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A novel, specific interaction involving the Csk SH3 domain and its natural ligand.

Ghose R, Shekhtman A, Goger MJ, Ji H, Cowburn D
Nat Struct Biol 8 998-1004 (2001)
Cited: 93 times
EuropePMC logo PMID: 11685249

Abstract

C-terminal Src kinase (Csk) takes part in a highly specific, high affinity interaction via its Src homology 3 (SH3) domain with the proline-enriched tyrosine phosphatase PEP in hematopoietic cells. The solution structure of the Csk-SH3 domain in complex with a 25-residue peptide from the Pro/Glu/Ser/Thr-rich (PEST) domain of PEP reveals the basis for this specific peptide recognition motif involving an SH3 domain. Three residues, Ala 40, Thr 42 and Lys 43, in the SH3 domain of Csk specifically recognize two hydrophobic residues, Ile 625 and Val 626, in the proline-rich sequence of the PEST domain of PEP. These two residues are C-terminal to the conventional proline-rich SH3 domain recognition sequence of PEP. This interaction is required in addition to the classic polyproline helix (PPII) recognition by the Csk-SH3 domain for the association between Csk and PEP in vivo. NMR relaxation analysis suggests that Csk-SH3 has different dynamic properties in the various subsites important for peptide recognition.

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  1. Diverse recognition of non-PxxP peptide ligands by the SH3 domains from p67(phox), Grb2 and Pex13p. Kami K, Takeya R, Sumimoto H, Kohda D. EMBO J 21 4268-4276 (2002)
  2. Genetic Basis of Common Human Disease: Insight into the Role of Missense SNPs from Genome-Wide Association Studies. Pal LR, Moult J. J Mol Biol 427 2271-2289 (2015)
  3. Structural, functional, and bioinformatic studies demonstrate the crucial role of an extended peptide binding site for the SH3 domain of yeast Abp1p. Stollar EJ, Garcia B, Chong PA, Rath A, Lin H, Forman-Kay JD, Davidson AR. J Biol Chem 284 26918-26927 (2009)
  4. The tyrosine kinase Csk dimerizes through Its SH3 domain. Levinson NM, Visperas PR, Kuriyan J. PLoS One 4 e7683 (2009)
  5. The autoimmunity risk variant LYP-W620 cooperates with CSK in the regulation of TCR signaling. de la Puerta ML, Trinidad AG, Rodríguez Mdel C, de Pereda JM, Sánchez Crespo M, Bayón Y, Alonso A. PLoS One 8 e54569 (2013)
  6. Structural determination of biomolecular interfaces by nuclear magnetic resonance of proteins with reduced proton density. Ferrage F, Dutta K, Shekhtman A, Cowburn D. J Biomol NMR 47 41-54 (2010)
  7. The Binding of Syndapin SH3 Domain to Dynamin Proline-rich Domain Involves Short and Long Distance Elements. Luo L, Xue J, Kwan A, Gamsjaeger R, Wielens J, von Kleist L, Cubeddu L, Guo Z, Stow JL, Parker MW, Mackay JP, Robinson PJ. J Biol Chem 291 9411-9424 (2016)
  8. Combining biophysical methods to analyze the disulfide bond in SH2 domain of C-terminal Src kinase. Liu D, Cowburn D. Biophys Rep 2 33-43 (2016)
  9. Identification of Hydrophobic Interfaces in Protein-Ligand Complexes by Selective Saturation Transfer NMR Spectroscopy. Ferrage F, Dutta K, Cowburn D. Molecules 20 21992-21999 (2015)
  10. SH3-domain mutations selectively disrupt Csk homodimerization or PTPN22 binding. Brian BF, Sjaastad FV, Freedman TS. Sci Rep 12 5875 (2022)


Reviews citing this publication (23)

