Very large residual dipolar couplings from deuterated ubiquitin

Journal of Biomolecular NMR

Volumn 54, Issue 1, 2012, Pages 53-67

  Ward, Joshua M ^a,b   Skrynnikov, Nikolai R ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF OULU   (Finland)

Author keywords

Alignment media; Deuteration; Differential line broadening; HSQC; J resolved and J modulated spectroscopy; Pf1 phage; Residual dipolar couplings; TROSY; Ubiquitin

Indexed keywords

DEUTERIUM; NITROGEN 15; UBIQUITIN;

ARTICLE; CHEMICAL REACTION; CRYSTAL STRUCTURE; DIPOLE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HYDROGEN BOND; LIQUID CRYSTAL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTON TRANSPORT;

BACTERIOPHAGE PF1; CARBON ISOTOPES; DEUTERIUM; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; UBIQUITIN;

EID: 84865618816     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-012-9651-4     Document Type: Article

References (93)

1. Abragam A (1961) The principles of nuclear magnetism. Clarendon Press, Oxford
2. V Agarwal B Reif 2008 Residual methyl protonation in perdeuterated proteins for multi-dimensional correlation experiments in MAS solid-state NMR spectroscopy J Magn Reson 194 16 24 2008JMagR.194...16A 10.1016/j.jmr.2008.05. 021
3. U Akbey S Lange WT Franks R Linser K Rehbein A Diehl BJ van Rossum B Reif H Oschkinat 2010 Optimum levels of exchangeable protons in perdeuterated proteins for proton detection in MAS solid-state NMR spectroscopy J Biomol NMR 46 67 73 10.1007/s10858-009-9369-0
4. A Bax 2003 Weak alignment offers new NMR opportunities to study protein structure and dynamics Protein Sci 12 1 16 10.1110/ps.0233303 (Pubitemid 36020129)
5. KB Briggman JR Tolman 2003 De Novo determination of bond orientations and order parameters from residual dipolar couplings with high accuracy J Am Chem Soc 125 10164 10165 10.1021/ja035904+ (Pubitemid 37022214)
6. BR Brooks CL Brooks AD Mackerell L Nilsson RJ Petrella B Roux Y Won G Archontis C Bartels S Boresch A Caflisch L Caves Q Cui AR Dinner M Feig S Fischer J Gao M Hodoscek W Im K Kuczera T Lazaridis J Ma V Ovchinnikov E Paci RW Pastor CB Post JZ Pu M Schaefer B Tidor RM Venable HL Woodcock X Wu W Yang DM York M Karplus 2009 CHARMM: the biomolecular simulation program J Comput Chem 30 1545 1614 10.1002/jcc.21287
7. Brunger AT (1992) X-PLOR, version 3.1. A system for X-ray crystallography and NMR. Yale University Press, New Haven
8. S Cai C Seu Z Kovacs AD Sherry Y Chen 2006 Sensitivity enhancement of multidimensional NMR experiments by paramagnetic relaxation effects J Am Chem Soc 128 13474 13478 10.1021/ja0634526 (Pubitemid 44583032)
9. Cavanagh J, Fairbrother WJ, Palmer AG, Skelton NJ, Rance M (2007) Protein NMR spectroscopy. Principles and practice, 2nd edn. Academic Press Inc., San Diego
10. ZJ Chen G Krause B Reif 2005 Structure and orientation of peptide inhibitors bound to beta-amyloid fibrils J Mol Biol 354 760 776 10.1016/j.jmb.2005.09.055 (Pubitemid 41742051)
11. GG Chernik 1999 Phase studies of surfactant-water systems Curr Opin Colloid Interface Sci 4 381 390 10.1016/S1359-0294(00)00023-6 (Pubitemid 30449765)
12. V Chevelkov K Rehbein A Diehl B Reif 2006 Ultra-high resolution in proton solid-state NMR spectroscopy at high levels of deuteration Angew Chem Int Ed 45 3878 3881 10.1002/anie.200600328 (Pubitemid 44098947)
13. 15N dipolar couplings in MAS solid-state NMR experiments J Am Chem Soc 131 14018 14022 10.1021/ja902649u
14. G Cornilescu JL Marquardt M Ottiger A Bax 1998 Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase J Am Chem Soc 120 6836 6837 10.1021/ja9812610 (Pubitemid 28347351)
