Low-dose food contaminants trigger sex-specific, hepatic metabolic changes in the progeny of obese mice

FASEB Journal

Volumn 27, Issue 9, 2013, Pages 3860-3870

  Naville, Danielle ^a,b,c   Pinteur, Claudie ^a,b,c   Vega, Nathalie ^a,b,c   Menade, Yoan ^a,b,c   Vigier, Michèle ^a,b,c   Le Bourdais, Alexandre ^a,b,c   Labaronne, Emmanuel ^a,b,c   Debard, Cyrille ^a,b,c   Luquain Costaz, Céline ^a,b,c,d   Bégeot, Martine ^a,b,c   Vidal, Hubert ^a,b,c,d   Le Magueresse Battistoni, Brigitte ^a,b,c  

^a INSERM   (France)

^b CEMAGREF   (France)

^c UNIVERSITÉ LYON 1   (France)

^d Univ Lyon   (France)

Author keywords

BPA; Cholesterol biosynthesis; DEHP; Estrogen sulfotransferase; Persistent organic pollutant

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 4,4' ISOPROPYLIDENEDIPHENOL; CELL NUCLEUS RECEPTOR; CHOLESTEROL; CYTOCHROME P450 1A1; CYTOCHROME P450 4A; CYTOCHROME P450 4A14; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN SULFOTRANSFERASE; INSULIN; LEPTIN; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; POLYCHLORINATED BIPHENYL; POLYCHLORINATED BIPHENYL 153; TRANSCRIPTION FACTOR; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DISEASE EXACERBATION; ENZYME INDUCTION; ESTROGEN METABOLISM; EXPOSURE; FEMALE; FOOD CONTAMINATION; GENE EXPRESSION; GLUCOSE TOLERANCE; IMPAIRED GLUCOSE TOLERANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LEAN BODY WEIGHT; LIPID DIET; LIPID LIVER LEVEL; LIVER METABOLISM; MALE; METABOLIC DISORDER; METABOLIC PARAMETERS; MOUSE; NONHUMAN; OBESITY; POLLUTANT; PRIORITY JOURNAL; PROGENY; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TOXICITY TESTING; WEIGHT GAIN;

BPA; CHOLESTEROL BIOSYNTHESIS; DEHP; ESTROGEN SULFOTRANSFERASE; PERSISTENT ORGANIC POLLUTANT;

ANIMALS; BENZHYDRYL COMPOUNDS; BLOTTING, WESTERN; BODY WEIGHT; FEMALE; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; PHENOLS; POLYCHLORINATED BIPHENYLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TETRACHLORODIBENZODIOXIN;

EID: 84883377306     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-231670     Document Type: Article

References (58)

