Evaluation of the role of AMP-activated protein kinase and its downstream targets in mammalian hibernation

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 142, Issue 4, 2005, Pages 374-382

  Horman, Sandrine ^a   Hussain, Nusrat ^a   Dilworth, Stephen M ^b   Storey, Kenneth B ^c   Rider, Mark H ^a  

^a DE DUVE INSTITUTE   (Belgium)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

^c CARLETON UNIVERSITY   (Canada)

Author keywords

Acetyl CoA carboxylase; Elongation factor 2; Ground squirrels; Hormone sensitive lipase; Metabolic rate suppression; Protein phosphorylation

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ELONGATION FACTOR 2; HORMONE SENSITIVE LIPASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHOSPECIFIC ANTIBODY; SERINE DERIVATIVE; THREONINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BROWN ADIPOSE TISSUE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HIBERNATION; IMMUNOBLOTTING; LIVER; MAMMAL; METABOLIC RATE; METABOLIC REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; SPERMOPHILUS TRIDECEMLINEATUS; SQUIRREL; WHITE ADIPOSE TISSUE;

ANIMALIA; EUKARYOTA; MAMMALIA; SCIURIDAE; SPERMOPHILUS; SPERMOPHILUS TRIDECEMLINEATUS;

EID: 27844481571     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2005.08.010     Document Type: Article

References (53)

