Bisphenol-A: a new diabetogenic factor?

The aim of this review was to analyze the potential effects of environmental chemicals on homeostatic control related to glycemia and energy balance. Many of the environmental chemicals can mimic or interfere with the action of hormones and are generally referred to as “endocrine disruptors”. Among these compounds, polychlorinated biphenyls, dioxins, phthalates and bisphenol-A have been correlated with alterations in blood glucose homeostasis in humans. In rodents it has been demonstrated that small doses of bisphenol-A have profound effects on glucose metabolism. Therefore, this altered blood glucose homeostasis may enhance the development of type 2 diabetes.

[1]  F. Olea-Serrano,et al.  Estrogenicity of resin-based composites and sealants used in dentistry. , 1996, Environmental health perspectives.

[2]  I. Quesada,et al.  REVIEW Physiology of the pancreatic a -cell and glucagon secretion: role in glucose homeostasis and diabetes , 2008 .

[3]  P. Mathur,et al.  Bisphenol A induces reactive oxygen species generation in the liver of male rats. , 2003, Toxicology.

[4]  Angel Nadal,et al.  Homologous and heterologous asynchronicity between identified α‐, β‐ and δ‐cells within intact islets of Langerhans in the mouse , 1999 .

[5]  Godsland If.  The influence of female sex steroids on glucose metabolism and insulin action. , 1996 .

[6]  T. León‐Quinto,et al.  Rapid insulinotropic effect of 17β‐estradiol via a plasma membrane receptor , 1998, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[7]  B. Soria,et al.  Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[8]  M. Collison,et al.  Sex steroids and insulin resistance. , 2002, Clinical science.

[9]  J. Callés-Escandon,et al.  Menopause, central body fatness, and insulin resistance: effects of hormone‐replacement therapy , 1998, Coronary artery disease.

[10]  P. Rorsman,et al.  Regulation of glucagon release in mouse α‐cells by KATP channels and inactivation of TTX‐sensitive Na+ channels , 2000, The Journal of physiology.

[11]  Margaret Warner,et al.  Estrogen receptors: how do they signal and what are their targets. , 2007, Physiological reviews.

[12]  C. Diazzi,et al.  Human models of aromatase deficiency , 2008, The Journal of Steroid Biochemistry and Molecular Biology.

[13]  T. Colborn,et al.  Environmental estrogens: health implications for humans and wildlife. , 1995, Environmental health perspectives.

[14]  K. Dahlman-Wright,et al.  Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in high-fat diet-fed mice. , 2008, American journal of physiology. Endocrinology and metabolism.

[15]  R. Latorre,et al.  Acute Activation of Maxi-K Channels (hSlo) by Estradiol Binding to the β Subunit , 1999 .

[16]  I. Quesada,et al.  The role of estrogen receptors in the control of energy and glucose homeostasis , 2008, Steroids.

[17]  E. Dodds,et al.  Synthetic Œstrogenic Agents without the Phenanthrene Nucleus , 1936, Nature.

[18]  John Calvin Reed,et al.  cAMP promotes pancreatic β-cell survival via CREB-mediated induction of IRS2 , 2003 .

[19]  K. Korach,et al.  Estrogen receptor null mice: what have we learned and where will they lead us? , 1999, Endocrine reviews.

[20]  J. Alexander,et al.  Bisphenol A at Environmentally Relevant Doses Inhibits Adiponectin Release from Human Adipose Tissue Explants and Adipocytes , 2008, Environmental health perspectives.

[21]  K. Sakurai,et al.  Bisphenol A affects glucose transport in mouse 3T3‐F442A adipocytes , 2004, British journal of pharmacology.

[22]  V. Wynn,et al.  Some effects of oral contraceptives on carbohydrate metabolism. , 1966, Lancet.

[23]  G. Iwamoto,et al.  Increased adipose tissue in male and female estrogen receptor-α knockout mice , 2000 .

[24]  B. Soria,et al.  Low doses of the endocrine disruptor Bisphenol‐A and the native hormone 17β‐estradiol rapidly activate the transcription factor CREB , 2002, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[25]  A. Soto,et al.  Bisphenol A: Perinatal exposure and body weight , 2009, Molecular and Cellular Endocrinology.

[26]  C. Kahn,et al.  From mice to men: insights into the insulin resistance syndromes. , 2006, Annual review of physiology.

[27]  K. Honda,et al.  Bisphenol a accelerates terminal differentiation of 3T3-L1 cells into adipocytes through the phosphatidylinositol 3-kinase pathway. , 2005, Toxicological sciences : an official journal of the Society of Toxicology.

