Structural analysis of a complex between small ubiquitin-like modifier 1 (SUMO1) and the ZZ domain of CREB-binding protein (CBP/p300) reveals a new interaction surface on SUMO

Journal of Biological Chemistry

Volumn 291, Issue 24, 2016, Pages 12658-12672

  Diehl, Carl ^a,b   Akke, Mikael ^c   Bekker Jensen, Simon ^a   Mailand, Niels ^a   Streicher, Werner ^a,d   Wikström, Mats ^a,e  

^a University of Copenhagen   (Denmark)

^b SARomics Biostructures   (Sweden)

^c LUND UNIVERSITY   (Sweden)

^d NOVOZYMES A S   (Denmark)

^e AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINDING SITES; CHEMICAL SHIFT; EPITOPES; LIGANDS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS;

CARRPURCELL-MEIBOOM-GILL (CPMG); CHEMICAL SHIFT PERTURBATIONS; CREB BINDING PROTEINS; ISOTHERMAL TITRATION CALORIMETRY; RELAXATION DISPERSION; RESIDUAL DIPOLAR COUPLINGS; SMALL UBIQUITIN-LIKE MODIFIERS; STRUCTURAL MODELING;

BINS;

HISTONE ACETYLTRANSFERASE PCAF; NITROGEN 15; SUMO 1 PROTEIN; CREBBP PROTEIN, HUMAN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; EPITOPE; LIGAND; PROTEIN BINDING; SUMO1 PROTEIN, HUMAN;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MOLECULAR DOCKING; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ANALYSIS; ZINC FINGER MOTIF; AMINO ACID SEQUENCE; CALORIMETRY; CHEMISTRY; GENETICS; HUMAN; KINETICS; METABOLISM; MOLECULAR MODEL; PROCEDURES; PROTEIN DOMAIN; PROTEIN MOTIF; THERMODYNAMICS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; CALORIMETRY; CREB-BINDING PROTEIN; EPITOPES; HUMANS; KINETICS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN DOMAINS; SUMO-1 PROTEIN; THERMODYNAMICS;

EID: 84974559357     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.711325     Document Type: Article

References (47)

