Gestational exposure to di(2-ethylhexyl) phthalate (DEHP) impairs pancreatic β-cell function in F1 rat offspring

Toxicology Letters

Volumn 232, Issue 1, 2015, Pages 46-57

  Rajesh, P ^a   Balasubramanian, K ^a  

^a UNIVERSITY OF MADRAS   (India)

Author keywords

Di(2 ethylhexyl) phthalate; Endocrine disruptor; Insulin; MafA; cell

Indexed keywords

DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; GLUCOKINASE; GLUCOSE; GLUCOSE TRANSPORTER 2; HISTONE DEACETYLASE 2; INSULIN; MESSENGER RNA; MICRORNA; OLIVE OIL; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; PROTEIN KINASE B; ENDOCRINE DISRUPTOR; GLUCOSE BLOOD LEVEL; PLASTICIZER;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL GENE; DNA METHYLATION; EPIGENETICS; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; INSULIN RELEASE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN WEIGHT; PANCREAS INSUFFICIENCY; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PREGNANCY; PRENATAL EXPOSURE; PROGENY; RAT; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BLOOD; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GESTATIONAL AGE; INSULIN RESISTANCE; MATERNAL EXPOSURE; METABOLISM; NEWBORN; PATHOLOGY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BLOOD GLUCOSE; DIETHYLHEXYL PHTHALATE; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GESTATIONAL AGE; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MATERNAL EXPOSURE; PLASTICIZERS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS, WISTAR; RNA, MESSENGER;

EID: 84909994284     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.09.025     Document Type: Article

References (78)

