Unmasking differential effects of rosiglitazone and pioglitazone in the combination treatment with n-3 fatty acids in mice fed a high-fat diet

. 2011 ; 6 (11) : e27126. [epub] 20111103

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid22073272

Combining pharmacological treatments and life style interventions is necessary for effective therapy of major diseases associated with obesity, which are clustered in the metabolic syndrome. Acting via multiple mechanisms, combination treatments may reduce dose requirements and, therefore, lower the risk of adverse side effects, which are usually associated with long-term pharmacological interventions. Our previous study in mice fed high-fat diet indicated additivity in preservation of insulin sensitivity and in amelioration of major metabolic syndrome phenotypes by the combination treatment using n-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFA) and rosiglitazone, i.e. an anti-diabetic drug of the thiazolidinedione (TZD) family. We investigated here whether pioglitazone, a TZD-drug in clinical use, could elicit the additive beneficial effects when combined with n-3 LC-PUFA. Adult male mice (C57BL/6N) were fed an obesogenic corn oil-based high-fat diet (cHF) for 8 weeks, or randomly assigned to various dietary treatments (i) cHF+F, cHF with n-3 LC-PUFA concentrate replacing 15% of dietary lipids; (ii) cHF+ROSI, cHF with 10 mg rosiglitazone/kg diet; (iii) cHF+F+ROSI; (iv) cHF+PIO, cHF with 50 mg pioglitazone/kg diet; and (v) cHF+F+PIO, or chow-fed. Plasma concentrations of 163 metabolites were evaluated using a targeted metabolomics approach. Both TZDs preserved glucose homeostasis and normal plasma lipid levels while inducing adiponectin, with pioglitazone showing better effectiveness. The beneficial effects of TZDs were further augmented by the combination treatments. cHF+F+ROSI but not cHF+F+PIO counteracted development of obesity, in correlation with inducibility of fatty acid β-oxidation, as revealed by the metabolomic analysis. By contrast, only cHF+F+PIO eliminated hepatic steatosis and this treatment also reversed insulin resistance in dietary obese mice. Our results reveal differential effects of rosiglitazone and pioglitazone, unmasked in the combination treatment with n-3 LC-PUFA, and support the notion that n-3 LC-PUFA could be used as add-on treatment to TZDs in order to improve diabetic patient's therapy.

Zobrazit více v PubMed

Galgani JE, Moro C, Ravussin E. Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab. 2008;295:E1009–E1017. PubMed PMC

Kopelman PG. Obesity as a medical problem. Nature. 2000;404:635–643. PubMed

Bays HE, Maki KC, McKenney J, Snipes R, Meadowcroft A, et al. Long-term up to 24-month efficacy and safety of concomitant prescription omega-3-acid ethyl esters and simvastatin in hypertriglyceridemic patients. Curr Med Res Opin. 2010;26:907–915. PubMed

Reyes-Soffer G, Rondon-Clavo C, Ginsberg HN. Combination therapy with statin and fibrate in patients with dyslipidemia associated with insulin resistance, metabolic syndrome and type 2 diabetes mellitus. Expert Opin Pharmacother. 2011;12:1429–1438. PubMed

Nathan DM, Buse JB, Davidson MB, Ferrannini E, Holman RR, et al. Management of hyperglycaemia in type 2 diabetes mellitus: a consensus algorithm for the initiation and adjustment of therapy. Update regarding the thiazolidinediones. Diabetologia. 2008;51:8–11. PubMed

Edelstein SL, Knowler WC, Bain RP, Andres R, Barrett-Connor EL, et al. Predictors of progression from impaired glucose tolerance to NIDDM: an analysis of six prospective studies. Diabetes. 1997;46:701–710. PubMed PMC

Bell DS, Al Badarin F, O'Keefe JH., Jr Therapies for diabetic dyslipidaemia. Diabetes Obes Metab. 2011;13:313–325. PubMed

Loke YK, Kwok CS, Singh S. Comparative cardiovascular effects of thiazolidinediones: systematic review and meta-analysis of observational studies. BMJ. 2011;342:d1309. PubMed PMC

Yang X, Smith U. Adipose tissue distribution and risk of metabolic disease: does thiazolidinedione-induced adipose tissue redistribution provide a clue to the answer? Diabetologia. 2007;50:1127–1139. PubMed

Goldberg RB, Kendall DM, Deeg MA, Buse JB, Zagar AJ, et al. A comparison of lipid and glycemic effects of pioglitazone and rosiglitazone in patients with type 2 diabetes and dyslipidemia. Diabetes Care. 2005;28:1547–1554. PubMed

