Metabolic transformation of rabbit skeletal muscle cells in primary culture in response to low glucose

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 5, 2008, Pages 813-825

  Hanke, Nina ^a   Meissner, Joachim D ^a   Scheibe, Renate J ^a   Endeward, Volker ^a   Gros, Gerolf ^a   Kubis, Hans Peter ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b BANGOR UNIVERSITY   (United Kingdom)

Author keywords

AMP activated protein kinase (AMPK); Glucose dependent gene regulation; Glycogen; Muscle plasticity; Peroxisome proliferator activated receptor coactivator 1 (PGC 1 )

Indexed keywords

ACETYL COENZYME A ACETYLTRANSFERASE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; CALCIUM IONOPHORE; CITRATE SYNTHASE; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN KINASE B;

ADAPTATION; ANAEROBIC GLYCOLYSIS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXERCISE; FAST MUSCLE FIBER; GENE CONTROL; GENETIC TRANSFECTION; GLYCOGEN ANALYSIS; MUSCLE FIBER CULTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SKELETAL MUSCLE; SLOW MUSCLE FIBER; STATISTICAL ANALYSIS; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOLOGICAL MARKERS; CALCIMYCIN; CELLS, CULTURED; CITRATE (SI)-SYNTHASE; CULTURE MEDIA; GLUCOSE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GLYCOGEN; GUANIDINES; IONOPHORES; MULTIENZYME COMPLEXES; MUSCLE FIBERS; MUSCLE, SKELETAL; PROPIONIC ACIDS; PROTEIN-SERINE-THREONINE KINASES; RABBITS;

ORYCTOLAGUS CUNICULUS;

EID: 41949109147     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2007.12.012     Document Type: Article

References (72)