  1. Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Li SS. Biochem J 390 641-653 (2005)
  2. Role of PTPN22 in type 1 diabetes and other autoimmune diseases. Bottini N, Vang T, Cucca F, Mustelin T. Semin Immunol 18 207-213 (2006)
  3. Structural systems biology: modelling protein interactions. Aloy P, Russell RB, Russell RB. Nat Rev Mol Cell Biol 7 188-197 (2006)
  4. Protein tyrosine phosphatases in lymphocyte activation and autoimmunity. Rhee I, Veillette A. Nat Immunol 13 439-447 (2012)
  5. Recognition of proline-rich motifs by protein-protein-interaction domains. Ball LJ, Kühne R, Schneider-Mergener J, Oschkinat H. Angew Chem Int Ed Engl 44 2852-2869 (2005)
  6. SH3 domain ligand binding: What's the consensus and where's the specificity? Saksela K, Permi P. FEBS Lett 586 2609-2614 (2012)
  7. Protein tyrosine phosphatases as potential therapeutic targets. He RJ, Yu ZH, Zhang RY, Zhang ZY. Acta Pharmacol Sin 35 1227-1246 (2014)
  8. Protein tyrosine phosphatase PTPN22 in human autoimmunity. Vang T, Miletic AV, Bottini N, Mustelin T. Autoimmunity 40 453-461 (2007)
  9. Protein tyrosine phosphatases in autoimmunity. Vang T, Miletic AV, Arimura Y, Tautz L, Rickert RC, Mustelin T. Annu Rev Immunol 26 29-55 (2008)
  10. PEST family phosphatases in immunity, autoimmunity, and autoinflammatory disorders. Veillette A, Rhee I, Souza CM, Davidson D. Immunol Rev 228 312-324 (2009)
  11. SH3 domains: modules of protein-protein interactions. Kurochkina N, Guha U. Biophys Rev 5 29-39 (2013)
  12. Regulation of TCR signalling by tyrosine phosphatases: from immune homeostasis to autoimmunity. Stanford SM, Rapini N, Bottini N. Immunology 137 1-19 (2012)
  13. Redox circuitries driving Src regulation. Giannoni E, Chiarugi P. Antioxid Redox Signal 20 2011-2025 (2014)
  14. Lymphoid tyrosine phosphatase and autoimmunity: human genetics rediscovers tyrosine phosphatases. Stanford SM, Mustelin TM, Bottini N. Semin Immunopathol 32 127-136 (2010)
  15. The putative role of the C1858T polymorphism of protein tyrosine phosphatase PTPN22 gene in autoimmunity. Gianchecchi E, Palombi M, Fierabracci A. Autoimmun Rev 12 717-725 (2013)
  16. The application of modular protein domains in proteomics. Jadwin JA, Ogiue-Ikeda M, Machida K. FEBS Lett 586 2586-2596 (2012)
  17. Interfacial water molecules in SH3 interactions: Getting the full picture on polyproline recognition by protein-protein interaction domains. Zafra-Ruano A, Luque I. FEBS Lett 586 2619-2630 (2012)
  18. High affinity molecules disrupting GRB2 protein complexes as a therapeutic strategy for chronic myelogenous leukaemia. Feller SM, Tuchscherer G, Voss J. Leuk Lymphoma 44 411-427 (2003)
  19. Dynamic proteomics in modeling of the living cell. Protein-protein interactions. Terentiev AA, Moldogazieva NT, Shaitan KV. Biochemistry (Mosc) 74 1586-1607 (2009)
  20. Two Sides of the Coin: Ezrin/Radixin/Moesin and Merlin Control Membrane Structure and Contact Inhibition. Michie KA, Bermeister A, Robertson NO, Goodchild SC, Curmi PMG. Int J Mol Sci 20 (2019)
  21. Protein Tyrosine Phosphatases: Regulators of CD4 T Cells in Inflammatory Bowel Disease. Pike KA, Tremblay ML. Front Immunol 9 2504 (2018)
  22. Dissection of the catalytic and regulatory structure-function relationships of Csk protein tyrosine kinase. Sun G, Ayrapetov MK. Front Cell Dev Biol 11 1148352 (2023)
