Sirtuin3 dysfunction is the key determinant of skeletal muscle insulin resistance by angiotensin II

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Macconi, Daniela ^a   Perico, Luca ^a   Longaretti, Lorena ^a   Morigi, Marina ^a   Cassis, Paola ^a   Buelli, Simona ^a   Perico, Norberto ^a   Remuzzi, Giuseppe ^a,b   Benigni, Ariela ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b Azienda Ospedaliera Papa Giovanni XXIII   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; GLUCOSE TRANSPORTER 4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LEVACECARNINE; MANGANESE SUPEROXIDE DISMUTASE; MYC PROTEIN; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; REACTIVE OXYGEN METABOLITE; SIRTUIN 3; SMALL INTERFERING RNA; SUPEROXIDE; ACETYLCARNITINE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME ACTIVITY; GLUCOSE TRANSPORT; IN VITRO STUDY; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MUSCLE CELL; MUSCLE METABOLISM; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; CELL LINE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

RATTUS;

ACETYLCARNITINE; ANGIOTENSIN II; ANIMALS; CELL LINE; INSULIN RESISTANCE; MITOCHONDRIA; MUSCLE, SKELETAL; RATS; REACTIVE OXYGEN SPECIES; SIRTUIN 3;

EID: 84930620549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127172     Document Type: Article

References (59)

1. Gallagher EJ, Leroith D, Karnieli E. The metabolic syndrome-from insulin resistance to obesity and diabetes. Med Clin North Am. 2011; 95: 855-873. doi: 10.1016/j.mcna.2011.06.001 PMID: 21855696
2. Karalliedde J, Gnudi L. Diabetes mellitus, a complex and heterogeneous disease, and the role of insulin resistance as a determinant of diabetic kidney disease. Nephrol Dial Transplant. 2014;
3. Grundy SM. Metabolic syndrome pandemic. Arterioscler Thromb Vasc Biol. 2008; 28: 629-636. doi: 10.1161/ATVBAHA.107.151092 PMID: 18174459
4. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet. 2005; 365: 1415-1428. PMID: 15836891
5. Katz LD, Glickman MG, Rapoport S, Ferrannini E, DeFronzo RA. Splanchnic and peripheral disposal of oral glucose in man. Diabetes. 1983; 32: 675-679. PMID: 6862113
6. Baron AD, Brechtel G, Wallace P, Edelman SV. Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. Am J Physiol. 1988; 255: E769-774. PMID: 3059816
7. Petersen KF, Dufour S, Savage DB, Bilz S, Solomon G, et al. The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci U S A. 2007; 104: 12587-12594. PMID: 17640906
8. DeFronzo RA, Tripathy D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care. 2009; 32 Suppl 2: S157-163. doi: 10.2337/dc09-S302 PMID: 19875544
9. Samuel VT, Shulman GI. Mechanisms for insulin resistance: common threads and missing links. Cell. 2012; 148: 852-871. doi: 10.1016/j.cell.2012.02.017 PMID: 22385956
10. Underwood PC, Adler GK. The renin angiotensin aldosterone system and insulin resistance in humans. Curr Hypertens Rep. 2013; 15: 59-70. doi: 10.1007/s11906-012-0323-2 PMID: 23242734
11. Olivares-Reyes JA, Arellano-Plancarte A, Castillo-Hernandez JR. Angiotensin II and the development of insulin resistance: implications for diabetes. Mol Cell Endocrinol. 2009; 302: 128-139. doi: 10.1016/j.mce.2008.12.011 PMID: 19150387
12. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem. 2006; 281: 35137-35146. PMID: 16982630
