Top

Reviews in Endocrine and Metabolic Disorders

Published in:

01-12-2014

Metabolic syndrome and the environmental pollutants from mitochondrial perspectives

Authors: Jin Taek Kim, Hong Kyu Lee

Published in: Reviews in Endocrine and Metabolic Disorders | Issue 4/2014

Abstract

The worldwide epidemic of diabetes and metabolic syndrome in the last few decades cannot be fully accounted for only by changes in the lifestyle factors, such as sedentary lifestyle and overeating. Besides genetic factors, there must be other causes to explain this rapid change. They could not be infectious in nature and induce insulin resistance as key biochemical abnormality. Mitochondrial dysfunction could be underlying mechanism behind the insulin resistance, thus metabolic syndrome. Then there have been increasing number of reports suggesting that chronic exposure to and accumulation of endocrine disrupting chemicals (EDCs), especially so-called the persistent organic pollutants (POPs) within the body might be associated with metabolic syndrome. Combining two concepts, we developed new “EDCs-induced mitochondrial dysfunction hypothesis of metabolic syndrome”. In this review we suggest that classifying those chemicals into 5 groups might be clinically useful considering their removal or avoidance; POPs, non-persistent organic pollutants, heavy metals, air pollutants and drugs. We will also discuss briefly how those insights could be applied to clinical medicine.

Available only for authorised users

Meigs JB. Invited commentary: insulin resistance syndrome? Syndrome X? Multiple metabolic syndrome? A syndrome at all? Factor analysis reveals patterns in the fabric of correlated metabolic risk factors. Am JEpidemiol. 2000;152:908–11.CrossRef

Reaven GM. Banting lecture, Role of insulin resistance in human disease. Diabetes. 1998;37:1595–607.CrossRef

Lee HK, Cho YM, Kwak SH, Lim S, Park KS, Shim EB. Mitochondrial dysfunction and metabolic syndrome-looking for environmental factors. Biochim Biophys Acta. 2010;1800(3):282–9.PubMedCrossRef

Lee HK, Shim EB. Extension of Mitochondria Dysfunction Hypothesis of Metabolic Syndrome to Atherosclerosis with Emphasis on the Endocrine Disrupting Chemicals and Biophysical Laws. J Diabetes Investig. 2013;4(1):19–33.PubMedCrossRefPubMedCentral

Meyer JN, Leung MC, Rooney JP, Sendoel A, Hengartner MO, Kisby GE, et al. Mitochondria as a target of environmental toxicants. Toxicol Sci. 2013;134(1):1–17.PubMedCrossRefPubMedCentral

Lee DH, Porta M, Jacobs Jr DR, Vandenberg LN. Chlorinated persistent organic pollutants, obesity, and type 2 diabetes. Endocr Rev. 2014;35(4):557–601.PubMedCrossRef

Lee HK, Song JH, Shin CS, Park DJ, Park KS, Lee KU, et al. Decreased mitochondrial DNA content in peripheral blood precedes the development of non-insulin-dependent diabetes mellitus. Diabetes Res Clin Pract. 1998;42:161–7.PubMedCrossRef

Jucker BM, Dufour S, Ren J, Cao X, Previs SF, Underhill B, et al. Shulman GI.Assessment of mitochondrial energy coupling in vivo by 13C/31P NMR. Proc Natl Acad Sci U S A. 2000;97:6880–4.PubMedCrossRefPubMedCentral

Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science. 2003;300:1140–2.PubMedCrossRefPubMedCentral

10.

Smith RE. Quantitative relations between liver mitochondria metabolism and total body weight in mammals. Ann NY Acad Sci. 1956;62:403–22.CrossRef

11.

Rasmussen UF, Rasmussen HN, Krustrup P, Quistorff B, Saltin B, Bangsbo J. Aerobic metabolism of human quadriceps muscle: in vivo data parallel measurements on isolated mitochondria. Am J Physiol Endocrinol Metab. 2001;280:301–7.

12.

