The emerging role of endocrine disruptors in pathogenesis of insulin resistance: A concept implicating nonalcoholic fatty liver disease

Current Molecular Medicine

Volumn 12, Issue 1, 2012, Pages 68-82

  Polyzos, S A ^a   Kountouras, J ^a   Deretzi, G ^a   Zavos, C ^a   Mantzoros, C S ^b  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bisphenol A; Dioxins; Endocrine disruptors; Insulin resistance; Nonalcoholic fatty liver disease; Nonalcoholic steatohepatitis; Persistent organic pollutants; Phthalates

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; DIOXIN; ENDOCRINE DISRUPTOR; PHTHALIC ACID;

ARTICLE; HUMAN; IN VITRO STUDY; INSULIN RESISTANCE; LIVER TOXICITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; PATHOGENESIS;

EID: 83455218004     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/156652412798376161     Document Type: Article

References (137)

1. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 2009; 30: 293-342.
2. Braw-Tal R. Endocrine disruptors and timing of human exposure. Pediatr Endocrinol Rev 2010; 8: 41-6.
3. Sharpe RM, Drake AJ. Bisphenol a and metabolic syndrome. Endocrinology 2010; 151: 2404-7.
4. Lubick N. EPA releases list of potential endocrine disrupters. Environ Sci Technol 2007; 41: 5170.
5. Baldi F, Mantovani A. A new database for food safety: EDID (Endocrine disrupting chemicals - Diet Interaction Database). Ann Ist Super Sanita 2008; 44: 57-63.
6. Taboureau O, Nielsen SK, Audouze K, et al. ChemProt: a disease chemical biology database. Nucleic Acids Res 2011; 39: 367-72.
7. Soto AM, Sonnenschein C. Environmental causes of cancer: endocrine disruptors as carcinogens. Nat Rev Endocrinol 2010; 6: 363-70.
8. Landau-Ossondo M, Rabia N, Jos-Pelage J, et al. Why pesticides could be a common cause of prostate and breast cancers in the French Caribbean Island, Martinique. An overview on key mechanisms of pesticide-induced cancer. Biomed Pharmacother 2009; 63: 383-95.
9. Walker NJ, Crockett PW, Nyska A, et al. Dose-additive carcinogenicity of a defined mixture of "dioxin-like compounds". Environ Health Perspect 2005; 113: 43-8.
10. Ovando BJ, Ellison CA, Vezina CM, Olson JR. Toxicogenomic analysis of exposure to TCDD, PCB126 and PCB153: identification of genomic biomarkers of exposure to AhR ligands. BMC Genomics 2010; 11: 583.
11. Gore AC. Neuroendocrine targets of endocrine disruptors. Hormones (Athens) 2010; 9: 16-27.
12. Jugan ML, Levi Y, Blondeau JP. Endocrine disruptors and thyroid hormone physiology. Biochem Pharmacol 2010; 79: 939-47.
13. Hatch EE, Nelson JW, Stahlhut RW, Webster TF. Association of endocrine disruptors and obesity: perspectives from epidemiological studies. Int J Androl 2010; 33: 324-32.
14. Newbold RR. Impact of environmental endocrine disrupting chemicals on the development of obesity. Hormones (Athens) 2010; 9: 206-17.
15. Casals-Casas C, Desvergne B. Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol 2011; 73: 135-62.
16. Polyzos SA, Kountouras J, Zavos C. Nonalcoholic fatty liver disease: the pathogenetic roles of insulin resistance and adipocytokines. Curr Mol Med 2009; 9: 299-314.
17. Bellentani S, Marino M. Epidemiology and natural history of non-alcoholic fatty liver disease (NAFLD). Ann Hepatol 2009; 8 (Suppl 1): 4-8.
18. Williams CD, Stengel J, Asike MI, et al. Prevalence of Nonalcoholic Fatty Liver Disease and Nonalcoholic Steatohepatitis among a Largely Middle-Aged Population Utilizing Ultrasound and Liver Biopsy: A Prospective Study. Gastroenterology 2010; 140: 124-31.
19. Loria P, Adinolfi LE, Bellentani S, et al. Practice guidelines for the diagnosis and management of nonalcoholic fatty liver disease. A decalogue from the Italian Association for the Study of the Liver (AISF) Expert Committee. Dig Liver Dis 2010; 42: 272-82.
20. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004; 27: 1047-53.