  23. Regulation, targets and functions of CSK. Zhu S, Wang H, Ranjan K, Zhang D. Front Cell Dev Biol 11 1206539 (2023)

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  1. A functional variant of lymphoid tyrosine phosphatase is associated with type I diabetes. Bottini N, Musumeci L, Alonso A, Rahmouni S, Nika K, Rostamkhani M, MacMurray J, Meloni GF, Lucarelli P, Pellecchia M, Eisenbarth GS, Comings D, Mustelin T. Nat Genet 36 337-338 (2004)
  2. The autoimmune disease-associated PTPN22 variant promotes calpain-mediated Lyp/Pep degradation associated with lymphocyte and dendritic cell hyperresponsiveness. Zhang J, Zahir N, Jiang Q, Miliotis H, Heyraud S, Meng X, Dong B, Xie G, Qiu F, Hao Z, McCulloch CA, Keystone EC, Peterson AC, Siminovitch KA. Nat Genet 43 902-907 (2011)
  3. Can we infer peptide recognition specificity mediated by SH3 domains? Cesareni G, Panni S, Nardelli G, Castagnoli L. FEBS Lett 513 38-44 (2002)
  4. LYP inhibits T-cell activation when dissociated from CSK. Vang T, Liu WH, Delacroix L, Wu S, Vasile S, Dahl R, Yang L, Musumeci L, Francis D, Landskron J, Tasken K, Tremblay ML, Lie BA, Page R, Mustelin T, Rahmouni S, Rickert RC, Tautz L. Nat Chem Biol 8 437-446 (2012)
  5. Structure of an ultraweak protein-protein complex and its crucial role in regulation of cell morphology and motility. Vaynberg J, Fukuda T, Chen K, Vinogradova O, Velyvis A, Tu Y, Ng L, Wu C, Qin J. Mol Cell 17 513-523 (2005)
  6. Structural basis for specific binding of the Gads SH3 domain to an RxxK motif-containing SLP-76 peptide: a novel mode of peptide recognition. Liu Q, Berry D, Nash P, Pawson T, McGlade CJ, Li SS. Mol Cell 11 471-481 (2003)
  7. Structural basis for SH3 domain-mediated high-affinity binding between Mona/Gads and SLP-76. Harkiolaki M, Lewitzky M, Gilbert RJ, Jones EY, Bourette RP, Mouchiroud G, Sondermann H, Moarefi I, Feller SM. EMBO J 22 2571-2582 (2003)
  8. The CAP-Gly domain of CYLD associates with the proline-rich sequence in NEMO/IKKgamma. Saito K, Kigawa T, Koshiba S, Sato K, Matsuo Y, Sakamoto A, Takagi T, Shirouzu M, Yabuki T, Nunokawa E, Seki E, Matsuda T, Aoki M, Miyata Y, Hirakawa N, Inoue M, Terada T, Nagase T, Kikuno R, Nakayama M, Ohara O, Tanaka A, Yokoyama S. Structure 12 1719-1728 (2004)
  9. Structure of a regulatory complex involving the Abl SH3 domain, the Crk SH2 domain, and a Crk-derived phosphopeptide. Donaldson LW, Gish G, Pawson T, Kay LE, Forman-Kay JD. Proc Natl Acad Sci U S A 99 14053-14058 (2002)
  10. The W620 Polymorphism in PTPN22 Disrupts Its Interaction With Peptidylarginine Deiminase Type 4 and Enhances Citrullination and NETosis. Chang HH, Dwivedi N, Nicholas AP, Ho IC. Arthritis Rheumatol 67 2323-2334 (2015)
  11. Yeast display evolution of a kinetically efficient 13-amino acid substrate for lipoic acid ligase. Puthenveetil S, Liu DS, White KA, Thompson S, Ting AY. J Am Chem Soc 131 16430-16438 (2009)
  12. Recognition of tandem PxxP motifs as a unique Src homology 3-binding mode triggers pathogen-driven actin assembly. Aitio O, Hellman M, Kazlauskas A, Vingadassalom DF, Leong JM, Saksela K, Permi P. Proc Natl Acad Sci U S A 107 21743-21748 (2010)
  13. The R620W C/T polymorphism of the gene PTPN22 is associated with SLE independently of the association of PDCD1. Reddy MV, Johansson M, Sturfelt G, Jönsen A, Gunnarsson I, Svenungsson E, Rantapää-Dahlqvist S, Alarcón-Riquelme ME. Genes Immun 6 658-662 (2005)
