Autoinhibition of Bruton's tyrosine kinase (Btk) and activation by soluble inositol hexakisphosphate

eLife

Volumn 2015, Issue 4, 2015, Pages

  Wang, Qi ^a,b   Vogan, Erik M ^c,e   Nocka, Laura M ^a   Rosen, Connor E ^a,b   Zorn, Julie A ^a,b   Harrison, Stephen C ^c   Kuriyan, John ^a,b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e Beryllium Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRUTON TYROSINE KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHYTIC ACID; PLASMID VECTOR; ABELSON KINASE; AGAMMAGLOBULINAEMIA TYROSINE KINASE; PROTEIN TYROSINE KINASE; SOLUTION AND SOLUBILITY;

AFFINITY CHROMATOGRAPHY; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BINDING SITE; CONTROLLED STUDY; CRYSTALLIZATION; CRYSTALLOGRAPHY; DIMERIZATION; EC50; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; GEL PERMEATION CHROMATOGRAPHY; ISOTHERMAL TITRATION CALORIMETRY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SEQUENCE HOMOLOGY; WESTERN BLOTTING; ALLOSTERISM; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOCATALYSIS; BOVINE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; LIPID METABOLISM; METABOLISM; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; SOLUBILITY; SOLUTION AND SOLUBILITY; SRC HOMOLOGY DOMAIN; STATIC ELECTRICITY; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ANIMALIA;

ALLOSTERIC REGULATION; ANIMALS; BINDING SITES; BIOCATALYSIS; CATTLE; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; LIPID METABOLISM; MICE; MODELS, MOLECULAR; PHOSPHORYLATION; PHYTIC ACID; PROTEIN MULTIMERIZATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-ABL; SOLUBILITY; SOLUTIONS; SRC HOMOLOGY DOMAINS; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 85003048330     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06074     Document Type: Article

References (78)