Lee HK. Method of proof and evidences for the concept that mitochondrial genome is a thrifty genome. Diabetes Res Clin Pract. (Suppl. 2) 2001;54–63.

13.

Kleiber M. Body size and metabolism. Hilgardia. 1932;6:315–53.CrossRef

14.

West GB, Woodruff WH, Brown JH. Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. Proc Natl Acad Sci U S A. 2002;99 Suppl 1:2473–8.PubMedCrossRefPubMedCentral

15.

Ravussin E, Lillioja S, Knowler WC, Christin L, Freymond D, Abbott WG, et al. Reduced rate of energy expenditure as a risk factor for bodyweight gain. N Engl J Med. 1988;318:467–72.PubMedCrossRef

16.

Chun PW. Why does the human body maintain a constant 37-degree temperature?: thermodynamic switch controls chemical equilibrium in biological systems. Phys Scr. 2005;118:219–22.CrossRef

17.

Patti ME, Corvera S. The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr Rev. 2010;31(3):364–95.PubMedCrossRefPubMedCentral

18.

Szendroedi J, Phielix E, Roden M. The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol. 2012;8(2):92–103.CrossRef

19.

Pravenec M, Hyakukoku M, Houstek J, Zidek V, Landa V, Mlejnek P, et al. Direct linkage of mitochondrial genome variation to risk factors for type 2 diabetes in conplastic strains. Genome Res. 2007;17:1319–26.PubMedCrossRefPubMedCentral

20.

Fuku N, Park KS, Yamada Y, Nishigaki Y, Cho YM, Matsuo H, et al. Mitochondrial haplogroup N9a confers resistance against type 2 diabetes in Asians. Am J Hum Genet. 2007;80:407–15.PubMedCrossRefPubMedCentral

21.

Park KS, Chan JC, Chuang LM, Suzuki S, Araki E, Nanjo K, et al. A mitochondrial DNA variant at position 16189 is associated with type 2 diabetes mellitus in Asians. Diabetologia. 2008;51:602–8.PubMedCrossRef

22.

Flaquer A, Baumbach C, Kriebel J, Meitinger T, Peters A, Waldenberger M, et al. Mitochondrial Genetic Variants Identified to Be Associated with BMI in Adults. PLoS One. 2014;9(8):e105116.PubMedCrossRefPubMedCentral

23.

Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992;35:595–601.PubMedCrossRef

24.

Knowler WC, Pettitt DJ, Bennett PH, Williams RC. Diabetes mellitus in the Pima Indians: genetic and evolutionary considerations. Am J Phys Anthropol. 1983;62:107–14.PubMedCrossRef

25.

Cannon B, Nedergaard J. Thermogenesis challenges the adipostat hypothesis for body-weight control. Proc Nutr Soc. 2009;68(4):401–7.PubMedCrossRef

26.

Koleva DI, Orbetzova MM, Atanassova PK. Adipose tissue hormones and appetite and body weight regulators in insulin resistance. Folia Med (Plovdiv). 2013;55(1):25–32.

27.

Krebs HA, Eggleston LV. The effect of insulin on oxidations in isolated muscle tissue. Biochem J. 1938;32(5):913913.

28.

Echave P1, Machado-da-Silva G, Arkell RS, Duchen MR, Jacobson J, Mitter R, et al. Extracellular growth factors and mitogens cooperate to drive mitochondrial biogenesis. J Cell Sci. 2009;122(24):4516–22.PubMedCrossRefPubMedCentral

29.

Damstra T, Barlow S, Aake B, Kavlock R, Van Der Kraak G. International Programme on Chemical Safety: Global Assessment of the State-of-the-Science on Endocrine Disruptors. 2002. http://www.who.int/pcs/emerg_site/edc/global_edc_TOC.htm

30.

Thayer KA, Heindel JJ, Bucher JR, Gallo MA. Role of environmental chemicals in diabetes and obesity: a National Toxicology Program workshop review. Environ Health Perspect. 2012;120(6):779–89.PubMedCrossRefPubMedCentral

31.

