Activation of AMP-activated protein Kinase revealed by hydrogen/deuterium exchange mass spectrometry

Structure

Volumn 21, Issue 11, 2013, Pages 1942-1953

  Landgraf, Rachelle R ^a   Goswami, Devrishi ^a   Rajamohan, Francis ^b   Harris, Melissa S ^b   Calabrese, Matthew F ^b   Hoth, Lise R ^b   Magyar, Rachelle ^b   Pascal, Bruce D ^a   Chalmers, Michael J ^a   Busby, Scott A ^a   Kurumbail, Ravi G ^b   Griffin, Patrick R ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6,7 DIHYDRO 4 HYDROXY 3 (2' HYDROXY 1,1' BIPHENYL 4 YL) 6 OXOTHIENO[2,3 B]PYRIDINE 5 CARBONITRILE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; CYCLODEXTRIN; DEUTERIUM; GLYCOGEN; HYDROGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LIGAND; NUCLEOTIDE;

ALPHA CHAIN; ARTICLE; BETA CHAIN; BINDING SITE; CELL ENERGY; CONFORMATIONAL TRANSITION; DEUTERIUM HYDROGEN EXCHANGE; ENZYME ACTIVATION; GENE CONTROL; HUMAN; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN;

ALLOSTERIC REGULATION; AMP-ACTIVATED PROTEIN KINASES; CATALYTIC DOMAIN; DEUTERIUM EXCHANGE MEASUREMENT; ENZYME ACTIVATION; ENZYME ACTIVATORS; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PYRONES; THIOPHENES;

EID: 84887408835     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.08.023     Document Type: Article

References (53)

