Competitive binding of UBPY and ubiquitin to the STAM2 SH3 domain revealed by NMR

FEBS Letters

Volumn 586, Issue 19, 2012, Pages 3379-3384

  Lange, Anja ^a   Ismail, Mouhamad Baligh ^a   Rivière, Gwladys ^a   Hologne, Maggy ^a   Lacabanne, Denis ^a   Guillière, Florence ^a   Lancelin, Jean Marc ^a   Krimm, Isabelle ^a   Walker, Olivier ^a  

^a UNIVERSITÉ LYON 1   (France)

Author keywords

Deubiquitinating enzyme; Endocytosis; Nuclear magnetic resonance; Protein protein interaction; STAM2 UIM SH3; UBPY

Indexed keywords

SIGNAL TRANSDUCING ADAPTOR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN 2; UBIQUITIN; UBIQUITIN CARBOXY TERMINAL HYDROLASE 8; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING COMPETITION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; STRUCTURAL HOMOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BINDING, COMPETITIVE; ENDOPEPTIDASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SRC HOMOLOGY DOMAINS; UBIQUITIN; UBIQUITIN THIOLESTERASE;

EID: 84866611630     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.07.047     Document Type: Article

References (43)

1. R.C. Piper, and P.J. Lehner Endosomal transport via ubiquitination Trends Cell Biol. 21 2011 647 655
2. W.M. Henne, N.J. Buchkovich, and S.D. Emr The ESCRT pathway Dev. Cell 21 2011 77 91
3. E. Lauwers, C. Jacob, and B. Andre K63-Linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway J. Cell Biol. 185 2009 493 502
4. I. Dikic, S. Wakatsuki, and K.J. Walters Ubiquitin-binding domains-from structures to functions Nat. Rev. Mol. Cell Biol. 10 2009 659 671
5. O. Lohi, and V.P. Lehto VHS domain marks a group of proteins involved in endocytosis and vesicular trafficking FEBS Lett. 440 1998 255 257
6. K. Hofmann, and L. Falquet A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems Trends Biochem. Sci. 26 2001 347 350
7. S. Hirano, M. Kawasaki, H. Ura, R. Kato, C. Raiborg, H. Stenmark, and S. Wakatsuki Double-sided ubiquitin binding of Hrs-UIM in endosomal protein sorting Nat. Struct. Mol. Biol. 13 2006 272 277
8. A.Y. Amerik, and M. Hochstrasser Mechanism and function of deubiquitinating enzymes Biochim. Biophys. Acta 1695 2004 189 207
9. I. Berlin, H. Schwartz, and P.D. Nash Regulation of epidermal growth factor receptor ubiquitination and trafficking by the USP8.STAM complex J. Biol. Chem. 285 2010 34909 34921
10. T. Kaneko, T. Kumasaka, T. Ganbe, T. Sato, K. Miyazawa, N. Kitamura, and N. Tanaka Structural insight into modest binding of a non-PXXP ligand to the signal transducing adaptor molecule-2 Src homology 3 domain J. Biol. Chem. 278 2003 48162 48168
11. J. McCullough, M.J. Clague, and S. Urbé AMSH is an endosome-associated ubiquitin isopeptidase J. Cell Biol. 166 2004 487 492
12. S. Niendorf Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo Mol. Cell. Biol. 27 2007 5029 5039
13. I. Berlin, K.M. Higginbotham, R.S. Dise, M.I. Sierra, and P.D. Nash The deubiquitinating enzyme USP8 promotes trafficking and degradation of the chemokine receptor 4 at the sorting endosome J. Biol. Chem. 285 2010 37895 37908
14. A. Lange, D. Hoeller, H. Wienk, O. Marcillat, J.-M. Lancelin, and O. Walker NMR reveals a different mode of binding of the Stam2 VHS domain to ubiquitin and diubiquitin Biochemistry 50 2011 48 62
15. R. Varadan, O. Walker, C.M. Pickart, and D. Fushman Structural properties of polyubiquitin chains in solution J. Mol. Biol. 324 2002 637 647
16. C.M. Pickart, and S. Raasi Controlled synthesis of polyubiquitin chains Methods Enzymol. 399 2005 21 36
17. D. Zhang, S. Raasi, and D. Fushman Affinity makes the difference. Non-selective interaction of the UBA domain of ubiquilin-1 with monomeric ubiquitin and polyubiquitin chains J. Mol. Biol. 377 2008 162 180
18. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMR pipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
19. B.A. Johnson, and R.A. Blevins NMR view: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
