Crystal Structures of the p21-Activated Kinases PAK4, PAK5, and PAK6 Reveal Catalytic Domain Plasticity of Active Group II PAKs

Structure

Volumn 15, Issue 2, 2007, Pages 201-213

  Eswaran, Jeyanthy ^a   Lee, Wen Hwa ^a   Debreczeni, Judit É ^a   Filippakopoulos, Panagis ^a   Turnbull, Andrew ^a   Fedorov, Oleg ^a   Deacon, Sean W ^b   Peterson, Jeffrey R ^b   Knapp, Stefan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

CELLBIO; SIGNALING

Indexed keywords

GLYCINE; P21 ACTIVATED KINASE; P21 ACTIVATED KINASE 4; P21 ACTIVATED KINASE 5; P21 ACTIVATED KINASE 6; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE; PURINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PURINES;

EID: 33846818859     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2007.01.001     Document Type: Article

References (63)

1. Abo A., Qu J., Cammarano M.S., Dan C., Fritsch A., Baud V., Belisle B., and Minden A. PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia. EMBO J. 17 (1998) 6527-6540
2. Adams J.A. Activation loop phosphorylation and catalysis in protein kinases: is there functional evidence for the autoinhibitor model?. Biochemistry 42 (2003) 601-607
3. Aimes R.T., Hemmer W., and Taylor S.S. Serine-53 at the tip of the glycine-rich loop of cAMP-dependent protein kinase: role in catalysis, P-site specificity, and interaction with inhibitors. Biochemistry 39 (2000) 8325-8332
4. Aleem E., Kiyokawa H., and Kaldis P. Cdc2-cyclin E complexes regulate the G1/S phase transition. Nat. Cell Biol. 7 (2005) 831-836
5. Bokoch G.M. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72 (2003) 743-781
6. Bullock A.N., Debreczeni J.E., Fedorov O.Y., Nelson A., Marsden B.D., and Knapp S. Structural basis of inhibitor specificity of the human protooncogene proviral insertion site in moloney murine leukemia virus (PIM-1) kinase. J. Med. Chem. 48 (2005) 7604-7614
7. Callow M.G., Clairvoyant F., Zhu S., Schryver B., Whyte D.B., Bischoff J.R., Jallal B., and Smeal T. Requirement for PAK4 in the anchorage-independent growth of human cancer cell lines. J. Biol. Chem. 277 (2002) 550-558
8. Canagarajah B.J., Khokhlatchev A., Cobb M.H., and Goldsmith E.J. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90 (1997) 859-869
9. Ching Y.P., Leong V.Y., Wong C.M., and Kung H.F. Identification of an autoinhibitory domain of p21-activated protein kinase 5. J. Biol. Chem. 278 (2003) 33621-33624
10. Cotteret S., and Chernoff J. Nucleocytoplasmic shuttling of Pak5 regulates its antiapoptotic properties. Mol. Cell. Biol. 26 (2006) 3215-3230
11. Cotteret S., Jaffer Z.M., Beeser A., and Chernoff J. p21-Activated kinase 5 (Pak5) localizes to mitochondria and inhibits apoptosis by phosphorylating BAD. Mol. Cell. Biol. 23 (2003) 5526-5539
12. Dai Y., Dent P., and Grant S. Induction of apoptosis in human leukemia cells by the CDK1 inhibitor CGP74514A. Cell Cycle 1 (2002) 143-152
13. Dalgarno D., Stehle T., Narula S., Schelling P., van Schravendijk M.R., Adams S., Andrade L., Keats J., Ram M., Jin L., et al. Structural basis of Src tyrosine kinase inhibition with a new class of potent and selective trisubstituted purine-based compounds. Chem. Biol. Drug Des. 67 (2006) 46-57
14. Dan C., Kelly A., Bernard O., and Minden A. Cytoskeletal changes regulated by the PAK4 serine/threonine kinase are mediated by LIM kinase 1 and cofilin. J. Biol. Chem. 276 (2001) 32115-32121
15. Daub H., Gevaert K., Vandekerckhove J., Sobel A., and Hall A. Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J. Biol. Chem. 276 (2001) 1677-1680
16. Dharmawardhane S., Sanders L.C., Martin S.S., Daniels R.H., and Bokoch G.M. Localization of p21-activated kinase 1 (PAK1) to pinocytic vesicles and cortical actin structures in stimulated cells. J. Cell Biol. 138 (1997) 1265-1278
17. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
