Pregnancy hormonal environment and mother's breast cancer risk

Hormone Molecular Biology and Clinical Investigation

Volumn 9, Issue 1, 2012, Pages 11-23

  Hilakivi Clarke, Leena ^a   Assis, Sonia de ^a   Warri, Anni ^a   Luoto, Riitta ^b  

^a GEORGETOWN UNIVERSITY   (United States)

^b UKK INSTITUTE FOR HEALTH PROMOTION RESEARCH   (Finland)

Author keywords

breast cancer; estradiol; leptin; pregnancy

Indexed keywords

CHORIONIC GONADOTROPIN; ESTROGEN; ESTROGEN RECEPTOR; GROWTH FACTOR; LEPTIN; PROGESTERONE;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM CELL; CANCER RISK; CELL DIFFERENTIATION; FEMALE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION; HORMONE BLOOD LEVEL; HORMONE DETERMINATION; HUMAN; INVOLUTION; NONHUMAN; PARITY; PREGNANCY; PRIORITY JOURNAL; STEM CELL; WEIGHT GAIN;

EID: 84994862966     PISSN: 18681883     EISSN: 18681891     Source Type: Journal    
DOI: 10.1515/hmbci-2012-0019     Document Type: Article

References (138)

1. Lyons TR, Schedin PJ, Borges VF. Pregnancy and breast cancer: when they collide. J Mammary Gland Biol Neoplasia 2009;14:87–98.
2. Bernstein L. Epidemiology of endocrine-related risk factors for breast cancer. J Mammary Gland Biol Neoplasia 2002;7:3–15.
3. MacMahon B, Cole P, Lin TM, Lowe CR, Mirra AP, Ravnihar B, Salber EJ, Valaoras VG, Yuasa S. Age at first birth and breast cancer. Bull World Health Org 1970;43:209–221.
4. Bruzzi P, Negri E, La Vecchia C. Short term increase in risk of breast cancer after full term pregnancy. Br Med J 1988;297: 1096–1098.
5. Williams EM, Jones L, Vessey MP, McPherson K. Short term increase in risk of breast cancer associated with full pregnancy. Br Med J 1990;300:578–579.
6. Albrektsen G, Heuch I, Hansen S, Kvale G. Breast cancer risk by age at birth, time since birth and time intervals between births: exploring interaction effects. Br J Cancer 2005;92:167–175.
7. Liu Q, Wuu J, Lambe M, Hsieh SF, Ekbom A, Hsieh CC. Transient increase in breast cancer risk after giving birth: postpartum period with the highest risk (Sweden). Cancer Causes Control 2002;13:299–305.
8. Ma H, Bernstein L, Pike MC, Ursin G. Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res 2006;8:R43.
9. Lord SJ, Bernstein L, Johnson KA, Malone KE, McDonald JA, Marchbanks PA, Simon MS, Strom BL, Press MF, Folger SG, Burkman RT, Deapen D, Spirtas R, Ursin G. Breast cancer risk and hormone receptor status in older women by parity, age of first birth, and breastfeeding: a case-control study. Cancer Epidemiol Biomarkers Prev 2008;17:1723–1730.
10. Ursin G, Bernstein L, Lord SJ, Karim R, Deapen D, Press MF, Daling JR, Norman SA, Liff JM, Marchbanks PA, Folger SG, Simon MS, Strom BL, Burkman RT, Weiss LK, Spirtas R. Reproductive factors and subtypes of breast cancer defined by hormone receptor and histology. Br J Cancer 2005;93:364–371.
11. Britt K, Ashworth A, Smalley M. Pregnancy and the risk of breast cancer. Endocr-Relat Cancer 2007;14:907–933.
12. Russo IH, Russo J. Pregnancy-induced changes in breast cancer risk. J Mammary Gland Biol Neoplasia 2011;16:221–233.
13. Guzman RC, Yang J, Rajkumar L, Thordarson G, Chen X, Nandi S. Hormonal prevention of breast cancer: mimicking the protective effect of pregnancy. Proc Natl Acad Sci USA 1999;96:2520–2525.
