Endocrine disruptors: Can it be the missing link explaining the diabetes epidemic in India?

Deep Dutta; Rajesh Khadgawat

doi:10.4103/2321-0656.140878

Journal of Social Health and Diabetes, Table of Contents

CC BY-NC-ND 4.0 · Journal of Social Health and Diabetes 2015; 03(01): 016-021
DOI: 10.4103/2321-0656.140878

Review Article

NovoNordisk Education Foundation

Endocrine disruptors: Can it be the missing link explaining the diabetes epidemic in India?

Deep Dutta

Department of Endocrinology, Post Graduate Institute of Medical Education and Research and Dr. Ram Manohar Lohia Hospital, New Delhi, India

,

Rajesh Khadgawat

¹Department of Endocrinology, All India Institute of Medical Sciences, Ansari Nagar, New Delhi, India

› Author Affiliations

Abstract

India is the diabetes capital of the world with an exponential increase in diabetes prevalence in the last few decades. It may not be just a simple co-incidence that the global increase in diabetes is associated with an exponential increase in industrial chemical output. Literature searches through PubMed, Medline and Embase for articles published until July 2014 evaluating link between endocrine disrupting chemicals (EDCs) and diabetes was done. This review observed that a large volume of data is available from preclinical studies implicating commonly used synthetic compounds in the pathogenesis of diabetes. EDCs have been demonstrated to interact with almost all the steps of insulin homeostasis starting from its synthesis to its signaling and action. Bisphenol-A, 2,3,7,8-tetrachlorod-ibenzo-dioxin (TCDD)/dioxin, polychlorinated biphenyls (PCBs), persistent organic pollutants, diethylhexylphthalate, cadmium and arsenic are some of the important EDCs which interfere with a maximal number of pathways of insulin homeostasis. However data from humans establishing the causality lacks from across the globe, with maximal data available from bisphenol-A and TCDD from USA. Their evaluation among Indians, especially with regards to dysglycemia, insulin resistance and beta cell function is non-existent, thus warranting urgent research in this area.

Beta cell function - diabetes - endocrine disruptors - insulin resistance - prediabetes

