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Mechanisms by which high maternal fat intake during pregnancy increases breast cancer risk in female rodent offspring

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Abstract

Emerging evidence indicates that a high in utero estrogenic environment increases breast cancer risk in women. We have proposed that a maternal intake of a high-fat diet is a source for high pregnancy estrogen levels and increases breast cancer risk among female offspring. In this review, the role of dietary fat in breast cancer, particularly during fetal life, is discussed. In addition, we provide possible mechanisms of action of the effects of a high-fat diet on the breast. These mechanisms include protein kinase C, estrogens and estrogen receptor, and alterations in mammary parenchymal structures.

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References

  1. Kato I, Tominaga S, Kuroishi T: Relationship between westernization of dietary habits and mortality from breast cancer in Japan. Gann 78:349–357, 1987

    PubMed  Google Scholar 

  2. Carroll KK, Khor HT: Dietary fat in relation to tumorigenesis. Prog Biochem Pharm 10:308–353, 1975

    Google Scholar 

  3. Pisani P: Breast cancer: geographic variation and risk factors. J Environ Pathol Toxicol Oncol 11:313–316, 1992

    PubMed  Google Scholar 

  4. Wynder EL, Fujita Y, Harris RE, Hirayama T, Hiyama T: Comparative epidemiology of cancer between the United States and Japan. A second look. Cancer 67:746–763, 1991

    PubMed  Google Scholar 

  5. Boyd NF, Martin LJ, Noffel M, Lockwood GA, Tritchler DL: A meta-analysis of studies of dietary fat and breast cancer risk. Br J Cancer 68:627–636, 1993

    PubMed  Google Scholar 

  6. Howe GR, Hirohata T, Hislop TG, Iscovich JM, Yuan JM, Katsoyanni K, Lubin F, Marubini E, Modan B, Rohan T: Dictary factors and risk of breast cancer: combined analysis of 12 case-control studies. J Natl Cancer Inst 82:561–569, 1990

    PubMed  Google Scholar 

  7. Macrae FA: Fat and calories in colon and breast cancer: from animal studies to controlled clinical trials. Prev Med 22:750–766, 1993

    Article  PubMed  Google Scholar 

  8. Jain M, Miller AB, To T: Premorbid diet and the prognosis of women with breast cancer. J Natl Cancer Inst 86:1390–1397, 1994

    PubMed  Google Scholar 

  9. Sasaki S, Horacsek M, Kasteloot H: An ecological study of the relationship between dietary fat intake and breast cancer mortality. Prev Med 22:187–202, 1993

    Article  PubMed  Google Scholar 

  10. Zhang S, Folsom AR, Sellers TA, Kushi LH, Potter JD: Better breast cancer survival for postmenopausal women who are less overweight and eat less fat. The Iowa Women's Health Study. Cancer 76:275–283, 1995

    PubMed  Google Scholar 

  11. Freedman LS, Clifford CK, Messina M: Analysis of dietary fat, calories, body weight, and the development of mammary tumors in rats and mice: a review. Cancer Res 50:5710–5719, 1990

    PubMed  Google Scholar 

  12. Welsch CW: Relationship between dietary fat and experimental mammary tumorigenesis: a review and critique. Cancer Res 52:2040–2048, 1992

    Google Scholar 

  13. Willett WC, Hunter DJ: Prospective studies of diet and breast cancer. Cancer 74:1085–1089, 1994

    PubMed  Google Scholar 

  14. Witte JS, Ursin G, Siemiatycki J, Thompson WD, Paganini-Hill A, Haile RW: Diet and premenopausal bilateral breast cancer: A case-control study. Breast Cancer Res Treat 42:243–251, 1997

    Article  PubMed  Google Scholar 

  15. Willett WC, Hunter DJ, Stampfer MJ, Colditz G, Manson JE, Spiegelman D, Rosner B, Hennekens CH, Speizer FE: Dietary fat and fiber in relation to risk of breast cancer. JAMA 268:2037–2044, 1992

