Multimeric and differential binding of CIN85/CD2AP with two atypical proline-rich sequences from CD2 and Cbl-b

FEBS Journal

Volumn 280, Issue 14, 2013, Pages 3399-3415

  Ceregido, M Angeles ^a,b,c   Garcia Pino, Abel ^b,c   Ortega Roldan, Jose L ^d   Casares, Salvador ^a   Lõpez Mayorga, Obdulio ^a   Bravo, Jeronimo ^e   Van Nuland, Nico A J ^b,c   Azuaga, Ana I ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

CIN85 CD2AP; ITC; NMR; SAXS; SH3 domain

Indexed keywords

ADAPTOR PROTEIN; CASITAS B LINEAGE LYMPHOMA PROTEIN; CB1 INTERACTING PROTEIN 85 KDA; CD2 ASSOCIATED PROTEIN; CLUSTER DIFFERENTIATIOM 2 PROTEIN; DIMER; PROLINE; PROTEIN SH3; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL ADHESION; COMPLEX FORMATION; CRYSTAL STRUCTURE; DOWN REGULATION; ENZYME SPECIFICITY; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; T LYMPHOCYTE ACTIVATION; X RAY CRYSTALLOGRAPHY;

CIN85/CD2AP; ITC; NMR; SAXS; SH3 DOMAIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANTIGENS, CD2; CYTOSKELETAL PROTEINS; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROLINE; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTO-ONCOGENE PROTEINS C-CBL; SCATTERING, SMALL ANGLE; SRC HOMOLOGY DOMAINS; THERMODYNAMICS; TITRIMETRY; X-RAY DIFFRACTION;

EID: 84879994954     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12333     Document Type: Article

References (34)

