BPA, an Energy Balance Disruptor

Critical Reviews in Food Science and Nutrition

Volumn 55, Issue 6, 2015, Pages 769-777

  Le Corre, L ^a   Besnard, P ^a   Chagnon, M C ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Bisphenol A; endocrine disruptor; lipid and glucose homeostasis; obesogens; toxic chemical

Indexed keywords

DENTAL MATERIALS; HEALTH RISKS; PHENOLS; RISK ASSESSMENT;

BIS-PHENOL A; ENDOCRINE DISRUPTOR; GLUCOSE HOMEOSTASIS; OBESOGENS; TOXIC CHEMICALS;

ENERGY BALANCE;

4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; ENDOCRINE DISRUPTOR; PHENOL DERIVATIVE;

ADVERSE EFFECTS; ANIMAL; DRUG EFFECTS; ENERGY METABOLISM; ENVIRONMENTAL EXPOSURE; FEMALE; HUMAN; MALE; RAT; WEIGHT GAIN;

ANIMALS; BENZHYDRYL COMPOUNDS; ENDOCRINE DISRUPTORS; ENERGY METABOLISM; ENVIRONMENTAL EXPOSURE; FEMALE; HUMANS; MALE; PHENOLS; RATS; WEIGHT GAIN;

EID: 84912117316     PISSN: 10408398     EISSN: 15497852     Source Type: Journal    
DOI: 10.1080/10408398.2012.678421     Document Type: Article

References (87)