1. Friedman, J. M. (2000) Obesity in the new millennium. Nature 404, 632-634
2. Casals-Casas, C., and Desvergne, B. (2011) Endocrine disruptors: from endocrine to metabolic disruption. Annu. Rev. Physiol. 73, 135-162
3. Alonso-Magdalena, P., Quesada, I., and Nadal, A. (2011) Endocrine disruptors in the etiology of type 2 diabetes mellitus. Nat. Rev. 7, 346-353
4. Carpenter, D. O. (2008) Environmental contaminants as risk factors for developing diabetes. Rev. Environ. Health 23, 59-74
5. Diamanti-Kandarakis, E., Bourguignon, J. P., Giudice, L. C., Hauser, R., Prins, G. S., Soto, A. M., Zoeller, R. T., and Gore, A. C. (2009) Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr. Rev. 30, 293-342
6. Thayer, K. A., Heindel, J. J., Bucher, J. R., and Gallo, M. A. (2012) Role of environmental chemicals in diabetes and obesity: a national toxicology program workshop review. Environ. Health Perspect. 120, 779-789
7. Ibrahim, M. M., Fjaere, E., Lock, E. J., Naville, D., Amlund, H., Meugnier, E., Le Magueresse Battistoni, B., Froyland, L., Madsen, L., Jessen, N., Lund, S., Vidal, H., and Ruzzin, J. (2011) Chronic consumption of farmed salmon containing persistent organic pollutants causes insulin resistance and obesity in mice. PLoS One 6, e25170
8. Ruzzin, J., Petersen, R., Meugnier, E., Madsen, L., Lock, E. J., Lillefosse, H., Ma, T., Pesenti, S., Sonne, S. B., Marstrand, T. T., Malde, M. K., Du, Z. Y., Chavey, C., Fajas, L., Lundebye, A. K., Brand, C. L., Vidal, H., Kristiansen, K., and Froyland, L. (2010) Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ. Health Perspect. 118, 465-471
9. Schafer, K. S., and Kegley, S. E. (2002) Persistent toxic chemicals in the US food supply. J. Epidemiol. Commun. Health 56, 813-817
10. Koch, H. M., and Calafat, A. M. (2009) Human body burdens of chemicals used in plastic manufacture. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 2063-2078
11. Vandenberg, L. N., Hauser, R., Marcus, M., Olea, N., and Welshons, W. V. (2007) Human exposure to bisphenol A (BPA). Reprod. Toxicol. 24, 139-177
12. Silins, I., and Hogberg, J. (2011) Combined toxic exposures and human health: biomarkers of exposure and effect. Int. J. Environ. Res. Public Health 8, 629-647
13. Heindel, J. J., and vom Saal, F. S. (2009) Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity. Mol. Cell. Endocrinol. 304, 90-96
14. Dorne, J. L. (2010) Metabolism, variability and risk assessment. Toxicology 268, 156-164
15. Marmugi, A., Ducheix, S., Lasserre, F., Polizzi, A., Paris, A., Priymenko, N., Bertrand-Michel, J., Pineau, T., Guillou, H., Martin, P. G., and Mselli-Lakhal, L. (2011) Low doses of bisphenol A induce gene expression related to lipid synthesis and trigger triglyceride accumulation in adult mouse liver. Hepatology 55, 395-407
16. Vandenberg, L. N., Colborn, T., Hayes, T. B., Heindel, J. J., Jacobs, D. R., Jr., Lee, D. H., Shioda, T., Soto, A. M., Vom Saal, F. S., Welshons, W. V., Zoeller, R. T., and Myers, J. P. (2012) Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr. Rev. 33, 378-455
17. Lee, D. H., Lee, I. K., Song, K., Steffes, M., Toscano, W., Baker, B. A., and Jacobs, D. R., Jr. (2006) A strong dose-response relation between serum concentrations of persistent organic pollutants and diabetes: results from the National Health and Examination Survey 1999-2002. Diabetes Care 29, 1638-1644
18. Wei, J., Lin, Y., Li, Y., Ying, C., Chen, J., Song, L., Zhou, Z., Lv, Z., Xia, W., Chen, X., and Xu, S. (2011) Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology 152, 3049-3061
19. Wahlang, B., Falkner, K. C., Gregory, B., Ansert, D., Young, D., Conklin, D. J., Bhatnagar, A., McClain, C. J., and Cave, M. (2013) Polychlorinated biphenyl 153 is a diet-dependent obesogen that worsens nonalcoholic fatty liver disease in male C57BL6/J mice. [E-pub ahead of print] J. Nutr. Biochem. doi: 10.1016/j.jnutbio.2013.01.009
