Apelin treatment increases complete fatty acid oxidation, mitochondrial oxidative capacity, and biogenesis in muscle of insulin-resistant mice

Diabetes

Volumn 61, Issue 2, 2012, Pages 310-320

  Attané, Camille ^a   Foussal, Camille ^a   Le Gonidec, Sophie ^a   Benani, Alexandre ^b   Daviaud, Danièle ^a   Wanecq, Estelle ^a   Guzmán Ruiz, Rocío ^c   Dray, Cédric ^a   Bezaire, Veronic ^a   Rancoule, Chloé ^a   Kuba, Keiji ^d   Ruiz Gayo, Mariano ^c   Levade, Thierry ^a   Penninger, Josef ^e   Burcelin, Rémy ^a   Pénicaud, Luc ^b   Valet, Philippe ^a   Castan Laurell, Isabelle ^a  

^a University Hospital of Toulouse   (France)

^b CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

^c UNIVERSIDAD SAN PABLO CEU   (Spain)

^d AKITA UNIVERSITY   (Japan)

^e INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLCARNITINE; APELIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOGENESIS; BODY FAT; CALORIMETRY; CHRONIC DRUG ADMINISTRATION; CITRIC ACID CYCLE; CONTROLLED STUDY; FATTY ACID OXIDATION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HORMONE ACTION; HYPERINSULINEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID METABOLISM; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE METABOLISM; NONHUMAN; OBESITY; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; SKELETAL MUSCLE; SOLEUS MUSCLE; TISSUE SPECIFICITY; TRIACYLGLYCEROL BLOOD LEVEL;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIET, HIGH-FAT; ENERGY METABOLISM; FATTY ACIDS; INSULIN RESISTANCE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID METABOLISM; MICE; MICE, INBRED C57BL; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OXIDATION-REDUCTION;

EID: 84856527230     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0100     Document Type: Article

References (39)