14. Siwko SK, Dong J, Lewis MT, Liu H, Hilsenbeck SG, Li Y. Evidence that an early pregnancy causes a persistent decrease in the number of functional mammary epithelial stem cells. implications for pregnancy-induced protection against breast cancer. Stem Cells 2008;26:3205–3209.
15. D'Cruz CM, Moody SE, Master SR, Hartman JL, Keiper EA, Imielinski MB, Cox JD, Wang JY, Ha SI, Keister BA, Chodosh LA. Persistent parity-induced changes in growth factors, TGF-β 3, and differentiation in the rodent mammary gland. Mol Endocrinol 2002;16:2034–2051.
16. Blakely CM, Stoddard AJ, Belka GK, Dugan KD, Notarfrancesco KL, Moody SE, D'Cruz CM, Chodosh LA. Hormone-induced protection against mammary tumorigenesis is conserved in multiple rat strains and identifies a core gene expression signature induced by pregnancy. Cancer Res 2006;66:6421–6431.
17. Belitskaya-Levy I, Zeleniuch-Jacquotte A, Russo J, Russo IH, Bordas P, Ahman J, Afanasyeva Y, Johansson R, Lenner P, Li X, de Cicco RL, Peri S, Ross E, Russo PA, Santucci-Pereira J, Sheriff FS, Slifker M, Hallmans G, Toniolo P, Arslan AA. Characterization of a genomic signature of pregnancy identified in the breast. Cancer Prev Res 2011;4:1457–1464.
18. Anonymous. Breast cancer and breastfeeding: collaborative reanalysis of individual data from 47 epidemiological studies in 30 countries, including 50302 women with breast cancer and 96973 women without the disease. Lancet 2002;360:187–195.
19. Lof M, Hilakivi-Clarke L, Sandin SS, de Assis S, Yu W, Weiderpass E. Dietary fat intake and gestational weight gain in relation to estradiol and progesterone plasma levels during pregnancy: a longitudinal study in Swedish women. BMC Women's Health 2009;9:10.
20. Al-Atawi FS, Addar MH, Warsy AS, Babay ZA. Leptin concentration during different trimesters of pregnancy and its relation to other pregnancy hormones. Saudi Med J 2004;25: 1617–1622.
21. Sivan E, Whittaker PG, Sinha D, Homko CJ, Lin M, Reece EA, Boden G. Leptin in human pregnancy: the relationship with gestational hormones. Am J Obstet Gynecol 1998;179: 1128–1132.
22. Stock SM, Sande EM, Bremme KA. Leptin levels vary significantly during the menstrual cycle, pregnancy, and in vitro fertilization treatment: possible relation to estradiol. Fertil Steril 1999;72:657–662.
23. Tamura T, Goldenberg RL, Johnston KE, Cliver SP. Serum leptin concentrations during pregnancy and their relationship to fetal growth. Obstet Gynecol 1998;91:389–395.
24. Spicer DV, Pike MC. Sex steroids and breast cancer prevention. J Natl Cancer Inst Monogr 1994;16:139–147.
25. Clarke R, Dickson RB, Lippman ME. Hormonal aspects of breast cancer. Growth factors, drugs and stromal interactions. Crit Rev Oncol Hematol 1992;12:1–23.
26. Twombly R. Estrogen's dual nature ? Studies highlight effects on breast cancer. J Natl Cancer Inst 2011;103:920–921.
27. Ellis MJ, Gao F, Dehdashti F, Jeffe DB, Marcom PK, Carey LA, Dickler MN, Silverman P, Fleming GF, Kommareddy A, Jamalabadi-Majidi S, Crowder R, Siegel BA. Lower-dose vs high-dose oral estradiol therapy of hormone receptor-positive, aromatase inhibitor-resistant advanced breast cancer: a phase 2 randomized study. J Am Med Assoc 2009;302:774–780.
28. Ariazi EA, Cunliffe HE, Lewis-Wambi JS, Slifker MJ, Willis AL, Ramos P, Tapia C, Kim HR, Yerrum S, Sharma CG, Nicolas E, Balagurunathan Y, Ross EA, Jordan VC. Estrogen induces apoptosis in estrogen deprivation-resistant breast cancer through stress responses as identified by global gene expression across time. Proc Natl Acad Sci USA 2011;108:18879–18886.