1. Adams PD, Grosse-Kunstleve RW, Hung L-W, loergerTR, McCoyAJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK & Terwilliger TC (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954.
2. Andreotti AH, Schwartzberg PL, Joseph RE & Berg LJ (2010) T-cell signaling regulated by the Tec family kinase, Itk. Cold Spring Harb Perspect Biol 2, a002287-a002287.
3. Banavali NK & Roux B (2009) Flexibility and charge asymmetry in the activation loop of Src tyrosine kinases. Proteins: Structure, Function, and Bioinformatics 74, 378-389.
4. Baraldi E, Carugo KD, Hyvönen M, Surdo PL, RileyAM, Potter BV, O'Brien R, Ladbury JE & Saraste M (1999) Structure of the PH domain from Bruton's tyrosine kinase in complex with inositol 1, 3, 4, 5-tetrakisphosphate. Structure 7, 449-460.
5. Barker SC, Kassel DB, Weigl D, Huang X, Luther MA & Knight WB (1995) Characterization of pp60c-src tyrosine kinase activities using a continuous assay: autoactivation of the enzyme is an intermolecular autophosphorylation process. Biochemistry 34, 14843-14851.
6. Bence K, Ma W, Kozasa T & Huang X-Y (1997) Direct stimulation of Bruton's tyrosine kinase by Gq-protein α-subunit. Nature 389, 296-299.
7. Brasher BB & Van Etten RA (2000) c-Abl has high intrinsic tyrosine kinase activity that is stimulated by mutation of the Src homology 3 domain and by autophosphorylation at two distinct regulatorytyrosines. J. Biol. Chem. 275, 35631-35637.
8. Bricogne G, Vonrhein C, Flensburg C, Schiltz M & Paciorek W (2003) Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2. 0. Acta Crystallogr. D Biol. Crystallogr. 59, 20232030.
9. Brunger AT (2007) Version 1. 2 of the Crystallography and NMR system. Nat Protoc 2, 27282733.
10. BrungerAT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T & Warren GL (1998) Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921.
11. Calleja V, Laguerre M, Parker PJ & Larijani B (2009) Role of a Novel PH-Kinase Domain Interface in PKB/Akt Regulation: Structural Mechanism forAllosteric Inhibition A. Toker, ed. PLoS Biol 7, e1000017.
12. Cambier JC, Bedzyk W, Campbell K, Chien N, Friedrich J, Harwood A, Jensen W, Pleiman C & Clark MR (1993) The B-cell antigen receptor: structure and function of primary, secondary, tertiary and quaternary components. Immunological Reviews 132, 85-106.
13. ChakrabortyA, Koldobskiy MA, Bello NT, Maxwell M, PotterJJ, Juluri KR, Maag D, Kim S, Huang AS, Dailey MJ, Saleh M, Snowman AM, Moran TH, Mezey E & Snyder SH (2010) Inositol Pyrophosphates Inhibit Akt Signaling, Thereby Regulating Insulin Sensitivity and Weight Gain. Cell 143, 897-910.
14. Chu DH, Morita CT & Weiss A (1998) The Syk family of protein tyrosine kinases in T-cell activation and development. Immunological Reviews 165, 167-180.
15. Cowtan KD & Main P (1993) Improvement of macromolecular electron-density maps by the simultaneous application of real and reciprocal space constraints. Acta Crystallogr. D Biol. Crystallogr. 49, 148-157.
16. Dal Porto JM, Gauld SB, Merrell KT, Mills D, Pugh-Bernard AE & Cambier J (2004) B cell antigen receptorsignaling 101. Molecular Immunology 41, 599-613.
17. De Braekeleer E, Douet-Guilbert N, Rowe D, Bown N, Morel F, Berthou C, Férec C&De Braekeleer M (2011) ABL1 fusion genes in hematological malignancies: a review. Eur. J. Haematol. 86, 361-371.
18. Di Paolo JA, Huang T, Balazs M, Barbosa J, Barck KH, Bravo BJ, Carano RAD, Darrow J, Davies DR, DeForge LE, Diehl L, Ferrando R, Gallion SL, Giannetti AM, Gribling P, Hurez V, Hymowitz SG, Jones R, KropfJE, Lee WP, Maciejewski PM, Mitchell SA, Rong H, Staker BL, Whitney JA, Yeh S, Young WB, Yu C, Zhang J, Reif K & Currie KS (2011) Specific Btk inhibition suppresses B cell-and myeloid cell-mediated arthritis. Nat. Chem. Biol. 7, 41-50.
19. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, Klebe G & Baker NA (2007) PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecularsimulations. Nucleic Acids Res. 35, W522-5.
20. Dolinsky TJ, Nielsen JE, McCammon JA & Baker NA (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32, W665-7.
21. Emsley P & Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
22. Eswar N, Webb B, Marti Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U & Sali A (2006) Comparative Protein Structure Modeling Using Modeller, Hoboken, NJ, USA: John Wiley & Sons, Inc.
23. Ferguson KM, Lemmon MA, SchlessingerJ & Sigler PB (1995) Structure ofthe high affinity complex of inositol trisphosphate with a phospholipase C pleckstrin homology domain. Cell 83, 1037-1046.
24. Filippakopoulos P, Kofler M, Hantschel O, Gish GD, Grebien F, Salah E, Neudecker P, Kay LE, Turk BE, Superti-Furga G, Pawson T & Knapp S (2008) Structural Coupling of SH2-Kinase Domains Links Fes and Abl Substrate Recognition and Kinase Activation. Cell 134, 793-803.