    PubMed  Google Scholar 

  16. Hunter DJ, Spiegelman D, Adami HO, Beeson L, van den Brandt PA, Folsom AR, Fraser GE, Goldbohm RA, Graham S, Howe GR, Kushi LH, Marshall JR, McDermott A, Miller AB, Speizer FE, Wolk A, Yuan S, Willett W: Cohort studies of fat intake and the risk of breast cancer — a pooled analysis. N Engl J Med 334:356–361, 1996

    Article  PubMed  Google Scholar 

  17. Boyd NF, Cousins M, Lockwood G, Tritchler D: The feasibility of testing experimentally the dietary fat-breast cancer hypothesis. Br J Cancer 62:878–881, 1990

    PubMed  Google Scholar 

  18. Howe GR: HIgh-fat diets and breast cancer risk. The epidemiological evidence. JAMA 268:2080–2081, 1992

    PubMed  Google Scholar 

  19. Holm L-E, Nordevang E, Hjalmar ML, Lidbrink E, Callmer E, Nilsson B: Treatment failure and dietary habits in women with breast cancer. J Natl Cancer Inst 85:32–36, 1993

    PubMed  Google Scholar 

  20. Sylvester PW, Russell M, Ip MM, Ip C: Comparative effects of different animal and vegetable fats fed before and during carcinogen administration on mammary tumorigenesis, sexual maturation, and endocrine function. Cancer Res 46:757–762, 1986

    PubMed  Google Scholar 

  21. Chan PC, Ferguson KA, Dao TL: Effects of different dietary fats on mammary carcinogenesis. Cancer Res 43:1079–1083, 1983

    PubMed  Google Scholar 

  22. Buckman DK, Chapkin RS, Erickson KL: Modulation of mouse mammary tumor growth and linoleate-enhanced metastasis by oleate. J Nutr 120:148–157, 1990

    PubMed  Google Scholar 

  23. Rose DP, Connolly JM, Rayburn J, Coleman M: Influence of diets containing eicosapentaenoic or docosahexaenoic acid on growth and metastasis of breast cancer cells in nude mice. J Natl Cancer Inst 87:587–592, 1995

    PubMed  Google Scholar 

  24. Pritchard GA, Jones DL, Mansel RE: Lipids in breast carcinogenesis. Br J Surg 76:1069–1073, 1989

    Google Scholar 

  25. Adams LM, Trout JR, Karmali RA: Effect of n-3 fatty acids on spontaneous and experimental metastasis of rat mammary tumor 13762. Br J Cancer 61:290–291, 1990

    PubMed  Google Scholar 

  26. Caygill CPJ, Charlett A, Hill MJ: Fat, fish, fish oil and cancer. Br J Cancer 74:159–164, 1996

    PubMed  Google Scholar 

  27. Caygill CPJ, Hill MJ: Fish n-3 fatty acids and human colorectal and breast cancer. Eur J Cancer Prev 4:329–332, 1995

    PubMed  Google Scholar 

  28. Al MD, v. Houwelingen AC, Badart-Smook A, Honstra G: Some aspects of neonatal essential fatty acid status are altered by linoleic acid supplementation of women during pregnancy. J Nutr 125:2822–2830, 1995

    PubMed  Google Scholar 

  29. Rahm JR, Holman RT: Effect of linoleic acid upon the metabolism of linolenic acid. J Nutr 84:15–19, 1964

    PubMed  Google Scholar 

  30. Parkin DM, Muir CS, Whelan SL: Cancer Incidence in Five Continents. IACR, Lyon, 1992

    Google Scholar 

  31. Dunn JEJ: Cancer epidemiology in populations of the United States — with emphasis on Hawaii and California — and Japan. Cancer Res 35:3240–3245, 1975

    PubMed  Google Scholar 

  32. Kolonel LN, Hinds MW, Hankin JH: Cancer patterns among migrant and native born Japanese in Hawaii in relation to smoking, drinking and dietary habits. In: Gelboin HV, MacMahon B, Matsushima T (eds) Genetic and Environmental Factors in Experimental and Human Cancer. Japan Science Society Press, Tokyo, 1980, pp 327–340

