Bisphenol A diglycidyl ether induces adipogenic differentiation of multipotent stromal stem cells through a peroxisome proliferator-activated receptor gamma-independent mechanism

Environmental Health Perspectives

Volumn 120, Issue 7, 2012, Pages 984-989

  Chamorro García, Raquel ^a   Kirchner, Séverine ^a   Li, Xia ^a   Janesick, Amanda ^a   Casey, Stephanie C ^a   Chow, Connie ^a   Blumberg, Bruce ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adipogenesis; BADGE; BPA; Endocrine disruption; MSCs; Obesogen; PPAR

Indexed keywords

2,2 BIS(4 GLYCIDYLOXYPHENYL)PROPANE; 4, 4' ISOPROPYLIDENEDIPHENOL; CELL NUCLEUS RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RETINOID X RECEPTOR; UNCLASSIFIED DRUG;

ADIPOGENESIS; ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; MESENCHYMAL STROMA CELL; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

3T3-L1 CELLS; ADIPOGENESIS; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EPOXY COMPOUNDS; FLOW CYTOMETRY; HUMANS; MICE; MULTIPOTENT STEM CELLS; POLYMERASE CHAIN REACTION; PPAR GAMMA;

EID: 84864120419     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1205063     Document Type: Article

References (60)

1. Avram MM, Avram AS, James WD. 2007. Subcutaneous fat in normal and diseased states 3. Adipogenesis: from stem cell to fat cell. J Am Acad Dermatol 56(3):472-492.
2. Biedermann M, Grob K. 1998. Food contamination from epoxy resins and organosols used as can coatings: analysis by gradient NPLC. Food Addit Contam 15(5):609-618.
3. Bishop-Bailey D, Hla T, Warner TD. 2000. Bisphenol A diglycidyl ether (BADGE) is a PPARgagonist in an ECV304 cell line. Br J Pharmacol 131(4):651-654.
4. Cabado AG, Aldea S, Porro C, Ojea G, Lago J, Sobrado C, et al. 2008. Migration of BADGE (bisphenol A diglycidyl-ether) and BFDGE (bisphenol F diglycidyl-ether) in canned seafood. Food Chem Toxicol 46(5):1674-1680.
5. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. 2008. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect 116:39-44.
6. Cao XL, Dufresne G, Clement G, Belisle S, Robichaud A, Beraldin F. 2009. Levels of bisphenol A diglycidyl ether (BADGE) and bisphenol F diglycidyl ether (BFDGE) in canned liquid infant formula products in Canada and dietary intake estimates. J AOAC Int 92(6):1780-1789.
7. 14C-DGEBPA. Xenobiotica 11(6):401-424.
8. Dhurandhar NV. 2004. Contribution of pathogens in human obesity. Drug News Perspect 17(5):307-313.
9. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, et al. 2009. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30(4):293-342.
10. Dix DJ, Houck KA, Martin MT, Richard AM, Setzer RW, KavlockRJ. 2007. The ToxCast program for prioritizing toxicity testing of environmental chemicals. Toxicol Sci 95(1):5-12.
11. Ebisawa M, Umemiya H, Ohta K, Fukasawa H, Kawachi E, Christoffel G, et al. 1999. Retinoid X receptor-antagonistic diazepinylbenzoic acids. Chem Pharm Bull (Tokyo) 47(12):1778-1786.
12. Environmental Working Group. 2005. Human Toxome Project: EWG Study #6, consumer product chemicals in mothers and daughters. Available: http://www.ewg.org/sites/humantoxome/participants/participant-group.php? group=rn [accessed 22 November 2010].
13. European Commission. 2002. Commission Directive 2002/16/EC. 20 February 2002. On the use of certain epoxy derivatives in materials and articles intended to come into contact with foodstuffs. Off J Eur Comm L151:27-31.
14. Fehlberg S, Trautwein S, Goke A, Goke R. 2002. Bisphenol A diglycidyl ether induces apoptosis in tumour cells independently of peroxisome proliferator-activated receptor-gamma, in caspase-dependent and-independent manners. Biochem J 362(pt 3):573-578.
15. Garruti G, Cotecchia S, Giampetruzzi F, Giorgino F, Giorgino R. 2008. Neuroendocrine deregulation of food intake, adipose tissue and the gastrointestinal system in obesity and metabolic syndrome. J Gastrointestin Liver Dis 17(2):193-198.
16. Grun F, Watanabe H, Zamanian Z, Maeda L, Arima K, CubachaR, et al. 2006. Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Mol Endocrinol 20(9):2141-2155.
