Diverging regulation of pyruvate dehydrogenase kinase isoform gene expression in cultured human muscle cells

FEBS Journal

Volumn 272, Issue 12, 2005, Pages 3004-3014

  Abbot, Emily L ^a   McCormack, James G ^b   Reynet, Christine ^b   Hassall, David G ^c   Buchan, Kevin W ^c,d   Yeaman, Stephen J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b Prosidion Limited   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

^d GE HEALTHCARE   (United Kingdom)

Author keywords

Gene regulation; Mitochondria; Peroxisome proliferator activated receptor; Pyruvate dehydrogenase kinase; Skeletal muscle

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 [1 CARBOXY 2 [4 [2 (5 METHYL 2 PHENYL 4 OXAZOLYL)ETHOXY]PHENYL]ETHYLAMINO]BENZOIC ACID METHYL ESTER; 2 MORPHOLINO 8 PHENYLCHROMONE; GW 0742; GW 7647; INSULIN; ISOENZYME; ISOPROTEIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PYRUVATE DEHYDROGENASE KINASE; PYRUVATE DEHYDROGENASE KINASE 1; PYRUVATE DEHYDROGENASE KINASE 2; PYRUVATE DEHYDROGENASE KINASE 3; PYRUVATE DEHYDROGENASE KINASE 4; PYRUVATE DEHYDROGENASE PHOSPHATASE; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; CONTROLLED STUDY; ENZYME REGULATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MUSCLE CELL; MUSCLE METABOLISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION;

BUTYRIC ACIDS; CELLS, CULTURED; FATTY ACIDS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; HUMANS; INSULIN; ISOENZYMES; MUSCLE FIBERS; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; OXAZOLES; PHENYLUREA COMPOUNDS; PPAR ALPHA; PPAR DELTA; PPAR GAMMA; PROTEIN KINASES; RNA, MESSENGER; THIAZOLES; TYROSINE;

MAMMALIA;

EID: 21344434775     PISSN: 1742464X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.04713.x     Document Type: Article

References (50)

