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PMID: 7774577 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Affinity and specificity requirements for the first Src homology 3 domain of the Crk proteins.

The EMBO journal ·Vol. 14 ·No. 10 ·1995-05-15 ·Pages 2191-8

Knudsen BS, Zheng J, Feller SM, Mayer JP, Burrell SK, Cowburn D, Hanafusa H

Abstract

The specificity of SH3 domain complex formation plays an important role in determining signal transduction events. We have previously identified a highly specific interaction between the first CrkSH3 domain [CrkSH3(1)] and proline-rich sequences in the guanine nucleotide exchange factor C3G. A 10 amino acid peptide derived from the first proline-rich sequence (P3P4P5A6L7P8P9K10K11R12) bound with a Kd of 1.89 +/- 0.06 microM and fully retained the high affinity and unique selectivity for the CrkSH3(1) domain. Mutational analysis showed that P5, P8, L7 and K10 are critical for high affinity binding. A conservative mutation, K10R, significantly decreased the affinity for the CrkSH3(1) domain while increasing the affinity for Grb2. Comparative binding studies with the K10R and K10A mutant peptides to c-Crk and v-Crk further suggested that K10 binds via a charge-dependent and a charge-independent interaction to the RT loop of the CrkSH3(1) domain. Besides determining important structural features necessary for high affinity and specificity binding to the CrkSH3(1) domain, our results also demonstrate that a conservative mutation in a single amino acid can significantly alter the specificity of an SH3 binding peptide.