Full Text

References

References
1 IDF. Diabetes Atlas. 4. Montreal, Canada: International Diabetes Federation; 2009
2 Joshi SR, Anjana RM, Deepa M, Pradeepa R, Bhansali A, Dhandania VK. et al. Prevalence of dyslipidemia in urban and rural India: The ICMR-INDIAB study. PLoS One 2014; 9: e96808
3 Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA. et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002; 346: 393-403
4 Yang W, Lin L, Qi J. The preventive effect of acarbose and metformin on the IGT population from becoming diabetes mellitus: A 3-year multi-centric prospective study. Chin J Endocrinol Metab 2001; 17: 131-136
5 Ramachandran A, Snehalatha C, Mary S, Mukesh B, Bhaskar AD, Vijay V. et al. The Indian Diabetes Prevention Programme shows that lifestyle modification and metformin prevent type 2 diabetes in Asian Indian subjects with impaired glucose tolerance (IDPP-1). Diabetologia 2006; 49: 289-297
6 Dutta D, Choudhuri S, Mondal SA, Mukherjee S, Chowdhury S. Urinary albumin: Creatinine ratio predicts prediabetes progression to diabetes and reversal to normoglycemia: Role of associated insulin resistance, inflammatory cytokines and low vitamin D. J Diabetes 2014; 6: 316-322
7 Dutta D, Mondal SA, Choudhuri S, Maisnam I, Hasanoor RezaAH, Bhattacharya B. et al. Vitamin-D supplementation in prediabetes reduced progression to type 2 diabetes and was associated with decreased insulin resistance and systemic inflammation: An open label randomized prospective study from Eastern India. Diabetes Res Clin Pract 2014; 103: e18-e23
8 Dutta D, Mondal SA, Kumar M, Hasanoor RezaAH, Biswas D, Singh P. et al. Serum fetuin - A concentration predicts glycaemic outcomes in people with prediabetes: A prospective study from eastern India. Diabet Med. 2014
9 Dutta D, Maisnam I, Shrivastava A, Sinha A, Ghosh S, Mukhopadhyay P. et al. Serum vitamin-D predicts insulin resistance in individuals with prediabetes. Indian J Med Res 2013; 138: 853-860
10 Dutta D, Choudhuri S, Mondal SA, Maisnam I, Reza AH, Ghosh S. et al. Tumor necrosis factor alpha-238G/A (rs 361525) gene polymorphism predicts progression to type-2 diabetes in an Eastern Indian population with prediabetes. Diabetes Res Clin Pract 2013; 99: e37-e41
11 Kuo CC, Moon K, Thayer KA, Navas-Acien A. Environmental chemicals and type 2 diabetes: An updated systematic review of the epidemiologic evidence. Curr Diab Rep 2013; 13: 831-849
12 Grün F. The obesogen tributyltin. Vitam Horm 2014; 94: 277-325
13 Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM. et al. Endocrine-disrupting chemicals: An Endocrine Society scientific statement. Endocr Rev 2009; 30: 293-342
14 Alonso-Magdalena P, Quesada I, Nadal A. Endocrine disruptors in the etiology of type 2 diabetes mellitus. Nat Rev Endocrinol 2011; 7: 346-353
15 Sargis RM. The hijacking of cellular signaling and the diabetes epidemic: Mechanisms of environmental disruption of insulin action and glucose homeostasis. Diabetes Metab J 2014; 38: 13-24
16 Calafat AM, Wong LY, Ye X, Reidy JA, Needham LL. Concentrations of the sunscreen agent benzophenone-3 in residents of the United States: National Health and Nutrition Examination Survey 2003-2004. Environ Health Perspect 2008; 116: 893-897
17 García-Estévez DA, Araújo-Vilar D, Fiestras-Janeiro G, Saavedra-González A, Cabezas-Cerrato J. Comparison of several insulin sensitivity indices derived from basal plasma insulin and glucose levels with minimal model indices. Horm Metab Res 2003; 35: 13-17
18 Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: Comparison with the euglycemic insulin clamp. Diabetes Care 1999; 22: 1462-1470
19 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
20 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: 245-252
21 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
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 ß. PLoS One 2012; 7: e31109
23 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
24 Sargis RM, Johnson DN, Choudhury RA, Brady MJ. Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity (Silver Spring) 2010; 18: 1283-1288
25 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: 761-768
26 Zuo Z, Chen S, Wu T, Zhang J, Su Y, Chen Y. et al. Tributyltin causes obesity and hepatic steatosis in male mice. Environ Toxicol 2011; 26: 79-85
27 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: 834-843
28 Indumathi D, Jayashree S, Selvaraj J, Sathish S, Mayilvanan C, Akilavalli N. et al. Effect of bisphenol-A on insulin signal transduction and glucose oxidation in skeletal muscle of adult male albino rat. Hum Exp Toxicol 2013; 32: 960-971
29 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 Cell Biochem 2013; 114: 558-569
30 Han JC, Park SY, Hah BG, Choi GH, Kim YK, Kwon TH. et al. Cadmium induces impaired glucose tolerance in rat by down-regulating GLUT4 expression in adipocytes. Arch Biochem Biophys 2003; 413: 213-220
31 Wang J, Sun B, Hou M, Pan X, Li X. The environmental obesogen bisphenol A promotes adipogenesis by increasing the amount of 11β-hydroxysteroid dehydrogenase type 1 in the adipose tissue of children. Int J Obes (Lond) 2013; 37: 999-1005
32 US Environmental Protection Agency Integrated Risk Information System. 2010 Available from: http://www.epa.gov/iris/subst/0356.htm [Last accessed on 2014 August 8].
33 European Food Safety Authority Bisphenol A. 2010 Available from: http://www.efsaeuropaeu/en/ceftopics/topic/bisphenol.htm [Last accessed on 2014 August 8].
34 Kurita H, Yoshioka W, Nishimura N, Kubota N, Kadowaki T, Tohyama C. Aryl hydrocarbon receptor-mediated effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on glucose-stimulated insulin secretion in mice. J Appl Toxicol 2009; 29: 689-694
35 Novelli M, Piaggi S, De Tata V. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced impairment of glucose-stimulated insulin secretion in isolated rat pancreatic islets. Toxicol Lett 2005; 156: 307-314