15. 1H couplings in proteins: effects of cross-correlated relaxation, selective pulses and dynamic frequency shifts J Magn Reson 183 160 165 2006JMagR.183..160A 10.1016/j.jmr.2006.08.003 (Pubitemid 44692528)
16. 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 10.1007/BF00197809
17. 13C spectroscopy J Biomol NMR 26 167 179 10.1023/A: 1023572320699 (Pubitemid 36609049)
18. Emsley JW, Lindon JC (1975) NMR spectroscopy using liquid crystal solvents. Pergamon Press, Oxford
19. K Furihata H Seto 1999 J-resolved HMBC, a new NMR technique for measuring heteronuclear long-range coupling constants Tetrahedron Lett 40 6271 6275 10.1016/S0040-4039(99)01233-2 (Pubitemid 29378428)
20. J Furrer M John H Kessler B Luy 2007 J-Spectroscopy in the presence of residual dipolar couplings: determination of one-bond coupling constants and scalable resolution J Biomol NMR 37 231 243 10.1007/s10858-006-9130-x (Pubitemid 46477000)
21. 15N multidimensional NMR to study the structure and dynamics of proteins Annu Rev Biophys Biomol Struct 27 357 406 10.1146/annurev.biophys.27.1. 357 (Pubitemid 28286019)
22. 2H-labeled proteins J Biomol NMR 13 369 374 10.1023/A:1008393201236 (Pubitemid 29210329)
23. MR Hansen L Mueller A Pardi 1998 Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions Nat Struct Biol 5 1065 1074 10.1038/4176 (Pubitemid 28546270)
24. TA Harroun M Koslowsky MP Nieh CF de Lannoy VA Raghunathan J Katsaras 2005 Comprehensive examination of mesophases formed by DMPC and DHPC mixtures Langmuir 21 5356 5361 10.1021/la050018t (Pubitemid 40850619)
25. RC Hewitt S Meiboom LC Snyder 1973 Proton NMR in nematic liquid crystalline solvents: use of deuterium decoupling J Chem Phys 58 5089 5095 1973JChPh..58.5089H 10.1063/1.1679098
26. M Hohwy CP Jaroniec B Reif CM Rienstra RG Griffin 2000 Local structure and relaxation in solid-state NMR: accurate measurement of amide N-H bond lengths and H-N-H bond angles J Am Chem Soc 122 3218 3219 10.1021/ja9913737 (Pubitemid 30207854)
27. JC Hus JJ Prompers R Bruschweiler 2002 Assignment strategy for proteins with known structure J Magn Reson 157 119 123 2002JMagR.157..119H 10.1006/jmre.2002.2569
28. P Jensen HJ Sass S Grzesiek 2004 Improved detection of long-range residual dipolar couplings in weakly aligned samples by Lee-Goldburg decoupling of homonuclear dipolar truncation J Biomol NMR 30 443 450 10.1007/s10858-004- 5318-0 (Pubitemid 40069208)
29. M Jonstromer R Strey 1992 Nonionic bilayers in dilute solutions: effect of additives J Phys Chem 96 5993 6000 10.1021/j100193a064
30. LE Kay P Keifer T Saarinen 1992 Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J Am Chem Soc 114 10663 10665 10.1021/ja00052a088
31. HNα. Application to paramagnetic proteins J Magn Reson Ser B 113 88 90 10.1006/jmrb.1996.0160 (Pubitemid 126758752)
32. AI Kishore JH Prestegard 2003 Molecular orientation and conformation of phosphatidylinositides in membrane mimetics using variable angle sample spinning (VASS) NMR Biophys J 85 3848 3857 10.1016/S0006-3495(03)74799-7 (Pubitemid 37490294)
33. BW Koenig G Kontaxis DC Mitchell JM Louis BJ Litman A Bax 2002 Structure and orientation of a G protein fragment in the receptor bound state from residual dipolar couplings J Mol Biol 322 441 461 10.1016/S0022-2836(02)00745-3
34. G Kontaxis GM Clore A Bax 2000 Evaluation of cross-correlation effects and measurement of one-bond couplings in proteins with short transverse relaxation times J Magn Reson 143 184 196 2000JMagR.143..184K 10.1006/jmre.1999.1979