1. Geiss-Friedlander, R., and Melchior, F. (2007) Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8, 947-956
2. Gareau, J. R., and Lima, C. D. (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation, and recognition. Nat. Rev. Mol. Cell Biol. 11, 861-871
3. Becker, J., Barysch, S. V., Karaca, S., Dittner, C., Hsiao, H. H., Berriel Diaz, M., Herzig, S., Urlaub, H., and Melchior, F. (2013) Detecting endogenous SUMO targets in mammalian cells and tissues. Nat. Struct. Mol. Biol. 20, 525-531
4. Rodriguez, M. S., Dargemont, C., and Hay, R. T. (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654-12659
5. Sampson, D. A., Wang, M., and Matunis, M. J. (2001) The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276, 21664-21669
6. Song, J., Zhang, Z., Hu, W., and Chen, Y. (2005) Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J. Biol. Chem. 280, 40122-40129
7. Chang, C. C., Naik, M. T., Huang, Y. S., Jeng, J. C., Liao, P. H., Kuo, H. Y., Ho, C. C., Hsieh, Y. L., Lin, C. H., Huang, N. J., Naik, N. M., Kung, C. C., Lin, S. Y., Chen, R. H., Chang, K. S., Huang, T. H., and Shih, H. M. (2011) Structural and functional roles of Daxx SIM phosphorylation in SUMO paralog-selective binding and apoptosis modulation. Mol. Cell 42, 62-74
8. Cappadocia, L., Mascle, X. H., Bourdeau, V., Tremblay-Belzile, S., Chaker-Margot, M., Lussier-Price, M., Wada, J., Sakaguchi, K., Aubry, M., Ferbeyre, G., and Omichinski, J. G. (2015) Structural and functional characterization of the phosphorylation-dependent interaction between PML and SUMO1. Structure 23, 126-138
9. Danielsen, J. R., Povlsen, L. K., Villumsen, B. H., Streicher, W., Nilsson, J., Wikström, M., Bekker-Jensen, S., and Mailand, N. (2012) DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding zinc finger. J. Cell Biol. 197, 179-187
10. Hecker, C.-M., Rabiller, M., Haglund, K., Bayer, P., and Dikic, I. (2006) Specification of SUMO1-and SUMO2-interacting motifs. J. Biol. Chem. 281, 16117-16127
11. Legge, G. B., Martinez-Yamout, M. A., Hambly, D. M., Trinh, T., Lee, B. M., Dyson, H. J., and Wright, P. E. (2004) ZZ domain of CBP: an unusual zinc finger fold in a protein interaction module. J. Mol. Biol. 343, 1081-1093
12. Ponting, C. P., Blake, D. J., Davies, K. E., Kendrick-Jones, J., and Winder, S. J. (1996) ZZ and TAZ: new putative zinc fingers in dystrophin and other proteins. Trends Biochem. Sci. 21, 11-13
13. Dominguez, C., Boelens, R., and Bonvin, A. M. (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125, 1731-1737
14. Aslanidis, C., and de Jong, P. J. (1990) Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res. 18, 6069-6074
15. Wang, W., and Malcolm, B. (1999) Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange site-directed mutagenesis. Biotechniques 26, 680-682
16. Neidhardt, F. C., Bloch, P. L., and Smith, D. F. (1974) Culture medium for enterobacteria. J. Bacteriol. 119, 736-747
17. Gileadi, O., Burgess-Brown, N. A., Colebrook, S. M., Berridge, G., Savitsky, P., Smee, C. E., Loppnau, P., Johansson, C., Salah, E., and Pantic, N. H. (2008) High throughput production of recombinant human proteins for crystallography. In Structural Proteomics, pp. 221-246, Springer-Verlag New York Inc., New York
18. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179, 131-137
19. Bayer, P., Arndt, A., Metzger, S., Mahajan, R., Melchior, F., Jaenicke, R., and Becker, J. (1998) Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 280, 275-286
20. Clore, G. M., Bax, A., Driscoll, P. C., Wingfield, P. T., and Gronenborn, A. M. (1990) Assignment of the side-chain proton and carbon-13 resonances of interleukin-1ô using double-and triple-resonance heteronuclear three-dimensional NMR spectroscopy. Biochemistry 29, 8172-8184
21. 15N-enriched proteins. J. Biomol. NMR 1, 99-104
22. Wittekind, M., and Mueller, L. (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the α-and β-carbon resonances in proteins. J. Magn. Reson. B 101, 201-205
23. Grzesiek, S., and Bax, A. (1992) Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114, 6291-6293
24. 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
25. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696
26. Ottiger, M., Delaglio, F., and Bax, A. (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131, 373-378
27. 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
28. Case, D. A., Cheatham, T. E., 3rd, Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. J. (2005) The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688
29. Bhattacharya, A., Tejero, R., and Montelione, G. T. (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66, 778-795
30. Zweckstetter, M., and Bax, A. (2000) Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR. J. Am. Chem. Soc. 122, 3791-3792
31. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., and Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
32. de Vries, S. J., van Dijk, M., and Bonvin, A. M. (2010) The HADDOCK web server for data-driven biomolecular docking. Nat. Protoc. 5, 883-897
33. Meiler, J., Blomberg, N., Nilges, M., and Griesinger, C. (2000) A new approach for applying residual dipolar couplings as restraints in structure elucidation. J. Biomol. NMR 16, 245-252
34. Loria, J. P., Rance, M., and Palmer, A. G. (1999) A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J. Am. Chem. Soc. 121, 2331-2332
35. Mulder, F. A., Mittermaier, A., Hon, B., Dahlquist, F. W., and Kay, L. E. (2001) Studying excited states of proteins by NMR spectroscopy. Nat. Struct. Mol. Biol. 8, 932-935
36. 15N relaxation experiment. J. Magn. Reson. 171, 25-36
37. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55
38. 13C relaxation dispersion measurements of aromatic side chain dynamics and activation barriers in basic pancreatic trypsin inhibitor. Biochemistry 53, 4519-4525
39. Carver, J. P., and Richards, R. E. (1972) A general two-site solution for the chemical exchange produced dependence of T2 upon the carr-Purcell pulse separation. J. Magn. Reson. (1969) 6, 89-105
40. Davis, D. G., Perlman, M. E., and London, R. E. (1994) Direct measurements of the dissociation-rate constant for inhibitor-enzyme complexes via the T1 [rho] and T2 (CPMG) methods. J. Magn. Reson. B 104, 266-275
41. Press, W. H., Flannery, B. P., Teukolsky, S. A., and Vetterling, W. T. (1986) Numerical Recipes: The Art of Scientific Computing, Cambridge University Press, Cambridge
42. Mandel, A. M., Akke, M., and Palmer, A. G. (1995) Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163
43. 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
44. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, Schrodinger, LLC, New York
45. Dosset, P., Hus, J. C., Marion, D., and Blackledge, M. (2001) A novel interactive tool for rigid-body modeling of multi-domain macromolecules using residual dipolar couplings. J. Biomol. NMR 20, 223-231
46. Bernier-Villamor, V., Sampson, D. A., Matunis, M. J., and Lima, C. D. (2002) Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345-356
47. Reverter, D., and Lima, C. D. (2006) Structural basis for SENP2 protease interactions with SUMO precursors and conjugated substrates. Nat. Struct. Mol. Biol. 13, 1060-1068