17. Hammarling L, Gustavsson H, Svensson K, Oskarsson A. 2000. Migration of bisphenol-A diglycidyl ether (BADGE) and its reaction products in canned foods. Food Addit Contam 17(11):937-943.
18. Herbert A. 2008. The fat tail of obesity as told by the genome. Curr Opin Clin Nutr Metab Care 11(4):366-370.
19. Hill JO, Peters JC. 1998. Environmental contributions to the obesity epidemic. Science 280(5368):1371-1374.
20. Holmes MJ, Hart A, Northing P, Oldring PK, Castle L, Stott D, et al. 2005. Dietary exposure to chemical migrants from food contact materials: a probabilistic approach. Food Addit Contam 22(10):907-919.
21. Hyoung UJ, Yang YJ, Kwon SK, Yoo JH, Myoung SC, Kim SC, et al. 2007. Developmental toxicity by exposure to bisphenol A diglycidyl ether during gestation and lactation period in Sprague-Dawley male rats. J Prev Med Public Health 40(2):155-161.
22. Janesick A, Blumberg B. 2011. Endocrine disrupting chemicals and the developmental programming of adipogenesis and obesity. Birth Defects Res C Embryo Today 93(1):34-50.
23. Joskow R, Barr DB, Barr JR, Calafat AM, Needham LL, Rubin C. 2006. Exposure to bisphenol A from bis-glycidyl dimethacrylate-based dental sealants. J Am Dent Assoc 137(3):353-362.
24. Kirchner S, Kieu T, Chow C, Casey S, Blumberg B. 2010. Prenatal exposure to the environmental obesogen tributyltin predisposes multipotent stem cells to become adipocytes. Mol Endocrinol 24(3):526-539.
25. La Merrill M, Birnbaum LS. 2011. Childhood obesity and environmental chemicals. Mt Sinai J Med 78(1):22-48.
26. Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M, Wallace RB, et al. 2008. Association of urinary bisphenolA concentration with medical disorders and laboratory abnormalities in adults. JAMA 300(11):1303-1310.
27. Li X, Ycaza J, Blumberg B. 2011. The environmental obesogen tributyltin chloride acts via peroxisome proliferator activated receptor gamma to induce adipogenesis in murine 3T3-L1 preadipocytes. J Steroid Biochem Mol Biol 127(1-2):9-15.
28. ΔΔCTMethod. Methods 25(4):402-408.
29. Mantena SK, King AL, Andringa KK, Eccleston HB, Bailey SM. 2008. Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol-and obesity-induced fatty liver diseases. Free Radic Biol Med 44(7):1259-1272.
30. Masuno H, Iwanami J, Kidani T, Sakayama K, Honda K. 2005. Bisphenol A accelerates terminal differentiation of 3T3-L1 cells into adipocytes through the phosphatidylinositol 3-kinase pathway. Toxicol Sci 84(2):319-327.
31. Milnes MR, Garcia A, Grossman E, Grun F, Shiotsugu J, TabbMM, et al. 2008. Activation of steroid and xenobio-tic receptor (SXR, NR1I2) and its orthologs in laboratory, toxicologic, and genome model species. Environ Health Perspect 116:880-885.
32. Miyawaki J, Sakayama K, Kato H, Yamamoto H, Masuno H. 2007. Perinatal and postnatal exposure to bisphenolA increases adipose tissue mass and serum cholesterol level in mice. J Atheroscler Thromb 14(5):245-252.
33. Nakamuta M, Enjoji M, Uchimura K, Ohta S, Sugimoto R, KotohK, et al. 2002. Bisphenol A diglycidyl ether (BADGE) suppresses tumor necrosis factor-aproduction as a PPARgagonist in the murine macrophage-like cell line, RAW 264.7. Cell Biol Int 26(3):235-241.
34. Nakazawa H, Yamaguchi A, Inoue K, Yamazaki T, Kato K, Yoshimura Y, et al. 2002. In vitro assay of hydrolysis and chlorohydroxy derivatives of bisphenol A diglycidyl ether for estrogenic activity. Food Chem Toxicol 40(12):1827-1832.
35. Nunez AA, Kannan K, Giesy JP, Fang J, Clemens LG. 2001. Effects of bisphenol A on energy balance and accumulation in brown adipose tissue in rats. Chemosphere 42(8):917-922.
36. Olea N, Pulgar R, Perez P, Olea-Serrano F, Rivas A, Novillo-Fertrell A, et al. 1996. Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 104:298-305.
37. Poole A, van Herwijnen P, Weideli H, Thomas MC, Ransbotyn G, Vance C. 2004. Review of the toxicology, human exposure and safety assessment for bisphenol A diglycidylether (BADGE). Food Addit Contam 21(9):905-919.
38. Power C, Jefferis BJ. 2002. Fetel environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol 31(2):413-419.
39. Ramilo G, Valverde I, Lago J, Vieites JM, Cabado AG. 2006. Cytotoxic effects of BADGE (bisphenol A diglycidyl ether) and BFDGE (bisphenol F diglycidyl ether) on Caco-2 cells in vitro. Arch Toxicol 80(11):748-755.
