Prenatal exposure to bisphenol A alters mouse fetal pancreatic morphology and islet composition

Hormone Molecular Biology and Clinical Investigation

Volumn 25, Issue 3, 2016, Pages 171-179

  Whitehead, Rebecca ^a   Guan, Haiyan ^a   Arany, Edith ^a   Cernea, Maria ^a   Yang, Kaiping ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

Bisphenol A; developmental exposure; endocrine disrupting chemical; pancreatic development

Indexed keywords

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

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS; IMMUNOHISTOCHEMISTRY; MALE; MORPHOLOGY; MOUSE; NONHUMAN; ORGANOGENESIS; PANCREAS DEVELOPMENT; PANCREAS ISLET; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; PATHOLOGY; PREGNANCY; ULTRASTRUCTURE;

ANIMALS; BENZHYDRYL COMPOUNDS; ENDOCRINE DISRUPTORS; FEMALE; GLUCAGON-SECRETING CELLS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84979463269     PISSN: 18681883     EISSN: 18681891     Source Type: Journal    
DOI: 10.1515/hmbci-2015-0052     Document Type: Article

References (57)

1. Rubin BS. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 2011;127:27-34.
2. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect 2010;118:1055-70.
3. CDC. Centers for Disease Control and Prevention: Fourth national report on human exposure to environmental chemicals. Department of Health and Human Services: National Center for Environmental Health 2010; online: http://www.cdc.gov/exposurereport/pdf/FourthReport-Executive Summary.pdf.
4. Rochester JR. Bisphenol A and human health: a review of the literature. Reprod Toxicol 2013;42:132-55.
5. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008;359:61-73.
6. Gerona RR, Woodruff TJ, Dickenson CA, Pan J, Schwartz JM, Sen S, Friesen MW, Fujimoto VY, Hunt PA. Bisphenol-A (BPA), BPA glucuronide, and BPA sulfate in midgestation umbilical cord serum in a northern and central California population. Environ Sci Technol 2013;47:12477-85.
7. Nishikawa M, Iwano H, Yanagisawa R, Koike N, Inoue H, Yokota H. Placental transfer of conjugated bisphenol A and subsequent reactivation in the rat fetus. Environ Health Perspect 2010;118:1196-203.
8. Elsworth JD, Jentsch JD, Vandevoort CA, Roth RH, Redmond Jr DE, Leranth C. Prenatal exposure to bisphenol A impacts midbrain dopamine neurons and hippocampal spine synapses in nonhuman primates. Neurotoxicology 2013;35:113-20.
9. Chapalamadugu KC, Vandevoort CA, Settles ML, Robison BD, Murdoch GK. Maternal bisphenol a exposure impacts the fetal heart transcriptome. PLoS One 2014;9:e89096.
10. Tharp AP, Maffini MV, Hunt PA, VandeVoort CA, Sonnenschein C, Soto AM. Bisphenol A alters the development of the rhesus monkey mammary gland. Proc Natl Acad Sci USA 2012;109:8190-5.
11. Vandenberg LN, Maffini MV, Wadia PR, Sonnenschein C, Rubin BS, Soto AM. Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 2007;148:116-27.
12. Calhoun KC, Padilla-Banks E, Jefferson WN, Liu L, Gerrish KE, Young SL, Wood CE, Hunt PA, Vandevoort CA, Williams CJ. Bisphenol A exposure alters developmental gene expression in the fetal rhesus macaque uterus. PLoS One 2014;9:e85894.
13. Susiarjo M, Hassold TJ, Freeman E, Hunt PA. Bisphenol a exposure in utero disrupts early oogenesis in the mouse. PLoS Genetics 2007;3:e5.
14. Horstman KA, Naciff JM, Overmann GJ, Foertsch LM, Richardson BD, Daston GP. Effects of transplacental 17-alphaethynyl estradiol or bisphenol A on the developmental profile of steroidogenic acute regulatory protein in the rat testis. Birth Defects Res B Dev Reprod Toxicol 2012;95:318-25.
15. DeBenedictis B, Guan H, Yang K. Prenatal exposure to bisphenol a disrupts mouse fetal liver maturation in a sex-specific manner. J Cell Biochem 2016;117:344-50.
