15NH/D-SOLEXSY experiment for accurate measurement of amide solvent exchange rates: Application to denatured drkN SH3

Journal of Biomolecular NMR

Volumn 46, Issue 3, 2010, Pages 227-244

  Chevelkov, Veniamin ^a,d   Xue, Yi ^a   Krishna Rao, D ^a,e   Forman Kay, Julie D ^b,c   Skrynnikov, Nikolai R ^a  

^a PURDUE UNIVERSITY   (United States)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^e University of Texas Medical Branch School of Medicine   (United States)

Author keywords

(HACACO)NH experiment; Amide solvent exchange; CLEANEX experiment; Drosophila drk N terminal SH3 domain; Exchange spectroscopy; Hydrophobic cluster; Isotopic shift; Protection factors; Residual structure

Indexed keywords

DEUTERIUM OXIDE; DROSOPHILA PROTEIN; N TERMINAL SH3 DOMAIN PROTEIN DRK; NITROGEN 15; UNCLASSIFIED DRUG; WATER; PROTEIN; PROTON; SOLVENT;

ACCURACY; ANALYTIC METHOD; ARTICLE; CONTROLLED STUDY; HYDROGEN BOND; HYDROPHOBICITY; INSTRUMENT VALIDATION; NITROGEN NUCLEAR MAGNETIC RESONANCE; PHASE MODULATED CLEAN CHEMICAL EXCHANGE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN INTERACTION; RESIDUE ANALYSIS; SOLVENT EFFECT; SOLVENT EXCHANGE SPECTROSCOPY; SPECTROSCOPY; SRC HOMOLOGY DOMAIN; CHEMISTRY; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE; PROTEIN FOLDING;

NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; PROTEINS; PROTONS; SOLVENTS;

EID: 77951667170     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-010-9398-8     Document Type: Article

References (101)

