The solution structure of pGolemi, a high affinity Mena EVH1 binding miniature protein, suggests explanations for paralog-specific binding to Ena/VASP homology (EVH) 1 domains

Biological Chemistry

Volumn 390, Issue 5-6, 2009, Pages 417-426

  Link, Nina M ^a   Hunke, Cornelia ^b   Mueller, Jonathan W ^a,c   Eichler, Jutta ^d   Bayer, Peter ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Ena VASP homology 1 (EVH1); Homology modeling; Listeria monocytogenes; NMR spectroscopy; Peptides; Structure elucidation

Indexed keywords

ADAPTOR PROTEIN; BINDING PROTEIN; MEMBRANE PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PGOLEMI PROTEIN; PHENYLALANINE; PROTEIN ACTA; PROTEIN HOMER; PROTEIN MENA EVH 1; SPROUTY PROTEIN; THREONINE; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ACTIN POLYMERIZATION; ARTICLE; LIGAND BINDING; LISTERIA MONOCYTOGENES; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; AVIAN PROTEINS; BACTERIAL PROTEINS; DNA-BINDING PROTEINS; LIGANDS; LISTERIA MONOCYTOGENES; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROLINE-RICH PROTEIN DOMAINS; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN;

AVES; BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

EID: 67649607968     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2009.045     Document Type: Article

References (64)

