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Structural basis for recognition of the T cell adaptor protein SLP-76 by the SH3 domain of phospholipase Cgamma1.

Deng L, Velikovsky CA, Swaminathan CP, Cho S, Mariuzza RA
J Mol Biol 352 1-10 (2005)
Cited: 20 times
EuropePMC logo PMID: 16061254

Abstract

The enzyme phospholipase Cgamma1 (PLCgamma1) is essential for T cell signaling and activation. Following T cell receptor ligation, PLCgamma1 interacts through its SH2 and SH3 domains with the adaptors LAT and SLP-76, respectively, to form a multiprotein signaling complex that leads to activation of PLCgamma1 by Syk tyrosine kinases. To identify the binding site for PLCgamma1 in SLP-76, we used isothermal titration calorimetry to measure affinities for the interaction of PLCgamma1-SH3 with a set of overlapping peptides spanning the central proline-rich region of SLP-76. PLCgamma1-SH3 bound with high specificity to the SLP-76 motif 186PPVPPQRP193, which represents the minimal binding site. To understand the basis for selective recognition, we determined the crystal structures of PLCgamma1-SH3 in free form, and bound to a 10-mer peptide containing this site, to resolutions of 1.60 A and 1.81 A, respectively. The structures reveal that several key contacting residues of the SH3 shift toward the SLP-76 peptide upon complex formation, optimizing the fit and strengthening hydrophobic interactions. Selectivity results mainly from strict shape complementarity between protein and peptide, rather than sequence-specific hydrogen bonding. In addition, Pro193 of SLP-76 assists in positioning Arg192 into the compass pocket of PLCgamma1-SH3, which coordinates the compass residue through an unusual aspartate. The PLCgamma1-SH3/SLP-76 structure provides insights into ligand binding by SH3 domains related to PLCgamma1-SH3, as well as into recognition by PLCgamma1 of signaling partners other than SLP-76.

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  7. Structural basis for recognition of the T cell adaptor protein SLP-76 by the SH3 domain of phospholipase Cgamma1. Deng L, Velikovsky CA, Swaminathan CP, Cho S, Mariuzza RA. J Mol Biol 352 1-10 (2005)
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Reviews citing this publication (2)

  1. Survey of the year 2005: literature on applications of isothermal titration calorimetry. Ababou A, Ladbury JE. J Mol Recognit 20 4-14 (2007)
  2. Keeping the (kinase) party going: SLP-76 and ITK dance to the beat. Qi Q, August A. Sci STKE 2007 pe39 (2007)

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  1. Structural basis for the activation of PLC-γ isozymes by phosphorylation and cancer-associated mutations. Hajicek N, Keith NC, Siraliev-Perez E, Temple BR, Huang W, Zhang Q, Harden TK, Sondek J. Elife 8 e51700 (2019)
  2. PLCγ1 promotes phase separation of T cell signaling components. Zeng L, Palaia I, Šarić A, Su X. J Cell Biol 220 e202009154 (2021)
  3. Scaffold Protein SLP-76 Primes PLCγ1 for Activation by ITK-Mediated Phosphorylation. Devkota S, Joseph RE, Min L, Bruce Fulton D, Andreotti AH. J Mol Biol 427 2734-2747 (2015)
  4. Disrupting the CD95-PLCγ1 interaction prevents Th17-driven inflammation. Poissonnier A, Guégan JP, Nguyen HT, Best D, Levoin N, Kozlov G, Gehring K, Pineau R, Jouan F, Morere L, Martin S, Thomas M, Lazaro E, Douchet I, Ducret T, van de Weghe P, Blanco P, Jean M, Vacher P, Legembre P. Nat Chem Biol 14 1079-1089 (2018)
  5. Molecular mechanisms underlying the evolution of the slp76 signalosome. Qu X, Lan X, Deng C, Zhou J, Du J, Huang S, Li Y. Sci Rep 7 1509 (2017)
  6. Understanding signal integration through targeted mutations of an adapter protein. Zou T, May RM, Koretzky GA. FEBS Lett 584 4901-4909 (2010)
  7. Recruitment of phospholipase Cγ1 to the non-structural membrane protein pK15 of Kaposi Sarcoma-associated herpesvirus promotes its Src-dependent phosphorylation. Samarina N, Ssebyatika G, Tikla T, Waldmann JY, Abere B, Nanna V, Marasco M, Carlomagno T, Krey T, Schulz TF. PLoS Pathog 17 e1009635 (2021)
  8. Crystal Structure of the SH3 Domain of ASAP1 in Complex with the Proline Rich Motif (PRM) of MICAL1 Reveals a Unique SH3/PRM Interaction Mode. Jia X, Lin L, Xu S, Li L, Wei Z, Yu C, Niu F. Int J Mol Sci 24 1414 (2023)


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