Solution structure, dynamics and thermodynamics of the three SH3 domains of CD2AP

Journal of Biomolecular NMR

Volumn 50, Issue 2, 2011, Pages 103-117

  Ortega Roldan, Jose L ^a   Blackledge, Martin ^b   Van Nuland, Nico A J ^c,d   Azuaga, Ana I ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

Adaptor protein; CD2AP; NMR; Protein structure; SH3 domain

Indexed keywords

ADAPTOR PROTEIN; CD2 ASSOCIATED PROTEIN; DEUTERIUM; HYDROGEN; NITROGEN 15; PROTEIN CIN85; PROTEIN SH3; UNCLASSIFIED DRUG;

ARTICLE; DEUTERIUM HYDROGEN EXCHANGE; DIFFERENTIAL SCANNING CALORIMETRY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMODYNAMICS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CYTOSKELETAL PROTEINS; DEUTERIUM EXCHANGE MEASUREMENT; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STABILITY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SOLUTIONS; SRC HOMOLOGY DOMAINS; THERMODYNAMICS;

EID: 80051688323     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-011-9505-5     Document Type: Article

References (51)

1. Bendsen S, Oestergaard VH, Skouboe C, Brinch M, Knudsen BR, Andersen AH (2009) The QTK loop is essential for the communication between the N-terminal ATPase domain and the central cleavage-ligation region in human topoisomerase IIalpha. Biochemistry 48(27):6508-6515. doi:10.1021/bi9005978
2. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54(Pt 5):905-921
3. Brutscher B(2001) Accurate measurement of small spin-spin couplings in partially aligned molecules using a novel J-mismatch compensated spin-state-selection filter. J Magn Reson 151(2):332-338. doi:10.1006/jmre.2001. 2375
4. Calvete JJ (2004) Structures of integrin domains and concerted conformational changes in the bidirectional signaling mechanism of alphaIIbbeta3. Exp Biol Med (Maywood) 229(8):732-744. doi: 229/8/732[pii] (Pubitemid 39166477)
5. Casares S, Lopez-Mayorga O, Vega MC, Camara-Artigas A, Conejero- Lara F (2007) Cooperative propagation of local stability changes from low-stability and high-stability regions in a SH3 domain. Proteins 67(3):531-547. doi:10.1002/prot.21284 (Pubitemid 46625571)
6. Chen S, Dumitrescu TP, Smithgall TE, Engen JR (2008) Abl N-terminal cap stabilization of SH3 domain dynamics. Biochemistry 47(21):5795-5803. doi:10.1021/bi800446b (Pubitemid 351747058)
7. 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(3):277-293
8. Dikic I (2002) CIN85/CMS family of adaptor molecules. FEBS Lett 529(1):110-115. doi:S0014579302031885[pii] (Pubitemid 35283919)
9. Dolinsky TJ, Nielsen JE,McCammonJA, BakerNA(2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic acids research 32 (Web Server issue):W665-W667. doi:10.1093/nar/gkh381 (Pubitemid 38997419)
10. Dosset P, Hus JC, Blackledge M, Marion D (2000) Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J Biomol NMR 16(1):23-28 (Pubitemid 30114721)
11. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, Gish G, Shoelson SE, Pawson T, Forman-Kay JD, Kay LE (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15 N NMR relaxation. Biochemistry 33(19):5984-6003 (Pubitemid 24184605)
12. Ferreon JC, Volk DE, Luxon BA, Gorenstein DG, Hilser VJ (2003) Solution structure, dynamics, and thermodynamics of the native state ensemble of the Sem-5 C-terminal SH3 domain. Biochemistry 42(19):5582-5591. doi:10.1021/ bi030005j (Pubitemid 36582848)
13. Filimonov VV, Azuaga AI, Viguera AR, Serrano L, Mateo PL (1999)A thermodynamic analysis of a family of small globular proteins: SH3 domains. Biophys Chem 77(2-3):195-208 (Pubitemid 29206652)
14. Goddard TD, Kneller DG (1993) Sparky 3, University of California, San Francisco
