Glycogen Content Regulates Peroxisome Proliferator Activated Receptor-∂ (PPAR-∂) Activity in Rat Skeletal Muscle

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Philp, Andrew ^a,b,c   MacKenzie, Matthew G ^c   Belew, Micah Y ^b   Towler, Mhairi C ^c,d   Corstorphine, Alan ^c   Papalamprou, Angela ^b   Hardie, D Grahame ^c   Baar, Keith ^b,c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d Vivomotion   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARNITINE PALMITOYLTRANSFERASE I; GLYCOGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENDURANCE TRAINING; ENZYME LOCALIZATION; FEMALE; GASTROCNEMIUS MUSCLE; GENE FUNCTION; GLYCOGEN ANALYSIS; GLYCOGEN MUSCLE LEVEL; MUSCLE CONTRACTION; MYOTUBE; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN LOCALIZATION; RANDOMIZATION; RAT; WISTAR RAT;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL LINE; ENZYME ACTIVATION; FEMALE; GLUCOSE; GLYCOGEN; MUSCLE, SKELETAL; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; PHYSICAL CONDITIONING, ANIMAL; RATS; TRANSCRIPTION FACTORS;

EID: 84885782133     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077200     Document Type: Article

References (44)

1. Bergstrom J, Hermansen L, Hultman E, Saltin B, (1967) Diet, muscle glycogen and physical performance. Acta Physiol Scand 71: 140-150.
2. Watt MJ, Heigenhauser GJ, Dyck DJ, Spriet LL, (2002) Intramuscular triacylglycerol, glycogen and acetyl group metabolism during 4 h of moderate exercise in man. J Physiol 541: 969-978.
3. Philp A, Hargreaves M, Baar K, (2012) More than a store: regulatory roles for glycogen in skeletal muscle adaptation to exercise. Am J Physiol Endocrinol Metab 302: E1343-1351.
4. Pilegaard H, Keller C, Steensberg A, Helge JW, Pedersen BK, et al. (2002) Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. J Physiol 541: 261-271.
5. de Lange P, Moreno M, Silvestri E, Lombardi A, Goglia F, et al. (2007) Fuel economy in food-deprived skeletal muscle: signaling pathways and regulatory mechanisms. FASEB J 21: 3431-3441.
6. Freyssenet D, (2007) Energy sensing and regulation of gene expression in skeletal muscle. J Appl Physiol 102: 529-540.
7. Hansen AK, Fischer CP, Plomgaard P, Andersen JL, Saltin B, et al. (2005) Skeletal muscle adaptation: training twice every second day vs. training once daily. J Appl Physiol 98: 93-99.
8. Hulston CJ, Venables MC, Mann CH, Martin C, Philp A, et al. (2010) Training with low muscle glycogen enhances fat metabolism in well-trained cyclists. Med Sci Sports Exerc 42: 2046-2055.
9. Yeo WK, Paton CD, Garnham AP, Burke LM, Carey AL, et al. (2008) Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens. J Appl Physiol 105: 1462-1470.
10. Baar K, (2004) Involvement of PPAR gamma co-activator-1, nuclear respiratory factors 1 and 2, and PPAR alpha in the adaptive response to endurance exercise. Proc Nutr Soc 63: 269-273.
11. Ehrenborg E, Krook A, (2009) Regulation of skeletal muscle physiology and metabolism by peroxisome proliferator-activated receptor delta. Pharmacol Rev 61: 373-393.
12. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, et al. (2004) Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2: e294.
13. Yan Z, Okutsu M, Akhtar YN, Lira VA, (2011) Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle. J Appl Physiol 110: 264-274.
14. Rowe GC, El-Khoury R, Patten IS, Rustin P, Arany Z, (2012) PGC-1alpha is dispensable for exercise-induced mitochondrial biogenesis in skeletal muscle. PLoS One 7: e41817.
15. Keller P, Vollaard NB, Gustafsson T, Gallagher IJ, Sundberg CJ, et al. (2011) A transcriptional map of the impact of endurance exercise training on skeletal muscle phenotype. J Appl Physiol 110: 46-59.
16. Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, et al. (2010) Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol 108: 1487-1496.
17. Calvo JA, Daniels TG, Wang X, Paul A, Lin J, et al. (2008) Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J Appl Physiol 104: 1304-1312.
18. Woods A, Salt I, Scott J, Hardie DG, Carling D, (1996) The a1 and a2 isoforms of the AMP-activated protein kinase have similar activities in rat liver but exhibit differences in substrate specificity in vitro. FEBS Lett 397: 347-351.
19. Bouskila M, Hirshman MF, Jensen J, Goodyear LJ, Sakamoto K, (2008) Insulin promotes glycogen synthesis in the absence of GSK3 phosphorylation in skeletal muscle. Am J Physiol Endocrinol Metab 294: E28-35.
20. McGee SL, Mustard KJ, Hardie DG, Baar K, (2008) Normal hypertrophy accompanied by phosphoryation and activation of AMP-activated protein kinase alpha1 following overload in LKB1 knockout mice. J Physiol 586: 1731-1741.
21. Philp A, Chen A, Lan D, Meyer GA, Murphy AN, et al. (2011) Sirtuin 1 (SIRT1) deacetylase activity is not required for mitochondrial biogenesis or peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1alpha) deacetylation following endurance exercise. J Biol Chem 286: 30561-30570.