16. Hijazi A, Guan H, Cernea M, Yang K. Bisphenol A exposure to pregnant mice disrupts fetal lung development. FASEB J 2015;29:4968-77.
17. LaKind JS, Goodman M, Mattison DR. Bisphenol A and indicators of obesity, glucose metabolism/type 2 diabetes and cardiovascular disease: a systematic review of epidemiologic research. Cr Rev Toxicol 2014;44:121-50.
18. Alonso-Magdalena P, Burks D, Menes L, Nadal A, Quesada I, Soriano S, Vieira E. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect 2010;118:1243-50.
19. Liu J, Yu P, Qian W, Li Y, Zhao J, Huan F, Wang J, Xiao H. Perinatal bisphenol A exposure and adult glucose homeostasis: identifying critical windows of exposure. PLoS One 2013;8:e64143.
20. Angle BM, Do RP, Ponzi D, Stahlhut RW, Drury BE, Nagel SC, Welshons WV, Besch-Williford CL, Palanza P, Parmigiani S, vom Saal FS, Taylor JA. Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation. Reprod Toxicol 2013;42:256-68.
21. Bodin J, Bølling AK, Becher R, Kuper F, Løvik M, Nygaard UC. Transmaternal bisphenol A exposure accelerates diabetes type 1 development in NOD mice. Toxicol Sci 2014;137:311-23.
22. Selvaratnam J, Guan H, Koropatnick J, Yang K. Metallothionein-Iand-II-deficient mice display increased susceptibility to cadmium-induced fetal growth restriction. Am J Physiol Endocrinol Metab 2013;305:E727-35.
23. Cox A, Gottheil SK, Arany EJ, Hill DJ. The effects of low protein during gestation on mouse pancreatic development and beta cell regeneration. Pediatr Res 2010;68:16-22.
24. Petrik J, Srinivasan M, Aalinkeel R, Coukell S, Arany E, Patel MS, Hill DJ. A long-term high-carbohydrate diet causes an altered ontogeny of pancreatic islets of Langerhans in the neonatal rat. Pediatr Res 2001;49:84-92.
25. Ramirez Z, Castro MF, Kuri HW. Quantitation of adipose conversion and triglycerides by staining intra-cyctoplasmic lipids with Oil Red O. Histochemistry 1992;97:493-7.
26. IRIS. Reference dose for chronic oral exposure: Bisphenol A Integrated Risk Information System.CASRN 80-05-7 (US-EPA IRIS Substance File) 2012; Available online: http://www.epa.gov/iris/subst/0356.htm.
27. Padmanabhan V, Siefert K, Ransom S, Johnson T, Pinkerton J, Anderson L, Tao L, Kannan K. Maternal bisphenol-A levels at delivery: a looming problem J Perinatol 2008;28:258-63.
28. Weir GC, Bonner-Weir S. Islet cell mass in diabetes and how it relates to function, birth, and death. Ann NY Acad Sci 2013;1281:92-105.
29. Wei J, Lin Y, Li Y, Ying C, Chen J, Song L, Zhou Z, Lv Z, Xia W, Chen X, Xu S. Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology 2011;152:3049-61.
30. Strakovsky RS, Wang H, Engeseth NJ, Flaws JA, Helferich WG, Pan YX, Lezmi S. Developmental bisphenol A (BPA) exposure leads to sex-specific modification of hepatic gene expression and epigenome at birth that may exacerbate high-fat diet-induced hepatic steatosis. Toxicol Appl Pharmacol 2015;284:101-12.
31. Fang C, Ning B, Waqar AB, Niimi M, Li S, Satoh K, Shiomi M, Ye T, Dong S, Fan J. Bisphenol A exposure enhances atherosclerosis in WHHL rabbits. PLoS One 2014;9:e110977.
32. Tushuizen M, Bunck MC, Pouwels PJ, Bontemps S, Van Waesberghe JH, Schindhelm RK, Mari A, Heine RJ, Diamant M. Pancreatic fat content and-cell function in men with and without type 2 diabetes. Diabetes Care 2007;30:2916-21.
33. Van Herpen N, Schrauwen-Hinderling VB. Lipid accumulation in non-adipose tissue and lipotoxicity. Physiol Behav 2008;98:231-41.
34. Oakes ND, Bell KS, Furler SM, Camilleri S, Saha AK, Ruderman NB, Chisholm DJ, Kraegen EW. Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise: parallel relationship between insulin stimulation of glucose uptake and suppression of long-chain fatty acyl-CoA. Diabetes 1997;46:2022-28.