29. LaCroix AZ, Chlebowski RT, Manson JE, Aragaki AK, Johnson KC, Martin L, Margolis KL, Stefanick ML, Brzyski R, Curb JD, Howard BV, Lewis CE, Wactawski-Wende J. Health outcomes after stopping conjugated equine estrogens among postmenopausal women with prior hysterectomy: a randomized controlled trial. J Am Med Assoc 2011;305:1305–1314.
30. Huggins C, Moon RC, Morii S. Extinction of experimental mammary cancer. I. Estradiol-17 β and progesterone. Proc Natl Acad Sci USA 1962;48:379–386.
31. Cabanes A, Wang M, Olivo S, de Assis S, Gustafsson JA, Khan G, Hilakivi-Clarke L. Prepubertal estradiol and genistein exposures up-regulate BRCA1 mRNA and reduce mammary tumorigenesis. Carcinogenesis 2004;25:741–748.
32. Grubbs CJ, Peckham JC, McDonough KD. Effect of ovarian hormones on the induction of l-methyl-l-nitrosourea-induced mammary cancer. Carcinogenesis 1983;4:495–497.
33. Sivaraman L, Stephens LC, Markaverich BM, Clark JA, Krnacik S, Conneely OM, O'Malley BW, Medina D. Hormone-induced refractoriness to mammary carcinogenesis in Wistar-Furth rats. Carcinogenesis 1998;19:1573–1581.
34. Grubbs CJ, Farneli DR, Hill DL, McDonough KC. Chemoprevention of N-nitro-N-methylurea-induced mammary cancers by pretreatment with 17 β-estradiol and progesterone. J Natl Cancer Inst 1985;74:927–931.
35. Rajkumar L, Guzman RC, Yang J, Thordarson G, Talamantes F, Nandi S. Short-term exposure to pregnancy levels of estrogen prevents mammary carcinogenesis. Proc Natl Acad Sci USA 2001;98:11755–11759.
36. Srivastava P, Russo J, Russo IH. Chorionic gonadotropin inhibits rat mammary carcinogenesis through activation of programmed cell death. Carcinogenesis 1997;18:1799–1808.
37. Beral V, Bull D, Doll R, Peto R, Reeves G. Breast cancer and abortion: collaborative reanalysis of data from 53 epidemiological studies, including 83,000 women with breast cancer from 16 countries. Lancet 2004;363:1007–1016.
38. Sinha DK, Pazik JE. Tumorigenesis of mammary gland by 7,12-dimethylbenz(α)anthracene during pregnancy: relationship with DNA synthesis. Int J Cancer 1981;27:807–810.
39. Laud K, Gourdou I, Pessemesse L, Peyrat JP, Djiane J. Identification of leptin receptors in human breast cancer: functional activity in the T47-D breast cancer cell line. Mol Cell Endocrinol 2002;188:219–226.
40. Laud K, Gourdou I, Bélair L, Keisler DH, Djiane J. Detection and regulation of leptin receptor mRNA in ovine mammary epithelial cells during pregnancy and lactation. FEBS Lett 1999;463:194–198.
41. O'Brien SN, Welter BH, Price TM. Presence of leptin in breast cell lines and breast tumors. Biochem Biophys Res Commun 1999;259:695–698.
42. Surmacz E. Obesity hormone leptin: a new target in breast cancer ? Breast Cancer Res 2007;9:301.
43. Petridou E, Papadiamantis Y, Markopoulos C, Spanos E, Dessypris N, Trichopoulos D. Leptin and insulin growth factor I in relation to breast cancer (Greece). Cancer Causes Control 2000;11:383–388.
44. Mantzoros CS, Bolhke K, Moschos S, Cramer DW. Leptin in relation to carcinoma in situ of the breast: a study of pre-menopausal cases and controls. Int J Cancer 1999;80:523–526.
45. Clapp JF 3rd, Schmidt S, Paranjape A, Lopez B. Maternal insulin-like growth factor-I levels (IGF-I) reflect placental mass and neonatal fat mass. Am J Obstet Gynecol 2004;190:730–736.
46. Chen T, Lukanova A, Grankvist K, Zeleniuch-Jacquotte A, Wulff M, Johansson R, Schock H, Lenner P, Hallmans G, Wadell G, Toniolo P, Lundin E. IGF-I during primiparous pregnancy and maternal risk of breast cancer. Breast Cancer Res Treat 2010;121:169–175.