[28]  M. Brandi,et al.  Genistein affects adipose tissue deposition in a dose-dependent and gender-specific manner , 2006 .

[29]  I. Quesada,et al.  The pancreatic β-cell as a target of estrogens and xenoestrogens: Implications for blood glucose homeostasis and diabetes , 2009, Molecular and Cellular Endocrinology.

[30]  A. Thorburn,et al.  Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Yoshiki Katayama,et al.  Human exposure to bisphenol A. , 2006, Toxicology.

[32]  J. Gustafsson,et al.  Muscle GLUT4 regulation by estrogen receptors ERβ and ERα , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Yonekubo,et al.  Sensitive method for the determination of bisphenol-A in serum using two systems of high-performance liquid chromatography. , 1999, Journal of chromatography. B, Biomedical sciences and applications.

[34]  M. Carlberg,et al.  Islet constitutive nitric oxide synthase: biochemical determination and regulatory function. , 1996, The American journal of physiology.

[35]  Bruce M. Spiegelman,et al.  Adipocytes as regulators of energy balance and glucose homeostasis , 2006, Nature.

[36]  J. P. Myers,et al.  Bisphenol A and risk of metabolic disorders. , 2008, JAMA.

[37]  E. Oetjen,et al.  Distinct properties of the cAMP-responsive element of the rat insulin I gene. , 1994, The Journal of biological chemistry.

[38]  H. Häring,et al.  How insulin receptor substrate proteins regulate the metabolic capacity of the liver--implications for health and disease. , 2008, Current medicinal chemistry.

[39]  P. Rorsman,et al.  Multisite regulation of insulin secretion by cAMP-increasing agonists: evidence that glucagon-like peptide 1 and glucagon act via distinct receptors , 1997, Pflügers Archiv.

[40]  A. Berts,et al.  Suppression of Ca2+ oscillations in glucagon-producing alpha 2-cells by insulin/glucose and amino acids. , 1996, Biochimica et biophysica acta.

[41]  B. Soria,et al.  Low Doses of Bisphenol A and Diethylstilbestrol Impair Ca2+ Signals in Pancreatic α-Cells through a Nonclassical Membrane Estrogen Receptor within Intact Islets of Langerhans , 2005, Environmental health perspectives.

[42]  Rosalind,et al.  Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop. , 1996, Environmental health perspectives.

[43]  Y. Ouchi,et al.  Estrogen receptor ß is involved in the anorectic action of estrogen , 2002, International Journal of Obesity.

[44]  E. Levin,et al.  Integration of the extranuclear and nuclear actions of estrogen. , 2005, Molecular endocrinology.

[45]  P. Heine,et al.  Effect of Ovariectomy on Adipose Tissue of Mice in the Absence of Estrogen Receptor Alpha (ERα): a Potential Role for Estrogen Receptor Beta (ERβ) , 2002 .

[46]  C. Ripoll,et al.  Disentangling the molecular mechanisms of action of endogenous and environmental estrogens , 2004, Pflügers Archiv.

[47]  D. Jacobs,et al.  Relationship between serum concentrations of persistent organic pollutants and the prevalence of metabolic syndrome among non-diabetic adults: results from the National Health and Nutrition Examination Survey 1999–2002 , 2007, Diabetologia.

[48]  H. Jarry,et al.  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. , 2005, Toxicology.

[49]  Carl D Langefeld,et al.  Association of the estrogen receptor-alpha gene with the metabolic syndrome and its component traits in African-American families: the Insulin Resistance Atherosclerosis Family Study. , 2007, Diabetes.

[50]  Robert B Wallace,et al.  Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. , 2008, JAMA.

[51]  J. Giesy,et al.  Effects of bisphenol A on energy balance and accumulation in brown adipose tissue in rats. , 2001, Chemosphere.

[52]  J. Gustafsson,et al.  Rapid regulation of K(ATP) channel activity by 17{beta}-estradiol in pancreatic {beta}-cells involves the estrogen receptor {beta} and the atrial natriuretic peptide receptor. , 2009, Molecular endocrinology.

[53]  Samuel P. Caudill,et al.  Urinary Concentrations of Bisphenol A and 4-Nonylphenol in a Human Reference Population , 2004, Environmental health perspectives.

[54]  K. Korach,et al.  Estrogens protect pancreatic beta-cells from apoptosis and prevent insulin-deficient diabetes mellitus in mice. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[55]  K. Dahlman-Wright,et al.  Evidence that oestrogen receptor-α plays an important role in the regulation of glucose homeostasis in mice: insulin sensitivity in the liver , 2006, Diabetologia.

[56]  B. Kahn,et al.  Glucose transport and sensing in the maintenance of glucose homeostasis and metabolic harmony. , 2006, The Journal of clinical investigation.