    Google Scholar 

  33. Locke FB, King H: Cancer mortality among Japanese in the United States. J Natl Cancer Inst 65:237–242, 1980

    Google Scholar 

  34. Thomas DB, Karagas MR: Cancer in first and second generation Americans. Cancer Res 47:5771–5776, 1987

    PubMed  Google Scholar 

  35. Ziegler RG, Hoover RN, Pike MC, Hildesheim A, Nomura AMY, West DW, Wu-Williams AH, Kolonel LN, Horn-Ross PL, Rosenthal JF, Hyer MB: Migration patterns and breast cancer risk in Asian-American women. J Natl Cancer Inst 85:1819–1827, 1993

    PubMed  Google Scholar 

  36. Walker BE: Tumors in female offspring of control and diethylstilbestrol-exposed mice fed high-fat diets. J Natl Cancer Inst 82:50–54, 1990

    PubMed  Google Scholar 

  37. Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman ME: A maternal diet high in n-6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proc Natl Acad Sci USA, in press, 1997

  38. Michels KB, Trichopoulos D, Robins JM, Rosner BA, Manson JE, Hunter D, Colditz GA, Hankinson SE, Spelzer FE, Willett WC: Birthweight as a risk factor for breast cancer. Lancet 348:1542–1546, 1996

    Article  PubMed  Google Scholar 

  39. Borgeson CE, Pardini L, Pardini R, Reitz RC: Effects of dietary fish oil on human mammary carcinoma and on lipid-metabolizing enzymes. Lipids 24:290–295, 1989

    PubMed  Google Scholar 

  40. Cheeseman KH, Emery S, Maddix SP, Slater TF, Burton GW, Ingold KU: Studies on lipid peroxidation in normal and tumor tissues. Biochem J 250:247–252, 1988

    PubMed  Google Scholar 

  41. Chajes V, Sattler W, Stranzl A, Kostner GM: Influence of n-3 fatty acids on the growth of human breast cancer cells in vitro: relationship to peroxidases and vitamin-E. Breast Cancer Res Treat 34:199–212, 1995

    PubMed  Google Scholar 

  42. Gonzalez MJ: Fish oil, lipid peroxidation and mammary tumorigenesis. J Am Coll Nutr 14:325–335, 1995

    PubMed  Google Scholar 

  43. Diplock AT, Rice-Evans CA, Burdon RH: Is there a significant role for lipid peroxidation in the causation of malignancy and the antioxidants in cancer prevention? Cancer Res 54:1952s–1956s, 1994

    PubMed  Google Scholar 

  44. Jurkowski JJ, Cave WT: Dietary effects of menhaden oil on the growth and membrane lipid composition of rat mammary tumors. J Natl Cancer Inst 74:1145–1150, 1985

    PubMed  Google Scholar 

  45. Stubbs CD, Smith AD: The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta 779:89–137, 1984

    PubMed  Google Scholar 

  46. Cave WT, Krickson-Lucas MJ: Effects of dietary lipids on lactogenic hormone receptor binding in rat mammary tumors. J Natl Cancer Inst 68:319–324, 1982

    PubMed  Google Scholar 

  47. Rao GA, Abrahams S: Enhanced growth rate of transplanted mammary adenocarcinoma induced in C3H mice by dietary linoleate. J Natl Cancer Inst 56:431–432, 1976

    PubMed  Google Scholar 

  48. Hillyard LA, Abraham S: Effect of dietary polyunsaturated fatty acids on growth of mammary adenocarcinomas in mice and rats. Cancer Res 39:4430–4437, 1979

    PubMed  Google Scholar 

  49. Abrahams S, Hillyard LA: Effect of dietary 18 carbon fatty acids on growth of transplantable mammary adenocarcinomas in mice. J Natl Cancer Inst 71:601–605, 1983

    PubMed  Google Scholar 

  50. Karmali RA: Prostaglandins and cancer. Prost Med 5:11–28, 1980

    Article  Google Scholar 

  51. Carroll KK: A proposed mechanism for effects of diet on mammary cancer. Nutr Cancer 16:79–83, 1991

    PubMed  Google Scholar 

  52. Rose DP, Hatala MA: Dietary fatty acids and breast cancer invasion and metastasis. Nutr Cancer 21:103–111, 1994

    PubMed  Google Scholar 

  53. Choe M, Kris ES, Luthra R, Copenhaver J, Pelling JC, Donnelly TE, Birt DE: Protein kinase C is activated and diacylglycerol is elevated in epidermal cells from SENCAR mice fed high fat diets. J Nutr 122:2322–2329, 1992