1. Aasland, R., Abrams, C., Ampe, C., Ball, L.J., Bedford, M.T., Cesareni, G., Gimona, M., Hurley, J.H., Jarchau, T., Lehto, V.P., et al. (2002). Normalization of nomenclature for peptide motifs as ligands of modular protein domains. FEBS Lett. 513, 141-144.
2. Ahern-Djamali, S.M., Comer, A.R., Bachmann, C., Kastenmeier, A.S., Reddy, S.K., Beckerle, M.C., Walter, U., and Hoffmann, F.M. (1998). Mutations in Drosophila enabled and rescue by human vasodilator-stimulated phosphoprotein (VASP) indicate important functional roles for Ena/VASP homology domain 1 (EVH1) and EVH2 domains. Mol. Biol. Cell 9, 2157-2171.
3. Aue, W.P., Bartholdi, E., and Ernst, R.R. (1976). Two-dimensional spectroscopy. Application to nuclear magnetic resonance. J. Chem. Phys. 64, 2229-2246.
4. Auerbuch, V., Loureiro, J.J., Gertler, F.B., Theriot, J.A., and Portnoy, D.A. (2003). Ena/VASP proteins contribute to Listeria monocytogenes pathogenesis by controlling temporal and spatial persistence of bacterial actin-based motility. Mol. Microbiol. 49, 1361-1375.
5. Bachmann, C., Fischer, L., Walter, U., and Reinhard, M. (1999). The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation. J. Biol. Chem. 274, 23549-23557.
6. Ball, L.J., Kuhne, R., Hoffmann, B., Hafner, A., Schmieder, P., Volkmer-Engert, R., Hof, M., Wahl, M., Schneider-Mergener, J., Walter, U., et al. (2000). Dual epitope recognition by the VASP EVH1 domain modulates polyproline ligand specificity and binding affinity. EMBO J. 19, 4903-4914.
7. Ball, L.J., Jarchau, T., Oschkinat, H., and Walter, U. (2002). EVH1 domains: structure, function and interactions. FEBS Lett. 513, 45-52.
8. Ball, L.J., Kuhne, R., Schneider-Mergener, J., and Oschkinat, H. (2005). Recognition of proline-rich motifs by protein-protein-interaction domains. Angew. Chem. Int. Ed. 44, 2852-2869.
9. Barzik, M., Kotova, T.I., Higgs, H.N., Hazelwood, L., Hanein, D., Gertler, F.B., and Schafer, D.A. (2005). Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J. Biol. Chem. 280, 28653-28662.
10. Bear, J.E., Svitkina, T.M., Krause, M., Schafer, D.A., Loureiro, J.J., Strasser, G.A., Maly, I.V., Chaga, O.Y., Cooper, J.A., Borisy, G.G., et al. (2002). Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109, 509-521.
11. Blundell, T.L., Pitts, J.E., Tickle, I.J., Wood, S.P., and Wu, C.W. (1981). X-ray analysis (1.4-Å resolution) of avian pancreatic polypeptide: small globular protein hormone. Proc. Natl. Acad. Sci. USA 78, 4175-4179.
12. Boeda, B., Briggs, D.C., Higgins, T., Garvalov, B.K., Fadden, A.J., McDonald, N.Q., and Way, M. (2007). Tes, a specific Mena interacting partner, breaks the rules for EVH1 binding. Mol. Cell 28, 1071-1082.
13. Braunschweiler, L. and Ernst, R.R. (1983). Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53, 521-528.
14. Brindle, N.P., Holt, M.R., Davies, J.E., Price, C.J., and Critchley, D.R. (1996). The focal-adhesion vasodilator-stimulated phosphoprotein (VASP) binds to the proline-rich domain in vinculin. Biochem. J. 318, 753-757.
15. Bundschu, K., Walter, U., and Schuh, K. (2007). Getting a first clue about SPRED functions. Bioessays 29, 897-907.
16. Chakraborty, T., Ebel, F., Domann, E., Niebuhr, K., Gerstel, B., Pistor, S., Temm-Grove, C.J., Jockusch, B.M., Reinhard, M., Walter, U., et al. (1995). A focal adhesion factor directly linking intracellularly motile Listeria monocytogenes and Listeria ivanovii to the actin-based cytoskeleton of mammalian cells. EMBO J. 14, 1314-1321.
17. Cornilescu, G., Delaglio, F., and Bax, A. (1999). Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302.
18. Cowan, P.M. and McGavin, S.T.E.W. (1955). Structure of poly-L-proline. Nature 176, 501-503.
19. Fedorov, A.A., Fedorov, E., Gertler, F., and Almo, S.C. (1999). Structure of EVH1, a novel proline-rich ligand-binding module involved in cytoskeletal dynamics and neural function. Nat. Struct. Biol. 6, 661-665.
20. Gertler, F.B., Niebuhr, K., Reinhard, M., Wehland, J., and Soriano, P. (1996). Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell 87, 227-239.
