Pubertal exposure to high fat diet causes mouse strain-dependent alterations in mammary gland development and estrogen responsiveness

International Journal of Obesity

Volumn 34, Issue 9, 2010, Pages 1415-1426

  Olson, L K ^a   Tan, Y ^a   Zhao, Y ^a   Aupperlee, M D ^a   Haslam, S Z ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

amphiregulin; estrogen; mammary gland; puberty

Indexed keywords

AMPHIREGULIN; ESTRADIOL;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; BODY WEIGHT; C57BL 6 MOUSE; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; ESTROGEN ACTIVITY; FEMALE; LIPID DIET; MAMMARY GLAND; MORPHOLOGY; MOUSE; NONHUMAN; OBESITY; ORGANOGENESIS; OVARIECTOMY; PRIORITY JOURNAL; PUBERTY; SIGNAL TRANSDUCTION; STIMULATION; WEIGHT REDUCTION;

ANIMALS; DIETARY FATS; ESTROGENS; FEMALE; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OBESITY; SEXUAL MATURATION;

MURINAE; MUS;

EID: 77956702041     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2010.51     Document Type: Article

References (50)

1. Rosenfield RL, Lipton RB, Drum ML. Thelarche, pubarche, and menarche attainment in children with normal and elevated body mass index. Pediatrics 2009; 123: 84-88.
2. Marchand L, Kolonel LN, Earle ME, Mi M-P. Body size at different periods of life and breast cancer risk. Am J Epidemiol 1988; 128: 137-152.
3. Magnusson C, Baron J, Persson I, Wolk A, Bergstrom R, Trichopoulos D et al. Body size in different periods of life and breast cancer risk in post-menopausal women. Int J Cancer 1998; 76: 29-34.
4. Berkey CS, Frazier AL, Gardner JD, Colditz GA. Adolescence and breast carcinoma risk. Cancer 1999; 85: 2400-2409.
5. Hilakivi-Clarke L, Forsen T, Eriksson JG, Luoto R, Tuomilehto J, Osmond C et al. Tallness and overweight during childhood have opposing effects on breast cancer risk. Br J Cancer 2001; 85: 1680-1684.
6. Ahlgren M, Melbye M, Wohlfahrt J, Sorensen TI. Growth patterns and the risk of breast cancer in women. N Engl J Med 2004; 351: 1619-1626.
7. Baer HJ, Colditz GA, Rosner B, Michels KB, Rich-Edwards JW, Hunter DJ et al. Body fatness during childhood and adolescence and incidence of breast cancer in premenopausal women: a prospective cohort study. Breast Cancer Res 2005; 7: R314-R325.
8. Garland M, Hunter DJ, Colditz GA, Manson JE, Stampfer MJ, Spiegelman D et al. Menstrual cycle characteristics and history of ovulatory infertility in relation to breast cancer risk in a large cohort of US women. Am J Epidemiol 1998; 147: 636-643.
9. Titus-Ernstoff L, Longnecker MP, Newcomb PA, Dain B, Greenberg ER, Mittendorf R et al. Menstrual factors in relation to breast cancer risk. Cancer Epidemiol Biomarkers Prev 1998; 7: 783-789. (Pubitemid 28420616)
10. Hannon TS, Rao G, Arslanian SA. Childhood obesity and type 2 diabetes mellitus. Pediatrics 2005; 116: 473-480.
11. Watson CJ, Khaled WT. Mammary development in the embryo and adult: a journey of morphogenesis and commitment. Development (Cambridge, England) 2008; 135: 995-1003.
12. Russo J, Russo IH. Biological and molecular bases of mammary carcinogenesis. Lab Invest 1987; 57: 112-137.
13. Welsch CW. Relationship between dietary fat and experimental mammary tumorigenesis: a review and critique. Cancer Res 1992; 52: 2040s-2048s.
14. Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman M. A maternal diet high in nF6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proc Natl Acad Sci USA 1997; 94: 9372-9377.
15. Hilakivi-Clarke L, Cho E, Cabanes A, DeAssis S, Olivo S, Helferich W et al. Dietary modulation of pregnancy estrogen levels and breast cancer risk among female rat offspring. Clin Cancer Res 2002; 8: 3601-3610.
16. Hilakivi-Clarke L, Stoica A, Raygada M, Martin MB. Consumption of a high-fat diet alters estrogen receptor content, protein kinase C activity, and mammary gland morphology in virgin and pregnant mice and female offspring. Cancer Res 1998; 58: 654-660.
17. Welsch CW, DeHoog JV, O'Connor DH, Sheffield LG. Influence of dietary fat levels on development and hormone responsiveness of the mouse mammary gland. Cancer Res 1985; 45: 6147-6154.
18. Welsch CW, O'Connor DH. Influence of the type of dietary fat on developmental growth of the mammary gland in immature and mature female BALB/c mice. Cancer Res 1989; 49: 5999-6007.
19. Kamikawa A, Ichii O, Yamaji D, Imao T, Suzuki C, Okamatsu-Ogura Y et al. Diet-induced obesity disrupts ductal development in the mammary glands of nonpregnant mice. Dev Dyn 2009; 238: 1092-1099.
20. Banerjee M, Wood B, Lin F, Crump L. Organ culture of whole mammary gland of the mouse. Tissue Cult Assoc Manual 1976; 2: 457-462.
21. Aupperlee MD, Smith KT, Kariagina A, Haslam SZ. Progesterone receptor isoforms A and B: temporal and spatial differences in expression during murine mammary gland development. Endocrinology 2005; 146: 3577-3588.
