Maternal dioxin exposure combined with a diet high in fat increases mammary cancer incidence in mice

Environmental Health Perspectives

Volumn 118, Issue 5, 2010, Pages 596-601

  la Merril, Michele ^a   Harper, Rachel ^a   Birnbaum, Linda S ^b,c   Cardiff, Robert D ^d   Threadgill, David W ^a,e  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

COMT; CYP1B1; Dioxin; High fat diet; Mammary cancer; Puberty. Environ health perspect

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CATECHOL METHYLTRANSFERASE; CYTOCHROME P450 1B1; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER INCIDENCE; CANCER RISK; CANCER SUSCEPTIBILITY; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; LIPID DIET; LOW FAT DIET; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; CATECHOL O-METHYLTRANSFERASE; COCARCINOGENESIS; DIETARY FATS; ENVIRONMENTAL POLLUTANTS; ESTROGENS, NON-STEROIDAL; FEMALE; GENE EXPRESSION; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS; TETRACHLORODIBENZODIOXIN;

MUS;

EID: 77951741901     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.0901047     Document Type: Article

References (62)

1. Alnouti Y, Klaassen CD. 2008. Tissue distribution, ontogeny, and regulation of aldehyde dehydrogenase (Aldh) enzymes mRNA by prototypical microsomal enzyme inducers in mice. Toxicol Sci 101(1):51-64.
2. Barbacioru CC, Wang Y, Canales RD, Sun YA, Keys DN, Chan F, et al. 2006. Effect of various normalization methods on Applied Biosystems expression array system data. BMC Bioinformatics 7:533; doi:10.1186/1471-2105-7-533 [Online 15 December 2006].
3. Birnbaum LS, Fenton SE. 2003. Cancer and developmental exposure to endocrine disruptors. Environ Health Perspect 111:389-394.
4. Bolton JL, Thatcher GR. 2008. Potential mechanisms of estrogen quinone carcinogenesis. Chem Res Toxicol 21(1):93-101.
5. Brown NM, Manzolillo PA, Zhang JX, Wang J, Lamartiniere CA. 1998. Prenatal TCDD and predisposition to mammary cancer in the rat. Carcinogenesis 19(9):1623-1629.
6. Budzowska M, Kanaar R. 2009. Mechanisms of dealing with DNA damage-induced replication problems. Cell Biochem Biophys 53(1):17-31.
7. Cavalieri EL, Rogan EG. 2004. A unifying mechanism in the initiation of cancer and other diseases by catechol quinones. Ann NY Acad Sci 1028:247-257.
8. Cavalieri EL, Stack DE, Devanesan PD, Todorovic R, Dwivedy I, Higginbotham S, et al. 1997. Molecular orgin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc Natl Acad Sci USA 94:10937-10942.
9. Chakravarti D, Mailander PC, Li KM, Higginbotham S, Zhang HL, Gross ML, et al. 2001. Evidence that a burst of DNA depurination in SENCAR mouse skin induces error-prone repair and forms mutations in the H-ras gene. Oncogene 20(55):7945-7953.
10. Currier N, Solomon SE, Demicco EG, Chang DL, Farago M, Ying H, et al. 2005. Oncogenic signaling pathways activated in DMBA-induced mouse mammary tumors. Toxicol Pathol 33(6):726-737.
11. De Assis S, Hilakivi-Clarke L. 2006. Timing of dietary estrogenic exposures and breast cancer risk. Ann NY Acad Sci 1089:14-35.
12. Dedieu S, Langlois B, Devy J, Sid B, Henriet P, Sartelet H, et al. 2008. LRP-1 silencing prevents malignant cell invasion despite increased pericellular proteolytic activities. Mol Cell Biol 28(9):2980-2995.
13. Den Hond E, Roels HA, Hoppenbrouwers K, Nawrot T, Thijs L, Vandermeulen C, et al. 2002. Sexual maturation in relation to polychlorinated aromatic hydrocarbons: Sharpe and Skakkebaek's hypothesis revisited. Environ Health Perspect 110:771-776.
14. Desaulniers D, Leingartner K, Russo J, Perkins G, Chittim BG, Archer MC, et al. 2001. Modulatory effects of neonatal exposure to TCDD, or a mixture of PCBs, p,p'-DDT, and p,p'-DDE, on methylnitrosourea-induced mammary tumor development in the rat. Environ Health Perspect 109:739-747.
15. Desaulniers D, Xiao GH, Leingartner K, Chu I, Musicki B, Tsang BK. 2005. Comparisons of brain, uterus, and liver mRNA expression for cytochrome p450s, DNA methyltransferase-1, and catechol-o-methyltransferase in prepubertal female Sprague-Dawley rats exposed to a mixture of aryl hydrocarbon receptor agonists. Toxicol Sci 86(1):175-184.
16. Dolinoy DC, Huang D, Jirtle RL. 2007. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci USA 104(32):13056-13061.
17. Dunn BK, Wickerham DL, Ford LG. 2005. Prevention of hormone-related cancers: breast cancer. J Clin Oncol 23(2):357-367.