47. Lukanova A, Toniolo P, Zeleniuch-Jacquotte A, Grankvist K, Wulff M, Arslan AA, Afanasyeva Y, Johansson R, Lenner P, Hallmans G, Wadell G, Lundin E. Insulin-like growth factor I in pregnancy and maternal risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2006;15:2489–2493.
48. Toriola AT, Lundin E, Schock H, Grankvist K, Pukkala E, Chen T, Zeleniuch-Jacquotte A, Toniolo P, Lehtinen M, Surcel HM, Lukanova A. Circulating insulin-like growth factor-I in pregnancy and maternal risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2011;20:1798–1801.
49. Jeffreys M, Northstone K, Holly J, Emmett P, Gunnell D. Levels of insulin-like growth factor during pregnancy and maternal cancer risk: a nested case-control study. Cancer Causes Control 2011;22:945–953.
50. Thordarson G, Slusher N, Leong H, Ochoa D, Rajkumar L, Guzman R, Nandi S, Talamantes F. Insulin-like growth factor (IGF)-I obliterates the pregnancy-associated protection against mammary carcinogenesis in rats: evidence that IGF-I enhances cancer progression through estrogen receptor-α activation via the mitogen-activated protein kinase pathway. Breast Cancer Res 2004;6:R423–36.
51. Lukanova A, Surcel HM, Lundin E, Kaasila M, Lakso HA, Schock H, Husing A, Kaaks R, Koskela P, Grankvist K, Pukkala E, Zeleniuch-Jacquotte A, Lehtinen M, Toniolo P. Circulating estrogens and progesterone during primiparous pregnancies and risk of maternal breast cancer. Int J Cancer 2012;130:910–920.
52. Cleary MP, Phillips FC. The presence of the “fa” gene in heterozygous (FA/fa) lean female rats, effects on body weight, body fat and serum leptin. Obes Res 1999;7:293–298.
53. de Assis S, Wang M, Goel S, Foxworth A, Helferich WG, Hilakivi-Clarke L. Excessive weight gain during pregnancy increases carcinogen-induced mammary tumorigenesis in Sprague-Dawley and lean and obese Zucker rats. J Nutr 2005;136:998–1004.
54. Russo J, Rivera R, Russo IH. Influence of age and parity on the development of the human breast. Breast Cancer Res Treat 1992;23:211–218.
55. Thordarson G, Jin E, Guzman RC, Swanson SM, Nandi S, Talamantes F. Refractoriness to mammary tumorigenesis in parous rats: is it caused by persistent changes in the hormonal environment or permanent biochemical alterations in the mammary epithelia ? Carcinogenesis 1995;16:2847–2853.
56. Misra Y, Bentley PA, Bond JP, Tighe S, Hunter T, Zhao FQ. Mammary gland morphological and gene expression changes underlying pregnancy protection of breast cancer tumorigenesis. Physiol Genomics 2012;44:76–88.
57. Sivaraman L, Conneely OM, Medina D, O'Malley BW. p53 is a potential mediator of pregnancy and hormone-induced resistance to mammary carcinogenesis. Proc Natl Acad Sci USA 2001;98:12379–12384.
58. Taipale J, Beachy PA. The Hedgehog and Wnt signalling pathways in cancer. Nature 2001;411:349–354.
59. Sharpless NE, DePinho RA. Telomeres, stem cells, senescence, and cancer. J Clin Invest 2004;113:160–168.
60. Paguirigan A, Beebe DJ, Liu B, Alexander C. Mammary stem and progenitor cells: tumour precursors ? Eur J Cancer 2006;42:1225–1236.
61. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nature 2006;439:84–88.
62. Smalley M, Ashworth A. Stem cells and breast cancer: a field in transit. Nat Rev Cancer 2003;3:832–844.
63. Ercan C, van Diest PJ, Vooijs M. Mammary development and breast cancer: the role of stem cells. Curr Mol Med 2011;11:270–285.
64. Britt KL, Kendrick H, Regan JL, Molyneux G, Magnay FA, Ashworth A, Smalley MJ. Pregnancy in the mature adult mouse does not alter the proportion of mammary epithelial stem/progenitor cells. Breast Cancer Res 2009;11:R20.
