Evaluation of low doses BPA-induced perturbation of glycemia by toxicogenomics points to a primary role of pancreatic islets and to the mechanism of toxicity

Cell Death and Disease

Volumn 6, Issue 10, 2015, Pages

  Carchia, E ^a   Porreca, I ^a   Almeida, P J ^b   D'Angelo, F ^a   Cuomo, D ^c   Ceccarelli, M ^a,c   Felice, M De ^d,e   Mallardo, M ^e   Ambrosino, C ^a,c  

^a Grande Ospedale Metropolitano   (Italy)

^b STAB VIDA Investigação e Serviços em Ciências Biológicas ^*  (Portugal)

^c UNIVERSITY OF SANNIO   (Italy)

^d CNR   (Italy)

^e UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; BENZHYDRYL DERIVATIVE; GLUCOSE BLOOD LEVEL; PHENOL DERIVATIVE;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; CELL DAMAGE; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EXPOSURE; GENOMICS; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HYPERGLYCEMIA; LIVER CELL; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PANCREAS ISLET; PRIORITY JOURNAL; TOXICOGENOMICS; TOXICOLOGY; ANIMAL; C57BL MOUSE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; HOMEOSTASIS; METABOLISM; PROCEDURES; TOXICOGENETICS;

ANIMALS; BENZHYDRYL COMPOUNDS; BLOOD GLUCOSE; DOSE-RESPONSE RELATIONSHIP, DRUG; HEPATOCYTES; HOMEOSTASIS; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; PHENOLS; TOXICOGENETICS;

EID: 84975230045     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2015.319     Document Type: Article

References (61)

