Conformational change upon ligand binding and dynamics of the PDZ domain from leukemia-associated Rho guanine nucleotide exchange factor

Protein Science

Volumn 17, Issue 6, 2008, Pages 1003-1014

  Liu, Jiangxin ^a   Zhang, Jiahai ^a   Yang, Yinshan ^b,c   Huang, Hongda ^a   Shen, Weiqun ^a   Hu, Qi ^a   Wang, Xingsheng ^a   Wu, Jihui ^a,d   Shi, Yunyu ^a,d  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^c CNRS   (France)

^d UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Complex structure; Conformational change; Internal motions; LARG PDZ; NMR; Protein peptide interaction

Indexed keywords

LEUKEMIA ASSOCIATED RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; LIGAND; NITROGEN 15; OCTAPEPTIDE; PDZ PROTEIN; PLEXIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DENSITY; LIGAND BINDING; MOLECULAR DYNAMICS; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; THERMODYNAMICS;

AMINO ACID SEQUENCE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 44349160152     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.073416508     Document Type: Article

References (47)

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. Artigiani, S., Comoglio, P.M., and Tamagnone, L. 1999. Plexins, semaphorins, and scatter factor receptors: A common root for cell guidance signals? IUBMB Life 48: 477-482.
3. Aurandt, J., Vikis, H.G., Gutkind, J.S., Ahn, N., and Guan, K.L. 2002. The semaphorin receptor plexin-B1 signals through a direct interaction with the Rho-specific nucleotide exchange factor, LARG. Proc. Natl. Acad. Sci. 99: 12085-12090.
4. Basdevant, N., Weinstein, H., and Ceruso, M. 2006. Thermodynamic basis for promiscuity and selectivity in protein-protein interactions: PDZ domains, a case study. J. Am. Chem. Soc. 128: 12766-12777.
5. Bezprozvanny, I. and Maximov, A. 2001. Classification of PDZ domains. FEBS Lett. 509: 457-462.
6. Birrane, G., Chung, J., and Ladias, J.A. 2003. Novel mode of ligand recognition by the Erbin PDZ domain. J. Biol. Chem. 278: 1399-1402.
7. 2+ signaling, and cytoskeleton modification in head and neck squamous cell carcinoma cells. J. Biol. Chem. 281: 14026-14040.
8. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
9. 1H NMR spectroscopy. Biochemistry 29: 7387-7401.
10. 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.
11. 1H PFG double-quantum experiments for the proton resonance assignment of a ligand bound to a protein. J. Magn. Reson. 131: 148-153.
12. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., and Bax, A. 1995. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6: 277-293.
13. Dosset, P., Hus, J.C., Blackledge, M., and Marion, D. 2000. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR 16: 23-28.
14. Dyson, H.J. and Wright, P.E. 2001. Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states. Methods Enzymol. 339: 258-270.
15. Eldho, N.V. and Dayie, K.T. 2007. Internal bulge and tetraloop of the catalytic domain 5 of a group II intron ribozyme are flexible: Implications for catalysis. J. Mol. Biol. 365: 930-944.
16. 15N NMR relaxation. Biochemistry 33: 5984-6003.
17. 15N relaxation data exclusively. J. Biomol. NMR 6: 153-162.
18. Feng, W., Fan, J.S., Jiang, M., Shi, Y.W., and Zhang, M. 2002. PDZ7 of glutamate receptor interacting protein binds to its target via a novel hydrophobic surface area. J. Biol. Chem. 277: 41140-41146.
19. Fuentes, E.J., Der, C.J., and Lee, A.L. 2004. Ligand-dependent dynamics and intramolecular signaling in a PDZ domain. J. Mol. Biol. 335: 1105-1115.
20. Gianni, S., Walma, T., Arcovito, A., Calosci, N., Bellelli, A., Engstrom, A., Travaglini-Allocatelli, C., Brunori, M., Jemth, P., and Vuister, G.W. 2006. Demonstration of long-range interactions in a PDZ domain by NMR, kinetics, and protein engineering. Structure 14: 1801-1809.
21. Hall, A. 1994. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10: 31-54.
22. Holm, L. and Sander, C. 1993. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233: 123-138.
23. Kaibuchi, K., Kuroda, S., and Amano, M. 1999. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68: 459-486.
24. Kang, B.S., Cooper, D.R., Devedjiev, Y., Derewenda, U., and Derewenda, Z.S. 2003. Molecular roots of degenerate specificity in syntenin's PDZ2 domain: Reassessment of the PDZ recognition paradigm. Structure 11: 845-853.
25. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28: 8972-8979.
26. Kelker, M.S., Dancheck, B., Ju, T., Kessler, R.P., Hudak, J., Nairn, A.C., and Peti, W. 2007. Structural basis for spinophilin-neurabin receptor interaction. Biochemistry 46: 2333-2344.
