Reduced mammary tumor progression in a transgenic mouse model fed an isoflavone-poor soy protein concentrate

Molecular Nutrition and Food Research

Volumn 52, Issue 10, 2008, Pages 1121-1129

  Chiesa, Giulia ^a   Rigamonti, Elena ^a   Lovati, Maria R ^a   Disconzi, Emanuela ^a   Soldati, Sabina ^a,b   Sacco, Maria G ^b   Catò, Enrica Mira ^b   Patton, Veronica ^c   Scanziani, Eugenio ^a   Vezzoni, Paolo ^b,d   Arnoldi, Anna ^a   Locati, Daniela ^a   Sirtori, Cesare R ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b CNR   (Italy)

^c Biology Department   (Italy)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

Breast cancer; Isoflavones; Lung metastasis; Soybean proteins; Transgenic mice

Indexed keywords

ANTINEOPLASTIC AGENT; ISOFLAVONE DERIVATIVE; SOYBEAN PROTEIN;

ANIMAL; ARTICLE; CELL PROLIFERATION; DIET; DIET THERAPY; DISEASE COURSE; EXPERIMENTAL NEOPLASM; FEMALE; MOUSE; TRANSGENIC MOUSE;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL PROLIFERATION; DIET; DISEASE PROGRESSION; FEMALE; ISOFLAVONES; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; SOYBEAN PROTEINS;

ANIMALIA; GLYCINE MAX; MUS; MUS MUSCULUS;

EID: 55449135320     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200700296     Document Type: Article

References (77)

