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Research Article

The diabetes medication canagliflozin promotes mitochondrial remodelling of adipocyte via the AMPK-Sirt1-Pgc-1α signalling pathway

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Pages 484-494 | Received 25 Feb 2020, Accepted 22 Jul 2020, Published online: 23 Aug 2020

References

  • Wai T, Langer T. Mitochondrial dynamics and metabolic regulation. Trends Endocrinol Metab. 2016;27(2):105–117.
  • Deveaud C, Beauvoit B, Salin B, et al. Regional differences in oxidative capacity of rat white adipose tissue are linked to the mitochondrial content of mature adipocytes. Mol Cell Biochem. 2004;267:157–166.
  • Rosen ED, Spiegelman BM. Adipocytes as regulators of energy balance and glucose homeostasis. Nature. 2006;444:847–853.
  • Patti ME, Corvera S. The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr Rev. 2010;31:364–395.
  • Wu Z, Puigserver P, Andersson U, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98:115–124.
  • Besseiche A, Riveline JP, Gautier JF, et al. Metabolic roles of PGC-1alpha and its implications for type 2 diabetes. Diabetes Metab. 2015;41:347–357.
  • Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005;1:361–370.
  • Kusminski CM, Scherer PE. Mitochondrial dysfunction in white adipose tissue. Trends Endocrinol Metab. 2012;23:435–443.
  • Yamauchi T, Kamon J, Minokoshi Y, et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med. 2002;8:1288–1295.
  • Romere C, Duerrschmid C, Bournat J, et al. Asprosin, a fasting-induced glucogenic protein hormone. Cell. 2016;165:566–579.
  • Choo HJ, Kim JH, Kwon OB, et al. Mitochondria are impaired in the adipocytes of type 2 diabetic mice. Diabetologia. 2006;49:784–791.
  • Gao CL, Zhu C, Zhao YP, et al. Mitochondrial dysfunction is induced by high levels of glucose and free fatty acids in 3T3-L1 adipocytes. Mol Cell Endocrinol. 2010;320:25–33.
  • de Mello AH, Costa AB, Jdg E, et al. Mitochondrial dysfunction in obesity. Life Sci. 2017;192:26–32.
  • Ferrannini E. Sodium-glucose co-transporters and their inhibition: clinical physiology. Cell Metab. 2017;26:27–38.
  • Haas B, Eckstein N, Pfeifer V, et al. Efficacy, safety and regulatory status of SGLT2 inhibitors: focus on canagliflozin. Nutr Diabetes. 2014;4:e143.
  • Naznin F, Sakoda H, Okada T, et al. Canagliflozin, a sodium glucose cotransporter 2 inhibitor, attenuates obesity-induced inflammation in the nodose ganglion, hypothalamus, and skeletal muscle of mice. Eur J Pharmacol. 2017;794:37–44.
  • Cefalu WT, Leiter LA, Yoon KH, et al. Efficacy and safety of canagliflozin versus glimepiride in patients with type 2 diabetes inadequately controlled with metformin (CANTATA-SU): 52 week results from a randomised, double-blind, phase 3 non-inferiority trial. Lancet. 2013;382:941–950.
  • Hollander P, Bays HE, Rosenstock J, et al. Coadministration of canagliflozin and phentermine for weight management in overweight and obese individuals without diabetes: a randomized clinical trial. Diabetes Care. 2017;40:632–639.
  • Gallo LA, Wright EM, Vallon V. Probing SGLT2 as a therapeutic target for diabetes: basic physiology and consequences. Diab Vasc Dis Res. 2015;12:78–89.
  • Merovci A, Solis-Herrera C, Daniele G, et al. Dapagliflozin improves muscle insulin sensitivity but enhances endogenous glucose production. J Clin Invest. 2014;124:509–514.
  • Xu L, Nagata N, Nagashimada M, et al. SGLT2 inhibition by empagliflozin promotes fat utilization and browning and attenuates inflammation and insulin resistance by polarizing M2 macrophages in diet-induced obese mice. EBioMedicine. 2017;20:137–149.
  • Hawley SA, Ford RJ, Smith BK, et al. The Na+/Glucose cotransporter inhibitor canagliflozin activates AMPK by inhibiting mitochondrial function and increasing cellular AMP levels. Diabetes. 2016;65:2784–2794.
  • Villani LA, Smith BK, Marcinko K, et al. The diabetes medication canagliflozin reduces cancer cell proliferation by inhibiting mitochondrial complex-I supported respiration. Mol Metab. 2016;5:1048–1056.
  • Yao L, Cui X, Chen Q, et al. Cold-inducible SIRT6 regulates thermogenesis of brown and beige fat. Cell Rep. 2017;20:641–654.
