Compensatory mammary growth following protein restriction during pregnancy and lactation increases early-onset mammary tumor incidence in rats

Carcinogenesis

Volumn 28, Issue 3, 2007, Pages 545-552

  Fernandez Twinn, D S ^c   Ekizoglou, S ^c   Gusterson, B A ^a   Luan, Jian'an ^b   Ozanne, S E ^c  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN; ESTROGEN RECEPTOR; GROWTH FACTOR; HORMONE RECEPTOR; INSULIN RECEPTOR; METHYLNITROSOUREA; SOMATOMEDIN C RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST DEVELOPMENT; CANCER INCIDENCE; CANCER RISK; CANCER SUSCEPTIBILITY; CELL ISOLATION; CELL LYSATE; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; LACTATION; MALE; MORPHOMETRICS; NONHUMAN; NUTRITION; PERINATAL PERIOD; PREGNANCY; PRIMORDIUM; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN RESTRICTION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; WISTAR RAT;

ANIMALS; ANIMALS, SUCKLING; BODY WEIGHT; BREAST NEOPLASMS; DISEASE SUSCEPTIBILITY; ESTRADIOL; FEMALE; HUMANS; LACTATION; MALE; MAMMARY NEOPLASMS, ANIMAL; NUTRITIONAL STATUS; PREGNANCY; RATS; RATS, WISTAR;

EID: 34047170361     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgl166     Document Type: Article

References (39)

