ANT1-mediated fatty acid-induced uncoupling as a target for improving myocellular insulin sensitivity

Diabetologia

Volumn 59, Issue 5, 2016, Pages 1030-1039

  Sparks, Lauren M ^a,b   Gemmink, Anne ^a   Phielix, Esther ^a   Bosma, Madeleen ^a,c   Schaart, Gert ^a   Moonen Kornips, Esther ^a   Jörgensen, Johanna A ^a   Nascimento, Emmani B M ^a   Hesselink, Matthijs K C ^a   Schrauwen, Patrick ^a   Hoeks, Joris ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b FLORIDA HOSPITAL   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

ANT1; Fatty acid induced uncoupling; Skeletal muscle insulin sensitivity

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENINE NUCLEOTIDE TRANSLOCASE 1; FATTY ACID; GLUCOSE; GLUTAMIC ACID; INSULIN; LIPID; MESSENGER RNA; OLEIC ACID; OLIGOMYCIN; PALMITIC ACID; PYRUVIC ACID; SMALL INTERFERING RNA; SUCCINIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BODY MASS; COMPARATIVE STUDY; CONTROLLED STUDY; ENDURANCE TRAINING; GENE SILENCING; GENETIC TRANSFECTION; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; HUMAN; HUMAN EXPERIMENT; INSULIN RESISTANCE; INSULIN RESPONSE; INSULIN SENSITIVITY; MALE; MUSCLE MITOCHONDRION; MYOTUBE; NONHUMAN; NORMAL HUMAN; OBSERVATIONAL STUDY; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SKELETAL MUSCLE; ANIMAL; DRUG EFFECTS; GENETICS; IN VITRO STUDY; METABOLISM; SKELETAL MUSCLE CELL; ZUCKER RAT;

ADENINE NUCLEOTIDE TRANSLOCATOR 1; ANIMALS; FATTY ACIDS; HUMANS; IN VITRO TECHNIQUES; INSULIN; INSULIN RESISTANCE; MALE; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL ADP, ATP TRANSLOCASES; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; OLEIC ACID; PALMITIC ACID; RATS; RATS, ZUCKER;

EID: 84958747163     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-016-3885-8     Document Type: Article

References (40)