Deeg MA, Buse JB, Goldberg RB, Kendall DM, Zagar AJ, et al. Pioglitazone and rosiglitazone have different effects on serum lipoprotein particle concentrations and sizes in patients with type 2 diabetes and dyslipidemia. Diabetes Care. 2007;30:2458–2464. PubMed

Lewis JD, Ferrara A, Peng T, Hedderson M, Bilker WB, et al. Risk of bladder cancer among diabetic patients treated with pioglitazone: interim report of a longitudinal cohort study. Diabetes Care. 2011;34:916–922. PubMed PMC

Whitehead JP. Diabetes: New conductors for the peroxisome proliferator-activated receptor gamma (PPARgamma) orchestra. Int J Biochem Cell Biol. 2011;43:1071–1074. PubMed

Wilson-Fritch L, Nicoloro S, Chouinard M, Lazar MA, Chui PC, et al. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J Clin Invest. 2004;114:1281–1289. PubMed PMC

Kim H, Haluzik M, Gavrilova O, Yakar S, Portas J, et al. Thiazolidinediones improve insulin sensitivity in adipose tissue and reduce the hyperlipidaemia without affecting the hyperglycaemia in a transgenic model of type 2 diabetes. Diabetologia. 2004;47:2215–2225. PubMed

Wang P, Renes J, Bouwman F, Bunschoten A, Mariman E, et al. Absence of an adipogenic effect of rosiglitazone on mature 3T3-L1 adipocytes: increase of lipid catabolism and reduction of adipokine expression. Diabetologia. 2007;50:654–665. PubMed PMC

Higashi Y, Holder K, Delafontaine P. Thiazolidinediones up-regulate insulin-like growth factor-1 receptor via a peroxisome proliferator-activated receptor gamma-independent pathway. J Biol Chem. 2010;285:36361–36368. PubMed PMC

Yamauchi T, Waki H, Kamon J, Murakami K, Motojima K, et al. Inhibition of RXR and PPARgamma ameliorates diet-induced obesity and type 2 diabetes. J Clin Invest. 2001;108:1001–1013. PubMed PMC

Yang KJ, Noh JR, Kim YH, Gang GT, Hwang JH, et al. Differential modulatory effects of rosiglitazone and pioglitazone on white adipose tissue in db/db mice. LIFE Sci. 2010;87:405–410. PubMed

Kuda O, Stankova B, Tvrzicka E, Hensler M, Jelenik T, et al. Prominent role of liver in elevated plasma palmitooleate levels in response to rosiglitazone in mice fed high-fat diet. J Physiol Pharmacol. 2009;60:135–140. PubMed

Kuda O, Jelenik T, Jilkova Z, Flachs P, Rossmeisl M, et al. n-3 Fatty acids and rosiglitazone improve insulin sensitivity through additive stimulatory effects on muscle glycogen synthesis in mice fed a high-fat diet. Diabetologia. 2009;52:941–951. PubMed

Djaouti L, Jourdan T, Demizieux L, Chevrot M, Gresti J, et al. Different effects of pioglitazone and rosiglitazone on lipid metabolism in mouse cultured liver explants. Diabetes Metab Res Rev. 2010;26:297–305. PubMed

Wilmsen HM, Ciaraldi TP, Carter L, Reehman N, Mudaliar SR, et al. Thiazolidinediones upregulate impaired fatty acid uptake in skeletal muscle of type 2 diabetic subjects. Am J Physiol Endocrinol Metab. 2003;285:E354–E362. PubMed

Rabol R, Boushel R, Almdal T, Hansen CN, Ploug T, et al. Opposite effects of pioglitazone and rosiglitazone on mitochondrial respiration in skeletal muscle of patients with type 2 diabetes. Diabetes Obes Metab. 2010;12:806–814. PubMed

Gillies CL, Abrams KR, Lambert PC, Cooper NJ, Sutton AJ, et al. Pharmacological and lifestyle interventions to prevent or delay type 2 diabetes in people with impaired glucose tolerance: systematic review and meta-analysis. BMJ. 2007;334:299. PubMed PMC

Nettleton JA, Katz R. n-3 long-chain polyunsaturated fatty acids in type 2 diabetes: a review. J Am Diet Assoc. 2005;105:428–440. PubMed

Ruxton CH, Reed SC, Simpson MJ, Millington KJ. The health benefits of omega-3 polyunsaturated fatty acids: a review of the evidence. J Hum Nutr Diet. 2007;17:449–459. PubMed

Riserus U, Willett WC, Hu FB. Dietary fats and prevention of type 2 diabetes. Prog Lipid Res. 2009;48:44–51. PubMed PMC

Kromhout D, Giltay EJ, Geleijnse JM. n-3 fatty acids and cardiovascular events after myocardial infarction. N Engl J Med. 2010;363:2015–2026. PubMed