1. YW Bai JS Milne L Mayne SW Englander 1993 Primary structure effects on peptide group hydrogen exchange Proteins Struct Funct Genet 17 75 86 (Pubitemid 23261059)
2. 1H chemical shifts in proteins J Biomol NMR 9 359 369 (Pubitemid 127505398)
3. RB Best M Vendruscolo 2006 Structural interpretation of hydrogen exchange protection factors in proteins: characterization of the native state fluctuations of CI2 Structure 14 97 106 (Pubitemid 43350077)
4. I Bezsonova A Singer WY Choy M Tollinger JD Forman-Kay 2005 Structural comparison of the unstable drkN SH3 domain and a stable mutant Biochemistry 44 15550 15560 (Pubitemid 41706139)
5. JM Böhlen M Rey G Bodenhausen 1989 Refocusing with chirped pulses for broadband excitation without phase dispersion J Magn Reson 84 191 197
6. B Brutscher JP Simorre MS Caffrey D Marion 1994 Design of a complete set of two-dimensional triple-resonance experiments for assigning labeled proteins J Magn Reson Ser B 105 77 82
7. M Buck SE Radford CM Dobson 1994 Amide hydrogen exchange in a highly denatured state. Hen egg-white lysozyme in urea J Mol Biol 237 247 254 (Pubitemid 124002098)
8. J Cavanagh M Rance 1992 Suppression of cross-relaxation effects in TOCSY spectra via a modified DIPSI-2 mixing sequence J Magn Reson 96 670 678
9. V Chevelkov K Faelber A Diehl U Heinemann H Oschkinat B Reif 2005 Detection of dynamic water molecules in a microcrystalline sample of the SH3 domain of α-spectrin by MAS solid-state NMR J Biomol NMR 31 295 310 (Pubitemid 41348906)
10. 15N relaxation data from solid- and solution-state NMR spectroscopy J Am Chem Soc 129 12594 12595 (Pubitemid 350004432)
11. WY Choy JD Forman-Kay 2001 Calculation of ensembles of structures representing the unfolded state of an SH3 domain J Mol Biol 308 1011 1032
12. WY Choy FAA Mulder KA Crowhurst DR Muhandiram IS Millett S Doniach JD Forman-Kay LE Kay 2002 Distribution of molecular size within an unfolded state ensemble using small-angle X-ray scattering and pulse field gradient NMR techniques J Mol Biol 316 101 112
13. GP Connelly YW Bai MF Jeng SW Englander 1993 Isotope effects in peptide group hydrogen exchange Proteins Struct Funct Genet 17 87 92
14. AK Covington RA Robinson RG Bates 1966 Ionization constant of deuterium oxide from 5 to 50 degrees J Phys Chem 70 3820 3824
15. d) scale and operational pH in heavy water Anal Chem 40 700 706
16. KA Crowhurst JD Forman-Kay 2003 Aromatic and methyl NOEs highlight hydrophobic clustering in the unfolded state of an SH3 domain Biochemistry 42 8687 8695
17. KA Crowhurst M Tollinger JD Forman-Kay 2002 Cooperative interactions and a non-native buried Trp in the unfolded state of an SH3 domain J Mol Biol 322 163 178
18. C Dalvit 1996 Homonuclear 1D and 2D NMR experiments for the observation of solvent-solute interactions J Magn Reson B 112 282 288
19. C Dalvit U Hommel 1995 Sensitivity-improved detection of protein hydration and its extension to the assignment of fast-exchanging resonances J Magn Reson B 109 334 338
20. F Delaglio S Grzesiek GW Vuister G Zhu J Pfeifer A Bax 1995 NMRPipe: a multidimensional spectral processing system based on unix pipes J Biomol NMR 6 277 293
21. M Delepierre CM Dobson M Karplus FM Poulsen DJ States RE Wedin 1987 Electrostatic effects and hydrogen exchange behavior in proteins. The pH dependence of exchange rates in lysozyme J Mol Biol 197 111 122
22. H Desvaux N Birlirakis C Wary P Berthault 1995 Study of slow molecular motions in solution using off-resonance irradiation in homonuclear NMR. 2. Fast chemical exchange processes Mol Phys 86 1059 1073 1995MolPh..86.1059D
23. CM Dobson L-Y Lian C Redfield KD Topping 1986 Measurement of hydrogen exchange rates using 2D NMR spectroscopy J Magn Reson 69 201 209
24. V Dötsch G Wider G Siegal K Wüthrich 1995 Interaction of urea with an unfolded protein-the DNA-binding domain of the 434-repressor FEBS Lett 366 6 10
25. 1ρ experiment permits accurate characterization of microsecond time-scale conformational exchange J Biomol NMR 32 281 293
26. L Emsley G Bodenhausen 1990 Gaussian pulse cascades-new analytical functions for rectangular selective inversion and in-phase excitation in NMR Chem Phys Lett 165 469 476 1990CPL...165..469E
27. L Emsley G Bodenhausen 1992 Optimization of shaped selective pulses for NMR using a quaternion description of their overall propagators J Magn Reson 97 135 148
28. SW Englander A Poulsen 1969 Hydrogen-tritium exchange of random chain polypeptide Biopolymers 7 379 393
29. Ernst RR, Bodenhausen G, Wokaun A (1987) Principles of nuclear magnetic resonance in one and two dimensions. Oxford University Press, Oxford
30. 1H NMR Biochemistry 45 14120 14128
31. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium J Biomol NMR 4 727 734
32. NA Farrow OW Zhang JD Forman-Kay LE Kay 1995 Comparison of the backbone dynamics of a folded and an unfolded SH3 domain existing in equilibrium in aqueous buffer Biochemistry 34 868 878
