Skeletal muscle triacylglycerol hydrolysis does not influence metabolic complications of obesity

Diabetes

Volumn 62, Issue 10, 2013, Pages 3350-3361

  Sitnick, Mitch T ^a   Basantani, Mahesh K ^a   Cai, Lingzhi ^a   Schoiswohl, Gabriele ^a   Yazbeck, Cynthia F ^a   Distefano, Giovanna ^a   Ritov, Vladimir ^a   DeLany, James P ^a   Schreiber, Renate ^b   Stolz, Donna B ^a   Gardner, Noah P ^c   Kienesberger, Petra C ^d   Pulinilkunnil, Thomas ^d   Zechner, Rudolf ^a   Goodpaster, Bret H ^a   Coen, Paul ^a,e   Kershaw, Erin E ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF GRAZ   (Austria)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^d DALHOUSIE UNIVERSITY   (Canada)

^e UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAT DROPLET; INSULIN; TRIACYLGLYCEROL; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CALORIC INTAKE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENERGY BALANCE; FAT MASS; FATTY ACID OXIDATION; FEMALE; GASTROCNEMIUS MUSCLE; GENE DELETION; GENE OVEREXPRESSION; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE TEST; HEART MUSCLE; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIPID DIET; LIPID HYDROLYSIS; LIPID STORAGE; LIPID TRANSPORT; LIPOLYSIS; METABOLIC DISORDER; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; MUSCLE MASS; NONHUMAN; OBESITY; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; ADIPOSE TISSUE; ANIMAL; ENERGY METABOLISM; HOMEOSTASIS; HYDROLYSIS; KNOCKOUT MOUSE; LIPID METABOLISM; METABOLISM; PHENOTYPE; PHOSPHORYLATION; PHYSIOLOGY; TRANSGENIC MOUSE;

ADIPOSE TISSUE; ANIMALS; DIET, HIGH-FAT; ENERGY METABOLISM; HOMEOSTASIS; HYDROLYSIS; INSULIN RESISTANCE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID METABOLISM; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE, SKELETAL; OBESITY; PHENOTYPE; PHOSPHORYLATION; TRIGLYCERIDES;

EID: 84888130465     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0500     Document Type: Article

References (50)