15. Guerois R, Nielsen JE, Serrano L (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol 320(2):369-387. doi:10.1016/S0022-2836(02)00442-4 (Pubitemid 34722226)
16. Guijarro JI, Morton CJ, Plaxco KW, Campbell ID, Dobson CM (1998) Folding kinetics of the SH3 domain of PI3 kinase by realtime NMR combined with optical spectroscopy. J Mol Biol 276(3):657-667. doi:10.1006/jmbi.1997.1553 (Pubitemid 28116136)
17. Guntert P (1997) Calculating protein structures from NMR data. Methods Mol Biol 60:157-194. doi:10.1385/0-89603-309-0:157
18. Guntert P, Mumenthaler C, Wuthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273(1):283-298. doi:10.1006/jmbi.1997. 1284 (Pubitemid 27460230)
19. Herrmann T, Guntert P, Wuthrich K (2002) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J Biomol NMR 24(3):171-189. doi:5111821[pii] (Pubitemid 36113646)
20. Hooft RW, Sander C, Vriend G (1996) Positioning hydrogen atoms by optimizing hydrogen-bond networks in protein structures. Proteins 26(4):363-376. doi:10.1002/(SICI)1097-0134(199612) 26:4\363:AID-PROT1[3.0.CO;2-Rfseq (Pubitemid 27024754)
21. Horita DA, Zhang W, Smithgall TE, Gmeiner WH, Byrd RA (2000) Dynamics of the Hck-SH3 domain: comparison of experiment with multiple molecular dynamics simulations. Protein Sci 9(1):95-103. doi:10.1110/ps.9.1.95 (Pubitemid 30070943)
22. Hus JC, Marion D, Blackledge M (2000) De novo determination of protein structure by NMR using orientational and long-range order restraints. J Mol Biol 298(5):927-936. doi:10.1006/ jmbi.2000.3714
23. Hwang TL, Shaka AJ (1998) Multiple-pulse mixing sequences that selectively enhance chemical exchange or cross-relaxation peaks in high-resolution NMR spectra. J Magn Reson 135(2):280-287. doi:10.1006/jmre.1998. 1598 (Pubitemid 128452123)
24. Jarymowycz VA, Stone MJ (2006) Fast time scale dynamics of protein backbones:NMRrelaxation methods, applications, and functional consequences. Chem Rev 106(5):1624-1671. doi:10.1021/cr0404 21p (Pubitemid 43792775)
25. JohnsonBA(2004) Using NMRView to visualize and analyze theNMR spectra of macromolecules. Methods Mol Biol 278:313-352. doi: 10.1385/1-59259-809-9:313
26. Knapp S, Mattson PT, Christova P, Berndt KD, Karshikoff A, Vihinen M, Smith CI, Ladenstein R (1998) Thermal unfolding of small proteins with SH3 domain folding pattern. Proteins 31(3): 309-319. doi:10.1002/(SICI)1097- 0134(19980515)31:3\309:AIDPROT7[ 3.0.CO;2-D[pii] (Pubitemid 28217818)
27. Larson SM, Davidson AR (2000) The identification of conserved interactions within the SH3 domain by alignment of sequences and structures. Protein Sci 9(11):2170-2180. doi:10.1110/ps.9.11. 2170 (Pubitemid 32104153)
28. Lenaerts T, Ferkinghoff-Borg J, Stricher F, Serrano L, Schymkowitz JW, Rousseau F (2008) Quantifying information transfer by protein domains: analysis of the Fyn SH2 domain structure. BMC Struct Biol 8:43. doi:10.1186/1472-6807-8- 43
29. Lescop E, Schanda P, Brutscher B (2007) A set of BEST tripleresonance experiments for time-optimized protein resonance assignment. J Magn Reson 187(1):163-169. doi:10.1016/j.jmr. 2007.04.002 (Pubitemid 46898871)
30. Li SS (2005) Specificity and versatility of SH3 and other prolinerecognition domains: structural basis and implications for cellular signal transduction. Biochem J 390(Pt 3):641-653. doi: 10.1042/BJ20050411 (Pubitemid 41395346)
31. Li C, Ruotsalainen V, Tryggvason K, Shaw AS, Miner JH (2000) CD2AP is expressed with nephrin in developing podocytes and is found widely in mature kidney and elsewhere. Am J Physiol Renal Physiol 279(4):F785-F792
32. Luque I, Freire E (1998) Structure-based prediction of binding affinities and molecular design of peptide ligands. Methods Enzymol 295:100-127 (Pubitemid 29349911)
