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Solution structure of the SH3 domain from Bruton's tyrosine kinase.

Hansson H, Mattsson PT, Allard P, Haapaniemi P, Vihinen M, Smith CI, Hard T
Biochemistry 37 2912-24 (1998)
Cited: 39 times
EuropePMC logo PMID: 9485443

Abstract

X-linked agammaglobulinemia (XLA) is a heritable immunodeficiency caused by mutations in the gene coding for Bruton's tyrosine kinase (Btk). Btk belongs to the Tec family of tyrosine kinases. Each member of the family contains five regions and mutations causing XLA have been isolated in all five regions. We have determined the solution structure of the Src homology 3 (SH3) domain of Btk using two- and three-dimensional nuclear magnetic resonance (NMR) spectroscopy on natural abundance and 15N-labeled protein material. The structure determination is complemented by investigation of backbone dynamics based on 15N NMR relaxation. The Btk SH3 forms a well-defined structure and shows the typical SH3 topology of two short antiparallel beta-sheets packed almost perpendicular to each other in a sandwich-like fold. The N- and C-termini are more flexible as are peptide fragments in the RT and n-Src loops. The studied Btk SH3 fragment adopts two slowly interconverting conformations with a relative concentration ratio of 7:1. The overall fold of the minor form is similar to that of the major form, as judged on the basis of observed NOE connectivities and small chemical shift differences. A tryptophan (W251) ring flip is the favored mechanism for interconversion, although other possibilities cannot be excluded. The side chain of Y223, which becomes autophosphorylated upon activation of Btk, is exposed within the potential SH3 ligand binding site. Finally, we compare the present Btk SH3 structure with other SH3 structures.

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Reviews citing this publication (9)

  1. Tec family kinases in T lymphocyte development and function. Berg LJ, Finkelstein LD, Lucas JA, Schwartzberg PL. Annu Rev Immunol 23 549-600 (2005)
  2. The Tec family of cytoplasmic tyrosine kinases: mammalian Btk, Bmx, Itk, Tec, Txk and homologs in other species. Smith CI, Islam TC, Mattsson PT, Mohamed AJ, Nore BF, Vihinen M. Bioessays 23 436-446 (2001)
  3. The Src, Syk, and Tec family kinases: distinct types of molecular switches. Bradshaw JM. Cell Signal 22 1175-1184 (2010)
  4. Bruton's tyrosine kinase: cell biology, sequence conservation, mutation spectrum, siRNA modifications, and expression profiling. Lindvall JM, Blomberg KE, Väliaho J, Vargas L, Heinonen JE, Berglöf A, Mohamed AJ, Nore BF, Vihinen M, Smith CI. Immunol Rev 203 200-215 (2005)
  5. BTKbase: the mutation database for X-linked agammaglobulinemia. Väliaho J, Smith CI, Vihinen M. Hum Mutat 27 1209-1217 (2006)
  6. Bruton's tyrosine kinase--an integral protein of B cell development that also has an essential role in the innate immune system. López-Herrera G, Vargas-Hernández A, González-Serrano ME, Berrón-Ruiz L, Rodríguez-Alba JC, Espinosa-Rosales F, Santos-Argumedo L. J Leukoc Biol 95 243-250 (2014)
  7. TEC family kinases in health and disease--loss-of-function of BTK and ITK and the gain-of-function fusions ITK-SYK and BTK-SYK. Hussain A, Yu L, Faryal R, Mohammad DK, Mohamed AJ, Smith CI. FEBS J 278 2001-2010 (2011)
  8. X-linked agammaglobulinemia: lack of mature B lineage cells caused by mutations in the Btk kinase. Smith CI, Bäckesjö CM, Berglöf A, Brandén LJ, Islam T, Mattsson PT, Mohamed AJ, Müller S, Nore B, Vihinen M. Springer Semin Immunopathol 19 369-381 (1998)
  9. A Systematic Compilation of Human SH3 Domains: A Versatile Superfamily in Cellular Signaling. Mehrabipour M, Jasemi NSK, Dvorsky R, Ahmadian MR. Cells 12 2054 (2023)