1. Block, G., Patterson, B., Subar, A., Fruit, vegetables, and cancer prevention: A review of the epidemiological evidence, Nutr. Cancer 1992, 18, 1-29.
2. Wattenberg, L. W., Effects of dietary constituents on the metabolism of chemical carcinogens, Cancer Res. 1975, 35, 3326-3331.
3. Johnson, I. T., Williamson, G., Musk, S. R., Anticarcinogenic factors in plant foods: A new class of nutrients? Nutr. Res. Rev. 1994, 7, 175-204.
4. Johnson, I. T., Phytochemicals and cancer, Proc. Nutr. Soc. 2007, 66, 207-215.
5. Tominaga, S., Cancer incidence in Japanese in Japan, Hawaii, and western United States, Natl. Cancer Inst. Monogr. 1985, 69, 83-92.
6. Parkin, D. M., Cancers of the breast, endometrium and ovary: Geographic correlations, Eur. J. Cancer Clin. Oncol. 1989, 25, 1917-1925.
7. Yan, L., Spitznagel, E. L., Meta-analysis of soy food and risk of prostate cancer in men, Int. J. Cancer 2005, 117, 667-669.
8. Wu, A. H., Wan, P., Hankin, J., Tseng, C. C., et al., Adolescent and adult soy intake and risk of breast cancer in Asian-Americans, Carcinogenesis 2002, 23, 1491-1496.
9. Trock, B. J., Hilakivi-Clarke, L., Clarke, R., Meta-analysis of soy intake and breast cancer risk, J. Natl. Cancer Inst. 2006, 98, 459-471.
10. Martinez, M. E., Thomson, C. A., Smith-Warner, S. A., Soy and breast cancer: The controversy continues, J. Natl. Cancer Inst. 2006, 98, 430-431.
11. Potter, S. M., Baum, J. A., Teng, H., Stillman, R. J., et al., Soy protein and isoflavones: Their effects on blood lipids and bone density in postmenopausal women, Am. J. Clin. Nutr. 1998, 68, 1375S-1379S.
12. Phipps, W. R., Duncan, A. M., Kurzer, M. S., Isoflavones and postmenopausalwomen: A critical review, Treat. Endocrinol. 2002, 1, 293-311.
13. Weaver, C. M., Cheong, J. M., Soy isoflavones and bone health: The relationship is still unclear, J. Nutr. 2005, 135, 1243-1247.
14. Sirtori, C. R., Lovati, M. R., Soy proteins and cardiovascular disease, Curr. Atheroscler. Rep. 2001, 3, 47-53.
15. Sacks, F. M., Lichtenstein, A., Van Horn, L., Harris, W., et al., Soy protein, isoflavones, and cardiovascular health: An American Heart Association Science Advisory for professionals from the Nutrition Committee, Circulation 2006, 113, 1034-1044.
16. Sirtori, C. R., Eberini, I., Arnoldi, A., Hypocholesterolaemic effects of soya proteins: Results of recent studies are predictable from the anderson meta-analysis data, Br. J. Nutr. 2007, 97, 816-822.
17. Hawrylewicz, E. J., Zapata, J. J., Blair, W. H., Soy and experimental cancer: Animal studies, J. Nutr. 1995, 125, 698S-708S.
18. Galvez, A. F., Chen, N., Macasieb, J., de Lumen, B. O., Chemopreventive property of a soybean peptide (lunasin) that binds to deacetylated histones and inhibits acetylation, Cancer Res. 2001, 61, 7473-7478.
19. Duncan, A. M., Phipps, W. R., Kurzer, M. S., Phyto-oestrogens, Best Pract. Res. Clin. Endocrinol. Metab. 2003, 17, 253-271.
20. Awad, A. B., Williams, H., Fink, C. S., Phytosterols reduce in vitro metastatic ability of MDA-MB-231 human breast cancer cells, Nutr. Cancer 2001, 40, 157-164.
21. Rao, A. V., Sung, M. K., Saponins as anticarcinogens, J. Nutr. 1995, 125, 717S-724S.
22. Zhou, J. R., Erdman, J. W., Jr., Phytic acid in health and disease, Crit. Rev. Food Sci. Nutr. 1995, 35, 495-508.
23. Hu, J., Reddy, M. B., Hendrich, S., Murphy, P. A., Soyasaponin I and sapongenol B have limited absorption by Caco-2 intestinal cells and limited bioavailability in women, J. Nutr. 2004, 134, 1867-1873.
24. Ling, W. H., Jones, P. J., Dietary phytosterols: A review of metabolism, benefits and side effects, Life Sci. 1995, 57, 195-206.
25. Inagaki, K., Kobayashi, H., Yoshida, R., Kanada, Y., et al., Suppression of urokinase expression and invasion by a soybean Kunitz trypsin inhibitor are mediated through inhibition of Src-dependent signaling pathways, J. Biol. Chem. 2005, 280, 31428-31437.
26. Kennedy, A. R., The Bowman-Birk inhibitor from soybeans as an anticarcinogenic agent, Am. J. Clin. Nutr. 1998, 68, 1406S-1412S.
27. Onishi, K., Matoba, N., Yamada, Y., Doyama, N., et al., Optimal designing of beta-conglycinin to genetically incorporate RPLKPW, a potent anti-hypertensive peptide, Peptides 2004, 25, 37-43.
28. Maruyama, N., Maruyama, Y., Tsuruki, T., Okuda, E., et al., Creation of soybean beta-conglycinin beta with strong phagocytosis-stimulating activity, Biochim. Biophys. Acta 2003, 1648, 99-104.
