3-D structure and dynamics of protein kinase B-new mechanism for the allosteric regulation of an AGC kinase

Journal of Chemical Biology

Volumn 2, Issue 1, 2009, Pages 11-25

  Calleja, Véronique ^a   Laguerre, Michel ^b   Larijani, Banafshé ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b INSTITUT EUROPÉEN DE CHIMIE ET BIOLOGIE   (France)

Author keywords

3 D structure; Akt; Dynamics; FRET FLIM; Molecular modelling; Multi disciplinary approach; Protein kinase B

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; PHOSPHATIDYLINOSITIDE; PLECKSTRIN; PROTEIN KINASE; PROTEIN KINASE B; THREONINE;

ALLOSTERISM; CELL ASSAY; CIRCULAR DICHROISM; CROSS LINKING; ENERGY TRANSFER; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME ISOLATION; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME STRUCTURE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; REACTION ANALYSIS; REVIEW; SIMULATION; SITE DIRECTED MUTAGENESIS; TANDEM MASS SPECTROMETRY; THREE DIMENSIONAL IMAGING; X RAY CRYSTALLOGRAPHY;

EID: 67349094328     PISSN: 18646158     EISSN: 18646166     Source Type: Journal    
DOI: 10.1007/s12154-009-0016-8     Document Type: Review

References (65)