27. Koradi, R., Billeter, M., and Wuthrich, K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14: 29-32, 51-55.
28. Kourlas, P.J., Strout, M.P., Becknell, B., Veronese, M.L., Croce, C.M., Theil, K.S., Krahe, R., Ruutu, T., Knuutila, S., Bloomfield, C.D., et al. 2000. Identification of a gene at 11q23 encoding a guanine nucleotide exchange factor: Evidence for its fusion with MLL in acute myeloid leukemia. Proc. Natl. Acad. Sci. 97: 2145-2150.
29. Kristelly, R., Gao, G., and Tesmer, J.J. 2004. Structural determinants of RhoA binding and nucleotide exchange in leukemia-associated Rho guanine-nucleotide exchange factor. J. Biol. Chem. 279: 47352-47362.
30. Kuang, Z., Yao, S., Keizer, D.W., Wang, C.C., Bach, L.A., Forbes, B.E., Wallace, J.C., and Norton, R.S. 2006. Structure, dynamics and heparin binding of the C-terminal domain of insulin-like growth factor-binding protein-2 (IGFBP-2). J. Mol. Biol. 364: 690-704.
31. Kurschner, C., Mermelstein, P.G., Holden, W.T., and Surmeier, D.J. 1998. CIPP, a novel multivalent PDZ domain protein, selectively interacts with Kir4.0 family members, NMDA receptor subunits, neurexins, and neuroligins. Mol. Cell. Neurosci. 11: 161-172.
32. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R., and Thornton, J.M. 1996. AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8: 477-486.
33. Longhurst, D.M., Watanabe, M., Rothstein, J.D., and Jackson, M. 2006. Interaction of PDZRhoGEF with microtubule-associated protein 1 light chains: Link between microtubules, actin cytoskeleton, and neuronal polarity. J. Biol. Chem. 281: 12030-12040.
34. Maguire, M.L., Guler-Gane, G., Nietlispach, D., Raine, A.R., Zorn, A.M., Standart, N., and Broadhurst, R.W. 2005. Solution structure and backbone dynamics of the KH-QUA2 region of the Xenopus STAR/GSG quaking protein. J. Mol. Biol. 348: 265-279.
35. Oinuma, I., Ishikawa, Y., Katoh, H., and Negishi, M. 2004. The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 305: 862-865.
36. Paduch, M., Biernat, M., Stefanowicz, P., Derewenda, Z.S., Szewczuk, Z., and Otlewski, J. 2007. Bivalent peptides as models for multimeric targets of PDZ domains. Chembiochem 8: 443-452.
37. Palmer III., A.G. 2004. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 104: 3623-3640.
38. Peng, J.W. and Wagner, G. 1992. Mapping of the spectral densities of N-H bond motions in Eglin c using heteronuclear relaxation experiments. Biochemistry 31: 8571-8586.
39. Reuther, G.W., Lambert, Q.T., Booden, M.A., Wennerberg, K., Becknell, B., Marcucci, G., Sondek, J., Caligiuri, M.A., and Der, C.J. 2001. Leukemia-associated Rho guanine nucleotide exchange factor, a Dbl family protein found mutated in leukemia, causes transformation by activation of RhoA. J. Biol. Chem. 276: 27145-27151.
40. Schmidt, A. and Hall, A. 2002. Guanine nucleotide exchange factors for Rho GTPases: Turning on the switch. Genes & Dev. 16: 1587-1609.
41. Skelton, N.J., Koehler, M.F., Zobel, K., Wong, W.L., Yeh, S., Pisabarro, M.T., Yin, J.P., Lasky, L.A., and Sidhu, S.S. 2003. Origins of PDZ domain ligand specificity. Structure determination and mutagenesis of the Erbin PDZ domain. J. Biol. Chem. 278: 7645-7654.
42. Songyang, Z., Fanning, A.S., Fu, C., Xu, J., Marfatia, S.M., Chishti, A.H., Crompton, A., Chan, A.C., Anderson, J.M., and Cantley, L.C. 1997. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275: 73-77.
43. Swiercz, J.M., Kuner, R., Behrens, J., and Offermanns, S. 2002. Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35: 51-63.
44. Tamagnone, L., Artigiani, S., Chen, H., He, Z., Ming, G.I., Song, H., Chedotal, A., Winberg, M.L., Goodman, C.S., Poo, M., et al. 1999. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99: 71-80.
45. Taya, S., Inagaki, N., Sengiku, H., Makino, H., Iwamatsu, A., Urakawa, I., Nagao, K., Kataoka, S., and Kaibuchi, K. 2001. Direct interaction of insulin-like growth factor-1 receptor with leukemia-associated RhoGEF. J. Cell Biol. 155: 809-820.
46. von Ossowski, I., Oksanen, E., von Ossowski, L., Cai, C., Sundberg, M., Goldman, A., and Keinanen, K. 2006. Crystal structure of the second PDZ domain of SAP97 in complex with a GluR-A C-terminal peptide. FEBS J. 273: 5219-5229.
47. Zhou, H., Xu, Y., Yang, Y., Huang, A., Wu, J., and Shi, Y. 2005. Solution structure of AF-6 PDZ domain and its interaction with the C-terminal peptides from Neurexin and Bcr. J. Biol. Chem. 280: 13841-13847.