1. D. Abraham, K. Podar, M. Pacher, M. Kubicek, N. Welzel, B.A. Hemmings, S.M. Dilworth, H. Mischak, W. Kolch, and M. Baccarini Raf-1-associated protein phosphatase 2A as a positive regulator of kinase activation J. Biol. Chem. 275 2000 22300 22304
2. M.W. Anthonsen, L. Ronnstraand, C. Wernstedt, E. Degerman, and C. Holm Identification of novel phosphorylation sites in hormone-sensitive lipase that are phosphorylated in response to isoproterenol and govern activation properties in vitro J. Biol. Chem. 273 1998 215 221
3. V.W. Bauer, T.L. Squire, M.E. Lowe, and M.T. Andrews Expression of a chimeric retroviral-lipase mRNA confers enhanced lipolysis in a hibernating mammal Am. J. Physiol. 281 2001 R1186 R1192
4. D.D. Belke, L.C. Wang, and G.D. Lopaschuk Acetyl-CoA carboxylase control of fatty acid oxidation in hearts from hibernating Richardson's ground squirrels Biochim. Biophys. Acta 1391 1998 25 36
5. D.R. Bolster, S.J. Crozier, S.R. Kimball, and L.S. Jefferson AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through downregulated mTOR signaling J. Biol. Chem. 277 2002 23977 23980
6. R.G. Boutilier Mechanisms of cell survival in hypoxia and hypothermia J. Exp. Biol. 204 2001 3171 3181
7. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
8. G.J. Browne, and C.G. Proud Regulation of peptide-chain elongation in mammalian cells Eur. J. Biochem. 269 2002 5360 5368
9. G.J. Browne, S.G. Finn, and C.G. Proud 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 2004 12220 12231
10. D. Carling The AMP-activated protein kinase cascade - a unifying system for energy control Trends Biochem. Sci. 29 2004 18 24
11. D. Carling, and D.G. Hardie The substrate and sequence specificity of the AMP-activated protein kinase. Phosphorylation of glycogen synthase and phosphorylase kinase Biochim. Biophys. Acta 1012 1989 81 86
12. Y. Chen, M. Matsushita, A.C. Nairn, Z. Damuni, D. Cai, K.U. Frerichs, and J.M. Hallenbeck Mechanisms for increased levels of phosphorylation of elongation factor-2 during hibernation in ground squirrels Biochemistry 40 2001 11565 11570
13. S.W.Y. Cheng, L.G.D. Fryer, D. Carling, and P.R. Shepherd T2446 is a novel mTOR phosphorylation site regulated by nutrient status J. Biol. Chem. 279 2004 15719 15722
14. M. Daval, F. Diot-Dupy, R. Bazin, I. Hainault, B. Viollet, S. Vaulont, E. Hajduch, P. Ferré, and F. Foufelle Anti-lipolytic action of AMP-activated protein kinase in rodent adipocytes J. Biol. Chem. 280 2005 25250 25257
15. S.P. Davies, D. Carling, and D.G. Hardie Tissue distribution of the AMP-activated protein kinase, and lack of activation by cyclic-AMP-dependent protein kinase, studied a specific and sensitive peptide assay Eur. J. Biochem. 186 1989 123 128
16. S.P. Davies, A.T.R. Sim, and D.G. Hardie Location and function of three sites phosphorylated on rat acetyl-CoA carboxylase by the AMP-activated protein kinase Eur. J. Biochem. 187 1990 183 190
17. P.B. Dennis, A. Jaeschke, M. Saitoh, B. Fowler, S.C. Kozma, and G. Thomas Mammalian TOR: a homeostatic ATP sensor Science 294 2001 1102 1105
18. P.F. Dubbelhuis, and A.J. Meijer Hepatic amino acid-dependent signaling is under control of AMP-dependent protein kinase FEBS Lett. 521 2002 39 42
19. J.R.B. Dyck, N. Kudo, S.P. Davies, D.G. Hardie, and G.D. Lopaschuk Phosphorylation control of cardiac acetyl-CoA carboxylase by cAMP-dependent protein kinase and 5′-AMP activated protein kinase Eur. J. Biochem. 262 1999 184 190
20. Z. el Hachimi, M. Tijane, G. Boissonnet, A. Benjouad, M. Desmadril, and J.M. Yon Regulation of the skeletal muscle metabolism during hibernation of Jaculus orientalis Comp. Biochem. Physiol. B 96 1990 457 459
21. T.E. English, and K.B. Storey Enzymes of adenylate metabolism and their role in hibernation of the white-tailed prairie dog, Cynomys leucurus Arch. Biochem. Biophys. 376 2000 91 100
22. K.U. Frerichs, C.B. Smith, M. Brenner, D.J. DeGracia, G.S. Krause, L. Marrone, T.E. Dever, and J.M. Hallenbeck Suppression of protein synthesis in brain during hibernation involves inhibition of protein synthesis initiation and elongation Proc. Natl. Acad. Sci. U. S. A. 95 1998 14511 14516
23. A.J. Garton, D.G. Campbell, P. Cohen, and S.J. Yeaman Primary structure of the site on bovine hormone-sensitive lipase phosphorylated by cyclic AMP-dependent protein kinase FEBS Lett. 229 1988 68 72
24. A.J. Garton, D.G. Campbell, D. Carling, D.G. Hardie, R.J. Colbran, and S.J. Yeaman Phosphorylation of bovine hormone-sensitive lipase by the AMP-activated protein kinase. A possible antilipolytic mechanism Eur. J. Biochem. 179 1989 249 254
25. D.G. Hardie, D. Carling, and M. Carlson The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu. Rev. Biochem. 67 1998 821 855
26. D.G. Hardie, J.W. Scott, D.A. Pan, and E.R. Hudson Management of cellular energy by the AMP-activated protein kinase system FEBS Lett. 546 2003 113 120