1. Ban N., Yamada Y., Someya Y., Miyawaki K., Ihara Y., Hosokawa M., Toyokuni S., Tsuda K., Seino Y. Hepatocyte nuclear factor-1alpha recruits the transcriptional co-activator p300 on the GLUT2 gene promoter. Diabetes 2002, 51:1409-1418.
2. Bennett A.M., Tonks N.K. Regulation of distinct stages of skeletal muscle differentiation by mitogen-activated protein kinases. Science 1997, 278:1288-1291.
3. Berman T., Hochner-Celnikier D., Calafat A.M., Needham L.L., Amitai Y., Wormser U., Richter E. Phthalate exposure among pregnant women in Jerusalem, Israel: results of a pilot study. Environ. Int. 2009, 35:353-357.
4. Bernal A.J., Jirtle R.L. Epigenomic disruption: the effects of early developmental exposures. Birth defects research Part A. Clinic. Mol. Teratol. 2010, 88:938-944.
5. Bouzakri K., Roques M., Gual P., Espinosa S., Guebre-Egziabher F., Riou J.P., Laville M., Le Marchand-Brustel Y., Tanti J.F., Vidal H. Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 2003, 52:1319-1325.
6. Brissova M., Shiota M., Nicholson W.E., Gannon M., Knobel S.M., Piston D.W., Wright C.V., Powers A.C. Reduction in pancreatic transcription factor PDX-1 impairs glucose-stimulated insulin secretion. J. Biol. Chem. 2002, 277:11225-11232.
7. Brun T., Gauthier B.R. A focus on the role of Pax4 in mature pancreatic islet beta-cell expansion and survival in health and disease. J. Mol. Endocrinol. 2008, 40:37-45.
8. Butler A.E., Janson J., Bonner-Weir S., Ritzel R., Rizza R.A., Butler P.C. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52:102-110.
9. Cantonwine D.E., Cordero J.F., Rivera-Gonzalez L.O., Anzalota Del Toro L.V., Ferguson K.K., Mukherjee B., Calafat A.M., Crespo N., Jimenez-Velez B., Padilla I.Y., Alshawabkeh A.N., Meeker J.D. Urinary phthalate metabolite concentrations among pregnant women in Northern Puerto Rico: distribution, temporal variability, and predictors. Environ. Int. 2014, 62:1-11.
10. Carter J.D., Dula S.B., Corbin K.L., Wu R., Nunemaker C.S. A practical guide to rodent islet isolation and assessment. Biol. Proced. Online 2009, 11:3-31.
11. Casals-Casas C., Desvergne B. Endocrine disruptors: from endocrine to metabolic disruption. Annu. Rev. Physiol. 2011, 73:135-162.
12. Chan C.B., De Leo D., Joseph J.W., McQuaid T.S., Ha X.F., Xu F., Tsushima R.G., Pennefather P.S., Salapatek A.M., Wheeler M.B. Increased uncoupling protein-2 levels in beta-cells are associated with impaired glucose-stimulated insulin secretion: mechanism of action. Diabetes 2001, 50:1302-1310.
13. Chan C.B., Saleh M.C., Koshkin V., Wheeler M.B. Uncoupling protein 2 and islet function. Diabetes 2004, 53(Suppl. 1):S136-142.
14. Dayeh T., Volkov P., Salo S., Hall E., Nilsson E., Olsson A.H., Kirkpatrick C.L., Wollheim C.B., Eliasson L., Ronn T., Bacos K., Ling C. Genome-wide DNA methylation analysis of human pancreatic islets from type 2 diabetic and non-diabetic donors identifies candidate genes that influence insulin secretion. PLoS Genet. 2014, 10:e1004160.
15. Diamanti-Kandarakis E., Bourguignon J.P., Giudice L.C., Hauser R., Prins G.S., Soto A.M., Zoeller R.T., Gore A.C. Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr. Rev. 2009, 30:293-342.
16. Dombrowski L., Roy D., Marcotte B., Marette A. A new procedure for the isolation of plasma membranes, T tubules, and internal membranes from skeletal muscle. Am. J. Physiol. 1996, 270:E667-676.
17. El Ouaamari A., Baroukh N., Martens G.A., Lebrun P., Pipeleers D., van Obberghen E. miR-375 targets 3'-phosphoinositide-dependent protein kinase-1 and regulates glucose-induced biological responses in pancreatic beta-cells. Diabetes 2008, 57:2708-2717.
18. Enke U., Schleussner E., Palmke C., Seyfarth L., Koch H.M. Phthalate exposure in pregnant women and newborns - the urinary metabolite excretion pattern differs distinctly. Int. J. Hyg. Environ. Health 2013, 216:735-742.
19. Ferguson K.K., McElrath T.F., Meeker J.D. Environmental phthalate exposure and preterm birth. JAMA Pediatr. 2013.
20. Fonseca S.G., Urano F., Burcin M., Gromada J. Stress hypERactivation in the beta-cell. Islets 2010, 2:1-9.