35. R Koradi M Billeter K Wüthrich 1996 MOLMOL: a program for display and analysis of macromolecular structures J Mol Graph 14 51 55 10.1016/0263-7855(96)00009-4 (Pubitemid 26152976)
36. NA Lakomek T Carlomagno S Becker C Griesinger J Meiler 2006 A thorough dynamic interpretation of residual dipolar couplings in ubiquitin J Biomol NMR 34 101 115 10.1007/s10858-005-5686-0
37. 15N CSA in soluble proteins J Biomol NMR 33 153 161 10.1007/s10858-005-3210-1 (Pubitemid 43149365)
38. GA Lazar JR Desjarlais TM Handel 1997 De novo design of the hydrophobic core of ubiquitin Protein Sci 6 1167 1178 10.1002/pro.5560060605 (Pubitemid 27260151)
39. TO Levante T Bremi RR Ernst 1996 Pulse-sequence optimization with analytical derivatives. Application to deuterium decoupling in oriented phases J Magn Reson Ser A 121 167 177 10.1006/jmra.1996.0157 (Pubitemid 126751790)
40. MH Levitt 1997 The signs of frequencies and phases in NMR J Magn Reson 126 164 182 1997JMagR.126..164L 10.1006/jmre.1997.1161 (Pubitemid 127451905)
41. Li MX, Corson DC, Sykes BD (2002) In: Vogel HJ (eds) Methods in molecular biology, vol 173, pp 255-265
42. R Lichtenecker ML Ludwiczek W Schmid R Konrat 2004 Simplification of protein NOESY spectra using bioorganic precursor synthesis and NMR spectral editing J Am Chem Soc 126 5348 5349 10.1021/ja049679n (Pubitemid 38596333)
43. 15N labeled human ubiquitin by triple resonance NMR J Am Chem Soc 118 12864 12865 10.1021/ja9630553 (Pubitemid 27042028)
44. JA Losonczi JH Prestegard 1998 Improved dilute bicelle solutions for high-resolution NMR of biological macromolecules J Biomol NMR 12 447 451 10.1023/A:1008302110884 (Pubitemid 128511311)
45. B Luy JP Marino 2003 JE-TROSY: combined J- and TROSY-spectroscopy for the measurement of one-bond couplings in macromolecules J Magn Reson 163 92 98 2003JMagR.163...92L 10.1016/S1090-7807(03)00105-8
46. B Luy K Kobzar H Kessler 2004 An easy and scalable method for the partial alignment of organic molecules for measuring residual dipolar couplings Angew Chem Int Ed 43 1092 1094 10.1002/anie.200352860 (Pubitemid 39257965)
47. N dipolar couplings in perdeuterated proteins J Am Chem Soc 125 44 45 10.1021/ja028740q (Pubitemid 36068640)
48. S Meier M Strohmeier M Blackledge S Grzesiek 2007 Direct observation of dipolar couplings and hydrogen bonds across a β-hairpin in 8 M urea J Am Chem Soc 129 754 755 10.1021/ja067522k (Pubitemid 46183913)
49. NC Nielsen H Bildsoe HJ Jakobsen OW Sorensen 1989 Composite refocusing sequences and their application for sensitivity enhancement and multiplicity filtration in INEPT and 2D correlation spectroscopy J Magn Reson 85 359 380
50. D Nietlispach 2005 Suppression of anti-TROSY lines in a sensitivity enhanced gradient selection TROSY scheme J Biomol NMR 31 161 166 10.1007/s10858-004-8195-7 (Pubitemid 40425224)
51. D Nietlispach RT Clowes RW Broadhurst Y Ito J Keeler M Kelly J Ashurst H Oschkinat PJ Domaille ED Laue 1996 An approach to the structure determination of larger proteins using triple resonance NMR experiments in conjunction with random fractional deuteration J Am Chem Soc 118 407 415 10.1021/ja952207b (Pubitemid 26050290)
52. DD Ojennus RM Mitton-Fry DS Wuttke 1999 Induced alignment and measurement of dipolar couplings of an SH2 domain through direct binding with filamentous phage J Biomol NMR 14 175 179 10.1023/A:1008304332574 (Pubitemid 29322972)
53. M Ottiger A Bax 1998 Characterization of magnetically oriented phospholipid micelles for measurement of dipolar couplings in macromolecules J Biomol NMR 12 361 372 10.1023/A:1008366116644 (Pubitemid 128511302)
