High levels of dietary soy decrease mammary tumor latency and increase incidence in MTB-IGFIR transgenic mice

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Watson, Katrina L ^a   Stalker, Leanne ^a   Jones, Robert A ^a   Moorehead, Roger A ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Amphiregulin; Breast cancer; IGF IR; Metaplastic breast cancer; Metastasis; Soy; Tumor initiation; Tumor progression

Indexed keywords

AMPHIREGULIN; CASEIN; CYTOKERATIN 5; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; PROGESTERONE RECEPTOR; PROTEIN P63; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR ALPHA; BIOLOGICAL MARKER; SOMATOMEDIN C RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AREG GENE; ARTICLE; BREAST CANCER; CANCER INCIDENCE; CELL PROLIFERATION; CONTROLLED STUDY; DIETARY INTAKE; GROWTH INHIBITION; GROWTH RATE; IGF IR GENE; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; MOUSE; NONHUMAN; ONCOGENE; PGR GENE; SOYBEAN; TRANSGENE; TUMOR GROWTH; ANIMAL; ANIMAL FOOD; CELL TRANSFORMATION; FEMALE; GENE EXPRESSION; GENETICS; HUMAN; MAMMARY NEOPLASMS, ANIMAL; METABOLISM; METASTASIS; MORTALITY; PATHOLOGY; SIGNAL TRANSDUCTION; SOY FOOD; TRANSGENIC MOUSE; TUMOR VOLUME;

ANIMAL FEED; ANIMALS; BIOMARKERS; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE EXPRESSION; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, TRANSGENIC; NEOPLASM METASTASIS; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; SOY FOODS; TUMOR BURDEN;

EID: 84924057880     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1037-z     Document Type: Article

References (77)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69-90.
2. Wu AH, Ziegler RG, Nomura AM, West DW, Kolonel LN, Horn-Ross PL, et al. Soy intake and risk of breast cancer in Asians and Asian Americans. Am J Clin Nutr. 1998;68(6 Suppl):1437S-43S.
3. Messina M, Barnes S. The role of soy products in reducing risk of cancer. J Natl Cancer Inst. 1991;83(8):541-6.
4. Mourouti N, Panagiotakos DB. Soy food consumption and breast cancer. Maturitas. 2013;76(2):118-22.
5. Messina M, McCaskill-Stevens W, Lampe JW. Addressing the soy and breast cancer relationship: review, commentary, and workshop proceedings. J Natl Cancer Inst. 2006;98(18):1275-84.
6. An J, Tzagarakis-Foster C, Scharschmidt TC, Lomri N, Leitman DC. Estrogen receptor beta-selective transcriptional activity and recruitment of coregulators by phytoestrogens. J Biol Chem. 2001;276(21):17808-14.
7. Margeat E, Bourdoncle A, Margueron R, Poujol N, Cavailles V, Royer C. Ligands differentially modulate the protein interactions of the human estrogen receptors alpha and beta. J Mol Biol. 2003;326(1):77-92.
8. Kostelac D, Rechkemmer G, Briviba K. Phytoestrogens modulate binding response of estrogen receptors alpha and beta to the estrogen response element. J Agric Food Chem. 2003;51(26):7632-5.
9. Douglas CC, Johnson SA, Arjmandi BH. Soy and its isoflavones: the truth behind the science in breast cancer. Anticancer Agents Med Chem. 2013;13(8):1178-87.
10. Chen M, Rao Y, Zheng Y, Wei S, Li Y, Guo T, et al. Association between soy isoflavone intake and breast cancer risk for pre- and post-menopausal women: a meta-analysis of epidemiological studies. PloS One. 2014;9(2):e89288.
11. Trock BJ, Hilakivi-Clarke L, Clarke R. Meta-analysis of soy intake and breast cancer risk. J Natl Cancer Inst. 2006;98(7):459-71.
12. Lee SA, Shu XO, Li H, Yang G, Cai H, Wen W, et al. Adolescent and adult soy food intake and breast cancer risk: results from the Shanghai Women's Health Study. Am J Clin Nutr. 2009;89(6):1920-6.
13. Fritz H, Seely D, Flower G, Skidmore B, Fernandes R, Vadeboncoeur S, et al. Soy, red clover, and isoflavones and breast cancer: a systematic review. PloS one. 2013;8(11):e81968.
14. Wu AH, Yu MC, Tseng CC, Pike MC. Epidemiology of soy exposures and breast cancer risk. Br J Cancer. 2008;98(1):9-14.
15. Grace PB, Taylor JI, Low YL, Luben RN, Mulligan AA, Botting NP, 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(5):698-708.
16. Shike M, Doane AS, Russo L, Cabal R, Reis-Filo J, Gerald W, et al. The effects of soy supplementation on gene expression in breast cancer: a randomized placebo-controlled study. J Natl Cancer Inst. 2014;106(9):dju189 doi:10.1093/jnci/dju189.