21. Gosmain Y., Katz L.S., Masson M.H., Cheyssac C., Poisson C., Philippe J. Pax6 is crucial for beta-cell function, insulin biosynthesis, and glucose-induced insulin secretion. Mol. Endocrinol. 2012, 26:696-709.
22. Goward C.R., Atkinson T., Scawen M.D. Rapid purification of glucokinase and glycerokinase from Bacillus stearothermophilus by hydrophobic interaction chromatography. J. Chromatogr. 1986, 369:235-239.
23. Grandjean P., Bellinger D., Bergman A., Cordier S., Davey-Smith G., Eskenazi B., Gee D., Gray K., Hanson M., van den Hazel P., Heindel J.J., Heinzow B., Hertz-Picciotto I., Hu H., Huang T.T., Jensen T.K., Landrigan P.J., McMillen I.C., Murata K., Ritz B., Schoeters G., Skakkebaek N.E., Skerfving S., Weihe P. The faroes statement: human health effects of developmental exposure to chemicals in our environment. Basic Clin. Pharmacol. Toxicol. 2008, 102:73-75.
24. Gupta R.K., Vatamaniuk M.Z., Lee C.S., Flaschen R.C., Fulmer J.T., Matschinsky F.M., Duncan S.A., Kaestner K.H. The MODY1 gene HNF-4alpha regulates selected genes involved in insulin secretion. J. Clin. Invest. 2005, 115:1006-1015.
25. Hao C., Cheng, X., Guo J., Xia H., Ma, X., 2013. Perinatal exposure to diethyl-hexyl-phthalate induces obesity in mice. Front Biosci (Elite Ed) 5, 725-733.
26. Hatch E.E., Nelson J.W., Qureshi M.M., Weinberg J., Moore L.L., Singer M., Webster T.F. Association of urinary phthalate metabolite concentrations with body mass index and waist circumference: a cross-sectional study of NHANES data, 1999-2002. Environ. Health 2008, 7:27.
27. Heimberg H., De Vos A., Vandercammen A., Van Schaftingen E., Pipeleers D., Schuit F. Heterogeneity in glucose sensitivity among pancreatic beta-cells is correlated to differences in glucose phosphorylation rather than glucose transport. EMBO J. 1993, 12:2873-2879.
28. Janjua N.R., Frederiksen H., Skakkebaek N.E., Wulf H.C., Andersson A.M. Urinary excretion of phthalates and paraben after repeated whole-body topical application in humans. Int. J. Androl. 2008, 31:118-130.
29. Jiang M., Zhang Y., Liu M., Lan M.S., Fei J., Fan W., Gao X., Lu D. Hypermethylation of hepatic glucokinase and L-type pyruvate kinase promoters in high-fat diet-induced obese rats. Endocrinology 2011, 152:1284-1289.
30. Jordan S.D., Kruger M., Willmes D.M., Redemann N., Wunderlich F.T., Bronneke H.S., Merkwirth C., Kashkar H., Olkkonen V.M., Bottger T., Braun T., Seibler J., Bruning J.C. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat. Cell Bio. 2011, 13:434-446.
31. Kaiser C., James S.R. Acetylation of insulin receptor substrate-1 is permissive for tyrosine phosphorylation. BMC Bio. 2004, 2:23.
32. Kaneto H., Matsuoka T.A., Kawashima S., Yamamoto K., Kato K., Miyatsuka T., Katakami N., Matsuhisa M. Role of MafA in pancreatic beta-cells. Adv. Drug Deliv. Rev. 2009, 61:489-496.
33. Kaneto H., Miyatsuka T., Kawamori D., Yamamoto K., Kato K., Shiraiwa T., Katakami N., Yamasaki Y., Matsuhisa M., Matsuoka T.A. PDX-1 and MafA play a crucial role in pancreatic beta-cell differentiation and maintenance of mature beta-cell function. Endocr. J. 2008, 55:235-252.
34. Kitamura T., Ido Kitamura Y. Role of FoxO Proteins in Pancreatic beta Cells. Endocr. J. 2007, 54:507-515.
35. Kitamura T., Nakae J., Kitamura Y., Kido Y., Biggs W.H., Wright C.V., White M.F., Arden K.C., Accili D. The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth. J. Clin. Invest. 2002, 110:1839-1847.
36. Kuroda A., Rauch T.A., Todorov I., Ku H.T., Al-Abdullah I.H., Kandeel F., Mullen Y., Pfeifer G.P., Ferreri K. Insulin gene expression is regulated by DNA methylation. PloS One 2009, 4:e6953.
37. Lacy P.E., Kostianovsky M. Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes 1967, 16:35-39.
38. Law C.M., Barker D.J., Osmond C., Fall C.H., Simmonds S.J. Early growth and abdominal fatness in adult life. J. Epidemiol. Community Health 1992, 46:184-186.
39. Leibiger I.B., Leibiger B., Berggren P.O. Insulin signaling in the pancreatic beta-cell. Annu. Rev. Nutrition 2008, 28:233-251.
40. Lin Y., Wei J., Li Y., Chen J., Zhou Z., Song L., Wei Z., Lv Z., Chen X., Xia W., Xu S. Developmental exposure to di(2-ethylhexyl) phthalate impairs endocrine pancreas and leads to long-term adverse effects on glucose homeostasis in the rat. Am. J. Physiol. Endocrinol. Metab. 2011, 301:E527-538.