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  1. The role of backbone motions in ligand binding to the c-Src SH3 domain. Wang C, Pawley NH, Nicholson LK. J Mol Biol 313 873-887 (2001)
  2. Mutations of the human BTK gene coding for bruton tyrosine kinase in X-linked agammaglobulinemia. Vihinen M, Kwan SP, Lester T, Ochs HD, Resnick I, Väliaho J, Conley ME, Smith CI. Hum Mutat 13 280-285 (1999)
  3. Conformation of full-length Bruton tyrosine kinase (Btk) from synchrotron X-ray solution scattering. Márquez JA, Smith CI, Petoukhov MV, Lo Surdo P, Mattsson PT, Knekt M, Westlund A, Scheffzek K, Saraste M, Svergun DI. EMBO J 22 4616-4624 (2003)
  4. Partial unfolding of diverse SH3 domains on a wide timescale. Wales TE, Engen JR. J Mol Biol 357 1592-1604 (2006)
  5. Autoinhibition of Bruton's tyrosine kinase (Btk) and activation by soluble inositol hexakisphosphate. Wang Q, Vogan EM, Nocka LM, Rosen CE, Zorn JA, Harrison SC, Kuriyan J. Elife 4 (2015)
  6. Effect of pH and salt bridges on structural assembly: molecular structures of the monomer and intertwined dimer of the Eps8 SH3 domain. Kishan KV, Newcomer ME, Rhodes TH, Guilliot SD. Protein Sci 10 1046-1055 (2001)
  7. Ligand-induced changes in dynamics in the RT loop of the C-terminal SH3 domain of Sem-5 indicate cooperative conformational coupling. Ferreon JC, Hilser VJ. Protein Sci 12 982-996 (2003)
  8. Intermolecular interactions between the SH3 domain and the proline-rich TH region of Bruton's tyrosine kinase. Hansson H, Okoh MP, Smith CI, Vihinen M, Härd T. FEBS Lett 489 67-70 (2001)
  9. Proline isomerization preorganizes the Itk SH2 domain for binding to the Itk SH3 domain. Severin A, Joseph RE, Boyken S, Fulton DB, Andreotti AH. J Mol Biol 387 726-743 (2009)
  10. Competing modes of self-association in the regulatory domains of Bruton's tyrosine kinase: intramolecular contact versus asymmetric homodimerization. Laederach A, Cradic KW, Brazin KN, Zamoon J, Fulton DB, Huang XY, Andreotti AH. Protein Sci 11 36-45 (2002)
  11. Mechanism and functional significance of Itk autophosphorylation. Joseph RE, Fulton DB, Andreotti AH. J Mol Biol 373 1281-1292 (2007)
  12. Stability and peptide binding specificity of Btk SH2 domain: molecular basis for X-linked agammaglobulinemia. Tzeng SR, Pai MT, Lung FD, Wu CW, Roller PP, Lei B, Wei CJ, Tu SC, Chen SH, Soong WJ, Cheng JW. Protein Sci 9 2377-2385 (2000)
  13. The response of internal dynamics to hydrophobic core mutations in the SH3 domain from the Fyn tyrosine kinase. Mittermaier A, Kay LE. Protein Sci 13 1088-1099 (2004)
  14. Phosphorylation of Bruton's tyrosine kinase by c-Abl. Bäckesjö CM, Vargas L, Superti-Furga G, Smith CI. Biochem Biophys Res Commun 299 510-515 (2002)
  15. Achieving a Graded Immune Response: BTK Adopts a Range of Active/Inactive Conformations Dictated by Multiple Interdomain Contacts. Joseph RE, Wales TE, Fulton DB, Engen JR, Andreotti AH. Structure 25 1481-1494.e4 (2017)
  16. Multidomain Control Over TEC Kinase Activation State Tunes the T Cell Response. Andreotti AH, Joseph RE, Conley JM, Iwasa J, Berg LJ. Annu Rev Immunol 36 549-578 (2018)
  17. Conformational snapshots of Tec kinases during signaling. Joseph RE, Andreotti AH. Immunol Rev 228 74-92 (2009)
  18. Regulation of nucleocytoplasmic shuttling of Bruton's tyrosine kinase (Btk) through a novel SH3-dependent interaction with ankyrin repeat domain 54 (ANKRD54). Gustafsson MO, Hussain A, Mohammad DK, Mohamed AJ, Nguyen V, Metalnikov P, Colwill K, Pawson T, Smith CI, Nore BF. Mol Cell Biol 32 2440-2453 (2012)
  19. Solution structure of the human BTK SH3 domain complexed with a proline-rich peptide from p120cbl. Tzeng SR, Lou YC, Pai MT, Jain ML, Cheng JW. J Biomol NMR 16 303-312 (2000)
  20. Backbone dynamics of the human MIA protein studied by (15)N NMR relaxation: implications for extended interactions of SH3 domains. Stoll R, Renner C, Buettner R, Voelter W, Bosserhoff AK, Holak TA. Protein Sci 12 510-519 (2003)
  21. Interaction between Btk TH and SH3 domain. Okoh MP, Vihinen M. Biopolymers 63 325-334 (2002)
  22. Letter Identification of novel non-pathogenic mutation in SH3 domain of Btk in an XLA patient. Pérez de Diego R, Bravo J, Allende LM, López-Granados E, Rivera J, Ferreira A, Fontán G, García Rodríguez MC. Mol Immunol 45 301-303 (2008)
  23. Murine Itk SH3 domain. Severin A, Fulton DB, Andreotti AH. J Biomol NMR 40 285-290 (2008)
  24. Both proline-rich sequences in the TH region of Bruton's tyrosine kinase stabilize intermolecular interactions with the SH3 domain. Hansson H, Smith CI, Härd T. FEBS Lett 508 11-15 (2001)
  25. Dynamics of the Tec-family tyrosine kinase SH3 domains. Roberts JM, Tarafdar S, Joseph RE, Andreotti AH, Smithgall TE, Engen JR, Wales TE. Protein Sci 25 852-864 (2016)
  26. Rational design and purification of human Bruton's tyrosine kinase SH3-SH2 protein for structure-function studies. Nera KP, Brockmann E, Vihinen M, Smith CI, Mattsson PT. Protein Expr Purif 20 365-371 (2000)
  27. Consequences of two naturally occurring missense mutations in the structure and function of Bruton agammaglobulinemia tyrosine kinase. Vargas-Hernández A, López-Herrera G, Maravillas-Montero JL, Vences-Catalán F, Mogica-Martínez D, Rojo-Domínguez A, Espinosa-Rosales FJ, Santos-Argumedo L. IUBMB Life 64 346-353 (2012)
  28. Observing enzyme ternary transition state analogue complexes by 19F NMR spectroscopy. Ampaw A, Carroll M, von Velsen J, Bhattasali D, Cohen A, Bowler MW, Jakeman DL. Chem Sci 8 8427-8434 (2017)


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