17. Fritz WA, Coward L, Wang J, Lamartiniere CA. Dietary genistein: perinatal mammary cancer prevention, bioavailability and toxicity testing in the rat. Carcinogenesis. 1998;19(12):2151-8.
18. Hilakivi-Clarke L, Onojafe I, Raygada M, Cho E, Skaar T, Russo I, et al. Prepubertal exposure to zearalenone or genistein reduces mammary tumorigenesis. Br J Cancer. 1999;80(11):1682-8.
19. Mukhopadhyay S, Ballard BR, Mukherjee S, Kabir SM, Das SK. Beneficial effects of soy protein in the initiation and progression against dimethylbenz [a] anthracene-induced breast tumors in female rats. Mol Cell Biochem. 2006;290(1-2):169-76.
20. Constantinou AI, Lantvit D, Hawthorne M, Xu X, van Breemen RB, Pezzuto JM. Chemopreventive effects of soy protein and purified soy isoflavones on DMBA-induced mammary tumors in female Sprague-Dawley rats. Nutr Cancer. 2001;41(1-2):75-81.
21. Gallo D, Giacomelli S, Cantelmo F, Zannoni GF, Ferrandina G, Fruscella E, et al. Chemoprevention of DMBA-induced mammary cancer in rats by dietary soy. Breast Cancer Res Treat. 2001;69(2):153-64.
22. Murrill WB, Brown NM, Zhang JX, Manzolillo PA, Barnes S, Lamartiniere CA. Prepubertal genistein exposure suppresses mammary cancer and enhances gland differentiation in rats. Carcinogenesis. 1996;17(7):1451-7.
23. Hakkak R, Shaaf S, Jo CH, Macleod S, Korourian S. Effects of high-isoflavone soy diet vs. casein protein diet and obesity on DMBA-induced mammary tumor development. Oncol Lett. 2011;2(1):29-36.
24. Qin LQ, Xu JY, Tezuka H, Wang PY, Hoshi K. Commercial soy milk enhances the development of 7,12-dimethylbenz(a)anthracene-induced mammary tumors in rats. In Vivo. 2007;21(4):667-71.
25. Lamartiniere CA, Wang J, Smith-Johnson M, Eltoum IE. Daidzein: bioavailability, potential for reproductive toxicity, and breast cancer chemoprevention in female rats. Toxicol Sci. 2002;65(2):228-38.
26. Rahal OM, Machado HL, Montales MT, Pabona JM, Heard ME, Nagarajan S, et al. Dietary suppression of the mammary CD29(hi)CD24(+) epithelial subpopulation and its cytokine/chemokine transcriptional signatures modifies mammary tumor risk in MMTV-Wnt1 transgenic mice. Stem Cell Res. 2013;11(3):1149-62.
27. Zhang GP, Han D, Liu G, Gao SG, Cai XQ, Duan RH, et al. Effects of soy isoflavone and endogenous oestrogen on breast cancer in MMTV-erbB2 transgenic mice. J Int Med Res. 2012;40(6):2073-82.
28. Davis VL, Shaikh F, Gallagher KM, Villegas M, Rea SL, Cline JM, et al. Inhibition of Neu-induced mammary carcinogenesis in transgenic mice expressing ERDelta3, a dominant negative estrogen receptor alpha variant. Horm Cancer. 2012;3(5-6):227-39.
29. Korde LA, Wu AH, Fears T, Nomura AM, West DW, Kolonel LN, et al. Childhood soy intake and breast cancer risk in Asian American women. Cancer Epidemiol Biomarkers Prev. 2009;18(4):1050-9.
30. Brown NM, Belles CA, Lindley SL, Zimmer-Nechemias L, Witte DP, Kim MO, et al. Mammary gland differentiation by early life exposure to enantiomers of the soy isoflavone metabolite equol. Food Chem Toxicol. 2010;48(11):3042-50.
31. Mehrara E, Forssell-Aronsson E, Ahlman H, Bernhardt P. Specific growth rate versus doubling time for quantitative characterization of tumor growth rate. Cancer Res. 2007;67(8):3970-5.
32. Lynch HT, Snyder C, Casey MJ. Hereditary ovarian and breast cancer: what have we learned? Ann Oncol. 2013;24 Suppl 8:viii83-95.
33. Watson KL, Moorehead RA. Loss of Akt1 or Akt2 delays mammary tumor onset and suppresses tumor growth rate in MTB-IGFIR transgenic mice. BMC cancer. 2013;13:375.
34. Jones RA, Campbell CI, Gunther EJ, Chodosh LA, Petrik JJ, Khokha R, et al. Transgenic overexpression of IGF-IR disrupts mammary ductal morphogenesis and induces tumor formation. Oncogene. 2007;26(11):1636-44.