21. Ben-Jonathan N, Hugo ER, Brandebourg TD. Effects of bisphenol A on adipokine release from human adipose tissue: Implications for the metabolic syndrome. Mol Cell Endocrinol 2009; 304: 49-54.
22. Lim S, Cho YM, Park KS, Lee HK. Persistent organic pollutants, mitochondrial dysfunction, and metabolic syndrome. Ann N Y Acad Sci 2010; 1201: 166-76.
23. Lim JS, Lee DH, Jacobs DR, Jr. Association of brominated flame retardants with diabetes and metabolic syndrome in the U.S. population, 2003-2004. Diabetes Care 2008; 31: 1802-7.
24. Remillard RB, Bunce NJ. Linking dioxins to diabetes: epidemiology and biologic plausibility. Environ Health Perspect 2002; 110: 853-8.
25. Baranova A, Tran TP, Birerdinc A, Younossi ZM. Systematic review: association of polycystic ovary syndrome with metabolic syndrome and non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2011; 33: 801-14.
26. Gasnier C, Dumont C, Benachour N, Clair E, Chagnon MC, Seralini GE. Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines. Toxicology 2009; 262: 184-91.
27. Lu C, Wang Y, Sheng Z, et al. NMR-based metabonomic analysis of the hepatotoxicity induced by combined exposure to PCBs and TCDD in rats. Toxicol Appl Pharmacol 2010; 248: 178-84.
28. Wilczynski NL, Haynes RB. Robustness of empirical search strategies for clinical content in MEDLINE. Proc AMIA Symp 2002; 904-8.
29. Foster WG, Maharaj-Briceno S, Cyr DG. Dioxin-induced changes in epididymal sperm count and spermatogenesis. Environ Health Perspect 2010; 118: 458-64.
30. Kulkarni PS, Crespo JG, Afonso CA. Dioxins sources and current remediation technologies--a review. Environ Int 2008; 34: 139-53.
31. Kern PA, Fishman RB, Song W, Brown AD, Fonseca V. The effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on oxidative enzymes in adipocytes and liver. Toxicology 2002; 171: 117-25.
32. Dragin N, Dalton TP, Miller ML, Shertzer HG, Nebert DW. For dioxin-induced birth defects, mouse or human CYP1A2 in maternal liver protects whereas mouse CYP1A1 and CYP1B1 are inconsequential. J Biol Chem 2006; 281: 18591-600.
33. Diani-Moore S, Ram P, Li X, et al. Identification of the aryl hydrocarbon receptor target gene TiPARP as a mediator of suppression of hepatic gluconeogenesis by 2,3,7,8- tetrachlorodibenzo-p-dioxin and of nicotinamide as a corrective agent for this effect. J Biol Chem 2010; 285: 38801-10.
34. Lee JH, Wada T, Febbraio M, et al. A novel role for the dioxin receptor in fatty acid metabolism and hepatic steatosis. Gastroenterology 2010; 139: 653-63.
35. Kim JH, In YJ, Kim WK, Bae KH, Kang S, Lee SC. Differential signatures of protein glycosylation and phosphorylation in human Chang liver cells induced by TCDD treatment. Toxicol Lett 2008; 178: 20-8.
36. Kern PA, cker-Brown A, Said ST, Kennedy R, Fonseca VA. The stimulation of tumor necrosis factor and inhibition of glucose transport and lipoprotein lipase in adipose cells by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Metabolism 2002; 51: 65-8.
37. Nishiumi S, Yoshida M, Azuma T, Yoshida K, Ashida H. 2,3,7,8-tetrachlorodibenzo-p-dioxin impairs an insulin signaling pathway through the induction of tumor necrosis factor-alpha in adipocytes. Toxicol Sci 2010; 115: 482-91.
38. Marchand A, Tomkiewicz C, Marchandeau JP, Boitier E, Barouki R, Garlatti M. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces insulin-like growth factor binding protein-1 gene expression and counteracts the negative effect of insulin. Mol Pharmacol 2005; 67: 444-52.
39. Hokanson R, Miller S, Hennessey M, Flesher M, Hanneman W, Busbee D. Disruption of estrogen-regulated gene expression by dioxin: downregulation of a gene associated with the onset of non-insulin-dependent diabetes mellitus (type 2 diabetes). Hum Exp Toxicol 2004; 23: 555-64.