1. Linn TC, Pettit FH & Reed LJ (1969) Alpha-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.
2. Yeaman SJ, Hutcheson ET, Roche TE, Pettit FH, Brown JR, Reed EJ, Watson DC & Dixon GH (1978) Sites of phosphorylation on pyruvate dehydrogenase from bovine kidney and heart. Biochemistry 17, 2364-2370.
3. Gudi R, Bowker-Kinley MM, Kedishvili, NY, Zhao Y & Popov KM (1995) Diversity of the pyruvate dehydrogenase kinase gene family in humans. J Biol Chem 270, 28989-28994.
4. Rowles J, Scherer SW, Xi T, Majer M, Nickle DC, Rommens JM, Popov KM, Harris RA, Riebow NL, Xia J et al. (1996) Cloning and characterization of PDK4 on 7q21.3 encoding a fourth pyruvate dehydrogenase kinase isoenzyme in human. J Biol Chem 271, 22376-22382.
5. Huang B, Gudi R, Wu P, Harris RA, Hamilton J & Popov KM (1998) Isoenzymes of pyruvate dehydrogenase phosphatase. DNA-derived amino acid sequences, expression and regulation. J Biol Chem 273, 17680-17688.
6. Bowker-Kinley MM, Davis WI, Wu P, Harris RA & Popov KM (1998) Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem J 329, 191-196.
7. Bennett PH, Burch TA & Miller M (1971) Diabetes mellitus in American (Pima) Indians. Lancet 2, 125-128.
8. Majer M, Popov KM, Harris RA, Bogardus C & Prochazka M (1998) Insulin downregulates pyruvate dehydrogenase kinase (PDK) mRNA: potential mechanism contributing to increased lipid oxidation in insulin-resistant subjects. Mol Genet Metab 65, 181-186.
9. Abou MJ, Yakubu F, Lin D, Peters JC, Atkinson JB & Hill JO (1992) Skeletal muscle composition in dietary obesity-susceptible and dietary obesity-resistant rats. Am J Physiol 262, R684-R688.
10. Hickey MS, Carey JO, Azevedo JL, Houmard JA, Pories WJ, Israel RG & Dohm GL (1995) Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans. Am J Physiol 268, E543-E547.
11. Sugden MC & Holness MJ (2003) Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 284, E855-E862.
12. Wu P, Inskeep K, Bowker-Kinley MM, Popov KM & Harris RA (1999) Mechanism responsible for inactivation of skeletal muscle pyruvate dehydrogenase complex in starvation and diabetes. Diabetes 48, 1593-1599.
13. Sugden MC, Lall HS, Harris RA & Holness MJ (2000) Selective modification of the pyruvate dehydrogenase kinase isoform profile in skeletal muscle in hyperthyroidism: implications for the regulatory impact of glucose on fatty acid oxidation. J Endocrinol 167, 339-345.
14. Peters SJ, Harris RA, Heigenhauser GJ & Spriet LL (2001) Muscle fiber type comparison of PDH kinase activity and isoform expression in fed and fasted rats. Am J Physiol Regul Integr Comp Physiol 280, R661-R668.
15. Holness MJ, Kraus A, Harris RA & Sugden MC (2000) Targeted upregulation of pyruvate dehydrogenase kinase (PDK)-4 in slow-twitch skeletal muscle underlies the stable modification of the regulatory characteristics of PDK induced by high-fat feeding. Diabetes 49, 775-781.
16. Berger J & Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53, 409-435.
17. Muoio DM, MacLean PS, Lang DB, Li S, Houmard JA, Way JM, Winegar DA, Corton JC, Dohm GL & Kraus WE (2002) Fatty acid homeostasis and induction of lipid regulatory genes in skeletal muscles of peroxisome proliferator-activated receptor (PPAR) alpha knock-out mice. Evidence for compensatory regulation by PPAR delta. J Biol Chem 277, 26089-26097.
18. Muoio DM, Way JM, Tanner CJ, Winegar DA, Kliewer SA, Houmard JA, Kraus WE & Dohm GL (2002) Peroxisome proliferator-activated receptor-alpha regulates fatty acid utilization in primary human skeletal muscle cells. Diabetes 51, 901-909.
19. Way JM, Harrington WW, Brown KK, Gottschalk WK, Sundseth SS, Mansfield TA, Ramachandran RK, Willson TM & Kliewer SA (2001) Comprehensive messenger ribonucleic acid profiling reveals that peroxisome proliferator-activated receptor gamma activation has coordinate effects on gene expression in multiple insulin-sensitive tissues. Endocrinology 142, 1269-1277.
20. Borthwick AC, Wells AM, Rochford JJ, Hurel SJ, Turnbull DM & Yeaman SJ (1995) Inhibition of glycogen synthase kinase-3 by insulin in cultured human skeletal muscle myoblasts. Biochem Biophys Res Commun 210, 738-745.
21. Hurel SJ, Rochford JJ, Borthwick AC, Wells AM, Vandenheede JR, Turnbull DM & Yeaman SJ (1996) Insulin action in cultured human myoblasts: contribution of different signalling pathways to regulation of glycogen synthesis. Biochem J 320, 871-877.
22. Armstrong JL, Bonavaud SM, Toole BJ & Yeaman SJ (2001) Regulation of glycogen synthesis by amino acids in cultured human muscle cells. J Biol Chem 276, 952-956.
23. Halse R, Pearson SL, McCormack JG, Yeaman SJ & Taylor R (2001) Effects of tumor necrosis factor-alpha on insulin action in cultured human muscle cells. Diabetes 50, 1102-1109.