35. Jones RA, Campbell CI, Petrik JJ, Moorehead RA. Characterization of a novel primary mammary tumor cell line reveals that cyclin D1 is regulated by the type I insulin-like growth factor receptor. Mol Cancer Res. 2008;6(5):819-28.
36. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):RESEARCH0034.
37. Jones RA, Campbell CI, Wood GA, Petrik JJ, Moorehead RA. Reversibility and recurrence of IGF-IR-induced mammary tumors. Oncogene. 2009;13:407-13.
38. MacLennan MB, Anderson BM, Ma DW. Differential mammary gland development in FVB and C57Bl/6 mice: implications for breast cancer research. Nutrients. 2011;3(11):929-36.
39. Weber Lozada K, Keri RA. Bisphenol A increases mammary cancer risk in two distinct mouse models of breast cancer. Biol Reprod. 2011;85(3):490-7.
40. Hilakivi-Clarke L, Cho E, Onojafe I, Raygada M, Clarke R. Maternal exposure to genistein during pregnancy increases carcinogen-induced mammary tumorigenesis in female rat offspring. Oncol Rep. 1999;6(5):1089-95.
41. Lamartiniere CA, Cotroneo MS, Fritz WA, Wang J, Mentor-Marcel R, Elgavish A. Genistein chemoprevention: timing and mechanisms of action in murine mammary and prostate. J Nutr. 2002;132(3):552S-8S.
42. El Sheikh SH, Meduri G, Phrakonkham P, Berges R, Vacher S, Djallali M, et al. Abnormal peripubertal development of the rat mammary gland following exposure in utero and during lactation to a mixture of genistein and the food contaminant vinclozolin. Reprod Toxicol. 2011;32(1):15-25.
43. Delclos KB, Bucci TJ, Lomax LG, Latendresse JR, Warbritton A, Weis CC, et al. Effects of dietary genistein exposure during development on male and female CD (Sprague-Dawley) rats. Reprod Toxicol. 2001;15(6):647-63.
44. Chiesa G, Rigamonti E, Lovati MR, Disconzi E, Soldati S, Sacco MG, et al. Reduced mammary tumor progression in a transgenic mouse model fed an isoflavone-poor soy protein concentrate. Mol Nutr Food Res. 2008;52(10):1121-9.
45. Luijten M, Thomsen AR, van den Berg JA, Wester PW, Verhoef A, Nagelkerke NJ, et al. Effects of soy-derived isoflavones and a high-fat diet on spontaneous mammary tumor development in Tg.NK (MMTV/c-neu) mice. Nutr Cancer. 2004;50(1):46-54.
46. Yang X, Edgerton SM, Kosanke SD, Mason TL, Alvarez KM, Liu N, et al. Hormonal and dietary modulation of mammary carcinogenesis in mouse mammary tumor virus-c-erbB-2 transgenic mice. Cancer Res. 2003;63(10):2425-33.
47. Jin Z, MacDonald RS. Soy isoflavones increase latency of spontaneous mammary tumors in mice. J Nutr. 2002;132(10):3186-90.
48. Sampayo R, Recouvreux S, Simian M. The hyperplastic phenotype in PR-A and PR-B transgenic mice: lessons on the role of estrogen and progesterone receptors in the mouse mammary gland and breast cancer. Vitam Horm. 2013;93:185-201.
49. Feng Y, Manka D, Wagner KU, Khan SA. Estrogen receptor-alpha expression in the mammary epithelium is required for ductal and alveolar morphogenesis in mice. Proc Natl Acad Sci USA. 2007;104(37):14718-23.
50. Tekmal RR, Liu YG, Nair HB, Jones J, Perla RP, Lubahn DB, et al. Estrogen receptor alpha is required for mammary development and the induction of mammary hyperplasia and epigenetic alterations in the aromatase transgenic mice. J Steroid Biochem Mol Biol. 2005;95(1-5):9-15.
51. Mueller SO, Clark JA, Myers PH, Korach KS. Mammary gland development in adult mice requires epithelial and stromal estrogen receptor alpha. Endocrinology. 2002;143(6):2357-65.
52. Macias H, Hinck L. Mammary gland development. Wiley Interdiscip Rev Dev Biol. 2012;1(4):533-57.
53. Stingl J. Estrogen and progesterone in normal mammary gland development and in cancer. Horm Cancer. 2011;2(2):85-90.
54. Brisken C, O'Malley B. Hormone action in the mammary gland. Cold Spring Harb Perspect Biol. 2010;2(12):a003178.
55. Setchell KD. Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones. Am J Clin Nutr. 1998;68(6 Suppl):1333S-46S.
56. Luetteke NC, Qiu TH, Fenton SE, Troyer KL, Riedel RF, Chang A, et al. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development. 1999;126(12):2739-50.
