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Article

Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle

  • Authors:
    • Wenjuan Tang
    • Sunyinyan Tang
    • Hongdong Wang
    • Zhijuan Ge
    • Dalong Zhu
    • Yan Bi
  • View Affiliations / Copyright

    Affiliations: Department of Endocrinology, Drum Tower Hospital Affiliated to Nanjing University Medical School, Nanjing, Jiangsu 210008, P.R. China
  • Pages: 2000-2010
    |
    Published online on: October 2, 2017
       https://doi.org/10.3892/ijmm.2017.3169
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Abstract

An early insulin regimen ameliorates glucotoxicity but also lipotoxicity in type 2 diabetes; however, the underlying mechanism remains elusive. In the present study, we investigated the role of mitochondria in lipid regulation following early insulin administration in insulin-resistant skeletal muscle cells. Male C57BL/6 mice, fed a high-fat diet (HFD) for 8 weeks, were treated with insulin for 3 weeks, and L6 myotubes cultured with palmitate (PA) for 24 h were incubated with insulin for another 12 h. The results showed that insulin facilitated systemic glucose disposal and attenuated muscular triglyceride accumulation in vivo. Recovery of AMP-activated protein kinase (AMPK) phosphorylation, inhibition of sterol-regulated element binding protein-1c (SREBP-1c) and increased carnitine palmitoyltransferase‑1B (CPT1B) expression were observed after insulin administration. Moreover, increased ATP concentration and cellular energy charge elicited by over-nutrition were suppressed by insulin. Despite maintaining respiratory complex activities, insulin restored muscular uncoupling protein 3 (UCP3) protein expression in vitro and in vivo. By contrast, knockdown of UCP3 abrogated insulin-induced restoration of AMPK phosphorylation in vitro. Importantly, the PA-induced decrease in UCP3 was blocked by the proteasome inhibitor MG132, and insulin reduced UCP3 ubiquitination, thereby prohibiting its degradation. Our findings, focusing on energy balance, provide a mechanistic understanding of the promising effect of early insulin initiation on lipotoxicity. Insulin, by recovering UCP3 activity, alleviated energy surfeit and potentiated AMPK-mediated lipid homeostasis in skeletal muscle cells following exposure to PA and in gastrocnemius of mice fed HFD.
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1 

Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U and Shaw JE: Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 103:137–149. 2014. View Article : Google Scholar : PubMed/NCBI

2 

Kramer CK, Zinman B and Retnakaran R: Short-term intensive insulin therapy in type 2 diabetes mellitus: A systematic review and meta-analysis. Lancet Diabetes Endocrinol. 1:28–34. 2013. View Article : Google Scholar

3 

Hu Y, Li L, Xu Y, Yu T, Tong G, Huang H, Bi Y, Weng J and Zhu D: Short-term intensive therapy in newly diagnosed type 2 diabetes partially restores both insulin sensitivity and β-cell function in subjects with long-term remission. Diabetes Care. 34:1848–1853. 2011. View Article : Google Scholar : PubMed/NCBI

4 

Weng J, Li Y, Xu W, Shi L, Zhang Q, Zhu D, Hu Y, Zhou Z, Yan X, Tian H, et al: Effect of intensive insulin therapy on beta-cell function and glycaemic control in patients with newly diagnosed type 2 diabetes: A multicentre randomised parallel-group trial. Lancet. 371:1753–1760. 2008. View Article : Google Scholar : PubMed/NCBI

5 

Samuel VT, Petersen KF and Shulman GI: Lipid-induced insulin resistance: Unravelling the mechanism. Lancet. 375:2267–2277. 2010. View Article : Google Scholar : PubMed/NCBI

6 

Shulman GI, Rothman DL, Jue T, Stein P, DeFronzo RA and Shulman RG: Quantitation of muscle glycogen synthesis in normal subjects and subjects with non-insulin-dependent diabetes by 13C nuclear magnetic resonance spectroscopy. N Engl J Med. 322:223–228. 1990. View Article : Google Scholar : PubMed/NCBI