    PubMed  Google Scholar 

  54. Kris E, Choe M, Luthra R, Conway H, Barnett T, Yakine A, Birt DE: Protein kinase C activity is reduced in epidermal cells from energy restricted SENCAR mice. J Nutr 124:485–492, 1994

    PubMed  Google Scholar 

  55. Reddy BS, Simi B, Patel N, Aliaga C, Rao CV: Effect of amount and types of dietary fat on intestinal bacterial 7alpha-dehydroxylase and phosphatidylinositol-specific phospholipase C and colonic mucosal diacylglycerol kinase and PKC activites during different stages of colon tumor promotion. Cancer Res 56:2314–2320, 1996

    PubMed  Google Scholar 

  56. Hilakivi-Clarke LA, Raygada M, Stoica A, Martin M-B: Consumption of a high-fat diet during pregnancy alters estrogen receptor content, protein kinase C activity and morphology of mammary gland in the mother and her female offspring. Cancer Res, submitted, 1997

  57. Birt DE, Barnett T, Pour PM, Copenhaver J: High-fat diet blocks the inhibition of skin carcinogenesis and reductions in protein kinase C by moderate energy restriction. Molec Carcinogenesis 16:115–120, 1996

    Article  Google Scholar 

  58. Dekker LV, Parker PJ: Protein kinase C — a question of specificity. Trends Biochem Sci 19:73–77, 1994

    Article  PubMed  Google Scholar 

  59. Azzi A, Boscoboinik D, Hensey C: The protein kinase C family. Eur J Biochem 208:547–557, 1992

    PubMed  Google Scholar 

  60. Hug H, Sarre TF: Protein kinase C isoenzymes: divergence in signal transduction. Biochem J 291:329–343, 1993

    PubMed  Google Scholar 

  61. Nishizuka Y: Intracellular signalling by hydrolysis of phospholipids and activation of protein kinase C. Science 258:607–614, 1992

    PubMed  Google Scholar 

  62. Clarke R, Dickson RB, Lippman EM: Hormonal aspects of breast cancer. Growth factors, drugs and stromal interactions. Crit Rev Oncol Hematol 12:1–23, 1992

    PubMed  Google Scholar 

  63. Marte BM, Meyer T, Stabel S, Standke GJR, Jaken S, Fabbro D, Hynes NE: Protein kinase C and mammary cell differentiation: involvement of protein kinase C α in the induction of β-casein expession. Cell Growth Differen 5:239–247, 1994

    Google Scholar 

  64. O'Brian CA, Ward N: Biology of the protein kinase C family. Cancer Metast Rev 8:199–214, 1989

    Google Scholar 

  65. Blobe GC, Sachs CW, Wasiuddin AK, Fabbro D, Stabel S, Wetzel WC, Obeid LM, Fine RL, Hannun YA: Selective regulation of expression of protein kinase (PKC) isoenzymes in multidrug resistant MCF-7 cells. J Cell Biol 268:658–664, 1993

    Google Scholar 

  66. Ways DK, Kukoly CA, de Vente J, Hooker JL, Bryant WO, Posekany KJ, Fletcher DJ, Cook PP, Parker PP: MCF-7 breast cancer cells transfected with PKC-alpha exhibit altered expression of other protein kinase C isoforms and display a more aggressive neoplastic phenotype. J Clin Invest 95:1906–1915, 1995

    PubMed  Google Scholar 

  67. Manni A, Buckalter E, Etindi R, Kunselman S, Rossini A, Mauger D, Dabbs D, Demers L: Induction of less aggressive breast cancer phenotype by protein kinase C-alpha and-beta overexpression. Cell Growth Diff 7:1187–1198, 1996