1. Kirkley AG, Sargis RM. Environmental endocrine disruption of energy metabolism and cardiovascular risk. Curr Diab Rep 2014; 14: 494.
2. Chevalier N, Fénichel P. Endocrine disruptors: new players in the pathophysiology of type 2 diabetes? Diabetes Metab 2014; 41: 107-115.
3. Peng H, Hagopian W. Environmental factors in the development of Type 1 diabetes. Rev Endocr Metab Disord 2006; 7: 149-162.
4. Cnop M, Welsh N, Jonas JC, Jörns A, Lenzen S, Eizirik DL et al. Mechanisms of pancreatic -cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 2005; 54: S97-S107.
5. Nadal A, Alonso-Magdalena P, Soriano S, Quesada I, Ropero AB. The pancreatic beta-cell as a target of estrogens and xenoestrogens: Implications for blood glucose homeostasis and diabetes. Mol Cell Endocrinol 2009; 304: 63-68.
6. Ropero AB, Alonso-Magdalena P, Quesada I, Nadal A. The role of estrogen receptors in the control of energy and glucose homeostasis. Steroids 2008; 73: 874-879.
7. Liu S, Le May C, Wong WP, Ward RD, Clegg DJ, Marcelli M et al. Importance of extranuclear estrogen receptor-alpha and membrane G protein-coupled estrogen receptor in pancreatic islet survival. Diabetes 2009; 58: 2292-2302.
8. Alonso-Magdalena P, Ropero AB, Soriano S, Quesada I, Nadal A. Bisphenol-A: a new diabetogenic factor? Hormones (Athens) 2010; 9: 118-126.
9. Ropero AB, Alonso-Magdalena P, García-García E, Ripoll C, Fuentes E, Nadal A. Bisphenol-A disruption of the endocrine pancreas and blood glucose homeostasis. Int J Androl 2008; 31: 194-200.
10. Mirmira P, Evans-Molina C. Bisphenol A, obesity, and type 2 diabetes mellitus: genuine concern or unnecessary preoccupation? Transl Res 2014; 164: 13-21.
11. Fenichel P, Chevalier N, Brucker-Davis F. Bisphenol A: an endocrine and metabolic disruptor. Ann Endocrinol (Paris) 2013; 74: 211-220.
12. Andra SS, Kalyvas H, Andrianou XD, Charisiadis P, Christophi CA, Makris KC. Preliminary evidence of the association between monochlorinated bisphenol A exposure and type II diabetes mellitus: a pilot study. J Environ Sci Health A Tox Hazard Subst Environ Eng 2015; 50: 243-259.
13. EFSA CEF Panel. Scientific Opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs: Part I-Exposure assessment. EFSA J 2015; 13: 3978.
14. EFSA CEF Panel. Scientific Opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs: PART II-Toxicological assessment and risk characterisation. EFSA J 2015; 13: 3978.
15. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol 2007; 24: 139-177.
16. Fernandez MF, Arrebola JP, Taoufiki J, Navalón A, Ballesteros O, Pulgar R et al. Bisphenol-A and chlorinated derivatives in adipose tissue of women. Reprod Toxicol 2007; 24: 259-264.
17. Calafat AM, Ye X, Wong L-Y, Reidy JA, Needham LL. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect 2008; 116: 39-44.
18. Shankar A, Teppala S. Relationship between urinary bisphenol A levels and diabetes mellitus. J Clin Endocrinol Metab 2011; 96: 3822-3826.
19. Quesada I, Fuentes E, Viso-León MC, Soria B, Ripoll C, Nadal A. Low doses of the endocrine disruptor bisphenol-A and the native hormone 17beta-estradiol rapidly activate transcription factor CREB. FASEB J 2002; 16: 1671-1673.
20. Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A. The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Environ Health Perspect 2006; 114: 106-112.
21. Alonso-Magdalena P, Vieira E, Soriano S, Menes L, Burks D, Quesada I et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect 2010; 118: 1243-1250.
22. Soriano S, Alonso-Magdalena P, García-Arévalo M, Novials A, Muhammed SJ, Salehi A et al. Rapid insulinotropic action of low doses of bisphenol-A on mouse and human islets of Langerhans: role of estrogen receptor β. PLoS One 2012; 7: e31109.
23. Song L, Xia W, Zhou Z, Li Y, Lin Y, Wei J et al. Low-level phenolic estrogen pollutants impair islet morphology and β-cell function in isolated rat islets. J Endocrinol 2012; 215: 303-311.
24. Alonso-Magdalena P, Ropero AB, Carrera MP, Cederroth CR, Baquié M, Gauthier BR et al. Pancreatic insulin content regulation by the estrogen receptor ER alpha. PLoS One 2008; 3: e2069.
25. Lin Y, Sun X, Qiu L, Wei J, Huang Q, Fang C et al. Exposure to bisphenol A induces dysfunction of insulin secretion and apoptosis through the damage of mitochondria in rat insulinoma (INS-1) cells. Cell Death Dis 2013; 4: e460.
26. Alonso-Magdalena P, Ropero AB, Soriano S, García-Arévalo M, Ripoll C, Fuentes E et al. Bisphenol-A acts as a potent estrogen via non-classical estrogen triggered pathways. Mol Cell Endocrinol 2012; 355: 201-207.
27. Pottenger LH, Domoradzki JY, Markham DA, Hansen SC, Cagen SZ, Waechter JM Jr. The relative bioavailability and metabolism of bisphenol A in rats is dependent upon the route of administration. Toxicol Sci 2000; 54: 3-18.
28. Bindhumol V, Chitra KC, Mathur PP. Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology 2003; 188: 117-124.
29. Hanioka N, Jinno H, Nishimura T, Ando M. Suppression of male-specific cytochrome P450 isoforms by bisphenol A in rat liver. Arch Toxicol 1998; 72: 387-394.
30. Rönn M, Kullberg J, Karlsson H, Berglund J, Malmberg F, Orberg J et al. Bisphenol A exposure increases liver fat in juvenile fructose-fed Fischer 344 rats. Toxicology 2013; 303: 125-132.
31. Marmugi A, Ducheix S, Lasserre F, Polizzi A, Paris A, Priymenko N et al. Low doses of bisphenol A induce gene expression related to lipid synthesis and trigger triglyceride accumulation in adult mouse liver. Hepatology 2012; 55: 395-407.