  14. Syndapin I and endophilin I bind overlapping proline-rich regions of dynamin I: role in synaptic vesicle endocytosis. Anggono V, Robinson PJ. J Neurochem 102 931-943 (2007)
  15. Kinetics of Src homology 3 domain association with the proline-rich domain of dynamins: specificity, occlusion, and the effects of phosphorylation. Solomaha E, Szeto FL, Yousef MA, Palfrey HC. J Biol Chem 280 23147-23156 (2005)
  16. Structural characterization of Lyn-SH3 domain in complex with a herpesviral protein reveals an extended recognition motif that enhances binding affinity. Bauer F, Schweimer K, Meiselbach H, Hoffmann S, Rösch P, Sticht H. Protein Sci 14 2487-2498 (2005)
  17. The tryptophan switch: changing ligand-binding specificity from type I to type II in SH3 domains. Fernandez-Ballester G, Blanes-Mira C, Serrano L. J Mol Biol 335 619-629 (2004)
  18. Evolving specificity from variability for protein interaction domains. Kaneko T, Sidhu SS, Li SS. Trends Biochem Sci 36 183-190 (2011)
  19. The autoimmune-predisposing variant of lymphoid tyrosine phosphatase favors T helper 1 responses. Vang T, Landskron J, Viken MK, Oberprieler N, Torgersen KM, Mustelin T, Tasken K, Tautz L, Rickert RC, Lie BA. Hum Immunol 74 574-585 (2013)
  20. SH3 domains of Grb2 adaptor bind to PXpsiPXR motifs within the Sos1 nucleotide exchange factor in a discriminate manner. McDonald CB, Seldeen KL, Deegan BJ, Farooq A. Biochemistry 48 4074-4085 (2009)
  21. The helically extended SH3 domain of the T cell adaptor protein ADAP is a novel lipid interaction domain. Heuer K, Arbuzova A, Strauss H, Kofler M, Freund C. J Mol Biol 348 1025-1035 (2005)
  22. Activation of the superoxide-producing phagocyte NADPH oxidase requires co-operation between the tandem SH3 domains of p47phox in recognition of a polyproline type II helix and an adjacent alpha-helix of p22phox. Nobuhisa I, Takeya R, Ogura K, Ueno N, Kohda D, Inagaki F, Sumimoto H. Biochem J 396 183-192 (2006)
  23. Blood pressure homeostasis is maintained by a P311-TGF-β axis. Badri KR, Yue M, Carretero OA, Aramgam SL, Cao J, Sharkady S, Kim GH, Taylor GA, Byron KL, Schuger L. J Clin Invest 123 4502-4512 (2013)
  24. Quantitative relation between intermolecular and intramolecular binding of pro-rich peptides to SH3 domains. Zhou HX. Biophys J 91 3170-3181 (2006)
  25. A region C-terminal to the proline-rich core of p47phox regulates activation of the phagocyte NADPH oxidase by interacting with the C-terminal SH3 domain of p67phox. Mizuki K, Takeya R, Kuribayashi F, Nobuhisa I, Kohda D, Nunoi H, Takeshige K, Sumimoto H. Arch Biochem Biophys 444 185-194 (2005)
  26. A molecular signature of preclinical rheumatoid arthritis triggered by dysregulated PTPN22. Chang HH, Liu GY, Dwivedi N, Sun B, Okamoto Y, Kinslow JD, Deane KD, Demoruelle MK, Norris JM, Thompson PR, Sparks JA, Rao DA, Karlson EW, Hung HC, Holers VM, Ho IC. JCI Insight 1 e90045 (2016)
  27. PTPN22.6, a dominant negative isoform of PTPN22 and potential biomarker of rheumatoid arthritis. Chang HH, Tai TS, Lu B, Iannaccone C, Cernadas M, Weinblatt M, Shadick N, Miaw SC, Ho IC. PLoS One 7 e33067 (2012)
  28. An autism-linked missense mutation in SHANK3 reveals the modularity of Shank3 function. Wang L, Pang K, Han K, Adamski CJ, Wang W, He L, Lai JK, Bondar VV, Duman JG, Richman R, Tolias KF, Barth P, Palzkill T, Liu Z, Holder JL, Zoghbi HY. Mol Psychiatry 25 2534-2555 (2020)