65. Tiede BJ, Owens LA, Li F, DeCoste C, Kang Y. A novel mouse model for non-invasive single marker tracking of mammary stem cells in vivo reveals stem cell dynamics throughout pregnancy. PLoS ONE 2009;4:e8035.
66. Boulanger CA, Wagner KU, Smith GH. Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-β 1 expression. Oncogene 2005;24:552–560.
67. Wagner KU, Smith GH. Pregnancy and stem cell behavior. J Mammary Gland Biol Neoplasia 2005;10:25–36.
68. Asztalos S, Gann PH, Hayes MK, Nonn L, Beam CA, Dai Y, Wiley EL, Tonetti DA. Gene expression patterns in the human breast after pregnancy. Cancer Prev Res 2010;3:301–311.
69. Balogh GA, Russo J, Mailo DA, Heulings R, Russo PA, Morrison P, Sheriff F, Russo IH. The breast of parous women without cancer has a different genomic profile compared to those with cancer. Int J Oncol 2007;31:1165–1175.
70. Wiseman BS, Werb Z. Stromal effects on mammary gland development and breast cancer. Science 2002;296:1046–1049.
71. Arendt LM, Rudnick JA, Keller PJ, Kuperwasser C. Stroma in breast development and disease. Semin Cell Dev Biol 2010;21:11–18.
72. Tlsty TD, Hein PW. Know thy neighbor: stromal cells can contribute oncogenic signals. Curr Opin Genet Dev 2001;11:54–59.
73. Yang J, Yoshizawa K, Nandi S, Tsubura A. Protective effects of pregnancy and lactation against N-methyl-N-nitrosourea-induced mammary carcinomas in female Lewis rats. Carcinogenesis 1999;20:623–628.
74. Medina D, Smith GH. Chemical carcinogen-induced tumorigenesis in parous, involuted mouse mammary glands. J Natl Cancer Inst 1999;91:967–969.
75. Nathanson KL, Wooster R, Weber BL. Breast cancer genetics: what we know and what we need. Nat Med 2001;7:552–556.
76. Jacinto FV, Esteller M. Mutator pathways unleashed by epigenetic silencing in human cancer. Mutagenesis 2007;22:247–253.
77. Fan S, Wang J-A, Yuan R, Ma Y, Meng Q, Erdos MR, Pestell RG, Yuan F, Auborn KJ, Goldberg ID, Rosen EM. BRCA1 inhibition of estrogen receptor signalling in transfected cells. Science 1999;284:1354–1356.
78. Deng CX. BRCA1: cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res 2006;34:1416–1426.
79. Furuta S, Jiang X, Gu B, Cheng E, Chen PL, Lee WH. Depletion of BRCA1 impairs differentiation but enhances proliferation of mammary epithelial cells. Proc Natl Acad Sci USA 2005;102:9176–9181.
80. de Assis S, Warri A, Benitez C, Helferich W, Hilakivi-Clarke L. Protective effects of prepubertal genistein exposure on mammary tumorigenesis are dependent on BRCA1 expression. Cancer Prev Res 2011;4:1436–1448.
81. Hilakivi-Clarke L, Forsen T, Eriksson JG, Luoto R, Tuomilehto J, Osmond C, Barker DJ. Tallness and overweight during childhood have opposing effects on breast cancer risk. Br J Cancer 2001;85:1680–1684.
82. Ahlgren M, Melbye M, Wohlfahrt J, Sørensen TI. Growth patterns and the risk of breast cancer in women. N Engl J Med 2004;351:1619–1626.
83. Warri A, Saarinen NM, Makela SI, Hilakivi-Clarke L. The role of early life genistein exposures in modifying breast cancer risk. Br J Cancer 2008;98:1485–1493.
84. Stensheim H, Møller B, van Dijk T, Foss a SD. Cause-specific survival for women diagnosed with cancer during pregnancy or lactation: a registry-based cohort study. J Clin Oncol 2009;27:45–51.
85. Murphy CG, Mallam D, Stein S, Patil S, Howard J, Sklarin N, Hudis CA, Gemignani ML, Seidman AD. Current or recent pregnancy is associated with adverse pathologic features but not impaired survival in early breast cancer. Cancer 2011.
