A Ca2+-calmodulin-eEF2K-eEF2 signalling cascade, but not AMPK, contributes to the suppression of skeletal muscle protein synthesis during contractions

Journal of Physiology

Volumn 587, Issue 7, 2009, Pages 1547-1563

  Rose, Adam J ^a   Alsted, Thomas J ^a   Jensen, Thomas E ^a   Kobberø, J Bjarke ^a   Maarbjerg, Stine J ^a   Jensen, Jørgen ^b   Richter, Erik A ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NATIONAL INSTITUTE OF OCCUPATIONAL HEALTH   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALMODULIN; ELONGATION FACTOR 2; ELONGATION FACTOR 2 KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INITIATION FACTOR 4E BINDING PROTEIN 1; ELONGATION FACTOR; EUKARYOTIC ELONGATION FACTOR 2; EUKARYOTIC ELONGATION FACTOR 2 KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL PH; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MALE; MOUSE; MUSCLE CONTRACTION; MUSCLE TWITCH; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; RAT; CALCIUM CELL LEVEL; ENZYME REPRESSION; EXERCISE; IN VITRO STUDY; PROTEIN SYNTHESIS; SKELETAL MUSCLE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CALMODULIN; CARRIER PROTEINS; DOWN-REGULATION; ELECTRIC STIMULATION; ELONGATION FACTOR 2 KINASE; ENERGY METABOLISM; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE CONTRACTION; MUSCLE FIBERS, FAST-TWITCH; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUTATION; PEPTIDE ELONGATION FACTOR 2; PHOSPHOPROTEINS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 63849188637     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2008.167528     Document Type: Article

References (65)