Liu C, Ying Z, Harkema J, Sun Q, Rajagopalan S. Epidemiological and experimental links between air pollution and type 2 diabetes. Toxicol Pathol. 2013;41(2):361–73.PubMedCrossRefPubMedCentral

32.

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(7):1638–44.PubMedCrossRef

33.

Ruzzin J, Petersen R, Meugnier E, Madsen L, Lock EJ, Lillefosse H, et al. Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect. 2010;118(4):465–71.PubMedCrossRefPubMedCentral

34.

Virtanen MT. Histopathological and ultrastructural changes in the gills of Poeciliareticulatus induced by an organochlorine pesticide. J Environ Pathol Toxicol Oncol. 1986;7:73–85.PubMed

35.

Shertzer HG, Genter MB, Shen D, Nebert DW, Chen Y, Dalton TP. TCDD decreases ATP levels and increases reactive oxygen production through changes in mitochondrial F (0) F (1)-ATP synthase and ubiquinone. Toxicol Appl Pharmacol. 2006;217:363–74.PubMedCrossRefPubMedCentral

36.

Nakagawa Y, Suzuki T, Ishii H, Ogata A. Biotransformation and cytotoxicity of a brominated flame retardant, tetrabromobisphenol A, and its analogues in rat hepatocytes. Xenobiotica. 2007;37:693–708.PubMedCrossRef

37.

Lind L, Zethelius B, Salihovic S, van Bavel B, Lind PM. Circulating levels of perfluoroalkyl substances and prevalent diabetes in the elderly. Diabetologia. 2014;57(3):473–9.PubMedCrossRef

38.

Esposti MD, Ngo A, Myers MA. Inhibition of mitochondrial complex I may account for IDDM induced by intoxication with the rodenticide Vacor. Diabetes. 1996;45:1531–4.PubMedCrossRef

39.

Rahimi R, Abdollahi MA. review on the mechanism involved in hyperglycaemia induced by organophosphorus pesticides. Pestic Biochem Physiol. 2007;88:115–21.CrossRef

40.

Karami-Mohajeri S, Hadian MR, Fouladdel S, Azizi E, Ghahramani MH, Hosseini R, et al. Mechanisms of muscular electrophysiological and mitochondrial dysfunction following exposure tomalathion, an organophosphorus pesticide. Hum ExpToxicol. 2014;33(3):251–63.CrossRef

41.

McKinlay R, Plant JA, Bell JNB, Voulvoulis N. Endocrine disrupting pesticides: implications for risk assessment. Environ Int. 2008;34:168–83.PubMedCrossRef

42.

Jeong SH, Kim BY, Kang HG, Ku HK, Cho JH. Effect of chlorpyrifos-methyl on steroid and thyroid hormones in rat F0− andF1-generations. Toxicology. 2006;220:189–202.PubMedCrossRef

43.

Soloman KR, Baker DB, Richards RP, Dixon KR, Klaine SJ. Ecological risk assessment of atrazine in North American surface waters. Environ Toxicol Chem. 1996;15:31–76.CrossRef

44.

Lim S, Ahn SY, Song IC, Chung MH, Jang HC, Park KS, et al. Chronic exposure to the herbicide, atrazine, causes mitochondrial dysfunction and insulin resistance. PLoS One. 2009;4(4):e5186.PubMedCrossRefPubMedCentral

45.

Nicodemo D, Maioli MA, Medeiros HC, Guelfi M, Balieira KV, De Jong D, et al. Fipronil and imidacloprid reduce honeybee mitochondrial activity. Environ Toxicol Chem. 2014;33(9):2070–5.PubMedCrossRef

46.

Lind PM, Zethelius B. Circulating levels of phthalate metabolites are associated with prevalent diabetes in the elderly. Diabetes Care. 2012;35(7):1519–24.PubMedCrossRefPubMedCentral

47.

Hurst CH, Waxman DJ. Activation of PPARalpha and PPARgamma by environmental phthalate monoesters. Toxicol Sci. 2003;74:297–308.PubMedCrossRef

48.