18. Evans, P.R. (1993). Data reduction. Proceedings of CCP4 Study Weekend on Data Collection & Processing, Daresbury Laboratory, Warrington, UK, 114-122.
19. Giocanti N., Sadri R., Legraverend M., Ludwig O., Bisagni E., Leclerc S., Meijer L., and Favaudon V. In vitro evaluation of a novel 2,6,9-trisubstituted purine acting as a cyclin-dependent kinase inhibitor. Ann. N Y Acad. Sci. 886 (1999) 180-182
20. Gizachew D., Guo W., Chohan K.K., Sutcliffe M.J., and Oswald R.E. Structure of the complex of Cdc42Hs with a peptide derived from P-21 activated kinase. Biochemistry 39 (2000) 3963-3971
21. Grant B.D., Tsigelny I., Adams J.A., and Taylor S.S. Examination of an active-site electrostatic node in the cAMP-dependent protein kinase catalytic subunit. Protein Sci. 5 (1996) 1316-1324
22. Hayward S. Identification of specific interactions that drive ligand-induced closure in five enzymes with classic domain movements. J. Mol. Biol. 339 (2004) 1001-1021
23. Hayward S., and Lee R.A. Improvements in the analysis of domain motions in proteins from conformational change: DynDom version 1.50. J. Mol. Graph. Model. 21 (2002) 181-183
24. Hoffman G.R., Nassar N., and Cerione R.A. Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell 100 (2000) 345-356
25. Hubbard S.R. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 16 (1997) 5572-5581
26. Hubbard S.R., Wei L., Ellis L., and Hendrickson W.A. Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 372 (1994) 746-754
27. Huse M., and Kuriyan J. The conformational plasticity of protein kinases. Cell 109 (2002) 275-282
28. Jaffer Z.M., and Chernoff J. p21-activated kinases: three more join the Pak. Int. J. Biochem. Cell Biol. 34 (2002) 713-717
29. Jeffrey P.D., Russo A.A., Polyak K., Gibbs E., Hurwitz J., Massague J., and Pavletich N.P. Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376 (1995) 313-320
30. Kaur R., Liu X., Gjoerup O., Zhang A., Yuan X., Balk S.P., Schneider M.C., and Lu M.L. Activation of p21-activated kinase 6 by MAP kinase kinase 6 and p38 MAP kinase. J. Biol. Chem. 280 (2005) 3323-3330
31. Knaus U.G., Morris S., Dong H.J., Chernoff J., and Bokoch G.M. Regulation of human leukocyte p21-activated kinases through G protein-coupled receptors. Science 269 (1995) 221-223
32. Kumar R., Gururaj A.E., and Barnes C.J. p21-activated kinases in cancer. Nat. Rev. Cancer 6 (2006) 459-471
33. Leeuw T., Wu C., Schrag J.D., Whiteway M., Thomas D.Y., and Leberer E. Interaction of a G-protein β-subunit with a conserved sequence in Ste20/PAK family protein kinases. Nature 391 (1998) 191-195
34. Lei M., Lu W., Meng W., Parrini M.C., Eck M.J., Mayer B.J., and Harrison S.C. Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 102 (2000) 387-397
35. Lei M., Robinson M.A., and Harrison S.C. The active conformation of the PAK1 kinase domain. Structure 13 (2005) 769-778
36. Lo M.C., Aulabaugh A., Jin G., Cowling R., Bard J., Malamas M., and Ellestad G. Evaluation of fluorescence-based thermal shift assays for hit identification in drug discovery. Anal. Biochem. 332 (2004) 153-159
37. Lu B., Wong C.F., and McCammon J.A. Release of ADP from the catalytic subunit of protein kinase A: a molecular dynamics simulation study. Protein Sci. 14 (2005) 159-168
38. Manser E., Leung T., Salihuddin H., Zhao Z.S., and Lim L. A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367 (1994) 40-46
39. Maroni P., Bendinelli P., Zuccorononno C., Schiaffonati L., and Piccoletti R. Cellular signalling after in vivo heat shock in the liver. Cell Biol. Int. 24 (2000) 145-152
40. Martin G.A., Bollag G., McCormick F., and Abo A. A novel serine kinase activated by rac1/CDC42Hs-dependent autophosphorylation is related to PAK65 and STE20. EMBO J. 14 (1995) 1970-1978
41. Matulis D., Kranz J.K., Salemme F.R., and Todd M.J. Thermodynamic stability of carbonic anhydrase: measurements of binding affinity and stoichiometry using ThermoFluor. Biochemistry 44 (2005) 5258-5266