1. D Alcor V Calleja B Larijani 2009 Revealing signaling in single cells by single- and two-photon fluorescence lifetime imaging microscopy Methods Mol Biol 462 307
2. DR Alessi M Andjelkovic B Caudwell 1996 Mechanism of activation of protein kinase B by insulin and IGF-1 Embo J 15 23 6541 (Pubitemid 26413787)
3. DR Alessi M Deak A Casamayor 1997 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase Curr Biol 7 10 776 (Pubitemid 27441832)
4. B Ananthanarayanan M Fosbrink M Rahdar 2007 Live-cell molecular analysis of Akt activation reveals roles for activation loop phosphorylation J Biol Chem 282 50 366334
5. B Ananthanarayanan Q Ni J Zhang 2005 Signal propagation from membrane messengers to nuclear effectors revealed by reporters of phosphoinositide dynamics and Akt activity Proc Natl Acad Sci U S A 102 42 15081 (Pubitemid 41513338)
6. M Andjelkovic DR Alessi R Meier 1997 Role of translocation in the activation and function of protein kinase B J Biol Chem 272 50 31515 (Pubitemid 28013293)
7. M Andjelkovic T Jakubowicz P Cron 1996 Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/PKB) promoted by serum and protein phosphatase inhibitors Proc Natl Acad Sci U S A 93 12 5699 (Pubitemid 26190743)
8. D Auguin P Barthe MT Auge-Senegas 2004 Solution structure and backbone dynamics of the pleckstrin homology domain of the human protein kinase B (PKB/Akt). Interaction with inositol phosphates J Biomol NMR 28 2 137 (Pubitemid 38232793)
9. SF Barnett MT Bilodeau CW Lindsley 2005 The Akt/PKB family of protein kinases: a review of small molecule inhibitors and progress towards target validation Curr Top Med Chem 5 2 109 (Pubitemid 40514509)
10. SF Barnett D Defeo-Jones S Fu 2005 Identification and characterization of pleckstrin-homology-domain-dependent and isoenzyme-specific Akt inhibitors Biochem J 385 Pt 2 399 (Pubitemid 40165072)
11. A Bellacosa TO Chan NN Ahmed 1998 Akt activation by growth factors is a multiple-step process: the role of the PH domain Oncogene 17 3 313 (Pubitemid 28383008)
12. DP Brazil BA Hemmings 2001 Ten years of protein kinase B signalling: a hard Akt to follow Trends Biochem Sci 26 11 657 (Pubitemid 33042488)
13. J Brugge MC Hung GB Mills 2007 A new mutational AKTivation in the PI3K pathway Cancer Cell 12 2 104 (Pubitemid 47199129)
14. V Calleja D Alcor M Laguerre 2007 Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo PLoS Biol 5 4 e95 (Pubitemid 46631855)
15. V Calleja SM Ameer-Beg B Vojnovic 2003 Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy Biochem J 372 Pt 1 33 (Pubitemid 36609604)
16. V Calleja M Laguerre PJ Parker 2009 Role of a novel PH-kinase domain interface in PKB/Akt regulation: structural mechanism for allosteric inhibition PLoS Biol 7 1 e17
17. AJ Cameron M De Rycker V Calleja 2007 Protein kinases, from B to C Biochem Soc Trans 35 Pt 5 1013 (Pubitemid 350206416)
18. TO Chan SE Rittenhouse PN Tsichlis 1999 AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide- dependent phosphorylation Annu Rev Biochem 68 965 (Pubitemid 29449213)
19. R Chen O Kim J Yang 2001 Regulation of Akt/PKB activation by tyrosine phosphorylation J Biol Chem 276 34 31858 (Pubitemid 37384838)
20. J Cicenas 2008 The potential role of Akt phosphorylation in human cancers Int J Biol Markers 23 1 1
21. BJ Collins M Deak JS Arthur 2003 In vivo role of the PIF-binding docking site of PDK1 defined by knock-in mutation EMBO J 22 16 4202 (Pubitemid 37021748)
22. BJ Collins M Deak V Murray-Tait 2005 In vivo role of the phosphate groove of PDK1 defined by knockin mutation J Cell Sci 118 Pt 21 5023 (Pubitemid 41672433)
23. NM Conus KM Hannan BE Cristiano 2002 Direct identification of tyrosine 474 as a regulatory phosphorylation site for the Akt protein kinase J Biol Chem 277 41 38021 (Pubitemid 35154653)
24. J Feng J Park P Cron 2004 Identification of a PKB/Akt hydrophobic motif Ser-473 kinase as DNA-dependent protein kinase J Biol Chem 279 39 41189 (Pubitemid 39287721)
25. KM Ferguson JM Kavran VG Sankaran 2000 Structural basis for discrimination of 3-phosphoinositides by pleckstrin homology domains Mol Cell 6 2 373
26. A Gambhir G Hangyas-Mihalyne I Zaitseva 2004 Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins Biophys J 86 4 2188 (Pubitemid 38524409)
27. T Gao F Furnari AC Newton 2005 PHLPP: a phosphatase that directly dephosphorylates Akt, promotes apoptosis, and suppresses tumor growth Mol Cell 18 1 13 (Pubitemid 40444644)
28. MG Gold D Barford D Komander 2006 Lining the pockets of kinases and phosphatases Curr Opin Struct Biol 16 6 693
29. CJ Green O Goransson GS Kular 2008 Use of Akti and a drug-resistant mutant validates a critical role for PKB/Akt in the insulin-dependent regulation of glucose and system A amino acid uptake J Biol Chem 283 27653 27667
30. C Hauge TL Antal D Hirschberg 2007 Mechanism for activation of the growth factor-activated AGC kinases by turn motif phosphorylation EMBO J 26 9 2251 (Pubitemid 46685864)
31. BX Huang HY Kim 2006 Interdomain conformational changes in Akt activation revealed by chemical cross-linking and tandem mass spectrometry Mol Cell Proteomics 5 6 1045 (Pubitemid 43985929)