1. Schaffer JE. Lipotoxicity: when tissues overeat. Curr Opin Lipidol 2003;14: 281-287
2. Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 2001;86:5755-5761
3. Samuel VT, Shulman GI. Mechanisms for insulin resistance: common threads and missing links. Cell 2012;148:852-871
4. Cowart LA. Sphingolipids: players in the pathology of metabolic disease. Trends Endocrinol Metab 2009;20:34-42
5. Amati F. Revisiting the diacylglycerol-induced insulin resistance hypothesis. Obes Rev 2012;13(Suppl. 2):40-50
6. Bosma M, Kersten S, Hesselink MK, Schrauwen P. Re-evaluating lipotoxic triggers in skeletal muscle: relating intramyocellular lipid metabolism to insulin sensitivity. Prog Lipid Res 2012;51:36-49
7. Coen PM, Goodpaster BH. Role of intramyocelluar lipids in human health. Trends Endocrinol Metab 2012;23:391-398
8. van Loon LJ, Goodpaster BH. Increased intramuscular lipid storage in the insulin-resistant and endurance-trained state. Pflugers Arch 2006;451:606-616
9. Goodpaster BH. Mitochondrial deficiency is associated with insulin resistance. Diabetes 2013;62:1032-1035
10. Funai K, Semenkovich CF. Skeletal muscle lipid flux: running water carries no poison. Am J Physiol Endocrinol Metab 2011;301:E245-E251
11. Zhang L, Keung W, Samokhvalov V, Wang W, Lopaschuk GD. Role of fatty acid uptake and fatty acid beta-oxidation in mediating insulin resistance in heart and skeletal muscle. Biochim Biophys Acta 2010;1801:1-22
12. Holloszy JO. "Deficiency" of mitochondria in muscle does not cause insulin resistance. Diabetes 2013;62:1036-1040
13. Liu L, Zhang Y, Chen N, Shi X, Tsang B, Yu YH. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J Clin Invest 2007;117:1679-1689
14. Liu L, Shi X, Choi CS, et al. Paradoxical coupling of triglyceride synthesis and fatty acid oxidation in skeletal muscle overexpressing DGAT1. Diabetes 2009;58:2516-2524
15. Levin MC, Monetti M, Watt MJ, et al. Increased lipid accumulation and insulin resistance in transgenic mice expressing DGAT2 in glycolytic (type II) muscle. Am J Physiol Endocrinol Metab 2007;293:E1772-E1781
16. Haemmerle G, Lass A, Zimmermann R, et al. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 2006;312:734-737
17. Kienesberger PC, Lee D, Pulinilkunnil T, et al. Adipose triglyceride lipase deficiency causes tissue-specific changes in insulin signaling. J Biol Chem 2009;284:30218-30229
18. Hoy AJ, Bruce CR, Turpin SM, Morris AJ, Febbraio MA, Watt MJ. Adipose triglyceride lipase-null mice are resistant to high-fat diet-induced insulin resistance despite reduced energy expenditure and ectopic lipid accumulation. Endocrinology 2011;152:48-58
19. Huijsman E, van de Par C, Economou C, et al. Adipose triacylglycerol lipase deletion alters whole body energy metabolism and impairs exercise performance in mice. Am J Physiol Endocrinol Metab 2009;297:E505-E513
20. Kraemer FB, Shen WJ. Hormone-sensitive lipase knockouts. Nutr Metab (Lond) 2006;3:12
21. Haemmerle G, Moustafa T, Woelkart G, et al. ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-a and PGC-1. Nat Med 2011;17:1076-1085
22. Reid BN, Ables GP, Otlivanchik OA, et al. Hepatic overexpression of hormone-sensitive lipase and adipose triglyceride lipase promotes fatty acid oxidation, stimulates direct release of free fatty acids, and ameliorates steatosis. J Biol Chem 2008;283:13087-13099
23. Ahmadian M, Duncan RE, Varady KA, et al. Adipose overexpression of desnutrin promotes fatty acid use and attenuates diet-induced obesity. Diabetes 2009;58:855-866
24. Li S, Czubryt MP, McAnally J, et al. Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc Natl Acad Sci USA 2005;102:1082-1087
25. Brüning JC, Michael MD, Winnay JN, et al. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 1998;2:559-569
26. Basantani MK, Sitnick MT, Cai L, et al. Pnpla3/Adiponutrin deficiency in mice does not contribute to fatty liver disease or metabolic syndrome. J Lipid Res 2011;52:318-329
27. Bielawski J, Szulc ZM, Hannun YA, Bielawska A. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatographytandem mass spectrometry. Methods 2006;39:82-91
28. Sun D, Cree MG, Wolfe RR. Quantification of the concentration and 13C tracer enrichment of long-chain fatty acyl-coenzyme A in muscle by liquid chromatography/mass spectrometry. Anal Biochem 2006;349:87-95
29. Berggren JR, Boyle KE, Chapman WH, Houmard JA. Skeletal muscle lipid oxidation and obesity: influence of weight loss and exercise. Am J Physiol Endocrinol Metab 2008;294:E726-E732
30. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS. Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 2008;3:965-976
31. Koopman R, Schaart G, Hesselink MK. Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem Cell Biol 2001;116:63-68
32. Kershaw EE, Hamm JK, Verhagen LA, Peroni O, Katic M, Flier JS. Adipose triglyceride lipase: function, regulation by insulin, and comparison with adiponutrin. Diabetes 2006;55:148-157
33. Badin PM, Louche K, Mairal A, et al. Altered skeletal muscle lipase expression and activity contribute to insulin resistance in humans. Diabetes 2011;60:1734-1742
34. Eichmann TO, Kumari M, Haas JT, et al. Studies on the substrate and stereo/regioselectivity of adipose triglyceride lipase, hormone-sensitive lipase, and diacylglycerol-O-acyltransferases. J Biol Chem 2012;287:41446-41457
35. Cantley JL, Yoshimura T, Camporez JP, et al. CGI-58 knockdown sequesters diacylglycerols in lipid droplets/ER-preventing diacylglycerolmediated hepatic insulin resistance. Proc Natl Acad Sci USA 2013;110: 1869-1874
36. Mottillo EP, Bloch AE, Leff T, Granneman JG. Lipolytic products activate peroxisome proliferator-activated receptor (PPAR) a and d in brown adipocytes to match fatty acid oxidation with supply. J Biol Chem 2012;287: 25038-25048
37. Ong KT, Mashek MT, Bu SY, Greenberg AS, Mashek DG. Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning. Hepatology 2011;53:116-126
38. Sapiro JM, Mashek MT, Greenberg AS, Mashek DG. Hepatic triacylglycerol hydrolysis regulates peroxisome proliferator-activated receptor alpha activity. J Lipid Res 2009;50:1621-1629
39. Ahmadian M, Abbott MJ, Tang T, et al. Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab 2011;13: 739-748
40. Bosma M, Sparks LM, Hooiveld GJ, et al. Overexpression of PLIN5 in skeletal muscle promotes oxidative gene expression and intramyocellular lipid content without compromising insulin sensitivity. Biochim Biophys Acta 2013;1831:844-852
41. Badin PM, Loubière C, Coonen M, et al. Regulation of skeletal muscle lipolysis and oxidative metabolism by the co-lipase CGI-58. J Lipid Res 2012; 53:839-848
42. Nunes PM, van de Weijer T, Veltien A, et al. Increased intramyocellular lipids but unaltered in vivo mitochondrial oxidative phosphorylation in skeletal muscle of adipose triglyceride lipase-deficient mice. Am J Physiol Endocrinol Metab 2012;303:E71-E81
43. Zierler KA, Jaeger D, Pollak NM, et al. Functional cardiac lipolysis in mice critically depends on comparative gene identification-58. J Biol Chem 2013; 288:9892-9904
44. 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
45. Timmers S, de Vogel-van den Bosch J, Hesselink MK, et al. Paradoxical increase in TAG and DAG content parallel the insulin sensitizing effect of unilateral DGAT1 overexpression in rat skeletal muscle. PLoS ONE 2011;6: e14503
46. Schoiswohl G, Schweiger M, Schreiber R, et al. Adipose triglyceride lipase plays a key role in the supply of the working muscle with fatty acids. J Lipid Res 2010;51:490-499
47. Wu JW,Wang SP, Alvarez F, et al. Deficiency of liver adipose triglyceride lipase in mice causes progressive hepatic steatosis. Hepatology 2011;54:122-132
48. Das SK, Eder S, Schauer S, et al. Adipose triglyceride lipase contributes to cancer-associated cachexia. Science 2011;333:233-238
49. Kienesberger PC, Pulinilkunnil T, Sung MM, et al. Myocardial ATGL overexpression decreases the reliance on fatty acid oxidation and protects against pressure overload-induced cardiac dysfunction. Mol Cell Biol 2012; 32:740-750
50. Pulinilkunnil T, Kienesberger PC, Nagendran J, et al. Myocardial adipose triglyceride lipase overexpression protects diabetic mice from the development of lipotoxic cardiomyopathy. Diabetes 2013;62:1464-1477 M.T. SITNICK AND ASSOCIATES diabetes.diabetesjournals.