    PubMed  Google Scholar 

  68. Bryant WO, Kukoly CA, Garris TO, Cook PP, Parker PJ, Pettit GR, Wyas DK: Anchorage independent growth of breast cancer cells. Proceedings of the 77th Annual Meeting of the Endocrine Society, Abstract P2-639, 1995

  69. Masso Welh P, Verstovsek G, Tagliarno C, Ip M: Protein kinase C-beta upregulation and secretion during postnatal mammary gland development. Proceedings of the 88th Annual Meeting of AACR, Abstract 3364, 1997

  70. Goldin BR, Adlercreutz H, Gorbach SL, Warram JH: Estrogen excretion patterns and plasma levels in vegetarian and omnivorous women. N Engl J Med 307:1452–1547, 1982

    Google Scholar 

  71. Bennett FC, Ingram DM: Diet and female sex hormone concentrations: an intervention study for the type of fat consumed. Am J Clin Nutr 52:808–812, 1990

    PubMed  Google Scholar 

  72. Rose DP, Boyar AP, Cohen C, Strong LE: Effect of a low-fat diet on hormone levels in women with cystic breast disease. J Natl Cancer Inst 78:623–626, 1987

    PubMed  Google Scholar 

  73. Rose DP, Connolly JM, Chlebowski RT, Buzzard IM, Wynder EL: The effects of a low-fat dietary intervention and tamoxifen adjuvant therapy on the serum estrogen and sex hormone-binding globulin concentrations of postmenopausal breast cancer patients. Breast Cancer Res Treat 27:253–262, 1993

    PubMed  Google Scholar 

  74. Chan PC, Head JF, Cohen LA, Wynder EL: Influence of dietary fat on the induction of mammary tumors by nitrosomethylurea: associated hormone changes and differences between Sprague-Dawley and F344 rats. J Natl Cancer Inst 59:1279–1283, 1977

    PubMed  Google Scholar 

  75. Ip C, Ip MM: Serum estrogens and estrogen responsiveness in 7,12-dimethylbenz(a)anthracene-induced mammary tumors as influenced by dietary fat. J Natl Cancer Inst 66:291–295, 1981

    PubMed  Google Scholar 

  76. Hilakivi-Clarke L, Onojafe I, Cho E: High-fat diet induces aggressive behavior in male mice and rats. Life Sci 58:1653–1660, 1996

    Article  PubMed  Google Scholar 

  77. Frisch RE: Adipose Tissue and Reproduction. Karger, Basel, 1990

    Google Scholar 

  78. Noble LS, Simpson ER, Johns A, Bulun SE: Aromatase expression in endometriosis. J Clin Endocrin Metab 81:179–182, 1996

    Google Scholar 

  79. Bruning PF, Bonfrer JMG: Possible relevance of steroid availability and breast cancer. Ann N Y Acad Sci 257–264, 1990

  80. Glass AG, Hoover RN: Rising incidence of breast cancer: relationship to stage and receptor status. J Natl Cancer Inst 82:693–696, 1990

    PubMed  Google Scholar 

  81. Pasqualini JR, Sumida C, Giambiagi N: Biological effects of estrogens and antiestrogens in the fetus and newborns. In: McLachlan JA (ed) Estrogens in the Environment. Elsevier Science Publishing, New York, 1985, pp 252–271

    Google Scholar 

  82. Haslam S: The ontogeny of mouse mammary gland responsiveness to ovarian steroid hormones. Endocrinology 125:2766–2772, 1989

    PubMed  Google Scholar 

  83. Kelly PA, Djianc J, Malancon R: Characterization of estrogen, progesterone and glucocorticoid receptors in rabbit mammary glands and their measurement during pregnancy and lactation. J Steroid Biochem 18:215–221, 1983

    Article  PubMed  Google Scholar 

  84. Yu WC, Leung BS: Variation of cytoplasmic content of estrogen and progesterone receptors in the mammary gland and uterus of rats at time of parturition. Biol Reprod 27:658–664, 1982

    PubMed  Google Scholar 

  85. Haslam SZ, Nummy KA: The ontogeny and cellular distribution of estrogen receptors in normal mouse mammary gland. J Steroid Biochem Molec Biol 42:589–595, 1992

