AMP-activated protein kinase β-subunit requires internal motion for optimal carbohydrate binding

Biophysical Journal

Volumn 102, Issue 2, 2012, Pages 305-314

  Bieri, Michael ^a   Mobbs, Jesse I ^a   Koay, Ann ^a   Louey, Gavin ^a   Mok, Yee Foong ^a   Hatters, Danny M ^a   Park, Jong Tae ^c   Park, Kwan Hwa ^d   Neumann, Dietbert ^e   Stapleton, David ^b   Gooley, Paul R ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c Chungnam National University   (South Korea)

^d Sangmyung University   (South Korea)

^e MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

AMINO ACID SEQUENCE; ARTICLE; CARBOHYDRATE METABOLISM; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MOVEMENT (PHYSIOLOGY); MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; AMP-ACTIVATED PROTEIN KINASES; CARBOHYDRATE METABOLISM; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOVEMENT; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 84862907765     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.12.012     Document Type: Article

References (52)

1. G.R. Steinberg, and B.E. Kemp AMPK in health and disease Physiol. Rev. 89 2009 1025 1078
2. J.W. Scott, J.S. Oakhill, and B.J. van Denderen AMPK/SNF1 structure: a menage à trois of energy-sensing Front. Biosci. 14 2009 596 610
3. Z.P. Chen, and G.K. McConell B.E. Kemp AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation Am. J. Physiol. Endocrinol. Metab. 279 2000 E1202 E1206
4. S.H. Park, and S.R. Gammon W.W. Winder Phosphorylation-activity relationships of AMPK and acetyl-CoA carboxylase in muscle J. Appl. Physiol. 92 2002 2475 2482 (Pubitemid 34666373)
5. L. Hue, and C. Beauloye M.H. Rider Insulin and ischemia stimulate glycolysis by acting on the same targets through different and opposing signaling pathways J. Mol. Cell. Cardiol. 34 2002 1091 1097 (Pubitemid 35205153)
6. X. Xi, J. Han, and J.Z. Zhang Stimulation of glucose transport by AMP-activated protein kinase via activation of p38 mitogen-activated protein kinase J. Biol. Chem. 276 2001 41029 41034
7. D.G. Hardie AMPK: a key regulator of energy balance in the single cell and the whole organism Int. J. Obes. (Lond) 32 Suppl 4 2008 S7 S12
8. I. Leclerc, and B. Viollet G.A. Rutter Role of AMP-activated protein kinase in the regulation of gene transcription Biochem. Soc. Trans. 30 2002 307 311
9. S. Horman, and G. Browne M. 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 (Pubitemid 34915545)
10. K.S. Röckl, and M.F. Hirshman L.J. Goodyear Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift Diabetes 56 2007 2062 2069 (Pubitemid 47195818)
11. L.G. Fryer, A. Parbu-Patel, and D. Carling The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways J. Biol. Chem. 277 2002 25226 25232 (Pubitemid 34951829)
12. B.E. Kemp, and D. Stapleton L.A. Witters AMP-activated protein kinase, super metabolic regulator Biochem. Soc. Trans. 31 2003 162 168 (Pubitemid 36241420)
13. S.A. Hawley, and M. Davison D.G. Hardie Characterization of the AMP-activated protein kinase 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 (Pubitemid 26367365)
14. A. Ferrer, and C. Caelles F.G. Hegardt Activation of rat liver cytosolic 3-hydroxy-3-methylglutaryl coenzyme A reductase kinase by adenosine 5′-monophosphate Biochem. Biophys. Res. Commun. 132 1985 497 504 (Pubitemid 16198655)
15. J.S. Oakhill, and R. Steel B.E. Kemp AMPK is a direct adenylate charge-regulated protein kinase Science 332 2011 1433 1435
16. A. McBride, and S. Ghilagaber D.G. Hardie The glycogen-binding domain on the AMPK β subunit allows the kinase to act as a glycogen sensor Cell Metab. 9 2009 23 34
17. G. Polekhina, and A. Gupta M.W. Parker Structural basis for glycogen recognition by AMP-activated protein kinase Structure 13 2005 1453 1462 (Pubitemid 41427585)
18. A. Koay, and B. Woodcroft P.R. Gooley AMPK β subunits display isoform specific affinities for carbohydrates FEBS Lett. 584 2010 3499 3503
19. M. Umetsu, and T. Nakanishi I. Kumagai Protein-protein interactions and selection: generation of molecule-binding proteins on the basis of tertiary structural information FEBS J. 277 2010 2006 2014
20. S. Vemparala, S. Mehrotra, and H. Balaram Role of loop dynamics in thermal stability of mesophilic and thermophilic adenylosuccinate synthetase: a molecular dynamics and normal mode analysis study Biochim. Biophys. Acta 1814 2011 630 637
21. M.C. Peeters, and G.J.P. van Westen A.P. IJzerman Importance of the extracellular loops in G protein-coupled receptors for ligand recognition and receptor activation Trends Pharmacol. Sci. 32 2011 35 42
22. T. Kaneko, S.S. Sidhu, and S.S.C. Li Evolving specificity from variability for protein interaction domains Trends Biochem. Sci. 36 2011 183 190
