PGC-1α increases PDH content but does not change acute PDH regulation in mouse skeletal muscle

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 5, 2010, Pages

  Kiilerich, Kristian ^a   Adser, Helle ^a   Jakobsen, Anne H ^a   Pedersen, Per A ^a   Hardie, D Grahame ^b   Wojtaszewski, Jorgen F P ^a   Pilegaard, Henriette ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Pyruvate dehydrogenase kinase

Indexed keywords

GLYCOGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE E1 ALPHA; PYRUVATE DEHYDROGENASE KINASE 4; UNCLASSIFIED DRUG; MESSENGER RNA; MITOCHONDRIAL PROTEIN; PPARGC1A PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; PYRUVATE DEHYDROGENASE (ACETYL TRANSFERRING) KINASE; PYRUVATE DEHYDROGENASE (ACETYL-TRANSFERRING) KINASE; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVATE DEHYDROGENASE E1ALPHA SUBUNIT; TRANSACTIVATOR PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INDUCTION; FEMALE; GLYCOGEN MUSCLE LEVEL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUADRICEPS FEMORIS MUSCLE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; RNA ISOLATION; SKELETAL MUSCLE; UPREGULATION; ANIMAL; CONVALESCENCE; DIET RESTRICTION; EATING; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; MUSCLE CONTRACTION; MUSCLE MITOCHONDRION; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; TIME;

ANIMALS; EATING; FASTING; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOGEN; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCLE CONTRACTION; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PYRUVATE DEHYDROGENASE (LIPOAMIDE); PYRUVATE DEHYDROGENASE COMPLEX; QUADRICEPS MUSCLE; RECOVERY OF FUNCTION; RNA, MESSENGER; TIME FACTORS; TRANS-ACTIVATORS; UP-REGULATION;

EID: 78149488032     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00400.2010     Document Type: Article

References (51)

1. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1α. Nature 451: 1008-1012, 2008.
2. Behal RH, Buxton DB, Robertson JG, Olson MS. Regulation of the pyruvate dehydrogenase multienzyme complex. Annu Rev Nutr 13: 497-520, 1993. (Pubitemid 23227794)
3. Bergmeyer HU. Methods of Enzymatic Analysis. New York: Academic, 1974.
4. Bowker-Kinley MM, Davis WI, Wu P, Harris RA, Popov KM. Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem J 329: 191-196, 1998.
5. Calvo JA, Daniels TG, Wang X, Paul A, Lin J, Spiegelman BM, Stevenson SC, Rangwala SM. Muscle-specific expression of PPARγ coactivator-1α improves exercise performance and increases peak oxygen uptake. J Appl Physiol 104: 1304-1312, 2008.
6. Cederblad G, Carlin JI, Constantin-Teodosiu D, Harper P, Hultman E. Radioisotopic assays of CoASH and carnitine and their acetylated forms in human skeletal muscle. Anal Biochem 185: 274-278, 1990.
7. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
8. Constantin-Teodosiu D, Cederblad G, Hultman E. A sensitive radioisotopic assay of pyruvate dehydrogenase complex in human muscle tissue. Anal Biochem 198: 347-351, 1991.
9. Constantin-Teodosiu D, Peirce NS, Fox J, Greenhaff PL. Muscle pyruvate availability can limit the flux, but not activation, of the pyruvate dehydrogenase complex during submaximal exercise in humans. J Physiol 561: 647-655, 2004.
10. Denton RM. Regulation of mitochondrial dehydrogenases by calcium ions. Biochim Biophys Acta 2009.
11. Handschin C, Chin S, Li P, Liu F, Maratos-Flier E, Lebrasseur NK, Yan Z, Spiegelman BM. Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1α muscle-specific knock-out animals. J Biol Chem 282: 30014-30021, 2007.
12. Harris RA, Bowker-Kinley MM, Huang B, Wu P. Regulation of the activity of the pyruvate dehydrogenase complex. Adv Enzyme Regul 42: 249-259, 2002.
13. Huang B, Gudi R, Wu P, Harris RA, Hamilton J, Popov KM. Isoenzymes of pyruvate dehydrogenase phosphatase. DNA-derived amino acid sequences, expression, and regulation. J Biol Chem 273: 17680-17688, 1998.
14. Huang B, Wu P, Popov KM, Harris RA. Starvation and diabetes reduce the amount of pyruvate dehydrogenase phosphatase in rat heart and kidney. Diabetes 52: 1371-1376, 2003. (Pubitemid 36666190)
15. Kiilerich K, Birk JB, Damsgaard R, Wojtaszewski JF, Pilegaard H. Regulation of PDH in human arm and leg muscles at rest and during intense exercise. Am J Physiol Endocrinol Metab 294: E36-E42, 2008.
16. Kiilerich K, Birk JB, Saltin B, Pedersen PA, Wojtaszewski JFP, Pilegaard H. Exercise induces increased PDK4 expression in human skeletal muscles independent of a fasting effect (Abstract). Diabetes 57, Suppl 1: A308, 2008.
17. Kiilerich K, Gudmundsson M, Birk JB, Lundby C, Taudorf S, Plomgaard P, Saltin B, Pedersen PA, Wojtaszewski JF, Pilegaard H. Low muscle glycogen and elevated plasma free fatty acid modify but do not prevent exercise-induced PDH activation in human skeletal muscle. Diabetes 59: 26-32, 2010.
18. Korotchkina LG, Patel MS. Probing the mechanism of inactivation of human pyruvate dehydrogenase by phosphorylation of three sites. J Biol Chem 276: 5731-5738, 2001.
19. Korotchkina LG, Patel MS. Probing the mechanism of inactivation of human pyruvate dehydrogenase by phosphorylation of three sites. J Biol Chem 276: 5731-5738, 2001.
20. LeBlanc PJ, Harris RA, Peters SJ. Skeletal muscle fiber type comparison of pyruvate dehydrogenase phosphatase activity and isoform expression in fed and food-deprived rats. Am J Physiol Endocrinol Metab 292: E571-E576, 2007.
21. LeBlanc PJ, Peters SJ, Tunstall RJ, Cameron-Smith D, Heigenhauser GJ. Effects of aerobic training on pyruvate dehydrogenase and pyruvate dehydrogenase kinase in human skeletal muscle. J Physiol 557: 559-570, 2004. (Pubitemid 38807394)
22. Leick L, Hellsten Y, Fentz J, Lyngby SS, Wojtaszewski JF, Hidalgo J, Pilegaard H. PGC-1α mediates exercise-induced skeletal muscle VEGF expression in mice. Am J Physiol Endocrinol Metab 297: E92-E103, 2009.
23. Leick L, Wojtaszewski JF, Johansen ST, Kiilerich K, Comes G, Hellsten Y, Hidalgo J, Pilegaard H. PGC-1α is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle. Am J Physiol Endocrinol Metab 294: E463-E474, 2008.
24. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature 418: 797-801, 2002.
25. Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY, Mootha VK, Jager S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, Lowell BB, Krainc D, Spiegelman BM. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119: 121-135, 2004.
26. Linn TC, Pettit FH, Reed LJ. α-Keto acid dehydrogenase complexes. X. Regulation of the activity of the pyruvate dehydrogenase complex from beef kidney mitochondria by phosphorylation and dephosphorylation. Proc Natl Acad Sci USA 62: 234-241, 1969.
27. Liu C, Li S, Liu T, Borjigin J, Lin JD. Transcriptional coactivator PGC-1α integrates the mammalian clock and energy metabolism. Nature 447: 477-481, 2007.
