NMR analysis of protein interactions

Current Opinion in Chemical Biology

Volumn 9, Issue 5, 2005, Pages 501-508

  Bonvin, Alexandre M J J ^a   Boelens, Rolf ^a   Kaptein, Robert ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOTROPY; DNA RNA HYBRIDIZATION; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN DNA INTERACTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW;

DNA; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS;

EID: 25144506939     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2005.08.011     Document Type: Review

References (68)

1. K. Pervushin, R. Riek, G. Wider, and K. Wüthrich Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution Proc Natl Acad Sci USA 94 1997 12366 12371
2. J.H. Prestegard, and A.I. Kishore Partial alignment of biomolecules: an aid to NMR characterization Curr Opin Chem Biol 5 2001 584 590
3. M. Blackledge Recent progress in the study of biomolecular structure and dynamics in solution from residual dipolar couplings Prog Nucl Magn Reson Spectrosc 46 2005 23 61
4. T. Diercks, M. Coles, and H. Kessler Applications of NMR in drug discovery Curr Opin Chem Biol 5 2001 285 291
5. H.O. Villar, J. Yan, and M.R. Hansen Using NMR for ligand discovery and optimization Curr Opin Chem Biol 8 2004 387 391
6. G.M. Clore Accurate and rapid docking of protein-protein complexes on the basis of intermolecular nuclear Overhauser enhancement data and dipolar couplings by rigid body minimization Proc Natl Acad Sci USA 97 2000 9021 9025
7. M.A. McCoy, and D.F. Wyss Structures of protein-protein complexes are docked using only NMR restraints from residual dipolar coupling and chemical shift perturbations J Am Chem Soc 124 2002 2104 2105
8. X.P. Xu, and D.A. Case Automated prediction of N-15, C-13(alpha), C-13(beta) and C-13′ chemical shifts in proteins using a density functional database J Biomol NMR 21 2001 321 333
9. C. Dominguez, R. Boelens, and Bonvin AMJJ HADDOCK: a protein-protein docking approach based on biochemical or biophysical information J Am Chem Soc 125 2003 1731 1737 The use of CSP and mutagenesis data to model biomolecular interactions is demonstrated for three protein-protein complexes. Interface mapping information is introduced as ambiguous interaction restraints to drive the docking process using a combination of rigid body minimization and semi-flexible simulated annealing refinement.
10. ••] is complemented by RDC restraints which can resolve possible orientational ambiguities.
11. A.D.J. van Dijk, D. Fushman, and A.M.J.J. Bonvin Various strategies of using residual dipolar couplings in NMR-driven protein docking: application to Lys48-linked di-ubiquitin and validation against 15N-relaxation data Proteins 60 2005 367 381
12. X.J. Morelli, P.N. Palma, F. Guerlesquin, and A.C. Rigby A novel approach for assessing macromolecular complexes combining soft-docking calculations with NMR data Protein Sci 10 2001 2131 2137
13. A. Dobrodumov, and A.M. Gronenborn Filtering and selection of structural models: combining docking and NMR Proteins 53 2003 18 32
14. A. Fahmy, and G. Wagner TreeDock: a tool for protein docking based on minimizing van der Waals energies J Am Chem Soc 124 2002 1241 1250
15. P.J. Hajduk, J.C. Mack, E.T. Olejniczak, C. Park, P.J. Dandliker, and B.A. Beutel SOS-NMR: A saturation transfer NMR-based method for determining the structures of protein-ligand complexes J Am Chem Soc 126 2004 2390 2398
16. M.L. Reese, and V. Dotsch Fast mapping of protein-protein interfaces by NMR spectroscopy J Am Chem Soc 125 2003 14250 14251
17. H. Takahashi, T. Nakanishi, K. Kami, Y. Arata, and I. Shimada A novel NMR method for determining the interfaces of large protein-protein complexes Nat Struct Biol 7 2000 220 223
18. T. Matsuda, T. Ikegami, N. Nakajima, T. Yamazaki, and H. Nakamura Model building of a protein-protein complexed structure using saturation transfer and residual dipolar coupling without paired intermolecular NOE J Biomol NMR 29 2004 325 338
19. M. Prudêncio, and M. Ubbink Transient complexes of redox proteins: structural and dynamic details from NMR studies J Mol Recognit 17 2004 524 539
20. V. Gaponenko, S.P. Sarma, A.S. Altieri, D.A. Horita, J. Li, and R.A. Byrd Improving the accuracy of NMR structures of large proteins using pseudocontact shifts as long-range restraints J Biomol NMR 28 2004 205 212
21. S. Arumugam, and S.R. Van Doren Global orientation of bound MMP-3 and N-TIMP-1 in solution via residual dipolar couplings Biochemistry 42 2003 7950 7958