40. Hsu HF, Tsou TC, Chao HR, Kuo YT, Tsai FY, Yeh SC. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on adipogenic differentiation and insulin-induced glucose uptake in 3T3-L1 cells. J Hazard Mater 2010; 182: 649-55.
41. Kim YH, Shim YJ, Shin YJ, Sul D, Lee E, Min BH. 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD) induces calcium influx through T-type calcium channel and enhances lysosomal exocytosis and insulin secretion in INS-1 cells. Int J Toxicol 2009; 28: 151-61.
42. Sato S, Shirakawa H, Tomita S, et al. Low-dose dioxins alter gene expression related to cholesterol biosynthesis, lipogenesis, and glucose metabolism through the aryl hydrocarbon receptor-mediated pathway in mouse liver. Toxicol Appl Pharmacol 2008; 229: 10-9.
43. Boverhof DR, Burgoon LD, Tashiro C, et al. Temporal and dose-dependent hepatic gene expression patterns in mice provide new insights into TCDD-Mediated hepatotoxicity. Toxicol Sci 2005; 85: 1048-63.
44. Ciftci O, Ozdemir I, Tanyildizi S, Yildiz S, Oguzturk H. Antioxidative effects of curcumin, {beta}-myrcene and 1,8- cineole against 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced oxidative stress in rats liver. Toxicol Ind Health 2011; 27: 447-53.
45. Chang H, Wang YJ, Chang LW, Lin P. A histochemical and pathological study on the interrelationship between TCDDinduced AhR expression, AhR activation, and hepatotoxicity in mice. J Toxicol Environ Health A 2005; 68: 1567-79.
46. Wu CH, Chen HL, Su HJ, et al. The topical application of 2,3,7,8-tetrachlorodibenzo-p-dioxin lacks skin tumorpromoting potency but induces hepatic injury and tumor necrosis factor-alpha expression in ICR male mice. Food Chem Toxicol 2004; 42: 1217-25.
47. Kanzawa N, Kondo M, Okushima T, et al. Biochemical and molecular biological analysis of different responses to 2,3,7,8-tetrachlorodibenzo-p-dioxin in chick embryo heart and liver. Arch Biochem Biophys 2004; 427: 58-67.
48. National Toxicology Program. NTP technical report on the toxicology and carcinogenesis studies of 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD) (CAS No. 1746-01-6) in female Harlan Sprague-Dawley rats (Gavage Studies). Natl Toxicol Program Tech Rep Ser 2006; 521: 4-232.
49. Kim S, Dere E, Burgoon LD, Chang CC, Zacharewski TR. Comparative analysis of AhR-mediated TCDD-elicited gene expression in human liver adult stem cells. Toxicol Sci 2009; 112: 229-44.
50. Korenaga T, Fukusato T, Ohta M, et al. Long-term effects of subcutaneously injected 2,3,7,8-tetrachlorodibenzo-p-dioxin on the liver of rhesus monkeys. Chemosphere 2007; 67: 399-404.
51. Niittynen M, Simanainen U, Syrjala P, et al. Differences in acute toxicity syndromes of 2,3,7,8-tetrachlorodibenzo-pdioxin and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin in rats. Toxicology 2007; 235: 39-51.
52. Ishida T, Takeda T, Koga T, et al. Attenuation of 2,3,7,8- tetrachlorodibenzo-p-dioxin toxicity by resveratrol: a comparative study with different routes of administration. Biol Pharm Bull 2009; 32: 876-81.
53. Ozeki J, Uno S, Ogura M, et al. Aryl hydrocarbon receptor ligand 2,3,7,8-tetrachlorodibenzo-p-dioxin enhances liver damage in bile duct-ligated mice. Toxicology 2011; 280: 10-7.
54. Patterson RM, Stachlewitz R, Germolec D. Induction of apoptosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin following endotoxin exposure. Toxicol Appl Pharmacol 2003; 190: 120-34.
55. Pelclova D, Urban P, Preiss J, et al. Adverse health effects in humans exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Rev Environ Health 2006; 21: 119-38.
56. Michalek JE, Akhtar FZ, Kiel JL. Serum dioxin, insulin, fasting glucose, and sex hormone-binding globulin in veterans of Operation Ranch Hand. J Clin Endocrinol Metab 1999; 84: 1540-3.