Kunesova M, Braunerova R, Hlavaty P, Tvrzicka E, Stankova B, et al. The influence of n-3 polyunsaturated fatty acids and very low calorie diet during a short-term weight reducing regimen on weight loss and serum fatty acid composition in severely obese women. Physiol Res. 2006;55:63–72. PubMed

Fasching P, Ratheiser K, Waldhausl W, Rohac M, Osterrode W, et al. Metabolic effects of fish-oil supplementation in patients with impaired glucose tolerance. Diabetes. 1991;40:583–589. PubMed

Pelikanova T, Kohout M, Valek J, Kazdova L, Base J. Metabolic effects of omega-3 fatty acids in type 2 (non-insulin-dependent) diabetic patients. Ann N Y Acad Sci. 1993;683:272–278. PubMed

Storlien LH, Kraegen EW, Chisholm DJ, Ford GL, Bruce DG, et al. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science. 1987;237:885–888. PubMed

Jucker BM, Cline GW, Barucci N, Shulman GI. Differential effects of safflower oil versus fish oil feeding on insulin-stimulated glycogen synthesis, glycolysis, and pyruvate dehydrogenase flux in skeletal muscle: a 13C nuclear magnetic resonance study. Diabetes. 1999;48:134–140. PubMed

Flachs P, Mohamed-Ali V, Horakova O, Rossmeisl M, Hosseinzadeh-Attar MJ, et al. Polyunsaturated fatty acids of marine origin induce adiponectin in mice fed high-fat diet. Diabetologia. 2006;49:394–397. PubMed

Neschen S, Morino K, Rossbacher JC, Pongratz RL, Cline GW, et al. Fish oil regulates adiponectin secretion by a peroxisome proliferator-activated receptor-gamma-dependent mechanism in mice. Diabetes. 2006;55:924–928. PubMed

Jelenik T, Rossmeisl M, Kuda O, Jilkova ZM, Medrikova D, et al. AMP-activated protein kinase alpha2 subunit is required for the preservation of hepatic insulin sensitivity by n-3 polyunsaturated fatty acids. Diabetes. 2010;59:2737–2746. PubMed PMC

Flachs P, Ruhl R, Hensler M, Janovská P, Zouhar P, et al. Synergistic induction of lipid catabolism and anti-inflammatory lipids in white fat of dietary obese mice in response to calorie restriction and n-3 fatty acids. Diabetologia. 2011;54:2626–2638. PubMed

Ikemoto S, Takahashi M, Tsunoda N, Maruyama K, Itakura H, et al. High-fat diet-induced hyperglycemia and obesity in mice: Differential effects of dietary oils. Metabolism. 1996;45:1539–1546. PubMed

Ruzickova J, Rossmeisl M, Prazak T, Flachs P, Sponarova J, et al. Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids. 2004;39:1177–1185. PubMed

Flachs P, Horakova O, Brauner P, Rossmeisl M, Pecina P, et al. Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia. 2005;48:2365–2375. PubMed

Todoric J, Loffler M, Huber J, Bilban M, Reimers M, et al. Adipose tissue inflammation induced by high-fat diet in obese diabetic mice is prevented by n-3 polyunsaturated fatty acids. Diabetologia. 2006;49:2109–2119. PubMed

Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, et al. GPR120 Is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell. 2010;142:687–698. PubMed PMC

Libby P, Plutzky J. Inflammation in diabetes mellitus: role of peroxisome proliferator-activated receptor-alpha and peroxisome proliferator-activated receptor-gamma agonists. Am J Cardiol. 2007;99:27B–40B. PubMed

Saravanan P, Davidson NC, Schmidt EB, Calder PC. Cardiovascular effects of marine omega-3 fatty acids. Lancet. 2010;376:540–550. PubMed

Jump DB. Fatty acid regulation of gene transcription. Crit Rev Clin Lab Sci. 2004;41:41–78. PubMed

Madsen L, Petersen RK, Kristiansen K. Regulation of adipocyte differentiation and function by polyunsaturated fatty acids. Biochim Biophys Acta. 2005;1740:266–286. PubMed

Serhan CN. Novel omega-3-derived local mediators in anti-inflammation and resolution. Pharmacol Ther. 2005;105:7–21. PubMed

van Schothorst EM, Flachs P, Franssen-van Hal NL, Kuda O, Bunschoten A, et al. Induction of lipid oxidation by polyunsaturated fatty acids of marine origin in small intestine of mice fed a high-fat diet. BMC Genomics. 2009;10:110. PubMed PMC

Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 2008;7:45–56. PubMed

Pietilainen KH, Sysi-Aho M, Rissanen A, Seppanen-Laakso T, Yki-Jarvinen H, et al. Acquired obesity is associated with changes in the serum lipidomic profile independent of genetic effects--a monozygotic twin study. PLoS ONE. 2007;2:e218. PubMed PMC