Bility MT, Thompson JT, McKee RH, David RM, Butala JH, VandenHeuvel JP. Activation of mouse and human peroxisome proliferator-activated receptors (PPARs) by phthalate monoesters. Toxicol Sci. 2004;82:170.182.PubMed

49.

Posnack NG, Swift LM, Kay MW, Lee NH, Sarvazyan N. Phthalate exposure changes the metabolic profile of cardiac muscle cells. Environ Health Perspect. 2012;120(9):1243–51.PubMedCrossRefPubMedCentral

50.

Ishido M, Suzuki J. Classification of phthalates based on an in vitro neurosphere assay using rat mesencephalic neural stem cells. J Toxicol Sci. 2014;39(1):25–32.PubMedCrossRef

51.

Goodman M, Lakind JS, Mattison DR. Do phthalates act as obesogens in humans? A systematic review of the epidemiological literature. Crit Rev Toxicol. 2014;44(2):151–75.PubMedCrossRef

52.

Polyzos SA, Kountouras J, Deretzi G, Zavos C, Mantzoros CS. The emerging role of endocrine disruptors in pathogenesis of insulin resistance: a concept implicating nonalcoholic fatty liver disease. Curr Mol Med. 2012;12(1):68–82.PubMedCrossRef

53.

Alonso-Magdalena P, Quesada I, Nadal A. Endocrine disruptors in the etiology of type 2 diabetes mellitus. Nat Rev Endocrinol. 2011;7(6):346–53.PubMedCrossRef

54.

Moon MK, Kim MJ, Jung IK, Koo YD, Ann HY, Lee KJ, et al. Bisphenol A impairs mitochondrial function in the liver at doses below the no observed adverse effect level. J Korean Med Sci. 2012;27(6):644–552.PubMedCrossRefPubMedCentral

55.

Kaur K, Chauhan V, Gu F, Chauhan A. Bisphenol A induces oxidative stress and mitochondrial dysfunction in lymphoblasts from children with autism and unaffected siblings. Free Radic Biol Med. 2014;76C:25–33.PubMedCrossRef

56.

Chen YW, Yang CY, Huang CF, Hung DZ, Leung YM, Liu SH. Heavy metals and islet function and diabetes development. Islets. 2009;1:169–76.PubMedCrossRef

57.

Edwards JR, Prozialeck WC. Cadmium, diabetes and chronic kidney disease. Toxicol Appl Pharmacol. 2009;238:289–93.PubMedCrossRefPubMedCentral

58.

Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, et al. Arsenic: toxicity, oxidative stress and human disease. J Appl Toxicol. 2011;31(2):95–107.PubMed

59.

Liu C, Ying Z, Harkema J, Sun Q, Rajagopalan S. Epidemiological and experimental links between air pollution and type 2 diabetes. Toxicol Pathol. 2013;41(2):361–73.PubMedCrossRefPubMedCentral

60.

Andersen ZJ, Raaschou-Nielsen O, Ketzel M, Jensen SS, Hvidberg M, Loft S, et al. Diabetes incidence and long-term exposure to air pollution: a cohort study. Diabetes Care. 2012;35(1):92–8.PubMedCrossRefPubMedCentral

61.

Coogan PF, White LF, Jerrett M, Brook RD, Su JG, Seto E, et al. Air pollution and incidence of hypertension and diabetes mellitus in black women living in Los Angeles. Circulation. 2012;125(6):767–72.PubMedCrossRefPubMedCentral

62.

Liu C, Bai Y, Xu X, Sun L, Wang A, Wang TY, et al. Exaggerated effects of particulate matter air pollution in genetic type II diabetes mellitus. Part Fibre Toxicol. 2014; 11:27.

63.

Adar SD, Filigrana PA, Clements N, Peel JL. Ambient Coarse Particulate Matter and Human Health: A Systematic Review and Meta-Analysis. Curr Environ Health Rep. 2014;8(1):258–74.

64.

Lewis W, Day BJ, Copeland WC. Mitochondrial toxicity of NRTI antiviral drugs: an integrated cellular perspective. Nat Rev Drug Discov. 2003;2:812–22.PubMedCrossRef

65.

