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The solution structure and intramolecular associations of the Tec kinase SRC homology 3 domain.

Pursglove SE, Mulhern TD, Mackay JP, Hinds MG, Booker GW
J Biol Chem 277 755-62 (2002)
Cited: 23 times
EuropePMC logo PMID: 11684687

Abstract

Tec is the prototypic member of a family of intracellular tyrosine kinases that includes Txk, Bmx, Itk, and Btk. Tec family kinases share similarities in domain structure with Src family kinases, but one of the features that differentiates them is a proline-rich region (PRR) preceding their Src homology (SH) 3 domain. Evidence that the PRR of Itk can bind in an intramolecular fashion to its SH3 domain and the lack of a regulatory tyrosine in the C terminus indicates that Tec kinases must be regulated by a different set of intramolecular interactions to the Src kinases. We have determined the solution structure of the Tec SH3 domain and have investigated interactions with its PRR, which contains two SH3-binding sites. We demonstrate that in vitro, the Tec PRR can bind in an intramolecular fashion to the SH3. However, the affinity is lower than that for dimerization via reciprocal PRR-SH3 association. Using site-directed mutagenesis we show that both sites can bind the Tec SH3 domain; site 1 (155KTLPPAP161) binds intramolecularly, while site 2 (165KRRPPPPIPP174) cannot and binds in an intermolecular fashion. These distinct roles for the SH3 binding sites in Tec family kinases could be important for protein targeting and enzyme activation.

Articles - 1gl5 mentioned but not cited (5)

  1. Identifying unexpected therapeutic targets via chemical-protein interactome. Yang L, Chen J, Shi L, Hudock MP, Wang K, He L. PLoS One 5 e9568 (2010)
  2. Conformational snapshots of Tec kinases during signaling. Joseph RE, Andreotti AH. Immunol. Rev. 228 74-92 (2009)
  3. The accessory factor Nef links HIV-1 to Tec/Btk kinases in an Src homology 3 domain-dependent manner. Tarafdar S, Poe JA, Smithgall TE. J. Biol. Chem. 289 15718-15728 (2014)
  4. Conserved patterns and interactions in the unfolding transition state across SH3 domain structural homologues. Demakis C, Childers MC, Daggett V. Protein Sci 30 391-407 (2021)
  5. 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)


Reviews citing this publication (6)

  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 Src, Syk, and Tec family kinases: distinct types of molecular switches. Bradshaw JM. Cell. Signal. 22 1175-1184 (2010)
  3. T-cell signaling regulated by the Tec family kinase, Itk. Andreotti AH, Schwartzberg PL, Joseph RE, Berg LJ. Cold Spring Harb Perspect Biol 2 a002287 (2010)
  4. New insights into the regulation and functions of Tec family tyrosine kinases in the immune system. Miller AT, Berg LJ. Curr. Opin. Immunol. 14 331-340 (2002)
  5. A survey of the year 2002 commercial optical biosensor literature. Rich RL, Myszka DG. J. Mol. Recognit. 16 351-382 (2003)
  6. New ways to skin a kap: mechanisms for controlling nuclear transport. Lusk CP, Makhnevych T, Wozniak RW. Biochem. Cell Biol. 82 618-625 (2004)

Articles citing this publication (12)

  1. Etk/Bmx as a tumor necrosis factor receptor type 2-specific kinase: role in endothelial cell migration and angiogenesis. Pan S, An P, Zhang R, He X, Yin G, Min W. Mol. Cell. Biol. 22 7512-7523 (2002)
  2. Crystal structures of interleukin-2 tyrosine kinase and their implications for the design of selective inhibitors. Brown K, Long JM, Vial SC, Dedi N, Dunster NJ, Renwick SB, Tanner AJ, Frantz JD, Fleming MA, Cheetham GM. J. Biol. Chem. 279 18727-18732 (2004)
  3. The structure of a tandem pair of spectrin repeats of plectin reveals a modular organization of the plakin domain. Sonnenberg A, Rojas AM, de Pereda JM. J. Mol. Biol. 368 1379-1391 (2007)
  4. Btk is required for an efficient response to erythropoietin and for SCF-controlled protection against TRAIL in erythroid progenitors. Schmidt U, van den Akker E, Parren-van Amelsvoort M, Litos G, de Bruijn M, Gutiérrez L, Hendriks RW, Ellmeier W, Löwenberg B, Beug H, von Lindern M. J. Exp. Med. 199 785-795 (2004)
  5. Regulation of RhoGEF activity by intramolecular and intermolecular SH3 domain interactions. Schiller MR, Chakrabarti K, King GF, Schiller NI, Eipper BA, Maciejewski MW. J Biol Chem 281 18774-18786 (2006)
  6. 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)
  7. Quantitative relation between intermolecular and intramolecular binding of pro-rich peptides to SH3 domains. Zhou HX. Biophys. J. 91 3170-3181 (2006)
  8. Determinants of intra versus intermolecular self-association within the regulatory domains of Rlk and Itk. Laederach A, Cradic KW, Fulton DB, Andreotti AH. J. Mol. Biol. 329 1011-1020 (2003)
  9. Mechanism and functional significance of Itk autophosphorylation. Joseph RE, Fulton DB, Andreotti AH. J. Mol. Biol. 373 1281-1292 (2007)
  10. Tyrosine kinase BMX phosphorylates phosphotyrosine-primed motif mediating the activation of multiple receptor tyrosine kinases. Chen S, Jiang X, Gewinner CA, Asara JM, Simon NI, Cai C, Cantley LC, Balk SP. Sci Signal 6 ra40 (2013)
  11. Disrupting the intermolecular self-association of Itk enhances T cell signaling. Min L, Wu W, Joseph RE, Fulton DB, Berg L, Andreotti AH. J. Immunol. 184 4228-4235 (2010)
  12. Folding of the alphaII-spectrin SH3 domain under physiological salt conditions. Petzold K, Ohman A, Backman L. Arch. Biochem. Biophys. 474 39-47 (2008)


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