18. Emond C, Birnbaum LS, DeVito MJ. 2006. Use of a physiologically based pharmacokinetic model for rats to study the influence of body fat mass and induction of CYP1A2 on the pharmacokinetics of TCDD. Environ Health Perspect 114:1394-1400.
19. Eriksson AL, Suuriniemi M, Mahonen A, Cheng S, Ohlsson C. 2005. The COMT val158met polymorphism is associated with early pubertal development, height and cortical bone mass in girls. Pediatr Res 58(1):71-77.
20. Fenton SE, Hamm JT, Birnbaum LS, Youngblood GL. 2002. Persistent abnormalities in the rat mammary gland following gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Sci 67(1):63-74.
21. Harrad S, Wang Y, Sandaradura S, Leeds A. 2003. Human dietary intake and excretion of dioxin-like compounds. J Environ Monit 5(2):224-228.
22. Hilakivi-Clarke L, Cho E, Onojafe I, Liao DJ, Clarke R. 2000. Maternal exposure to tamoxifen during pregnancy increases carcinogen-induced mammary tumorigenesis among female rat offspring. Clin Cancer Res 6(1):305-308.
23. Hilakivi-Clarke L, Cho E, Onojafe I, Raygada M, Clarke R. 1999. Maternal exposure to genistein during pregnancy increases carcinogen-induced mammary tumorigenesis in female rat offspring. Oncol Rep 6(5):1089-1095.
24. Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman M. 1997. 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 94(17):9372-9377.
25. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. 2006. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 66(11):5624-5632.
26. Hofmann SM, Zhou L, Perez-Tilve D, Greer T, Grant E, Wancata L, et al. 2007. Adipocyte LDL receptor-related protein-1 expression modulates postprandial lipid transport and glucose homeostasis in mice. J Clin Invest 117(11):3271-3282.
27. Holcomb M, Safe S. 1994. Inhibition of 7,12-dimethylbenzanthracene-induced rat mammary tumor growth by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Cancer Lett 82(1):43-47.
28. Hooper K, Petreas MX, Chuvakova T, Kazbekova G, Druz N, Seminova G, et al. 1998. Analysis of breast milk to assess exposure to chlorinated contaminants in Kazakstan: high levels of 2,3,7, 8-tetrachlorodibenzo-p-dioxin (TCDD) in agricultural villages of southern Kazakstan. Environ Health Perspect 106:797-806.
29. Inoue K, Tice LW, Creveling CR. 1980. Immunocytochemical localization of catechol-O-methyltransferase in the pregnant rat uterus. Endocrinology 107(6):1833-1840.
30. Justenhoven C, Hamann U, Schubert F, Zapatka M, Pierl CB, Rabstein S, et al. 2007. Breast cancer: a candidate gene approach across the estrogen metabolic pathway. Breast Cancer Res Treat 108(1):137-149.
31. Kocabas NA, Sardas S, Cholerton S, Daly AK, Elhan AH, Karakaya AE. 2005. Genetic polymorphism of manganese superoxide dismutase (MnSOD) and breast cancer susceptibility. Cell Biochem Funct 23(1):73-76.
32. Kocabas NA, Sardas S, Cholerton S, Daly AK, Karakaya AE. 2002. Cytochrome P450 CYP1B1 and catechol O-methyltransferase (COMT) genetic polymorphisms and breast cancer susceptibility in a Turkish population. Arch Toxicol 76(11):643-649.
33. La Merrill M, Baston DS, Denison MS, Birnbaum LS, Pomp D, Threadgill DW. 2009a. Mouse breast cancer model-dependent changes in metabolic syndrome-associated phenotypes caused by maternal dioxin exposure and dietary fat. Am J Physiol Endocrinol Metab 296(1):E203-E210.
34. La Merrill M, Kuruvilla BS, Pomp D, Birnbaum LS, Threadgill DW. 2009b. Dietary fat alters body composition, mammary development and P450 induction following maternal TCDD exposure in DBA/2J mice with low responsive aryl hydrocarbon receptors. Environ Health Perspect 117:1414-1419.
35. Leijs MM, Koppe JG, Olie K, van Aalderen WM, Voogt P, Vulsma T, et al. 2008. Delayed initiation of breast development in girls with higher prenatal dioxin exposure; a longitudinal cohort study. Chemosphere 73(6):999-1004.
36. Le Marchand L, Donlon T, Kolonel LN, Henderson BE, Wilkens LR. 2005. Estrogen metabolism-related genes and breast cancer risk: the multiethnic cohort study. Cancer Epidemiol Biomarkers Prev 14(8):1998-2003.
37. Li S, Washburn KA, Moore R, Uno T, Teng C, Newbold RR, et al. 1997. Developmental exposure to diethylstilbestrol elicits demethylation of estrogen-responsive lactoferrin gene in mouse uterus. Cancer Res 57(19):4356-4359.
