Elucidating transient macromolecular interactions using paramagnetic relaxation enhancement

Current Opinion in Structural Biology

Volumn 17, Issue 5, 2007, Pages 603-616

  Clore, G Marius ^a   Tang, Chun ^a   Iwahara, Junji ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; TRANSCRIPTION FACTOR;

CONTRAST ENHANCEMENT; DNA STRUCTURE; DYNAMICS; ELECTRON SPIN RESONANCE; GENE TRANSLOCATION; MACROMOLECULE; NUCLEAR MAGNETIC RESONANCE; PARAMAGNETIC RELAXATION ENHACEMENT; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS;

DNA; ELECTRON SPIN RESONANCE SPECTROSCOPY; HOMEODOMAIN PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SEX-DETERMINING REGION Y PROTEIN; SPIN LABELS; THERMODYNAMICS;

EID: 35548943472     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2007.08.013     Document Type: Review

References (58)

1. Solomon I. Relaxation processes in a system of two spins. Phys Rev 99 (1955) 559-565
2. Wüthrich K. NMR of Proteins and Nucleic Acids (1986), John Wiley, New York
3. Clore G.M., and Gronenborn A.M. Two, three and four dimensional NMR methods for obtaining larger and more precise three-dimensional structures of protein in solution. Ann Rev Biophys Biophys Chem 20 (1991) 29-63
4. Bloembergen N., and Morgan L.O. Proton relaxation times in paramagnetic solutions: effects of electron spin relaxation. J Chem Phys 34 (1961) 842-850
5. Cheng H., and Markley J.L. NMR spectroscopic of paramagnetic proteins: iron sulfur proteins. Ann Rev Biophys Biomol Struct 24 (1995) 209-237
6. Bertini I., Luchinat C., and Licciolini M. Paramagnetic probes in metalloproteins. Methods Enzymol 339 (2001) 314-340
7. Ubbink M., Worral J.A.R., Canters G.W., Groenen E.J.J., and Huber M. Paramagnetic resonance of biological metal centers. Ann Rev Biophys Biomolec Struct 31 (2002) 393-422
8. Schmidt P.G., and Kuntz I.D. Distance measurements in spin-labeled lyzozyme. Biochemistry 23 (1984) 4261-4266
9. 1H-NMR of three spin-labeled derivatives of bovine pancreatic trypsin inhibitor. Biochemistry 25 (1986) 2356-2364
10. Kosen P.A. Spin labeling of proteins. Methods Enzymol 177 (1989) 86-121
11. Battiste J.L., and Wagner G. Utilization of site-directed spin-labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear Overhauser effect data. Biochemistry 39 (2000) 5355-5365
12. Gaponenko V., Howarth J.W., Columbus G., Gasmi-Seabrook J., Yuan W.L., Hubbell P.R., and Rosevear P.R. Protein global fold determination using site-directed spin and isotope labeling. Protein Sci 9 (2000) 302-309
13. Donaldson L.W., Skrynnikov W.Y., Choy D.R., Muhandiram B., Sarkar J.D., Forman-Kay J.D., and Kay L.E. Structural characterization of proteins with an attached ATCUN motif by paramagnetic relaxation enhancement NMR spectroscopy. J Am Chem Soc 123 (2001) 9843-9847
14. Dvotretzky A., Gaponenko V., and Rosevear P.R. Derivation of structural restraints using a thiol-reactive chelator. FEBS Lett 528 (2002) 189-192
15. Pintacuda G., Mosref A., Leonchiks A., Shapiro A., and Otting G. Site-specific labeling with a metal chelator for protein structure refinement. J Biomol NMR 29 (2004) 351-361
16. Gillespie J.R., and Shortle D. Characterization of long-range structure in the denatured state of staphylococcal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels. J Mol Biol 268 (1997) 158-169
17. Bertoncini C.W., Jung Y.S., Fernandrez C.O., Hoyer W., Griesinger C., Jovin T.M., and Zweckstetter M. Release of long-range tertiary interactions potentiates aggregation of natively unstructured α-synuclein. Proc Natl Acad Sci USA 102 (2005) 1430-1435. In this study, using both PRE and dipolar coupling measurements, the authors show that intrinsically disordered α-synuclein assumes transient conformations that are stabilized by long-range interactions and act to inhibit oligomerization and aggregation.
18. Dedmon M.M., Lindorff-Larsen K., Chistodoulou J., Vendruscolo M., and Dobson C.M. Mapping long-range interactions in α-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J Am Chem Soc 127 (2005) 476-477. In this study, using PRE measurements the authors show that α-synuclein adopts a broad distribution of conformations with an ensemble averaged hydrodynamic radius that is significantly smaller than that expected for a random coil.
19. Krisjansdottir S., Lindorff-Larsen K., Fieber W., Dobson C.M., Vendruscolo M., and Poulsen F.M. Formation of native and non-native interactions in ensembles of denatured ACBP molecules from paramagnetic relaxation enhancement studies. J Mol Biol 347 (2005) 1053-1062. In this study, the authors use the PRE to show that denatured acyl coenzyme A binding protein has some residual structure with long-range interactions present.
20. Vise P., Baral B., Stancik A., Lowry D.F., and Daughdrill G.W. Identifying long-range structure in the intrinsically unstructured transactivation domain of p53. Proteins: Struct Funct Bioinformatics 67 (2007) 526-530. In this study, the PRE is used to demonstrate the presence of long-range transient structure for the intrinsically disordered activation domain of p53.