22. M. Sakakura, S. Noba, P.A. Luchette, I. Shimada, and R.S. Prosser An NMR method for the determination of protein-binding interfaces using dioxygen-induced spin-lattice relaxation enhancement J Am Chem Soc 127 2005 5826 5832
23. D. Fushman, R. Varadan, M. Assfalg, and O. Walker Determining domain orientation in macromolecules by using spin-relaxation and residual dipolar coupling measurements Prog Nucl Magn Reson Spectrosc 44 2004 189 214
24. -3 M) was solved de novo using a combination of NOEs and RDCs, nicely illustrating the power of NMR when it comes to studying weak interactions.
25. Z.-YJ. Sun, S.T. Kim, I.C. Kim, A. Fahmy, E.L. Reinherz, and G. Wagner Solution structure of the CD3epsilondelta ectodomain and comparison with CD3epsilongamma as a basis for modeling T cell receptor topology and signaling Proc Natl Acad Sci USA 101 2004 16867 16872
26. S.L. Alam, J. Sun, M. Payne, B.D. Welch, B.K. Blake, D.R. Davis, H.H. Meyer, S.D. Emr, and W.I. Sundquist Ubiquitin interactions of NZF zinc fingers EMBO J 23 2004 1411 1421
27. A. Thiru, D. Nietlispach, H.R. Mott, M. Okuwaki, D. Lyon, P.R. Nielsen, M. Hirshberg, A. Verreault, N.V. Murzina, and E.D. Laue Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin EMBO J 23 2004 489 499
28. I. Vakonakis LiWang AC: Structure of the C-terminal domain of the clock protein KaiA in complex with a KaiC-derived peptide: implications for KaiC regulation Proc Natl Acad Sci USA 101 2004 10925 10930
29. W. Feng, J.-F. Long, J.-S. Fan, T. Suetake, and M. Zhang The tetrameric L27 domain complex as an organization platform for supramolecular assemblies Nat Struct Mol Biol 11 2004 475 480
30. R.N. De Guzman, M.A. Martinez-Yamout, H.J. Dyson, and P.E. Wright Interaction of the TAZ1 domain of the CREB-binding protein with the activation domain of CITED2: regulation by competition between intrinsically unstructured ligands for non-identical binding sites J Biol Chem 279 2004 3042 3049
31. J.D. Gross, N.J. Moerke, T. von der Haar, A.A. Lugovskoy, A.B. Sachs, J.E.G. McCarthy, and G. Wagner Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E Cell 115 2003 739 750 The solution structure of the large (312 amino acid) complex between the eukaryotic initiation factors 4G and 4E is described. The NOE information was supplemented by restraints derived from paramagnetic broadening effects. An interesting aspect of this complex is that it is the result of a coupled folding transition of its components.
32. M. Cai, D.C. Williams, G. Wang, B.R. Lee, A. Peterkofsky, and G.M. Clore Solution structure of the phosphoryl transfer complex between the signal-transducing protein IIAGlucose and the cytoplasmic domain of the glucose transporter IICBGlucose of the Escherichia coli glucose phosphotransferase system J Biol Chem 278 2003 25191 25206 This complex was solved de novo to high precision using a combination of NOEs, several sets of RDCs and CαCβ chemical shift restraints. This work illustrates state-of-the art NMR methodology for the structural studies of protein-protein complexes.
33. R.S. Kang, C.M. Daniels, S.A. Francis, S.C. Shih, W.J. Salerno, L. Hicke, and I. Radhakrishnan Solution structure of a CUE-ubiquitin complex reveals a conserved mode of ubiquitin binding Cell 113 2003 621 630
34. T.D. Mueller, and J. Feigon Structural determinants for the binding of ubiquitin-like domains to the proteasome EMBO J 22 2003 4634 4645
35. S.J. Freedman, Z.-YJ. Sun, A.L. Kung, D.S. France, G. Wagner, and M.J. Eck Structural basis for negative regulation of hypoxia-inducible factor-1alpha by CITED2 Nat Struct Biol 10 2003 504 512
36. mannose was assembled from the unbound components using a conjoint rigid body/torsion angle simulated annealing procedure on the basis of intermolecular NOEs and RDCs.
37. F. Arnesano, L. Banci, I. Bertini, and A.M.J.J. Bonvin A docking approach to the study of copper trafficking proteins; interaction between metallochaperones and soluble domains of copper ATPases Structure (Camb) 12 2004 669 676
38. I. Díaz-Moreno, A. Díaz-Quintana, M.A. De la Rosa, and M. Ubbink Structure of the complex between plastocyanin and cytochrome f from the cyanobacterium Nostoc sp. PCC 7119 as determined by paramagnetic NMR: the balance between electrostatic and hydrophobic interactions within the transient complex determines the relative orientation of the two proteins J Biol Chem 280 2005 18908 18915 The potential of paramagnetic NMR for the study of weak and transient complexes is demonstrated: CSP data and intermolecular pseudo contact shifts are introduced in a rigid-body calculation to determine the relative orientation of the two molecules.