38. Ling S, Pi X, Holoshitz J. 2007. The rheumatoid arthritis shared epitope triggers innate immune signaling via cell surface calreticulin. J Immunol 179(9):6359-6367.
39. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402-408.
40. Lorincz AM, Sukumar S. 2006. Molecular links between obesity and breast cancer. Endocr Relat Cancer 13(2):279-292.
41. McGrath M, Hankinson SE, Arbeitman L, Colditz GA, Hunter DJ, De Vivo I. 2004. Cytochrome P450 1B1 and catechol-O-methyltransferase polymorphisms and endometrial cancer susceptibility. Carcinogenesis 25(4):559-565.
42. Michalek JE, Tripathi RC. 1999. Pharmacokinetics of TCDD in veterans of Operation Ranch Hand: 15-year follow-up. J Toxicol Environ Health A 57(6):369-378.
43. Mitrunen K, Hirvonen A. 2003. Molecular epidemiology of sporadic breast cancer. The role of polymorphic genesinvolved in oestrogen biosynthesis and metabolism. Mutat Res 544(1):9-41.
44. Mitrunen K, Jourenkova N, Kataja V, Eskelinen M, Kosma VM, Benhamou S, et al. 2001. Polymorphic catechol-O-methyltransferase gene and breast cancer risk. Cancer Epidemiol Biomarkers Prev 10(6):635-640.
45. Nock NL, Cicek MS, Li L, Liu X, Rybicki BA, Moreira A, et al. 2006. Polymorphisms in estrogen bioactivation, detoxification and oxidative DNA base excision repair genes and prostate cancer risk. Carcinogenesis 27(9):1842-1848.
46. Pitroda SP, Khodarev NN, Beckett MA, Kufe DW, Weichselbaum RR. 2009. MUC1-induced transcriptional programs associated with tumorigenesis predict outcome in breast and lung cancer. Cancer Res 69(7):2833-2837.
47. Prins GS, Tang WY, Belmonte J, Ho SM. 2008. Perinatal exposure to oestradiol and bisphenol A alters the prostate epigenome and increases susceptibility to carcinogenesis. Basic Clin Pharmacol Toxicol 102(2):134-138.
48. Rosner A, Miyoshi K, Landesman-Bollag E, Xu X, Seldin DC, Moser AR, et al. 2002. Pathway pathology: histological differences between ErbB/Ras and Wnt pathway transgenic mammary tumors. Am J Pathol 161(3):1087-1097.
49. Russo IH, Russo J. 1978. Developmental stage of the rat mammary gland as determinant of its susceptibility to 7,12-dimethylbenz[a]anthracene. J Natl Cancer Inst 61(6):1439-1449.
50. Sata F, Yamada H, Suzuki K, Saijo Y, Yamada T, Minakami H, et al. 2006. Functional maternal catechol-O-methyltransferase polymorphism and fetal growth restriction. Pharmacogenet Genomics 16(11):775-781.
51. Sellers TA, Schildkraut JM, Pankratz VS, Vierkant RA, Fredericksen ZS, Olson JE, et al. 2005. Estrogen bioactivation, genetic polymorphisms, and ovarian cancer. Cancer Epidemiol Biomarkers Prev 14(111):2536-2543.
52. Simpson ER. 2003. Sources of estrogen and their importance. J Steroid Biochem Mol Biol 86(3-5):225-230.
53. Syed HA, Threadgill DW. 2006. Enhanced oligonucleotide microarray labeling and hybridization. Biotechniques 41(6):685-686.
54. Thompson PA, Shields PG, Freudenheim JL, Stone A, Vena JE, Marshall JR, et al. 1998. Genetic polymorphisms in catechol-O-methyltransferase, menopausal status, and breast cancer risk. Cancer Res 58(10):2107-2110.
55. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98(9):5116-5121.
56. Vihko R, Apter D. 1984. Endocrine characteristics of adolescent menstrual cycles: impact of early menarche. J Steroid Biochem 20(1):231-236.
57. Warner M, Eskenazi B, Mocarelli P, Gerthoux PM, Samuels S, Needham L, et al. 2002. Serum dioxin concentrations and breast cancer risk in the Seveso Women's Health Study. Environ Health Perspect 110:625-628.
58. Wen W, Ren Z, Shu XO, Cai Q, Ye C, Gao YT, et al. 2007. Expression of cytochrome P450 1B1 and catechol-O-methyltransferase in breast tissue and their associations with breast cancer risk. Cancer Epidemiol Biomarkers Prev 16(5):917-920.
59. Wilson KS, Roberts H, Leek R, Harris AL, Geradts J. 2002. Differential gene expression patterns in HER2/neu-positive and -negative breast cancer cell lines and tissues. Am J Pathol 161(4):1171-1185.
60. Yager JD, Davidson NE. 2006. Estrogen carcinogenesis in breast cancer. N Engl J Med 354(3):270-282.
61. Yang YH, Thorne NP. 2003. Normalization for two-color cDNA microarray data. In: Statistics and Science: A Festschrift for Terry Speed (Goldstein DR, ed). Beachwood, OH:Institute of Mathematical Statistics, 403-418.
62. Zimarina TC, Kristensen VN, Imianitov EN, Bershtein LM. 2004. [Polymorphisms of CYP1B1 and COMT in breast and endometrial cancer] [in Russian]. Mol Biol (Mosk) 38(3):386-393.