Short-term treatment with Bisphenol-A leads to metabolic abnormalities in adult male mice

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Batista, Thiago M ^a,b   Alonso Magdalena, Paloma ^c,d   Vieira, Elaine ^c,d   Amaral, Maria Esmeria C ^f   Cederroth, Christopher R ^e   Nef, Serge ^e   Quesada, Ivan ^c,d   Carneiro, Everardo M ^a,b   Nadal, Angel ^c,d  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b Instituto Nacional de Ciência e Tecnologia de Obesidade e Diabetes   (Brazil)

^c MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

^e UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^f CENTRO UNIVERSITÁRIO HERMÍNIO OMETTO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR BETA; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; THREONINE; TYROSINE; UNCLASSIFIED DRUG; ESTROGEN; GLUCOSE; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, MOUSE; PHENOL DERIVATIVE;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CALORIMETRY; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FOOD INTAKE; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE TEST; INSULIN RELEASE; INSULIN RESISTANCE; LIVER; LOCOMOTION; MALE; METABOLIC DISORDER; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN PHOSPHORYLATION; RISK FACTOR; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION; WESTERN BLOTTING; ANIMAL; DRUG EFFECT; ENERGY METABOLISM; METABOLISM; PHOSPHORYLATION; SUBCUTANEOUS DRUG ADMINISTRATION;

MUS;

ANIMALS; ENERGY METABOLISM; ESTROGENS, NON-STEROIDAL; GLUCOSE; INJECTIONS, SUBCUTANEOUS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; LIVER; MALE; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE, SKELETAL; PHENOLS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84859012821     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033814     Document Type: Article

References (51)