21. 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
22. Mal T.K., Ikura M., and Kay L.E. The ATCUN domain as a probe of intermolecular interactions: application to calmodulin-peptide complexes. J Am Chem Soc 124 (2002) 14002-14003
23. Gross J.D., Moerke N.J., van deer Haar R., Lugovsky A.A., Sachs A.B., McCarthy J.E., and Wagner G. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115 (2003) 739-750
24. Card P.B., Erbel P.J.A., and Gardner K.H. Structural basis of ARNT PAS-B dimerization: use of a common β-sheet interface for hetero- and homodimerization. J Mol Biol 353 (2005) 664-677
25. Johnson P.E., Brun E., MacKenzie L.F., Withers S.G., and McIntosh L.P. The cellulose-binding domains from Cellulomonas fimi β-1,4-glucanase CenC bind nitroxide spin-labeled cellooligosaccharides in multiple orientations. J Mol Biol 287 (1999) 609-625
26. Jain N.U., Venot K., Umemoto H., Leffler H., and Prestegard J.H. Distance mapping of protein binding sites using spin-labeled oligosaccharide ligands. Protein Sci 10 (2001) 2393-2400
27. Macnaughtan M.A., Kamar M., Alvarez-Manilla G., Venot A., Glushka J., Pierce J.M., and Prestegard J.H. NMR structural characterization of substrates bound to N-acetylglucosaminyltransferase. J Mol Biol 366 (2007) 1266-1281. In this study, the authors make use of a novel PRE experiment arising from a spin-labeled analogue of one of the two ligands of the 95 kDa enzyme N-acetylglucosaminyltransferase V to elucidate the orientation of the bound donor and acceptor ligands.
28. Ramos A., and Varani G. A new method to detect long-range protein-RNA contacts; NMR detection of electron-proton relaxation induced by nitroxide spin-labeled RNA. J Am Chem Soc 120 (1998) 10992-10993
29. Varani L., Gundersdon I.W., Mattaj I.W., Kay L.E., Neuhaus D., and Varani G. The NMR structure of the 38 kDa U1A protein-PIE RNA complex reveals the basis of cooperativity in regulation of polyadenylation by human U1A protein. Nat Struct Biol 7 (2000) 329-335
30. Iwahara J., Anderson D.E., Murphy E.C., and Clore G.M. EDTA-derivatized deoxythymidine as a tool for rapid determination of protein binding polarity to DNA by intermolecular paramagnetic relaxation enhancement. J Am Chem Soc 125 (2003) 6634-6635
31. 1H paramagnetic relaxation enhancement data arising from flexible paramagnetic group attached to a macromolecule. J Am Chem Soc 126 (2004) 5879-5896
32. Ueda T., Kato A., Ogawa T., Torizawa T., Kuramitsu S., Iwai S., Terasawa H., and Shimada I. NMR study of repair mechanism of DNA photolyase by FAD-induced paramagnetic relaxation enhancement. J Biol Chem 279 (2004) 52574-52579
33. Roosild T.P., Greenwald J., Vega S., Castronovo S., Riek R., and Choe S. NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307 (2005) 1317-1321. In this study an example of the use of the PRE as an aid in structure determination of membrane bound proteins.
34. Liang B., Bushweller J.H., and Tamm L.K. Site-directed parallel spin-labeling and paramagnetic relaxation enhancement in structure determination of membrane proteins by solution NMR spectroscopy. J Am Chem Soc 128 (2006) 4389-4397. In this study a demonstration of the utility of the PRE arising from multiple spin-labeled sites to facilitate the structure determination of a membrane-bound protein for which traditional NOE data are sparse and difficult to obtain.
35. Iwahara J., and Clore G.M. Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature 440 (2006) 1227-1230. PRE data collected on the HoxD9 homeodomain/DNA specific complex at moderate salt concentrations provides the first direct demonstration for the existence of transient intermediates formed in a stochastic manner at noncognate sites involving both intramolecular sliding of HoxD9 along the DNA and intermolecular hopping of HoxD9 from one DNA molecule to another.
36. Hansen D.F., Hass M.A.S., Christensen H.M., Ulstrup J., and Led J.J. Detection of short-lived transient protein-protein interactions by intermolecular nuclear paramagnetic relaxation: plastocyanin from Anabaena variabilis. J Am Chem Soc 125 (2003) 6858-6859
37. Tang C., Iwahara J., and Clore G.M. Visualization of transient encounter complexes in protein-protein association. Nature 444 (2006) 383-386. This paper illustrates the first quantitative demonstration of the use of the PRE to demonstrate the existence and visualize the distribution of an ensemble of transient nonspecific encounter complexes under equilibrium conditions in protein-protein association. The existence of such encounter complexes is demonstrated for three different protein-protein associations involving complexes from the bacterial phosphotransferase system.