86. Pilewskie M, Gorodinsky P, Fought A, Hansen N, Bethke K, Jeruss J, Scholtens D, Khan SA. Association between recency of last pregnancy and biologic subtype of breast cancer. Ann Surg Oncol 2011;19:1167–1173.
87. Azim Jr. HA, Botteri E, Renne G, Dell'orto P, Rotmensz N, Gentilini O, Sangalli C, Pruneri G, Di NB, Locatelli M, Sotiriou C, Piccart M, Goldhirsch A, Viale G, Peccatori FA. The biological features and prognosis of breast cancer diagnosed during pregnancy: a case-control study. Acta Oncol 2011.
88. Johansson AL, Andersson TM, Hsieh CC, Cnattingius S, Lambe M. Increased mortality in women with breast cancer detected during pregnancy and different periods postpartum. Cancer Epidemiol Biomarkers Prev 2011;20:1865–1872.
89. Colton T, Greenberg R, Noller K, Resseguie L, Van Bennekom C, Heeren T, Zhang Y. Breast cancer in mothers prescribed diethylstilbestrol in pregnancy. J Am Med Assoc 1993;269:2096–2100.
90. Peck JD, Hulka BS, Poole C, Savitz DA, Baird D, Richardson BE. Steroid hormone levels during pregnancy and incidence of maternal breast cancer. Cancer Epidemiol Biomarkers Prev 2002;11:361–368.
91. Kinnunen TI, Luoto R, Gissler M, Hemminki E, Hilakivi-Clarke L. Pregnancy weight gain and breast cancer risk. BMC Women's Health 2004;4:7–17.
92. Dawson SI. Long-term risk of malignant neoplasm associated with gestational glucose intolerance. Cancer 2004;100: 149–155.
93. Lawlor DA, Smith GD, Ebrahim S. Hyperinsulinaemia and increased risk of breast cancer: findings from the British Women's Heart and Health Study. Cancer Causes Control 2004;15:267–275.
94. Morisset AS, Tchernof A, Dube MC, Veillette J, Weisnagel SJ, Robitaille J. Weight gain measures in women with gestational diabetes mellitus. J Women's Health 2011;20:375–380.
95. Luke CJ, Silverman GA. Necrotic cell death: harnessing the Dark side of the Force in mammary gland involution. Nat Cell Biol 2011;13:197–199.
96. Faupel-Badger JM, Hoover RN, Potischman N, Roberts JM, Troisi R. Pregnancy weight gain is not associated with maternal or mixed umbilical cord estrogen and androgen concentrations. Cancer Causes Control 2009;20:263–267.
97. Festa A, Shnawa N, Krugluger W, Hopmeier P, Schernthaner G, Haffner SM. Relative hypoleptinaemia in women with mild gestational diabetes mellitus. Diabet Med 1999;16:656–662.
98. Kirwan JP, Hauguel-De Mouzon S, Lepercq J, Challier JC, Huston-Presley L, Friedman JE, Kalhan SC, Catalano PM. TNF-α is a predictor of insulin resistance in human pregnancy. Diabetes 2002;51:2207–2213.
99. Institute of Medicine. Weight gain during pregnancy: reexamining the guidelines. Consensus Report, May 28, 2009.
100. Althuizen E, van Poppel MN, Seidell JC, van Mechelen W. Correlates of absolute and excessive weight gain during pregnancy. J Women's Health 2009;18:1559–1566.
101. Dabelea D, Snell-Bergeon JK, Hartsfield CL, Bischoff KJ, Hamman RF, McDuffie RS. Increasing prevalence of gestational diabetes mellitus (GDM) over time and by birth cohort: Kaiser Permanente of Colorado GDM Screening Program. Diabetes Care 2005;28:579–584.
102. Gajewska M, Sobolewska A, Kozlowski M, Motyl T. Role of autophagy in mammary gland development. J Physiol Pharmacol 2008;59(Suppl 9):237–249.
103. Hilakivi-Clarke L, Onojafe I, Raygada M, Cho E, Clarke R, Lippman M. Breast cancer risk in rats fed a diet high in n-6 polyunsaturated fatty acids during pregnancy. J Natl Cancer Inst 1996;88:1821–1827.