1. Adachi, T., Yasuda, K., Mori, C., Yoshinaga, M., Aoki, N., Tsujimoto, G. and Tsuda, K. (2005). Promoting insulin secretion in pancreatic islets by means of bisphenol A and nonylphenol via intracellular estrogen receptors. Food Chem. Toxicol. 43:713–719.
2. Alonso-Magdalena, P., Laribi, O., Ropero, A.B., Fuentes, E., Ripoll, C., Soria, B. and Nadal, A. (2005). Low doses of bisphenol A and diethylstilbestrol impair Ca2+ signals in pancreatic alpha-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans. Environ. Health Perspect. 113:969–977.
3. Alonso-Magdalena, P., Ropero, A.B., Carrera, M.P., Cederroth, C.R., Baquie, M., Gauthier, B.R., Nef, S., Stefani, E. and Nadal, A. (2008). Pancreatic insulin content regulation by the estrogen receptor ER alpha. PLoS One. 3:e2069.
4. Alonso-Magdalena, P., Vieira, E., Soriano, S., Menes, L., Burks, D., Quesada, I. and Nadal, A. (2010). Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ. Health Perspect. 118:1243–1250.
5. Anderson, L.M., Diwan, B.A., Fear, N.T. and Roman, E. (2000). Critical windows of exposure for children's health: Cancer in human epidemiological studies and neoplasms in experimental animal models. Environ. Health Perspect. 108 Suppl 3:573–594.
6. Anway, M.D. and Skinner, M.K. (2006). Epigenetic transgenerational actions of endocrine disruptors. Endocrinology. 147:S43–S49.
7. Baillie-Hamilton, P.F. (2002). Chemical toxins: A hypothesis to explain the global obesity epidemic. J. Altern. Complement Med. 8:185–192.
8. Balakrishnan, B., Henare, K., Thorstensen, E.B., Ponnampalam, A.P. and Mitchell, M.D. (2010). Transfer of bisphenol A across the human placenta. Am. J. Obstet. Gynecol. 202:393 e391e397.
9. Biedermann, S., Tschudin, P. and Grob, K. (2010). Transfer of bisphenol A from thermal printer paper to the skin. Anal. Bioanal. Chem. 398:571–576.
10. Bindhumol, V., Chitra, K.C. and Mathur, P.P. (2003). Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology. 188:117–124.
11. Braniste, V., Jouault, A., Gaultier, E., Polizzi, A., Buisson-Brenac, C., Leveque, M., Martin, P.G., Theodorou, V., Fioramonti, J. and Houdeau, E. (2010). Impact of oral bisphenol A at reference doses on intestinal barrier function and sex differences after perinatal exposure in rats. Proc. Natl. Acad. Sci. U S A. 107:448–453.
12. Calabrese, E.J. and Baldwin, L.A. (2001). The frequency of U-shaped dose responses in the toxicological literature. Toxicol. Sci. 62:330–338.
13. Ceddia, R.B., Koistinen, H.A., Zierath, J.R. and Sweeney, G. (2002). Analysis of paradoxical observations on the association between leptin and insulin resistance. FASEB J. 16:1163–1176.
14. Conolly, R.B. and Lutz, W.K. (2004). Nonmonotonic dose–response relationships: Mechanistic basis, kinetic modeling, and implications for risk assessment. Toxicol. Sci. 77:151–157.
15. EFSA (2006). Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food on a request from the Commission related to 2,2-bis(4-hydroxyphenyl)propane (Bisphenol A): Question number EFSA-Q-2005-100 adopted on 29 November 2006. The EFSA J. 428:
16. Elsby, R., Maggs, J.L., Ashby, J. and Park, B.K. (2001). Comparison of the modulatory effects of human and rat liver microsomal metabolism on the estrogenicity of bisphenol A: Implications for extrapolation to humans. J. Pharmacol. Exp. Ther. 297:103–113.
17. Farooqi, I.S. and O’Rahilly, S. (2009). Leptin: A pivotal regulator of human energy homeostasis. Am. J. Clin. Nutr. 89:980S–984S.
18. Feige, J.N., Gelman, L., Rossi, D., Zoete, V., Metivier, R., Tudor, C., Anghel, S.I., Grosdidier, A., Lathion, C., Engelborghs, Y., Michielin, O., Wahli, W. and Desvergne, B. (2007). The endocrine disruptor monoethyl-hexyl-phthalate is a selective peroxisome proliferator-activated receptor gamma modulator that promotes adipogenesis. J. Biol. Chem. 282:19152–19166.
19. Fernandez, M.F., Arrebola, J.P., Taoufiki, J., Navalon, A., Ballesteros, O., Pulgar, R., Vilchez, J.L. and Olea, N. (2007). Bisphenol-A and chlorinated derivatives in adipose tissue of women. Reprod. Toxicol. 24:259–264.
20. Fung, E.Y., Ewoldsen, N.O., St Germain, H.A., Jr., Marx, D.B., Miaw, C.L., Siew, C., Chou, H.N., Gruninger, S.E. and Meyer, D.M. (2000). Pharmacokinetics of bisphenol A released from a dental sealant. J. Am. Dent. Assoc. 131:51–58.