1. G.A. Amodeo, M.J. Rudolph, and L. Tong Crystal structure of the heterotrimer core of Saccharomyces cerevisiae AMPK homologue SNF1 Nature 449 2007 492 495
2. M. Bieri, J.I. Mobbs, A. Koay, G. Louey, Y.F. Mok, D.M. Hatters, J.T. Park, K.H. Park, D. Neumann, D. Stapleton, and P.R. Gooley AMP-activated protein kinase β-subunit requires internal motion for optimal carbohydrate binding Biophys. J. 102 2012 305 314
3. J.B. Bruning, M.J. Chalmers, S. Prasad, S.A. Busby, T.M. Kamenecka, Y. He, K.W. Nettles, and P.R. Griffin Partial agonists activate PPARgamma using a helix 12 independent mechanism Structure 15 2007 1258 1271
4. J.M. Cacicedo, M.S. Gauthier, N.K. Lebrasseur, R. Jasuja, N.B. Ruderman, and Y. Ido Acute exercise activates AMPK and eNOS in the mouse aorta Am. J. Physiol. Heart Circ. Physiol. 301 2011 H1255 H1265
5. D. Carling, C. Thornton, A. Woods, and M.J. Sanders AMP-activated protein kinase: new regulation, new roles? Biochem. J. 445 2012 11 27
6. J.L. Celenza, and M. Carlson Cloning and genetic mapping of SNF1, a gene required for expression of glucose-repressible genes in Saccharomyces cerevisiae Mol. Cell. Biol. 4 1984 49 53
7. M.J. Chalmers, S.A. Busby, B.D. Pascal, Y. He, C.L. Hendrickson, A.G. Marshall, and P.R. Griffin Probing protein ligand interactions by automated hydrogen/deuterium exchange mass spectrometry Anal. Chem. 78 2006 1005 1014
8. K. Chen, X. Xu, S. Kobayashi, D. Timm, T. Jepperson, and Q. Liang Caloric restriction mimetic 2-deoxyglucose antagonizes doxorubicin-induced cardiomyocyte death by multiple mechanisms J. Biol. Chem. 286 2011 21993 22006
9. L. Chen, J. Wang, Y.Y. Zhang, S.F. Yan, D. Neumann, U. Schlattner, Z.X. Wang, and J.W. Wu AMP-activated protein kinase undergoes nucleotide-dependent conformational changes Nat. Struct. Mol. Biol. 19 2012 716 718
10. L. Chen, F.J. Xin, J. Wang, J. Hu, Y.Y. Zhang, S. Wan, L.S. Cao, C. Lu, P. Li, and S.F. Yan Conserved regulatory elements in AMPK Nature 498 2013 E8 E10
11. J.H. Choi, A.S. Banks, J.L. Estall, S. Kajimura, P. Boström, D. Laznik, J.L. Ruas, M.J. Chalmers, T.M. Kamenecka, and M. Blüher Anti-diabetic drugs inhibit obesity-linked phosphorylation of PPARgamma by Cdk5 Nature 466 2010 451 456
12. J.H. Choi, A.S. Banks, T.M. Kamenecka, S.A. Busby, M.J. Chalmers, N. Kumar, D.S. Kuruvilla, Y. Shin, Y. He, and J.B. Bruning Antidiabetic actions of a non-agonist PPARγ ligand blocking Cdk5-mediated phosphorylation Nature 477 2011 477 481
13. B. Cool, B. Zinker, W. Chiou, L. Kifle, N. Cao, M. Perham, R. Dickinson, A. Adler, G. Gagne, and R. Iyengar Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome Cell Metab. 3 2006 403 416
14. S.Y. Dai, M.J. Chalmers, J. Bruning, K.S. Bramlett, H.E. Osborne, C. Montrose-Rafizadeh, R.J. Barr, Y. Wang, M. Wang, and T.P. Burris Prediction of the tissue-specificity of selective estrogen receptor modulators by using a single biochemical method Proc. Natl. Acad. Sci. USA 105 2008 7171 7176
15. 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
16. F. Giordanetto, and D. Karis Direct AMP-activated protein kinase activators: a review of evidence from the patent literature Expert Opin Ther Pat 22 2012 1467 1477
17. D.G. Hardie AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy Nat. Rev. Mol. Cell Biol. 8 2007 774 785
18. D.G. Hardie, D. Carling, and S.J. Gamblin AMP-activated protein kinase: also regulated by ADP? Trends Biochem. Sci. 36 2011 470 477
19. D.G. Hardie, F.A. Ross, and S.A. Hawley AMPK: a nutrient and energy sensor that maintains energy homeostasis Nat. Rev. Mol. Cell Biol. 13 2012 251 262
20. S.A. Hawley, J. Boudeau, J.L. Reid, K.J. Mustard, L. Udd, T.P. Mäkelä, D.R. Alessi, and D.G. Hardie Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade J. Biol. 2 2003 28
21. S.A. Hawley, D.A. Pan, K.J. Mustard, L. Ross, J. Bain, A.M. Edelman, B.G. Frenguelli, and D.G. Hardie Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase Cell Metab. 2 2005 9 19
22. S.A. Hawley, M.D. Fullerton, F.A. Ross, J.D. Schertzer, C. Chevtzoff, K.J. Walker, M.W. Peggie, D. Zibrova, K.A. Green, and K.J. Mustard The ancient drug salicylate directly activates AMP-activated protein kinase Science 336 2012 918 922
23. R.L. Hurley, K.A. Anderson, J.M. Franzone, B.E. Kemp, A.R. Means, and L.A. Witters The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases J. Biol. Chem. 280 2005 29060 29066
24. J.T. Hwang, D.Y. Kwon, and S.H. Yoon AMP-activated protein kinase: a potential target for the diseases prevention by natural occurring polyphenols New Biotechnol. 26 2009 17 22
25. S.I. Itani, A.K. Saha, T.G. Kurowski, H.R. Coffin, K. Tornheim, and N.B. Ruderman Glucose autoregulates its uptake in skeletal muscle: involvement of AMP-activated protein kinase Diabetes 52 2003 1635 1640
26. E.C. Johnson, N. Kazgan, C.A. Bretz, L.J. Forsberg, C.E. Hector, R.J. Worthen, R. Onyenwoke, and J.E. Brenman Altered metabolism and persistent starvation behaviors caused by reduced AMPK function in Drosophila PLoS ONE 5 2010 5
27. B.B. Kahn, T. Alquier, D. Carling, and D.G. Hardie AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism Cell Metab. 1 2005 15 25
28. B.E. Kemp, J.S. Oakhill, and J.W. Scott AMPK structure and regulation from three angles Structure 15 2007 1161 1163