104. de Assis S, Galam K, Hilakivi-Clarke L. High birth weight increases mammary tumorigenesis in rats. Int J Cancer 2006;119:1537–1546.
105. 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 1990;50: 5710–5719.
106. Moulder SL, Yakes FM, Muthuswamy SK, Bianco R, Simpson JF, Arteaga CL. Epidermal growth factor receptor (HER1) tyrosine kinase inhibitor ZD1839 (Iressa) inhibits HER2/neu (erbB2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res 2001;61:8887–8895.
107. Turner LB. A meta-analysis of fat intake, reproduction, and breast cancer risk: an evolutionary perspective. Am J Hum Biol 2011;23:601–608.
108. Murff HJ, Shu XO, Li H, Yang G, Wu X, Cai H, Wen W, Gao YT, Zheng W. Dietary polyunsaturated fatty acids and breast cancer risk in Chinese women: a prospective cohort study. Int J Cancer 2011;128:1434–1441.
109. Key TJ, Appleby PN, Cairns BJ, Luben R, Dahm CC, Akbaraly T, Brunner EJ, Burley V, Cade JE, Greenwood DC, Stephen AM, Mishra G, Kuh D, Keogh RH, White IR, Bhaniani A, Borgulya G, Mulligan AA, Khaw KT. Dietary fat and breast cancer: comparison of results from food diaries and food-frequency questionnaires in the UK Dietary Cohort Consortium. Am J Clin Nutr 2011;94:1043–1052.
110. Thiébaut AC, Chaj e s V, Gerber M, Boutron-Ruault MC, Joulin V, Lenoir G, Berrino F, Riboli E, Bénichou J, Clavel-Chapelon F. Dietary intakes of omega-6 and omega-3 polyunsaturated fatty acids and the risk of breast cancer. Int J Cancer 2009;124:924–931.
111. Klein V, Chajès V, Germain E, Schulgen G, Pinault M, Malvy D, Lefrancq T, Fignon A, Le Floch O, Lhuillery C, Bougnoux P. Low α-linolenic acid content of adipose breast tissue is associated with an increased risk of breast cancer. Eur J Cancer 2001;36:335–340.
112. Eid A, Berry EM. The relationship between dietary fat, adipose tissue composition, and neoplasms of the breast. Nutr Cancer 1988;11:173–177.
113. Caygill CP, Charlett A, Hill MJ. Fat, fish, fish oil and cancer. Br J Cancer 1996;74:159–164.
114. Olivo SE, Hilakivi-Clarke L. Opposing effects of prepubertal low and high fat n-3 polyunsaturated fatty acid diets on rat mammary tumorigenesis. Carcinogenesis 2005;26:1563–1572.
115. Catalano S, Mauro L, Marsico S, Giordano C, Rizza P, Rago V, Montanaro D, Maggiolini M, Panno ML, Ando S. Leptin induces, via ERK1/ERK2 signal, functional activation of estrogen receptor α in MCF-7 cells. J Biol Chem 2004;279:19908–19915.
116. Fusco R, Galgani M, Procaccini C, Franco R, Pirozzi G, Fucci L, Laccetti P, Matarese G. Cellular and molecular crosstalk between leptin receptor and estrogen receptor-{ α } in breast cancer: molecular basis for a novel therapeutic setting. Endocr-Relat Cancer 2010;17:373–382.
117. Tanentsapf I, Heitmann BL, Adegboye AR. Systematic review of clinical trials on dietary interventions to prevent excessive weight gain during pregnancy among normal weight, overweight and obese women. BMC Pregnancy Childbirth 2011;11:81.
118. Kinnunen TI, Pasanen M, Aittasalo M, Fogelholm M, Hilakivi-Clarke L, Weiderpass E, Luoto R. Preventing excessive weight gain during pregnancy. a controlled trial in primary health care. Eur J Clin Nutr 2007;61:884–891.
119. Luoto R, Kinnunen TI, Aittasalo M, Kolu P, Raitanen J, Ojala K, Mansikkam a ki K, Lamberg S, Vasankari T, Komulainen T, Tulokas S. Primary prevention of gestational diabetes mellitus and large-for-gestational-age newborns by lifestyle counseling: a cluster-randomized controlled trial. PLoS Med 2011;8:e1001036.