7 

Eckardt K, Taube A and Eckel J: Obesity-associated insulin resistance in skeletal muscle: Role of lipid accumulation and physical inactivity. Rev Endocr Metab Disord. 12:163–172. 2011. View Article : Google Scholar : PubMed/NCBI

8 

Itani SI, Ruderman NB, Schmieder F and Boden G: Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes. 51:2005–2011. 2002. View Article : Google Scholar : PubMed/NCBI

9 

Samuel VT and Shulman GI: Mechanisms for insulin resistance: Common threads and missing links. Cell. 148:852–871. 2012. View Article : Google Scholar : PubMed/NCBI

10 

Guillet-Deniau I, Mieulet V, Le Lay S, Achouri Y, Carré D, Girard J, Foufelle F and Ferré P: Sterol regulatory element binding protein-1c expression and action in rat muscles: Insulin-like effects on the control of glycolytic and lipogenic enzymes and UCP3 gene expression. Diabetes. 51:1722–1728. 2002. View Article : Google Scholar : PubMed/NCBI

11 

Guillet-Deniau I, Pichard AL, Koné A, Esnous C, Nieruchalski M, Girard J and Prip-Buus C: Glucose induces de novo lipogenesis in rat muscle satellite cells through a sterol-regulatory-element-binding-protein-1c-dependent pathway. J Cell Sci. 117:1937–1944. 2004. View Article : Google Scholar : PubMed/NCBI

12 

Tsintzas K, Jewell K, Kamran M, Laithwaite D, Boonsong T, Littlewood J, Macdonald I and Bennett A: Differential regulation of metabolic genes in skeletal muscle during starvation and refeeding in humans. J Physiol. 575:291–303. 2006. View Article : Google Scholar : PubMed/NCBI

13 

Bruce CR, Anderson MJ, Carey AL, Newman DG, Bonen A, Kriketos AD, Cooney GJ and Hawley JA: Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J Clin Endocrinol Metab. 88:5444–5451. 2003. View Article : Google Scholar : PubMed/NCBI

14 

Kim JY, Hickner RC, Cortright RL, Dohm GL and Houmard JA: Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab. 279:E1039–E1044. 2000.PubMed/NCBI

15 

Ukropcova B, Sereda O, de Jonge L, Bogacka I, Nguyen T, Xie H, Bray GA and Smith SR: Family history of diabetes links impaired substrate switching and reduced mitochondrial content in skeletal muscle. Diabetes. 56:720–727. 2007. View Article : Google Scholar : PubMed/NCBI

16 

Li Y, Xu S, Mihaylova MM, Zheng B, Hou X, Jiang B, Park O, Luo Z, Lefai E, Shyy JY, et al: AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metab. 13:376–388. 2011. View Article : Google Scholar : PubMed/NCBI

17 

Ronnett GV, Kleman AM, Kim EK, Landree LE and Tu Y: Fatty acid metabolism, the central nervous system, and feeding. Obesity (Silver Spring). 14(Suppl 5): 201S–207S. 2006. View Article : Google Scholar

18 

Kjøbsted R, Pedersen AJ, Hingst JR, Sabaratnam R, Birk JB, Kristensen JM, Højlund K and Wojtaszewski JF: Intact regulation of the AMPK signaling network in response to exercise and insulin in skeletal muscle of male patients with type 2 diabetes: Illumination of AMPK activation in recovery from exercise. Diabetes. 65:1219–1230. 2016. View Article : Google Scholar : PubMed/NCBI

19 

Tang S, Wu W, Tang W, Ge Z, Wang H, Hong T, Zhu D and Bi Y: Suppression of Rho-kinase 1 is responsible for insulin regulation of the AMPK/SREBP-1c pathway in skeletal muscle cells exposed to palmitate. Acta Diabetol. Mar 7–2017.Epub ahead of print. View Article : Google Scholar