29. A. Koay, B. Woodcroft, E.J. Petrie, H. Yue, S. Emanuelle, M. Bieri, M.F. Bailey, M. Hargreaves, J.T. Park, and K.H. Park AMPK beta subunits display isoform specific affinities for carbohydrates FEBS Lett. 584 2010 3499 3503
30. T.E.F. Maniatis, and J. Sambrook Molecular Cloning: A Laboratory Manual 1982 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
31. A. Marx, C. Nugoor, S. Panneerselvam, and E. Mandelkow Structure and function of polarity-inducing kinase family MARK/Par-1 within the branch of AMPK/Snf1-related kinases FASEB J. 24 2010 1637 1648
32. A. McBride, S. Ghilagaber, A. Nikolaev, and D.G. Hardie The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor Cell Metab. 9 2009 23 34
33. M.M. Mihaylova, and R.J. Shaw The AMPK signalling pathway coordinates cell growth, autophagy and metabolism Nat. Cell Biol. 13 2011 1016 1023
34. M. Momcilovic, S.P. Hong, and M. Carlson Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro J. Biol. Chem. 281 2006 25336 25343
35. D. Neumann, A. Woods, D. Carling, T. Wallimann, and U. Schlattner Mammalian AMP-activated protein kinase: functional, heterotrimeric complexes by co-expression of subunits in Escherichia coli Protein Expr. Purif. 30 2003 230 237
36. J.S. Oakhill, Z.P. Chen, J.W. Scott, R. Steel, L.A. Castelli, N. Ling, S.L. Macaulay, and B.E. Kemp β-Subunit myristoylation is the gatekeeper for initiating metabolic stress sensing by AMP-activated protein kinase (AMPK) Proc. Natl. Acad. Sci. USA 107 2010 19237 19241
37. J.S. Oakhill, J.W. Scott, and B.E. Kemp AMPK functions as an adenylate charge-regulated protein kinase Trends Endocrinol. Metab. 23 2012 125 132
38. T. Pang, Z.S. Zhang, M. Gu, B.Y. Qiu, L.F. Yu, P.R. Cao, W. Shao, M.B. Su, J.Y. Li, F.J. Nan, and J. Li Small molecule antagonizes autoinhibition and activates AMP-activated protein kinase in cells J. Biol. Chem. 283 2008 16051 16060
39. G. Polekhina, A. Gupta, B.J. Michell, B. van Denderen, S. Murthy, S.C. Feil, I.G. Jennings, D.J. Campbell, L.A. Witters, and M.W. Parker AMPK beta subunit targets metabolic stress sensing to glycogen Curr. Biol. 13 2003 867 871
40. G. Polekhina, A. Gupta, B.J. van Denderen, S.C. Feil, B.E. Kemp, D. Stapleton, and M.W. Parker Structural basis for glycogen recognition by AMP-activated protein kinase Structure 13 2005 1453 1462
41. F. Rajamohan, M.S. Harris, R.K. Frisbie, L.R. Hoth, K.F. Geoghegan, J.J. Valentine, A.R. Reyes, J.A. Landro, X. Qiu, and R.G. Kurumbail Escherichia coli expression, purification and characterization of functional full-length recombinant alpha2beta2gamma3 heterotrimeric complex of human AMP-activated protein kinase Protein Expr. Purif. 73 2010 189 197
42. U. Riek, R. Scholz, P. Konarev, A. Rufer, M. Suter, A. Nazabal, P. Ringler, M. Chami, S.A. Müller, and D. Neumann Structural properties of AMP-activated protein kinase: dimerization, molecular shape, and changes upon ligand binding J. Biol. Chem. 283 2008 18331 18343
43. M.J. Rudolph, G.A. Amodeo, and L. Tong An inhibited conformation for the protein kinase domain of the Saccharomyces cerevisiae AMPK homolog Snf1 Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66 2010 999 1002
44. M.J. Sanders, Z.S. Ali, B.D. Hegarty, R. Heath, M.A. Snowden, and D. Carling Defining the mechanism of activation of AMP-activated protein kinase by the small molecule A-769662, a member of the thienopyridone family J. Biol. Chem. 282 2007 32539 32548
45. G. Schimmack, R.A. Defronzo, and N. Musi AMP-activated protein kinase: Role in metabolism and therapeutic implications Diabetes Obes. Metab. 8 2006 591 602
46. J.W. Scott, B.J. van Denderen, S.B. Jorgensen, J.E. Honeyman, G.R. Steinberg, J.S. Oakhill, T.J. Iseli, A. Koay, P.R. Gooley, D. Stapleton, and B.E. Kemp Thienopyridone drugs are selective activators of AMP-activated protein kinase beta1-containing complexes Chem. Biol. 15 2008 1220 1230
47. L. Shang, and X. Wang AMPK and mTOR coordinate the regulation of Ulk1 and mammalian autophagy initiation Autophagy 7 2011 924 926
48. G.R. Steinberg, and B.E. Kemp AMPK in Health and Disease Physiol. Rev. 89 2009 1025 1078
49. V. Vingtdeux, P. Chandakkar, H. Zhao, P. Davies, and P. Marambaud Small-molecule activators of AMP-activated protein kinase (AMPK), RSVA314 and RSVA405, inhibit adipogenesis Mol. Med. 17 2011 1022 1030
50. B. Xiao, R. Heath, P. Saiu, F.C. Leiper, P. Leone, C. Jing, P.A. Walker, L. Haire, J.F. Eccleston, and C.T. Davis Structural basis for AMP binding to mammalian AMP-activated protein kinase Nature 449 2007 496 500
51. B. Xiao, M.J. Sanders, E. Underwood, R. Heath, F.V. Mayer, D. Carmena, C. Jing, P.A. Walker, J.F. Eccleston, and L.F. Haire Structure of mammalian AMPK and its regulation by ADP Nature 472 2011 230 233
52. J. Zhang, M.J. Chalmers, K.R. Stayrook, L.L. Burris, Y. Wang, S.A. Busby, B.D. Pascal, R.D. Garcia-Ordonez, J.B. Bruning, and M.A. Istrate DNA binding alters coactivator interaction surfaces of the intact VDR-RXR complex Nat. Struct. Mol. Biol. 18 2011 556 563
53. L. Zhu, L. Chen, X.M. Zhou, Y.Y. Zhang, Y.J. Zhang, J. Zhao, S.R. Ji, J.W. Wu, and Y. Wu Structural insights into the architecture and allostery of full-length AMP-activated protein kinase Structure 19 2011 515 522