57. Kern PA, Said S, Jackson WG, Jr., Michalek JE. Insulin sensitivity following agent orange exposure in Vietnam veterans with high blood levels of 2,3,7,8-tetrachlorodibenzop- dioxin. J Clin Endocrinol Metab 2004; 89: 4665-72.
58. Cranmer M, Louie S, Kennedy RH, Kern PA, Fonseca VA. Exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) is associated with hyperinsulinemia and insulin resistance. Toxicol Sci 2000; 56: 431-6.
59. Uemura H, Arisawa K, Hiyoshi M, et al. Prevalence of metabolic syndrome associated with body burden levels of dioxin and related compounds among Japan's general population. Environ Health Perspect 2009; 117: 568-73.
60. Chang JW, Chen HL, Su HJ, Liao PC, Guo HR, Lee CC. Dioxin exposure and insulin resistance in Taiwanese living near a highly contaminated area. Epidemiology 2010; 21: 56-61.
61. Lee DH, Lee IK, Porta M, Steffes M, Jacobs DR, Jr. 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. Diabetologia 2007; 50: 1841-51.
62. Chang JW, Chen HL, Su HJ, Liao PC, Guo HR, Lee CC. Simultaneous exposure of non-diabetics to high levels of dioxins and mercury increases their risk of insulin resistance. J Hazard Mater 2011; 185: 749-55.
63. Chang JW, Ou HY, Chen HL, Guo HR, Liao PC, Lee CC. Interrelationship between exposure to PCDD/Fs and hypertension in metabolic syndrome in Taiwanese living near a highly contaminated area. Chemosphere 2010; 81: 1027-32.
64. Wang SL, Tsai PC, Yang CY, Leon GY. Increased risk of diabetes and polychlorinated biphenyls and dioxins: a 24- year follow-up study of the Yucheng cohort. Diabetes Care 2008; 31: 1574-9.
65. Uemura H, Arisawa K, Hiyoshi M, et al. Associations of environmental exposure to dioxins with prevalent diabetes among general inhabitants in Japan. Environ Res 2008; 108: 63-8.
66. Michalek JE, Pavuk M. Diabetes and cancer in veterans of Operation Ranch Hand after adjustment for calendar period, days of spraying, and time spent in Southeast Asia. J Occup Environ Med 2008; 50: 330-40.
67. Consonni D, Pesatori AC, Zocchetti C, et al. Mortality in a population exposed to dioxin after the Seveso, Italy, accident in 1976: 25 years of follow-up. Am J Epidemiol 2008; 167: 847-58.
68. Pazderova-Vejlupkova J, Lukas E, Nemcova M, Pickova J, Jirasek L. The development and prognosis of chronic intoxication by tetrachlordibenzo-p-dioxin in men. Arch Environ Health 1981; 36: 5-11.
69. Lee CC, Yao YJ, Chen HL, Guo YL, Su HJ. Fatty liver and hepatic function for residents with markedly high serum PCDD/Fs levels in Taiwan. J Toxicol Environ Health A 2006; 69: 367-80.
70. Hu SW, Cheng TJ, ChangChien GP, Chan CC. Association between dioxins/furans exposures and incinerator workers' hepatic function and blood lipids. J Occup Environ Med 2003; 45: 601-8.
71. Bajanowski T, Furst P, Wilmers K, Beike J, Kohler H, Brinkmann B. Dioxin in infants-an environmental hazard? Int J Legal Med 2002; 116: 27-32.
72. Kundakovic M, Champagne FA. Epigenetic perspective on the developmental effects of bisphenol A. Brain Behav Immun 2011; 25: 1084-93.
73. Hugo ER, Brandebourg TD, Woo JG, Loftus J, Alexander JW, Ben-Jonathan N. Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ Health Perspect 2008; 116: 1642-7.
74. Wada K, Sakamoto H, Nishikawa K, et al. Life style-related diseases of the digestive system: endocrine disruptors stimulate lipid accumulation in target cells related to metabolic syndrome. J Pharmacol Sci 2007; 105: 133-7.
75. 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: 63-8.
76. Kidani T, Kamei S, Miyawaki J, Aizawa J, Sakayama K, Masuno H. Bisphenol A downregulates Akt signaling and inhibits adiponectin production and secretion in 3T3-L1 adipocytes. J Atheroscler Thromb 2010; 17: 834-43.
77. Polyzos SA, Toulis KA, Goulis DG, Zavos C, Kountouras J. Serum total adiponectin in nonalcoholic fatty liver disease: a systematic review and meta-analysis. Metabolism 2011; 60: 313-26.