1. Boucher J, Masri B, Daviaud D, et al. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology 2005;146:1764-1771 (Pubitemid 40396885)
2. Tatemoto K, Hosoya M, Habata Y, et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun 1998;251:471-476 (Pubitemid 28505047)
3. Carpéné C, Dray C, Attané C, et al. Expanding role for the apelin/APJ system in physiopathology. J Physiol Biochem 2007;63:359-373
4. Dray C, Knauf C, Daviaud D, et al. Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab 2008;8:437-445
5. Yue P, Jin H, Aillaud M, et al. Apelin is necessary for the maintenance of insulin sensitivity. Am J Physiol Endocrinol Metab 2010;298:E59-E67
6. Dray C, Debard C, Jager J, et al. Apelin and APJ regulation in adipose tissue and skeletal muscle of type 2 diabetic mice and humans. Am J Physiol Endocrinol Metab 2010;298:E1161-E1169
7. Higuchi K, Masaki T, Gotoh K, et al. Apelin, an APJ receptor ligand, regulates body adiposity and favors the messenger ribonucleic acid expression of uncoupling proteins in mice. Endocrinology 2007;148:2690-2697 (Pubitemid 46984786)
8. Yue P, Jin H, Xu S, et al. Apelin decreases lipolysis via G(q), G(i), and AMPK-dependent mechanisms. Endocrinology 2011;152:59-68
9. Attané C, Daviaud D, Dray C, et al. Apelin stimulates glucose uptake but not lipolysis in human adipose tissue ex vivo. J Mol Endocrinol 2011;46: 21-28
10. Kuba K, Zhang L, Imai Y, et al. Impaired heart contractility in Apelin gene-deficient mice associated with aging and pressure overload [corrected in: Circ Res 2008;102:e36]. Circ Res 2007;101:e32-e42 (Pubitemid 47267711)
11. Lee DK, Saldivia VR, Nguyen T, Cheng R, George SR, O'Dowd BF. Modification of the terminal residue of apelin-13 antagonizes its hypotensive action. Endocrinology 2005;146:231-236 (Pubitemid 40051744)
12. Dyck DJ, Miskovic D, Code L, Luiken JJ, Bonen A. Endurance training increases FFA oxidation and reduces triacylglycerol utilization in contracting rat soleus. Am J Physiol Endocrinol Metab 2000;278:E778-E785 (Pubitemid 30366393)
13. Benani A, Barquissau V, Carneiro L, et al. Method for functional study of mitochondria in rat hypothalamus. J Neurosci Methods 2009;178:301-307
14. Knauf C, Cani PD, Ait-Belgnaoui A, et al. Brain glucagon-like peptide 1 signaling controls the onset of high-fat diet-induced insulin resistance and reduces energy expenditure. Endocrinology 2008;149:4768-4777
15. Bonnard C, Durand A, Peyrol S, et al. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 2008;118:789-800 (Pubitemid 351206566)
16. Bezaire V, Bruce CR, Heigenhauser GJ, et al. Identification of fatty acid translocase on human skeletal muscle mitochondrial membranes: essential role in fatty acid oxidation. Am J Physiol Endocrinol Metab 2006;290: E509-E515 (Pubitemid 43671698)
17. Chace DH, Hillman SL, Van Hove JL, Naylor EW. Rapid diagnosis of MCAD deficiency: quantitative analysis of octanoylcarnitine and other acylcarnitines in newborn blood spots by tandem mass spectrometry. Clin Chem 1997;43: 2106-2113 (Pubitemid 27497809)
18. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911-917
19. Barrans A, Collet X, Barbaras R, et al. Hepatic lipase induces the formation of pre-beta 1 high density lipoprotein (HDL) from triacylglycerol-rich HDL2. A study comparing liver perfusion to in vitro incubation with lipases. J Biol Chem 1994;269:11572-11577
20. McGarry JD, Stark MJ, Foster DW. Hepatic malonyl-CoA levels of fed, fasted and diabetic rats as measured using a simple radioisotopic assay. J Biol Chem 1978;253:8291-8293 (Pubitemid 9073730)
21. Iglesias-Osma MC, Bour S, Garcia-Barrado MJ, et al. Methylamine but not mafenide mimics insulin-like activity of the semicarbazide-sensitive amine oxidase-substrate benzylamine on glucose tolerance and on human adipocyte metabolism. Pharmacol Res 2005;52:475-484 (Pubitemid 41562233)
22. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 2005;1:361-370 (Pubitemid 43960626)
23. Patti ME, Corvera S. The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr Rev 2010;31:364-395
24. 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
25. Reznick RM, Shulman GI. The role of AMP-activated protein kinase in mitochondrial biogenesis. J Physiol 2006;574:33-39 (Pubitemid 43905794)
26. Koves TR, Ussher JR, Noland RC, et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 2008;7:45-56
27. Mihalik SJ, Goodpaster BH, Kelley DE, 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
28. Morino K, Petersen KF, Shulman GI. Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 2006;55(Suppl. 2):S9-S15 (Pubitemid 44927027)
29. Turner N, Heilbronn LK. Is mitochondrial dysfunction a cause of insulin resistance? Trends Endocrinol Metab 2008;19:324-330
30. Summermatter S, Troxler H, Santos G, Handschin C. Coordinated balancing of muscle oxidative metabolism through PGC-1α increases metabolic flexibility and preserves insulin sensitivity. Biochem Biophys Res Commun 2011;408:180-185
31. Koves TR, Li P, An J, et al. Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J Biol Chem 2005;280:33588-33598 (Pubitemid 41397160)
32. Bruce CR, Kriketos AD, Cooney GJ, Hawley JA. Disassociation of muscle triglyceride content and insulin sensitivity after exercise training in patients with Type 2 diabetes. Diabetologia 2004;47:23-30 (Pubitemid 38141936)
33. Kim JA, Wei Y, Sowers JR. Role of mitochondrial dysfunction in insulin resistance. Circ Res 2008;102:401-414 (Pubitemid 351651099)
34. Muoio DM, Koves TR. Skeletal muscle adaptation to fatty acid depends on coordinated actions of the PPARs and PGC1 alpha: implications for metabolic disease. Appl Physiol Nutr Metab 2007;32:874-883
35. Mootha VK, Lindgren CM, Eriksson KF, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003;34:267-273 (Pubitemid 36792858)
36. Patti ME, Butte AJ, Crunkhorn S, et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A 2003;100:8466-8471 (Pubitemid 36842568)
37. Frier BC, Williams DB, Wright DC. The effects of apelin treatment on skeletal muscle mitochondrial content. Am J Physiol Regul Integr Comp Physiol 2009;297:R1761-R1768
38. Yamamoto T, Habata Y, Matsumoto Y, et al. Apelin-transgenic mice exhibit a resistance against diet-induced obesity by increasing vascular mass and mitochondrial biogenesis in skeletal muscle. Biochim Biophys Acta 2011; 1810:853-862
39. Gaidhu MP, Fediuc S, Ceddia RB. 5-Aminoimidazole-4-carboxamide-1- beta-D-ribofuranoside-induced AMP-activated protein kinase phosphorylation inhibits basal and insulin-stimulated glucose uptake, lipid synthesis, and fatty acid oxidation in isolated rat adipocytes. J Biol Chem 2006;281: 25956-25964 (Pubitemid 44401801)