Structural Insights into the Specific Binding of Huntingtin Proline-Rich Region with the SH3 and WW Domains

Structure

Volumn 14, Issue 12, 2006, Pages 1755-1765

  Gao, Yong Guang ^a,c   Yan, Xian Zhong ^b   Song, Ai Xin ^a   Chang, Yong Gang ^a,c   Gao, Xue Chao ^a,c   Jiang, Nan ^b   Zhang, Qi ^b   Hu, Hong Yu ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b NATIONAL CENTER OF BIOMEDICAL ANALYSIS   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

MOLNEURO; PROTEINS

Indexed keywords

HUNTINGTIN; PROLINE; PROTEIN SH3;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; HUNTINGTON CHOREA; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BINDING SITES; HUMANS; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDES; PROLINE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SPIN LABELS; SRC HOMOLOGY DOMAINS;

EID: 33845204276     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2006.09.014     Document Type: Article

References (56)

1. Bao W.J., Gao Y.G., Chang Y.G., Zhang T.Y., Lin X.J., Yan X.Z., and Hu H.Y. Highly efficient expression and purification system of small-size protein domains in Escherichia coli for biochemical characterization. Protein Expr. Purif. 47 (2006) 599-606
2. Barnett P., Bottger G., Klein A.T., Tabak H.F., and Distel B. The peroxisomal membrane protein Pex13p shows a novel mode of SH3 interaction. EMBO J. 19 (2000) 6382-6391
3. Bates G., Harper P., and Jones L. Huntington's Disease (2002), Oxford University Press, Oxford, UK
4. Bedford M.T., Chan D.C., and Leder P. FBP WW domains and the Abl SH3 domain bind to a specific class of proline-rich ligands. EMBO J. 16 (1997) 2376-2383
5. Bompard G., and Caron E. Regulation of WASP/WAVE proteins: making a long story short. J. Cell Biol. 166 (2004) 957-962
6. 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. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
7. Bruschweiler R. New approaches to the dynamic interpretation and prediction of NMR relaxation data from proteins. Curr. Opin. Struct. Biol. 13 (2003) 175-183
8. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
9. Dalgarno D.C., Botfield M.C., and Rickles R.J. SH3 domains and drug design: ligands, structure, and biological function. Biopolymers 43 (1997) 383-400
10. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
11. DiFiglia M., Sapp E., Chase K., Schwarz C., Meloni A., Young C., Martin E., Vonsattel J.P., Carraway R., Reeves S.A., et al. Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14 (1995) 1075-1081
12. DiProspero N.A., Chen E.Y., Charles V., Plomann M., Kordower J.H., and Tagle D.A. Early changes in Huntington's disease patient brains involve alterations in cytoskeletal and synaptic elements. J. Neurocytol. 33 (2004) 517-533
13. Douangamath A., Filipp F.V., Klein A.T., Barnett P., Zou P., Voorn-Brouwer T., Vega M.C., Mayans O.M., Sattler M., Distel B., and Wilmanns M. Topography for independent binding of α-helical and PPII-helical ligands to a peroxisomal SH3 domain. Mol. Cell 10 (2002) 1007-1017
14. Faber P.W., Barnes G.T., Srinidhi J., Chen J., Gusella J.F., and MacDonald M.E. Huntingtin interacts with a family of WW domain proteins. Hum. Mol. Genet. 7 (1998) 1463-1474
15. Farrow N.A., Muhandiram R., Singer A.U., Pascal S.M., Kay C.M., Gish G., Shoelson S.E., Pawson T., Forman-Kay J.D., and Kay L.E. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
16. Feany M.B., and La Spada A.R. Polyglutamines stop traffic: axonal transport as a common target in neurodegenerative diseases. Neuron 40 (2003) 1-2