  29. Recognition of non-canonical peptides by the yeast Fus1p SH3 domain: elucidation of a common mechanism for diverse SH3 domain specificities. Kim J, Lee CD, Rath A, Davidson AR. J Mol Biol 377 889-901 (2008)
  30. Segmental isotopic labeling of proteins for nuclear magnetic resonance. Liu D, Xu R, Cowburn D. Methods Enzymol 462 151-175 (2009)
  31. Solution structure of a Hck SH3 domain ligand complex reveals novel interaction modes. Schmidt H, Hoffmann S, Tran T, Stoldt M, Stangler T, Wiesehan K, Willbold D. J Mol Biol 365 1517-1532 (2007)
  32. P311 binds to the latency associated protein and downregulates the expression of TGF-beta1 and TGF-beta2. Paliwal S, Shi J, Dhru U, Zhou Y, Schuger L. Biochem Biophys Res Commun 315 1104-1109 (2004)
  33. Structure of a helically extended SH3 domain of the T cell adapter protein ADAP. Heuer K, Kofler M, Langdon G, Thiemke K, Freund C. Structure 12 603-610 (2004)
  34. Estrogen receptor alpha--identification by a modeling approach of a potential polyproline II recognizing domain within the AF-2 region of the receptor that would play a role of prime importance in its mechanism of action. Jacquot Y, Gallo D, Leclercq G. J Steroid Biochem Mol Biol 104 1-10 (2007)
  35. Identification of a variant form of tyrosine phosphatase LYP. Wang S, Dong H, Han J, Ho WT, Fu X, Zhao ZJ. BMC Mol Biol 11 78 (2010)
  36. NMR solution structure and backbone dynamics of domain III of the E protein of tick-borne Langat flavivirus suggests a potential site for molecular recognition. Mukherjee M, Dutta K, White MA, Cowburn D, Fox RO. Protein Sci 15 1342-1355 (2006)
  37. Versatile retargeting of SH3 domain binding by modification of non-conserved loop residues. Hiipakka M, Saksela K. FEBS Lett 581 1735-1741 (2007)
  38. A proline to glycine mutation in the Lck SH3-domain affects conformational sampling and increases ligand binding affinity. Bauer F, Sticht H. FEBS Lett 581 1555-1560 (2007)
  39. ASPP proteins discriminate between PP1 catalytic subunits through their SH3 domain and the PP1 C-tail. Bertran MT, Mouilleron S, Zhou Y, Bajaj R, Uliana F, Kumar GS, van Drogen A, Lee R, Banerjee JJ, Hauri S, O'Reilly N, Gstaiger M, Page R, Peti W, Tapon N. Nat Commun 10 771 (2019)
  40. Backbone dynamics of a symmetric calmodulin dimer in complex with the calmodulin-binding domain of the basic-helix-loop-helix transcription factor SEF2-1/E2-2: a highly dynamic complex. Larsson G, Schleucher J, Onions J, Hermann S, Grundström T, Wijmenga SS. Biophys J 89 1214-1226 (2005)
  41. Binding of the cSH3 domain of Grb2 adaptor to two distinct RXXK motifs within Gab1 docker employs differential mechanisms. McDonald CB, Seldeen KL, Deegan BJ, Bhat V, Farooq A. J Mol Recognit 24 585-596 (2011)
  42. Biochemical and functional studies of lymphoid-specific tyrosine phosphatase (Lyp) variants S201F and R266W. Liu J, Chen M, Li R, Yang F, Shi X, Zhu L, Wang HM, Yao W, Liu Q, Meng FG, Sun JP, Pang Q, Yu X. PLoS One 7 e43631 (2012)
  43. Distinct peptide binding specificities of Src homology 3 (SH3) protein domains can be determined by modulation of local energetics across the binding interface. Gorelik M, Davidson AR. J Biol Chem 287 9168-9177 (2012)