1. Hotamisligil GS, (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
2. Beard JC, Ward WK, Halter JB, Wallum BJ, Porte D Jr, (1987) Relationship of islet function to insulin action in human obesity. J Clin Endocrinol Metab 65: 59-64.
3. Alonso-Magdalena P, Quesada I, Nadal A, (2011) Endocrine disruptors in the etiology of type 2 diabetes mellitus. Nat Rev Endocrinol 7: 346-353.
4. Hectors TL, Vanparys C, van der Ven K, Martens GA, Jorens PG, et al. (2011) Environmental pollutants and type 2 diabetes: a review of mechanisms that can disrupt beta cell function. Diabetologia 54: 1273-1290.
5. Casals-Casas C, Desvergne B, (2011) Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol 73: 135-162.
6. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV, (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24: 139-177.
7. Shankar A, Teppala S, (2011) Relationship between urinary bisphenol A levels and diabetes mellitus. J Clin Endocrinol Metab 96: 3822-3826.
8. Wang T, Li M, Chen B, Xu M, Xu Y, et al. (2012) Urinary Bisphenol A (BPA) Concentration Associates with Obesity and Insulin Resistance. J Clin Endocrinol Metab 97: E223-227.
9. Nadal A, Alonso-Magdalena P, Soriano S, Quesada I, Ropero AB, (2009) The pancreatic beta-cell as a target of estrogens and xenoestrogens: Implications for blood glucose homeostasis and diabetes. Mol Cell Endocrinol 304: 63-68.
10. Talsness CE, Andrade AJ, Kuriyama SN, Taylor JA, vom Saal FS, (2009) Components of plastic: experimental studies in animals and relevance for human health. Philos Trans R Soc Lond B Biol Sci 364: 2079-2096.
11. Taylor JA, Vom Saal FS, Welshons WV, Drury B, Rottinghaus G, et al. (2011) Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: relevance for human exposure. Environ Health Perspect 119: 422-430.
12. Stahlhut RW, Welshons WV, Swan SH, (2009) Bisphenol A data in NHANES suggest longer than expected half-life, substantial nonfood exposure, or both. Environ Health Perspect 117: 784-789.
13. Zalko D, Jacques C, Duplan H, Bruel S, Perdu E, (2011) Viable skin efficiently absorbs and metabolizes bisphenol A. Chemosphere 82: 424-430.
14. 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.
15. Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A, (2006) The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Environ Health Perspect 114: 106-112.
16. Alonso-Magdalena P, Vieira E, Soriano S, Menes L, Burks D, et al. (2010) Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect 118: 1243-1250.
17. Ruzzin J, Petersen R, Meugnier E, Madsen L, Lock EJ, et al. (2010) Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect 118: 465-471.
18. Wei J, Lin Y, Li Y, Ying C, Chen J, et al. (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. Alonso-Magdalena P, Ropero AB, Carrera MP, Cederroth CR, Baquie M, et al. (2008) Pancreatic insulin content regulation by the estrogen receptor ER alpha. PLoS One 3: e2069.
20. Oliveira AG, Carvalho BM, Tobar N, Ropelle ER, Pauli JR, et al. (2011) Physical exercise reduces circulating lipopolysaccharide and TLR4 activation and improves insulin signaling in tissues of DIO rats. Diabetes 60: 784-796.
21. Adachi T, Yasuda K, Mori C, Yoshinaga M, Aoki N, et al. (2005) Promoting insulin secretion in pancreatic islets by means of bisphenol A and nonylphenol via intracellular estrogen receptors. Food Chem Toxicol 43: 713-719.
22. Soriano S, Alonso-Magdalena P, Garcia-Arevalo M, Novials A, Muhammed SJ, et al. (2012) Rapid Insulinotropic Action of Low Doses of Bisphenol-A on Mouse and Human Islets of Langerhans: Role of Estrogen Receptor beta. PLoS One 7: e31109.
23. Wong WP, Tiano JP, Liu S, Hewitt SC, Le May C, et al. (2010) Extranuclear estrogen receptor-alpha stimulates NeuroD1 binding to the insulin promoter and favors insulin synthesis. Proc Natl Acad Sci U S A 107: 13057-13062.
24. Barros RP, Machado UF, Gustafsson JA, (2006) Estrogen receptors: new players in diabetes mellitus. Trends Mol Med 12: 425-431.
25. Ropero AB, Alonso-Magdalena P, Quesada I, Nadal A, (2008) The role of estrogen receptors in the control of energy and glucose homeostasis. Steroids 73: 874-879.
26. Faulds MH, Zhao C, Dahlman-Wright K, Gustafsson JA, (2011) The diversity of sex steroid action: regulation of metabolism by estrogen signaling. J Endocrinol 212: 3-12.
27. Park CJ, Zhao Z, Glidewell-Kenney C, Lazic M, Chambon P, et al. (2011) Genetic rescue of nonclassical ERalpha signaling normalizes energy balance in obese ERalpha-null mutant mice. J Clin Invest 121: 604-612.
28. Soriano S, Ropero AB, Alonso-Magdalena P, Ripoll C, Quesada I, et al. (2009) Rapid regulation of K(ATP) channel activity by 17β-estradiol in pancreatic β-cells involves the estrogen receptor β and the atrial natriuretic peptide receptor. Mol Endocrinol 23: 1973-1982.
29. Meyer MR, Clegg DJ, Prossnitz ER, Barton M, (2011) Obesity, insulin resistance and diabetes: sex differences and role of oestrogen receptors. Acta Physiol (Oxf) 203: 259-269.
30. Wetherill YB, Akingbemi BT, Kanno J, McLachlan JA, Nadal A, et al. (2007) In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol 24: 178-198.
31. Clegg DJ, Brown LM, Woods SC, Benoit SC, (2006) Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 55: 978-987.
32. Gao Q, Mezei G, Nie Y, Rao Y, Choi CS, et al. (2007) Anorectic estrogen mimics leptin's effect on the rewiring of melanocortin cells and Stat3 signaling in obese animals. Nat Med 13: 89-94.
33. Musatov S, Chen W, Pfaff DW, Mobbs CV, Yang XJ, et al. (2007) Silencing of estrogen receptor alpha in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci U S A 104: 2501-2506.
34. Cederroth CR, Vinciguerra M, Kuhne F, Madani R, Doerge DR, et al. (2007) A phytoestrogen-rich diet increases energy expenditure and decreases adiposity in mice. Environ Health Perspect 115: 1467-1473.
35. Hugo ER, Brandebourg TD, Woo JG, Loftus J, Alexander JW, et al. (2008) Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ Health Perspect 116: 1642-1647.
36. Leng Y, Karlsson HK, Zierath JR, (2004) Insulin signaling defects in type 2 diabetes. Rev Endocr Metab Disord 5: 111-117.
37. Karlsson HK, Zierath JR, Kane S, Krook A, Lienhard GE, et al. (2005) Insulin-stimulated phosphorylation of the Akt substrate AS160 is impaired in skeletal muscle of type 2 diabetic subjects. Diabetes 54: 1692-1697.
38. Cusi K, Maezono K, Osman A, Pendergrass M, Patti ME, et al. (2000) Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J Clin Invest 105: 311-320.
39. Lazar DF, Wiese RJ, Brady MJ, Mastick CC, Waters SB, et al. (1995) Mitogen-activated protein kinase kinase inhibition does not block the stimulation of glucose utilization by insulin. J Biol Chem 270: 20801-20807.
40. Glass DJ, (2010) PI3 kinase regulation of skeletal muscle hypertrophy and atrophy. Curr Top Microbiol Immunol 346: 267-278.
41. Hamdi MM, Mutungi G, (2011) Dihydrotestosterone stimulates amino acid uptake and the expression of LAT2 in mouse skeletal muscle fibres through an ERK1/2-dependent mechanism. J Physiol 589: 3623-3640.
42. Maroni P, Citterio L, Piccoletti R, Bendinelli P, (2009) Sam68 and ERKs regulate leptin-induced expression of OB-Rb mRNA in C2C12 myotubes. Mol Cell Endocrinol 309: 26-31.
43. DeFronzo RA, (1997) Pathogenesis of type 2 diabetes: metabolic and molecular implications for identifying diabetes genes. Diabetes 5: 177-269.
44. McGarry JD, (1992) What if Minkowski had been ageusic? An alternative angle on diabetes. Science 258: 766-770.
45. Devedjian JC, George M, Casellas A, Pujol A, Visa J, et al. (2000) Transgenic mice overexpressing insulin-like growth factor-II in beta cells develop type 2 diabetes. J Clin Invest 105: 731-740.
46. Del Prato S, Leonetti F, Simonson DC, Sheehan P, Matsuda M, et al. (1994) Effect of sustained physiologic hyperinsulinaemia and hyperglycaemia on insulin secretion and insulin sensitivity in man. Diabetologia 37: 1025-1035.
47. Phrakonkham P, Viengchareun S, Belloir C, Lombes M, Artur Y, et al. (2008) Dietary xenoestrogens differentially impair 3T3-L1 preadipocyte differentiation and persistently affect leptin synthesis. J Steroid Biochem Mol Biol 110: 95-103.
48. Sakurai K, Kawazuma M, Adachi T, Harigaya T, Saito Y, et al. (2004) Bisphenol A affects glucose transport in mouse 3T3-F442A adipocytes. Br J Pharmacol 141: 209-214.
49. Wada K, Sakamoto H, Nishikawa K, Sakuma S, Nakajima A, et al. (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.
50. Prins GS, Ye SH, Birch L, Ho SM, Kannan K, (2011) Serum bisphenol A pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Reprod Toxicol 31: 1-9.
51. Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M, et al. (2008) Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. Jama 300: 1303-1310.