38. Volkov A.N., Worall J.A.R., Holtzmann H., and Ubbink M. Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proc Natl Acad Sci USA 103 (2006) 18945-18950. In this study, the conformational space sampled by two electron transfer proteins before the formation of a stereospecific electron transfer complex is investigated using the PRE.
39. 1H paramagnetic relaxation enhancement. J Am Chem Soc 126 (2004) 12800-12808
40. Iwahara J., Zweckstetter M., and Clore G.M. NMR structural and kinetic characterization of a homeodomain diffusing and hopping on non-specific DNA. Proc Nat Acad Sci USA 103 (2006) 15062-15067. This paper makes use of multiple NMR spectroscopic techniques to characterize the structural and kinetic features of a nonspecific protein-DNA complex in which the protein can both hop and slide on the DNA. The data demonstrate unambiguously that HoxD9 binds to nonspecific DNA with the same binding mode and orientation as that observed for the specific complex.
41. + channel is in close proximity to the tetramerization domain, providing direct evidence for large-scale interdomain motions.
42. 1H transverse paramagnetic relaxation enhancement measurements on macromolecules. J Magn Reson 184 (2007) 185-195. In this study, a detailed analysis of the practical aspects of PRE measurements is presented.
43. Kuszewski J., Schwieters C.D., Garrett D.S., Byrd R.A., Tjandra N., and Clore G.M. Completely automated, highly error tolerant macromolecular structure determination from multidimensional nuclear Overhauser enhancement spectra and chemical shift assignments. J Am Chem Soc 126 (2004) 6258-6273
44. Berg O.G., and von Hippel P.H. Diffusion-controlled macromolecular interactions. Ann Rev Biophys Biophys Chem 14 (1985) 131-160
45. von Hippel P.H., and Berg O.G. Facilitated target location in biological systems. J Biol Chem 264 (1989) 675-678
46. Halford S.E., and Marko J.F. How do site-specific DNA-binding proteins find their targets?. Nucl Acids Res 32 (2004) 3040-3052
47. Zhou H.X., and Szabo A. Enhancement of association rates by non-specific binding to DNA and cell membranes. Phys Rev Lett 204 93 (2004) 101-178
48. Iwahara J., and Clore G.M. Direct observation of enhanced translocation of a homeodomain between DNA cognates sites by NMR exchange spectroscopy. J Am Chem Soc 128 (2006) 404-405. In this study, a novel approach is described to analyze the kinetics of specific protein-DNA interactions using z-exchange spectroscopy on a system in which the DNA-binding protein is mixed with equimolar amounts of two DNA duplexes differing by a single base pair mutation at the edge of the DNA recognition site thereby producing slightly different chemical shifts for the two complexes without perturbing the equilibrium dissociation constant. Rapid direct hopping of HoxD9 from one DNA molecule to another without going through the intermediary of free protein is demonstrated with translocation rates that are over three orders of magnitude faster than the dissociation rate constant determined from gel shift assays at very low concentrations of free DNA.
49. Schreiber G., and Fersht A.R. Rapid electrostatically assisted association of proteins. Nat Struct Biol 3 (1996) 427-431
50. Selzer T., Albeck S., and Schreiber G. Rational design of faster associating and tighter binding complexes. Nat Struct Biol 7 (2000) 537-541
51. Northrup S.H., Boles J.O., and Reynolds J.C.L. Brownian dynamics of cytochrome c and cytochrome c peroxidase association. Science 241 (1988) 67-70
52. Spaar A., Dammer C., Gabdoulline R.R., Wade R.C., and Helms V. Diffusional encounter of barnase and barstar. Biophys J 90 (2006) 1913-1924
53. Adams G., and Delbruck M. Reduction of dimensionality in biological diffusion processes. In: Rich A., and Davdison N. (Eds). Structural Chemistry and Molecular Biology (1968), Freeman & Co., San Francisco 198-215
54. r phosphoryl transfer complex between the N-terminal domain of enzyme I and HPr. Nat Struct Biol 6 (1999) 166-173
55. Schwieters C.D., Kuszewski J., and Clore G.M. Using Xplor-NIH for NMR molecular structure determination. Progr Nucl Magn Reson Spectrosc 38 (2006) 47-62
56. Sugase K., Dyson J.H., and Wright P.E. Mechanism of coupled folding and binding of an intrinsically disordered peptide. Nature (2007) Advance online publication doi:10.1038/nature05860. In this study, using chemical shift mapping and NMR relaxation dispersion analysis the authors show that nonspecific encounter complexes are formed during the course of coupled folding and binding of an intrinsically disordered peptide to its target protein.
57. Hillisch A., Lorenz M., and Diekman S. Recent advances in FRET: distance determination in protein-DNA complexes. Curr Opin Struct Biol 11 (2001) 201-207
58. Murphy E.C., Zhurkin V.B., Louis J.M., Cornilescu G., and Clore G.M. Structural basis for SRY-dependent 46-X,Y sex reversal: modulation of DNA bending by a naturally occuring point mutation. J Mol Biol 312 (2001) 481-499