22. He TC, Chan TA, Vogelstein B, Kinzler KW, (1999) PPARdelta is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell 99: 335-345.
23. Burkart EM, Sambandam N, Han X, Gross RW, Courtois M, et al. (2007) Nuclear receptors PPARbeta/delta and PPARalpha direct distinct metabolic regulatory programs in the mouse heart. J Clin Invest 117: 3930-3939.
24. Philp A, Belew MY, Evans A, Pham D, Sivia I, et al. (2011) The PGC-1alpha-related coactivator promotes mitochondrial and myogenic adaptations in C2C12 myotubes. Am J Physiol Regul Integr Comp Physiol 301: R864-872.
25. Wojtaszewski JF, Jorgensen SB, Hellsten Y, Hardie DG, Richter EA, (2002) Glycogen-dependent effects of 5-aminoimidazole-4-carboxamide (AICA)-riboside on AMP-activated protein kinase and glycogen synthase activities in rat skeletal muscle. Diabetes 51: 284-292.
26. Wojtaszewski JF, MacDonald C, Nielsen JN, Hellsten Y, Hardie DG, et al. (2003) Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. Am J Physiol Endocrinol Metab 284: E813-822.
27. Braissant O, Foufelle F, Scotto C, Dauca M, Wahli W, (1996) Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha,-beta, and-gamma in the adult rat. Endocrinology 137: 354-366.
28. Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA, (2005) Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. Faseb J 19: 1498-1500.
29. Watt MJ, Southgate RJ, Holmes AG, Febbraio MA, (2004) Suppression of plasma free fatty acids upregulates peroxisome proliferator-activated receptor (PPAR) alpha and delta and PPAR coactivator 1alpha in human skeletal muscle, but not lipid regulatory genes. J Mol Endocrinol 33: 533-544.
30. Fritz T, Kramer DK, Karlsson HK, Galuska D, Engfeldt P, et al. (2006) Low-intensity exercise increases skeletal muscle protein expression of PPARdelta and UCP3 in type 2 diabetic patients. Diabetes Metab Res Rev 22: 492-498.
31. Russell AP, Feilchenfeldt J, Schreiber S, Praz M, Crettenand A, et al. (2003) Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-gamma coactivator-1 and peroxisome proliferator-activated receptor-alpha in skeletal muscle. Diabetes 52: 2874-2881.
32. Fyffe SA, Alphey MS, Buetow L, Smith TK, Ferguson MA, et al. (2006) Recombinant human PPAR-beta/delta ligand-binding domain is locked in an activated conformation by endogenous fatty acids. J Mol Biol 356: 1005-1013.
33. Holst D, Luquet S, Nogueira V, Kristiansen K, Leverve X, et al. (2003) Nutritional regulation and role of peroxisome proliferator-activated receptor delta in fatty acid catabolism in skeletal muscle. Biochim Biophys Acta 1633: 43-50.
34. Burns KA, Vanden Heuvel JP, (2007) Modulation of PPAR activity via phosphorylation. Biochim Biophys Acta 1771: 952-960.
35. Steinberg GR, Watt MJ, McGee SL, Chan S, Hargreaves M, et al. (2006) Reduced glycogen availability is associated with increased AMPKalpha2 activity, nuclear AMPKalpha2 protein abundance, and GLUT4 mRNA expression in contracting human skeletal muscle. Appl Physiol Nutr Metab 31: 302-312.
36. Kramer DK, Al-Khalili L, Guigas B, Leng Y, Garcia-Roves PM, et al. (2007) Role of AMP kinase and PPARdelta in the regulation of lipid and glucose metabolism in human skeletal muscle. J Biol Chem 282: 19313-19320.
37. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, et al. (2008) AMPK and PPARdelta agonists are exercise mimetics. Cell 134: 405-415.
38. Gan Z, Burkart-Hartman EM, Han DH, Finck B, Leone TC, et al. (2011) The nuclear receptor PPARbeta/delta programs muscle glucose metabolism in cooperation with AMPK and MEF2. Genes Dev 25: 2619-2630.
39. Terada S, Tabata I, (2004) Effects of acute bouts of running and swimming exercise on PGC-1alpha protein expression in rat epitrochlearis and soleus muscle. Am J Physiol Endocrinol Metab 286: E208-216.
40. Terada S, Kawanaka K, Goto M, Shimokawa T, Tabata I, (2005) Effects of high-intensity intermittent swimming on PGC-1alpha protein expression in rat skeletal muscle. Acta Physiol Scand 184: 59-65.
41. Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, et al. (2007) Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J Biol Chem 282: 194-199.
42. Little JP, Safdar A, Cermak N, Tarnopolsky MA, Gibala MJ, (2010) Acute endurance exercise increases the nuclear abundance of PGC-1alpha in trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 298: R912-917.
43. Little JP, Safdar A, Bishop D, Tarnopolsky MA, Gibala MJ, (2011) An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1alpha and activates mitochondrial biogenesis in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 300: R1303-1310.
44. Stellingwerff T, (2012) Case study: nutrition and training periodization in three elite marathon runners. Int J Sport Nutr Exerc Metab 22: 392-400.