120. Kinnunen TI, Aittasalo M, Koponen P, Ojala K, Mansikkam a ki K, Weiderpass E, Fogelholm M, Luoto R. Feasibility of a controlled trial aiming to prevent excessive pregnancy-related weight gain in primary health care. BMC Pregnancy Childbirth 2008;8:37.
121. Balthazart J, Evrard L, Surlemont C. Effects of the nonsteroid inhibitor R76713 on testosterone-induced sexual behavior in the Japanese quail (Coturnix coturnix japonica). Horm Behav 1990;24:510–531.
122. Luoto R, Kharazmi E, Saarinen N, Smeds A, Raitanen J, Makela S, Hilakivi-Clarke L. Effect of dietary intervention on serum lignan concentrations among pregnant women. a controlled trial. Reprod Health 2010;7:26.
123. Engel SM, Levy B, Liu Z, Kaplan D, Wolff MS. Xenobiotic phenols in early pregnancy amniotic fluid. Reprod Toxicol 2006;21:110–112.
124. Adlercreutz H. Lignans and human health. Crit Rev Clin Lab Sci 2007;44:483–525.
125. Power KA, Saarinen NM, Chen JM, Thompson LU. 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.
126. Saarinen NM, Warri A, Airio M, Smeds A, Makela S. Role of dietary lignans in the reduction of breast cancer risk. Mol Nutr Food Res 2007;51:857–866.
127. Monks J, Smith-Steinhart C, Kruk ER, Fadok VA, Henson PM. Epithelial cells remove apoptotic epithelial cells during postlactation involution of the mouse mammary gland. Biol Reprod 2008;78:586–594.
128. Sandahl M, Hunter DM, Strunk KE, Earp HS, Cook RS. Epithelial cell-directed efferocytosis in the post-partum mammary gland is necessary for tissue homeostasis and future lactation. BMC Dev Biol 2010;10:122.
129. Lofgren KA, Ostrander JH, Housa D, Hubbard GK, Locatelli A, Bliss RL, Schwertfeger KL, Lange CA. Mammary gland specific expression of Brk/PTK6 promotes delayed involution and tumor formation associated with activation of p38 MAPK. Breast Cancer Res 2011;13:R89.
130. Schwertfeger KL, Richert MM, Anderson SM. Mammary gland involution is delayed by activated Akt in transgenic mice. Mol Endocrinol 2001;15:867–881.
131. Blanchard A, Shiu R, Booth S, Sorensen G, DeCorby N, Nistor A, Wong P, Leygue E, Myal Y. Gene expression profiling of early involuting mammary gland reveals novel genes potentially relevant to human breast cancer. Front Biosci 2007;12:2221–2232.
132. Zhao H, Huang M, Chen Q, Wang Q, Pan Y. Comparative gene expression analysis in mouse models for identifying critical pathways in mammary gland development. Breast Cancer Res Treat 2011.
133. Stein T, Morris JS, Davies CR, Weber-Hall SJ, Duffy MA, Heath VJ, Bell AK, Ferrier RK, Sandilands GP, Gusterson BA. Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3. Breast Cancer Res 2004;6:R75–91.
134. Hughes K, Wickenden JA, Allen JE, Watson CJ. Conditional deletion of Stat3 in mammary epithelium impairs the acute phase response and modulates immune cell numbers during post-lactational regression. J Pathol 2011.
135. Lyons TR, O'Brien J, Borges VF, Conklin MW, Keely PJ, Eliceiri KW, Marusyk A, Tan AC, Schedin P. Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat Med 2011;17:1109–1115.
136. Pagani O, Partridge A, Korde L, Badve S, Bartlett J, Albain K, Gelber R, Goldhirsch A. Pregnancy after breast cancer: if you wish, ma'am. Breast Cancer Res Treat 2011;129:309–317.
137. Azim Jr. HA, Peccatori FA, de AE, Piccart MJ. Motherhood after breast cancer: searching for la dolce vita. Expert Rev Anticancer Ther 2011;11:287–298.
138. Dalberg K, Eriksson J, Holmberg L. Birth outcome in women with previously treated breast cancer. a population-based cohort study from Sweden. PLoS Med 2006;3:e336.