Crystal Structures of IRAK-4 Kinase in Complex with Inhibitors: A Serine/Threonine Kinase with Tyrosine as a Gatekeeper

Structure

Volumn 14, Issue 12, 2006, Pages 1835-1844

  Wang, Zhulun ^a   Liu, Jinsong ^a   Sudom, Athena ^a   Ayres, Merrill ^a   Li, Shyun ^a   Wesche, Holger ^a   Powers, Jay P ^a   Walker, Nigel P C ^a  

^a AMGEN INC   (United States)

Author keywords

MOLIMMUNO; SIGNALING

Indexed keywords

GLUTAMIC ACID; INTERLEUKIN 4 RECEPTOR; PHOSPHATE; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; STAUROSPORINE; TYROSINE;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; GLUTAMIC ACID; HUMANS; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; MOLECULAR SEQUENCE DATA; PHOSPHATES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN-TYROSINE KINASES; TYROSINE;

PYRONIA TITHONUS;

EID: 33845231575     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2006.11.001     Document Type: Article

References (50)

1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
2. Boggon T.J., Li Y., Manley P.W., and Eck M.J. Crystal structure of the Jak3 kinase domain in complex with a staurosporine analog. Blood 106 (2005) 996-1002
3. Brown N.R., Noble M.E., Endicott J.A., and Johnson L.N. The structural basis for specificity of substrate and recruitment peptides for cyclin dependent kinases. Nat. Cell Biol. 1 (1999) 438-443
4. Brown K., Long J.M., Vial S.C., Dedi N., Dunster N.J., Renwick S.B., Tanner A.J., Frantz J.D., Fleming M.A., and Cheetham G.M. Crystal structures of interleukin-2 tyrosine kinase and their implications for the design of selective inhibitors. J. Biol. Chem. 279 (2004) 18727-18732
5. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
6. 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
7. Cao Z., Henzel W.J., and Gao X. IRAK: a kinase associated with the interleukin-1 receptor. Science 271 (1996) 1128-1131
8. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 760-763
9. de la Fortelle E., and Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276 (1997) 472-494
10. Favelyukis S., Till J.H., Hubbard S.R., and Miller W.T. Structure and autoregulation of the insulin-like growth factor 1 receptor kinase. Nat. Struct. Biol. 8 (2001) 1058-1063
11. Hirayama T., and Oka A. Novel protein kinase of Arabidopsis thaliana (APK1) that phosphorylates tyrosine, serine and threonine. Plant Mol. Biol. 20 (1992) 653-662
12. 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
13. Janssens S., and Beyaert R. Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell 11 (2003) 293-302
14. Johnson L.N., Noble M.E., and Owen D.J. Active and inactive protein kinases: structural basis for regulation. Cell 85 (1996) 149-158
15. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
16. Kanakaraj P., Schafer P.H., Cavender D.E., Wu Y., Ngo K., Grealish P.F., Wadsworth S.A., Peterson P.A., Siekierka J.J., Harris C.A., and Fung-Leung W.P. Interleukin (IL)-1 receptor-associated kinase (IRAK) requirement for optimal induction of multiple IL-1 signaling pathways and IL-6 production. J. Exp. Med. 187 (1998) 2073-2079
17. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2256-2268
18. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
19. Lawrie A.M., Noble M.E., Tunnah P., Brown N.R., Johnson L.N., and Endicott J.A. Protein kinase inhibition by staurosporine revealed in details of the molecular interaction with CDK2. Nat. Struct. Biol. 4 (1997) 796-801
20. Lei M., Robinson M.A., and Harrison S.C. The active conformation of the PAK1 kinase domain. Structure 13 (2005) 769-778
21. Li X., Commane M., Burns C., Vithalani K., Cao Z., and Stark G.R. Mutant cells that do not respond to interleukin-1 (IL-1) reveal a novel role for IL 1 receptor-associated kinase. Mol. Cell. Biol. 19 (1999) 4643-4652
22. Li S., Strelow A., Fontana E.J., and Wesche H. IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl. Acad. Sci. USA 99 (2002) 5567-5572
23. Lougheed J.C., Chen R.H., Mak P., and Stout T.J. Crystal structures of the phosphorylated and unphosphorylated kinase domains of the Cdc42 associated tyrosine kinase ACK1. J. Biol. Chem. 279 (2004) 44039-44045
24. Lowe E.D., Noble M.E., Skamnaki V.T., Oikonomakos N.G., Owen D.J., and Johnson L.N. The crystal structure of a phosphorylase kinase peptide substrate complex: kinase substrate recognition. EMBO J. 16 (1997) 6646-6658
25. Lucet I.S., Fantino E., Styles M., Bamert R., Patel O., Broughton S.E., Walter M., Burns C.J., Treutlein H., Wilks A.F., and Rossjohn J. The structural basis of Janus kinase 2 inhibition by a potent and specific pan-Janus kinase inhibitor. Blood 107 (2006) 176-183
26. Lye E., Mirtsos C., Suzuki N., Suzuki S., and Yeh W.C. The role of interleukin 1 receptor-associated kinase-4 (IRAK-4) kinase activity in IRAK-4 mediated signaling. J. Biol. Chem. 279 (2004) 40653-40658