42. McRee D.E. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
43. Morreale A., Venkatesan M., Mott H.R., Owen D., Nietlispach D., Lowe P.N., and Laue E.D. Structure of Cdc42 bound to the GTPase binding domain of PAK. Nat. Struct. Biol. 7 (2000) 384-388
44. Nolen B., Taylor S., and Ghosh G. Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell 15 (2004) 661-675
45. Russo A.A., Jeffrey P.D., Patten A.K., Massague J., and Pavletich N.P. Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382 (1996) 325-331
46. Schindler T., Bornmann W., Pellicena P., Miller W.T., Clarkson B., and Kuriyan J. Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 289 (2000) 1938-1942
47. Schrantz N., da Silva Correia J., Fowler B., Ge Q., Sun Z., and Bokoch G.M. Mechanism of p21-activated kinase 6-mediated inhibition of androgen receptor signaling. J. Biol. Chem. 279 (2004) 1922-1931
48. Sells M.A., Knaus U.G., Bagrodia S., Ambrose D.M., Bokoch G.M., and Chernoff J. Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells. Curr. Biol. 7 (1997) 202-210
49. Shewchuk L.M., Hassell A.M., Ellis B., Holmes W.D., Davis R., Horne E.L., Kadwell S.H., McKee D.D., and Moore J.T. Structure of the Tie2 RTK domain: self-inhibition by the nucleotide binding loop, activation loop, and C-terminal tail. Structure 8 (2000) 1105-1113
50. Sicheri F., and Kuriyan J. Structures of Src-family tyrosine kinases. Curr. Opin. Struct. Biol. 7 (1997) 777-785
51. Stols L., Gu M., Dieckman L., Raffen R., Collart F.R., and Donnelly M.I. A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site. Protein Expr. Purif. 25 (2002) 8-15
52. Storoni L.C., McCoy A.J., and Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 432-438
53. Taylor S.S., Kim C., Vigil D., Haste N.M., Yang J., Wu J., and Anand G.S. Dynamics of signaling by PKA. Biochim. Biophys. Acta 1754 (2005) 25-37
54. Thompson G., Owen D., Chalk P.A., and Lowe P.N. Delineation of the Cdc42/Rac-binding domain of p21-activated kinase. Biochemistry 37 (1998) 7885-7891
55. Vadlamudi R.K., and Kumar R. P21-activated kinases in human cancer. Cancer Metastasis Rev. 22 (2003) 385-393
56. Vogtherr M., Saxena K., Hoelder S., Grimme S., Betz M., Schieborr U., Pescatore B., Robin M., Delarbre L., Langer T., et al. NMR characterization of kinase p38 dynamics in free and ligand-bound forms. Angew. Chem. Int. Ed. Engl. 45 (2006) 993-997
57. Wang Y., Metcalf III C.A., Shakespeare W.C., Sundaramoorthi R., Keenan T.P., Bohacek R.S., van Schravendijk M.R., Violette S.M., Narula S.S., Dalgarno D.C., et al. Bone-targeted 2,6,9-trisubstituted purines: novel inhibitors of Src tyrosine kinase for the treatment of bone diseases. Bioorg. Med. Chem. Lett. 13 (2003) 3067-3070
58. Wang Y., Yu Q., Cho A.H., Rondeau G., Welsh J., Adamson E., Mercola D., and McClelland M. Survey of differentially methylated promoters in prostate cancer cell lines. Neoplasia 7 (2005) 748-760
59. Xu W., Doshi A., Lei M., Eck M.J., and Harrison S.C. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3 (1999) 629-638
60. Yamaguchi H., and Hendrickson W.A. Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384 (1996) 484-489
61. Yu C., Rahmani M., Dai Y., Conrad D., Krystal G., Dent P., and Grant S. The lethal effects of pharmacological cyclin-dependent kinase inhibitors in human leukemia cells proceed through a phosphatidylinositol 3-kinase/Akt-dependent process. Cancer Res. 63 (2003) 1822-1833
62. Zhao Z.S., and Manser E. PAK and other Rho-associated kinases-effectors with surprisingly diverse mechanisms of regulation. Biochem. J. 386 (2005) 201-214
63. Zhou T., Raman M., Gao Y., Earnest S., Chen Z., Machius M., Cobb M.H., and Goldsmith E.J. Crystal structure of the TAO2 kinase domain: activation and specificity of a Ste20p MAP3K. Structure 12 (2004) 1891-1900