancer growth and metastasis and downregulates expression of insulin-like growth factor and epidermal growth factor receptor, Nutr. Cancer 2002, 43, 187-192.
52. Thompson, L. U., Rickard, S., Orcheson, L., Seidl, M., Flaxseed and its lignan and oil components reduce mammary tumor growth at a late stage of carcinogenesis, Carcinogenesis 1996, 17, 1373-1376.
53. Braden, L. M., Carroll, K. K., Dietary polyunsaturated fat in relation to mammary carcinogenesis in rats, Lipids 1986, 21, 285-288.
54. Abou-el-Ela, S. H., Prasse, K. W., Carroll, R., Wade, A. E., et al., Eicosanoid synthesis in 7,12-dimethylbenz(a)anthracene-induced mammary carcinomas in Sprague-Dawley rats fed primrose oil, menhaden oil or corn oil diet, Lipids 1988, 23, 948-954.
55. Cohen, L. A., Chen-Backlund, J. Y., Sepkovic, D. W., Sugie, S., Effect of varying proportions of dietary menhaden and corn oil on experimental rat mammary tumor promotion, Lipids 1993, 28, 449-456.
56. Wang, L., Chen, J., Thompson, L. U., The inhibitory effect of flaxseed on the growth and metastasis of estrogen receptor negative human breast cancer xenografts is attributed to both its lignan and oil components, Int. J. Cancer 2005, 116, 793-798.
57. Saarinen, N. M., Huovinen, R., Warri, A., Makela, S., Enterolactone inhibits the growth of 7,12 dimethylbenz(a)anthracene-induced mammary carcinomas in the rat, Mol. Cancer Ther. 2002, 10, 869-876.
58. Linseisen, J., Piller, R., Hermann, S., Chang-Claude, J., Dietary phytoestrogen intake and premenopausal breast cancer risk in a German case-control study, Int. J. Cancer 2004, 110, 284-290.
59. Mueller, S. O., Simon, S., Chae, K., Metzler, M., Korach, K. S., Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor alpha (ERalpha) and ERbeta in human cells, Toxicol. Sci. 2004, 80, 14-25.
60. Kuiper, G. G., Lemmen, J. G., Carlsson, B., Corton, J. C., et al., Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta, Endocrinology 1998, 139, 4252-4263.
61. Tsai, M., O'Malley, B., Molecular mechanisms of action of steroid/thyroid receptor superfamily, Annu. Rev. Biochem. 1994, 63, 451-486.
62. Nilsson, S., Gustafsson, J. A., Biological role of estrogen and estrogen receptors, Crit. Rev. Biochem. Mol. Biol. 2002, 37, 1-28.
63. Osborne, C. K., Schiff, R., Estrogen-receptor biology: Continuing progress and therapeutic implications, J. Clin. Oncol. 2005, 23, 1616-1622.
64. Katzenellenbogen, B. S., Katzenellenbogen, J. A., Estrogen receptor transcription and transactivation: Estrogen receptor alpha and estrogen receptor beta: Regulation by selective estrogen receptor modulators and importance in breast cancer, Breast Cancer Res. 2000, 2, 335-344.
65. Ciocca, D., Fanelli, M., Estrogen receptors and cell proliferation in breast cancer, Trends Endocrinol. Metab. 1997, 8, 313-321.
66. Schiff, R., Massarweh, S., Shou, J., Osborne, C. K., Breast cancer endocrine resistance: How growth factor signaling and estrogen receptor coregulators modulate response, Clin. Cancer Res. 2003, 9, 447S-454S.
67. Likhite, V. S., Stossi, F., Kim, K., Katzenellenbogen, B. S., et al., Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity, Mol. Endocrinol. 2006, 20, 3120-3132.
68. Santen, R. J., Song, R. X., McPherson, R., Kumar, R., et al., The role of mitogen-activated protein (MAP) kinase in breast cancer, J. Steroid Biochem. Mol. Biol. 2002, 80, 239-256.
69. Power, K. A., Saarinen, N. M., Chen, J., Thompson, L. U., Flaxseed and soy in human breast cancer: Mechanisms of action, Proceedings of the 61th Flax Institute of the United States, Fargo, North Dakota 2006, pp. 100-105.
70. Nakagawa, H., Yamamoto, D., Kiyozuka, Y., Tsuta, K., et al., Effects of genistein and synergistic action in combination with eicosapentaenoic acid on the growth of breast cancer cell lines, J. Cancer Res. Clin. Oncol. 2000, 126, 448-454.
71. Maubach, J., Depypere, H. T., Goeman, J., Van der Eycken, J., et al., Distribution of soy-derived phytoestrogens in human breast tissue and biological fluids, Obstet. Gynecol. 2004, 103, 892-898.
72. Tham, D. M., Gardner, C. D., Haskell, W. L., Clinical review 97: Potential health benefits of dietary phytoestrogens: A review of the clinical, epidemiological, and mechanistic evidence, J. Clin. Endocrinol. Metab. 1998, 83, 2223-2235.
73. Allred, C. D., Twaddle, N. C., Allred, K. F., Goeppinger, T. S., et al., Soy processing affects metabolism and disposition of dietary isoflavones in ovariectomized BALB/c mice, J. Agric. Food Chem. 2005, 53, 8542-8550.
74. Thompson, L. U., Analysis and bioavailability of lignans, in: Thompson, L. U., Cunanne, S. (Eds.), Flaxseed in Human Nutrition, 2nd edn., AOCS Press, Champaign, Illinois, US 2004, pp. 92-116.
75. Wolf, D. M., Jordan, V. C., Characterization of tamoxifen stimulated MCF-7 tumor variants grown in athymic mice, Breast Cancer Res. Treat. 1994, 31, 117-127.
76. Brodie, A., Jelovac, D., Sabnis, G., Long, B., et al., The intratumoral aromatase model: Studies with aromatase inhibitors and antiestrogens, J. Steroid Biochem. Mol. Biol. 2005, 95, 41-48.
77. Lonning, P. E., Geisler, J., Johannessen, D. C., Ekse, D., Plasma estrogen suppression with aromatase inhibitors evaluated by a novel, sensitive assay for estrone sulphate, J. Steroid Biochem. Mol. Biol. 1997, 61, 255-260.
78. Dowsett, M., Lee, K., Macaulay, V. M., Detre, S., et al., The control and biological importance of intratumoural aromatase in breast cancer, J. Steroid Biochem. Mol. Biol. 1996, 56, 145-150.
79. Power, K. A., Ward, W. E., Chen, J. M., Saarinen, N. M., Thompson, L. U., Genistein alone and in combination with the mammalian lignans, enterolactone and enterodiol, induce estrogenic effects on bone and uterus in a postmenopausal breast cancer mouse model, Bone 2006, 39, 117-124.