22. Yang C, Tan YS, Harkema JR, Haslam SZ. Differential effects of peripubertal exposure to perfluorooctanoic acid on mammary gland development in C57Bl/6 and Balb/c mouse strains. Reprod Toxicol 2009; 27: 299-306.
23. Aupperlee MD, Haslam SZ. Differential hormonal regulation and function of progesterone receptor isoforms in normal adult mouse mammary gland. Endocrinology 2007; 148: 2290-2300.
24. van Dierendonck JH, Wijsman JH, Keijzer R, van de Velde CJ, Cornelisse CJ. Cell-cycle-related staining patterns of anti-proliferating cell nuclear antigen monoclonal antibodies. Comparison with BrdUrd labeling and Ki-67 staining. Am J Pathol 1991; 138: 1165-1172.
25. Daniel CW, Silberstein GB, Strickland P. Direct action of 17 beta-estradiol on mouse mammary ducts analyzed by sustained release implants and steroid autoradiography. Cancer Res 1987; 47: 6052-6057.
26. Ciarloni L, Mallepell S, Brisken C. Amphiregulin is an essential mediator of estrogen receptor alpha function in mammary gland development. Proc Natl Acad Sci USA 2007; 104: 5455-5460.
27. Aupperlee MD, Drolet AA, Durairaj S, Wang W, Schwartz RC, Haslam SZ. Strain-specific differences in the mechanisms of progesterone regulation of murine mammary gland development. Endocrinology 2009; 150: 1485-1494.
28. Surwit RS, Feinglos MN, Rodin J, Sutherland A, Petro AE, Opara EC et al. Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J mice. Metab Clin Exp 1995; 44: 645-651.
29. Clee SM, Attie AD. The genetic landscape of type 2 diabetes in mice. Endocr Rev 2007; 28: 48-83.
30. Haramizu S, Nagasawa A, Ota N, Hase T, Tokimitsu I, Murase T. Different contribution of muscle and liver lipid metabolism to endurance capacity and obesity susceptibility of mice. J Appl Physiol 2009; 106: 871-879.
31. Silberstein GB, Van Horn K, Shyamala G, Daniel CW. Essential role of endogenous estrogen in directly stimulating mammary growth demonstrated by implants containing pure antiestrogens. Endocrinology 1994; 134: 84-90.
32. Korach KS, Couse JF, Curtis SW, Washburn TF, Lindzey J, Kimbro KS et al. Estrogen receptor gene disruption: molecular characterization and experimental and clinical phenotypes. Recent ProgHorm Res 1996; 51: 159-186; discussion 186-188.
33. Eckstein B, Golan R, Shani J. Onset of puberty in the immature female rat induced by 5-androstane-3 ,17-diol. Endocrinology 1973; 92: 941-945.
34. Sternlicht MD, Sunnarborg SW. The ADAM17-amphiregulin-EGFR axis in mammary development and cancer. J Mammary Gland Biol Neoplasia 2008; 13: 181-194.
35. McBryan J, Howlin J, Napoletano S, Martin F. Amphiregulin: role in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia 2008; 13: 159-169.
36. Hu X, Juneja SC, Maihle NJ, Cleary MP. LeptinFa growth factor in normal and malignant breast cells and for normal mammary gland development. J Natl Cancer Inst 2002; 94: 1704-1711.
37. Coleman DL, Hummel KP. Studies with the mutation, diabetes, in the mouse. Diabetologia 1967; 3: 238-248.
38. Barash IA, Cheung CC, Weigle DS, Ren H, Kabigting EB, Kuijper JL et al. Leptin is a metabolic signal to the reproductive system. Endocrinology 1996; 137: 3144-3147.
39. Silva LF, Etchebarne BE, Nielsen MS, Liesman JS, Kiupel M, VandeHaar MJ. Intramammary infusion of leptin decreases proliferation of mammary epithelial cells in prepubertal heifers. J Dairy Sci 2008; 91: 3034-3044.
40. Hadsell DL, Bonnette SG. IGF and insulin action in the mammary gland: lessons from transgenic and knockout models. J Mammary Gland Biol Neoplasia 2000; 5: 19-30.
41. Naylor MJ, Ormandy CJ. Mouse strain-specific patterns of mammary epithelial ductal side branching are elicited by stromal factors. Dev Dyn 2002; 225: 100-105.
42. Yant Y, Gusterson B, Kamalati T. Induction of strain-specific mouse mammary gland ductal architecture. Breast 1998; 7: 269-272.
43. Rasouli N, Kern PA. Adipocytokines and the metabolic complications of obesity. J Clin Endocrinol Metab 2008; 93: S64-S73.
44. Gouon-Evans V, Rothenberg ME, Pollard JW. Postnatal mammary gland development requires macrophages and eosinophils. Development 2000; 127: 2269-2282.
45. Wueest S, Rapold RA, Rytka JM, Schoenle EJ, Konrad D. Basal lipolysis, not the degree of insulin resistance, differentiates large from small isolated adipocytes in high-fat fed mice. Diabetologia 2009; 52: 541-546.
46. Hinck L, Silberstein GB. Key stages in mammary gland development: the mammary end bud as a motile organ. Breast Cancer Res 2005; 7: 245-251.
47. Rausch ME, Weisberg S, Vardhana P, Tortoriello DV. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obes (2005) 2008; 32: 451-463.
48. Trayhurn P, Wang B, Wood IS. Hypoxia and the endocrine and signalling role of white adipose tissue. Arch Physiol Biochem 2008; 114: 267-276.
49. Hilakivi-Clarke L. Nutritional modulation of terminal end buds: its relevance to breast cancer prevention. Curr Cancer Drug Targets 2007; 7: 465-474.
50. Oza AM, Boyd NF. Mammographic parenchymal patterns: a marker of breast cancer risk. Epidemiol Rev 1993; 15: 196-208.