27. S.A. Hawley, M. Davison, A. Woods, S.P. Davies, R.K. Beri, D. Carling, and D.G. Hardie Characterization of the AMP-activated protein kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase J. Biol. Chem. 271 1996 27879 27887
28. S.A. Hawley, J. Boudeau, J.L. Reid, K.J. Mustard, L. Udd, T.P. Makela, D.R. Alessi, and D.G. Hardie Complexes between the LKB1 tumor suppressor, STRAD α/β and MO25 α/β are upstream kinases in the AMP-activated protein kinase cascade J. Biol. 2 2003 28
29. D. Hittel, and K.B. Storey The translation state of differentially expressed mRNAs in the hibernating thirteen-lined ground squirrel (Spermophilus tridecemlineatus) Arch. Biochem. Biophys. 401 2002 244 254
30. S.-P. Hong, F.C. Leiper, A. Woods, D. Carling, and M. Carlson Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases Proc. Natl. Acad. Sci. U. S. A. 100 2003 8839 8843
31. S. Horman, G.J. Browne, U. Krause, J.V. Patel, D. Vertommen, L. Bertrand, A. Lavoine, L. Hue, C.G. Proud, and M.H. Rider Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis Curr. Biol. 12 2002 1419 1423
32. S. Horman, C. Beauloye, D. Vertommen, J.-L. Vanoverschelde, L. Hue, and M.H. Rider Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2 J. Biol. Chem. 278 2003 41970 41976
33. K. Inoki, T. Zhu, and K.-L. Guan TSC2 mediates cellular energy response to control cell growth and survival Cell 115 2003 577 590
34. D.A. Kelly, and K.B. Storey Glycolysis and energetics in organs of hibernating mice (Zapus hudsonius) Can. J. Zool. 73 1995 202 207
35. B.E. Kemp, K.I. Mitchelhill, D. Stapleton, B.J. Michell, Z.P. Chen, and L.A. Witters Dealing with energy demand: the AMP-activated protein kinase Trends Biochem. Sci. 24 1999 22 25
36. U. Krause, L. Bertrand, and L. Hue Control of p70 ribosomal protein S6 kinase and acetyl-CoA carboxylase by AMP-activated protein kinase and protein phosphatases in isolated hepatocytes Eur. J. Biochem. 269 2002 3751 3759
37. +-ATPase activity by reversible phosphorylation during hibernation Biochem. Biophys. Res. Commun. 254 1999 424 429
38. A.S. Marsin, L. Bertrand, M.H. Rider, J. Deprez, C. Beauloye, M.F. Vincent, G. Van den Berghe, D. Carling, and L. Hue Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia Curr. Biol. 10 2000 1247 1255
39. O. Matejkova, K.J. Mustard, J. Sponarova, P. Flachs, M. Rossmeisl, I. Miksik, M. Thomason-Hughes, D.G. Hardie, and J. Kopecky Possible involvement of AMP-activated protein kinase in obesity resistance induced by respiratory uncoupling in white fat FEBS Lett. 569 2004 245 248
40. L.E. McLeod, and C.G. Proud ATP depletion increases phosphorylation of elongation factor eEF2 in adult cardiomyocytes independently of inhibition of mTOR signalling FEBS Lett. 531 2002 448 452
41. G.F. Merrill, E.J. Kurth, D.G. Hardie, and W.W. Winder AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle Am. J. Physiol. 273 1997 E1107 E1112
42. N.T. Redpath, and C.G. Proud Activity of protein phosphatases against initiation factor-2 and elongation factor-2 Biochem. J. 272 1990 175 180
43. N.T. Redpath, N.T. Price, K.V. Severinov, and C.G. Proud Regulation of elongation factor-2 by multisite phosphorylation Eur. J. Biochem. 213 1993 689 699
44. M.H. Rider, and E.D. Saggerson Regulation by noradrenaline of the mitochondrial and microsomal forms of glycerol phosphate acyltransferase Biochem. J. 214 1983 235 246
45. R.R. Russell, R. Bergeron, G.I. Shulman, and L.H. Young Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR Am. J. Physiol. 277 1999 H643 H649
46. I. Salt, J.W. Celler, S.A. Hawley, A. Prescott, A. Woods, D. Carling, and D.G. Hardie AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform Biochem. J. 334 1998 177 187
47. D. Stapleton, K.I. Mitchelhill, G. Gao, J. Widmer, B.J. Michell, T. The, C.M. House, C.S. Fernandez, T. Cox, L.A. Witters, and B.E. Kemp Mammalian AMP-activated protein kinase subfamily J. Biol. Chem. 271 1996 611 614
48. K.B. Storey Mammalian hibernation: transcriptional and translational controls Adv. Exp. Med. Biol. 543 2003 21 38
49. K.B. Storey, and J.M. Storey Metabolic rate depression in animals: transcriptional and translational controls Biol. Rev. 79 2004 207 233
50. P. Stralfors, P. Bjorgell, and P. Belfrage Hormonal regulation of hormone-sensitive lipase in intact adipocytes: identification of phosphorylated sites and effects on the phosphorylation by lipolytic hormones and insulin Proc. Natl. Acad. Sci. U. S. A. 81 1984 3317 3321
51. RSK1 and p70S6 kinase EMBO J. 20 2001 4370 4379
52. B.E. Wilson, S. Deeb, and G.L. Florant Seasonal changes in hormone-sensitive and lipoprotein lipase mRNA concentrations in marmot white adipose tissue Am. J. Physiol. 262 1992 R177 R181
53. A. Woods, I. Salt, J. Scott, D.G. Hardie, and D. Carling The alpha1 and alpha2 isoforms of the AMP-activated protein kinase have similar activities in rat liver but exhibit differences in substrate specificity in vitro FEBS Lett. 397 1996 347 351