25. Gulik-Krzywicki T, Rivas E & Luzzati V (1967) Structure et polymorphisme des lipides: Étude par diffraction des rayons X du système formé de lipides de mitochondries de coeur de boeuf et d'Eau. J. Mol. Biol. 27, 303-322.
26. Hansson H, Mattsson PT, Allard P, Haapaniemi P, Vihinen M, Smith Cl & Hard T (1998) Solution structure of the SH3 domain from Bruton's tyrosine kinase. Biochemistry 37, 2912-2924.
27. Huang YH, Grasis JA, Miller AT, Xu R, Soonthornvacharin S, Andreotti AH, Tsoukas CD, Cooke MP & Sauer K (2007) Positive regulation of Itk PH domain function by soluble IP4. Science 316, 886-889.
28. Humphrey W, Dalke A & Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14, 33-8-27-8.
29. Hyvönen M & Saraste M (1997) Structure ofthe PH domain and Btk motiffrom Bruton's tyrosine kinase: molecular explanations for X-linked agammaglobulinaemia. The EMBO Journal 16, 3396-3404.
30. Hyvönen M, Macias MJ, Nilges M, Oschkinat H, Saraste M & Wilmanns M (1995) Structure of the binding site for inositol phosphates in a PH domain. The EMBO Journa A, 46764685.
31. Irvine RF & Schell MJ (2001) Back in the water: the return of the inositol phosphates. Nat Rev Mol Cell Biol 2, 327-338.
32. Jefferies CA, Doyle S, Brunner C, Dunne A, Brint E, Wietek C, Walch E, Wirth T & O'Neill LAJ (2002) Bruton's Tyrosine Kinase Is a Toll/Interleukin-1 Receptor Domain-binding Protein That Participates in Nuclear Factor kB Activation by Toll-like Receptor 4. J. Biol. Chem. 278, 26258-26264.
33. Jones TA, Zou JY, Cowan SW & Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., A, Found. Crystallogr. 47(Pt2), 110-119.
34. Joseph RE, Kleino I, Wales TE, Xie Q, Fulton DB, Engen JR, Berg LJ & Andreotti AH (2013) Activation loop dynamics determine the different catalytic efficiencies of B cell-and T cell-specific tec kinases. Sci Signal 6, ra76-ra76.
35. Kawakami Y, Yao L, Miura T, Tsukada S, Witte ON & Kawakami T (1994) Tyrosine phosphorylation and activation of Bruton tyrosine kinase upon Fc epsilon Rl cross-linking. Mol. Cell. Biol. 14, 5108-5113.
36. Kurosaki T (2011) Regulation of BCR signaling. Molecular Immunology 48, 1287-1291.
37. Laederach A, Cradic KW, Brazin KN, Zamoon J, Fulton DB, Huang X-Y & Andreotti AH (2002) Competing modes of self-association in the regulatory domains of Bruton's tyrosine kinase: Intramolecular contact versus asymmetric homodimerization. Protein Science 11, 36-57.
38. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ & Higgins DG (2007) Clustal W and Clustal X version 2. 0. Bioinformatics 23, 2947-2948.
39. Lee W-K, Son SH, Jin B-S, Na J-H, Kim S-Y, Kim K-H, Kim EE, Yu YG & Lee HH (2013) Structural and functional insights into the regulation mechanism of CK2 by IP6 and the intrinsically disordered protein Nopp140. Proc. Natl. Acad. Sci. U. S. A. 110, 19360-19365.
40. Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9, 99-111.
41. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dror RO & Shaw DE (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins: Structure, Function, and Bioinformatics 78, 1950-1958.
42. Lindvall JM, Blomberg KEM, Väliaho J, Vargas L, Heinonen JE, BerglöfA, Mohamed AJ, Nore BF, Vihinen M & Smith CIE (2005) Bruton's tyrosine kinase: cell biology, sequence conservation, mutation spectrum, siRNA modifications, and expression profiling. Immunological Reviews 203, 200-215.
43. Maignan S, Guilloteau JP, Fromage N &Arnoux B (1995) Crystal structure ofthe mammalian Grb2 adaptor. Science 268, 291-293.
44. Marquez JA, Smith CIE, Petoukhov MV, Surdo PL, Mattsson PT, Knekt M, Westlund A, Scheffzek K, Saraste M & Svergun Dl (2003) Conformation of full-length Bruton tyrosine kinase (Btk) from synchrotron X-ray solution scattering. The EMBO Journal 22, 46164624.
45. Middendorp S, Dingjan GM, Maas A, Dahlenborg K & Hendriks RW (2003) Function of Bruton's tyrosine kinase during B cell development is partially independent of its catalytic activity. J Immunol 171, 5988-5996.
46. Millard CJ, Watson PJ, Celardo I, Gordiyenko Y, Cowley SM, Robinson CV, Fairall L & Schwabe JWR (2013) Class I HDACs share a common mechanism of regulation by inositol phosphates. Molecular Cell 51, 57-67.
47. Moarefi I, LaFevre-Bernt M, Sicheri F, Huse M, Lee C-H, Kuriyan J & MillerWT (1997) Activation ofthe Sire-family tyrosine kinase Hck by SH3 domain displacement., Published online: 13 February 1997; doi: 10. 1038/385650a0 385, 650-653.
48. Morrogh LM, Hinshelwood S, Costello P, Cory GOC & Kinnon C (1999) The SH3 domain of Bruton's tyrosine kinase displays altered ligand binding properties when auto-phosphorylated in vitro. Eur. J. Immunol 29, 2269-2279.
49. Mócsai A, Ruland J & Tybulewicz V (2010) The SYK tyrosine kinase: a crucial player in diverse biological functions. Nature Reviews Immunology 10, 387-402.