1. Pawson T, Raina M, &, Nash P, (2002) Interaction domains: from simple binding events to complex cellular behavior. FEBS Lett 513, 2-10.
2. Dikic I, (2002) CIN85/CMS family of adaptor molecules. FEBS Lett 529, 110-115.
3. Kowanetz K, Szymkiewicz I, Haglund K, Kowanetz M, Husnjak K, Taylor JD, Soubeyran P, Engstrom U, Ladbury JE, &, Dikic I, (2003) Identification of a novel proline-arginine motif involved in CIN85-dependent clustering of Cbl and down-regulation of epidermal growth factor receptors. J Biol Chem 278, 39735-397346.
4. Kurakin AV, Wu S, &, Bredesen DE, (2003) Atypical recognition consensus of CIN85/SETA/Ruk SH3 domains revealed by target-assisted iterative screening. J Biol Chem 278, 34102-34109.
5. Jozic D, Cardenes N, Deribe YL, Moncalian G, Hoeller D, Groemping Y, Dikic I, Rittinger K, &, Bravo J, (2005) Cbl promotes clustering of endocytic adaptor proteins. Nat Struct Mol Biol 12, 972-979.
6. Dustin ML, Olszowy MW, Holdorf AD, Li J, Bromley S, Desai N, Widder P, Rosenberger F, van der Merwe PA, Allen PM, et al,. (1998) A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell 94, 667-677.
7. Zarrinpar A, Bhattacharyya RP, &, Lim WA, (2003) The structure and function of proline recognition domains. Sci STKE 2003, RE8.
8. Moncalian G, Cardenes N, Deribe YL, Spinola-Amilibia M, Dikic I, &, Bravo J, (2006) Atypical polyproline recognition by the CMS N-terminal Src homology 3 domain. J Biol Chem 281, 38845-38853.
9. Ababou A, Pfuhl M, &, Ladbury JE, (2008) The binding stoichiometry of CIN85 SH3 domain A and cbl-b. Nat Struct Mol Biol 15, 890-891.
10. Jozic D, Cardenes N, Deribe YL, Moncalian G, Hoeller D, Groemping Y, Dikic I, Rittinger K, &, Bravo J, (2008) Reply to 'The binding stoichiometry of CIN85 SH3 domain A and Cbl-b'. Nat Struct Mol Biol 15, 891-892.
11. Zuiderweg ER, (2002) Mapping protein-protein interactions in solution by NMR spectroscopy. Biochemistry 41, 1-7.
12. Ababou A, Pfuhl M, &, Ladbury JE, (2009) Novel insights into the mechanisms of CIN85 SH3 domains binding to Cbl proteins: solution-based investigations and in vivo implications. J Mol Biol 387, 1120-1136.
13. Leavitt S, &, Freire E, (2001) Direct measurement of protein binding energetics by isothermal titration calorimetry. Curr Opin Struct Biol 11, 560-566.
14. Gomez J, Hilser VJ, Xie D, &, Freire E, (1995) The heat capacity of proteins. Proteins 22, 404-412.
15. Murphy KP, &, Freire E, (1992) Thermodynamics of structural stability and cooperative folding behavior in proteins. Adv Protein Chem 43, 313-361.
16. Konarev PV, Volkov VV, Sokolova AV, Koch MH, &, Svergun DI, (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Crystallogr 36, 1277-1282.
17. Svergun DI, (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76, 2879-2886.
18. Bache KG, Slagsvold T, &, Stenmark H, (2004) Defective downregulation of receptor tyrosine kinases in cancer. EMBO J 23, 2707-2712.
19. Hashimoto S, Hirose M, Hashimoto A, Morishige M, Yamada A, Hosaka H, Akagi K, Ogawa E, Oneyama C, Agatsuma T, et al,. (2006) Targeting AMAP1 and cortactin binding bearing an atypical src homology 3/proline interface for prevention of breast cancer invasion and metastasis. Proc Natl Acad Sci USA 103, 7036-7041.
20. Martin-Garcia JM, Luque I, Ruiz-Sanz J, &, Camara-Artigas A, (2012) The promiscuous binding of the Fyn SH3 domain to a peptide from the NS5A protein. Acta Crystallogr D Biol Crystallogr 68, 1030-1040.
21. Shih NY, Li J, Karpitskii V, Nguyen A, Dustin ML, Kanagawa O, Miner JH, &, Shaw AS, (1999) Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science 286, 312-315.
22. Grunkemeyer JA, Kwoh C, Huber TB, &, Shaw AS, (2005) CD2-associated protein (CD2AP) expression in podocytes rescues lethality of CD2AP deficiency. J Biol Chem 280, 29677-29681.
23. Ortega Roldan JL, Romero Romero ML, Ora A, Ab E, Lopez Mayorga O, Azuaga AI, &, van Nuland NA, (2007) The high resolution NMR structure of the third SH3 domain of CD2AP. J Biomol NMR 39, 331-336.
24. Casares S, Ab E, Eshuis H, Lopez-Mayorga O, van Nuland NA, &, Conejero-Lara F, (2007) The high-resolution NMR structure of the R21A Spc-SH3:P41 complex: understanding the determinants of binding affinity by comparison with Abl-SH3. BMC Struct Biol 7, 22.
25. Velazquez-Campoy A, Leavitt SA, &, Freire E, (2004) Characterization of protein-protein interactions by isothermal titration calorimetry. Methods Mol Biol 261, 35-54.
26. Sattler M, Schleucher J, &, Griesinger C, (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog NMR Spectrosc 34, 93-158.
27. Roldan JL, Blackledge M, van Nuland NA, &, Azuaga AI, (2011) Solution structure, dynamics and thermodynamics of the three SH3 domains of CD2AP. J Biomol NMR 50, 103-117.
28. Houben K, Marion D, Tarbouriech N, Ruigrok RW, &, Blanchard L, (2007) Interaction of the C-terminal domains of Sendai virus N and P proteins: comparison of polymerase-nucleocapsid interactions within the paramyxovirus family. J Virol 81, 6807-6816.
29. Auguin D, Barthe P, Royer C, Stern MH, Noguchi M, Arold ST, &, Roumestand C, (2004) Structural basis for the co-activation of protein kinase B by T-cell leukemia-1 (TCL1) family proto-oncoproteins. J Biol Chem 279, 35890-35902.
30. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, &, Bax A, (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277-293.
31. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas M, Ulrich EL, Markley JL, Ionides J, &, Laue ED, (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696.
32. Johnson BA, (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 278, 313-352.
33. Konarev PV, Petoukhov MV, Volkov VV, &, Svergun DI, (2006) ATSAS 2.1, a program package for small-angle scattering data analysis. J Appl Crystallogr 39, 277-286.
34. Svergun DI, Barberato C, &, Koch MHJ, (1995) CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Crystallogr 28, 768-773.