1. Booth F.W., and Thomason D.B. Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. Physiol. Rev. 71 (1991) 541-585
2. Pette D. Training effects on the contractile apparatus. Acta Physiol. Scand. 162 (1998) 367-376
3. Olson E.N., and Williams R.S. Remodeling muscles with calcineurin. Bioessays 22 (2000) 510-519
4. Wang Y.X., Zhang C.L., Yu R.T., Cho H.K., Nelson M.C., Bayuga-Ocampo C.R., Ham J., Kang H., and Evans R.M. Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol. 2 (2004) e294
5. Kubis H.P., Haller E.A., Wetzel P., and Gros G. Adult fast myosin pattern and Ca2+-induced slow myosin pattern in primary skeletal muscle culture. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 4205-4210
6. Meissner J.D., Kubis H.P., Scheibe R.J., and Gros G. Reversible Ca2+-induced fast-to-slow transition in primary skeletal muscle culture cells at the mRNA level. J. Physiol. 523 (2000) 19-28
7. Meissner J.D., Gros G., Scheibe R.J., Scholz M., and Kubis H.P. Calcineurin regulates slow myosin, but not fast myosin or metabolic enzymes, during fast-to-slow transformation in rabbit skeletal muscle cell culture. J. Physiol. 533 (2001) 215-226
8. Kubis H.P., Scheibe R.J., Meissner J.D., Hornung G., and Gros G. Fast-to-slow transformation and nuclear import/export kinetics of the transcription factor NFATc1 during electrostimulation of rabbit muscle cells in culture. J. Physiol. 541 (2002) 835-847
9. Kubis H.P., Hanke N., Scheibe R.J., Meissner J.D., and Gros G. Ca2+ transients activate calcineurin/NFATc1 and initiate fast-to-slow transformation in a primary skeletal muscle culture. Am. J. Physiol., Cell Physiol. 285 (2003) C56-C63
10. Shoubridge E.A., Challiss R.A.J., Hayes D.J., and Radda G.K. Biochemical adaptation in the skeletal-muscle of rats depleted of creatine with the substrate-analog beta-guanidinopropionic acid. Biochem. J. 232 (1985) 125-131
11. Yaspelkis B.B., Castle A.L., Ding Z., and Ivy J.L. Attenuating the decline in ATP arrests the exercise training-induced increases in muscle GLUT4 protein and citrate synthase activity. Acta Physiol. Scand. 165 (1999) 71-79
12. Winder W.W., Holmes B.F., Rubink D.S., Jensen E.B., Chen M., and Holloszy J.O. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol. 88 (2000) 2219-2226
13. Bergeron R., Ren J.M., Cadman K.S., Moore I.K., Perret P., Pypaert M., Young L.H., Semenkovich C.F., and Shulman G.I. Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am. J. Physiol: Endocrinol. Metab. 281 (2001) E1340-E1346
14. Ojuka E.O., Jones T.E., Nolte L.A., Chen M., Wamhoff B.R., Sturek M., and Holloszy J.O. Regulation of GLUT4 biogenesis in muscle: evidence for involvement of AMPK and Ca2+. Am. J. Physiol: Endocrinol. Metab. 282 (2002) E1008-E1013
15. Pilegaard H., Keller C., Steensberg A., Helge J.W., Pedersen B.K., Saltin B., and Neufer P.D. Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. J. Physiol. 541 (2002) 261-271
16. Hargreaves M. Muscle glycogen and metabolic regulation. Proc. Nutr. Soc. 63 (2004) 217-220
17. Hansen A.K., Fischer C.P., Plomgaard P., Andersen J.L., Saltin B., and Pedersen B.K. Skeletal muscle adaptation: training twice every second day vs. training once daily. J. Appl. Physiol. 98 (2005) 93-99
18. Stralfors P., Hiraga A., and Cohen P. The protein phosphatases involved in cellular regulation. Purification and characterisation of the glycogen-bound form of protein phosphatase-1 from rabbit skeletal muscle. Eur. J. Biochem. 149 (1985) 295-303
19. Newgard C.B., Brady M.J., O'Doherty R.M., and Saltiel A.R. Organizing glucose disposal: emerging roles of the glycogen targeting subunits of protein phosphatase-1. Diabetes 49 (2000) 1967-1977
20. Polekhina G., Gupta A., Michell B.J., van Denderen B., Murthy S., Feil S.C., Jennings I.G., Campbell D.J., Witters L.A., Parker M.W., Kemp B.E., and Stapleton D. AMPK beta subunit targets metabolic stress sensing to glycogen. Curr. Biol. 13 (2003) 867-871
21. Bassam B.J., Caetanoanolles G., and Gresshoff P.M. Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal. Biochem. 196 (1991) 80-83
22. Bass A., Brdiczka D., Eyer P., Hofer S., and Pette D. Metabolic differentiation of distinct muscle types at level of enzymatic organization. Eur. J. Biochem. 10 (1969) 198-206
23. Oyama V.I., and Eagle H. Measurement of cell growth in tissue culture with a phenol reagent (Folin-Ciocalteau). Proc. Soc. Exp. Biol. Med. 91 (1956) 305-307
24. Katz J., Golden S., and Wals P.A. Stimulation of hepatic glycogen-synthesis by amino-acids. Proc. Natl. Acad. Sci. U. S. A. 73 (1976) 3433-3437
25. Nordeen S.K. Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques 6 (1988) 454-458