32. Xia W, Jiang Y, Li Y, Wan Y, Liu J, Ma Y et al. Early-life exposure to bisphenol a induces liver injury in rats involvement of mitochondria-mediated apoptosis. PLoS One 2014; 9: e90443.
33. MaY, XiaW, Wang DQ, Wan YJ, XuB, Chen X et al. Hepatic DNA methylation modifications in early development of rats resulting from perinatal BPA exposure contribute to insulin resistance in adulthood. Diabetologia 2013; 56: 2059-2067.
34. Harding AK, Daston GP, Boyd GR, Lucier GW, Safe SH, Stewart J et al. Endocrine disrupting chemicals research program of the U.S. Environmental Protection Agency: summary of a peer-review report. Environ Health Perspect 2006; 114: 1276-1282.
35. Hamadeh HK. Prediction of Compound Signature Using High Density Gene Expression Profiling. Toxicol Sci 2002; 67: 232-240.
36. Kiyosawa N, Manabe S, Yamoto T, Sanbuissho A. Practical application of toxicogenomics for profiling toxicant-induced biological perturbations. Int J Mol Sci 2010; 11: 3397-3412.
37. Degoul F, Brulé H, Cepanec C, Helm M, Marsac C, Leroux J et al. Isoleucylation properties of native human mitochondrial tRNAIle and tRNAIle transcripts. Implications for cardiomyopathy-related point mutations (4269, 4317) in the tRNAIle gene. Hum Mol Genet 1998; 7: 347-354.
38. Kanak MA, Takita M, Kunnathodi F, Lawrence MC, Levy MF, Naziruddin B. Inflammatory response in islet transplantation. Int J Endocrinol 2014; 2014: 451035.
39. Thomas DA, Stauffer C, Zhao K, Yang H, Sharma VK, Szeto HH et al. Mitochondrial targeting with antioxidant peptide SS-31 prevents mitochondrial depolarization, reduces islet cell apoptosis, increases islet cell yield, and improves posttransplantation function. JAmSoc Nephrol 2007; 18: 213-222.
40. Federici M, Hribal M, Perego L, Ranalli M, Caradonna Z, Perego C et al. High glucose causes apoptosis in cultured human pancreatic islets of Langerhans: a potential role for regulation of specific Bcl family genes toward an apoptotic cell death program. Diabetes 2001; 50: 1290-1301.
41. Broniowska KA, Mathews CE, Corbett JA. Do β-cells generate peroxynitrite in response to cytokine treatment? J Biol Chem 2013; 288: 36567-36578.
42. Gentilcore D, Porreca I, Rizzo F, Ganbaatar E, Carchia E, Mallardo M et al. Bisphenol A interferes with thyroid specific gene expression. Toxicology 2013; 304: 21-31.
43. Sun SC, Ganchi PA, Ballard DW, Greene WC. NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway. Science 1993; 259: 1912-1915.
44. Ohzato H, Porter J, Monaco AP, Montana E, Maki T. Minimum number of islets required to maintain euglycemia and their reduced immunogenicity after transplantation into diabetic mice. Transplantation 1993; 56: 270-274.
45. Kang HS, Yang H, Ahn C, Kang HY, Hong EJ, Jaung EB. Effects of xenoestrogens on streptozotocin-induced diabetic mice. J Physiol Pharmacol 2014; 65: 273-282.
46. Huc L, Lemarié A, Guéraud F, Héliès-Toussaint C. Low concentrations of bisphenol A induce lipid accumulation mediated by the production of reactive oxygen species in the mitochondria of HepG2 cells. Toxicol In Vitro 2012; 26: 709-717.
47. Supale S, Li N, Brun T, Maechler P. Mitochondrial dysfunction in pancreatic β cells. Trends Endocrinol Metab 2012; 23: 477-487.
48. Maechler P, Kennedy ED, Pozzan T, Wollheim CB. Mitochondrial activation directly triggers the exocytosis of insulin in permeabilized pancreatic beta-cells. EMBO J 1997; 16: 3833-3841.
49. Wang P, Luo C, Li Q, Chen S, Hu Y. Mitochondrion-mediated apoptosis is involved in reproductive damage caused by BPA in male rats. Environ Toxicol Pharmacol 2014; 38: 1025-1033.
50. Santulli G, Pagano G, Sardu C, Xie W, Reiken S, D'Ascia SL et al. Calcium release channel RyR2 regulates insulin release and glucose homeostasis. J Clin Invest 2015; 125: 1968-1978.
51. Kovacic P. How safe is bisphenol A? Fundamentals of toxicity: metabolism, electron transfer and oxidative stress. Med Hypotheses 2010; 75: 1-4.
52. Gloire G, Legrand-Poels S, Piette J. NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol 2006; 72: 1493-1505.
53. Graciano MFR, Valle MMR, Kowluru A, Curi R, Carpinelli AR. Regulation of insulin secretion and reactive oxygen species production by free fattyacids in pancreatic islets. Islets 2011; 3: 213-223.
54. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010; 87: 4-14.
55. Natalicchio A, Labarbuta R, Tortosa F, Biondi G, Marrano N, Peschechera A et al. Exendin-4 protects pancreatic beta cells from palmitate-induced apoptosis by interfering with GPR40 and the MKK4/7 stress kinase signalling pathway. Diabetologia 2013; 56: 2456-2466.
56. Chowdhury A, Dyachok O, Tengholm A, Sandler S, Bergsten P. Functional differences between aggregated and dispersed insulin-producing cells. Diabetologia 2013; 56: 1557-1568.
57. Li W-C, Ralphs KL, Tosh D. Isolation and culture of adult mouse hepatocytes. Methods Mol Biol 2010; 633: 185-196.
58. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 2007; 8: R19.
59. Porreca I, D'Angelo F, Gentilcore D, Carchia E, Amoresano A, Affuso A et al. Cross-species toxicogenomic analyses and phenotypic anchoring in response to groundwater low-level pollution. BMC Genomics 2014; 15: 1067.
60. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix Gene Chip probe level data. Nucleic Acids Res 2003; 31: e15.
61. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A et al. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 2005; 21: 2933-2942.