20 

Saltiel AR: New therapeutic approaches for the treatment of obesity. Sci Transl Med. 8:323rv22016. View Article : Google Scholar : PubMed/NCBI

21 

Busiello RA, Savarese S and Lombardi A: Mitochondrial uncoupling proteins and energy metabolism. Front Physiol. 6:362015. View Article : Google Scholar : PubMed/NCBI

22 

Krook A, Digby J, O'Rahilly S, Zierath JR and Wallberg-Henriksson H: Uncoupling protein 3 is reduced in skeletal muscle of NIDDM patients. Diabetes. 47:1528–1531. 1998. View Article : Google Scholar : PubMed/NCBI

23 

Mensink M, Hesselink MK, Borghouts LB, Keizer H, Moonen-Kornips E, Schaart G, Blaak EE and Schrauwen P: Skeletal muscle uncoupling protein-3 restores upon intervention in the prediabetic and diabetic state: Implications for diabetes pathogenesis? Diabetes Obes Metab. 9:594–596. 2007. View Article : Google Scholar : PubMed/NCBI

24 

Schrauwen P, Hesselink MK, Blaak EE, Borghouts LB, Schaart G, Saris WH and Keizer HA: Uncoupling protein 3 content is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes. 50:2870–2873. 2001. View Article : Google Scholar : PubMed/NCBI

25 

Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, Moore GB, Piercy V, Carter SA, Lehner I, Smith SA, et al: Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature. 406:415–418. 2000. View Article : Google Scholar : PubMed/NCBI

26 

Costford SR, Chaudhry SN, Salkhordeh M and Harper ME: Effects of the presence, absence, and overexpression of uncoupling protein-3 on adiposity and fuel metabolism in congenic mice. Am J Physiol Endocrinol Metab. 290:E1304–E1312. 2006. View Article : Google Scholar : PubMed/NCBI

27 

Son C, Hosoda K, Ishihara K, Bevilacqua L, Masuzaki H, Fushiki T, Harper ME and Nakao K: Reduction of diet-induced obesity in transgenic mice overexpressing uncoupling protein 3 in skeletal muscle. Diabetologia. 47:47–54. 2004. View Article : Google Scholar

28 

Petersen KF, Dufour S and Shulman GI: Decreased insulin-stimulated ATP synthesis and phosphate transport in muscle of insulin-resistant offspring of type 2 diabetic parents. PLoS Med. 2:e2332005. View Article : Google Scholar : PubMed/NCBI

29 

Stump CS, Short KR, Bigelow ML, Schimke JM and Nair KS: Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc Natl Acad Sci USA. 100:7996–8001. 2003. View Article : Google Scholar : PubMed/NCBI

30 

Bi Y, Cai M, Liang H, Sun W, Li X, Wang C, Zhu Y, Chen X, Li M and Weng J: Increased carnitine palmitoyl transferase 1 expression and decreased sterol regulatory element-binding protein 1c expression are associated with reduced intramuscular triglyceride accumulation after insulin therapy in high-fat-diet and streptozotocin-induced diabetic rats. Metabolism. 58:779–786. 2009. View Article : Google Scholar : PubMed/NCBI

31 

Bi Y, Wu W, Shi J, Liang H, Yin W, Chen Y, Tang S, Cao S, Cai M, Shen S, et al: Role for sterol regulatory element binding protein-1c activation in mediating skeletal muscle insulin resistance via repression of rat insulin receptor substrate-1 transcription. Diabetologia. 57:592–602. 2014. View Article : Google Scholar

32 

Xie B, Chen Q, Chen L, Sheng Y, Wang HY and Chen S: The Inactivation of RabGAP function of AS160 promotes lysosomal degradation of GLUT4 and causes postprandial hyperglycemia and hyperinsulinemia. Diabetes. 65:3327–3340. 2016. View Article : Google Scholar : PubMed/NCBI

