Persistent organic pollutant exposure leads to insulin resistance syndrome

Environmental Health Perspectives

Volumn 118, Issue 4, 2010, Pages 465-471

  Ruzzin, Jérôme ^a   Petersen, Rasmus ^b,c   Meugnier, Emmanuelle ^d   Madsen, Lise ^a,c   Lock, Erik Jan ^a   Lillefosse, Haldis ^a   Ma, Tao ^b,c   Pesenti, Sandra ^d   Sonne, Si Brask ^c   Marstrand, Troels Torben ^e   Malde, Marian Kjellevold ^a   Du, Zhen Yu ^a   Chavey, Carine ^d   Fajas, Lluis ^d   Lundebye, Anne Katrine ^a   Brand, Christian Lehn ^f   Vidal, Hubert ^d   Kristiansen, Karsten ^c   Frøyland, Livar ^a  

^a INSTITUTE OF MARINE RESEARCH   (Norway)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d INSERM   (France)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f NOVO NORDISK A S   (Denmark)

Author keywords

Contaminants; Farmed salmon; Metabolic syndrome; Nonalcoholic fatty liver; Obesity; Pollution; Public health; Type 2 diabetes

Indexed keywords

CITRATE SYNTHASE; FAS ANTIGEN; FISH OIL; GENE PRODUCT; INSULIN; LIPIN 1 PROTEIN; LIVER X RECEPTOR; MEDIUM CHAIN ACYL COENZYME A DEHYDROGENASE; OMEGA 3 FATTY ACID; ORGANOCHLORINE PESTICIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; SUCCINATE DEHYDROGENASE; UNCLASSIFIED DRUG;

ABDOMINAL OBESITY; ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATLANTIC SALMON; BODY WEIGHT; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; FATTY LIVER; GENE EXPRESSION; GLUCOSE HOMEOSTASIS; HOMEOSTASIS; INSULIN INDUCED GENE 1; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIPID HOMEOSTASIS; LIPOPHILICITY; MALE; MICROARRAY ANALYSIS; NONHUMAN; ORGANIC POLLUTION; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT;

3T3-L1 CELLS; ANIMALS; CARBOHYDRATE METABOLISM; ENVIRONMENTAL POLLUTANTS; GLUCOSE; GLUCOSE CLAMP TECHNIQUE; HYDROCARBONS, CHLORINATED; INSULIN RESISTANCE; LIPID METABOLISM; MALE; METABOLIC SYNDROME X; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PESTICIDES; POLYMERASE CHAIN REACTION; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS; SALMO SALAR;

EID: 77951668711     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.0901321     Document Type: Article

References (59)

1. Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A. 2006. The estrogenic effect of bisphenol A disrupts pancreatic β-cell function in vivo and induces insulin resistance. Environ Health Perspect 114:106-112.
2. Angulo P. 2002. Nonalcoholic fatty liver disease. N Engl J Med 346(16):1221-1231.
3. Atlas E, Giam CS. 1981. Global transport of organic pollutants: ambient concentrations in the remote marine atmosphere. Science 211(4478):163-165.
4. Begum N, Sandu OA, Ito M, Lohmann SM, Smolenski A. 2002. Active Rho kinase (ROK-α) associates with insulin receptor substrate-1 and inhibits insulin signaling in vascular smooth muscle cells. J Biol Chem 277(8):6214-6222.
5. Berntssen MHG, Lundebye AK, Torstensen BE. 2005. Reducing the levels of dioxins and dioxin-like PCBs in farmed Atlantic salmon by substitution of fish oil with vegetable oil in the feed. Aquac Nutr 11(3):219-231.
6. Biddinger SB, Kahn CR. 2006. From mice to men: insights into the insulin resistance syndromes. Annu Rev Physiol 68:123-158.
7. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, et al. 2008. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118(2):789-800.
8. Brand CL, Sturis J, Gotfredsen CF, Fleckner J, Fledelius C, Hansen BF, et al. 2003. Dual PPARalpha/gamma activation provides enhanced improvement of insulin sensitivity and glycemic control in ZDF rats. Am J Physiol 284(4):E841-854.
9. Buren J, Liu HX, Jensen J, Eriksson JW. 2002. Dexamethasone impairs insulin signalling and glucose transport by depletion of insulin receptor substrate-1, phosphatidylinositol 3-kinase and protein kinase B in primary cultured rat adipocytes. Eur J Endocrinol 146(3):419-429.
10. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56(7):1761-1772.
11. Croce MA, Eagon JC, LaRiviere LL, Korenblat KM, Klein S, Finck BN. 2007. Hepatic lipin 1β expression is diminished in insulin-resistant obese subjects and is reactivated by marked weight loss. Diabetes 56(9):2395-2399.
12. Dougherty CP, Holtz SH, Reinert JC, Panyacosit L, Axelrad DA, Woodruff TJ. 2000. Dietary exposures to food contaminants across the United States. Environ Res 84(2):170-185.
13. Engelking LJ, Kuriyama H, Hammer RE, Horton JD, Brown MS, Goldstein JL, et al. 2004. Overexpression of Insig-1 in the livers of transgenic mice inhibits SREBP processing and reduces insulin-stimulated lipogenesis. J Clin Invest 113(8):1168-1175.
14. European Union. 2006. Amending regulation (EC) No 466/2001 setting maximum levels for certain contaminants in foodstuffs as regards dioxins and dioxin-like PCBs. Commission Regulation (EC) No 199/2006. Official Journal of the European Union L32:34-38. Available: http://www.health.gov.mt/fsc/fsc_euleg_files/RegEC199_2006e.pdf [accessed 19 February 2010].
15. European Union. 2008. Amending regulation (EC) No 396/2005 on maximum residue levels of pesticides in or on food and feed of plant and animal origin, as regards the implementing powers conferred on the Commission. Regulation (EC) No 299/2008. Official Journal of the European Union L97:37-71. Available: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2008:097:0067:0071:EN:PDF [accessed 19 February 2010].
16. Fierens S, Mairesse H, Heilier JF, De Burbure C, Focant JF, Eppe G, et al. 2003. Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: findings in a population-based study in Belgium. Biomarkers 8(6):529-534.
17. Finck BN, Gropler MC, Chen Z, Leone TC, Croce MA, Harris TE, et al. 2006. Lipin 1 is an inducible amplifier of the hepatic PGC-1alpha/PPARalpha regulatory pathway. Cell Metab 4(3):199-210.
18. Fisher BE. 1999. Most unwanted. Environ Health Perspect 107:A18-23.
19. Ford ES, Giles WH, Mokdad AH. 2004. Increasing prevalence of the metabolic syndrome among U.S adults. Diabetes Care 27(10):2444-2449.
20. Furukawa N, Ongusaha P, Jahng WJ, Araki K, Choi CS, Kim HJ, et al. 2005. Role of Rho-kinase in regulation of insulin action and glucose homeostasis. Cell Metab 2(2):119-129.
21. Guallar E, Aro A, Jimenez FJ, Martin-Moreno JM, Salminen I, van't Veer P, et al. 1999. Omega-3 fatty acids in adipose tissue and risk of myocardial infarction-The EURAMIC study. Arterioscler Thromb 19(4):1111-1118.
22. Henriksen GL, Ketchum NS, Michalek JE, Swaby JA. 1997. Serum dioxin and diabetes mellitus in veterans of Operation Ranch Hand. Epidemiology 8(3):252-258.
23. Hill JO, Peters JC. 1998. Environmental contributions to the obesity epidemic. Science 280(5368):1371-1374.
24. Hites RA, Foran JA, Carpenter DO, Hamilton MC, Knuth BA, Schwager SJ. 2004. Global assessment of organic contaminants in farmed salmon. Science 303(5655):226-229.
25. Jordal AEO, Lie O, Torstensen BE. 2007. Complete replacement of dietary fish oil with a vegetable oil blend affect liver lipid and plasma lipoprotein levels in Atlantic salmon (Salmo salar L.). Aquac Nutr 13(2):114-130.
26. Jorgenson JL. 2001. Aldrin and dieldrin: a review of research on their production, environmental deposition and fate, bioaccumulation, toxicology and epidemiology in the United States. Environ Health Perspect 109(suppl 1):113-139.
27. Julshamn K, Lundebye AK, Heggstad K, Berntssen MHG, Boe B. 2004. Norwegian monitoring programme on the inorganic and organic contaminants in fish caught in the Barents Sea, Norwegian Sea and North Sea, 1994-2001. Food Addit Contam 21(4):365-376.
28. Jump DB. 2002. The biochemistry of n-3 polyunsaturated fatty acids. J Biol Chem 277(11):8755-8758.