  44. Insulin-like growth factor binding protein-2: NMR analysis and structural characterization of the N-terminal domain. Galea CA, Mobli M, McNeil KA, Mulhern TD, Wallace JC, King GF, Forbes BE, Norton RS. Biochimie 94 608-616 (2012)
  45. Altered expression of protein tyrosine phosphatase, non-receptor type 22 isoforms in systemic lupus erythematosus. Chang HH, Tseng W, Cui J, Costenbader K, Ho IC. Arthritis Res Ther 16 R14 (2014)
  46. Peroxin 5-peroxin 14 association in the protozoan Leishmania donovani involves a novel protein-protein interaction motif. Madrid KP, Jardim A. Biochem J 391 105-114 (2005)
  47. The common, autoimmunity-predisposing 620Arg > Trp variant of PTPN22 modulates macrophage function and morphology. Li M, Beauchemin H, Popovic N, Peterson A, d'Hennezel E, Piccirillo CA, Sun C, Polychronakos C. J Autoimmun 79 74-83 (2017)
  48. Solution NMR studies of Chlorella virus DNA ligase-adenylate. Piserchio A, Nair PA, Shuman S, Ghose R. J Mol Biol 395 291-308 (2010)
  49. A Conserved residue in the yeast Bem1p SH3 domain maintains the high level of binding specificity required for function. Gorelik M, Stanger K, Davidson AR. J Biol Chem 286 19470-19477 (2011)
  50. Novel insights into the mechanisms of CIN85 SH3 domains binding to Cbl proteins: solution-based investigations and in vivo implications. Ababou A, Pfuhl M, Ladbury JE. J Mol Biol 387 1120-1136 (2009)
  51. NMR determination that an extended BH3 motif of pro-apoptotic BID is specifically bound to BCL-XL. Ji H, Shekhtman A, Ghose R, McDonnell JM, Cowburn D. Magn Reson Chem 44 Spec No S101-7 (2006)
  52. Reciprocal regulation of C-Maf tyrosine phosphorylation by Tec and Ptpn22. Liu CC, Lai CY, Yen WF, Lin YH, Chang HH, Tai TS, Lu YJ, Tsao HW, Ho IC, Miaw SC. PLoS One 10 e0127617 (2015)
  53. A tetrapeptide-based method for polyproline II-type secondary structure prediction. Vlasov PK, Vlasova AV, Tumanyan VG, Esipova NG. Proteins 61 763-768 (2005)
  54. Substrate-specific reorganization of the conformational ensemble of CSK implicates novel modes of kinase function. Jamros MA, Oliveira LC, Whitford PC, Onuchic JN, Adams JA, Jennings PA. PLoS Comput Biol 8 e1002695 (2012)
  55. Structure, stability, and flexibility of ribosomal protein L14e from Sulfolobus solfataricus. Edmondson SP, Turri J, Smith K, Clark A, Shriver JW. Biochemistry 48 5553-5562 (2009)
  56. The PEST sequence does not contribute to the stability of the cystic fibrosis transmembrane conductance regulator. Chen EY, Clarke DM. BMC Biochem 3 29 (2002)
  57. Molecular and structural characterization of the SH3 domain of AHI-1 in regulation of cellular resistance of BCR-ABL(+) chronic myeloid leukemia cells to tyrosine kinase inhibitors. Liu X, Chen M, Lobo P, An J, Grace Cheng SW, Moradian A, Morin GB, Van Petegem F, Jiang X. Proteomics 12 2094-2106 (2012)
  58. Most yeast SH3 domains bind peptide targets with high intrinsic specificity. Brown T, Brown N, Stollar EJ. PLoS One 13 e0193128 (2018)
  59. Large-Scale Screening of Preferred Interactions of Human Src Homology-3 (SH3) Domains Using Native Target Proteins as Affinity Ligands. Kazlauskas A, Schmotz C, Kesti T, Hepojoki J, Kleino I, Kaneko T, Li SS, Saksela K. Mol Cell Proteomics 15 3270-3281 (2016)
  60. 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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