33 

Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar

34 

Bhatt DP, Chen X, Geiger JD and Rosenberger TA: A sensitive HPLC-based method to quantify adenine nucleotides in primary astrocyte cell cultures. J Chromatogr B Analyt Technol Biomed Life Sci. 889–890:110–115. 2012. View Article : Google Scholar

35 

Azzu V, Mookerjee SA and Brand MD: Rapid turnover of mitochondrial uncoupling protein 3. Biochem J. 426:13–17. 2010. View Article : Google Scholar

36 

Mookerjee SA and Brand MD: Characteristics of the turnover of uncoupling protein 3 by the ubiquitin proteasome system in isolated mitochondria. Biochim Biophys Acta. 1807:1474–1481. 2011. View Article : Google Scholar : PubMed/NCBI

37 

Bi Y, Sun WP, Chen X, Li M, Liang H, Cai MY, Zhu YH, He XY, Xu F and Weng JP: Effect of early insulin therapy on nuclear factor kappaB and cytokine gene expressions in the liver and skeletal muscle of high-fat diet, streptozotocin-treated diabetic rats. Acta Diabetol. 45:167–178. 2008. View Article : Google Scholar : PubMed/NCBI

38 

Pagel-Langenickel I, Bao J, Pang L and Sack MN: The role of mitochondria in the pathophysiology of skeletal muscle insulin resistance. Endocr Rev. 31:25–51. 2010. View Article : Google Scholar :

39 

Szendroedi J, Phielix E and Roden M: The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol. 8:92–103. 2011. View Article : Google Scholar : PubMed/NCBI

40 

Zhang Y and Ye J: Mitochondrial inhibitor as a new class of insulin sensitizer. Acta Pharm Sin B. 2:341–349. 2012. View Article : Google Scholar

41 

Bridges HR, Jones AJ, Pollak MN and Hirst J: Effects of metformin and other biguanides on oxidative phosphorylation in mitochondria. Biochem J. 462:475–487. 2014. View Article : Google Scholar : PubMed/NCBI

42 

Foretz M, Hébrard S, Leclerc J, Zarrinpashneh E, Soty M, Mithieux G, Sakamoto K, Andreelli F and Viollet B: Metformin inhibits hepatic gluconeogenesis in mice independently of the LKB1/AMPK pathway via a decrease in hepatic energy state. J Clin Invest. 120:2355–2369. 2010. View Article : Google Scholar : PubMed/NCBI

43 

Owen MR, Doran E and Halestrap AP: Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J. 348:607–614. 2000. View Article : Google Scholar : PubMed/NCBI

44 

Turner N, Li JY, Gosby A, To SW, Cheng Z, Miyoshi H, Taketo MM, Cooney GJ, Kraegen EW, James DE, et al: Berberine and its more biologically available derivative, dihydroberberine, inhibit mitochondrial respiratory complex I: A mechanism for the action of berberine to activate AMP-activated protein kinase and improve insulin action. Diabetes. 57:1414–1418. 2008. View Article : Google Scholar : PubMed/NCBI

45 

Xia X, Yan J, Shen Y, Tang K, Yin J, Zhang Y, Yang D, Liang H, Ye J and Weng J: Berberine improves glucose metabolism in diabetic rats by inhibition of hepatic gluconeogenesis. PLoS One. 6:e165562011. View Article : Google Scholar : PubMed/NCBI

46 

Gledhill JR, Montgomery MG, Leslie AG and Walker JE: Mechanism of inhibition of bovine F1-ATPase by resveratrol and related polyphenols. Proc Natl Acad Sci USA. 104:13632–13637. 2007. View Article : Google Scholar : PubMed/NCBI

47 

Szendroedi J, Schmid AI, Chmelik M, Toth C, Brehm A, Krssak M, Nowotny P, Wolzt M, Waldhausl W and Roden M: Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med. 4:e1542007. View Article : Google Scholar : PubMed/NCBI