29. Gonzalez de Mejia, E., Vasconez, M., de Lumen, B. O., Nelson, R., Lunasin concentration in different soybean genotypes, commercial soy protein, and isoflavone products, J. Agric. Food Chem. 2004, 52, 5882-5887.
30. Gallo, D., Giacomelli, S., Cantelmo, F., Zannoni, G. F., et al., Chemoprevention of DMBA-induced mammary cancer in rats by dietary soy, Breast Cancer Res. Treat. 2001, 69, 153-164.
31. Moore, A. B., Castro, L., Yu, L., Zheng, X., et al., Stimulatory and inhibitory effects of genistein on human uterine leiomyoma cell proliferation are influenced by the concentration, Hum. Reprod. 2007, 22, 2623-2631.
32. Limer, J. L., Speirs, V., Phyto-oestrogens and breast cancer chemoprevention, Breast Cancer Res. 2004, 6, 119-127.
33. Galvez, A. F., de Lumen, B. O., A soybean cDNA encoding a chromatin-binding peptide inhibits mitosis of mammalian cells, Nat. Biotechnol. 1999, 17, 495-500.
34. Lucchini, F., Sacco, M. G., Hu, N., Villa, A., et al., Early and multifocal tumors in breast, salivary, harderian and epididymal tissues developed in MMTY-Neu transgenic mice, Cancer Lett. 1992, 64, 203-209.
35. Sacco, M. G., Soldati, S., Mira Cato, E., Cattaneo, L., et al., Combined effects on tumor growth and metastasis by antiestrogenic and antiangiogenic therapies in MMTV-neu mice, Gene Ther. 2002, 9, 1338-1341.
36. Sacco, M. G., Mangiarini, L., Villa, A., Macchi, P., et al., Local regression of breast tumors following intramammary ganciclovir administration in double transgenic mice expressing neu oncogene and herpes simplex virus thymidine kinase, Gene Ther. 1995, 2, 493-497.
37. Sacco, M. G., Benedetti, S., Duflot-Dancer, A., Mesnil, M., et al., Partial regression, yet incomplete eradication of mammary tumors in transgenic mice by retrovirally mediated HSVtk transfer 'in vivo', Gene Ther. 1996, 3, 1151-1156.
38. Sacco, M. G., Barbieri, O., Piccini, D., Noviello, E., et al., In vitro and in vivo antisense-mediated growth inhibition of a mammary adenocarcinoma from MMTV-neu transgenic mice, Gene Ther. 1998, 5, 388-393.
39. Sacco, M. G., Caniatti, M., Catò, E. M., Frattini, A., et al., Liposome-delivered angiostatin strongly inhibits tumor growth and metastatization in a transgenic model of spontaneous breast cancer, Cancer Res. 2000, 60, 2660-2665.
40. Sacco, M. G., Gribaldo, L., Barbieri, O., Turchi, G., et al., Establishment and characterization of a new mammary adenocarcinoma cell line derived from MMTV neu transgenic mice, Breast Cancer Res. Treat. 1998, 47, 171-180.
41. Sacco, M. G., Soldati, S., Indraccolo, S., Cato, E. M., et al., Combined antiestrogen, antiangiogenic and anti-invasion therapy inhibits primary and metastatic tumor growth in the MMTVneu model of breast cancer, Gene Ther. 2003, 10, 1903-1909.
42. Siegel, P. M., Shu, W., Cardiff, R. D., Muller, W. J., Massague, J., Transforming growth factor beta signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis, Proc. Natl. Acad. Sci. USA 2003, 100, 8430-5.
43. Lovati, M. R., Manzoni, C., Canavesi, A., Sirtori, M., et al., Soybean protein diet increases low density lipoprotein receptor activity in mononuclear cells from hypercholesterolemic patients, J. Clin. Invest. 1987, 80, 1498-1502.
44. Sirtori, C. R., Gianazza, E., Manzoni, C., Lovati, M. R., Murphy, P. A., Role of isoflavones in the cholesterol reduction by soy proteins in the clinic, Am. J. Clin. Nutr. 1997, 65, 166-167.
45. Gianazza, E., Eberini, I., Arnoldi, A., Wait, R., Sirtori, C. R., A proteomic investigation of isolated soy proteins with variable effects in experimental and clinical studies, J. Nutr. 2003, 133, 9-14.
46. Morandi, S., Locati, D., Ferrario, F., Chiesa, G., Arnoldi, A., A simple method for the characterization and quantification of soy isoflavone metabolites in the serum of MMTV-Neu mice using high-performance liquid chromatography/electrospray ionization mass spectrometry with multiple reaction monitoring, Rapid Commun. Mass Spectrom. 2005, 19, 153-161.
47. Cardiff, R. D., Anver, M. R., Gusterson, B. A., Hennighausen, L. et al., The mammary pathology of genetically engineered mice: The consensus report and recommendations from the Annapolis meeting, Oncogene 2000, 19, 968-988.
48. deFazio, A., Leary, J. A., Hedley, D. W., Tattersall, M. H., Immunohistochemical detection of proliferating cells in vivo, J. Histochem. Cytochem. 1987, 35, 571-577.
49. Hendrich, S., Bioavailability of isoflavones, J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2002, 777, 203-10.
50. Clarke, C. A., Glaser, S. L., Declines in breast cancer after the WHI: Apparent impact of hormone therapy, Cancer Causes Control. 2007, 18, 847-852.