35. Vandenberg L, Maffini MV, Sonnenschein C, Rubin BS, Soto AM. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 2009;30:75-95.
36. Van Assche F, Aerts L, De Prins FA. The fetal endocrine pancreas. Europ J Obstet Gynec Reprod Biol 1984;18:267-72.
37. Hill D, Duvillié B. Pancreatic development and adult diseases. Pediatr Res 2000;48:269-74.
38. Hard W. The origin and differentiation of the alpha and beta cells in the pancreatic islets of the rat. Amer J Anat 1944;75:369-403.
39. Yamaoka T, Itakura M. Development of pancreatic islets (review). Int J Mol Med 1999;3:247-308.
40. Schwitzgebel V, Scheel DW, Connors JR, Kalamaras J, Lee JE, Anderson DJ, Sussel L, Johnson DJ, German MS. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 2000;127:3533-42.
41. Slack J. Developmental biology of the pancreas. Development 1995;121:1569-80.
42. Fowden A, Hill DJ. Intra-uterine programming of the endocrine pancreas. Br Med Bull 2001;60:123-42.
43. Gelling R, Vuguin PM, Du VQ, Cui L, Romer J, Pederson RA, Leiser M, Sorensen H, Holst JJ, Fledelius C, Johansen PB, Fleischer N, McIntosh CH, Nishimura E, Charron MJ. Pancreatic-cell overexpression of the glucagon receptor gene results in enhanced-cell function and mass. Am J Physiol 2009;297:695-707.
44. Reddy S, Elliott RB. Ontogenic development of peptide hormones in the mammalian fetal pancreas. Experientia 1988;44:1-9.
45. Pictet R, Clark WR, Williams RH, Rutter WJ. An ultrastructural analysis of the developing embryonic pancreas. Dev Biol 1972;29:436-567.
46. Dunning BE, Gerich JE. The role of alpha-cell dysregulation in fasting and postprandial hyperglycemia in type 2 diabetes and therapeutic implications. Endocr Rev 2007;28:253-83.
47. Quesada I, Tudurí E, Ripoll C, Nadal A. Physiology of the pancreatic alpha-cell and glucagon secretion: role in glucose homeostasis and diabetes. J Endocrinol 2008;199:5-19.
48. Gaisano HY, MacDonald PE, Vranic M. Glucagon secretion and signaling in the development of diabetes. Front Physiol 2012;3:349.
49. Gerich JE, Langlois M, Noacco C, Karam JH, Forsham PH. Lack of glucagon response to hypoglycaemia in diabetes: evidence for an intrinsic pancreatic alpha cell defect. Science 1973;182:171-3.
50. Cryer PE. Hypoglycemia: the limiting factor in the glycemic management of Type I and Type II diabetes. Diabetologia 2002;4:937-48.
51. van Esterik JC, Dollé ME, Lamoree MH, van Leeuwen SP, Hamers T, Legler J, van der Ven LT. Programming of metabolic effects in C57BL/6JxFVB mice by exposure to bisphenol A during gestation and lactation. Toxicology 2014;321:40-52.
52. Alonso-Magdalena P, Laribi O, Ropero AB. Fuentes E, Ripoll C, Soria B, Nadal A. Low doses of bisphenol A and diethylstilbestrol impair Ca2signals in pancreatic alpha-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans. Environ Health Perspect 2005;113:969-77.
53. Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A. The estrogenic effect of bisphenol A disrupts pancreatic-cell function in vivo and induces insulin resistance. Environ Health Perspect 2006;114:106-12.
54. Alonso-Magdalena P, Ropero A, Carrera MP, Cedderroth CR, Baquie M, Gauthier BR, Nef S, Stefani E, Nadal A. Pancreatic islet content regulation by the estrogen receptor ER. PLoS One 2008;3:e2069.
55. Butler A, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC.-Cell deficit and increased-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-10.
56. Ropero A, Alonso-Magdalena P, Garcia-Garcia 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.
57. Alonso-Magdalena P, Garciá-Arévalo M, Quesada I, Nadal Á. Bisphenol-A treatment during pregnancy in mice: a new window of susceptibility for the development of diabetes in mothers later in life. Endocrinology 2015;156:1659-70.