β2-adrenergic activation increases glycogen synthesis in L6 skeletal muscle cells through a signalling pathway independent of cyclic AMP

Diabetologia

Volumn 50, Issue 1, 2007, Pages 158-167

  Yamamoto, D L ^a   Hutchinson, D S ^a,b   Bengtsson, T ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b MONASH UNIVERSITY   (Australia)

Author keywords

2 Adrenoceptor; AMPK; Cyclic AMP; Glycogen; GSK3; L6; PI3K; Skeletal muscle

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 [1 (3 DIMETHYLAMINOPROPYL) 5 METHOXY 1H INDOL 3 YL] 3 (1H INDOL 3 YL)MALEIMIDE; 8 BROMO CYCLIC AMP; ALPHA 1 ADRENERGIC RECEPTOR STIMULATING AGENT; ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; BETA 2 ADRENERGIC RECEPTOR; CHOLERA TOXIN; CIRAZOLINE; CLONIDINE; CYCLIC AMP; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN; ISOPRENALINE; PERTUSSIS TOXIN; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE C; WORTMANNIN;

ADRENERGIC ACTIVITY; ADRENERGIC STIMULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GLUCOSE TRANSPORT; GLYCOGEN SYNTHESIS; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADRENERGIC BETA-AGONISTS; ANDROSTADIENES; ANIMALS; CELL LINE; CYCLIC AMP; GLUCOSE; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; INSULIN; ISOPROTERENOL; MULTIENZYME COMPLEXES; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; RATS; RECEPTORS, ADRENERGIC, BETA-2; SIGNAL TRANSDUCTION;

EID: 33845942588     PISSN: 0012186X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00125-006-0484-0     Document Type: Article

References (50)

