Influence of Prevastein®, an isoflavone-rich soy product, on mammary gland development and tumorigenesis in Tg.NK (MMTV/c-neu) mice

Nutrition and Cancer

Volumn 52, Issue 2, 2005, Pages 176-188

  Thomsen, Anni R ^a   Mortensen, Alicja ^a   Breinholt, Vibeke M ^b   Lindecrona, Rikke H ^a   Peñalvo, José L ^c   Sørensen, Ilona K ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b Maxygen APS   (Denmark)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYRESORUFIN O DEETHYLASE; CYTOCHROME P450; DAIDZEIN; ENZYME; ETHOXYRESORUFIN DEETHYLASE; GENISTEIN; GLUTATHIONE PEROXIDASE; GLYCITEIN; ISOFLAVONE DERIVATIVE; METHOXYRESORUFIN O DEETHYLASE; PENTOXYRESORUFIN O DEETHYLASE; UNCLASSIFIED DRUG; CYCLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CARCINOGENESIS; BREAST DEVELOPMENT; BREAST EPITHELIUM; CANCER GROWTH; CELL COUNT; CELL DIVISION; CONTROLLED STUDY; ENZYME ACTIVITY; EXPOSURE; FEMALE; MOUSE; MOUSE STRAIN; NONHUMAN; SOYBEAN; TUMOR VOLUME; ANIMAL; BLOOD; CHEMISTRY; DOSE RESPONSE; DRUG EFFECT; EXPERIMENTAL NEOPLASM; FEEDING BEHAVIOR; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; RANDOMIZATION; TRANSGENIC MOUSE; UDDER;

ANIMALIA; GLYCINE MAX;

ANIMALS; APOPTOSIS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FOOD HABITS; IMMUNOHISTOCHEMISTRY; ISOFLAVONES; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; PROLIFERATING CELL NUCLEAR ANTIGEN; RANDOM ALLOCATION; SOYBEANS;

EID: 27644442443     PISSN: 01635581     EISSN: None     Source Type: Journal    
DOI: 10.1207/s15327914nc5202_8     Document Type: Article

References (67)