20. Moraes, R. C., Blondet, A., Birkenkamp-Demtroeder, K., Tirard, J., Orntoft, T. F., Gertler, A., Durand, P., Naville, D., and Begeot, M. (2003) Study of the alteration of gene expression in adipose tissue of diet-induced obese mice by microarray and reverse transcription-polymerase chain reaction analyses. Endocrinology 144, 4773-4782
21. European Food Safety Authority Panel on Food Additives, Flavourings, Processing Aids, and Materials in Contact with Food (2005) Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food (AFC) related to bis(2-ethylhexyl)phthalate (DEHP) for use in food contact materials. Question N° EFSA-Q-2003-191. EFSA J. 243, 1-20; doi: 10.2903/j.efsa.2005.243
22. Van Leeuwen, F. X., Feeley, M., Schrenk, D., Larsen, J. C., Farland, W., and Younes, M. (2000) Dioxins: WHO's tolerable daily intake (TDI) revisited. Chemosphere 40, 1095-1101
23. World Health Organization. (2003) Polychlorinated biphenyls: human health aspects. Concise International Chemical Assessment Document 55. World Heath Organization, Geneva, Switzerland
24. Beylot, M., Neggazi, S., Hamlat, N., Langlois, D., and Forcheron, F. (2012) Perilipin 1 ablation in mice enhances lipid oxidation during exercise and does not impair exercise performance. Metabolism 61, 415-423
25. Gout, J., Sarafian, D., Mutel, E., Vigier, M., Rajas, F., Mithieux, G., Begeot, M., and Naville, D. (2010) Metabolic and melanocortin gene expression alterations in male offspring of obese mice. Mol. Cell. Endocrinol. 319, 99-118
26. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
27. Pageaux, J. F., Bechoua, S., Bonnot, G., Fayard, J. M., Cohen, H., Lagarde, M., and Laugier, C. (1996) Biogenesis and metabolic fate of docosahexaenoic and arachidonic acids in rat uterine stromal cells in culture. Arch. Biochem. Biophys. 327, 142-150
28. Naville, D., Rebourcet, D., Chauvin, M. A., Vega, N., Jalabert, A., Vigier, M., Loizon, E., Begeot, M., and Le Magueresse-Battistoni, B. (2011) Direct and indirect impact of 2,3,7,8-tetrachlorodibenzo- p-dioxin (TCDD) on adult mouse Leydig cells: an in vitro study. Toxicol. Lett. 207, 251-257
29. Fromenty, B. (2013) Drug-induced liver injury in obesity. J. Hepatol. 58, 824-826
30. Zanger, U. M., and Schwab, M. (2013) Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol. Ther. 138, 103-141
31. Wagner, M., Zollner, G., and Trauner, M. (2011) Nuclear receptors in liver disease. Hepatology 53, 1023-1034
32. Martens, K., Ver Loren van Themaat, E., van Batenburg, M. F., Heinaniemi, M., Huyghe, S., Van Hummelen, P., Carlberg, C., Van Veldhoven, P. P., Van Kampen, A., and Baes, M. (2008) Coordinate induction of PPARα and SREBP2 in multifunctional protein 2 deficient mice. Biochim. Biophys. Acta 1781, 694-702
33. He, J., Lee, J. H., Febbraio, M., and Xie, W. (2011) The emerging roles of fatty acid translocase/CD36 and the aryl hydrocarbon receptor in fatty liver disease. Exp. Biol. Med. 236, 1116-1121
34. Zhao, C., and Dahlman-Wright, K. (2010) Liver X receptor in cholesterol metabolism. J. Endocrinol. 204, 233-240
35. Leiter, E. H., and Chapman, H. D. (1994) Obesity-induced diabetes (diabesity) in C57BL/KsJ mice produces aberrant trans-regulation of sex steroid sulfotransferase genes. J. Clin. Invest. 93, 2007-2013
36. Mauvais-Jarvis, F. (2011) Estrogen and androgen receptors: regulators of fuel homeostasis and emerging targets for diabetes and obesity. Trends Endocrinol. Metab. 22, 24-33
37. Zhou, X., Smith, A. M., Failla, M. L., Hill, K. E., and Yu, Z. (2012) Estrogen status alters tissue distribution and metabolism of selenium in female rats. J. Nutr. Biochem. 23, 532-538
38. Della Torre, S., Rando, G., Meda, C., Stell, A., Chambon, P., Krust, A., Ibarra, C., Magni, P., Ciana, P., and Maggi, A. (2011) Amino acid-dependent activation of liver estrogen receptor - integrates metabolic and reproductive functions via IGF-1. Cell Metab. 13, 205-214