39. C. Dominguez, A.M.J.J. Bonvin, G.S. Winkler, F.M.A. van Schaik, H.T.M. Timmers, and R. Boelens Structural model of the UbcH5B/CNOT4 complex revealed by combining NMR, mutagenesis, and docking approaches Structure (Camb) 12 2004 633 644 CSP data in combination with site-directed mutagenesis were used in HADDOCK to model the UbcH5B/CNOT4 complex. Charge reversal mutants could be generated based on the docking models in which the identity of a Lys and Glu were switched across the interface. These swapped mutations were shown to restore binding in a two-hybrid binding assay.
40. A.I. Arunkumar, V. Klimovich, X. Jiang, R.D. Ott, L. Mizoue, E. Fanning, and W.J. Chazin Insights into hRPA32 C-terminal domain-mediated assembly of the simian virus 40 replisome Nat Struct Mol Biol 12 2005 332 339 The interaction between hRPA32C and the Tag origin DBD is studied by affinity chromatography, NMR and site-directed mutagenesis. The latter was guided by a structural model of the complex generated from CSP data and independently validated with RDC data.
41. B. Dangi, A.M. Gronenborn, J.L. Rosner, and R.G. Martin Versatility of the carboxy-terminal domain of the alpha subunit of RNA polymerase in transcriptional activation: use of the DNA contact site as a protein contact site for MarA Mol Microbiol 54 2004 45 59 The ternary complex of the C-terminal domain of the α-subunit of RNA polymerase with the transcription factor MarA and DNA was modeled with HADDOCK using NMR-based chemical shift mapping.
42. N.U. Jain, T.J.O. Wyckoff, C.R.H. Raetz, and J.H. Prestegard Rapid analysis of large protein-protein complexes using NMR-derived orientational constraints: the 95 kDa complex of LpxA with acyl carrier protein J Mol Biol 343 2004 1379 1389 This article demonstrates that NMR can play a role in the analysis of very large complexes: by combining RDC and CSP data measured for the small (9 kDa) acyl carrier protein with mutagenesis data for LpxA and exploiting the internal C3 symmetry for alignment, the 95kDa homotrimeric complex could be modelled.
43. A. Messias, and M. Sattler Structural basis of single-stranded RNA recognition Acc Chem Res 37 2004 279 287
44. C. Maris, C. Dominguez, and F. Allain The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression FEBS J. 272 2005 2118 2131
45. C. Johansson, L. Finger, L. Trantirek, T. Mueller, S. Kim, I. Laird-Offringa, and J. Feigon Solution structure of the complex formed by the two N-terminal RNA-binding domains of nucleolin and a pre-rRNA target J Mol Biol 337 2004 799 816 The first two RNA-binding domains of nucleolin are responsible for RNA-binding specificity and affinity. The linker between the domains, flexible in free nucleolin, becomes structured in the complex due to extensive contacts to the b2NRE major groove.
46. F. Allain, Y. Yen, J. Masse, and P. Schultze T D, J F: Molecular basis of sequence-specific recognition of pre-ribosomal RNA by nucleolin EMBO J 19 2000 6870 6881
47. Z. Liu, I. Luyten, M. Bottomley, A. Messias, S. Houngninou-Molango, R. Sprangers, K. Zanier, A. Kramer, and M. Sattler Structural basis for recognition of the intron branch site RNA by splicing factor 1 Science 294 2001 1098 1102
48. D. Lu, M. Searles, and A. Klug Crystal structure of a zinc-finger-RNA complex reveals two modes of molecular recognition Nature 426 2003 96 100
49. B. Hudson, M. Martinez-Yamout, H. Dyson, and P. Wright Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d Nat Struct Mol Biol 11 2004 257 264 Two CCCH zinc finger motifs, that represent a large family of eukaryotic proteins, present a platform for highly specific recognition of an AU-rich mRNA sequence. Sequence specificity comes mostly from TIS11d main chain hydrogen bond contacts with the Watson-Crick edges of the bases along the extended mRNA chain.
50. V. D'Souza, and M. Summers Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus Nature 431 2004 586 590
51. A. Dey, and D. York A S-M, MF S: Composition and sequence-dependent binding of RNA to the nucleocapsid protein of Moloney murine leukemia virus Biochemistry 44 2005 3735 3744
52. K. Chang, and A. Ramos The double-stranded RNA-binding motif, a versatile macromolecular docking platform FEBS J. 272 2005 2109 2117