1. Armstrong RB & Phelps RO (1984). Muscle fiber type composition of the rat hindlimb. Am J Anat 171, 259-272.
2. Arora S, Yang JM, Kinzy TG, Utsumi R, Okamoto T, Kitayama T, Ortiz PA & Hait WN (2003). Identification and characterization of an inhibitor of eukaryotic elongation factor 2 kinase against human cancer cell lines. Cancer Res 63, 6894-6899.
3. Aslesen R, Engebretsen EM, Franch J & Jensen J (2001). Glucose uptake and metabolic stress in rat muscles stimulated electrically with different protocols. J Appl Physiol 91, 1237-1244.
4. Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ & Wackerhage H (2005). Selective activation of AMPK-PGC-1α or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19, 786-788.
5. Barclay CJ, Lichtwark GA & Curtin NA (2008). The energetic cost of activation in mouse fast-twitch muscle is the same whether measured using reduced filament overlap or N-benzyl-p-toluenesulphonamide. Acta Physiol (Oxf) 193, 381-391.
6. 2+ cycling in skeletal muscle. J Muscle Res Cell Motil 28, 259-274.
7. Bolster DR, Crozier SJ, Kimball SR & Jefferson LS (2002). AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 277, 23977-23980.
8. Browne GJ, Finn SG & Proud CG (2004). Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J Biol Chem 279, 12220-12231.
9. Browne GJ & Proud CG (2002). Regulation of peptide-chain elongation in mammalian cells. Eur J Biochem 269, 5360-5368.
10. Bylund-Fellenius AC, Ojamaa KM, Flaim KE, Li JB, Wassner SJ & Jefferson LS (1984). Protein synthesis versus energy state in contracting muscles of perfused rat hindlimb. Am J Physiol Endocrinol Metab 246, E297-E305.
11. Carlberg U, Nilsson A & Nygård O (1990). Functional properties of phosphorylated elongation factor 2. Eur J Biochem 191, 639-645.
12. Cheung A, Dantzig JA, Hollingworth S, Baylor SM, Goldman YE, Mitchison TJ & Straight AF (2002). A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4, 83-88.
13. Davies SP, Reddy H, Caivano M & Cohen P (2000). Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351, 95-105.
14. Deshmukh AS, Treebak JT, Long YC, Viollet B, Wojtaszewski JF & Zierath JR (2008). Role of adenosine 5′-monophosphate-activated protein kinase subunits in skeletal muscle mammalian target of rapamycin signaling. Mol Endocrinol 22, 1105-1112.
15. 2+/ calmodulin-independent activity. Biochem J 353, 621-626.
16. Dohm GL, Tapscott EB, Barakat HA & Kasperek GJ (1982). Measurement of in vivo protein synthesis in rats during an exercise bout. Biochem Med 27, 367-373.
17. Dorovkov MV, Pavur KS, Petrov AN & Ryazanov AG (2002). Regulation of elongation factor-2 kinase by pH. Biochemistry 41, 13444-13450.
18. Dreyer HC, Fujita S, Cadenas JG, Chinkes DL, Volpi E & Rasmussen BB (2006). Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J. Physiol 576, 613-624.
19. Dudley GA & Terjung RL (1985). Influence of acidosis on AMP deaminase activity in contracting fast-twitch muscle. Am J Physiol Cell Physiol 248, C43-C50.
20. 2+ regulation by the sarcoplasmic reticulum in saponin-permeabilized skeletal muscle fibres. Pflugers Arch 436, 104-111.
21. Gschwendt M, Kittstein W & Marks F (1994). Elongation factor-2 kinase: Effective inhibition by the novel protein kinase inhibitor rottlerin and relative insensitivity towards staurosporine. FEBS Lett 338, 85-88.
22. Herrmann-Frank A, Lüttgau HC & Stephenson DG (1999). Caffeine and excitation-contraction coupling in skeletal muscle: A stimulating story. J Muscle Res Cell Motil 20, 223-237.
23. Hori H, Nagasawa H, Ishibashi M, Uto Y, Hirata A, Saijo K, Ohkura K, Kirk KL & Uehara Y (2002). TX-1123: An antitumor 2-hydroxyarylidene-4-cyclopentene-1,3-dione as a protein tyrosine kinase inhibitor having low mitochondrial toxicity. Bioorg Med Chem 10, 3257-3265.
24. Horman S, Beauloye C, Vertommen D, Vanoverschelde JL, Hue L & Rider MH (2003). Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2. J Biol Chem 278, 41970-41976.
25. Horman S, Browne G, Krause U, Patel J, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud C & Rider M (2002). Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12, 1419-1423.
26. 2+ release increases AMPK-dependent glucose uptake in rodent soleus muscle. Am J Physiol Endocrinol Metab 292, E1308-E1317.
27. 2+ concentrations in the inhibition of mRNA translation. Arch Biochem Biophys 354, 270-280.
28. 2+ on the K eq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J Biol Chem 254, 6528-6537.
29. Lefort N, St-Amand E, Morasse S, Cote CH & Marette A (2008). The α subunit of AMPK is essential for submaximal contraction-mediated glucose transport in skeletal muscle in vitro. Am J Physiol Endocrinol Metab 295, E1447-E1454.
30. Lowry OH & Passonneau JV (1972). A Flexible System of Enzymatic Analysis. Academic Press, Inc., London.
31. Macdonald WA, Pedersen TH, Clausen T & Nielsen OB (2005). N-Benzyl-p-toluene sulphonamide allows the recording of trains of intracellular action potentials from nerve-stimulated intact fast-twitch skeletal muscle of the rat. Exp Physiol 90, 815-825.
32. McLeod LE, Wang L & Proud CG (2001). β-Adrenergic agonists increase phosphorylation of elongation factor 2 in cardiomyocytes without eliciting calcium-independent eEF2 kinase activity. FEBS Lett 489, 225-228.
33. 2+ ions in excitation-contraction coupling of skeletal muscle fibres. Biochim Biophys Acta 1241, 59-116.