48 

Sreekumar R, Halvatsiotis P, Schimke JC and Nair KS: Gene expression profile in skeletal muscle of type 2 diabetes and the effect of insulin treatment. Diabetes. 51:1913–1920. 2002. View Article : Google Scholar : PubMed/NCBI

49 

Retnakaran R and Zinman B: Short-term intensified insulin treatment in type 2 diabetes: Long-term effects on β-cell function. Diabetes Obes Metab. 14(Suppl 3): 161–166. 2012. View Article : Google Scholar

50 

Parascandola J: Dinitrophenol and bioenergetics: An historical perspective. Mol Cell Biochem. 5:69–77. 1974. View Article : Google Scholar : PubMed/NCBI

51 

Perry RJ, Kim T, Zhang XM, Lee HY, Pesta D, Popov VB, Zhang D, Rahimi Y, Jurczak MJ, Cline GW, et al: Reversal of hypertriglyceridemia, fatty liver disease, and insulin resistance by a liver-targeted mitochondrial uncoupler. Cell Metab. 18:740–748. 2013. View Article : Google Scholar : PubMed/NCBI

52 

Tao H, Zhang Y, Zeng X, Shulman GI and Jin S: Niclosamide ethanolamine-induced mild mitochondrial uncoupling improves diabetic symptoms in mice. Nat Med. 20:1263–1269. 2014. View Article : Google Scholar : PubMed/NCBI

53 

Ligeret H, Barthélémy S, Bouchard Doulakas G, Carrupt PA, Tillement JP, Labidalle S and Morin D: Fluoride curcumin derivatives: New mitochondrial uncoupling agents. FEBS Lett. 569:37–42. 2004. View Article : Google Scholar : PubMed/NCBI

54 

Lim HW, Lim HY and Wong KP: Uncoupling of oxidative phosphorylation by curcumin: Implication of its cellular mechanism of action. Biochem Biophys Res Commun. 389:187–192. 2009. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Tang W, Tang S, Wang H, Ge Z, Zhu D and Bi Y: Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle. Int J Mol Med 40: 2000-2010, 2017.
APA
Tang, W., Tang, S., Wang, H., Ge, Z., Zhu, D., & Bi, Y. (2017). Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle. International Journal of Molecular Medicine, 40, 2000-2010. https://doi.org/10.3892/ijmm.2017.3169
MLA
Tang, W., Tang, S., Wang, H., Ge, Z., Zhu, D., Bi, Y."Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle". International Journal of Molecular Medicine 40.6 (2017): 2000-2010.
Chicago
Tang, W., Tang, S., Wang, H., Ge, Z., Zhu, D., Bi, Y."Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle". International Journal of Molecular Medicine 40, no. 6 (2017): 2000-2010. https://doi.org/10.3892/ijmm.2017.3169
Copy and paste a formatted citation
x
Spandidos Publications style
Tang W, Tang S, Wang H, Ge Z, Zhu D and Bi Y: Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle. Int J Mol Med 40: 2000-2010, 2017.
APA
Tang, W., Tang, S., Wang, H., Ge, Z., Zhu, D., & Bi, Y. (2017). Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle. International Journal of Molecular Medicine, 40, 2000-2010. https://doi.org/10.3892/ijmm.2017.3169
MLA
Tang, W., Tang, S., Wang, H., Ge, Z., Zhu, D., Bi, Y."Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle". International Journal of Molecular Medicine 40.6 (2017): 2000-2010.
Chicago
Tang, W., Tang, S., Wang, H., Ge, Z., Zhu, D., Bi, Y."Insulin restores UCP3 activity and decreases energy surfeit to alleviate lipotoxicity in skeletal muscle". International Journal of Molecular Medicine 40, no. 6 (2017): 2000-2010. https://doi.org/10.3892/ijmm.2017.3169
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