32. X Huang M Begley KA Morgenstern 2003 Crystal structure of an inactive Akt2 kinase domain Structure 11 1 21 (Pubitemid 36071494)
33. T Ikenoue K Inoki Q Yang 2008 Essential function of TORC2 in PKC and Akt turn motif phosphorylation, maturation and signalling EMBO J 27 14 1919
34. PD Jeffrey AA Russo K Polyak 1995 Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex Nature 376 6538 313
35. N Kannan N Haste SS Taylor 2007 The hallmark of AGC kinase functional divergence is its C-terminal tail, a cis-acting regulatory module Proc Natl Acad Sci U S A 104 4 1272 (Pubitemid 46183994)
36. C Kim NH Xuong SS Taylor 2005 Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA Science 307 5710 690 (Pubitemid 40194632)
37. DR Knighton JH Zheng LF Ten Eyck 1991 Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase Science 253 5018 407 (Pubitemid 21917165)
38. MT Kunkel Q Ni RY Tsien 2005 Spatio-temporal dynamics of protein kinase B/Akt signaling revealed by a genetically encoded fluorescent reporter J Biol Chem 280 7 5581 (Pubitemid 40280036)
39. M Laguerre M Saux J-P Dubost 1997 MLPP: a program for the calculation of molecular lipophilicity in proteins Pharm. Sci 3 217 (Pubitemid 28067693)
40. R Lasserre XJ Guo F Conchonaud 2008 Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation Nat Chem Biol 4 9 538
41. CW Lindsley Z Zhao WH Leister 2005 Allosteric Akt (PKB) inhibitors: discovery and SAR of isozyme selective inhibitors Bioorg Med Chem Lett 15 3 761 (Pubitemid 40143162)
42. BD Manning LC Cantley 2007 AKT/PKB signaling: navigating downstream Cell 129 7 1261 (Pubitemid 46962095)
43. R Meier M Thelen BA Hemmings 1998 Inactivation and dephosphorylation of protein kinase Balpha (PKBalpha) promoted by hyperosmotic stress EMBO J 17 24 7294 (Pubitemid 29002698)
44. CC Milburn M Deak SM Kelly 2003 Binding of phosphatidylinositol 3,4,5-trisphosphate to the pleckstrin homology domain of protein kinase B induces a conformational change Biochem J 375 Pt 3 531 (Pubitemid 37433501)
45. A Mora D Komander DM van Aalten 2004 PDK1, the master regulator of AGC kinase signal transduction Semin Cell Dev Biol 15 2 161 (Pubitemid 38251644)
46. AC Newton 2003 Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm Biochem J 370 Pt 2 361 (Pubitemid 36315124)
47. B Nolen S Taylor G Ghosh 2004 Regulation of protein kinases; controlling activity through activation segment conformation Mol Cell 15 5 661 (Pubitemid 39194898)
48. T Obata MB Yaffe GG Leparc 2000 Peptide and protein library screening defines optimal substrate motifs for AKT/PKB J Biol Chem 275 46 36108
49. DW Parsons TL Wang Y Samuels 2005 Colorectal cancer: mutations in a signalling pathway Nature 436 7052 792 (Pubitemid 41160630)
50. P Pellicena J Kuriyan 2006 Protein-protein interactions in the allosteric regulation of protein kinases Curr Opin Struct Biol 16 6 702
51. CL Sable N Filippa C Filloux 1998 Involvement of the pleckstrin homology domain in the insulin-stimulated activation of protein kinase B J Biol Chem 273 45 29600 (Pubitemid 28509968)
52. DD Sarbassov DA Guertin SM Ali 2005 Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex Science 307 5712 1098 (Pubitemid 40262113)
53. K Sasaki M Sato Y Umezawa 2003 Fluorescent indicators for Akt/protein kinase B and dynamics of Akt activity visualized in living cells J Biol Chem 278 33 30945 (Pubitemid 36994606)
54. MP Scheid JR Woodgett 2001 PKB/AKT: functional insights from genetic models Nat Rev Mol Cell Biol 2 10 760 (Pubitemid 33679838)
55. Z Shi KA Resing NG Ahn 2006 Networks for the allosteric control of protein kinases Curr Opin Struct Biol 16 6 686
56. L Stephens K Anderson D Stokoe 1998 Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B Science 279 5351 710
57. JR Testa PN Tsichlis 2005 AKT signaling in normal and malignant cells Oncogene 24 50 7391 (Pubitemid 41637978)
58. CC Thomas M Deak DR Alessi 2002 High-resolution structure of the pleckstrin homology domain of protein kinase b/akt bound to phosphatidylinositol (3,4,5)-trisphosphate Curr Biol 12 14 1256
59. A Toker AC Newton 2000 Akt/protein kinase B is regulated by autophosphorylation at the hypothetical PDK-2 site J Biol Chem 275 12 8271 (Pubitemid 30180163)
60. E Tokunaga E Oki A Egashira 2008 Deregulation of the Akt pathway in human cancer Curr Cancer Drug Targets 8 1 27
61. J Yang P Cron VM Good 2002 Crystal structure of an activated Akt/protein kinase B ternary complex with GSK3-peptide and AMP-PNP Nat Struct Biol 9 12 940 (Pubitemid 35417064)
62. J Yang P Cron V Thompson 2002 Molecular mechanism for the regulation of protein kinase B/Akt by hydrophobic motif phosphorylation Mol Cell 9 6 1227 (Pubitemid 34722302)
63. J Zhang MD Allen 2007 FRET-based biosensors for protein kinases: illuminating the kinome Mol Biosyst 3 11 759 (Pubitemid 47587185)
64. L Zhang KC Lee MS Bhojani 2007 Molecular imaging of Akt kinase activity Nat Med 13 9 1114 (Pubitemid 47517501)
65. Z Zhao WH Leister RG Robinson 2005 Discovery of 2,3,5-trisubstituted pyridine derivatives as potent Akt1 and Akt2 dual inhibitors Bioorg Med Chem Lett 15 4 905 (Pubitemid 40458621)