Gerschenson M, Kim C, Berzins B, Taiwo B, Libutti DE J, Choi J, et al. Mitochondrial function, morphology and metabolic parameters improve after switching from stavudine to a tenofovir-containing regimen. J Antimicrob Chemother. 2009;63:1244–50.PubMedCrossRef

66.

Boelsterli UA, Lim PL. Mitochondrial abnormalities-a link to idiosyncratic drug hepatotoxicity? Toxicol Appl Pharmacol. 2007;220:92–107.PubMedCrossRef

67.

Amacher DE. Drug-associated mitochondrial toxicity and its detection. Curr Med Chem. 2005;12(16):1829–39.PubMedCrossRef

68.

Hectors TL, Vanparys C, Van Gaal LF, Jorens PG, Covaci A, Blust R. Insulin resistance and environmental pollutants: experimental evidence and future perspectives. Environ Health Perspect. 2013;121(11–12):1273–81.PubMedPubMedCentral

69.

Park WH, Jun DW, Kim JT, Jeong JH, Park H, Chang YS, et al. Novel cell-based assay reveals associations of circulating serum AhR-ligands with metabolic syndrome and mitochondrial dysfunction. Biofactors. 2013;39(4):494–504.PubMedCrossRef

70.

Shanle EK, Xu W. Endocrine disrupting chemicals targeting estrogen receptor signaling: identification and mechanisms of action. Chem Res Toxicol. 2011;24(1):6–19.PubMedCrossRefPubMedCentral

71.

Shizu R, Benoki S, Numakura Y, Kodama S, Miyata M, Yamazoe Y, et al. Xenobiotic-induced hepatocyte proliferation associated with constitutive active/androstane receptor (CAR) or peroxisome proliferator-activated receptor α (PPARα) is enhanced by pregnane X receptor (PXR) activation in mice. PLoS One. 2013;8(4):e61802.PubMedCrossRefPubMedCentral

72.

Gao J, Xie W. Targeting xenobiotic receptors PXR and CAR for metabolic diseases. Trends Pharmacol Sci. 2012;33(10):552–8.PubMedCrossRefPubMedCentral

73.

Pereira-Fernandes A, Demaegdt H, Vandermeiren K, Hectors TL, Jorens PG, Blust R, et al. Evaluation of screening system for obesogenic compounds: screening of endocrinedisrupting compounds and evaluation of the PPAR dependency of the effect. PLoS One. 2013;8(10):e77481.PubMedCrossRefPubMedCentral

74.

Patel CJ, Bhattacharya J, Butte AJ. An Environment-Wide Association Study (EWAS) on type 2 diabetes mellitus. PLoS One. 2010;5(5):e10746.PubMedCrossRefPubMedCentral

75.

Kim JT, Kim SS, Jun DW, Hwang YH, Park WH, Pak YK, et al. Serum arylhydrocarbon receptor transactivating activity is elevated in type 2 diabetic patients with diabetic nephropathy. J Diabetes Investig. 2013;4(5):483–91.PubMedCrossRefPubMedCentral

Title: Metabolic syndrome and the environmental pollutants from mitochondrial perspectives
Authors: Jin Taek Kim
Hong Kyu Lee
Publication date: 01-12-2014
Publisher: Springer US
Published in: Reviews in Endocrine and Metabolic Disorders / Issue 4/2014
Print ISSN: 1389-9155
Electronic ISSN: 1573-2606
DOI: https://doi.org/10.1007/s11154-014-9297-5

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Metabolic syndrome and the environmental pollutants from mitochondrial perspectives

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2014

Metabolic syndrome and lifestyle modification

Genetics of metabolic syndrome

Ectopic visceral fat: A clinical and molecular perspective on the cardiometabolic risk

Pharmacological treatment and therapeutic perspectives of metabolic syndrome

Fat sensing and metabolic syndrome

Skeletal muscle glucose metabolism and inflammation in the development of the metabolic syndrome

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page