26. Kano M., Fukao T., Yamaguchi S., Orii T., Osumi T., and Hashimoto T. Structure and expression of the human mitochondrial acetoacetyl-CoA thiolase-encoding gene. Gene 109 (1991) 285-290
27. Sambrook J., Fritsch E.F., and Maniatis T. Molecular cloning. 2. ed. (1989), Cold Spring Harbour Laboratory Press, Woodbury, NY, USA
28. Cannon-Carlson S., and Tang J. Modification of the Laemmli sodium dodecyl sulfate-polyacrylamide gel electrophoresis procedure to eliminate artifacts on reducing and nonreducing gels. Anal. Biochem. 246 (1997) 146-148
29. Winder W.W. Energy-sensing and signaling by AMP-activated protein kinase in skeletal muscle. J. Appl. Physiol. 91 (2001) 1017-1028
30. Lopez-Lluch G., Hunt N., Jones B., Zhu M., Jamieson H., Hilmer S., Cascajo M.V., Allard J., Ingram D.K., Navas P., and de Cabo R. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 1768-1773
31. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., and Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92 (1998) 829-839
32. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., and Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98 (1999) 115-124
33. Miyazawa S., Osumi T., and Hashimoto T. The presence of a new 3-oxoacyl-CoA thiolase in rat liver peroxisomes. Eur. J. Biochem. 103 (1980) 589-596
34. Vyas D.R., Spangenburg E.E., Abraha T.W., Childs T.E., and Booth F.W. GSK-3beta negatively regulates skeletal myotube hypertrophy. Am. J. Physiol., Cell Physiol. 283 (2002) C545-C551
35. Hardt S.E., and Sadoshima J. Glycogen synthase kinase-3 beta - A novel regulator of cardiac hypertrophy and development. Circ. Res. 90 (2002) 1055-1063
36. Halse R., Bonavaud S.M., Armstrong J.L., McCormack J.G., and Yeaman S.J. Control of glycogen synthesis by glucose, glycogen, and insulin in cultured human muscle cells. Diabetes 50 (2001) 720-726
37. Helander I., Westerblad H., and Katz A. Effects of glucose on contractile function, [Ca2+]i, and glycogen in isolated mouse skeletal muscle. Am. J. Physiol., Cell Physiol. 282 (2002) C1306-C1312
38. Sandstrom M.E., Abbate F., Andersson D.C., Zhang S.J., Westerblad H., and Katz A. Insulin-independent glycogen supercompensation in isolated mouse skeletal muscle: role of phosphorylase inactivation. Pflugers Arch. 448 (2004) 533-538
39. Halse R., Fryer L.G., McCormack J.G., Carling D., and Yeaman S.J. Regulation of glycogen synthase by glucose and glycogen: a possible role for AMP-activated protein kinase. Diabetes 52 (2003) 9-15
40. Holloszy J.O. Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. Biol. Chem. 242 (1967) 2278-2282
41. Davies K.J., Packer L., and Brooks G.A. Biochemical adaptation of mitochondria, muscle, and whole-animal respiration to endurance training. Arch. Biochem. Biophys. 209 (1981) 539-554
42. Ojuka E.O., Jones T.E., Han D.H., Chen M., and Holloszy J.O. Raising Ca2+ in L6 myotubes mimics effects of exercise on mitochondrial biogenesis in muscle. FASEB J. 17 (2003) 675-681
43. Pette D., and Dusterhoft S. Altered gene-expression in fast-twitch muscle induced by chronic low-frequency stimulation. Am. J. Physiol., Regul. Integr. Comp. Physiol. 262 (1992) R333-R338
44. Mayne C.N., Sutherland H., Jarvis J.C., Gilroy S.J., Craven A.J., and Salmons S. Induction of a fast-oxidative phenotype by chronic muscle stimulation: histochemical and metabolic studies. Am. J. Physiol., Cell Physiol. 39 (1996) C313-C320
45. Lawrence J.C., and Salsgiver W.J. Levels of enzymes of energy-metabolism are controlled by activity of cultured rat myotubes. Am. J. Physiol. Cell Physiol. 244 (1983) C348-C355
46. Ojuka E.O., Jones T.E., Han D.H., Chen M., Wamhoff B.R., Sturek M., and Holloszy J.O. Intermittent increases in cytosolic Ca2+ stimulate mitochondrial biogenesis in muscle cells. Am. J. Physiol: Endocrinol. Metab. 283 (2002) E1040-E1045
47. Handschin C., Rhee J., Lin J.D., Tarr P.T., and Spiegelman B.M. An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1 alpha expression in muscle. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 7111-7116
48. Freyssenet D. Energy sensing and regulation of gene expression in skeletal muscle. J. Appl. Physiol. 102 (2007) 529-540
49. Green H.J., Jones S., Ball-Burnett M., Farrance B., and Ranney D. Adaptations in muscle metabolism to prolonged voluntary exercise and training. J. Appl. Physiol. 78 (1995) 138-145
50. Pilegaard H., Saltin B., and Neufer P.D. Effect of short-term fasting and refeeding on transcriptional regulation of metabolic genes in human skeletal muscle. Diabetes 52 (2003) 657-662