    Article  PubMed  Google Scholar 

  86. Haslam SZ: Role of sex steroid hormones in normal mammary gland function. In: Neville MC, Daniel CW (eds) The Mammary Gland: Development, Regulation and Function. Plenum Press, New York, 1987 pp 499–510

    Google Scholar 

  87. Bern HA, Mills KT, Jones LA: Critical period for neonatal estrogen exposure in occurrence of mammary gland abnormalities in adult mice. Proc Soc Exp Biol Med 172:239–242, 1983

    PubMed  Google Scholar 

  88. Potter JD, Cerhan JR, Sellers TA, McGovern PG, Drinkard C, Kushi LR, Folsom AR: Progesterone and estrogen receptors and mammary neoplasia in the Iowa Women's Health Study: How many kinds of breast cancer are there? J Natl Cancer Inst 85:32–36, 1995

    Google Scholar 

  89. Russo III, Mcdado J, Russo J: Endocrine influences on the mammary gland. In: Jones TC, Mohr U, Hunt RD (eds) Integument and Mammary Glands. Springer-Verlag, Berlin, 1994 pp 252–266

    Google Scholar 

  90. Bern HA, Mills KT, Edery M: Estrogen-associated defects in rodent mammary gland development. In: McLachlan JA (ed) Estrogens in the Environment. Elsevier Science Publishing, New York, 1985, pp 319–326

    Google Scholar 

  91. King RJB: Estrogen and progestin effects in human breast carcinogenesis. Breast Cancer Res Treat 27:3–15, 1993

    PubMed  Google Scholar 

  92. Vladusic EA, Hornby AE, Guerra FK, Lupu R: Expression of ER-beta in breast cancer cells: Does it play an improtant role? Proc AACR 38: Abstract 1995, 1997

  93. Imagawa W, Bandyopadhyay GK, Nandi S: Regulation of mammary epithelial cell growth in mice and rats. Endocrine Rev 11:494–523, 1990

    Google Scholar 

  94. Sakakura T: Mammary embryogenesis. In: Neville MC, Daniel CW (eds) Mammary Gland: Development, Regulation, and Function. Plenum Press, New York, 1987, pp 37–55

    Google Scholar 

  95. Pitelka DR. Cell contacts in the mammary gland. In: Larson BL (ed) Lactation: A Comprehensive Treatment. Academic Press, New York, 1978, pp 41–60

    Google Scholar 

  96. Daniel CW, Silberstein GB: Postnatal development of the rodent mammary gland. In: Silberstein GB, Daniel CW (eds) The Mammary Gland: Development, Regulation, and Function. Plenum Press, New York, 1987, pp 3–36

    Google Scholar 

  97. Russo J, Russo IH: Biological and molecular bases of mammary carcinogenesis. Lab Invest 57:112–137, 1987

    PubMed  Google Scholar 

  98. Russo J, Gusterson BA, Rogers AE, Russo IH, Wellings SR, van Zwieten MJ: Comparative study of human and rat mammary tumorigenesis. Lab Invest 62:244–278, 1990

    PubMed  Google Scholar 

  99. Rosen JM, Humphreys R, Krnacik S, Juo P, Raught B: The regulation of mammary gland development by hormones, growth factors, and oncogenes. Prog Clin Biol Res 387:95–111, 1994

    PubMed  Google Scholar 

  100. New MI: Premature thelarche and estrogen intoxication. In: McLachlan (ed) Estrogens in the Environment. Elsevier Science Publishing, New York, 1985, pp 349–357

    Google Scholar 

  101. Raymaud A: Observations sur les modifications provoquees par les hormones oestrogenes, du mode de developpement des mamelons des foetus de souris. C R Acad Sci 240:674–676, 1955

    Google Scholar 

  102. Warner MR: Effect of various doses of estrogen to BALB/cCrgl neonatal female mice on mammary growth and branching at 5 weeks of age. Cell Tissue Kinet 9:429–438, 1976

    PubMed  Google Scholar 

  103. Tamooka T, Bern HA: Growth of mouse mammary glands after neonatal sex hormone treatment. J Natl Cancer Inst 69:1347–1352, 1982