20. J.B. Hall, and D. Fushman Characterization of the overall and local dynamics of a protein with intermediate rotational anisotropy: differentiating between conformational exchange and anisotropic diffusion in the B3 domain of protein G J. Biomol. NMR 27 2003 261 275
21. D. Fushman, S. Cahill, and D. Cowburn The main-chain dynamics of the dynamin pleckstrin homology (PH) domain in solution: analysis of 15N relaxation with monomer/dimer equilibration J. Mol. Biol. 266 1997 173 194
22. Goddard, T.D. and Kneller, D.G. SPARKY 3, University of California, San francisco, CA.
23. A. Lange, C. Castaneda, D. Hoeller, J.M. Lancelin, D. Fushman, and O. Walker Evidence for cooperative and domain-specific binding of the signal transducing adaptor molecule 2 (STAM2) to Lys63-linked diubiquitin J. Biol. Chem. 287 2012 18687 18699
24. K.A. Swanson, R.S. Kang, S.D. Stamenova, L. Hicke, and I. Radhakrishnan Solution structure of Vps27 UIM-ubiquitin complex important for endosomal sorting and receptor downregulation EMBO J. 22 2003 4597 4606
25. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
26. D.S. Wishart, and B.D. Sykes The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data J. Biomol. NMR 4 1994 171 180
27. Y. Shen, F. Delaglio, G. Cornilescu, and A. Bax TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44 2009 213 223
28. M.H. Wright, I. Berlin, and P.D. Nash Regulation of endocytic sorting by ESCRT-DUB-mediated deubiquitination Cell Biochem. Biophys. 60 2011 39 46
29. M. Kato, K. Miyazawa, and N. Kitamura A deubiquitinating enzyme UBPY interacts with the Src homology 3 domain of Hrs-binding protein via a novel binding motif PX(V/I)(D/N)RXXKP J. Biol. Chem. 275 2000 37481 37487
30. M. Komada, and N. Kitamura Hrs and hbp: possible regulators of endocytosis and exocytosis Biochem. Biophys. Res. Commun. 281 2001 1065 1069
31. R. Ren, B.J. Mayer, P. Cicchetti, and D. Baltimore Identification of a ten-amino acid proline-rich SH3 binding site Science 259 1993 1157 1161
32. S. Feng, J.K. Chen, H. Yu, J.A. Simon, and S.L. Schreiber Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions Science 266 1994 1241 1247
33. Q. Liu, D. Berry, P. Nash, T. Pawson, C.J. McGlade, and S.S. Li Structural basis for specific binding of the Gads SH3 domain to an RxxK motif-containing SLP-76 peptide: a novel mode of peptide recognition Mol. Cell 11 2003 471 481
34. I. Bezsonova, M.C. Bruce, S. Wiesner, H. Lin, D. Rotin, and J.D. Forman-Kay Interactions between the three CIN85 SH3 domains and ubiquitin: implications for CIN85 ubiquitination Biochemistry 47 2008 8937 8949
35. S.D. Stamenova, M.E. French, Y. He, S.A. Francis, Z.B. Kramer, and L. Hicke Ubiquitin binds to and regulates a subset of SH3 domains Mol. Cell 25 2007 273 284
36. Y. He, L. Hicke, and I. Radhakrishnan Structural basis for ubiquitin recognition by SH3 domains J. Mol. Biol. 373 2007 190 196
37. Y.J. Im, T. Wollert, E. Boura, and J.H. Hurley Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis Dev. Cell 17 2009 234 243
38. C. Raiborg, and H. Stenmark The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins Nature 458 2009 445 452
39. S. Saksena, J. Sun, T. Chu, and S.D. Emr ESCRTing proteins in the endocytic pathway Trends Biochem. Sci. 32 2007 561 573
40. E. Mizuno, T. Iura, A. Mukai, T. Yoshimori, N. Kitamura, and M. Komada Regulation of epidermal growth factor receptor down-regulation by UBPY-mediated deubiquitination at endosomes Mol. Biol. Cell 16 2005 5163 5174
41. K. Bowers, S.C. Piper, M.A. Edeling, S.R. Gray, D.J. Owen, P.J. Lehner, and J.P. Luzio Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class I is independent of mammalian ESCRTII J. Biol. Chem. 281 2006 5094 5105
42. P.E. Row, I.A. Prior, J. McCullough, M.J. Clague, and S. Urbé The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation J. Biol. Chem. 281 2006 12618 12624
43. E. Mizuno, K. Kobayashi, A. Yamamoto, N. Kitamura, and M. Komada A deubiquitinating enzyme UBPY regulates the level of protein ubiquitination on endosomes Traffic 7 2006 1017 1031