1. Parkin DM and Muir CS: Cancer incidence in five continents. Comparability and quality of data. IARC Sci Publ 120, 45-173, 1992.
2. Lee HP, Gourley L, Duffy SW, Esteve J, Lee J, et al.: Dietary effects on breast-cancer risk in Singapore. Lancer 337, 1197-1200, 1991.
3. Wu AH, Stanczyk FZ, Seow A, Lee HP, and Yu MC: Soy intake and other lifestyle determinants of serum estrogen levels among postmenopausal Chinese women in Singapore. Cancer Epidemiol Biomarkers Prev 9, 844-851, 2002.
4. Horn-Ross PL, John EM, Lee M, Stewart SL, Koo J, et al.: Phytoestrogen consumption and breast cancer risk in a multiethnic population: the Bay Area Breast Cancer Study. Am J Epidemiol 154, 434-441, 2001.
5. Setchell KD, Borriello SP, Hulme P, Kirk DN, and Axelson M: Nonsteroidal estrogens of dietary origin: possible roles in hormone-dependent disease. Am J Clin Nutr 40, 569-578, 1984.
6. Yamamoto S, Sobue T, Kobayashi M, Sasaki S, and Tsugane S: Soy isoflavones and breast cancer risk in Japan. J Natl Cancer Inst 18, 906-913, 2003.
7. Ziegler RG, Hoover RN, Pike MC, Hildesheim A, Nomura AM, et al.: Migration patterns and breast cancer risk in Asian-American women. J Natl Cancer Inst 85, 1819-1827, 1993.
8. Martin PM, Horwitz KB, Ryan DS, and Mcguire W: Phytoestrogen interaction with estrogen receptors in human breat cancer eel Is. Endocrinology 103, 1860-1867, 1978.
9. Sathyamoorthy N, Wang TTY, and Pang JM: Stimulation of pS2 expression by diet-derived compounds. Cancer Res 54, 961, 1994.
10. Santell RC, Chang YC, Nair MG, and Helferich WG: Dietary genistein exerts estrogenic effects upon the uterus, mammary gland and hypothalamic/pituitary axis in rats. J Nutr 127, 263-269, 1997.
11. Hsieh CY, Santell RC, Haslam SZ, and Helferich WG: Estrogenic effects of genistein on the growth of estrogen receptor positive human breast cancer (MCF-7) cells in vitro and in vivo. Cancer Res 58, 3833-3838, 1998.
12. Cheng E, Story CD, Yoder L, Hale WH, and Burroughs W: Estrogenic activity of isoflavone derivatives extracted and prepared from soybean oil meal. Science 188, 164-165, 1980.
13. Peterson TG, Coward L, Kirk M, Falany CN, and Barnes S: The role of metabolism in mammary epithelial cell growth inhibition by the isoflavones genistein and biochanin A. Carcinogenesis 17, 1861-1869, 1996.
14. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, et al.: Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262, 5592-5595, 1987.
15. Kaufmann WK: Human topoisomerase Il function, tyrosine phosphorylation and cell cycle checkpoints. Proc Soc Exp Biol Med 217, 327-334, 1998.
16. Fotsis T, Pepper M, Adlercreutz HO, Fleischmann G, Hase T, et al.: Genistein, a dietary-derived inhibitor of in vitro angiogenesis. Proc Natl Acad Sci U S A 90, 2690-2694, 1993.
17. Santibanez JF, Navarro A, and Martinez J: Genistein inhibits proliferation and in vitro invasive potential of human prostatic cancer cell lines Anticancer Res 17, 1199-1204, 1997.
18. Dai Q, Shu XO, Jin F, Potter JD, Kushi LH, et al.: Population-based case-control study of soyfood intake and breast cancer risk in Shanghai. Br J Cancer 85, 372-378, 2001.
19. Shu XO, Jin F, Dai Q, Wen W, Potter JD, et al.: Soyfood intake during adolescence and subsequent risk of breast cancer among Chinese women. Cancer Epidemiol Biomarkers Prev 10, 483-488, 2001.
20. Wu AH, Wan P, Hankin J, Tseng CC, Yu MC, et al.: Adolescent and adult soy intake and risk of breast cancer in Asian-Americans. Carcinogenesis 23, 1491-1496, 2002.
21. Lamartiniere CA, Murrill WB, Manzolillo PA, Zhang JX, Barnes S, et al.: Genistein alters the ontogeny of mammary gland development and protects against chemically-induced mammary cancer in rats. Proc Soc Exp Biol Med 217, 358-364, 1998.
22. Lamartiniere CA: Protection against breast cancer with genistein: a component of soy. Am J Clin Nutr 71, 1705S-1707S, 2001.