41. Lind P.M., Zethelius B., Lind L. Circulating levels of phthalate metabolites are associated with prevalent diabetes in the elderly. Diabetes Care 2012, 35:1519-1524.
42. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
43. Luan B., Zhao J., Wu H., Duan B., Shu G., Wang X., Li D., Jia W., Kang J., Pei G. Deficiency of a beta-arrestin-2 signal complex contributes to insulin resistance. Nature 2009, 457:1146-1149.
44. Main K.M., Mortensen G.K., Kaleva M.M., Boisen K.A., Damgaard I.N., Chellakooty M., Schmidt I.M., Suomi A.M., Virtanen H.E., Petersen D.V., Andersson A.M., Toppari J., Skakkebaek N.E. Human breast milk contamination with phthalates and alterations of endogenous reproductive hormones in infants three months of age. Environ. Health Perspect. 2006, 114:270-276.
45. Martinez-Arguelles D.B., McIntosh M., Rohlicek C.V., Culty M., Zirkin B.R., Papadopoulos V. Maternal in utero exposure to the endocrine disruptor di-(2-ethylhexyl) phthalate affects the blood pressure of adult male offspring. Toxicol. Appl. Pharmacol. 2013, 266:95-100.
46. Miyake K., Horikawa Y., Hara K., Yasuda K., Osawa H., Furuta H., Hirota Y., Yamagata K., Hinokio Y., Oka Y., Iwasaki N., Iwamoto Y., Yamada Y., Seino Y., Maegawa H., Kashiwagi A., Yamamoto K., Tokunaga K., Takeda J., Makino H., Nanjo K., Kadowaki T., Kasuga M. Association of TCF7L2 polymorphisms with susceptibility to type 2 diabetes in 4087 Japanese subjects. J. Human Genet. 2008, 53:174-180.
47. Morgan C.R., Lazarow A. Immunoassay of pancreatic and plasma insulin following alloxan injection of rats. Diabetes 1965, 14:669-671.
48. Odom D.T., Zizlsperger N., Gordon D.B., Bell G.W., Rinaldi N.J., Murray H.L., Volkert T.L., Schreiber J., Rolfe P.A., Gifford D.K., Fraenkel E., Bell G.I., Young R.A. Control of pancreas and liver gene expression by HNF transcription factors. Science 2004, 303:1378-1381.
49. Okada T., Liew C.W., Hu J., Hinault C., Michael M.D., Krtzfeldt J., Yin C., Holzenberger M., Stoffel M., Kulkarni R.N. Insulin receptors in beta-cells are critical for islet compensatory growth response to insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8977-8982.
50. Oyadomari S., Araki E., Mori M. Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis: An Int. J. Program. Cell Death 2002, 7:335-345.
51. Pearson S.D., Trissel L.A. Leaching of diethylhexyl phthalate from polyvinyl chloride containers by selected drugs and formulation components. Am. J. Hospital Pharm. 1993, 50:1405-1409.
52. Poy M.N., Eliasson L., Krutzfeldt J., Kuwajima S., Ma X., Macdonald P.E., Pfeffer S., Tuschl T., Rajewsky N., Rorsman P., Stoffel M. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004, 432:226-230.
53. Rajesh P., Balasubramanian K. Di(2-ethylhexyl) phthalate exposure impairs insulin receptor and glucose transporter 4 gene expression in L6 myotubes. Human Exp. Toxicol. 2013, 33:685-700.
54. Rajesh P., Sathish S., Srinivasan C., Selvaraj J., Balasubramanian K. Phthalate is associated with insulin resistance in adipose tissue of male rat: role of antioxidant vitamins. J. Cellular Biochem. 2013, 114:558-569.
55. Rengarajan S., Parthasarathy C., Anitha M., Balasubramanian K. Diethylhexyl phthalate impairs insulin binding and glucose oxidation in Chang liver cells. Toxicol. in vitro 2007, 21:99-102.
56. Rhodes C.J., White M.F., Leahy J.L., Kahn S.E. Direct autocrine action of insulin on beta-cells: does it make physiological sense?. Diabetes 2013, 62:2157-2163.
57. Sander M., Neubuser A., Kalamaras J., Ee H.C., Martin G.R., German M.S. Genetic analysis reveals that PAX6 is required for normal transcription of pancreatic hormone genes and islet development. Genes Dev. 1997, 11:1662-1673.
58. Sathyanarayana S., Barrett E., Butts S., Wang C.W., Swan S. Phthalate exposure and reproductive hormone concentrations in pregnancy. Reproduction 2013.
59. Schuit F.C., Huypens P., Heimberg H., Pipeleers D.G. Glucose sensing in pancreatic beta-cells: a model for the study of other glucose-regulated cells in gut, pancreas, and hypothalamus. Diabetes 2001, 50:1-11.