39. Hevir, N., Ribic-Pucelj, M., and Lanisnik Rizner, T. (2013) Disturbed balance between phase I and II metabolizing enzymes in ovarian endometriosis: a source of excessive hydroxy-estrogens and ROS? Mol. Cell. Endocrinol. 367, 74-84
40. Gao, J., He, J., Shi, X., Stefanovic-Racic, M., Xu, M., O'Doherty, R. M., Garcia-Ocana, A., and Xie, W. (2012) Sex-specific effect of estrogen sulfotransferase on mouse models of type 2 diabetes. Diabetes 61, 1543-1551
41. Jacobsen, P. R., Axelstad, M., Boberg, J., Isling, L. K., Christiansen, S., Mandrup, K. R., Berthelsen, L. O., Vinggaard, A. M., and Hass, U. (2012) Persistent developmental toxicity in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reprod. Toxicol. 34, 237-250
42. Xi, W., Wan, H. T., Zhao, Y. G., Wong, M. H., Giesy, J. P., and Wong, C. K. (2011) Effects of perinatal exposure to bisphenol A and di(2-ethylhexyl)- phthalate on gonadal development of male mice. Environ. Sci. Pollut. Res. Int. 19, 2515-2527
43. Croutch, C. R., Lebofsky, M., Schramm, K. W., Terranova, P. F., and Rozman, K. K. (2005) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin (HxCDD) alter body weight by decreasing insulin-like growth factor I (IGF-I) signaling. Toxicol. Sci. 85, 560-571
44. Nault, R., Kim, S., and Zacharewski, T. R. (2013) Comparison of TCDD-elicited genome-wide hepatic gene expression in Sprague-Dawley rats and C57BL/6 mice. Toxicol. Appl. Pharmacol. 267, 184-191
45. Boutros, P. C., Yan, R., Moffat, I. D., Pohjanvirta, R., and Okey, A. B. (2008) Transcriptomic responses to 2,3,7,8-tetrachlorodibenzo- p-dioxin (TCDD) in liver: comparison of rat and mouse. BMC Genomics 9, 419
46. Baars, A. J., Bakker, M. I., Baumann, R. A., Boon, P. E., Freijer, J. I., Hoogenboom, L. A., Hoogerbrugge, R., van Klaveren, J. D., Liem, A. K., Traag, W. A., and de Vries, J. (2004) Dioxins, dioxin-like PCBs and non-dioxin-like PCBs in foodstuffs: occurrence and dietary intake in The Netherlands. Toxicol. Lett. 151, 51-61
47. Waxman, D. J., and Holloway, M. G. (2009) Sex differences in the expression of hepatic drug metabolizing enzymes. Mol. Pharmacol. 76, 215-228
48. Gao, H., Falt, S., Sandelin, A., Gustafsson, J. A., and Dahlman-Wright, K. (2008) Genome-wide identification of estrogen receptor alpha-binding sites in mouse liver. Mol. Endocrinol. 22, 10-22
49. Barros, R. P., Machado, U. F., and Gustafsson, J. A. (2006) Estrogen receptors: new players in diabetes mellitus. Trends Mol. Med. 12, 425-431
50. Riant, E., Waget, A., Cogo, H., Arnal, J. F., Burcelin, R., and Gourdy, P. (2009) Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 150, 2109-2117
51. Stubbins, R. E., Najjar, K., Holcomb, V. B., Hong, J., and Nunez, N. P. Oestrogen alters adipocyte biology and protects female mice from adipocyte inflammation and insulin resistance. Diabetes Obes. Metab. 14, 58-66
52. Mauvais-Jarvis, F. (2012) Estrogen sulfotransferase: intracrinology meets metabolic diseases. Diabetes 61, 1353-1354
53. Schug, T. T., Janesick, A., Blumberg, B., and Heindel, J. J. (2011) Endocrine disrupting chemicals and disease susceptibility. J. Steroid Biochem. Mol. Biol. 127, 204-215
54. Grün, F., and Blumberg, B. (2007) Perturbed nuclear receptor signaling by environmental obesogens as emerging factors in the obesity crisis. Rev. Endocr. Metab. Disord. 8, 161-171
55. Taxvig, C., Dreisig, K., Boberg, J., Nellemann, C., Schelde, A. B., Pedersen, D., Boergesen, M., Mandrup, S., and Vinggaard, A. M. (2012) Differential effects of environmental chemicals and food contaminants on adipogenesis, biomarker release and PPAR activation. Mol. Cell. Endocrinol. 361, 106-115
56. Nadal, A. (2013) Obesity: fat from plastics? Linking bisphenol A exposure and obesity. Nat. Rev. Endocrinol. 9, 9-10
57. Barker, D. J. (2005) The developmental origins of insulin resistance. Horm. Res. 64(Suppl. 3), 2-7
58. Barouki, R., Gluckman, P. D., Grandjean, P., Hanson, M., and Heindel, J. J. (2012) Developmental origins of non-communicable disease: implications for research and public health. Environ. Health 11, 42