53. H. Wu, A. Henras, G. Chanfreau, and J. Feigon Structural basis for recognition of the AGNN tetraloop RNA fold by the double-stranded RNA-binding domain of Rnt1p RNase III Proc Natl Acad Sci USA 101 2004 8307 8312 Recognition of the dsRNA by the dsRBD is mostly structure specific.
54. A. Lingel, B. Simon, E. Izaurralde, and M. Sattler Nucleic acid 3′-end recognition by the Argonaute2 PAZ domain Nat Struct Mol Biol 11 2004 576 577 This structure reveals a unique mode of single-stranded nucleic acid binding. Specific recognition is mediated by binding of the two-nucleotide 3′ overhang characteristic of siRNAs to a hydrophobic cleft in the PAZ domain.
55. V. Calabro, M. Daugherty, and A. Frankel A single intermolecular contact mediates intramolecular stabilization of both RNA and protein Proc Natl Acad Sci USA 102 2005 6849 6854
56. D.C. Williams, M. Cai, and G.M. Clore Molecular basis for synergistic transcriptional activation by Oct1 and Sox2 revealed from the solution structure of the 42-kDa Oct1.Sox2.Hoxb1-DNA ternary transcription factor complex J Biol Chem 279 2004 1449 1457 This large ternary protein-DNA complex was solved using state of the art NMR methodology. The interaction of two transcription factor domains (Oct1-POU and Sox2) bound to adjacent sites on the DNA suggests a mechanism for cell-specific transcription regulation.
57. C.G. Kalodimos, N. Biris, A.M.J.J. Bonvin, M.M. Levandoski, M. Guennuegues, R. Boelens, and R. Kaptein Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes Science 305 2004 386 389 The structure of a complex of a covalently linked lac repressor headpiece with non-operator DNA is described (see Figure 4). Large differences in structure and dynamics between non-specific and specific complexes provide insight into the way gene regulatory proteins locate their DNA target sites.
58. J. Iwahara, C.D. Schwieters, and G.M. Clore Ensemble approach for NMR structure refinement against (1)H paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule J Am Chem Soc 126 2004 5879 5896
59. J. Iwahara, C.D. Schwieters, and G.M. Clore Characterization of nonspecific protein-DNA interactions by 1H paramagnetic relaxation enhancement J Am Chem Soc 126 2004 12800 12808
60. R.M. Mitton-Fry, E.M. Anderson, D.L. Theobald, L.W. Glustrom, and D.S. Wuttke Structural basis for telemoric single-stranded DNA recognition by Yeast Cdc13 J Mol Biol 338 2004 241 255 Cdc13 binds to single-stranded GT-rich telomere ends and protects them from degradation. The complex of the DNA-binding domain of Cdc13 with telomeric ssDNA explains the high affinity and specificity towards GT-rich single-stranded DNA.
61. S. Rumpel, A. Razeto, C.M. Pillar, V. Vijayan, A. Taylor, K. Giller, M.S. Gilmore, S. Becker, and M. Zweckstetter Structure DNA-binding properties of the cytolysin regulator CylR2 from Enterococcus faecalis EMBO J 23 2004 3632 3642
62. P.L. Surdo, M.J. Bottomley, M. Sattler, and K. Scheffzek Crystal structure and nuclear magnetic resonance analyses of the SAND domain from glucocorticoid modulatory element binding protein-1 reveals deoxyribonucleic acid and zinc binding regions Mol Endocrinol 17 2003 1283 1295
63. C.M. Dupureur NMR studies of restriction enzyme-DNA interactions: role of conformation in sequence specificity Biochemistry 44 2005 5065 5074
64. P. Pristovsek, K. Sengupta, F. Löhr, B. Schäfer, M.W. von Trebra, H. Rüterjans, and F. Bernhard Structural analysis of the DNA-binding domain of the Erwinia amylovora RcsB protein and its interaction with the RcsAB box J Biol Chem 278 2003 17752 17759
65. J.-H. Lee, C.-J. Park, A.I. Arunkumar, W.J. Chazin, and B.-S. Choi NMR study on the interaction between RPA and DNA decamer containing cis-syn cyclobutane pyrimidine dimer in the presence of XPA: implication for damage verification and strand-specific dual incision in nucleotide excision repair Nucleic Acids Res 31 2003 4747 4754
66. G.W. Daughdrill, G.W. Buchko, M.V. Botuyan, C. Arrowsmith, M.S. Wold, M.A. Kennedy, and D.F. Lowry Chemical shift changes provide evidence for overlapping single-stranded DNA- and XPA-binding sites on the 70 kDa subunit of human replication protein A Nucleic Acids Res 31 2003 4176 4183
67. M.E. Stauffer, and W.J. Chazin Physical interaction between replication protein A and Rad51 promotes exchange on single-stranded DNA J Biol Chem 279 2004 25638 25645
68. P.D. Vise, B. Baral, A.J. Latos, and G.W. Daughdrill NMR chemical shift and relaxation measurements provide evidence for the coupled folding and binding of the p53 transactivation domain Nucleic Acids Res 33 2005 2061 2077