1. MacAulay K, Blair AS, Hajduch E et al (2005) Constitutive activation of GSK3 down-regulates glycogen synthase abundance and glycogen deposition in rat skeletal muscle cells. J Biol Chem 280:9509-9518
2. Halse R, Rochford JJ, McCormack JG, Vandenheede JR, Hemmings BA, Yeaman SJ (1999) Control of glycogen synthesis in cultured human muscle cells. J Biol Chem 274:776-780
3. Aschenbach WG, Suzuki Y, Breeden K et al (2001) The muscle-specific protein phosphatase PP1G/R(GL)(G(M)) is essential for activation of glycogen synthase by exercise. J Biol Chem 276:39959-39967
4. O'Gorman DJ, Del Aguila LF, Williamson DL, Krishnan RK, Kirwan JP (2000) Insulin and exercise differentially regulate PI3-kinase and glycogen synthase in human skeletal muscle. J Appl Physiol 89:1412-1419
5. 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
6. Ahmad Z, DePaoli-Roach AA, Roach PJ (1982) Purification and characterization of a rabbit liver calmodulin-dependent protein kinase able to phosphorylate glycogen synthase. J Biol Chem 257:8348-8355
7. Fang X, Yu SX, Lu Y, Bast RC, Woodgett JR, Mills GB (2000) Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci USA 97:11960-11965
8. 2+- and phospholipid-activated protein kinase (protein kinase C). J Biol Chem 259:8743-8747
9. Chasiotis D, Hultman E (1985) The effect of adrenaline infusion on the regulation of glycogenolysis in human muscle during isometric contraction. Acta Physiol Scand 123:55-60
10. Ahren B (1999) Regulation of insulin secretion by nerves and neuropeptides. Ann Acad Med Singapore 28:99-104
11. Chasiotis D, Brandt R, Harris RC, Hultman E (1983) Effects of β-blockade on glycogen metabolism in human subjects during exercise. Am J Physiol 245:E166-E170
12. 2-adrenergic receptor function, response, and regulation. J Allergy Clin Immunol 117:18-24
13. Wymann MP, Bjorklof K, Calvez R et al (2003) Phosphoinositide 3-kinaseγ: a key modulator in inflammation and allergy. Biochem Soc Trans 31:275-280
14. Machida K, Inoue H, Matsumoto H et al (2004) Activation of PI3K-Akt pathway mediates antiapoptotic effects of β-adrenergic agonist in airway eosinophils. Am J Physiol Lung Cell Mol Physiol 288:L860-L867
15. 2-AR, PI3K, Akt, IKK, and NF-κB. Biochem Biophys Res Commun 319:304-311
16. Ezrailson EG, Entman ML, Garber AJ (1983) Adrenergic and serotonergic regulation of skeletal muscle metabolism in rat. I. The effects of adrenergic and serotonergic antagonists on the regulation of muscle amino acid release, glycogenolysis, and cyclic nucleotide levels. J Biol Chem 258:12494-12498
17. Gross ER, Hsu AK, Gross GJ (2004) Opioid-induced cardioprotection occurs via glycogen synthase kinase β inhibition during reperfusion in intact rat hearts. Circ Res 94:960-966
18. Sanchez C, Velasco G, Guzman M (1997) Delta9-tetrahydrocannabinol stimulates glucose utilization in C6 glioma cells. Brain Res 767:64-71
19. Beaulieu JM, Sotnikova TD, Yao WD et al (2004) Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc Natl Acad Sci USA 101:5099-5104
20. Lawrence JC Jr, James C, Hiken JF (1986) Control of glycogen synthase by insulin and isoproterenol in rat adipocytes. Changes in the distribution of phosphate in the synthase subunit in response to insulin and β-adrenergic receptor activation. J Biol Chem 261:669-677
21. Moule SK, Welsh GI, Edgell NJ, Foulstone EJ, Proud CG, Denton RM (1997) Regulation of protein kinase B and glycogen synthase kinase-3 by insulin and β-adrenergic agonists in rat epididymal fat cells. Activation of protein kinase B by wortmannin-sensitive and -insensitive mechanisms. J Biol Chem 272:7713-7719
22. 3-adrenoceptors through a cAMP, PKA and PI3-kinase-dependent pathway stimulating conventional and novel PKCs. Endocrinology 145:269-280
23. 3-adrenoceptor deficiency in brown adipocyte norepinephrine-stimulated glucose uptake. Endocrinology 146:2271-2284
24. 2-adrenoceptor-mediated glucose uptake in rat skeletal muscle cells. Br J Pharmacol 147:446-454
25. 1A-Adrenoceptors activate glucose uptake in L6 muscle cells through a phospholipase C-, phosphatidylinositol-3 kinase-, and atypical protein kinase C-dependent pathway. Endocrinology 146:901-912
26. Nevzorova J, Bengtsson T, Evans BA, Summers RJ (2002) Characterization of the β-adrenoceptor subtype involved in mediation of glucose transport in L6 cells. Br J Pharmacol 137:9-18
27. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265-275
28. 3H]CGP 12177. FEBS Lett 298:162-164
29. 1- adrenoceptors causing glucose uptake. Diabetes 55:682-690
30. Barker D, Saito M (1981) Autonomic innervation of receptors and muscle fibres in cat skeletal muscle. Proc R Soc Lond B Biol Sci 212:317-332
31. Vallerand AL, Perusse F, Bukowiecki LJ (1987) Cold exposure potentiates the effect of insulin on in vivo glucose uptake. Am J Physiol 253:E179-E186
32. 3- adrenoceptor agonist, BRL 35135, on tissue glucose utilisation. Br J Pharmacol 114:888-894
33. 3-adrenergic agonist BRL37344 increases glucose transport into L6 myocytes through a mechanism different from that of insulin. J Biochem (Tokyo) 122:90-95
34. 12 cells. Naunyn Schmiedebergs Arch Pharmacol 362: 122-127
35. Liu Y-L, Cawthorne MA, Stock MJ (1996) Biphasic effects of the β-adrenoceptor agonist, BRL 37344, on glucose utilization in rat isolated skeletal muscle. Br J Pharmacol 117:1355-1361
36. Challiss RA, Lozeman FJ, Leighton B, Newsholme EA (1986) Effects of the β-adrenoceptor agonist isoprenaline on insulin-sensitivity in soleus muscle of the rat. Biochem J 233:377-381
37. Morisco C, Zebrowski D, Condorelli G, Tsichlis P, Vatner SF, Sadoshima J (2000) The Akt-glycogen synthase kinase 3 β pathway regulates transcription of atrial natriuretic factor induced by β-adrenergic receptor stimulation in cardiac myocytes. J Biol Chem 275:14466-14475
38. James DE, Burleigh KM, Kraegen EW (1986) In vivo glucose metabolism in individual tissues of the rat. Interaction between epinephrine and insulin. J Biol Chem 261:6366-6374
39. Aslesen R, Jensen J (1998) Effects of epinephrine on glucose metabolism in contracting rat skeletal muscles. Am J Physiol 275:E448-E456
40. Pan SJ, Hancock J, Ding Z, Fogt D, Lee M, Ivy JL (2001) Effects of clenbuterol on insulin resistance in conscious obese Zucker rats. Am J Physiol Endocrinol Metab 280:E554-E561
41. 3-adrenergic agonist CL-316243 in obese Zucker-ZDF rats. Am J Physiol 274:R1212-R1219
42. Kurth-Kraczek EJ, Hirshman MF, Goodyear LJ, Winder WW (1999) 5′ AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48:1667-1671
43. Koistinen HA, Galuska D, Chibalin AV et al (2003) 5-Aminoimidazole carboxamide riboside increases glucose transport and cell-surface GLUT4 content in skeletal muscle from subjects with type 2 diabetes. Diabetes 52:1066-1072
44. Chen HC, Bandyopadhyay G, Sajan MP et al (2002) Activation of the ERK pathway and atypical protein kinase C isoforms in exercise-and aminoimidazole-4-carboxamide-1-β-D-riboside (AICAR)-stimulated glucose transport. J Biol Chem 277:23554-23562
45. Joost HG, Steinfelder HJ (1987) Forskolin inhibits insulin-stimulated glucose transport in rat adipose cells by a direct interaction with the glucose transporter. Mol Pharmacol 31:279-283
46. Klip A, Ramlal T, Douen AG, Bilan PJ, Skorecki KL (1988) Inhibition by forskolin of insulin-stimulated glucose transport in L6 muscle cells. Biochem J 255:1023-1029
47. i proteins. Br J Pharmacol 138:1358-1366
48. Braiman L, Alt A, Kuroki T et al (2001) Activation of protein kinase C zeta induces serine phosphorylation of VAMP2 in the GLUT4 compartment and increases glucose transport in skeletal muscle. Mol Cell Biol 21:7852-7861
49. Lavoie L, Band CJ, Kong M, Bergeron JJM, Posner BI (1999) Regulation of glycogen synthesis in rat hepatocytes. Evidence for multiple signaling pathways. J Biol Chem 274:28279-28285
50. Bacqueville D, Deleris P, Mendre C et al (2001) Characterization of a G protein-activated phosphoinositide 3-kinase in vascular smooth muscle cell nuclei. J Biol Chem 276:22170-22176