1. Godfrey,K.M. and Barker,D.J. (2000) Fetal nutrition and adult disease. Am. J. Clin. Nutr., 71, 1344S-1352S.
2. Hales,C.N. and Barker,D.J. (2001) The thrifty phenotype hypothesis. Br. Med. Bull., 60, 5-20.
3. Leong,N.M., Mignone,L.I., Newcomb,P.A., Titus-Ernstoff,L., Baron,J.A., Trentham-Dietz,A., Stampfer,M.J., Willett,W.C. and Egan,K.M. (2003) Early life risk factors in cancer: The relation of birth weight to adult obesity. Int. J. Cancer, 103, 789-791.
4. Innes,K., Byers,T. and Schymura,M. (2000) Birth characteristics and subsequent risk for breast cancer in very young women. Am. J. Epidemiol., 152, 1121-1128.
5. Mellemkjaer,L., Olsen,M.L., Sorensen,H.T., Thulstrup,A.M., Olsen,J. and Olsen,J.H. (2003) Birth weight and risk of early-onset breast cancer (Denmark). Cancer Causes Control, 14, 61-64.
6. Sanderson,M., Williams,M.A., Malone,K.E., Stanford,J.L., Emanuel,I., White,E. and Daling,J.R. (1996) Perinatal factors and risk of breast cancer. Epidemiology, 7, 34-37.
7. de Assis,S., Khan,G. and Hilakivi-Clarke,L. (2006) High birth weight increases mammary tumorigenesis in rats. Int. J. Cancer, 119, 1537-1546.
8. Aerts,L. and Van Assche,F.A. (2003) Intra-uterine transmission of disease. Placenta, 24, 905-911.
9. Ravelli,A.C., van der Meulen,J.H., Michels,R.P., Osmond,C., Barker,D.J., Hales,C.N. and Bleker,O.P. (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet, 351, 173-177.
10. Forsen,T., Eriksson,J., Tuomilehto,J., Reunanen,A., Osmond,C. and Barker,D. (2000) The fetal and childhood growth of persons who develop type 2 diabetes. Ann. Intern. Med., 133, 176-182.
11. Kyle,U.G. and Pichard,C. (2006) The Dutch famine of 1944-1945: A pathophysiological model of long-term consequences of wasting disease. Curr. Opin. Clin. Nutr. Metab. Care, 9, 388-394.
12. Wolf,I., Sadetzki,S., Catane,R., Karasik,A. and Kaufman,B. (2005) Diabetes mellitus and breast cancer. Lancet Oncol., 6, 103-111.
13. Fernandez-Twinn,D.S., Wayman,A., Ekizoglou,S., Martin,M.S., Hales,C.N. and Ozanne,S.E. (2005) Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R368-R373.
14. Petry,C.J., Dorling,M.W., Pawlak,D.B., Ozanne,S.E. and Hales,C.N. (2001) Diabetes in old male offspring of rat dams fed a reduced protein diet. Int. J. Exp. Diabetes Res., 2, 139-143.
15. Ozanne,S.E. (2001) Metabolic programming in animals. Br. Med. Bull., 60, 143-152.
16. Ozanne,S.E. and Hales,C.N. (2004) Lifespan: Catch-up growth and obesity in male mice. Nature, 427, 411-412.
17. Fernandez-Twinn,D.S., Ozanne,S.E., Ekizoglou,S., Doherty,C., James,L., Gusterson,B. and Hales,C.N. (2003) The maternal endocrine environment in the low-protein model of intra-uterine growth restriction. Br. J. Nutr., 90, 815-822.
18. Ekbom,A., Trichopoulos,D., Adami,H.O., Hsieh,C.C. and Lan,S.J. (1992) Evidence of prenatal influences on breast cancer risk. Lancet, 340, 1015-1018.
19. Hilakivi-Clarke,L., Clarke,R. and Lippman,M. (1999) The influence of maternal diet on breast cancer risk among female offspring. Nutrition, 15, 392-401.
20. Trichopoulos,D. (2003) Intrauterine environment, mammary gland mass and breast cancer risk. Breast Cancer Res., 5, 42-44.
21. Snoeck,A., Remacle,C., Reusens,B. and Hoet,J.J. (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol. Neonate, 57, 107-118.
22. Imagawa,W., Tomooka,Y., Hamamoto,S. and Nandi,S. (1985) Stimulation of mammary epithelial cell growth in vitro: Interaction of epidermal growth factor and mammogenic hormones. Endocrinology, 116, 1514-1524.
23. Palmer,J.R., Wise,L.A., Hatch,E.E., Troisi,R., Titus-Ernstoff,L., Strohsnitter,W., Kaufman,R., Herbst,A.L., Noller,K.L., Hyer,M. and Hoover,R.N. (2006) Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol. Biomarkers Prev., 15, 1509-1514.
24. Li,S., Hursting,S.D., Davis,B.J., McLachlan,J.A. and Barrett,J.C. (2003) Environmental exposure, DNA methylation, and gene regulation: Lessons from diethylstilbesterol-induced cancers. Ann. NY Acad. Sci., 983, 161-169.
25. Lamartiniere,C.A., Luther,M.A., Lucier,G.W. and Illsley,N.P. (1982) Altered imprinting of rat liver monoamine oxidase by o, p'-DDT and methoxychlor. Biochem. Pharmacol., 31, 647-651.
26. Lamartiniere,C.A. and Pardo,G.A. (1988) Altered activation/detoxication enzymology following neonatal diethylstilbestrol treatment. J. Biochem. Toxicol., 3, 87-103.
27. Williams,J.A. and Phillips,D.H. (2000) Mammary expression of xenobiotic metabolizing enzymes and their potential role in breast cancer. Cancer Res., 60, 4667-4677.
28. Albanes,D. and Winick,M. (1988) Are cell number and cell proliferation risk factors for cancer? J. Natl Cancer Inst., 80, 772-774.
29. London,S.J., Connolly,J.L., Schnitt,S.J. and Colditz,G.A. (1992) A prospective study of benign breast disease and the risk of breast cancer. JAMA, 267, 941-944.
30. Ahlgren,M., Melbye,M., Wohlfahrt,J. and Sorensen,T.I. (2004) Growth patterns and the risk of breast cancer in women. N. Engl. J. Med., 351, 1619-1626.
31. McCormack,V.A., dos Santos Silva,I., De Stavola,B.L., Mohsen,R., Leon,D.A. and Lithell,H.O. (2003) Fetal growth and subsequent risk of breast cancer: Results from long term follow up of Swedish cohort. BMJ, 326, 248.
32. Tlsty,T.D., Crawford,Y.G., Holst,C.R., Fordyce,C.A., Zhang,J., McDermott,K., Kozakiewicz,K. and Gauthier,M.L. (2004) Genetic and epigenetic changes in mammary epithelial cells may mimic early events in carcinogenesis. J. Mammary Gland Biol. Neoplasia, 9, 263-274.
33. Park,C.S. (2005) Role of compensatory mammary growth in epigenetic control of gene expression. FASEB J., 19, 1586-1591.
34. Bonnette,S.G. and Hadsell,D.L. (2001) Targeted disruption of the IGF-I receptor gene decreases cellular proliferation in mammary terminal end buds. Endocrinology, 142, 4937-4945.
35. Carboni,J.M., Lee,A.V., Hadsell,D.L. et al. (2005) Tumor development by transgenic expression of a constitutively active insulin-like growth factor I receptor. Cancer Res., 65, 3781-3787.
36. Frittitta,L., Vigneri,R., Stampfer,M.R. and Goldfine,I.D. (1995) Insulin receptor overexpression in 184B5 human mammary epithelial cells induces a ligand-dependent transformed phenotype. J. Cell. Biochem., 57, 666-669.
37. Lee,A.V., Cui,X. and Oesterreich,S. (2001) Cross-talk among estrogen receptor, epidermal growth factor, and insulin-like growth factor signaling in breast cancer. Clin. Cancer Res., 7, 4429s-4435s, 4411s 4412s discussion.
38. Surmacz,E. and Bartucci,M. (2004) Role of estrogen receptor alpha in modulating IGF-I receptor signaling and function in breast cancer. J. Exp. Clin. Cancer Res., 23, 385-394.
39. Thorne,C. and Lee,A.V. (2003) Cross talk between estrogen receptor and IGF signaling in normal mammary gland development and breast cancer. Breast Dis., 17, 105-114.