27. Manning G., Whyte D.B., Martinez R., Hunter T., and Sudarsanam S. The protein kinase complement of the human genome. Science 298 (2002) 1912-1934
28. Medvedev A.E., Lentschat A., Kuhns D.B., Blanco J.C., Salkowski C., Zhang S., Arditi M., Gallin J.I., and Vogel S.N. Distinct mutations in IRAK-4 confer hyporesponsiveness to lipopolysaccharide and interleukin-1 in a patient with recurrent bacterial infections. J. Exp. Med. 198 (2003) 521-531
29. Medvedev A.E., Thomas K., Awomoyi A., Kuhns D.B., Gallin J.I., Li X., and Vogel S.N. Cutting edge: expression of IL-1 receptor-associated kinase 4 (IRAK-4) proteins with mutations identified in a patient with recurrent bacterial infections alters normal IRAK-4 interaction with components of the IL-1 receptor complex. J. Immunol. 174 (2005) 6587-6591
30. Mol C.D., Lim K.B., Sridhar V., Zou H., Chien E.Y., Sang B.C., Nowakowski J., Kassel D.B., Cronin C.N., and McRee D.E. Structure of a c-kit product complex reveals the basis for kinase transactivation. J. Biol. Chem. 278 (2003) 31461-31464
31. Muzio M., Ni J., Feng P., and Dixit V.M. IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278 (1997) 1612-1615
32. Picard C., Puel A., Bonnet M., Ku C.L., Bustamante J., Yang K., Soudais C., Dupuis S., Feinberg J., Fieschi C., et al. Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299 (2003) 2076-2079
33. Powers J.P., Li S., Jaen J.C., Liu J., Walker N.P.C., Wang Z., and Wesche H. Discovery and initial SAR of inhibitors of interleukin-1 receptor-associated kinase-4. Bioorg. Med. Chem. Lett. 16 (2006) 2842-2845
34. Prade L., Engh R.A., Girod A., Kinzel V., Huber R., and Bossemeyer D. Staurosporine-induced conformational changes of cAMP-dependent protein kinase catalytic subunit explain inhibitory potential. Structure 5 (1997) 1627-1637
35. Russo A.A., Jeffrey P.D., and Pavletich N.P. Structural basis of cyclin dependent kinase activation by phosphorylation. Nat. Struct. Biol. 3 (1996) 696-700
36. Shelton C.A., and Wasserman S.A. pelle encodes a protein kinase required to establish dorsoventral polarity in the Drosophila embryo. Cell 72 (1993) 515-525
37. Suzuki N., Suzuki S., Duncan G.S., Millar D.G., Wada T., Mirtsos C., Takada H., Wakeham A., Itie A., Li S., et al. Severe impairment of interleukin-1 and Toll-like receptor signaling in mice lacking IRAK-4. Nature 416 (2002) 750-756
38. Suzuki N., Suzuki S., Millar D.G., Unno M., Hara H., Calzascia T., Yamasaki S., Yokosura T., Chen N.J., Elford A.R., et al. A critical role for the innate immune signaling molecule IRAK-4 in T cell activation. Science 311 (2006) 1927-1932
39. Swiderski M.R., and Innes R.W. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J. 26 (2001) 101-112
40. Terwilliger T.C., and Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 849-861
41. Theologis A., Ecker J.R., Palm C.J., Federspiel N.A., Kaul S., White O., Alonso J., Altafi H., Araujo R., Bowman C.L., et al. Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature 408 (2000) 816-820
42. Wan P.T., Garnett M.J., Roe S.M., Lee S., Niculescu-Duvaz D., Good V.M., Jones C.M., Marshall C.J., Springer C.J., Barford D., et al. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116 (2004) 855-867
43. Wang Z., Canagarajah B.J., Boehm J.C., Kassisa S., Cobb M.H., Young P.R., Abdel-Meguid S., Adams J.L., and Goldsmith E.J. Structural basis of inhibitor selectivity in MAP kinases. Structure 6 (1998) 1117-1128
44. Wesche H., Gao X., Li X., Kirschning C.J., Stark G.R., and Cao Z. IRAK-M is a novel member of the Pelle/interleukin-1 receptor-associated kinase (IRAK) family. J. Biol. Chem. 274 (1999) 19403-19410
45. Wood E.R., Truesdale A.T., McDonald O.B., Yuan D., Hassell A., Dickerson S.H., Ellis B., Pennisi C., Horne E., Lackey K., et al. A unique structure for epidermal growth factor receptor bound to GW572016 (Lapatinib): relationships among protein conformation, inhibitor off-rate, and receptor activity in tumor cells. Cancer Res. 64 (2004) 6652-6659
46. Yamaguchi H., and Hendrickson W.A. Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384 (1996) 484-489
47. Zhao B., Bower M.J., McDevitt P.J., Zhao H., Davis S.T., Johanson K.O., Green S.M., Concha N.O., and Zhou B.B. Structural basis for Chk1 inhibition by UCN-01. J. Biol. Chem. 277 (2002) 46609-46615
48. Zheng J., Knighton D.R., ten Eyck L.F., Karlsson R., Xuong N., Taylor S.S., and Sowadski J.M. Crystal structure of the catalytic subunit of cAMP dependent protein kinase complexed with MgATP and peptide inhibitor. Biochemistry 32 (1993) 2154-2161
49. 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
50. Zhu X., Kim J.L., Newcomb J.R., Rose P.E., Stover D.R., Toledo L.M., Zhao H., and Morgenstern K.A. Structural analysis of the lymphocyte specific kinase Lck in complex with non-selective and Src family selective kinase inhibitors. Structure 7 (1999) 651-661