21. Galloway, T., Cipelli, R., Guralnik, J., Ferrucci, L., Bandinelli, S., Corsi, A.M., Money, C., McCormack, P. and Melzer, D. (2010). Daily bisphenol A excretion and associations with sex hormone concentrations: Results from the InCHIANTI adult population study. Environ. Health Perspect. 118:1603–1608.
22. Giguere, V. (2008). Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr. Rev. 29:677–696.
23. Gluckman, P.D. and Hanson, M.A. (2004). The developmental origins of the metabolic syndrome. Trends Endocrinol. Metab. 15:183–187.
24. Grove, K.L., Grayson, B.E., Glavas, M.M., Xiao, X.Q. and Smith, M.S. (2005). Development of metabolic systems. Physiol. Behav. 86:646–660.
25. Grun, F. and Blumberg, B. (2006). Environmental obesogens: Organotins and endocrine disruption via nuclear receptor signaling. Endocrinology. 147:S50–S55.
26. Heidemann, C., Sun, Q., van Dam, R.M., Meigs, J.B., Zhang, C., Tworoger, S.S., Mantzoros, C.S. and Hu, F.B. (2008). Total and high-molecular-weight adiponectin and resistin in relation to the risk for type 2 diabetes in women. Ann. Intern. Med. 149:307–316.
27. Howdeshell, K.L., Hotchkiss, A.K., Thayer, K.A., Vandenbergh, J.G. and vom Saal, F.S. (1999). Exposure to bisphenol A advances puberty. Nature. 401:763–764.
28. Hugo, E.R., Brandebourg, T.D., Woo, J.G., Loftus, J., Alexander, J.W. and Ben-Jonathan, N. (2008). Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ. Health Perspect. 116:1642–1647.
29. Inadera, H. and Shimomura, A. (2005). Environmental chemical tributyltin augments adipocyte differentiation. Toxicol. Lett. 159:226–234.
30. Inoue, K., Kato, K., Yoshimura, Y., Makino, T. and Nakazawa, H. (2000). Determination of bisphenol A in human serum by high-performance liquid chromatography with multi-electrode electrochemical detection. J. Chromatogr B Biomed. Sci. Appl. 749:17–23.
31. Jung, K.K., Kim, S.Y., Kim, T.G., Kang, J.H., Kang, S.Y., Cho, J.Y. and Kim, S.H. (2007). Differential regulation of thyroid hormone receptor-mediated function by endocrine disruptors. Arch. Pharm. Res. 30:616–623.
32. Kern, P.A., Di Gregorio, G.B., Lu, T., Rassouli, N. and Ranganathan, G. (2003). Adiponectin expression from human adipose tissue: Relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression. Diabetes. 52:1779–1785.
33. Kohn, A.D., Summers, S.A., Birnbaum, M.J. and Roth, R.A. (1996). Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J. Biol. Chem. 271:31372–31378.
34. Kundakovic, M. and Champagne, F.A. (2011). Epigenetic perspective on the developmental effects of bisphenol A. Brain Behav. Immun. 25:1084–1093.
35. Kwon, S., Stedman, D.B., Elswick, B.A., Cattley, R.C. and Welsch, F. (2000). Pubertal development and reproductive functions of Crl:CD BR Sprague–Dawley rats exposed to bisphenol A during prenatal and postnatal development. Toxicol. Sci. 55:399–406.
36. Lang, I. A., Galloway, T. S., Scarlett, A., Henley, W. E., Depledge, M., Wallace, R. B. and Melzer, D. (2008). Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA. 300:1303–1310.
37. Lee, M.J., Lin, H., Liu, C.W., Wu, M.H., Liao, W.J., Chang, H.H., Ku, H.C. , Chien, Y.S., Ding, W.H. and Kao, Y.H. (2008). Octylphenol stimulates resistin gene expression in 3T3-L1 adipocytes via the estrogen receptor and extracellular signal-regulated kinase pathways. Am. J. Physiol. Cell Physiol. 294:C1542–C1551.
38. Li, J., Ma, M. and Wang, Z. (2007). A two-hybrid yeast assay to quantify the effects of xenobiotics on retinoid X receptor-mediated gene expression. Toxicol. Lett. 176:198–206.
39. Makaji, E., Raha, S., Wade, M.G. and Holloway, A.C. (2011). Effect of environmental contaminants on beta cell function. Int. J. Toxicol. 30:410–418.
40. Masuno, H., Iwanami, J., Kidani, T., Sakayama, K. and Honda, K. (2005). Bisphenol a accelerates terminal differentiation of 3T3-L1 cells into adipocytes through the phosphatidylinositol 3-kinase pathway. Toxicol. Sci. 84:319–327.
41. Masuno, H., Kidani, T., Sekiya, K., Sakayama, K., Shiosaka, T., Yamamoto, H. and Honda, K. (2002). Bisphenol A in combination with insulin can accelerate the conversion of 3T3-L1 fibroblasts to adipocytes. J. Lipid Res. 43:676–684.
42. Matsushima, A., Teramoto, T., Okada, H., Liu, X., Tokunaga, T., Kakuta, Y. and Shimohigashi, Y. (2008). ERRgamma tethers strongly bisphenol A and 4-alpha-cumylphenol in an induced-fit manner. Biochem. Biophys. Res. Commun. 373:408–413.