23. Hilakivi-Clarke L, Cho E, and Clarke R: Maternal genistein exposure mimics the effects of estrogen on mammary gland development in female mouse offspring. Oncol Rep 5, 609-616, 1998.
24. Hilakivi-Clarke L, Cho E, Onojafe I, Raygada M, and Clarke R: Maternal exposure to genistein during pregnancy increases carcinogen-induced mammary tumorigenesis in female rat offspring. Oncol Rep 6, 1089-1095, 1999.
25. Coward L, Wang J, and Lamartiniere CA: Dietary genistein: perinatal mammary cancer prevention, bioavailability and toxicity testing in the rat. Carcinogenesis 19, 2151-2158, 2001.
26. Fielden MR, Samy SM, Chou KC, and Zacharewski TR: Effect of human dietary exposure levels of genistein during gestation and lactation on long-term reproductive development and sperm quality in mice. Food Chem Toxicol 41, 447-454, 2003.
27. Lamartiniere CA, Cotroneo MS, Fritz WA, Wang J, Mentor-Marcel R, et al.: Genistein chemoprevention: timing and mechanisms of action in murine mammary and prostate. J Nutr 132, 552S-558S, 2002.
28. Day JK, Besch-Williford C, McMann TR, Hufford MG, Lubahn DB, et al.: Dietary genistein increased DMBA-induced mammary adenocarcinoma in wild-type, but not ER alpha KO, mice. Nutr Cancer 39, 226-232, 2001.
29. Hilakivi-Clarke L, Cho E, DeAssis S, Olivo S, Ealley E, et al.: Maternal and prepubertal diet, mammary development and breast cancer risk. J Nutr 131, 154S-157S, 2001.
30. Barnes S: The chemopreventive properties of soy isoflavonoids in animal models of breast cancer. Breast Cancer Res Treat 46, 169-179, 1997.
31. Muller WJ, Sinn E, Pattengale PK, Wallace R, and Leder P: Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54, 105-115, 1988.
32. Sorensen IK, Kristiansen E, Mortensen A, Nicolaisen GM, Wijnands JA, et al.: The effect of soy isoflavones on the development of intestinal neoplasia in ApcMin mouse. Cancer Lett 130, 217-225, 1998.
33. van Kranen HJ, van Iersel PW, Rijnkels JM, Beems DB, Alink GM, et al.: Effects of dietary fat and a vegetable-fruit mixture on the development of intestinal neoplasia in the ApcMin mouse. Carcinogenesis 9, 1597-1601, 1998.
34. Rao GN, Ney E, and Herbert RA: Influence of diet on mammary cancer in transgenic mice bearing an oncogene expressed in mammary tissue. Breast Cancer Res 45, 149-158, 1997.
35. Rugh, R. The Mouse and Its Reproduction and Development. Oxford, England: Oxford University Press, 1990.
36. Nurmi T, Mazur W, Heinonen S, Kokkonen J, and Adlercreutz H: Isoflavone content of the soy-based supplements. J Pharm Biomed Anal 28, 1-11, 2002.
37. Penalvo JL, Nurmi T, and Adlercreutz HA: Simplified HPLC method for total isoflavones in soy products. Food Chem 87, 297-305, 2004.
38. Wang GJ, Lapcik O, Hampl R, Uehara M, Al-Maharik N, et al.: Time-resolved fluoroimmunoassay of plasma daidzein and genistein. Steroids 65, 339-348, 2000.
39. Wiseman BS, Sternlicht MD, Lund LR, Alexander CM, Mott J, et al.: Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. J Cell Biol 162, 1123-1133, 2003.
40. Russo IH and Russo J: Developmental stage of the rat mammary gland as determinant of its susceptibility to 7,12-dimethylbenzaanthracene. J Natl Cancer Inst 61, 1439-1449, 1978.
41. Ausubel FM, Brent R, Kingston RE, Moore DD, Sidman JG, et al.: Current Protocols in Molecular Biology. New York: Wiley, 1994.
42. Staley K, Blaschke AJ, and Chun J: Apoptotic DNA fragmentation is detected by a semiquantitative ligation-mediated PCR of blunt DNA ends. Cell Death Differ 4, 66-75, 1997.
43. Dalgaard M, Nellemann C, Lam HR, Sorensen IK, and Ladefoged O: The acute effects of mono(2-ethylhexyl)phthalate (MEHP) on testes of prepubertal Wistar rats. Toxicol Lett 122, 69-79, 2001.