21. Glover, I., Haneef, I., Pitts, J., Wood, S., Moss, D., Tickle, I., and Blundell, T. (1983). Conformational flexibility in a small globular hormone: X-ray analysis of avian pancreatic polypeptide at 0.98-Å resolution. Biopolymers 22, 293-304.
22. Golemi-Kotra, D., Mahaffy, R., Footer, M.J., Holtzman, J.H., Pollard, T.D., Theriot, J.A., and Schepartz, A. (2004). High affinity, paralog-specific recognition of the Mena EVH1 domain by a miniature protein. J. Am. Chem. Soc. 126, 4-5.
23. Gronwald, W. and Kalbitzer, H.R. (2004). Automated structure determination of proteins by NMR spectroscopy. Prog. Nucl. Magn. Reson. Spectr. 44, 33-96.
24. Holtzman, J.H., Woronowicz, K., Golemi-Kotra, D., and Schepartz, A. (2007). Miniature protein ligands for EVH1 domains: interplay between affinity, specificity, and cell motility. Biochemistry 46, 13541-13553.
25. Hunke, C., Hirsch, T., and Eichler, J. (2006). Structure-based synthetic mimicry of discontinuous protein binding sites: inhibitors of the interaction of Mena EVH1 domain with proline-rich ligands. ChemBioChem 7, 1258-1264.
26. Huttelmaier, S., Harbeck, B., Steffens, O., Messerschmidt, T., Illenberger, S., and Jockusch, B.M. (1999). Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP. FEBS Lett. 451, 68-74.
27. Jeener, J., Meier, B.H., Bachmann, P., and Ernst, R.R. (1979). Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4553.
28. Jurt, S., Aemissegger, A., Guntert, P., Zerbe, O., and Hilvert, D. (2006). A photoswitchable miniprotein based on the sequence of avian pancreatic polypeptide. Angew. Chem. Int. Ed. 45, 6297-6300.
29. Kocks, C., Gouin, E., Tabouret, M., Berche, P., Ohayon, H., and Cossart, P. (1992). L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68, 521-531.
30. Krause, M., Dent, E.W., Bear, J.E., Loureiro, J.J., and Gertler, F.B. (2003). Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19, 541-564.
31. Krieger, E., Koraimann, G., and Vriend, G. (2002). Increasing the precision of comparative models with YASARA NOVA - a self-parameterizing force field. Proteins 47, 393-402.
32. Krieger, E., Darden, T., Nabuurs, S.B., Finkelstein, A., and Vriend, G. (2004). Making optimal use of empirical energy functions: force-field parameterization in crystal space. Proteins 57, 678-683.
33. Kuhnel, K., Jarchau, T., Wolf, E., Schlichting, I., Walter, U., Wittinghofer, A., and Strelkov, S.V. (2004). The VASP tetramerization domain is a right-handed coiled coil based on a 15-residue repeat. Proc. Natl. Acad. Sci. USA 101, 17027-17032.
34. Kuszewski, J., Gronenborn, A.M., and Clore, G.M. (1996). Improving the quality of NMR and crystallographic protein structures by means of a conformational database potential derived from structure databases. Protein Sci. 5, 1067-1080.
35. Lasa, I., Gouin, E., Goethals, M., Vancompernolle, K., David, V., Vandekerckhove, J., and Cossart, P. (1997). Identification of two regions in the N-terminal domain of ActA involved in the actin comet tail formation by Listeria monocytogenes. EMBO J. 16, 1531-1540.
36. Laurent, V., Loisel, T.P., Harbeck, B., Wehman, A., Grobe, L., Jockusch, B.M., Wehland, J., Gertler, F.B., and Carlier, M.F. (1999). Role of proteins of the Ena/VASP family in actinbased motility of Listeria monocytogenes. J. Cell Biol. 144, 1245-1258.
37. Machner, M.P., Urbanke, C., Barzik, M., Otten, S., Sechi, A.S., Wehland, J., and Heinz, D.W. (2001). ActA from Listeria monocytogenes can interact with up to four Ena/VASP homology 1 domains simultaneously. J. Biol. Chem. 276, 40096-40103.
38. Niebuhr, K., Ebel, F., Frank, R., Reinhard, M., Domann, E., Carl, U.D., Walter, U., Gertler, F.B., Wehland, J., and Chakraborty, T. (1997). A novel proline-rich motif present in ActA of Listeria monocytogenes and cytoskeletal proteins is the ligand for the EVH1 domain, a protein module present in the Ena/VASP family. EMBO J. 16, 5433-5444.
39. Nygaard, R., Nielbo, S., Schwartz, T.W., and Poulsen, F.M. (2006). The PP-fold solution structure of human polypeptide YY and human PYY3-36 as determined by NMR. Biochemistry 45, 8350-8357.