78. Polyzos SA, Kountouras J, Zavos C, Tsiaousi E. The role of adiponectin in the pathogenesis and treatment of nonalcoholic fatty liver disease. Diabetes Obes Metab 2010; 12: 365-83.
79. 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: 106-12.
80. Ropero AB, onso-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.
81. Alonso-Magdalena P, Laribi O, Ropero AB, et al. Low doses of bisphenol A and diethylstilbestrol impair Ca2+ signals in pancreatic alpha-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans. Environ Health Perspect 2005; 113: 969-77.
82. Bindhumol V, Chitra KC, Mathur PP. Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology 2003; 188: 117-24.
83. Korkmaz A, Ahbab MA, Kolankaya D, Barlas N. Influence of vitamin C on bisphenol A, nonylphenol and octylphenol induced oxidative damages in liver of male rats. Food Chem Toxicol 2010; 48: 2865-71.
84. Alonso-Magdalena P, Vieira E, Soriano S, et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect 2010; 118: 1243-50.
85. Somm E, Schwitzgebel VM, Toulotte A, et al. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect 2009; 117: 1549-55.
86. Mead MN. BPA and insulin resistance: evidence of effects in dams and offspring. Environ Health Perspect 2010; 118: 399.
87. Rubin BS, Murray MK, Damassa DA, King JC, Soto AM. Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. Environ Health Perspect 2001; 109: 675-80.
88. Miyawaki J, Sakayama K, Kato H, Yamamoto H, Masuno H. Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. J Atheroscler Thromb 2007; 14: 245-52.
89. Ryan KK, Haller AM, Sorrell JE, Woods SC, Jandacek RJ, Seeley RJ. Perinatal exposure to bisphenol-a and the development of metabolic syndrome in CD-1 mice. Endocrinology 2010; 151: 2603-12.
90. Lang IA, Galloway TS, Scarlett A, et al. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 2008; 300: 1303-10.
91. Melzer D, Rice NE, Lewis C, Henley WE, Galloway TS. Association of urinary bisphenol a concentration with heart disease: evidence from NHANES 2003/06. PLoS One 2010; 5: 8673.
92. Hong YC, Park EY, Park MS, et al. Community level exposure to chemicals and oxidative stress in adult population. Toxicol Lett 2009; 184: 139-44.
93. Kandaraki E, Chatzigeorgiou A, Livadas S, et al. Endocrine Disruptors and Polycystic Ovary Syndrome (PCOS): Elevated Serum Levels of Bisphenol A in Women with PCOS. J Clin Endocrinol Metab 2011; 96: 480-4.
94. Koniecki D, Wang R, Moody RP, Zhu J. Phthalates in cosmetic and personal care products: Concentrations and possible dermal exposure. Environ Res 2011; 111: 329-36.
95. Feige JN, Gerber A, Casals-Casas C, et al. The pollutant diethylhexyl phthalate regulates hepatic energy metabolism via species-specific PPARalpha-dependent mechanisms. Environ Health Perspect 2010; 118: 234-41.
96. Hurst CH, Waxman DJ. Activation of PPARalpha and PPARgamma by environmental phthalate monoesters. Toxicol Sci 2003; 74: 297-308.
97. Feige JN, Gelman L, Rossi D, et al. The endocrine disruptor monoethyl-hexyl-phthalate is a selective peroxisome proliferator-activated receptor gamma modulator that promotes adipogenesis. J Biol Chem 2007; 282: 19152-66.
98. Grun F, Blumberg B. Perturbed nuclear receptor signaling by environmental obesogens as emerging factors in the obesity crisis. Rev Endocr Metab Disord 2007; 8: 161-71.
99. 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.
100. Santhosh A, Nair KG, Arun P, et al. Effect of DEHP [di-(2- ethyl hexyl) phthalate]on lipid peroxidation in liver in rats and in primary cultures of rat hepatocytes. Indian J Med Res 1998; 108: 17-23.
101. Bu T, Liu M, Zheng L, Guo Y, Lin X. alpha-Glucosidase inhibition and the in vivo hypoglycemic effect of butylisobutyl- phthalate derived from the Laminaria japonica rhizoid. Phytother Res 2010; 24: 1588-91.
102. Liu M, Zhang W, Qiu L, Lin X. Synthesis of butyl-isobutylphthalate and its interaction with alpha-glucosidase in vitro. J Biochem 2011; 149: 27-33.