13. Wei Y, Sowers JR, Clark SE, Li W, Ferrario CM, et al. Angiotensin II-induced skeletal muscle insulin resistance mediated by NF-kappaB activation via NADPH oxidase. Am J Physiol Endocrinol Metab. 2008; 294: E345-351. PMID: 18073321
14. Diamond-Stanic MK, Henriksen EJ. Direct inhibition by angiotensin II of insulin-dependent glucose transport activity in mammalian skeletal muscle involves a ROS-dependent mechanism. Arch Physiol Biochem. 2010; 116: 88-95. doi: 10.3109/13813451003758703 PMID: 20384568
15. Kim JA, Wei Y, Sowers JR. Role of mitochondrial dysfunction in insulin resistance. Circ Res. 2008; 102: 401-414. doi: 10.1161/CIRCRESAHA.107.165472 PMID: 18309108
16. Martin SD, McGee SL. The role of mitochondria in the aetiology of insulin resistance and type 2 diabetes. Biochim Biophys Acta. 2014; 1840: 1303-1312. doi: 10.1016/j.bbagen.2013.09.019 PMID: 24060748
17. 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. doi: 10.1016/j.cmet.2007.10.013 PMID: 18177724
18. James AM, Collins Y, Logan A, Murphy MP. Mitochondrial oxidative stress and the metabolic syndrome. Trends Endocrinol Metab. 2012; 23: 429-434. doi: 10.1016/j.tem.2012.06.008 PMID: 22831852
19. Mitsuishi M, Miyashita K, Muraki A, Itoh H. Angiotensin II reduces mitochondrial content in skeletal muscle and affects glycemic control. Diabetes. 2009; 58: 710-717. doi: 10.2337/db08-0949 PMID: 19074984
20. Bell EL, Guarente L. The SirT3 divining rod points to oxidative stress. Mol Cell. 2011; 42: 561-568. doi: 10.1016/j.molcel.2011.05.008 PMID: 21658599
21. Benigni A, Corna D, Zoja C, Sonzogni A, Latini R, et al. Disruption of the Ang II type 1 receptor promotes longevity in mice. J Clin Invest. 2009; 119: 524-530. doi: 10.1172/JCI36703 PMID: 19197138
22. Rebouche CJ. Kinetics, pharmacokinetics, and regulation of L-carnitine and acetyl-L-carnitine metabolism. Ann N Y Acad Sci. 2004; 1033: 30-41. PMID: 15591001
23. Ruggenenti P, Cattaneo D, Loriga G, Ledda F, Motterlini N, et al. Ameliorating hypertension and insulin resistance in subjects at increased cardiovascular risk: effects of acetyl-L-carnitine therapy. Hypertension. 2009; 54: 567-574. doi: 10.1161/HYPERTENSIONAHA.109.132522 PMID: 19620516
24. Wang Q, Khayat Z, Kishi K, Ebina Y, Klip A. GLUT4 translocation by insulin in intact muscle cells: detection by a fast and quantitative assay. FEBS Lett. 1998; 427: 193-197. PMID: 9607310
25. Ueyama A, Yaworsky KL, Wang Q, Ebina Y, Klip A. GLUT-4myc ectopic expression in L6 myoblasts generates a GLUT-4-specific pool conferring insulin sensitivity. Am J Physiol. 1999; 277: E572-578. PMID: 10484371
26. Yonemitsu S, Nishimura H, Shintani M, Inoue R, Yamamoto Y, et al. Troglitazone induces GLUT4 translocation in L6 myotubes. Diabetes. 2001; 50: 1093-1101. PMID: 11334413
27. Mitsumoto Y, Klip A. Development regulation of the subcellular distribution and glycosylation of GLUT1 and GLUT4 glucose transporters during myogenesis of L6 muscle cells. J Biol Chem. 1992; 267: 4957-4962. PMID: 1311324
28. Hardie DG. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol. 2007; 8: 774-785. PMID: 17712357