    PubMed  Google Scholar 

  104. Jones LA, Bern HA: Cervicovaginal and mammary gland abnormalities in BALB/cCrgl mice treated neonatally with progesterone and estrogen, alone or in combination. Cancer Res 39:2560–2567, 1979

    PubMed  Google Scholar 

  105. Verhoeven G, Vandoren G, Heyns W, Kuhn ER, Janssens JP, Teuwen D, Goddeeris E, Lesaffre E, DeMoor P: J Endocrinol 95:357–368, 1982

    PubMed  Google Scholar 

  106. Hilakivi-Clarke L, Cho E, Raygada M, Kenney N: Alterations in mammary gland development following neonatal exposure to estradiol, transforming growth factor alpha, and estrogen receptor antagonist ICI 182,780. J Cell Physiol 170:279–289, 1997

    Article  PubMed  Google Scholar 

  107. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT: TGFα overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 61:1137–1146, 1990

    Article  PubMed  Google Scholar 

  108. Hilakivi-Clarke LA, Arora PK, Sabol MB, Clarke R, Dickson RB, Lippman ME: Alterations in behavior, steroid hormones and natural killer cell activity in male transgenic TGFα mice. Brain Res 588:97–103, 1992

    Article  PubMed  Google Scholar 

  109. Krane IM, Leder P: NDF/heregulin induces persistence of terminal end buds and adenocarcinomas in the mammay glands of transgenic mice. Oncogene 12:1781–1788, 1996

    PubMed  Google Scholar 

  110. Reece RP, Turner CW, Hill RT: Mammary gland development in the hypophysectomized albino rat. Proc Soc Exp Biol Med 34:204–217, 1936

    Google Scholar 

  111. Gardner WU, White A: Mammary growth in hypophysectomized male mice receiving estrogen and prolactin. Proc Soc Exp Biol Med 48:590–592, 1941

    Google Scholar 

  112. Lyons WR, Li CH, Johnson RE: The hormonal control of mammary growth and lactation. Rec Prog Horm Res 14:219–248, 1958

    PubMed  Google Scholar 

  113. Nandi S: Endocrine control of mammary gland development and function in the C3 11/HE Crgl mouse. J Natl Cancer Inst 21:1039–1062, 1958

    PubMed  Google Scholar 

  114. Kleinberg DL: Early mammary development: growth hormone and IGF-1. J Mammary Gland Biol Neoplasia 2:49–57, 1997

    Article  PubMed  Google Scholar 

  115. Vonderhaar BK: Prolactin: transport, function, and receptors in mammary gland development and differentiation. In: Neville MC, Daniel CW (eds) The Mammary Gland. Plenum, New York, 1987, pp 383–438

    Google Scholar 

  116. Vonderhaar BK: Local effects of EGF, alpha-TGF, and EGF-like growth factors on lobuloalveolar development of the mouse mammary gland in vivo. J Cell Physiol 132:581–584, 1987

    PubMed  Google Scholar 

  117. Coleman S, Silberstein GB, Daniel CW: Ductal morphogenesis in the mouse mammary gland: evidence supporting a role for epidermal growth factor. Dev Biology 127:304–315, 1988

    Article  Google Scholar 

  118. Dickson RB, Lippman ME: Growth factors in breast cancer. Endocr Rev 16:559–589, 1995

    Article  PubMed  Google Scholar 

  119. Welsch CW, O'Connor DH: Influence of dietary fat on developmental growth of the mammary gland in immature and mature female BALB/c mice. Cancer Res 49:5999–6007, 1989

    PubMed  Google Scholar 

  120. Hilakivi-Clarke L, Onojafe I, Raygada M, Cho E, Clarke R, Lippman M: High-fat diet during pregnancy increases breast cancer risk in rats. J Natl Cancer Inst 88:1821–1827, 1996

    PubMed  Google Scholar 

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    Leena Hilakivi-Clarke

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Hilakivi-Clarke, L. Mechanisms by which high maternal fat intake during pregnancy increases breast cancer risk in female rodent offspring. Breast Cancer Res Treat 46, 199–214 (1997). https://doi.org/10.1023/A:1005983621612

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