103. Rachek LI, Yuzefovych LV, Ledoux SP, Julie NL, Wilson GL. Troglitazone, but not rosiglitazone, damages mitochondrial DNA and induces mitochondrial dysfunction and cell death in human hepatocytes. Toxicol Appl Pharmacol 2009; 240: 348-54.
104. Isenberg JS, Kamendulis LM, Ackley DC, et al. Reversibility and persistence of di-2-ethylhexyl phthalate (DEHP) - and phenobarbital-induced hepatocellular changes in rodents. Toxicol Sci 2001; 64: 192-9.
105. Boberg J, Metzdorff S, Wortziger R, et al. Impact of diisobutyl phthalate and other PPAR agonists on steroidogenesis and plasma insulin and leptin levels in fetal rats. Toxicology 2008; 250: 75-81.
106. Holemans K, Aerts L, Van Assche FA. Lifetime consequences of abnormal fetal pancreatic development. J Physiol 2003; 547: 11-20.
107. Vickers MH. Developmental programming and adult obesity: the role of leptin. Curr Opin Endocrinol Diabetes Obes 2007; 14: 17-22.
108. Polyzos SA, Kountouras J, Zavos C, Deretzi G. The potential adverse role of leptin resistance in nonalcoholic fatty liver disease: A hypothesis based on critical review of literature. J Clin Gastroenterol 2011; 45: 50-4.
109. Stahlhut RW, van WE, Dye TD, Cook S, Swan SH. Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult U.S. males. Environ Health Perspect 2007; 115: 876-82.
110. Hatch EE, Nelson JW, Qureshi MM, et al. 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.
111. Weber R, Watson A, Forter M, Oliaei F. Review Article: Persistent organic pollutants and landfills - a review of past experiences and future challenges. Waste Manag Res 2011; 29: 107-21.
112. Kim MJ, Marchand P, Henegar C, et al. Fate and complex pathogenic effects of dioxins and polychlorinated biphenyls in obese subjects before and after drastic weight loss. Environ Health Perspect 2010; 119: 377-83.
113. Arzuaga X, Ren N, Stromberg A, et al. Induction of gene pattern changes associated with dysfunctional lipid metabolism induced by dietary fat and exposure to a persistent organic pollutant. Toxicol Lett 2009; 189: 96-101.
114. Arsenescu V, Arsenescu RI, King V, Swanson H, Cassis LA. Polychlorinated biphenyl-77 induces adipocyte differentiation and proinflammatory adipokines and promotes obesity and atherosclerosis. Environ Health Perspect 2008; 116: 761-8.
115. Mullerova D, Kopecky J, Matejkova D, et al. Negative association between plasma levels of adiponectin and polychlorinated biphenyl 153 in obese women under nonenergy- restrictive regime. Int J Obes (Lond) 2008; 32: 1875-8.
116. Ruzzin J, Petersen R, Meugnier E, et al. Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect 2010; 118: 465-71.
117. Sonne C, Wolkers H, Leifsson PS, et al. Organochlorineinduced histopathology in kidney and liver tissue from Arctic fox (Vulpes lagopus). Chemosphere 2008; 71: 1214-24.
118. National Toxicology Program. NTP toxicology and carcinogenesis studies of 3,3',4,4',5-pentachlorobiphenyl (PCB 126) (CAS No. 57465-28-8) in female Harlan Sprague- Dawley rats (Gavage Studies). Natl Toxicol Program Tech Rep Ser 2006; 520: 4-246.
119. National Toxicology Program. NTP technical report on the toxicology and carcinogenesis studies of 2,2',4,4',5,5'- hexachlorobiphenyl (PCB 153) (CAS No. 35065-27-1) in female Harlan Sprague-Dawley rats (Gavage studies). Natl Toxicol Program Tech Rep Ser 2006; 529: 4-168.
120. Sonne C, Fonfara S, Dietz R, et al. Multiple cytokine and acute-phase protein gene transcription in West Greenland sledge dogs (Canis familiaris) dietary exposed to organic environmental pollutants. Arch Environ Contam Toxicol 2007; 53: 110-8.
121. Fadhel Z, Lu Z, Robertson LW, Glauert HP. Effect of 3,3',4,4'-tetrachlorobiphenyl and 2,2',4,4',5,5'- hexachlorobiphenyl on the induction of hepatic lipid peroxidation and cytochrome P-450 associated enzyme activities in rats. Toxicology 2002; 175: 15-25.