17. Fedoroff O.Y., Townson S.A., Golovanov A.P., Baron M., and Avis J.M. The structure and dynamics of tandem WW domains in a negative regulator of notch signaling, Suppressor of deltex. J. Biol. Chem. 279 (2004) 34991-35000
18. Fielding L. NMR methods for the determination of protein-ligand dissociation constants. Curr. Top. Med. Chem. 3 (2003) 39-53
19. Goehler H., Lalowski M., Stelzl U., Waelter S., Stroedicke M., Worm U., Droege A., Lindenberg K.S., Knoblich M., Haenig C., et al. A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington's disease. Mol. Cell 15 (2004) 853-865
20. Harjes P., and Wanker E.E. The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem. Sci. 28 (2003) 425-433
21. Holbert S., Denghien I., Kiechle T., Rosenblatt A., Wellington C., Hayden M.R., Margolis R.L., Ross C.A., Dausset J., Ferrante R.J., and Neri C. The Gln-Ala repeat transcriptional activator CA150 interacts with huntingtin: neuropathologic and genetic evidence for a role in Huntington's disease pathogenesis. Proc. Natl. Acad. Sci. USA 98 (2001) 1811-1816
22. Ilsley J.L., Sudol M., and Winder S.J. The WW domain: linking cell signalling to the membrane cytoskeleton. Cell. Signal. 14 (2002) 183-189
23. Johnson B.A., and Blevins R.A. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4 (1994) 603-614
24. Kami K., Takeya R., Sumimoto H., and Kohda D. Diverse recognition of non-PxxP peptide ligands by the SH3 domains from p67(phox), Grb2 and Pex13p. EMBO J. 21 (2002) 4268-4276
25. Kay B.K., Williamson M.P., and Sudol M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14 (2000) 231-241
26. Khoshnan A., Ko J., and Patterson P.H. Effects of intracellular expression of anti-huntingtin antibodies of various specificities on mutant huntingtin aggregation and toxicity. Proc. Natl. Acad. Sci. USA 99 (2002) 1002-1007
27. Koradi R., Billeter M., and Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 (1996) 51-55 29-32
28. Landles C., and Bates G.P. Huntingtin and the molecular pathogenesis of Huntington's disease. Fourth in molecular medicine review series. EMBO Rep. 5 (2004) 958-963
29. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., and Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8 (1996) 477-486
30. Li J.Y., Plomann M., and Brundin P. Huntington's disease: a synaptopathy?. Trends Mol. Med. 9 (2003) 414-420
31. Li S.H., and Li X.J. Huntingtin-protein interactions and the pathogenesis of Huntington's disease. Trends Genet. 20 (2004) 146-154
32. Li S.S. Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem. J. 390 (2005) 641-653
33. Lin K.T., Lu R.M., and Tarn W.Y. The WW domain-containing proteins interact with the early spliceosome and participate in pre-mRNA splicing in vivo. Mol. Cell. Biol. 24 (2004) 9176-9185
34. Liu Y.F., Deth R.C., and Devys D. SH3 domain-dependent association of huntingtin with epidermal growth factor receptor signaling complexes. J. Biol. Chem. 272 (1997) 8121-8124
35. Liu Z., Macias M.J., Bottomley M.J., Stier G., Linge J.P., Nilges M., Bork P., and Sattler M. The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Struct. Fold. Des. 7 (1999) 1557-1566
36. MacDonald M.E., Ambrose C.M., Duyao M.P., Myers R.H., Lin C., Srinidhi L., Barnes G., Taylor S.A., James M., Groot N., et al. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72 (1993) 971-983