57. Aupperlee MD, Leipprandt JR, Bennett JM, Schwartz RC, Haslam SZ. Amphiregulin mediates progesterone-induced mammary ductal development during puberty. Breast Cancer Res. 2013;15(3):R44.
58. McBryan J, Howlin J, Napoletano S, Martin F. Amphiregulin: role in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia. 2008;13(2):159-69.
59. Howard BA, Lu P. Stromal regulation of embryonic and postnatal mammary epithelial development and differentiation. Semin Cell Dev Biol. 2014;25-26: 43-51
60. Hynes NE, Watson CJ. Mammary gland growth factors: roles in normal development and in cancer. Cold Spring Harb Perspect Biol. 2010;2(8):a003186.
61. McNally S, Martin F. Molecular regulators of pubertal mammary gland development. Ann Med. 2011;43(3):212-34.
62. Vantyghem SA, Wilson SM, Postenka CO, Al-Katib W, Tuck AB, Chambers AF. Dietary genistein reduces metastasis in a postsurgical orthotopic breast cancer model. Cancer Res. 2005;65(8):3396-403.
63. Singh AV, Franke AA, Blackburn GL, Zhou JR. Soy phytochemicals prevent orthotopic growth and metastasis of bladder cancer in mice by alterations of cancer cell proliferation and apoptosis and tumor angiogenesis. Cancer Res. 2006;66(3):1851-8.
64. Magee PJ, McGlynn H, Rowland IR. Differential effects of isoflavones and lignans on invasiveness of MDA-MB-231 breast cancer cells in vitro. Cancer Lett. 2004;208(1):35-41.
65. Farina HG, Pomies M, Alonso DF, Gomez DE. Antitumor and antiangiogenic activity of soy isoflavone genistein in mouse models of melanoma and breast cancer. Oncol Rep. 2006;16(4):885-91.
66. Magee PJ, Allsopp P, Samaletdin A, Rowland IR. Daidzein, R-(+)equol and S-(-)equol inhibit the invasion of MDA-MB-231 breast cancer cells potentially via the down-regulation of matrix metalloproteinase-2. Eur J Nutr. 2014;53(1):345-50.
67. Martinez-Montemayor MM, Otero-Franqui E, Martinez J, De La Mota-Peynado A, Cubano LA, Dharmawardhane S. Individual and combined soy isoflavones exert differential effects on metastatic cancer progression. Clin Exp Metastasis. 2010;27(7):465-80.
68. Pavese JM, Krishna SN, Bergan RC. Genistein inhibits human prostate cancer cell detachment, invasion, and metastasis. Am J Clin Nutr. 2014;100(Supplement 1):431S-6S.
69. Shu XO, Zheng Y, Cai H, Gu K, Chen Z, Zheng W, et al. Soy food intake and breast cancer survival. JAMA. 2009;302(22):2437-43.
70. Weigelt B, Eberle C, Cowell CF, Ng CKY, Reis-Filho JS. Metaplastic breast carcinoma: more than a special type. Nat Rev Cancer. 2014;8(8):1588-602.
71. Tse GM, Tan PH, Putti TC, Lui PC, Chaiwun B, Law BK. Metaplastic carcinoma of the breast: a clinicopathological review. J Clin Pathol. 2006;59(10):1079-83.
72. Al Sayed AD, El Weshi AN, Tulbah AM, Rahal MM, Ezzat AA. Metaplastic carcinoma of the breast clinical presentation, treatment results and prognostic factors. Acta Oncol. 2006;45(2):188-95.
73. Reis-Filho JS, Milanezi F, Steele D, Savage K, Simpson PT, Nesland JM, et al. Metaplastic breast carcinomas are basal-like tumours. Histopathology. 2006;49(1):10-21.
74. Reis-Filho JS, Pinheiro C, Lambros MB, Milanezi F, Carvalho S, Savage K, et al. EGFR amplification and lack of activating mutations in metaplastic breast carcinomas. J Pathol. 2006;209(4):445-53.
75. Cooper CL, Karim RZ, Selinger C, Carmalt H, Lee CS, O'Toole SA. Molecular alterations in metaplastic breast carcinoma. J Clin Pathol. 2013;66(6):522-8.
76. Nakai M, Cook L, Pyter LM, Black M, Sibona J, Turner RT, et al. Dietary soy protein and isoflavones have no significant effect on bone and a potentially negative effect on the uterus of sexually mature intact Sprague-Dawley female rats. Menopause. 2005;12(3):291-8.
77. Michael McClain R, Wolz E, Davidovich A, Pfannkuch F, Edwards JA, Bausch J. Acute, subchronic and chronic safety studies with genistein in rats. Food Chem Toxicol. 2006;44(1):56-80.