28. Lowry OH, Passonneau JV. A Flexible System of Enzymatic Analysis. New York: Academic, 1972.
29. Lundby C, Nordsborg N, Kusuhara K, Kristensen KM, Neufer PD, Pilegaard H. Gene expression in human skeletal muscle: alternative normalization method and effect of repeated biopsies. Eur J Appl Physiol 95: 351-360, 2005. (Pubitemid 43055098)
30. Olesen J, Kiilerich K, Pilegaard H. PGC-1α-mediated adaptations in skeletal muscle. Pflügers Arch 460: 153-162, 2010.
31. Peters SJ, Harris RA, Wu P, Pehleman TL, Heigenhauser GJ, Spriet LL. Human skeletal muscle PDH kinase activity and isoform expression during a 3-day high-fat/low-carbohydrate diet. Am J Physiol Endocrinol Metab 281: E1151-E1158, 2001.
32. Pilegaard H, Birk JB, Sacchetti M, Mourtzakis M, Hardie DG, Stewart G, Neufer PD, Saltin B, Van HG, Wojtaszewski JF. PDH-E1α dephosphorylation and activation in human skeletal muscle during exercise: effect of intralipid infusion. Diabetes 55: 3020-3027, 2006.
33. Pilegaard H, Keller C, Steensberg A, Helge JW, Pedersen BK, Saltin B, Neufer PD. Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. J Physiol 541: 261-271, 2002.
34. Pilegaard H, Neufer PD. Transcriptional regulation of pyruvate dehydrogenase kinase 4 in skeletal muscle during and after exercise. Proc Nutr Soc 63: 221-226, 2004.
35. Pilegaard H, Ordway GA, Saltin B, Neufer PD. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279: E806-E814, 2000.
36. Pilegaard H, Osada T, Andersen LT, Helge JW, Saltin B, Neufer PD. Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise. Metabolism 54: 1048-1055, 2005.
37. Pilegaard H, Saltin B, Neufer PD. Effect of short-term fasting and refeeding on transcriptional regulation of metabolic genes in human skeletal muscle. Diabetes 52: 657-662, 2003.
38. Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor- gamma coactivator 1α (PGC-1α): transcriptional coactivator and metabolic regulator. Endocr Rev 24: 78-90, 2003. (Pubitemid 36223280)
39. Putman CT, Spriet LL, Hultman E, Lindinger MI, Lands LC, Mc- Kelvie RS, Cederblad G, Jones NL, Heigenhauser GJ. Pyruvate dehydrogenase activity and acetyl group accumulation during exercise after different diets. Am J Physiol Endocrinol Metab 265: E752-E760, 1993.
40. Ravindran S, Radke GA, Guest JR, Roche TE. Lipoyl domain-based mechanism for the integrated feedback control of the pyruvate dehydrogenase complex by enhancement of pyruvate dehydrogenase kinase activity. J Biol Chem 271: 653-662, 1996.
41. St. Amand TA, Spriet LL, Jones NL, Heigenhauser GJ. Pyruvate overrides inhibition of PDH during exercise after a low-carbohydrate diet. Am J Physiol Endocrinol Metab 279: E275-E283, 2000.
42. Sugden C, Crawford RM, Halford NG, Hardie DG. Regulation of spinach SNF1-related (SnRK1) kinases by protein kinases and phosphatases is associated with phosphorylation of the T loop and is regulated by 5′-AMP. Plant J 19: 433-439, 1999.
43. Sugden MC, Orfali KA, Holness MJ. The pyruvate dehydrogenase complex: nutrient control and the pathogenesis of insulin resistance. J Nutr 125: 1746S-1752S, 1995.
44. Tsintzas K, Jewell K, Kamran M, Laithwaite D, Boonsong T. Differential regulation of metabolic genes in skeletal muscle during starvation and refeeding in humans. J Physiol 575: 291-303, 2006.
45. Watt MJ, Heigenhauser GJ, LeBlanc PJ, Inglis JG, Spriet LL, Peters SJ. Rapid upregulation of pyruvate dehydrogenase kinase activity in human skeletal muscle during prolonged exercise. J Appl Physiol 97: 1261-1267, 2004.
46. Wende AR, Huss JM, Schaeffer PJ, Giguere V, Kelly DP. PGC-1α coactivates PDK4 gene expression via the orphan nuclear receptor ERRα: a mechanism for transcriptional control of muscle glucose metabolism. Mol Cell Biol 25: 10684-10694, 2005.
47. Wende AR, Schaeffer PJ, Parker GJ, Zechner C, Han DH, Chen MM, Hancock CR, Lehman JJ, Huss JM, McClain DA, Holloszy JO, Kelly DP. A role for the transcriptional coactivator PGC-1α in muscle refueling. J Biol Chem 282: 36642-36651, 2007.
48. Wu P, Inskeep K, Bowker-Kinley MM, Popov KM, Harris RA. Mechanism responsible for inactivation of skeletal muscle pyruvate dehydrogenase complex in starvation and diabetes. Diabetes 48: 1593-1599, 1999.
49. Wu P, Peters JM, Harris RA. Adaptive increase in pyruvate dehydrogenase kinase 4 during starvation is mediated by peroxisome proliferator-activated receptorα. Biochem Biophys Res Commun 287: 391-396, 2001.
50. Yeaman SJ, Hutcheson ET, Roche TE, Pettit FH, Brown JR, Reed LJ, Watson DC, Dixon GH. Sites of phosphorylation on pyruvate dehydrogenase from bovine kidney and heart. Biochemistry 17: 2364-2370, 1978.
51. Zhang Y, Ma K, Sadana P, Chowdhury F, Gaillard S, Wang F, McDonnell DP, Unterman TG, Elam MB, Park EA. Estrogen-related receptors stimulate pyruvate dehydrogenase kinase isoform 4 gene expression. J Biol Chem 281: 39897-39906, 2006.