[57]  H. Kabuto,et al.  Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues. , 2003, Environmental Research.

[58]  J. Foley,et al.  Alpha cell function in health and disease: influence of glucagon-like peptide-1 , 2005, Diabetologia.

[59]  C. Kahn,et al.  Knockout Mice Challenge our Concepts of Glucose Homeostasis and the Pathogenesis of Diabetes , 2003, Experimental diabesity research.

[60]  S. Kahn,et al.  The beta cell lesion in type 2 diabetes: there has to be a primary functional abnormality , 2009, Diabetologia.

[61]  E. Salpeter,et al.  Meta‐analysis: effect of hormone‐replacement therapy on components of the metabolic syndrome in postmenopausal women , 2006, Diabetes, obesity & metabolism.

[62]  O. Tsutsumi,et al.  Serum bisphenol a concentrations showed gender differences, possibly linked to androgen levels. , 2002, Biochemical and biophysical research communications.

[63]  P. Heine,et al.  The role of estrogen and estrogen receptor-α in male adipose tissue , 2001, Molecular and Cellular Endocrinology.

[64]  Ana M Soto,et al.  Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. , 2009, Endocrine reviews.

[65]  B. Soria,et al.  The plasma membrane estrogen receptor: nuclear or unclear? , 2001, Trends in pharmacological sciences.

[66]  M. Prentki,et al.  Malonyl-CoA signaling, lipid partitioning, and glucolipotoxicity: role in beta-cell adaptation and failure in the etiology of diabetes. , 2002, Diabetes.

[67]  K. Melissinos,et al.  HEREDITARY RECURRENT HÆMATURIA , 1975, The Lancet.

[68]  C. Richter,et al.  In vivo effects of bisphenol A in laboratory rodent studies. , 2007, Reproductive toxicology.

[69]  Laura N. Vandenberg,et al.  Human exposure to bisphenol A (BPA). , 2007, Reproductive toxicology.

[70]  S. Wild,et al.  Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. , 2004, Diabetes care.

[71]  V. Go,et al.  Characterization and Control of Pulsatile Secretion of Insulin and Glucagon , 1988, Pancreas.

[72]  Lena Eliasson,et al.  Capacitance measurements of exocytosis in mouse pancreatic α‐, β‐ and δ‐cells within intact islets of Langerhans , 2004, The Journal of physiology.

[73]  Paloma Alonso-Magdalena,et al.  The Estrogenic Effect of Bisphenol A Disrupts Pancreatic β-Cell Function In Vivo and Induces Insulin Resistance , 2005, Environmental health perspectives.

[74]  E. Stefani,et al.  Pancreatic Insulin Content Regulation by the Estrogen Receptor ERα , 2008, PloS one.

[75]  J. King,et al.  Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. , 2001, Environmental health perspectives.

[76]  P. Rorsman,et al.  Voltage-activated currents in guinea pig pancreatic alpha 2 cells. Evidence for Ca2+-dependent action potentials , 1988, The Journal of general physiology.

[77]  S. Kahn,et al.  Mechanisms linking obesity to insulin resistance and type 2 diabetes , 2006, Nature.

[78]  J. Gustafsson,et al.  Estrogen receptors: new players in diabetes mellitus. , 2006, Trends in molecular medicine.

[79]  H. Seo,et al.  The ratio of estrogen receptor α to estrogen receptor β in adipose tissue is associated with leptin production and obesity , 2007, Steroids.

[80]  K. Sekiya,et al.  Bisphenol A in combination with insulin can accelerate the conversion of 3T3-L1 fibroblasts to adipocytes. , 2002, Journal of lipid research.

[81]  I. Godsland,et al.  Oestrogens and insulin secretion , 2005, Diabetologia.

[82]  K. Korach,et al.  Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. , 1994, The New England journal of medicine.

[83]  D. Jacobs,et al.  Graded Associations of Blood Lead and Urinary Cadmium Concentrations with Oxidative-Stress–Related Markers in the U.S. Population: Results from the Third National Health and Nutrition Examination Survey , 2005, Environmental health perspectives.

[84]  D. Pfaff,et al.  Silencing of estrogen receptor α in the ventromedial nucleus of hypothalamus leads to metabolic syndrome , 2007, Proceedings of the National Academy of Sciences.

[85]  D. Jacobs,et al.  Can persistent organic pollutants explain the association between serum γ-glutamyltransferase and type 2 diabetes ? , 2008 .

[86]  G. Tsujimoto,et al.  Promoting insulin secretion in pancreatic islets by means of bisphenol A and nonylphenol via intracellular estrogen receptors. , 2005, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.