MeSH Terms
Adaptor Proteins, Signal Transducing Amino Acid Sequence DNA Mutational Analysis GRB2 Adaptor Protein Genes, src Guanine Nucleotide Exchange Factors Molecular Sequence Data Oligopeptides/metabolism Oncogene Protein v-crk Protein Binding Protein-Tyrosine Kinases/genetics,metabolism Proteins/metabolism Proto-Oncogene Proteins/genetics,metabolism Proto-Oncogene Proteins c-crk Retroviridae Proteins, Oncogenic/genetics,metabolism Sequence Homology, Amino Acid Structure-Activity Relationship
Chemicals
Adaptor Proteins, Signal Transducing GRB2 Adaptor Protein Guanine Nucleotide Exchange Factors Oligopeptides Oncogene Protein v-crk Proteins Proto-Oncogene Proteins Proto-Oncogene Proteins c-crk Retroviridae Proteins, Oncogenic Protein-Tyrosine Kinases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Knudsen B S
Laboratory of Molecular Oncology, Rockefeller University, New York, NY 10021, USA.
Zheng J
Feller S M
Mayer J P
Burrell S K
Cowburn D
Hanafusa H
References (41)
41 references, click to expand
  1. Structure and function of the SH3 domain.
    Prog Biophys Mol Biol. 1994;61(3):283-97 PMID: 8073124
  2. High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides.
    Nat Struct Biol. 1994 Aug;1(8):546-51 PMID: 7664083
  3. An SH3 binding region in the epithelial Na+ channel (alpha rENaC) mediates its localization at the apical membrane.
    EMBO J. 1994 Oct 3;13(19):4440-50 PMID: 7925286
  4. Abl protein-tyrosine kinase selects the Crk adapter as a substrate using SH3-binding sites.
    Genes Dev. 1994 Apr 1;8(7):783-95 PMID: 7926767
  5. Identification and characterization of Src SH3 ligands from phage-displayed random peptide libraries.
    J Biol Chem. 1994 Sep 30;269(39):23853-6 PMID: 7929027
  6. Identification of a Src SH3 domain binding motif by screening a random phage display library.
    J Biol Chem. 1994 Sep 30;269(39):24034-9 PMID: 7929055
  7. Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1.
    Nature. 1994 Nov 10;372(6502):182-6 PMID: 7969452
  8. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains.
    Nature. 1994 Nov 24;372(6504):375-9 PMID: 7802869
  9. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice.
    Science. 1993 Jul 16;261(5119):358-61 PMID: 8332901
  10. SH3 domains direct cellular localization of signaling molecules.
    Cell. 1993 Jul 16;74(1):83-91 PMID: 8334708
  11. The v-Src SH3 domain binds phosphatidylinositol 3'-kinase.
    Mol Cell Biol. 1993 Sep;13(9):5225-32 PMID: 7689147
  12. Isolation and chromosomal localization of CRKL, a human crk-like gene.
    Oncogene. 1993 Sep;8(9):2469-74 PMID: 8361759
  13. The GTPase dynamin binds to and is activated by a subset of SH3 domains.
    Cell. 1993 Oct 8;75(1):25-36 PMID: 8402898
  14. The structure and function of proline-rich regions in proteins.
    Biochem J. 1994 Jan 15;297 ( Pt 2):249-60 PMID: 8297327
  15. Structural basis for the binding of proline-rich peptides to SH3 domains.
    Cell. 1994 Mar 11;76(5):933-45 PMID: 7510218
  16. Activation of phosphatidylinositol-3' kinase by Src-family kinase SH3 binding to the p85 subunit.
    Science. 1994 Mar 18;263(5153):1609-12 PMID: 8128248
  17. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3443-7 PMID: 7512734
  18. Mutagenic analysis of the roles of SH2 and SH3 domains in regulation of the Abl tyrosine kinase.
    Mol Cell Biol. 1994 May;14(5):2883-94 PMID: 8164650
  19. The C-terminal SH3 domain of the mouse c-Crk protein negatively regulates tyrosine-phosphorylation of Crk associated p130 in rat 3Y1 cells.
    Oncogene. 1994 Jun;9(6):1669-78 PMID: 8183562
  20. An SH3 domain and proline-rich sequence mediate an interaction between two components of the phagocyte NADPH oxidase complex.
    J Biol Chem. 1994 May 13;269(19):13752-5 PMID: 8188650
  21. c-Abl kinase regulates the protein binding activity of c-Crk.
    EMBO J. 1994 May 15;13(10):2341-51 PMID: 8194526
  22. Dynamin binds to SH3 domains of phospholipase C gamma and GRB-2.
    J Biol Chem. 1994 Jun 10;269(23):16009-14 PMID: 8206897
  23. CRK protein binds to two guanine nucleotide-releasing proteins for the Ras family and modulates nerve growth factor-induced activation of Ras in PC12 cells.
    Mol Cell Biol. 1994 Aug;14(8):5495-500 PMID: 8035825
  24. Binding of Bruton's tyrosine kinase to Fyn, Lyn, or Hck through a Src homology 3 domain-mediated interaction.
    Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8152-5 PMID: 8058772
  25. Characterization of p47gag-crk, a novel oncogene product with sequence similarity to a putative modulatory domain of protein-tyrosine kinases and phospholipase C.
    Cold Spring Harb Symp Quant Biol. 1988;53 Pt 2:907-14 PMID: 2855503
  26. A newly isolated avian sarcoma virus, ASV-1, carries the crk oncogene.
    Oncogene. 1989 Nov;4(11):1281-4 PMID: 2554234
  27. Association of the v-crk oncogene product with phosphotyrosine-containing proteins and protein kinase activity.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2638-42 PMID: 1690891
  28. Identification of a protein that binds to the SH3 region of Abl and is similar to Bcr and GAP-rho.
    Science. 1992 Aug 7;257(5071):803-6 PMID: 1379745
  29. High-efficiency expression/cloning of epidermal growth factor-receptor-binding proteins with Src homology 2 domains.
    Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):8894-8 PMID: 1409582
  30. The product of the cellular crk gene consists primarily of SH2 and SH3 regions.
    Cell Growth Differ. 1992 Jul;3(7):451-60 PMID: 1329926
  31. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases.
    Nature. 1992 Dec 17;360(6405):689-92 PMID: 1465135
  32. Identification of a ten-amino acid proline-rich SH3 binding site.
    Science. 1993 Feb 19;259(5098):1157-61 PMID: 8438166
  33. A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos.
    Cell. 1993 Apr 9;73(1):179-91 PMID: 8462098
  34. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2.
    Science. 1993 May 28;260(5112):1338-43 PMID: 8493579
  35. Solution structure and ligand-binding site of the SH3 domain of the p85 alpha subunit of phosphatidylinositol 3-kinase.
    Cell. 1993 May 21;73(4):813-22 PMID: 7684655
  36. Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions.
    Science. 1994 Nov 18;266(5188):1241-7 PMID: 7526465
  37. Four proline-rich sequences of the guanine-nucleotide exchange factor C3G bind with unique specificity to the first Src homology 3 domain of Crk.
    J Biol Chem. 1994 Dec 30;269(52):32781-7 PMID: 7806500
  38. SH2 and SH3 domains as molecular adhesives: the interactions of Crk and Abl.
    Trends Biochem Sci. 1994 Nov;19(11):453-8 PMID: 7855886
  39. Critical residues in an SH3 domain from Sem-5 suggest a mechanism for proline-rich peptide recognition.
    Nat Struct Biol. 1994 Apr;1(4):221-5 PMID: 7656049
  40. Helical encounter.
    Nat Struct Biol. 1994 Aug;1(8):489-91 PMID: 7664069
  41. Binding of the Grb2 SH2 domain to phosphotyrosine motifs does not change the affinity of its SH3 domains for Sos proline-rich motifs.
    EMBO J. 1994 Sep 1;13(17):4011-21 PMID: 7521298
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1995-05-15
Pages
2191-8
Language
English
Region
England
NLM ID
8208664
PMCID
PMC398325
Subset
IM
Grants
NCI NIH HHS · CA09673 · United States
NCI NIH HHS · CA44356 · United States
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