23. A.G. Palmer 3rd NMR characterization of the dynamics of biomacromolecules Chem. Rev. 104 2004 3623 3640
24. N. Doucet, E.D. Watt, and J.P. Loria The flexibility of a distant loop modulates active site motion and product release in ribonuclease A Biochemistry 48 2009 7160 7168
25. K. Siggers, C. Soto, and A.G. Palmer 3rd Conformational dynamics in loop swap mutants of homologous fibronectin type III domains Biophys. J. 93 2007 2447 2456 (Pubitemid 47511145)
26. M.D. Stewart, and B. Morgan T.I. Igumenova Probing the determinants of diacylglycerol binding affinity in the C1B domain of protein kinase Cα J. Mol. Biol. 408 2011 949 970
27. R. Scholz, and M. Suter D. Neumann Homo-oligomerization and activation of AMP-activated protein kinase are mediated by the kinase domain αG-helix J. Biol. Chem. 284 2009 27425 27437
28. M. Tollinger, and N.R. Skrynnikov L.E. Kay Slow dynamics in folded and unfolded states of an SH3 domain J. Am. Chem. Soc. 123 2001 11341 11352 (Pubitemid 33070591)
29. J.P. Loria, M. Rance, and A.G. Palmer A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy J. Am. Chem. Soc. 121 1999 2331 2332 (Pubitemid 29152458)
30. N.A. Farrow, and R. Muhandiram L.E. Kay Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation Biochemistry 33 1994 5984 6003 (Pubitemid 24184605)
31. F. Delaglio, and S. Grzesiek A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
32. W.F. Vranken, and W. Boucher E.D. Laue The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins 59 2005 687 696 (Pubitemid 40695845)
33. M. Bieri, and P.R. Gooley Automated NMR relaxation dispersion data analysis using NESSY BMC Bioinformatics 12 2011 421
34. M. Bieri, E.J. d'Auvergne, and P.R. Gooley relaxGUI: a new software for fast and simple NMR relaxation data analysis and calculation of ps-ns and μs motion of proteins J. Biomol. NMR 50 2011 147 155
35. C. Wang, M.J. Grey, and A.G. Palmer 3rd CPMG sequences with enhanced sensitivity to chemical exchange J. Biomol. NMR 21 2001 361 366 (Pubitemid 34071390)
36. Z. Luz, and S. Meiboom Nuclear magnetic resonance study of protolysis of trimethylammonium ion in aqueous solution - order of reaction with respect to solvent J. Chem. Phys. 39 1963 366 370
37. 2 upon Carr-Purcell pulse separation J. Magn. Reson. 6 1972 89 105
38. H. Akaike Information theory and an extension of the maximum likelihood principle B.N. Petrov, F. Csaki, 2nd International Symposium on Information Theory 1973 Akademiai Kiado Budapest, Hungary 267 281
39. P. Schuck, and P. Rossmanith Determination of the sedimentation coefficient distribution by least-squares boundary modeling Biopolymers 54 2000 328 341
40. G. Polekhina, and A. Gupta D. Stapleton AMPK β subunit targets metabolic stress sensing to glycogen Curr. Biol. 13 2003 867 871 (Pubitemid 36573256)
41. A.J. Baldwin, and L.E. Kay NMR spectroscopy brings invisible protein states into focus Nat. Chem. Biol. 5 2009 808 814
42. D.D. Boehr, H.J. Dyson, and P.E. Wright An NMR perspective on enzyme dynamics Chem. Rev. 106 2006 3055 3079 (Pubitemid 44376926)
43. A. Mittermaier, and L.E. Kay New tools provide new insights in NMR studies of protein dynamics Science 312 2006 224 228
44. M. Bieri, and A.H. Kwan P.R. Gooley Macromolecular NMR spectroscopy for the non-spectroscopist: beyond macromolecular solution structure determination FEBS J. 278 2011 704 715
45. C. Thornton, M.A. Snowden, and D. Carling Identification of a novel AMP-activated protein kinase β subunit isoform that is highly expressed in skeletal muscle J. Biol. Chem. 273 1998 12443 12450 (Pubitemid 28240617)
46. J.B. Birk, and J.F. Wojtaszewski Predominant α2/β2/γ3 AMPK activation during exercise in human skeletal muscle J. Physiol. 577 2006 1021 1032 (Pubitemid 44873663)
47. M. Kim, and R. Tian Targeting AMPK for cardiac protection: opportunities and challenges J. Mol. Cell. Cardiol. 51 2011 548 553
48. F. Bauer, and H. Sticht A proline to glycine mutation in the Lck SH3-domain affects conformational sampling and increases ligand binding affinity FEBS Lett. 581 2007 1555 1560 (Pubitemid 46528921)
49. T. Peng, and J.S. Zintsmaster J.W. Peng Sequence-specific dynamics modulate recognition specificity in WW domains Nat. Struct. Mol. Biol. 14 2007 325 331 (Pubitemid 46608337)
50. H.R. Bosshard Molecular recognition by induced fit: how fit is the concept? News Physiol. Sci. 16 2001 171 173 (Pubitemid 33713265)
51. D.D. Boehr, and D. McElheny P.E. Wright The dynamic energy landscape of dihydrofolate reductase catalysis Science 313 2006 1638 1642 (Pubitemid 44414038)
52. M. Vendruscolo, and C.M. Dobson Structural biology. Dynamic visions of enzymatic reactions Science 313 2006 1586 1587 (Pubitemid 44414023)