  • Pu S, Ren L, Liu Q, et al. Loss of 5-lipoxygenase activity protects mice against paracetamol-induced liver toxicity. Br J Pharmacol. 2016;173:66–76.
  • Schreiber SN, Emter R, Hock MB, et al. The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc Natl Acad Sci U S A. 2004;101:6472–6477.
  • Tahara A, Takasu T, Yokono M, et al. Characterization and comparison of sodium-glucose cotransporter 2 inhibitors in pharmacokinetics, pharmacodynamics, and pharmacologic effects. J Pharmacol Sci. 2016;130:159–169.
  • Scarpulla RC, Vega RB, Kelly DP. Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab. 2012;23:459–466.
  • Fan W, Evans R. PPARs and ERRs: molecular mediators of mitochondrial metabolism. Curr Opin Cell Biol. 2015;33:49–54.
  • Lowell BB, Shulman GI. Mitochondrial dysfunction and type 2 diabetes. Science. 2005;307:384–387.
  • Ikeda K, Maretich P, Kajimura S. The common and distinct features of brown and beige adipocytes. Trends Endocrinol Metab. 2018;29:191–200.
  • Harms M, Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med. 2013;19:1252–1263.
  • Pisani DF, Barquissau V, Chambard JC, et al. Mitochondrial fission is associated with UCP1 activity in human brite/beige adipocytes. Mol Metab. 2018;7:35–44.
  • Barquissau V, Beuzelin D, Pisani DF, et al. White-to-brite conversion in human adipocytes promotes metabolic reprogramming towards fatty acid anabolic and catabolic pathways. Mol Metab. 2016;5:352–365.
  • Butow RA, Bahassi EM. Adaptive thermogenesis: orchestrating mitochondrial biogenesis. Curr Biol. 1999;9:R767–R769.
  • Nakano J, Gin AC, Ishii T. Effect of age on norepinephrine-, ACTH-, theophylline- and dibutryl cyclic AMP-induced lipolysis in isolated rat fat cells. J Gerontol. 1971;26:8–12.
  • Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta. 2011;1813:1269–1278.
  • Forst T, Guthrie R, Goldenberg R, et al. Efficacy and safety of canagliflozin over 52 weeks in patients with type 2 diabetes on background metformin and pioglitazone. Diabetes Obes Metab. 2014;16:467–477.
  • Zaccardi F, Webb DR, Htike ZZ, et al. Efficacy and safety of sodium-glucose co-transporter-2 inhibitors in type 2 diabetes mellitus: systematic review and network meta-analysis. Diabetes Obes Metab. 2016;18:783–794.
  • Wikstrom JD, Mahdaviani K, Liesa M, et al. Hormone-induced mitochondrial fission is utilized by brown adipocytes as an amplification pathway for energy expenditure. Embo J. 2014;33:418–436.
  • Altshuler-Keylin S, Shinoda K, Hasegawa Y, et al. Beige adipocyte maintenance is regulated by autophagy-induced mitochondrial clearance. Cell Metab. 2016;24:402–419.
  • Gospodarska E, Nowialis P, Kozak LP. Mitochondrial turnover: a phenotype distinguishing brown adipocytes from interscapular brown adipose tissue and white adipose tissue. J Biol Chem. 2015;290:8243–8255.
  • Ferrannini E, Muscelli E, Frascerra S, et al. Metabolic response to sodium-glucose cotransporter 2 inhibition in type 2 diabetic patients. J Clin Invest. 2014;124:499–508.
  • Ferrannini E, Baldi S, Frascerra S, et al. Shift to fatty substrate utilization in response to sodium-glucose cotransporter 2 inhibition in subjects without diabetes and patients with type 2 diabetes. Diabetes. 2016;65:1190–1195.
  • Devineni D, Vaccaro N, Polidori D, et al. Single- and multiple-dose pharmacokinetics and pharmacodynamics of canagliflozin, a selective inhibitor of sodium glucose co-transporter 2, in healthy participants. Int J Clin Pharmacol Ther. 2015;53:129–138.
  • Wan Z, Root-McCaig J, Castellani L, et al. Evidence for the role of AMPK in regulating PGC-1 alpha expression and mitochondrial proteins in mouse epididymal adipose tissue. Obesity. 2014;22:730–738.
  • Brandauer J, Vienberg SG, Andersen MA, et al. AMP-activated protein kinase regulates nicotinamide phosphoribosyl transferase expression in skeletal muscle. J Physiol. 2013;591:5207–5220.
  • Ruderman NB, Xu XJ, Nelson L, et al. AMPK and SIRT1: a long-standing partnership? Am J Physiol Endocrinol Metab. 2010;298:E751–E760.
  • Yu SB, Pekkurnaz G. Mechanisms orchestrating mitochondrial dynamics for energy homeostasis. J Mol Biol. 2018;430:3922–3941.