37. Mahoney N.M., Rastogi V.K., Cahill S.M., Girvin M.E., and Almo S.C. Binding orientation of proline-rich peptides in solution: polarity of the profilin-ligand interaction. J. Am. Chem. Soc. 122 (2000) 7851-7852
38. Martin J.B., and Gusella J.F. Huntington's disease. Pathogenesis and management. N. Engl. J. Med. 315 (1986) 1267-1276
39. Mayer B.J. SH3 domains: complexity in moderation. J. Cell Sci. 114 (2001) 1253-1263
40. Mizutani K., Suetsugu S., and Takenawa T. FBP11 regulates nuclear localization of N-WASP and inhibits N-WASP-dependent microspike formation. Biochem. Biophys. Res. Commun. 313 (2004) 468-474
41. Modregger J., DiProspero N.A., Charles V., Tagle D.A., and Plomann M. PACSIN 1 interacts with huntingtin and is absent from synaptic varicosities in presymptomatic Huntington's disease brains. Hum. Mol. Genet. 11 (2002) 2547-2558
42. Musacchio A. How SH3 domains recognize proline. Adv. Protein Chem. 61 (2002) 211-268
43. Nilges M., Macias M.J., O'Donoghue S.I., and Oschkinat H. Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from β-spectrin. J. Mol. Biol. 269 (1997) 408-422
44. Passani L.A., Bedford M.T., Faber P.W., McGinnis K.M., Sharp A.H., Gusella J.F., Vonsattel J.P., and MacDonald M.E. Huntingtin's WW domain partners in Huntington's disease post-mortem brain fulfill genetic criteria for direct involvement in Huntington's disease pathogenesis. Hum. Mol. Genet. 9 (2000) 2175-2182
45. Peterson R.D., Theimer C.A., Wu H., and Feigon J. New applications of 2D filtered/edited NOESY for assignment and structure elucidation of RNA and RNA-protein complexes. J. Biomol. NMR 28 (2004) 59-67
46. Pires J.R., Parthier C., Aido-Machado R., Wiedemann U., Otte L., Bohm G., Rudolph R., and Oschkinat H. Structural basis for APPTPPPLPP peptide recognition by the FBP11WW1 domain. J. Mol. Biol. 348 (2005) 399-408
47. Press W.H., Teukolsky S.A., and Vetterling W.T. Numerical Recipes in C. Second Edition (1992), Cambridge University Press, Cambridge, UK
48. Qin Z.H., Wang Y., Sapp E., Cuiffo B., Wanker E., Hayden M.R., Kegel K.B., Aronin N., and DiFiglia M. Huntingtin bodies sequester vesicle-associated proteins by a polyproline-dependent interaction. J. Neurosci. 24 (2004) 269-281
49. Santamaria F., Wu Z., Boulegue C., Pal G., and Lu W. Reexamination of the recognition preference of the specificity pocket of the Abl SH3 domain. J. Mol. Recognit. 16 (2003) 131-138
50. Sittler A., Walter S., Wedemeyer N., Hasenbank R., Scherzinger E., Eickhoff H., Bates G.P., Lehrach H., and Wanker E.E. SH3GL3 associates with the Huntingtin exon 1 protein and promotes the formation of polygln-containing protein aggregates. Mol. Cell 2 (1998) 427-436
51. Sudol M. Structure and function of the WW domain. Prog. Biophys. Mol. Biol. 65 (1996) 113-132
52. Sugars K.L., and Rubinsztein D.C. Transcriptional abnormalities in Huntington disease. Trends Genet. 19 (2003) 233-238
53. Sun Y., Savanenin A., Reddy P.H., and Liu Y.F. Polyglutamine-expanded huntingtin promotes sensitization of N-methyl-D-aspartate receptors via post-synaptic density 95. J. Biol. Chem. 276 (2001) 24713-24718
54. Vonsattel J.P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., and Richardson Jr. E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44 (1985) 559-577
55. Wiesner S., Stier G., Sattler M., and Macias M.J. Solution structure and ligand recognition of the WW domain pair of the yeast splicing factor Prp40. J. Mol. Biol. 324 (2002) 807-822
56. Zarrinpar A., Bhattacharyya R.P., and Lim W.A. The structure and function of proline recognition domains. Sci. STKE 2003 (2003) RE8