40. Pawson, T. and Nash, P. (2003). Assembly of cell regulatory systems through protein interaction domains. Science 300, 445-452.
41. Piotto, M., Saudek, V., and Sklenar, V. (1992). Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661-665.
42. Pistor, S., Chakraborty, T., Walter, U., and Wehland, J. (1995). The bacterial actin nucleator protein ActA of Listeria monocytogenes contains multiple binding sites for host microfilament proteins. Curr. Biol. 5, 517-525.
43. Prehoda, K.E., Lee, D.J., and Lim, W.A. (1999). Structure of the enabled/VASP homology 1 domain-peptide complex: a key component in the spatial control of actin assembly. Cell 97, 471-480.
44. Reinhard, M., Halbrugge, M., Scheer, U., Wiegand, C., Joc-kusch, B.M., and Walter, U. (1992). The 46/50 kDa phosphoprotein VASP purified from human platelets is a novel protein associated with actin filaments and focal contacts. EMBO J. 11, 2063-2070.
45. Reinhard, M., Giehl, K., Abel, K., Haffner, C., Jarchau, T., Hoppe, V., Jockusch, B.M., and Walter, U. (1995a). The proline-rich focal adhesion and microfilament protein VASP is a ligand for profilins. EMBO J. 14, 1583-1589.
46. Reinhard, M., Jouvenal, K., Tripier, D., and Walter, U. (1995b). Identification, purification, and characterization of a zyxinrelated protein that binds the focal adhesion and microfilament protein VASP (vasodilator-stimulated phosphoprotein). Proc. Natl. Acad. Sci. USA 92, 7956-7960.
47. Reinhard, M., Rudiger, M., Jockusch, B.M., and Walter, U. (1996). VASP interaction with vinculin: a recurring theme of interactions with proline-rich motifs. FEBS Lett. 399, 103-107.
48. Rottner, K., Behrendt, B., Small, J.V., and Wehland, J. (1999). VASP dynamics during lamellipodia protrusion. Nat. Cell Biol. 1, 321-322.
49. Rucker, A.L., Pager, C.T., Campbell, M.N., Qualls, J.E., and Creamer, T.P. (2003). Host-guest scale of left-handed polyproline II helix formation. Proteins 53, 68-75.
50. Rutledge, S.E., Volkman, H.M., and Schepartz, A. (2003). Molecular recognition of protein surfaces: high affinity ligands for the CBP KIX domain. J. Am. Chem. Soc. 125, 14336-14347.
51. Schwieters, C.D. and Clore, G.M. (2002). Reweighted atomic densities to represent ensembles of NMR structures. J. Biomol. NMR 23, 221-225.
52. Schwieters, C.D., Kuszewski, J.J., Tjandra, N., and Clore, G.M. (2003). The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160, 65-73.
53. Schwieters, C.D., Kuszewski, J.J., and Marius Clore, G. (2006). Using Xplor-NIH for NMR molecular structure determination. Prog. Nucl. Magn. Reson. Spectr. 48, 47-62.
54. Shiraishi-Yamaguchi, Y. and Furuichi, T. (2007). The Homer family proteins. Genome Biol. 8, 206.
55. Skoble, J., Portnoy, D.A., and Welch, M.D. (2000). Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J. Cell Biol. 150, 527-538.
56. Smith, G.A., Theriot, J.A., and Portnoy, D.A. (1996). The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. J. Cell Biol. 135, 647-660.
57. Theobald, D.L. and Wuttke, D.S. (2006). THESEUS: maximum likelihood superpositioning and analysis of macromolecular structures. Bioinformatics 22, 2171-2172.
58. Vriend, G. (1990). WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8, 52-6, 29.
59. Walders-Harbeck, B., Khaitlina, S.Y., Hinssen, H., Jockusch, B.M., and Illenberger, S. (2002). The vasodilator-stimulated phosphoprotein promotes actin polymerisation through direct binding to monomeric actin. FEBS Lett. 529, 275-280.
60. Welch, M.D., Rosenblatt, J., Skoble, J., Portnoy, D.A., and Mitchison, T.J. (1998). Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281, 105-108.
61. Wishart, D.S., Sykes, B.D., and Richards, F.M. (1992). The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31, 1647-1651.
62. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids (New York, USA: John Wiley & Sons).
63. Zigmond, S.H. (2000). How WASP regulates actin polymerization. J. Cell Biol. 150, F117-F120.
64. Zimmermann, J., Labudde, D., Jarchau, T., Walter, U., Oschkinat, H., and Ball, L.J. (2002). Relaxation, equilibrium oligomerization, and molecular symmetry of the VASP (336-380) EVH2 tetramer. Biochemistry 41, 11143-11151.