40. Rippe JM, Hess S. 1998. The role of physical activity in the prevention and management of obesity. J Am Diet Assoc 98(10 Suppl 2):S31-S38.
41. Rosen ED, MacDougald OA. 2006. Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7(12):885-896.
42. Rubin BS. 2011. Bisphenol A: An endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 127:27-34.
43. Rubin BS, Murray MK, Damassa DA, King JC, Soto AM. 2001. Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. Environ Health Perspect 109:675-680.
44. Rubin BS, Soto AM. 2009. Bisphenol A: Perinatal exposure and body weight. Mol Cell Endocrinol 304(1-2):55-62.
45. Ryan KK, Haller AM, Sorrell JE, Woods SC, Jandacek RJ, SeeleyRJ. 2010. Perinatal exposure to bisphenol-A and the development of metabolic syndrome in CD-1 mice. Endocrinology 151(6):2603-2612.
46. Sargis RM, Johnson DN, Choudhury RA, Brady MJ. 2010. Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity (Silver Spring) 18(7):1283-1288.
47. Satoh K, Ohyama K, Aoki N, Iida M, Nagai F. 2004. Study on anti-androgenic effects of bisphenol A diglycidyl ether (BADGE), bisphenol F diglycidyl ether (BFDGE) and their derivatives using cells stably transfected with human androgen receptor, AR-EcoScreen. Food Chem Toxicol 42(6):983-993.
48. Seidlova-Wuttke D, Jarry H, Christoffel J, Rimoldi G, WuttkeW. 2005. Effects of bisphenol-A (BPA), dibutylphtalate (DBP), benzophenone-2 (BP2), procymidone (Proc), and linurone (Lin) on fat tissue, a variety of hormones and metabolic parameters: a 3 months comparison with effects of estradiol (E2) in ovariectomized (ovx) rats. Toxicology 213(1-2):13-24.
49. Seimandi M, Lemaire G, Pillon A, Perrin A, Carlavan I, VoegelJJ, et al. 2005. Differential responses of PPARa, PPARd, and PPARgreporter cell lines to selective PPAR synthetic ligands. Anal Biochem 344(1):8-15.
50. Shukla SJ, Huang R, Austin CP, Xia M. 2010. The future of toxicity testing: a focus on in vitro methods using a quantitative high-throughput screening platform. Drug Discov Today 15(23-24):997-1007.
51. Somm E, Schwitzgebel VM, Toulotte A, Cederroth CR, Combescure C, Nef S, et al. 2009. Perinatal exposure to bisphenol A alters early adipogenesis in the rat. Environ Health Perspect 117(10):1549-1555.
52. TabbmM, Kholodovych V, Grun F, Zhou C, Welsh WJ, BlumbergB. 2004. Highly chlorinated PCBs inhibit the human xenobiotic response mediated by the steroid and xenobiotic receptor (SXR). Environ Health Perspect 112(2):163-169.
53. Takada I, Suzawa M, Matsumoto K, Kato S. 2007. Suppression of PPAR transactivation switches cell fate of bone marrow stem cells from adipocytes into osteoblasts. Ann NY Acad Sci 1116:182-195.
54. Tang-Peronard JL, Andersen HR, Jensen TK, Heitmann BL. 2011. Endocrine-disrupting chemicals and obesity development in humans: a review. Obes Rev 12:622-636.
55. Taylor JA, Richter CA, Ruhlen RL, Vom Saal FS. 2011. Estrogenic environmental chemicals and drugs: Mechanisms for effects on the developing male urogenital system. JSteroid Biochem Mol Biol 127(1-2):83-95.
56. Tontonoz P, Spiegelman BM. 2008. Fat and beyond: the diverse biology of PPARg. Annu Rev Biochem 77:289-312.
57. Uematsu Y, Hirata K, Suzuki K, Iida K, Saito K. 2001. Chlorohydrins of bisphenol A diglycidyl ether (BADGE) and of bisphenol F diglycidyl ether (BFDGE) in canned foods and ready-to-drink coffees from the Japanese market. Food Addit Contam 18(2):177-185.
58. Wright HM, Clish CB, Mikami T, Hauser S, Yanagi K, HiramatsuR, et al. 2000. A synthetic antagonist for the peroxisome proliferator-activated receptor ginhibits adipocyte differentiation. J Biol Chem 275(3):1873-1877.
59. Yamauchi T, Waki H, Kamon J, Murakami K, Motojima K, KomedaK, et al. 2001. Inhibition of RXR and PPARgameliorates diet-induced obesity and type 2 diabetes. JClin Invest 108(7):1001-1013.
60. Yun JW, Shin ES, Cho SY, Kim SH, Kim CW, Lee TR, et al. 2008. The effects of BADGE and caffeine on the time-course response of adiponectin and lipid oxidative enzymes in high fat diet-fed C57BL/6J mice: correlation with reduced adiposity and steatosis. Exp Anim 57(5):461-469.