54. M Ottiger F Delaglio A Bax 1998 Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra J Magn Reson 131 373 378 1998JMagR.131..373O 10.1006/jmre.1998.1361 (Pubitemid 128450579)
55. A Pines DJ Ruben S Vega M Mehring 1976 New approach to high-resolution proton NMR in solids: deuterium spin decoupling by multiple-quantum transitions Phys Rev Lett 36 110 113 1976PhRvL..36..110P 10.1103/PhysRevLett.36.110
56. JH Prestegard AI Kishore 2001 Partial alignment of biomolecules: an aid to NMR characterization Curr Opin Chem Biol 5 584 590 10.1016/S1367-5931(00) 00247-7 (Pubitemid 32907612)
57. R Riek G Wider K Pervushin K Wuthrich 1999 Polarization transfer by cross-correlated relaxation in solution NMR with very large molecules Proc Natl Acad Sci USA 96 4918 4923 1999PNAS...96.4918R 10.1073/pnas.96.9.4918 (Pubitemid 29214511)
58. CR Sanders JP Schwonek 1992 Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR Biochemistry 31 8898 8905 10.1021/bi00152a029
59. P Schanda E Lescop M Falge R Sounier J Boisbouvier B Brutscher 2007 Sensitivity-optimized experiment for the measurement of residual dipolar couplings between amide protons J Biomol NMR 38 47 55 10.1007/s10858-006-9138-2 (Pubitemid 46745441)
60. KV Schenker D Suter A Pines 1987 Broadband heteronuclear decoupling in the presence of homonuclear dipolar and quadrupolar interactions J Magn Reson 73 99 113
61. CD Schwieters JJ Kuszewski N Tjandra GM Clore 2003 The Xplor-NIH NMR molecular structure determination package J Magn Reson 160 65 73 2003JMagR.160...65S 10.1016/S1090-7807(02)00014-9
62. AJ Shaka PB Barker R Freeman 1985 Computer-optimized decoupling scheme for wideband applications and low-level operation J Magn Reson 64 547 552
63. A Sidhu A Surolia AD Robertson M Sundd 2011 A hydrogen bond regulates slow motions in ubiquitin by modulating a -turn flip J Mol Biol 411 1037 1048 10.1016/j.jmb.2011.06.044
64. R Sounier L Blanchard ZR Wu J Boisbouvier 2007 High-accuracy distance measurement between remote methyls in specifically protonated proteins J Am Chem Soc 129 472 473 10.1021/ja067260m (Pubitemid 46147731)
65. XC Su G Otting 2010 Paramagnetic labelling of proteins and oligonucleotides for NMR J Biomol NMR 46 101 112 10.1007/s10858-009-9331-1
66. CM Thiele 2005 Scaling the alignment of small organic molecules in substituted polyglutamates by variable-angle sample spinning Angew Chem Int Ed 44 2787 2790 10.1002/anie.200461532 (Pubitemid 40689588)
67. F Tian JA Losonczi MWF Fischer JH Prestegard 1999 Sign determination of dipolar couplings in field-oriented bicelles by variable angle sample spinning (VASS) J Biomol NMR 15 145 150 10.1023/A:1008356210291
68. 1H dipolar couplings in proteins: a complement to traditional NOE measurements J Biomol NMR 18 23 31 10.1023/A:1008384904380
69. N Tjandra A Bax 1997 Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium Science 278 1111 1114 1997Sci...278.1111T 10.1126/science.278.5340.1111 (Pubitemid 27517889)
70. 15N NMR relaxation J Am Chem Soc 117 12562 12566 10.1021/ja00155a020 (Pubitemid 26201339)
71. 15N-enriched human ubiquitin resulting from relaxation interference and residual dipolar coupling J Am Chem Soc 118 6264 6272 10.1021/ja960106n (Pubitemid 26236864)
72. 1H couplings in proteins J Magn Reson Ser B 112 245 252 10.1006/jmrb.1996.0138 (Pubitemid 126758731)
73. JR Tolman K Ruan 2006 NMR residual dipolar couplings as probes of biomolecular dynamics Chem Rev 106 1720 1736 10.1021/cr040429z (Pubitemid 43792777)