33. NA Farrow OW Zhang JD Forman-Kay LE Kay 1997 Characterization of the backbone dynamics of folded and denatured states of an SH3 domain Biochemistry 36 2390 2402
34. V Forge RT Wijesinha J Balbach K Brew CV Robinson C Redfield CM Dobson 1999 Rapid collapse and slow structural reorganisation during the refolding of bovine α-lactalbumin J Mol Biol 288 673 688
35. M Gal P Schanda B Brutscher L Frydman 2007 UltraSOFAST HMQC NMR and the repetitive acquisition of 2D protein spectra at Hz rates J Am Chem Soc 129 1372 1377 (Pubitemid 46208609)
36. G Gemmecker W Jahnke H Kessler 1993 Measurement of fast proton exchange rates in isotopically labeled compounds J Am Chem Soc 115 11620 11621
37. 2O mixtures J Chem Soc A 936 943
38. C Griesinger RR Ernst 1987 Frequency offset effects and their elimination in NMR rotating-frame cross-relaxation spectroscopy J Magn Reson 75 261 271
39. S Grzesiek A Bax 1992 An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins J Magn Reson 99 201 207
40. 15N-enriched proteins J Biomol NMR 3 185 204
41. 2O in protein NMR: application to sensitivity enhancement and NOE measurements J Am Chem Soc 115 12593 12594 (Pubitemid 2010638)
42. PE Hansen 2000 Isotope effects on chemical shifts of proteins and peptides Magn Reson Chem 38 1 10
43. GS Harbison JE Roberts J Herzfeld RG Griffin 1988 Solid-state NMR detection of proton exchange between the bacteriorhodopsin Schiff-base and bulk water J Am Chem Soc 110 7221 7223
44. 15N nuclear magnetic resonance spectra of viomycin in aqueous solution Biochemistry 17 3986 3992
45. 15N INEPT spectra in water. Application to the measurement of hydrogen exchange rates in amides and proteins J Magn Reson B 102 193 200
46. 13C NMR hydrogen-deuterium isotope shifts Biochemistry 26 3626 3634
47. 13C-labeled proteins J Magn Reson 140 281 284 1999JMagR.140..281H
48. A Hvidt SO Nielsen 1966 Hydrogen exchange in proteins Adv Protein Chem 21 287 386
49. TL Hwang S Mori AJ Shaka PCM van Zijl 1997 Application of phase-modulated CLEAN chemical EXchange spectroscopy (CLEANEX-PM) to detect water-protein proton exchange and intermolecular NOEs J Am Chem Soc 119 6203 6204 (Pubitemid 27314859)
50. TL Hwang PCM van Zijl S Mori 1998 Accurate quantitation of water-amide proton exchange rates using the Phase-Modulated CLEAN chemical EXchange (CLEANEX-PM) approach with a Fast-HSQC (FHSQC) detection scheme J Biomol NMR 11 221 226 (Pubitemid 128511271)
51. J Jeener BH Meier P Bachmann RR Ernst 1979 Investigation of exchange processes by 2-dimensional NMR spectroscopy J Chem Phys 71 4546 4553 1979JChPh..71.4546J
52. MR Jensen SM Kristensen JJ Led 2007 Elimination of spin diffusion effects in saturation transfer experiments: application to hydrogen exchange in proteins Magn Reson Chem 45 257 261
53. V Kanelis L Donaldson DR Muhandiram D Rotin JD Forman-Kay LE Kay 2000 Sequential assignment of proline-rich regions in proteins: application to modular binding domain complexes J Biomol NMR 16 253 259 (Pubitemid 30217114)
54. F Kateb P Pelupessy G Bodenhausen 2007 Measuring fast hydrogen exchange rates by NMR spectroscopy J Magn Reson 184 108 113 2007JMagR.184..108K (Pubitemid 46049050)
55. JE Kohn IS Millett J Jacob B Zagrovic TM Dillon N Cingel RS Dothager S Seifert P Thiyagarajan TR Sosnick MZ Hasan VS Pande I Ruczinski S Doniach KW Plaxco 2004 Random-coil behavior and the dimensions of chemically unfolded proteins Proc Natl Acad Sci USA 101 12491 12496 2004PNAS..10112491K
56. 15N-labeled peptide J Biomol NMR 6 306 312
57. RW Kriwacki RB Hill JM Flanagan JP Caradonna JH Prestegard 1993 New NMR methods for the characterization of bound waters in macromolecules J Am Chem Soc 115 8907 8911
58. 13C solid-state NMR spectroscopy J Am Chem Soc 125 13336 13337
59. A Lesage C Gardiennet A Loquet R Verel G Pintacuda L Emsley BH Meier A Böckmann 2008 Polarization transfer over the water-protein interface in solids Angew Chem Int Ed 47 5851 5854
60. K Linderstrøm-Lang 1955 Deuterium exchange between peptides and water Chem Soc (London) Spec Publ 2 1 20
61. 15N labeled human ubiquitin by triple resonance NMR J Am Chem Soc 118 12864 12865
62. D Loftus GO Gbenle PS Kim RL Baldwin 1986 Effects of denaturants on amide proton exchange rates: a test for structure in protein fragments and folding intermediates Biochemistry 25 1428 1436
63. 1H spin-spin coupling constants in proteins Biochem Biophys Res Commun 113 967 974
64. JA Marsh JD Forman-Kay 2009 Structure and disorder in an unfolded state under nondenaturing conditions from ensemble models consistent with a large number of experimental restraints J Mol Biol 391 359 374
65. HM McConnell 1958 Reaction rates by nuclear magnetic resonance J Chem Phys 28 430 431 1958JChPh..28..430M
66. G Melacini R Kaptein R Boelens 1999 Editing of chemical exchange-relayed NOEs in NMR experiments for the observation of protein-water interactions J Magn Reson 136 214 218 1999JMagR.136..214M
67. K Modig E Liepinsh G Otting B Halle 2004 Dynamics of protein and peptide hydration J Am Chem Soc 126 102 114