33. Markus MA, Dayie KT, Matsudaira P, Wagner G (1996) Local mobility within villin 14T probed via heteronuclear relaxation measurements and a reduced spectral density mapping. Biochemistry 35(6):1722-1732. doi:10.1021/bi951933o (Pubitemid 26062620)
34. Mayer BJ (2001) SH3 domains: complexity in moderation. J Cell Sci 114(Pt 7):1253-1263 (Pubitemid 32409462)
35. 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(50): 38845-38853. doi:10.1074/jbc.M606411200 (Pubitemid 46042011)
36. Morel B, Casares S, Conejero-Lara F (2006) A single mutation induces amyloid aggregation in the alpha-spectrin SH3 domain: analysis of the early stages of fibril formation. J Mol Biol 356(2):453-468. doi:10.1016/j.jmb.2005. 11.062 (Pubitemid 43099983)
37. Nederveen AJ, Doreleijers JF, Vranken W, Miller Z, Spronk CA, Nabuurs SB, Guntert P, Livny M, Markley JL, Nilges M, Ulrich EL, Kaptein R, Bonvin AM (2005) RECOORD: a recalculated coordinate database of 500 + proteins from the PDB using restraints from the BioMagResBank. Proteins 59(4):662-672. doi: 10.1002/prot.20408 (Pubitemid 40695843)
38. 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(4):331-336 (Pubitemid 350055755)
39. Ortega-Roldan JL, Jensen MR, Brutscher B, Azuaga AI, Blackledge M, van Nuland NA (2009) Accurate characterization of weak macromolecular interactions by titration of NMR residual dipolar couplings: application to the CD2AP SH3-C:ubiquitin complex. Nucleic Acids Res 37(9):e70
40. Plaxco KW, Guijarro JI, Morton CJ, Pitkeathly M, Campbell ID, Dobson CM (1998) The folding kinetics and thermodynamics of the Fyn-SH3 domain. Biochemistry 37(8):2529-2537. doi: 10.1021/bi972075u (Pubitemid 28119329)
41. Ruckert M, Otting G (2000) Alignment of Biological Macromolecules in Novel Nonionic Liquid Crystalline Media for NMR Experiments. J Am Chem Soc 122(32):7793-7797. doi:10.1021/ ja001068h
42. Sadqi M, Casares S, Abril MA, Lopez-Mayorga O, Conejero-Lara F, Freire E (1999) The native state conformational ensemble of the SH3 domain from alpha-spectrin. Biochemistry 38(28): 8899-8906. doi:10.1021/bi990413g (Pubitemid 29334651)
43. Schanda P, Brutscher B (2006) Hadamard frequency-encoded SOFAST-HMQC for ultrafast two-dimensional protein NMR. J Magn Reson 178(2):334-339. doi:10.1016/j.jmr.2005.10.007 (Pubitemid 43107941)
44. Schanda P, Kupce E, Brutscher B (2005) SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J Biomol NMR 33(4): 199-211. doi:10.1007/s10858-005-4425-x (Pubitemid 43118574)
45. Schanda P, Van Melckebeke H, Brutscher B (2006) Speeding up three-dimensional protein NMR experiments to a few minutes. J Am Chem Soc 128(28):9042-9043. doi:10.1021/ja062025p (Pubitemid 44078980)
46. 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(5438):312-315. doi:7865[pii] (Pubitemid 29484698)
47. Varela L, Morel B, Azuaga AI, Conejero-Lara F (2009) A single mutation in an SH3 domain increases amyloid aggregation by accelerating nucleation, but not by destabilizing thermodynamically the native state. FEBS Lett 583(4):801-806. doi:10.1016/ j.febslet.2009.01.033
48. Viguera AR, Martinez JC, Filimonov VV, Mateo PL, Serrano L (1994) Thermodynamic and kinetic analysis of the SH3 domain of spectrin shows a two-state folding transition. Biochemistry 33(8):2142-2150 (Pubitemid 24099611)
49. Wang C, Pawley NH, Nicholson LK (2001) The role of backbone motions in ligand binding to the c-Src SH3 domain. J Mol Biol 313(4):873-887. doi:10.1006/jmbi.2001.5083 (Pubitemid 33063433)
50. Wilkins DK, Grimshaw SB, Receveur V, Dobson CM, Jones JA, Smith LJ (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38(50):16424-16431. doi:bi991765q[pii]
51. Wuthrich K (1986) NMR of proteins and nucleic acids