29. Kelishadi R, Mirghaffari N, Poursafa P, Gidding SS. 2009. Lifestyle and environmental factors associated with inflammation, oxidative stress and insulin resistance in children. Atherosclerosis 203(1):311-319.
30. Kiviranta H, Tuomisto JT, Tuomisto J, Tukiainen E, Vartiainen T. 2005. Polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in the general population in Finland. Chemosphere 60(7):854-869.
31. Kraegen EW, James DE, Bennett SP, Chisholm DJ. 1983. In vivo insulin sensitivity in the rat determined by euglycemic clamp. Am J Physiol 245(1):E1-E7.
32. Lavigne C, Tremblay F, Asselin G, Jacques H, Marette A. 2001. Prevention of skeletal muscle insulin resistance by dietary cod protein in high fat-fed rats. Am J Physiol 281(1):E62-E71.
33. Lee DH, Lee IK, Song K, Steffes M, Toscano W, Baker BA, et al. 2006. 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 29(7):1638-1644.
34. Lee JN, Ye J. 2004. Proteolytic activation of sterol regulatory element-binding protein induced by cellular stress through depletion of Insig-1. J Biol Chem 279(43):45257-45265.
35. Lee S, Muniyappa R, Yan X, Chen H, Yue LQ, Hong EG, et al. 2008. Comparison between surrogate indexes of insulin sensitivity and resistance and hyperinsulinemic euglycemic clamp estimates in mice. Am J Physiol 294(2):261-270.
36. Lowell BB, Shulman GI. 2005. Mitochondrial dysfunction and type 2 diabetes. Science 307(5708):384-387.
37. Nweke OC, Sanders WH III. 2009. Modern environmental health hazards: a public health issue of increasing significance in Africa. Environ Health Perspect 117:863-870.
38. Petersen RK, Madsen L, Pedersen LM, Hallenborg P, Hagland H, Viste K, et al. 2008. Cyclic AMP (cAMP)-mediated stimulation of adipocyte differentiation requires the synergistic action of Epac- and cAMP-dependent protein kinase-dependent processes. Mol Cell Biol 28(11):3804-3816.
39. Reaven GM. 2005. Why Syndrome X? From Harold Himsworth to the insulin resistance syndrome. Cell Metab 1(1):9-14.
40. Reeves PG, Nielsen FH, Fahey GC Jr. 1993. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123(11):1939-1951.
41. Rignell-Hydbom A, Rylander L, Hagmar L. 2007. Exposure to persistent organochlorine pollutants and type 2 diabetes mellitus. Hum Exp Toxicol 26(5):447-452.
42. Rissanen T, Voutilainen S, Nyyssonen K, Lakka TA, Salonen JT. 2000. Fish oil-derived fatty acids, docosahexaenoic acid and docosapentaenoic acid, and the risk of acute coronary events-the Kuopio Ischaemic Heart Disease Risk Factor Study. Circulation 102(22):2677-2679.
43. Roberts CK, Barnard RJ. 2005. Effects of exercise and diet on chronic disease. J Appl Physiol 98(1):3-30.
44. Rome S, Lecomte V, Meugnier E, Rieusset J, Debard C, Euthine V, et al. 2008. Microarray analyses of SREBP-1a and SREBP-1c target genes identify new regulatory pathways in muscle. Physiol Genomics 34(3):327-337.
45. Ruzzin J, Turcotte S, Leblanc V, Lavigne C, Froyland L, Remman TR, et al. 2007. Dietary salmon protein improves insulin sensitivity in high-fat fed obese rats [Abstract]. Ann Nutr Metab 51:347.
46. Ruzzin J, Wagman AS, Jensen J. 2005. Glucocorticoid-induced insulin resistance in skeletal muscles: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor. Diabetologia 48(10):2119-2130.
47. Schafer KS, Kegley SE. 2002. Persistent toxic chemicals in the US food supply. J Epidemiol Community Health 56(11):813-817.
48. Scientific Advisory Committee on Nutrition. 2004. Advice on Fish Consumption: Benefits and Risks. Available: http://cot.food.gov.uk/pdfs/fishreport2004full.pdf [accessed 19 February 2010].
49. Steele R, Wall JS, De Bodo RC, Altszuler N. 1956. Measurement of size and turnover rate of body glucose pool by the isotope dilution method. Am J Physiol 187(1):15-24.
50. Storlien LH, Kraegen E.W, Chisholm DJ, Ford GL, Bruce DG, Pascoe WS. 1987. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science 237(4817):885-888.
51. Sun Q, Yue P, Deiuliis JA, Lumeng CN, Kampfrath T, Mikolaj MB, et al. 2009. Ambient air pollution exaggerates adipose inflammation and insulin resistance in a mouse model of diet-induced obesity. Circulation 119(4):538-546.
52. Turyk M, Anderson HA, Knobeloch L, Imm P, Persky VW. 2009. Prevalence of diabetes and body burdens of polychlorinated biphenyls, polybrominated diphenyl ethers, and p,p ′-diphenyldichloroethene in Great Lakes sport fish consumers. Chemosphere 75(5):674-679.
53. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98(9):5116-5121.
54. Tzivion G, Shen YH, Zhu J. 2001. 14-3-3 Proteins; bringing new definitions to scaffolding. Oncogene 20(44):6331-6338.
55. Van den Berg H. 2009. Global status of DDT and its alternatives for use in vector control to prevent disease. Environ Health Perspect 17:1656-1663.
56. Van den Berg M, Birnbaum LS, Denison M, De Vito M, Farland W, Feeley M, et al. 2006. The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 93(2):223-241.
57. Wang SL, Tsai PC, Yang CY, Guo YL. 2008. Increased risk of diabetes and polychlorinated biphenyls and dioxins-a 24-year follow-up study of the Yucheng cohort. Diabetes Care 31(8):1574-1579.
58. WHO. 2005. Chronic Diseases: a Vital Investment. Geneva:World Health Organization. Available: http://www.who.int/chp/chronic_disease_report/contents/en/index.html [accessed 19 February 2010].
59. Zimmet P, Alberti KG, Shaw J. 2001. Global and societal implications of the diabetes epidemic. Nature 414(6865):782-787.