51. de Lange P., Ragni M., Silvestri E., Moreno M., Schiavo L., Lombardi A., Farina P., Feola A., Goglia F., and Lanni A. Combined cDNA array/RT-PCR analysis of gene expression profile in rat gastrocnemius muscle: relation to its adaptive function in energy metabolism during fasting. FASEB J. 18 (2004) 350-352
52. Cluberton L.J., McGee S.L., Murphy R.M., and Hargreaves M. Effect of carbohydrate ingestion on exercise-induced alterations in metabolic gene expression. J. Appl. Physiol. 99 (2005) 1359-1363
53. de Lange P., Farina P., Moreno M., Ragni M., Lombardi A., Silvestri E., Burrone L., Lanni A., and Goglia F. Sequential changes in the signal transduction responses of skeletal muscle following food deprivation. FASEB J. 20 (2006) 2579-2581
54. Wende A.R., Huss J.M., Schaeffer P.J., Giguere V., and Kelly D.P. PGC-1alpha coactivates PDK4 gene expression via the orphan nuclear receptor ERRalpha: a mechanism for transcriptional control of muscle glucose metabolism. Mol. Cell Biol. 25 (2005) 10684-10694
55. Lehman J.J., Barger P.M., Kovacs A., Saffitz J.E., Medeiros D.M., and Kelly D.P. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106 (2000) 847-856
56. Ichida M., Nemoto S., and Finkel T. Identification of a specific molecular repressor of the peroxisome proliferator-activated receptor gamma Coactivator-1 alpha (PGC-1alpha). J. Biol. Chem. 277 (2002) 50991-50995
57. Ojuka E.O. Role of calcium and AMP kinase in the regulation of mitochondrial biogenesis and GLUT4 levels in muscle. Proc. Nutr. Soc. 63 (2004) 275-278
58. Stephens T.J., Chen Z.P., Canny B.J., Michell B.J., Kemp B.E., and McConell G.K. Progressive increase in human skeletal muscle AMPKalpha2 activity and ACC phosphorylation during exercise. Am. J. Physiol: Endocrinol. Metab. 282 (2002) E688-E694
59. Derave W., Ai H., Ihlemann J., Witters L.A., Kristiansen S., Richter E.A., and Ploug T. Dissociation of AMP-activated protein kinase activation and glucose transport in contracting slow-twitch muscle. Diabetes 49 (2000) 1281-1287
60. Kawanaka K., Nolte L.A., Han D.H., Hansen P.A., and Holloszy J.O. Mechanisms underlying impaired GLUT-4 translocation in glycogen-supercompensated muscles of exercised rats. Am. J. Physiol. Endocrinol Metabol. 279 (2000) E1311-E1318
61. Richter E.A., MacDonald C., Kiens B., Hardie G., and Wojtaszewski J.F.P. Dissociation of 5′AMP-activated protein kinase activity and glucose clearence in human skeletal muscle during exercise. Diabetes 50 (2001) A62
62. Wojtaszewski J.F.P., Jorgensen S.B., Hellsten Y., Hardie D.G., and Richter E.A. 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 (2002) 284-292
63. de Lange P., Moreno M., Silvestri E., Lombardi A., Goglia F., and Lanni A. Fuel economy in food-deprived skeletal muscle: signaling pathways and regulatory mechanisms. FASEB J. 21 (2007) Electronic publication ahead of print
64. Kim Y.B., Peroni O.D., Aschenbach W.G., Minokoshi Y., Kotani K., Zisman A., Kahn C.R., Goodyear L.J., and Kahn B.B. Muscle-specific deletion of the Glut4 glucose transporter alters multiple regulatory steps in glycogen metabolism. Mol. Cell Biol. 25 (2005) 9713-9723
65. Antos C.L., McKinsey T.A., Frey N., Kutschke W., McAnally J., Shelton J.M., Richardson J.A., Hill J.A., and Olson E.N. Activated glycogen synthase-3 beta suppresses cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 907-912
66. Mahoney D.J., Parise G., Melov S., Safdar A., and Tarnopolsky M.A. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J. 19 (2005) 1498-1500
67. Bergstrom M., and Hultman E. Relaxation and force during fatigue and recovery of the human quadriceps muscle: relations to metabolite changes. Pflugers Arch. 418 (1991) 153-160
68. Katz A., Sahlin K., and Broberg S. Regulation of glucose utilization in human skeletal muscle during moderate dynamic exercise. Am. J. Physiol: Endocrinol. Metab. 260 (1991) E411-E415
69. Girard J., Ferre P., and Foufelle F. Mechanisms by which carbohydrates regulate expression of genes for glycolytic and lipogenic enzymes. Annu. Rev. Nutr. 17 (1997) 325-352
70. Towle H.C., Kaytor E.N., and Shih H.M. Regulation of the expression of lipogenic enzyme genes by carbohydrate. Annu. Rev. Nutr. 17 (1997) 405-433
71. Dentin R., Pegorier J.P., Benhamed F., Foufelle F., Ferre P., Fauveau V., Magnuson M.A., Girard J., and Postic C. Hepatic glucokinase is required for the synergistic action of ChREBP and SREBP-1c on glycolytic and lipogenic gene expression. J. Biol. Chem. 279 (2004) 20314-20326
72. Dentin R., Girard J., and Postic C. Carbohydrate responsive element binding protein (ChREBP) and sterol regulatory element binding protein-1c (SREBP-1c): two key regulators of glucose metabolism and lipid synthesis in liver. Biochimie 87 (2005) 81-86