36 Piaggi S, Novelli M, Martino L, Masini M, Raggi C, Orciuolo E. et al. Cell death and impairment of glucose-stimulated insulin secretion induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the beta-cell line INS-1E. Toxicol Appl Pharmacol 2007; 220: 333-340
37 Ebner K, Matsumura F, Enan E, Olsen H. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters pancreatic membrane tyrosine phosphorylation following acute treatment. J Biochem Toxicol 1993; 8: 71-81
38 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: 482-491
39 Enan E, Liu PC, Matsumura F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin causes reduction of glucose transporting activities in the plasma membranes of adipose tissue and pancreas from the guinea pig. J Biol Chem 1992; 267: 19785-19791
40 Viluksela M, Unkila M, Pohjanvirta R, Tuomisto JT, Stahl BU, Rozman KK. et al. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on liver phosphoenolpyruvate carboxykinase (PEPCK) activity, glucose homeostasis and plasma amino acid concentrations in the most TCDD-susceptible and the most TCDD-resistant rat strains. Arch Toxicol 1999; 73: 323-336
41 Porta M, Gasull M, Puigdomènech E, Garí M, Bosch de BaseaM, Guillén M. et al. Distribution of blood concentrations of persistent organic pollutants in a representative sample of the population of Catalonia. Environ Int 2010; 36: 655-664
42 Wassermann D, Wassermann M, Lemesch C. Ultrastructure of beta-cells of the endocrine pancreas in rats receiving polychlorinated biphenyls. Environ Physiol Biochem 1975; 5: 322-340
43 Fischer LJ, Zhou HR, Wagner MA. Polychlorinated biphenyls release insulin from RINm5F cells. Life Sci 1996; 59: 2041-2049
44 Fischer LJ, Wagner MA, Madhukar BV. Potential involvement of calcium, CaM kinase II, and MAP kinases in PCB-stimulated insulin release from RINm5F cells. Toxicol Appl Pharmacol 1999; 159: 194-203
45 Zhang W, Sargis RM, Volden PA, Carmean CM, Sun XJ, Brady MJ. PCB 126 and other dioxin-like PCBs specifically suppress hepatic PEPCK expression via the aryl hydrocarbon receptor. PLoS One 2012; 7: e37103
46 Sakurai T, Miyazawa S, Hashimoto T. Effects of di-(2-ethylhexyl)phthalate administration on carbohydrate and fatty acid metabolism in rat liver. J Biochem 1978; 83: 313-320
47 Feige JN, Gerber A, Casals-Casas C, Yang Q, Winkler C, Bedu E. et al. The pollutant diethylhexyl phthalate regulates hepatic energy metabolism via species-specific PPARalpha-dependent mechanisms. Environ Health Perspect 2010; 118: 234-241
48 Douillet C, Currier J, Saunders J, Bodnar WM, Matoušek T, Stýblo M. Methylated trivalent arsenicals are potent inhibitors of glucose stimulated insulin secretion by murine pancreatic islets. Toxicol Appl Pharmacol 2013; 267: 11-15
49 Chang KC, Hsu CC, Liu SH, Su CC, Yen CC, Lee MJ. et al. Cadmium induces apoptosis in pancreatic β-cells through a mitochondria-dependent pathway: The role of oxidative stress-mediated c-Jun N-terminal kinase activation. PLoS One 2013; 8: e54374
50 Meyer A, Strajhar P, Murer C, Da Cunha T, Odermatt A. Species-specific differences in the inhibition of human and zebrafish 11β-hydroxysteroid dehydrogenase 2 by thiram and organotins. Toxicology 2012; 301: 72-78
51 Paul DS, Walton FS, Saunders RJ, Stýblo M. Characterization of the impaired glucose homeostasis produced in C57BL/6 mice by chronic exposure to arsenic and high-fat diet. Environ Health Perspect 2011; 119: 1104-1109
52 Wauson EM, Langan AS, Vorce RL. Sodium arsenite inhibits and reverses expression of adipogenic and fat cell-specific genes during in vitro adipogenesis. Toxicol Sci 2002; 65: 211-219
53 Steffens AA, Hong GM, Bain LJ. Sodium arsenite delays the differentiation of C2C12 mouse myoblast cells and alters methylation patterns on the transcription factor myogenin. Toxicol Appl Pharmacol 2011; 250: 154-161
54 Yen YP, Tsai KS, Chen YW, Huang CF, Yang RS, Liu SH. Arsenic inhibits myogenic differentiation and muscle regeneration. Environ Health Perspect 2010; 118: 949-956
55 Henriksen GL, Ketchum NS, Michalek JE, Swaby JA. Serum dioxin and diabetes mellitus in veterans of Operation Ranch Hand. Epidemiology 1997; 8: 252-258
56 Kern PA, Said S, Jackson Jr WG, Michalek JE. Insulin sensitivity following agent orange exposure in Vietnam veterans with high blood levels of 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Clin Endocrinol Metab 2004; 89: 4665-4672
57 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: 330-340
58 Bertazzi PA, Consonni D, Bachetti S, Rubagotti M, Baccarelli A, Zocchetti C. et al. Health effects of dioxin exposure: A 20-year mortality study. Am J Epidemiol 2001; 153: 1031-1044
59 Lee DH, Lee IK, Song K, Steffes M, Toscano W, Baker BA. et al. A strong dose-response relation between serum concentrations of persistent organic pollutants and diabetes: Results from the National Health and Examination Survey 1999-2002. Diabetes Care 2006; 29: 1638-1644
60 Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M, Wallace RB. et al. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 2008; 300: 1303-1310
61 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: e8673
62 Islam R, Khan I, Hassan SN, McEvoy M, D′Este C, Attia J. et al. Association between type 2 diabetes and chronic arsenic exposure in drinking water: A cross sectional study in Bangladesh. Environ Health 2012; 11: 38
63 Johnson S, Saikia N, Sahu R. Phthalates in toys available in Indian market. Bull Environ Contam Toxicol 2011; 86: 621-626
64 Selvaraj KK, Sundaramoorthy G, Ravichandran PK, Girijan GK, Sampath S, Ramaswamy BR. Phthalate esters in water and sediments of the Kaveri River, India: Environmental levels and ecotoxicological evaluations. Environ Geochem Health. 2014
65 Kumar V, Chakraborty A, Viswanath G, Roy P. Androgenic endocrine disruptors in wastewater treatment plant effluents in India: Their influence on reproductive processes and systemic toxicity in male rats. Toxicol Appl Pharmacol 2008; 226: 60-73