122. Lai I, Chai Y, Simmons D, et al. Acute toxicity of 3,3',4,4',5- pentachlorobiphenyl (PCB 126) in male Sprague-Dawley rats: effects on hepatic oxidative stress, glutathione and metals status. Environ Int 2010; 36: 918-23.
123. Lee DH, Steffes MW, Sjodin A, Jones RS, Needham LL, Jacobs DR. Low dose organochlorine pesticides and polychlorinated biphenyls predict obesity, dyslipidemia, and insulin resistance among people free of diabetes. PLoS One 2011; 6: 15977.
124. Lee DH, Lee IK, Jin SH, Steffes M, Jacobs DR, Jr. Association between serum concentrations of persistent organic pollutants and insulin resistance among nondiabetic adults: results from the National Health and Nutrition Examination Survey 1999-2002. Diabetes Care 2007; 30: 622-8.
125. Elobeid MA, Padilla MA, Brock DW, Ruden DM, Allison DB. Endocrine disruptors and obesity: an examination of selected persistent organic pollutants in the NHANES 1999-2002 data. Int J Environ Res Public Health 2010; 7: 2988-3005.
126. Lee DH, Lee IK, Steffes M, Jacobs DR, Jr. Extended analyses of the association between serum concentrations of persistent organic pollutants and diabetes. Diabetes Care 2007; 30: 1596-8.
127. Ukropec J, Radikova Z, Huckova M, et al. High prevalence of prediabetes and diabetes in a population exposed to high levels of an organochlorine cocktail. Diabetologia 2010; 53: 899-906.
128. Longnecker MP, Klebanoff MA, Brock JW, Zhou H. Polychlorinated biphenyl serum levels in pregnant subjects with diabetes. Diabetes Care 2001; 24: 1099-101.
129. Lee DH, Jacobs DR, Jr., Steffes M. Association of organochlorine pesticides with peripheral neuropathy in patients with diabetes or impaired fasting glucose. Diabetes 2008; 57: 3108-11.
130. Lim JS, Son HK, Park SK, Jacobs DR, Jr., Lee DH. Inverse associations between long-term weight change and serum concentrations of persistent organic pollutants. Int J Obes (Lond) 2010; 35: 744-7.
131. Lee DH, Steffes MW, Jacobs DR, Jr. Can persistent organic pollutants explain the association between serum gammaglutamyltransferase and type 2 diabetes? Diabetologia 2008; 51: 402-7.
132. National Toxicology Program NTP. Toxicology and carcinogenesis studies of a binary mixture of 3,3',4,4',5- pentachlorobiphenyl (PCB 126) (CAS No. 57465-28-8) and 2,3',4,4',5-pentachlorobiphenyl (PCB 118) (CAS No. 31508-00-6) in female harlan sprague-dawley rats (Gavage Studies). Natl Toxicol Program Tech Rep Ser 2006; 531: 1-218.
133. National Toxicology Program NTP. Toxicology and carcinogenesis studies of a binary mixture of 3,3',4,4',5- pentachlorobiphenyl (PCB 126) (CAS No. 57465-28-8) and 2,2',4,4',5,5'-hexachlorobiphenyl (PCB 153) (CAS No. 35065-27-1) in female harlan sprague-dawley rats (Gavage Studies). Natl Toxicol Program Tech Rep Ser 2006; 530: 1-258.
134. National Toxicology Program. NTP toxicology and carcinogenesis studies of a mixture of 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD) (CAS No. 1746-01-6), 2,3,4,7,8-pentachlorodibenzofuran (PeCDF) (CAS No.57117-31-4), and 3,3',4,4',5-pentachlorobiphenyl (PCB 126) (CAS No. 57465-28-8) in female Harlan sprague-dawley rats (Gavage Studies). Natl Toxicol Program Tech Rep Ser 2006; 526: 1-180.
135. Grun F, Blumberg B. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology 2006; 147(Suppl 6): 50-5.
136. Newbold RR, Padilla-Banks E, Snyder RJ, Jefferson WN. Perinatal exposure to environmental estrogens and the development of obesity. Mol Nutr Food Res 2007; 51: 912-7.
137. Joffe MM, Rosenbaum PR. Invited commentary: propensity scores. Am J Epidemiol 1999; 150: 327-33.