50. Mukherjee S, Zhu J, Zikherman J, Parameswaran R, KadlecekTA, Wang Q, Au-Yeung B, Ploegh H, Kuriyan J, Das J & Weiss A (2013) Monovalent and multivalent ligation ofthe B cell receptor exhibit differential dependence upon Syk and Src family kinases. Sci Signal 6, ra1-ra1.
51. Nagar B, Hantschel O, Seeliger M, Davies JM, Weis Wl, Superti-Furga G & Kuriyan J (2006) Organization ofthe SH3-SH2 Unit in Active and Inactive Forms ofthe c-Abl Tyrosine Kinase. Molecular Cell 21, 787-798.
52. Nagar B, Hantschel O, Young MA, Scheffzek K, Veach D, Bornmann W, Clarkson B, Superti-Furga G & Kuriyan J (2003) Structural Basis for the Autoinhibition of c-Abl Tyrosine Kinase. Cell 112, 859-871.
53. Ozkirimli E & Post CB (2006) Src kinase activation: A switched electrostatic network. Protein Sci. 15, 1051-1062.
54. Park H, Wahl Ml, Afar DEH, Turck CW, Rawlings DJ, Tam C, Scharenberg AM, Kinet J-P & Witte ON (1996) Regulation of Btk Function by a MajorAutophosphorylation Site Within the SH3 Domain. Immunity 4, 515-525.
55. Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, Shirts MR, Smith JC, Kasson PM, van der Spoel D, Hess B & Lindahl E (2013) GROMACS 4. 5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29, 845-854.
56. Rawlings DJ, Scharenberg AM, Park H, Wahl Ml, Lin S, Kato RM, FluckigerA-C, Witte ON & Kinet J-P (1996) Activation of BTK by a Phosphorylation Mechanism Initiated by SRC Family Kinases. Science 271, 822-825.
57. Read RJ (1986) Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr., A, Found. Crystallogr. 42, 140-149.
58. Robert X & Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320-4.
59. Schiering N, Casale E, Caccia P, Giordano P & Battistini C (2000) Dimer Formation through Domain Swapping in the Crystal Structure ofthe Grb2-SH2-Ac-pYVNV Complex ¢. Biochemistry 39, 13376-13382.
60. Seeliger MA, Young M, Henderson MN, Pellicena P, King DS, FalickAM & Kuriyan J (2005) High yield bacterial expression of active c-Abl and c-Src tyrosine kinases. Protein Sci. 14, 3135-3139.
61. Shears SB (2001)Assessing the omnipotence of inositol hexakisphosphate. Cellular Signalling 13, 151-158.
62. Sicheri F, Moarefi I & Kuriyan J (1997) Crystal structure ofthe Srcfamily tyrosine kinase Hck. Nature 385, 602-609.
63. Sondhi D & Cole PA (1999) Domain Interactions in Protein Tyrosine Kinase Csk f. Biochemistry 38, 11147-11155.
64. 31P NMR. Biochem. Biophys. Res. Commun. 149, 874881.
65. Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M & Zheng N (2006) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645.
66. Taylor SS & Kornev AP (2011) Protein kinases: evolution of dynamic regulatory proteins. Trends in Biochemical Sciences 36, 65-77.
67. Tsukada S, Saffran DC, Rawlings DJ, Parolini O, Allen RC, Klisak I, Sparkes RS, Kubagawa H, Mohandas T & Quan S (1993) Deficient expression ofaB cell cytoplasmictyrosine kinase in human X-linked agammaglobulinemia. Cell 72, 279-290.
68. Tsukada S, Simon Ml, Witte ON & Katz A (1994) Binding of beta gamma subunits of heterotrimeric G proteins to the PH domain of Bruton tyrosine kinase. Proc. Natl. Acad. Sci. U. S. A 91, 11256-11260.
69. Tzeng SR, Lou YC, Pai MT, Jain ML & Cheng JW (2000) Solution structure of the human BTK SH3 domain complexed with a proline-rich peptide from p120cbl. J. Biomol. NMR 16, 303312.
70. Vallejo M, Jackson T, Lightman S & Hanley MR (1987) Occurrence and extracellular actions of inositol pentakis-and hexakisphosphate in mammalian brain. Nature 330, 656-658.
71. Wang H, Kadlecek TA, Au-Yeung BB, Goodfellow HES, Hsu L-Y, Freedman TS & Weiss A (2010) ZAP-70: an essential kinase in T-cell signaling. Cold Spring Harb Perspect Biol 2, a002279-a002279.
72. Watson PJ, Fairall L, Santos GM & Schwabe JWR (2012) Structure of HDAC3 bound to corepressor and inositol tetraphosphate. Nature 481, 335-340.
73. Weiss A & Littman DR (1994) Signal transduction by lymphocyte antigen receptors. Cell 76, 263-274.
74. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoyA, McNicholas SJ, MurshudovGN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A & Wilson KS (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242.
75. Wu W-l, Voegtli WC, Sturgis HL, Dizon FP, Vigers GPA & Brandhuber BJ (2010) Crystal Structure of Human AKT1 with an Allosteric Inhibitor Reveals a New Mode of Kinase Inhibition J. A. Gerrard, ed. PLoS ONE 5, e12913.
76. Xu W, Harrison SC & Eck MJ (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602.
77. Yamaguchi H & Hendrickson WA (1996) Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384, 484-489.
78. York JD, Odom AR, Murphy R, Ives EB & Wente SR (1999) A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 285, 96-100.