29. Witczak CA, Sharoff CG, Goodyear LJ. AMP-activated protein kinase in skeletal muscle: from structure and localization to its role as a master regulator of cellular metabolism. Cell Mol Life Sci. 2008; 65: 3737-3755. doi: 10.1007/s00018-008-8244-6 PMID: 18810325
30. Decleves AE, Sharma K, Satriano J. Beneficial effects of AMP-activated protein kinase agonists in kidney ischemia-reperfusion: autophagy and cellular stress markers. Nephron Exp Nephrol. 2014;
31. Fryer LG, Parbu-Patel A, Carling D. Protein kinase inhibitors block the stimulation of the AMP-activated protein kinase by 5-amino-4-imidazolecarboxamide riboside. FEBS Lett. 2002; 531: 189-192. PMID: 12417310
32. Costford SR, Bajpeyi S, Pasarica M, Albarado DC, Thomas SC, et al. Skeletal muscle NAMPT is induced by exercise in humans. Am J Physiol Endocrinol Metab. 2010; 298: E117-126. doi: 10.1152/ajpendo.00318.2009 PMID: 19887595
33. Brandauer J, Vienberg SG, Andersen MA, Ringholm S, Risis S, et al. AMP-activated protein kinase regulates nicotinamide phosphoribosyl transferase expression in skeletal muscle. J Physiol. 2013; 591: 5207-5220. doi: 10.1113/jphysiol.2013.259515 PMID: 23918774
34. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006; 440: 944-948. PMID: 16612386
35. Hoehn KL, Salmon AB, Hohnen-Behrens C, Turner N, Hoy AJ, et al. Insulin resistance is a cellular antioxidant defense mechanism. Proc Natl Acad Sci U S A. 2009; 106: 17787-17792. doi: 10.1073/pnas.0902380106 PMID: 19805130
36. Di Lisa F, Menabo R, Canton M, Barile M, Bernardi P. Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem. 2001; 276: 2571-2575. PMID: 11073947
37. Imai S. Nicotinamide phosphoribosyltransferase (Nampt): a link between NAD biology, metabolism, and diseases. Curr Pharm Des. 2009; 15: 20-28. PMID: 19149599
38. Pehmoller C, Treebak JT, Birk JB, Chen S, Mackintosh C, et al. Genetic disruption of AMPK signaling abolishes both contraction- and insulin-stimulated TBC1D1 phosphorylation and 14-3-3 binding in mouse skeletal muscle. Am J Physiol Endocrinol Metab. 2009; 297: E665-675. doi: 10.1152/ajpendo.00115.2009 PMID: 19531644
39. Fisher JS. Potential Role of the AMP-activated Protein Kinase in Regulation of Insulin Action. Cellscience. 2006; 2: 68-81. PMID: 18049717
40. Towler MC, Hardie DG. AMP-activated protein kinase in metabolic control and insulin signaling. Circ Res. 2007; 100: 328-341. PMID: 17307971
41. Ruderman NB, Carling D, Prentki M, Cacicedo JM. AMPK, insulin resistance, and the metabolic syndrome. J Clin Invest. 2013; 123: 2764-2772. doi: 10.1172/JCI67227 PMID: 23863634
42. Zhang BB, Zhou G, Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 2009; 9: 407-416. doi: 10.1016/j.cmet.2009.03.012 PMID: 19416711
43. Shinshi Y, Higashiura K, Yoshida D, Togashi N, Yoshida H, et al. Angiotensin II inhibits glucose uptake of skeletal muscle via the adenosine monophosphate-activated protein kinase pathway. J Am Soc Hypertens. 2007; 1: 251-255. doi: 10.1016/j.jash.2007.04.007 PMID: 20409857
44. Lastra G, Santos FR, Hooshmand P, Mugerfeld I, Aroor AR, et al. The Novel Angiotensin II Receptor Blocker Azilsartan Medoxomil Ameliorates Insulin Resistance Induced by Chronic Angiotensin II Treatment in Rat Skeletal Muscle. Cardiorenal Med. 2013; 3: 154-164. PMID: 23922555