74. JR Tolman JM Flanagan MA Kennedy JH Prestegard 1995 Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution Proc Natl Acad Sci USA 92 9279 9283 1995PNAS...92.9279T 10.1073/pnas.92.20.9279
75. JR Tolman HM Al-Hashimi LE Kay JH Prestegard 2001 Structural and dynamic analysis of residual dipolar coupling data for proteins J Am Chem Soc 123 1416 1424 10.1021/ja002500y (Pubitemid 32167334)
76. DA Torchia SW Sparks A Bax 1988 NMR signal assignments of amide protons in the α-helical domains of staphylococcal nuclease Biochemistry 27 5135 5141 10.1021/bi00414a028
77. JF Trempe E Pomerantseva K Gehring 2008 REDOR recoupling in polymer-stabilized liquid crystals undergoing MAS-two-dimensional NMR applications with strongly aligned proteins Can J Chem 86 608 615 10.1139/v08-048
78. TS Ulmer BE Ramirez F Delaglio A Bax 2003 Evaluation of backbone proton positions and dynamics in a small protein by liquid crystal NMR spectroscopy J Am Chem Soc 125 9179 9191 10.1021/ja0350684 (Pubitemid 36903834)
79. 15N residual dipolar coupling measurements J Biomol NMR 15 335 338 10.1023/A:1008387305293 (Pubitemid 30062957)
80. G Veglia T Gopinath 2010 Improved resolution in dipolar NMR spectra using constant time evolution PISEMA experiment Chem Phys Lett 494 104 110 2010CPL...494..104G 10.1016/j.cplett.2010.05.078
81. S Vijay-Kumar CE Bugg WJ Cook 1987 Structure of ubiquitin refined at 1.8 Å resolution J Mol Biol 194 531 544 10.1016/0022-2836(87)90679-6
82. 13C' dipolar couplings in a perdeuterated 30 kDa protein dissolved in a dilute liquid crystailine phase J Am Chem Soc 120 7385 7386 10.1021/ja980862o (Pubitemid 28389380)
83. 1H dipolar couplings in weakly aligned proteins. J Am Chem Soc 124:9672-9673
84. LS Yao B Vögeli JF Ying A Bax 2008 NMR determination of amide N-H equilibrium bond length from concerted dipolar coupling measurements J Am Chem Soc 130 16518 16520 10.1021/ja805654f
85. LS Yao JF Ying A Bax 2009 Improved accuracy of 15N-1H scalar and residual dipolar couplings from gradient-enhanced IPAP-HSQC experiments on protonated proteins J Biomol NMR 43 161 170 10.1007/s10858-009-9299-x
86. 1H Chemical Shift Anisotropy studied by cross-correlated relaxation and liquid crystal NMR spectroscopy J Am Chem Soc 132 10866 10875 10.1021/ja103629e
87. 15N chemical shift anisotropy tensors in a small protein from liquid crystal and cross-correlated relaxation measurements J Am Chem Soc 132 4295 4309 10.1021/ja910186u
88. T Yuwen CB Post NR Skrynnikov 2011 Domain cooperativity in multidomain proteins: what can we learn from molecular alignment in anisotropic media? J Biomol NMR 51 131 150 10.1007/s10858-011-9548-7
89. 15N NMR spectroscopy of peptides weakly associated to phospholipids: determination of large RDC J Biomol NMR 30 303 309 10.1007/s10858-004-3097-2 (Pubitemid 40069144)
90. G Zandomeneghi M Tomaselli PTF Williamson BH Meier 2003 NMR of bicelles: orientation and mosaic spread of the liquid-crystal director under sample rotation J Biomol NMR 25 113 123 10.1023/A:1022236217018 (Pubitemid 36267002)
91. M Zweckstetter 2008 NMR: prediction of molecular alignment from structure using the PALES software Nat Protoc 3 679 690 10.1038/nprot.2008.36 (Pubitemid 351522648)
92. M Zweckstetter A Bax 2001 Characterization of molecular alignment in aqueous suspensions of Pf1 bacteriophage J Biomol NMR 20 365 377 10.1023/A:1011263920003 (Pubitemid 32825731)
93. M Zweckstetter G Hummer A Bax 2004 Prediction of charge-induced molecular alignment of biomolecules dissolved in dilute liquid-crystalline phases Biophys J 86 3444 3460 10.1529/biophysj.103.035790 (Pubitemid 38780229)