68. YK Mok EL Elisseeva AR Davidson JD Forman-Kay 2001 Dramatic stabilization of an SH3 domain by a single substitution: roles of the folded and unfolded states J Mol Biol 307 913 928
69. S Mori C Abeygunawardana PCM van Zijl JM Berg 1996 Water exchange filter with improved sensitivity (WEX II) to study solvent-exchangeable protons. Application to the consensus zinc finger peptide CP-1 J Magn Reson B 110 96 101
70. S Mori PCM van Zijl D Shortle 1997 Measurement of water-amide proton exchange rates in the denatured state of staphylococcal nuclease by a magnetization transfer technique Proteins Struct Funct Genet 28 325 332
71. C Nishimura HJ Dyson PE Wright 2008 The kinetic and equilibrium molten globule intermediates of apoleghemoglobin differ in structure J Mol Biol 378 715 725
72. G Otting E Liepinsh 1995 Protein hydration viewed by high-resolution NMR spectroscopy: implications for magnetic resonance image contrast Accounts Chem Res 28 171 177
73. G Otting E Liepinsh K Wüthrich 1991 Protein hydration in aqueous solution Science 254 974 980 1991Sci...254..974O
74. U Reimer G Scherer M Drewello S Kruber M Schutkowski G Fischer 1998 Side-chain effects on peptidyl-prolyl cis/trans isomerisation J Mol Biol 279 449 460
75. H Roder GA Elöve SW Englander 1988 Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR Nature 335 700 704 1988Natur.335..700R
76. J Schleucher SS Wijmenga 2002 How to detect internal motion by homonuclear NMR J Am Chem Soc 124 5881 5889
77. BA Schulman C Redfield ZY Peng CM Dobson PS Kim 1995 Different subdomains are most protected from hydrogen exchange in the molten globule and native states of human α-lactalbumin J Mol Biol 253 651 657
78. AJ Shaka J Keeler T Frenkiel R Freeman 1983 An improved sequence for broad-band decoupling: WALTZ-16 J Magn Reson 52 335 338
79. AJ Shaka PB Barker R Freeman 1985 Computer-optimized decoupling scheme for wideband applications and low-level operation J Magn Reson 64 547 552
80. AJ Shaka CJ Lee A Pines 1988 Iterative schemes for bilinear operators-application to spin decoupling J Magn Reson 77 274 293
81. 13C constant-time evolution period J Am Chem Soc 119 9274 9278
82. V Sklenár M Piotto R Leppik V Saudek 1993 Gradient-tailored water suppression for 1H-15 N HSQC experiments optimized to retain full sensitivity J Magn Reson A 102 241 245
83. NR Skrynnikov RR Ernst 1999 Detection of intermolecular chemical exchange through decorrelation of two-spin order J Magn Reson 137 276 280 1999JMagR.137..276S
84. S Spera M Ikura A Bax 1991 Measurement of the exchange rates of rapidly exchanging amide protons. Application to the study of calmodulin and its complex with a myosin light chain kinase fragment J Biomol NMR 1 155 166
85. M Tollinger NR Skrynnikov FAA Mulder JD Forman-Kay LE Kay 2001 Slow dynamics in folded and unfolded states of an SH3 domain J Am Chem Soc 123 11341 11352
86. 15N relaxation measurements J Biomol NMR 30 347 352
87. FJM van de Ven HGJM Janssen A Graslund CW Hilbers 1988 Chemically relayed nuclear Overhauser effects: connectivities between resonances of nonexchangeable protons and water J Magn Reson 79 221 235
88. M Vendruscolo E Paci CM Dobson M Karplus 2003 Rare fluctuations of native proteins sampled by equilibrium hydrogen exchange J Am Chem Soc 125 15686 15687
89. 13C decoupling J Magn Reson 98 428 435
90. G Wagner K Wüthrich 1982 Amide proton exchange and surface conformation of the basic pancreatic trypsin inhibitor in solution: studies with two-dimensional nuclear magnetic resonance J Mol Biol 160 343 361
91. AC Wang A Bax 1993 Minimizing the effects of radiofrequency heating in multidimensional NMR experiments J Biomol NMR 3 715 720
92. 2O by deuterium-decoupled HA(CA)N and HA(CACO)N J Biomol NMR 5 376 382
93. J Wirmer W Peti H Schwalbe 2006 Motional properties of unfolded ubiquitin: a model for a random coil protein J Biomol NMR 35 175 186
94. 2H amide groups J Am Chem Soc 127 3220 3229
95. Y Xue IS Podkorytov DK Rao N Benjamin HL Sun NR Skrynnikov 2009 Paramagnetic relaxation enhancements in unfolded proteins: theory and application to drkN SH3 domain Protein Sci 18 1401 1424
96. J Yao J Chung D Eliezer PE Wright HJ Dyson 2001 NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding Biochemistry 40 3561 3571
97. K Zangger IM Armitage 1998 Sensitivity-enhanced detection of fast exchanging protons by an exchange-edited gradient HEHAHA-HSQC experiment J Magn Reson 135 70 75 1998JMagR.135...70Z
98. OW Zhang JD Forman-Kay 1997 NMR studies of unfolded states of an SH3 domain in aqueous solution and denaturing conditions Biochemistry 36 3959 3970
99. 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed-field gradient NMR techniques J Biomol NMR 4 845 858
100. 1H longitudinal spin relaxation J Magn Reson B 108 220 234
101. JY Zhou PCM van Zijl 2006 Chemical exchange saturation transfer imaging and spectroscopy Prog NMR Spectrosc 48 109 136