34. Miranda L, Horman S, De Potter I, Hue L, Jensen J & Rider MH (2008). Effects of contraction and insulin on protein synthesis, AMP-activated protein kinase and phosphorylation state of translation factors in rat skeletal muscle. Pflugers Arch 455, 1129-1140.
35. Mu J, Brozinick JT Jr, Valladares O, Bucan M & Birnbaum MJ (2001). A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7, 1085-1094.
36. Nairn AC, Matsushita M, Nastiuk K, Horiuchi A, Mitsui K, Shimizu Y & Palfrey HC (2001). Elongation factor-2 phosphorylation and the regulation of protein synthesis by calcium. Prog Mol Subcell Biol 27, 91-129.
37. r 100,000 substrate for calmodulin-dependent protein kinase III in mammalian cells as elongation factor-2. J Biol Chem 262, 17299-17303.
38. Nesher R, Karl IE, Kaiser KE & Kipnis DM (1980). Epitrochlearis muscle. I. Mechanical performance, energetics, and fiber composition. Am J Physiol Endocrinol Metab 239, E454-E460.
39. Pain VM & Manchester KL (1970). The influence of electrical stimulation in vitro on protein synthesis and other metabolic parameters of rat extensor digitorum longus muscle. Biochem J 118, 209-220.
40. Patel J, McLeod LE, Vries RG, Flynn A, Wang X & Proud CG (2002). Cellular stresses profoundly inhibit protein synthesis and modulate the states of phosphorylation of multiple translation factors. Eur J Biochem 269, 3076-3085.
41. Pinniger GJ, Bruton JD, Westerblad H & Ranatunga KW (2005). Effects of a myosin-II inhibitor (N-benzyl-p-toluene sulphonamide, BTS) on contractile characteristics of intact fast-twitch mammalian muscle fibres. J Muscle Res Cell Motil 26, 135-141.
42. 2+-ATPases by cyclopiazonic acid. J Biol Chem 272, 2794-2800.
43. Proud CG (2007). Signalling to translation: How signal transduction pathways control the protein synthetic machinery. Biochem J 403, 217-234.
44. Redpath NT, Price NT, Severinov KV & Proud CG (1993). Regulation of elongation factor-2 by multisite phosphorylation. Eur J Biochem 213, 689-699.
45. Redpath NT & Proud CG (1993). Cyclic AMP-dependent protein kinase phosphorylates rabbit reticulocyte elongation factor-2 kinase and induces calcium-independent activity. Biochem J 293, 31-34.
46. Rennie MJ (2005). Why muscle stops building when it's working. J Physiol 569, 3.
47. Richter EA, Cleland PJ, Rattigan S & Clark MG (1987). FEBS Lett 217, 232-236.
48. 2+-calmodulin-dependent protein kinase II of fast-twitch rat skeletal muscle. J Physiol 580, 993-1005.
49. Rose AJ, Bisiani B, Vistisen B, Kiens B & Richter EA (2008). Skeletal muscle eEF2 and 4EBP1 phosphorylation during endurance exercise is dependent on intensity and muscle fiber type. Am J Physiol Reg Int Comp Physiol 296, R326-333.
50. Rose AJ, Broholm C, Killerich K, Finn SG, Proud CG, Rider MH, Richter EA & Kiens B (2005). Exercise rapidly increases eukaryotic elongation factor 2 phosphorylation in skeletal muscle of men. J Physiol 569, 223-228.
51. Rose AJ & Richter EA (2008). Regulatory mechanisms of skeletal muscle protein turnover during exercise. J Appl Physiol; DOI 10.1152/ japplphysiol.91375.2008
52. 2+/calmodulin-dependent phosphorylation of elongation factor 2. FEBS Lett 214, 331-334.
53. Ryazanov AG & Davydova EK (1989). Mechanism of elongation factor 2 (EF-2) inactivation upon phosphorylation. Phosphorylated EF-2 is unable to catalyze translocation. FEBS Lett 251, 187-190.
54. Ryazanov AG, Shestakova EA & Natapov PG (1988). Phosphorylation of elongation factor 2 by EF-2 kinase affects rate of translation. Nature 334, 170-173.
55. Sahlin K, Harris RC & Hultman E (1975). Creatine kinase equilibrium and lactate content compared with muscle pH in tissue samples obtained after isometric exercise. Biochem J 152, 173-180.
56. 2+-ATPase of sarcoplasmic reticulum. J Biol Chem 264, 17816-17823.
57. Shaw MA, Ostap EM & Goldman YE (2003). Mechanism of inhibition of skeletal muscle actomyosin by N-benzyl-p-toluenesulfonamide. Biochemistry 42, 6128-6135.
58. 2+] i induced by several glucose transport-enhancing stimuli in rat epitrochlearis muscle. J Appl Physiol 94, 1813-1820.
59. Watt MJ, Steinberg GR, Heigenhauser GJ, Spriet LL & Dyck DJ (2003). Hormone-sensitive lipase activity and triacylglycerol hydrolysis are decreased in rat soleus muscle by cyclopiazonic acid. Am J Physiol Endocrinol Metab 285, E412-E419.
60. Williamson DL, Bolster DR, Kimball SR & Jefferson LS (2006a). Time course changes in signaling pathways and protein synthesis in C2C12 myotubes following AMPK activation by AICAR. Am J Physiol Endocrinol Metab 291, E80-E89.
61. Williamson DL, Kubica N, Kimball SR & Jefferson LS (2006b). Exercise-induced alterations in extracellular signal-regulated kinase 1/ 2 and mammalian target of rapamycin (mTOR) signalling to regulatory mechanisms of mRNA translation in mouse muscle. J Physiol 573, 497-510.
62. Winder WW & Hardie DG (1996). Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am J Physiol Endocrinol Metab 270, E299-E304.
63. Wojtaszewski JF, Nielsen P, Hansen BF, Richter EA & Kiens B (2000). Isoform-specific and exercise intensity-dependent activation of 5′-AMP-activated protein kinase in human skeletal muscle. J Physiol 528, 221-226.
64. 2+ pump ATP utilization in toadfish swimbladder muscle fibers. Am J Physiol Cell Physiol 285, C781-C787.
65. Zhang SJ, Andersson DC, Sandström ME, Westerblad H & Katz A (2006). Cross bridges account for only 20% of total ATP consumption during submaximal isometric contraction in mouse fast-twitch skeletal muscle. Am J Physiol Cell Physiol 291, C147-C154.