44. Lake BG: Preparation and characterization of microsomal fractions for studies on xenobiotic metabolism. In Biochemical Toxicology: A Practical Approach, Snell K and Mullock B (eds.). Oxford, England: IRL Press, 1987, pp 183-215.
45. Burke MD, Thompson S, Weaver RJ, Wolf CR, and Mayer RT: Cytochrome P450 specificities of alkoxyresorufin O-dealkylation in human and rat liver. Biochem Pharmacol 48, 923-936, 1994.
46. Breinholt V, Lauridsen ST, and Dragsted LO: Differential effects of dietary flavonoids on drug metabolizing and antioxidant enzymes in female rat. Xenobiotica 29, 1227-1240, 1999.
47. Ernster L: DT-diaphorase. Methods Enzymol 10, 309-317, 1967.
48. Habig WH, Pabst MJ, and Jakoby WB: Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249, 7140-7147, 1974.
49. Breinholt V, Lauridsen ST, Daneshvar B, and Jakobsen J: Dose-response effects of lycopene on selected drug-metabolizing and antioxidant enzymes in the rat. Cancer Lett 30, 2001-210, 2000.
50. Uehara M, Arai Y, Watanabe S, and Adlercreutz H: Comparison of plasma and urinary phytoestrogens in Japanese and Finnish women by time-resolved fluoroimmunoassay. Biofactors 12, 217-225, 2000.
51. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, et al.: Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244, 707-712, 1989.
52. Lamartiniere CA, Moore J, Holland M, and Barnes S: Neonatal genistein chemoprevents mammary cancer. Proc Soc Exp Biol Med 208, 120-123, 1995.
53. Constantinou AI, Lantvit D, Hawthorne M, Xu X, van Breemen RB, et al.: Chemopreventive effects of soy protein and purified soy isoflavones on DMBA-induced mammary tumors in female Sprague-Dawley rats. Nutr Cancer 41, 75-81, 2001.
54. Murrill WB, Brown NM, Zhang JX, Manzolillo PA, Barnes S, et al.: Prepubertal genistein exposure suppresses mammary cancer and enhances gland differentiation in rats. Carcinogenesis 17, 1451-1457, 1996.
55. Lamartiniere CA: Timing of exposure and mammary cancer risk. J Mammary Gland Biol Neoplasia 7, 67-76, 2002.
56. Humphreys RC, Krajewska M, Krnacik S, Jæger R, Weiher H, et al.: Apoptosis in the terminal endbuds of the murine mammary gland; a mechanism of ductal morphogenesis. Development 122, 4013-4022, 1996.
57. Jin Z and MacDonald RS: Soy isoflavones increase latency of spontaneous mammary tumors in mice. J Nutr 132, 3186-3190, 2002.
58. Luijten M, Thomsen AR, van den Berg JA, Wester PW, Yerhoef A, et al.: Effect of soy-derived isoflavones and a high-fat diet on spontaneous mammary tumor development in Tg.NK (MMTV/c-neu) mice. Nutr Cancer 50, 46-54, 2004.
59. Ju YH, Allred CD, Allred KF, Karko KL, Doerge DR, 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 131, 2957-2962, 2001.
60. Allred CD, Allred KF, Ju YH, Goeppinger TS, Doerge DR, et al.: Soy processing influences growth of estrogen-dependent breast cancer tumors in mice. Carcinogenesis 25, 1649-1667, 2004.
61. Key T: Risk factors for prostate cancer. Cancer Surv 23, 63-77, 1995.
62. Lipworth L: Epidemiology of breast cancer. Eur J Cancer Prev 4, 7-30, 1995.
63. Slattery ML, Potter JD, Duncan DM, and Berry TD: Dietary fats and colon cancer: assessment of risk associated with specific fatty acids. Int J Cancer 73, 670-677, 1997.
64. Helsby NA, Chipman JK, Gescher A, and Kerr D: Inhibition of mouse and human CYP 1A- and 2E1-dependent substrate metabolism by the isoflavonoids genistein and equol. Food Chem Toxicol 36, 375-382, 1998.
65. Helsby NA, Williams J, Kerr D, Gescher A, and Chipman JK: The isoflavones equol and genistein do not induce xenobiotic-metabolizing enzymes in mouse and in human cells. Xenobiotica 27, 587-596, 1997.
66. el Demerdash FM, Yousef MI, and Al Salhen KS: Protective effects of isoflavone on some biochemical parameters affected by cypermethrin in male rabbits. J Environ Sci Health B 38, 365-378, 2003.
67. Cai Q and Wei H: Effect of dietary genistein on antioxidant enzyme activities in SENCAR mice. Nutr Cancer 25, 1-7, 1996.