51. Uray, I. P., Brown, P. H., Prevention of breast cancer: Current state of the science and future opportunities, Expert Opin. Investig. Drugs 2006, 15, 1583-1600.
52. Dumitrescu, R. G., Cotarla, I., Understanding breast cancer risk - where do we stand in 2005? J. Cell. Mol. Med. 2005, 9, 208-221.
53. Wilson, J. L., Burchell, J., Grimshaw, M. J., Endothelins induce CCR7 expression by breast tumor cells via endothelin receptor A and hypoxia-inducible factor-1, Cancer Res. 2006, 66, 11802-11807.
54. Warri, A. M., Saarinen, N. M., Makela, S. I., Can modulation of mammary gland development by dietary factors support breast cancer prevention? Horm. Res. 2007, 68, 248-260.
55. Sirtori, C. R., Anderson, J. W., Arnoldi, A., Nutritional and nutraceutical considerations for dyslipidemia, Future Lipidol. 2007, 2, 313-339.
56. 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.
57. 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.
58. Magee, P. J., Rowland, I. R., Phyto-oestrogens, their mechanism of action: Current evidence for a role in breast and prostate cancer, Br. J. Nutr. 2004, 91, 513-531.
59. 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.
60. Kulling, S. E., Metzler, M., Induction of micronuclei, DNA strand breaks and HPRT mutations in cultured Chinese hamster V79 cells by the phytoestrogen coumoestrol, Food Chem. Toxicol. 1997, 35, 605-613.
61. Liggins, J., Bluck, L. J., Runswick, S., Atkinson, C., et al., Daidzein and genistein contents of vegetables, Br. J. Nutr. 2000, 84, 717-725.
62. Sirtori, C. R., Lovati, M. R., Manzoni, C., Castiglioni, S., et al., Proteins of white lupin seed, a naturally isoflavone-poor legume, reduce cholesterolemia in rats and increase LDL receptor activity in HepG2 cells, J. Nutr. 2004, 134, 18-23.
63. Sills, R. C., French, J. E., Cunningham, M. L., New models for assessing carcinogenesis: An ongoing process, Toxicol. Lett. 2001, 120, 187-198.
64. Fritz, P., Cabrera, C. M., Dippon, J., Gerteis, A., et al., cerbB2 and topoisomerase IIalpha protein expression independently predict poor survival in primary human breast cancer: A retrospective study, Breast Cancer Res. 2005, 7, R374-R384.
65. Fontana, L., Klein, S., Aging, adiposity, and calorie restriction, JAMA 2007, 297, 986-994.
66. Allred, C. D., Allred, K. F., Ju, Y. H., 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.
67. Lamartiniere, C. A., Moore, J. B., Brown, N. M., Thompson, R. et al., Genistein suppresses mammary cancer in rats, Carcinogenesis 1995, 16, 2833-2840.
68. Fritz, W. A., Coward, L., Wang, J., Lamartiniere, C. A., Dietary genistein: Perinatal mammary cancer prevention, bioavailability and toxicity testing in the rat, Carcinogenesis 1998, 19, 2151-2158.
69. Lamartiniere, C. A., Protection against breast cancer with genistein: A component of soy, Am. J. Clin. Nutr. 2000, 71, 1705S-1707S; discussion 1708S-1709S.
70. Lamartiniere, C. A., Cotroneo, M. S., Fritz, W. A., Wang, J., et al., Genistein chemoprevention: Timing and mechanisms of action in murine mammary and prostate, J. Nutr. 2002, 132, 552S-558S.
71. Lamartiniere, C. A., Timing of exposure and mammary cancer risk, J. Mammary Gland Biol. Neoplasia 2002, 7, 67-76.
72. Yamamoto, S., Sobue, T., Sasaki, S., Kobayashi, M. et al., Validity and reproducibility of a self-administered food-frequency questionnaire to assess isoflavone intake in a japanese population in comparison with dietary records and blood and urine isoflavones, J. Nutr. 2001, 131, 2741-2747.
73. Mordenti, J., Man versus beast: Pharmacokinetic scaling in mammals, J. Pharm. Sci. 1986, 75, 1028-1040.
74. Yellayi, S., Naaz, A., Szewczykowski, M. A., Sato, T., et al., The phytoestrogen genistein induces thymic and immune changes: A human health concern?, Proc. Natl. Acad. Sci. USA 2002, 99, 7616-7621.
75. Wen, X. F., Yang, G., Mao, W., Thornton, A., et al., HER2 signaling modulates the equilibrium between pro- and antiangiogenic factors via distinct pathways: Implications for HER2-targeted antibody therapy, Oncogene 2006, 25, 6986-6996.
76. Le, X. F., Pruefer, F., Bast, R. C., Jr., HER2-targeting antibodies modulate the cyclin-dependent kinase inhibitor p27Kip1 via multiple signaling pathways, Cell Cycle 2005, 4, 87-95.
77. Alamian, A., Rouleau, I., Simard, J., Dorval, M., Use of dietary supplements among women at high risk of hereditary breast and ovarian cancer (HBOC) tested for cancer susceptibility, Nutr. Cancer 2006, 54, 157-165.