1. Meex RC, Schrauwen-Hinderling VB, Moonen-Kornips E et al (2010) Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity. Diabetes 59:572–579
2. Phielix E, Meex R, Moonen-Kornips E, Hesselink MK, Schrauwen P (2010) Exercise training increases mitochondrial content and ex vivo mitochondrial function similarly in patients with type 2 diabetes and in control individuals. Diabetologia 53:1714–1721
3. Nielsen J, Mogensen M, Vind BF et al (2010) Increased subsarcolemmal lipids in type 2 diabetes: effect of training on localization of lipids, mitochondria, and glycogen in sedentary human skeletal muscle. Am J Physiol Endocrinol Metab 298:E706–713
4. Phielix E, Meex R, Ouwens DM et al (2012) High oxidative capacity due to chronic exercise training attenuates lipid-induced insulin resistance. Diabetes 61:2472–2478
5. Befroy DE, Petersen KF, Dufour S, Mason GF, Rothman DL, Shulman GI (2008) Increased substrate oxidation and mitochondrial uncoupling in skeletal muscle of endurance-trained individuals. Proc Natl Acad Sci U S A 105:16701–16706
6. Gates AC, Bernal-Mizrachi C, Chinault SL et al (2007) Respiratory uncoupling in skeletal muscle delays death and diminishes age-related disease. Cell Metab 6:497–505
7. Choi CS, Fillmore JJ, Kim JK et al (2007) Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J Clin Invest 117:1995–2003
8. Hesselink MK, Keizer HA, Borghouts LB et al (2001) Protein expression of UCP3 differs between human type 1, type 2a, and type 2b fibers. FASEB J 15:1071–1073
9. Russell AP, Wadley G, Hesselink MK et al (2003) UCP3 protein expression is lower in type I, IIa and IIx muscle fiber types of endurance-trained compared to untrained subjects. Pflugers Arch 445:563–569
10. Fernstrom M, Tonkonogi M, Sahlin K (2004) Effects of acute and chronic endurance exercise on mitochondrial uncoupling in human skeletal muscle. J Physiol 554:755–763
11. Nabben M, Shabalina IG, Moonen-Kornips E et al (2011) Uncoupled respiration, ROS production, acute lipotoxicity and oxidative damage in isolated skeletal muscle mitochondria from UCP3-ablated mice. Biochim Biophys Acta 1807:1095–1105
12. Shabalina IG, Hoeks J, Kramarova TV, Schrauwen P, Cannon B, Nedergaard J (2010) Cold tolerance of UCP1-ablated mice: a skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects. Biochim Biophys Acta 1797:968–980
13. Skulachev VP (1991) Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation. FEBS Lett 294:158–162
14. Andreyev A, Bondareva TO, Dedukhova VI et al (1989) The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria. Eur J Biochem 182:585–592
15. Goodpaster BH, He J, Watkins S, Kelley DE (2001) Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 86:5755–5761
16. Decombaz J, Schmitt B, Ith M et al (2001) Postexercise fat intake repletes intramyocellular lipids but no faster in trained than in sedentary subjects. Am J Physiol Regul Integr Comp Physiol 281:R760–769
17. DeFronzo RA, Tobin JD, Andres R (1979) Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol 237:E214–223
18. Bergstrom J (1975) Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35:609–616
19. Phielix E, Schrauwen-Hinderling VB, Mensink M et al (2008) Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes 57:2943–2949
20. Daubas P, Klarsfeld A, Garner I, Pinset C, Cox R, Buckingham M (1988) Functional activity of the two promoters of the myosin alkali light chain gene in primary muscle cell cultures: comparison with other muscle gene promoters and other culture systems. Nucleic Acids Res 16:1251–1271
21. Hoeks J, van Herpen NA, Mensink M et al (2010) Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as consequence rather than cause of human insulin resistance. Diabetes 59:2117–2125
22. Udenfriend S, Stein S, Bohlen P, Dairman W, Leimgruber W, Weigele M (1972) Fluorescamine: a reagent for assay of amino acids, peptides, proteins, and primary amines in the picomole range. Science 178:871–872
23. Hommelberg PP, Plat J, Sparks LM et al (2011) Palmitate-induced skeletal muscle insulin resistance does not require NF-kappaB activation. Cell Mol Life Sci 68:1215–1225
24. Richieri GV, Anel A, Kleinfeld AM (1993) Interactions of long-chain fatty acids and albumin: determination of free fatty acid levels using the fluorescent probe ADIFAB. Biochemistry 32:7574–7580
25. Nabben M, Hoeks J, Briede JJ et al (2008) The effect of UCP3 overexpression on mitochondrial ROS production in skeletal muscle of young versus aged mice. FEBS Lett 582:4147–4152
26. Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1:581–585
27. Sparks LM, Moro C, Ukropcova B et al (2011) Remodeling lipid metabolism and improving insulin responsiveness in human primary myotubes. PLoS One 6:e21068
28. Sparks LM, Xie H, Koza RA et al (2005) A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54:1926–1933
29. Hoeks J, Briede JJ, de Vogel J et al (2008) Mitochondrial function, content and ROS production in rat skeletal muscle: effect of high-fat feeding. FEBS Lett 582:510–516
30. Paglialunga S, van Bree B, Bosma M et al (2012) Targeting of mitochondrial reactive oxygen species production does not avert lipid-induced insulin resistance in muscle tissue from mice. Diabetologia 55:2759–2768
31. Brand MD, Pakay JL, Ocloo A et al (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392:353–362
32. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359
33. Bal NC, Maurya SK, Sopariwala DH et al (2012) Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nat Med 18:1575–1579
34. Chavez AO, Kamath S, Jani R et al (2010) Effect of short-term free fatty acids elevation on mitochondrial function in skeletal muscle of healthy individuals. J Clin Endocrinol Metab 95:422–429
35. Mielke C, Lefort N, McLean CG et al (2014) Adenine nucleotide translocase is acetylated in vivo in human muscle: modeling predicts a decreased ADP affinity and altered control of oxidative phosphorylation. Biochemistry 53:3817–3829
36. Yin H, Stahl JS, Andrade FH et al (2005) Eliminating the Ant1 isoform produces a mouse with CPEO pathology but normal ocular motility. Invest Ophthalmol Vis Sci 46:4555–4562
37. Houstis N, Rosen ED, Lander ES (2006) Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440:944–948
38. Anderson EJ, Lustig ME, Boyle KE et al (2009) Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119:573–581
39. Lefort N, Glancy B, Bowen B et al (2010) Increased reactive oxygen species production and lower abundance of complex I subunits and carnitine palmitoyltransferase 1B protein despite normal mitochondrial respiration in insulin-resistant human skeletal muscle. Diabetes 59:2444–2452
40. Taddeo EP, Laker RC, Breen DS et al (2014) Opening of the mitochondrial permeability transition pore links mitochondrial dysfunction to insulin resistance in skeletal muscle. Mol Metab 3:124–134