Lankinen M, Schwab U, Erkkila A, Seppanen-Laakso T, Hannila ML, et al. Fatty fish intake decreases lipids related to inflammation and insulin signaling-a lipidomics approach. PLoS ONE. 2009;4:e5258. PubMed PMC

Mihalik SJ, Goodpaster BH, Kelley DE, Chace DH, Vockley J, et al. Increased levels of plasma acylcarnitines in obesity and type 2 diabetes and identification of a marker of glucolipotoxicity. Obesity (Silver Spring) 2010;18:1695–1700. PubMed PMC

Lehmann R, Zhao X, Weigert C, Simon P, Fehrenbach E, et al. Medium chain acylcarnitines dominate the metabolite pattern in humans under moderate intensity exercise and support lipid oxidation. PLoS ONE. 2010;5:e11519. PubMed PMC

Hallows WC, Yu W, Smith BC, Devries MK, Ellinger JJ, et al. Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction. Mol Cell. 2011;41:139–149. PubMed PMC

Zhao X, Peter A, Fritsche J, Elcnerova M, Fritsche A, et al. Changes of the plasma metabolome during an oral glucose tolerance test: is there more than glucose to look at? Am J Physiol Endocrinol Metab. 2009;296:E384–E393. PubMed

Huo T, Cai S, Lu X, Sha Y, Yu M, et al. Metabonomic study of biochemical changes in the serum of type 2 diabetes mellitus patients after the treatment of metformin hydrochloride. J Pharm Biomed Anal. 2009;49:976–982. PubMed

Nawrocki AR, Rajala MW, Tomas E, Pajvani UB, Saha AK, et al. Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists. J Biol Chem. 2006;281:2654–2660. PubMed

Medrikova D, Macek JZ, Bardova K, Janovská P, Rossmeisl M et al. Int J Obes; 2011. Sex differences during the course of diet-induced obesity in mice: adipose tissue expandability and glycemic control. doi: 10.1038/ijo.2011.87. PubMed DOI

Illig T, Gieger C, Zhai G, Romisch-Margl W, Wang-Sattler R, et al. A genome-wide perspective of genetic variation in human metabolism. Nat Genet. 2010;42:137–141. PubMed PMC

The Endocrine Society Statement to providers on the suspension of sales of pioglitazone by regulatory agencies in France and Germany. 2011. Available: http://www.endo-society.org/advocacy/policy/upload/TES-Pioglitazone-Statement-Final.pdf Issued on June 13, 2011.

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Omega-3 PUFAs prevent bone impairment and bone marrow adiposity in mouse model of obesity

. 2023 Oct 14 ; 6 (1) : 1043. [epub] 20231014

Novel thiazolidinedione analog reduces a negative impact on bone and mesenchymal stem cell properties in obese mice compared to classical thiazolidinediones

. 2022 Nov ; 65 () : 101598. [epub] 20220911

Additive Effects of Omega-3 Fatty Acids and Thiazolidinediones in Mice Fed a High-Fat Diet: Triacylglycerol/Fatty Acid Cycling in Adipose Tissue

. 2020 Dec 04 ; 12 (12) : . [epub] 20201204

Omega-3 Phospholipids from Krill Oil Enhance Intestinal Fatty Acid Oxidation More Effectively than Omega-3 Triacylglycerols in High-Fat Diet-Fed Obese Mice

. 2020 Jul 09 ; 12 (7) : . [epub] 20200709

Reduced Number of Adipose Lineage and Endothelial Cells in Epididymal fat in Response to Omega-3 PUFA in Mice Fed High-Fat Diet

. 2018 Dec 18 ; 16 (12) : . [epub] 20181218

Plasma Acylcarnitines and Amino Acid Levels As an Early Complex Biomarker of Propensity to High-Fat Diet-Induced Obesity in Mice

. 2016 ; 11 (5) : e0155776. [epub] 20160516

Combined intervention with pioglitazone and n-3 fatty acids in metformin-treated type 2 diabetic patients: improvement of lipid metabolism

. 2015 ; 12 () : 52. [epub] 20151202

Adipose tissue-related proteins locally associated with resolution of inflammation in obese mice

. 2014 Feb ; 38 (2) : 216-23. [epub] 20130612

Preservation of metabolic flexibility in skeletal muscle by a combined use of n-3 PUFA and rosiglitazone in dietary obese mice

. 2012 ; 7 (8) : e43764. [epub] 20120831

Metabolic effects of n-3 PUFA as phospholipids are superior to triglycerides in mice fed a high-fat diet: possible role of endocannabinoids

. 2012 ; 7 (6) : e38834. [epub] 20120611

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...