24. Halse R, Bonavaud SM, Armstrong JL, McCormack JG & Yeaman SJ (2001) Control of glycogen synthesis by glucose, glycogen, and insulin in cultured human muscle cells. Diabetes 50, 720-726.
25. Cheatham B, Vlahos CJ, Cheatham L, Wang L, Blenis J & Kahn CR (1994) Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70, S6 kinase, DNA synthesis, and glucose transporter translocation. Mol Cell Biol 14, 4902-4911.
26. Okada T, Kawano Y, Sakakibara T, Hazeki O & Ui M (1994) Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J Biol Chem 269, 3568-3573.
27. Stambolic V & Woodgett JR (1994) Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem J 303, 701-704.
28. Sutherland C & Cohen P (1994) The alpha-isoform of glycogen synthase kinase-3 from rabbit skeletal muscle is inactivated by p70, S6 kinase or MAP kinase-activated protein kinase-1 in vitro. FEBS Lett 338, 37-42.
29. Klein PS & Melton DA (1996) A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 93, 8455-8459.
30. Proud CG (2004) Role of mTOR signalling in the control of translation initiation and elongation by nutrients. Curr Top Microbiol Immunol 279, 215-244.
31. Blenis J (1993) Signal transduction via the MAP kinases: proceed at your own RSK. Proc Natl Acad Sci USA 90, 5889-5892.
32. DeSilva DR, Jones EA, Favata MF, Jaffee BD, Magolda RL, Trzaskos JM & Scherle PA (1998) Inhibition of mitogen-activated protein kinase kinase blocks T cell proliferation but does not induce or prevent anergy. J Immunol 160, 4175-4181.
33. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F et al. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273, 18623-18632.
34. Elbrecht A, Chen Y, Cullinan CA, Hayes N, Leibowitz M, Moller DE & Berger J (1996) Molecular cloning, expression and characterization of human peroxisome proliferator activated receptors gamma 1 and gamma 2. Biochem Biophys Res Commun 224, 431-437.
35. Schmidt A, Endo N, Rutledge SJ, Vogel R, Shinar D & Rodan GA (1992) Identification of a new member of the steroid hormone receptor superfamily that is activated by a peroxisome proliferator and fatty acids. Mol Endocrinol 6, 1634-1641.
36. Sher T, Yi HF, McBride OW & Gonzalez FJ (1993) cDNA cloning, chromosomal mapping, and functional characterization of the human peroxisome proliferator activated receptor. Biochemistry 32, 5598-5604.
37. Wu P, Peters JM & Harris RA (2001) Adaptive increase in pyruvate dehydrogenase kinase 4 during starvation is mediated by peroxisome proliferator-activated receptor alpha. Biochem Biophys Res Commun 287, 391-396.
38. Wu P, Blair PV, Sato J, Jaskiewicz J, Popov KM & Harris RA (2000) Starvation increases the amount of pyruvate dehydrogenase kinase in several mammalian tissues. Arch Biochem Biophys 381, 1-7.
39. Wu P, Sato J, Zhao Y, Jaskiewicz J, Popov KM & Harris RA (1998) Starvation and diabetes increase the amount of pyruvate dehydrogenase kinase isoenzyme 4 in rat heart. Biochem J 329, 197-201.
40. Sugden MC, Kraus A, Harris RA & Holness MJ (2000) Fibre-type specific modification of the activity and regulation of skeletal muscle pyruvate dehydrogenase kinase (PDK) by prolonged starvation and refeeding is associated with targeted regulation of PDK isoenzyme 4 expression. Biochem J 346, 651-657.
41. Furuyama T, Kitayama K, Yamashita H & Mori N (2003) Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem J 375, 365-371.
42. Peters SJ, Harris RA, Wu P, Pehleman TL, Heigenhauser GJ & Spriet LL (2001) 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.
43. Harris RA, Huang B & Wu P (2001) Control of pyruvate dehydrogenase kinase gene expression. Adv Enzyme Regul 41, 269-288.
44. Frame S & Cohen P (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359, 1-16.
45. Kwon HS, Huang B, Unterman TG & Harris RA (2004) Protein kinase B-alpha inhibits human pyruvate dehydrogenase kinase-4 gene induction by dexamethasone through inactivation of FOXO transcription factors. Diabetes 53, 899-910.
46. Brown PJ, Stuart LW, Hurley KP, Lewis MC, Winegar DA, Wilson JG, Wilkison WO, Ittoop OR & Willson TM (2001) Identification of a subtype selective human PPARalpha agonist through parallel-array synthesis. Bioorg Med Chem Lett 11, 1225-1227.
47. Wang Y-X, Zhang C-L, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H & Evans RM (2004) Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2, e294.
48. Luquet S, Lopez-Soriano J, Holst D, Frederich A, Melki J, Rassoulazadegan M & Grimaldi P (2003) Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J 17, 2299-2301.
49. Shearer BG & Hoekstra WJ (2003) Recent advances in peroxisome proliferator-activated receptor science. Curr Med Chem 10, 267-280.
50. Huang B, Wu P, Popov KM & Harris RA (2003) Starvation and diabetes reduce the amount of pyruvate dehydrogenase phosphatase in rat heart and kidney. Diabetes 52, 1371-1376.