43. Melzer, D., Rice, N.E., Lewis, C., Henley, W.E. and Galloway, T.S. (2010). Association of urinary bisphenol a concentration with heart disease: Evidence from NHANES 2003/06. PLoS One. 5:e8673.
44. Miyawaki, J., Sakayama, K., Kato, H., Yamamoto, H. and Masuno, H. (2007). Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. J. Atheroscler. Thromb. 14:245–252.
45. Moriyama, K., Tagami, T., Akamizu, T., Usui, T., Saijo, M., Kanamoto, N., Hataya, Y., Shimatsu, A., Kuzuya, H. and Nakao, K. (2002). Thyroid hormone action is disrupted by bisphenol A as an antagonist. J. Clin. Endocrinol. Metab. 87:5185–5190.
46. Nadal, A., Ropero, A.B., Laribi, O., Maillet, M., Fuentes, E. and Soria, B. (2000). Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. Proc. Natl. Acad. Sci. U S A. 97:11603–11608.
47. Nakagawa, Y. and Tayama, S. (2000). Metabolism and cytotoxicity of bisphenol A and other bisphenols in isolated rat hepatocytes. Arch. Toxicol. 74:99–105.
48. Newbold, R.R., Padilla-Banks, E., Snyder, R.J. and Jefferson, W.N. (2005). Developmental exposure to estrogenic compounds and obesity. Birth Defects Res. A Clin. Mol. Teratol. 73:478–480.
49. Nikaido, Y., Yoshizawa, K., Danbara, N., Tsujita-Kyutoku, M., Yuri, T., Uehara, N. and Tsubura, A. (2004). Effects of maternal xenoestrogen exposure on development of the reproductive tract and mammary gland in female CD-1 mouse offspring. Reprod. Toxicol. 18:803–811.
50. Nishizawa, H., Morita, M., Sugimoto, M., Imanishi, S. and Manabe, N. (2005). Effects of in utero exposure to bisphenol A on mRNA expression of arylhydrocarbon and retinoid receptors in murine embryos. J. Reprod. Dev. 51:315–324.
51. Okada, H., Tokunaga, T., Liu, X., Takayanagi, S., Matsushima, A. and Shimohigashi, Y. (2008). Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor-gamma. Environ. Health Perspect. 116:32–38.
52. Palanza, P.L., Howdeshell, K.L., Parmigiani, S. and vom Saal, F.S. (2002). Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ. Health Perspect. 110 Suppl 3:415–422.
53. Phrakonkham, P., Viengchareun, S., Belloir, C., Lombes, M., Artur, Y. and Canivenc-Lavier, M.C. (2008). Dietary xenoestrogens differentially impair 3T3-L1 preadipocyte differentiation and persistently affect leptin synthesis. J Steroid. Biochem. Mol. Biol. 110:95–103.
54. Pottenger, L.H., Domoradzki, J.Y., Markham, D.A., Hansen, S.C., Cagen, S.Z. and Waechter, J.M., Jr. (2000). The relative bioavailability and metabolism of bisphenol A in rats is dependent upon the route of administration. Toxicol. Sci. 54:3–18.
55. Quesada, I., Fuentes, E., Viso-Leon, M.C., Soria, B., Ripoll, C. and Nadal, A. (2002). Low doses of the endocrine disruptor bisphenol-A and the native hormone 17beta-estradiol rapidly activate transcription factor CREB. FASEB J. 16:1671–1673.
56. Rangwala, S.M. and Lazar, M.A. (2000). Transcriptional control of adipogenesis. Annu. Rev. Nutr. 20:535–559.
57. Richter, C.A., Birnbaum, L.S., Farabollini, F., Newbold, R.R., Rubin, B.S., Talsness, C.E., Vandenbergh, J.G., Walser-Kuntz, D.R. and vom Saal, F.S. (2007). In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 24:199–224.
58. Ropero, A.B., Alonso-Magdalena, P., Garcia-Garcia, E., Ripoll, C., Fuentes, E. and Nadal, A. (2008). Bisphenol-A disruption of the endocrine pancreas and blood glucose homeostasis. Int. J. Androl. 31:194–200.
59. Ropero, A.B., Soria, B. and Nadal, A. (2002). A nonclassical estrogen membrane receptor triggers rapid differential actions in the endocrine pancreas. Mol. Endocrinol. 16:497–505.
60. Rubin, B.S., Murray, M.K., Damassa, D.A., King, J.C. and Soto, A.M. (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.
61. Ryan, K.K., Haller, A.M., Sorrell, J.E., Woods, S.C., Jandacek, R.J. and Seeley, R.J. (2010). Perinatal exposure to bisphenol-a and the development of metabolic syndrome in CD-1 mice. Endocrinology. 151:2603–2612.
62. Sajiki, J., Yanagibori, R. and Kobayashi, Y. (2010). Study of experiment on leaching of bisphenol A from infant books to artificial saliva. Nihon. Eiseigaku Zasshi. 65:467–470.
63. Sakurai, K., Kawazuma, M., Adachi, T., Harigaya, T., Saito, Y., Hashimoto, N. and Mori, C. (2004). Bisphenol A affects glucose transport in mouse 3T3-F442A adipocytes. Br. J. Pharmacol. 141:209–214.
64. Sargis, R.M., Johnson, D.N., Choudhury, R.A. and Brady, M.J. (2010). Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity (Silver Spring). 18:1283–1288.