60. Seo H.Y., Kim Y.D., Lee K.M., Min A.K., Kim M.K., Kim H.S., Won K.C., Park J.Y., Lee K.U., Choi H.S., Park K.G., Lee I.K. Endoplasmic reticulum stress-induced activation of activating transcription factor 6 decreases insulin gene expression via up-regulation of orphan nuclear receptor small heterodimer partner. Endocrinology 2008, 149:3832-3841.
61. Shelby, M.D., 2006. NTP-CERHR monograph on the potential human reproductive and developmental effects of di (2-ethylhexyl) phthalate (DEHP). Ntp Cerhr Mon v, vii-7, II-iii-xiii passim.
62. Sosa-Pineda B. The gene Pax4 is an essential regulator of pancreatic beta-cell development. Mol. Cells 2004, 18:289-294.
63. Sosa-Pineda B., Chowdhury K., Torres M., Oliver G., Gruss P. The Pax4 gene is essential for differentiation of insulin-producing beta cells in the mammalian pancreas. Nature 1997, 386:399-402.
64. Srinivasan C., Khan A.I., Balaji V., Selvaraj J., Balasubramanian K. Diethyl hexyl phthalate-induced changes in insulin signaling molecules and the protective role of antioxidant vitamins in gastrocnemius muscle of adult male rat. Toxicol. Appl. Pharmacol. 2011, 257:155-164.
65. Stahlhut R.W., van Wijngaarden E., Dye T.D., Cook S., Swan S.H. Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult US males. Environ. Health Perspect. 2007, 115:876-882.
66. Stocker C.J., Arch J.R., Cawthorne M.A. Fetal origins of insulin resistance and obesity. Proc. Nutr. Soc. 2005, 64:143-151.
67. Stoffel M., Duncan S.A. The maturity-onset diabetes of the young (MODY1) transcription factor HNF4alpha regulates expression of genes required for glucose transport and metabolism. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:13209-13214.
68. Svensson K., Hernandez-Ramirez R.U., Burguete-Garcia A., Cebrian M.E., Calafat A.M., Needham L.L., Claudio L., Lopez-Carrillo L. Phthalate exposure associated with self-reported diabetes among Mexican women. Environ. Res. 2011, 111:792-796.
69. Tefre de Renzy-Martin K., Frederiksen H., Christensen J., Boye Kyhl H., Andersson A.M., Husby S., Barington T., Main K.M., Jensen T.K. Current exposure of 200 pregnant Danish women to phthalates, parabens and phenols. Reproduction 2013.
70. Trasande L., Sathyanarayana S., Jo Messito M., Attina T.M., Mendelsohn A.L. Phthalates and the diets of U. S. children and adolescents. Environ. Res. 2013, 126:84-90.
71. Volkmar M., Dedeurwaerder S., Cunha D.A., Ndlovu M.N., Defrance M., Deplus R., Calonne E., Volkmar U., Igoillo-Esteve M., Naamane N., Del Guerra S., Masini M., Bugliani M., Marchetti P., Cnop M., Eizirik D.L., Fuks F. DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from type 2 diabetic patients. EMBO J. 2012, 31:1405-1426.
72. Wang H., Brun T., Kataoka K., Sharma A.J., Wollheim C.B. MAFA controls genes implicated in insulin biosynthesis and secretion. Diabetologia 2007, 50:348-358.
73. Wang H., Maechler P., Antinozzi P.A., Hagenfeldt K.A., Wollheim C.B. Hepatocyte nuclear factor 4alpha regulates the expression of pancreatic beta-cell genes implicated in glucose metabolism and nutrient-induced insulin secretion. J. Biol. Chem. 2000, 275:35953-35959.
74. Xu G.G., Rothenberg P.L. Insulin receptor signaling in the beta-cell influences insulin gene expression and insulin content: evidence for autocrine beta-cell regulation. Diabetes 1998, 47:1243-1252.
75. Yamagata K., Furuta H., Oda N., Kaisaki P.J., Menzel S., Cox N.J., Fajans S.S., Signorini S., Stoffel M., Bell G.I. Mutations in the hepatocyte nuclear factor-4alpha gene in maturity-onset diabetes of the young (MODY1). Nature 1996, 384:458-460.
76. Yuan Q., Chen L., Liu C., Xu K., Mao X. Postnatal pancreatic islet beta cell function and insulin sensitivity at different stages of lifetime in rats born with intrauterine growth retardation. PloS one 2011, 6:e25167.
77. Zhao J., Goldberg J., Bremner J.D., Vaccarino V. Global DNA methylation is associated with insulin resistance: a monozygotic twin study. Diabetes 2012, 61:542-546.
78. Zhao L., Li Z., Kullin M., Borg L.A., Karlsson F.A. Alterations in net glucose uptake and in the pancreatic B-cell GLUT2 transporter induced by diazoxide and by secretory stimuli. J. Endocrinol. 2005, 185:291-299.