45. Pillai VB, Sundaresan NR, Kim G, Gupta M, Rajamohan SB, et al. Exogenous NAD blocks cardiac hypertrophic response via activation of the SIRT3-LKB1-AMPK pathway. J Biol Chem. 2010; 285: 3133-3144. doi: 10.1074/jbc.M109.077271 PMID: 19940131
46. Palacios OM, Carmona JJ, Michan S, Chen KY, Manabe Y, et al. Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging (Albany NY). 2009; 1: 771-783. PMID: 20157566
47. Lin L, Chen K, Khalek WA, Ward JL 3rd, Yang H, et al. Regulation of skeletal muscle oxidative capacity and muscle mass by SIRT3. PLoS One. 2014; 9: e85636. doi: 10.1371/journal.pone.0085636 PMID: 24454908
48. Jing E, Emanuelli B, Hirschey MD, Boucher J, Lee KY, et al. Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc Natl Acad Sci U S A. 2011; 108: 14608-14613. doi: 10.1073/pnas.1111308108 PMID: 21873205
49. Dikalov S. Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med. 2011; 51: 1289-1301. doi: 10.1016/j.freeradbiomed.2011.06.033 PMID: 21777669
50. Zinkevich NS, Gutterman DD. ROS-induced ROS release in vascular biology: redox-redox signaling. Am J Physiol Heart Circ Physiol. 2011; 301: H647-653. doi: 10.1152/ajpheart.01271.2010 PMID: 21685266
51. Vajapey R, Rini D, Walston J, Abadir P. The impact of age-related dysregulation of the angiotensin system on mitochondrial redox balance. Front Physiol. 2014; 5: 439. doi: 10.3389/fphys.2014.00439 PMID: 25505418
52. Calabrese V, Colombrita C, Sultana R, Scapagnini G, Calvani M, et al. Redox modulation of heat shock protein expression by acetylcarnitine in aging brain: relationship to antioxidant status and mitochondrial function. Antioxid Redox Signal. 2006; 8: 404-416. PMID: 16677087
53. Liu J, Head E, Gharib AM, Yuan W, Ingersoll RT, et al. Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: partial reversal by feeding acetyl-L-carnitine and/or R- alpha-lipoic acid. Proc Natl Acad Sci U S A. 2002; 99: 2356-2361. PMID: 11854529
54. Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ. Vitagenes, cellular stress response, and acetylcarnitine: relevance to hormesis. Biofactors. 2009; 35: 146-160. doi: 10.1002/biof.22 PMID: 19449442
55. Rosca MG, Lemieux H, Hoppel CL. Mitochondria in the elderly: Is acetylcarnitine a rejuvenator? Adv Drug Deliv Rev. 2009; 61: 1332-1342. doi: 10.1016/j.addr.2009.06.009 PMID: 19720100
56. Zhang Z, Zhao M, Li Q, Zhao H, Wang J, et al. Acetyl-l-carnitine inhibits TNF-alpha-induced insulin resistance via AMPK pathway in rat skeletal muscle cells. FEBS Lett. 2009; 583: 470-474. doi: 10.1016/j.febslet.2008.12.053 PMID: 19121314
57. Cassano P, Sciancalepoe AG, Pesce V, Fluck M, Hoppeler H, et al. Acetyl-L-carnitine feeding to unloaded rats triggers in soleus muscle the coordinated expression of genes involved in mitochondrial biogenesis. Biochim Biophys Acta. 2006; 1757: 1421-1428. PMID: 16814248
58. Marcovina SM, Sirtori C, Peracino A, Gheorghiade M, Borum P, et al. Translating the basic knowledge of mitochondrial functions to metabolic therapy: role of L-carnitine. Transl Res. 2013; 161: 73-84. doi: 10.1016/j.trsl.2012.10.006 PMID: 23138103
59. Mingorance C, Duluc L, Chalopin M, Simard G, Ducluzeau PH, et al. Propionyl-L-carnitine corrects metabolic and cardiovascular alterations in diet-induced obese mice and improves liver respiratory chain activity. PLoS One. 2012; 7: e34268. doi: 10.1371/journal.pone.0034268 PMID: 22457831