65. Scherer, P.E., Williams, S., Fogliano, M., Baldini, G. and Lodish, H.F. (1995). A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 270:26746–26749.
66. Schonfelder, G., Wittfoht, W., Hopp, H., Talsness, C.E., Paul, M. and Chahoud, I. (2002). Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ. Health Perspect. 110:A703–A707.
67. Seidlova-Wuttke, D., Jarry, H., Christoffel, J., Rimoldi, G. and Wuttke, W. (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 in ovariectomized rats. Toxicology. 213:13–24.
68. Simerly, R.B. (2008). Hypothalamic substrates of metabolic imprinting. Physiol. Behav. 94:79–89.
69. Somm, E., Schwitzgebel, V.M., Toulotte, A., Cederroth, C.R., Combescure, C., Nef, S., Aubert, M.L. and Huppi, P.S. (2009). Perinatal exposure to bisphenol A alters early adipogenesis in the rat. Environ. Health Perspect. 117:1549–1555.
70. Steppan, C.M. and Lazar, M.A. (2004). The current biology of resistin. J. Intern. Med. 255:439–447.
71. Tabb, M.M. and Blumberg, B. (2006). New modes of action for endocrine-disrupting chemicals. Mol. Endocrinol. 20:475–482.
72. Takeshita, A., Koibuchi, N., Oka, J., Taguchi, M., Shishiba, Y. and Ozawa, Y. (2001). Bisphenol-A, an environmental estrogen, activates the human orphan nuclear receptor, steroid and xenobiotic receptor-mediated transcription. Eur J Endocrinol. 145:513–517.
73. Takeuchi, T. and Tsutsumi, O. (2002). Serum bisphenol A concentrations showed gender differences, possibly linked to androgen levels. Biochem. Biophys. Res. Commun. 291:76–78.
74. Taylor, J.A., Vom Saal, F.S., Welshons, W.V., Drury, B., Rottinghaus, G., Hunt, P.A., Toutain, P.L., Laffont, C.M. and VandeVoort, C.A. (2011). Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: Relevance for human exposure. Environ. Health Perspect. 119:422–430.
75. Trasande, L., Ziebold, C., Schiff, J.S., Wallinga, D., McGovern, P. and Oberg, C.N. (2008). The role of the environment in pediatric practice in Minnesota: Attitudes, beliefs, and practices. Minn. Med. 91:36–39.
76. Vandenberg, L.N., Maffini, M.V., Sonnenschein, C., Rubin, B.S. and Soto, A.M. (2009). Bisphenol-A and the great divide: A review of controversies in the field of endocrine disruption. Endocr. Rev. 30:75–95.
77. Vandenberg, L.N., Maffini, M.V., Wadia, P.R., Sonnenschein, C., Rubin, B.S. and Soto, A.M. (2007). Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology. 148:116–127.
78. Volkel, W., Colnot, T., Csanady, G.A., Filser, J.G. and Dekant, W. (2002). Metabolism and kinetics of bisphenol A in humans at low doses following oral administration. Chem. Res. Toxicol. 15:1281–1287.
79. vom Saal, F.S., Cooke, P.S., Buchanan, D.L., Palanza, P., Thayer, K.A., Nagel, S.C., Parmigiani, S. and Welshons, W.V. (1998). A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol. Ind. Health. 14:239–260.
80. vom Saal, F.S., Timms, B.G., Montano, M.M., Palanza, P., Thayer, K.A., Nagel, S.C., Dhar, M.D., Ganjam, V.K., Parmigiani, S. and Welshons, W.V. (1997). Prostate enlargement in mice due to fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses. Proc. Natl. Acad. Sci. U S A. 94:2056–2061.
81. Wada, K., Sakamoto, H., Nishikawa, K., Sakuma, S., Nakajima, A., Fujimoto, Y. and Kamisaki, Y. (2007). Life style-related diseases of the digestive system: Endocrine disruptors stimulate lipid accumulation in target cells related to metabolic syndrome. J. Pharmacol. Sci. 105:133–137.
82. 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.
83. Woods, S.C. and D’Alessio, D.A. (2008). Central control of body weight and appetite. J. Clin. Endocrinol. Metab. 93:S37–S50.
84. Xia, X. and Serrero, G. (1999). Inhibition of adipose differentiation by phosphatidylinositol 3-kinase inhibitors. J. Cell Physiol. 178:9–16.
85. Xiao, X.Q., Williams, S.M., Grayson, B.E., Glavas, M.M., Cowley, M.A., Smith, M.S. and Grove, K.L. (2007). Excess weight gain during the early postnatal period is associated with permanent reprogramming of brown adipose tissue adaptive thermogenesis. Endocrinology. 148:4150–4159.
86. Yang, Y.J., Hong, Y.C., Oh, S.Y., Park, M.S., Kim, H., Leem, J.H. and Ha, E.H. (2009). Bisphenol A exposure is associated with oxidative stress and inflammation in postmenopausal women. Environ. Res. 109:797–801.
87. Zalko, D., Jacques, C., Duplan, H., Bruel, S. and Perdu, E. (2011). Viable skin efficiently absorbs and metabolizes bisphenol A. Chemosphere. 82:424–430.