Information content of long-range NMR data for the characterization of conformational heterogeneity

Journal of Biomolecular NMR

Volumn 62, Issue 3, 2015, Pages 353-371

  Andrałojć, Witold ^a   Berlin, Konstantin ^b   Fushman, David ^b   Luchinat, Claudio ^a   Parigi, Giacomo ^a   Ravera, Enrico ^a   Sgheri, Luca ^c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b Bldg 142   (United States)

^c CNR   (Italy)

Author keywords

Conformational variability; Paramagnetic NMR; Protein mobility; Residual dipolar couplings; Two domain proteins

Indexed keywords

ANISOTROPY; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DATA PROCESSING; MAGNETIC FIELD; MAGNETISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; RESIDUAL DIPOLAR COUPLING; SIGNAL NOISE RATIO; ALGORITHM; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE; PROCEDURES; PROTEIN CONFORMATION;

PROTEIN;

ALGORITHMS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS;

EID: 84944441781     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-015-9951-6     Document Type: Article

References (132)

1. Al-Hashimi HM, Valafar H, Terrell M, Zartler ER, Eidsness MK, Prestegard JH (2000) Variation of molecular alignment as a means of resolving orientational ambiguities in protein structures from dipolar couplings. J Magn Reson 143:402-406
2. Allegrozzi M, Bertini I, Janik MBL, Lee Y-M, Liu G, Luchinat C (2000) Lanthanide induced pseudocontact shifts for solution structure refinements of macromolecules in shells up to 40 Å from the metal ion. J Am Chem Soc 122:4154-4161
3. Andralojc W, Luchinat C, Parigi G, Ravera E (2014) Exploring regions of conformational space occupied by two-domain proteins. J Phys Chem B 118:10576-10587
4. Balayssac S, Bertini I, Bhaumik A, Lelli M, Luchinat C (2008) Paramagnetic shifts in solid-state NMR of proteins to elicit strucutral information. Proc Natl Acad Sci USA 105:17284-17289
5. Banci L, Bertini I, Bren KL, Cremonini MA, Gray HB, Luchinat C, Turano P (1996) The use of pseudocontact shifts to refine solution structures of paramagnetic metalloproteins: Met80Ala cyanocytochrome c as an example. J Biol Inorg Chem 1:117-126
6. Banci L, Bertini I, Gori Savellini G, Romagnoli A, Turano P, Cremonini MA, Luchinat C, Gray HB (1997) Pseudocontact shifts as constraints for energy minimization and molecular dynamic calculations on solution structures of paramagnetic metalloproteins. Proteins Struct Funct Genet 29:68-76
7. 5 at high magnetic fields: magnetic susceptibility anisotropy contributions and consequences for protein solution structure determination. J Am Chem Soc 120:12903-12909
8. 15N relaxation using inverse detected two-dimensional NMR spectroscopy; the central helix is flexible. Biochemistry 31:5269-5278
9. Barthelmes K, Reynolds AM, Peisach E, Jonker HRA, DeNunzio NJ, Allen KN, Imperiali B, Schwalbe H (2011) Engineering encodable lanthanide-binding tags into loop regions of proteins. J Am Chem Soc 133:808-819
10. Bashir Q, Volkov AN, Ullmann GM, Ubbink M (2010) Visualization of the encounter ensemble of the transient electron transfer complex of cytochrome c and cytochrome c peroxidase. J Am Chem Soc 132:241-247
11. Berlin K, O'Leary DP, Fushman D (2009) Improvement and analysis of computational methods for prediction of residual dipolar couplings. J Magn Reson 201:25-33
12. Berlin K, Castañeda CA, Schneidman-Dohovny D, Sali A, Nava-Tudela A, Fushman D (2013) Recovering a representative conformational ensemble from underdetermined macromolecular structural data. J Am Chem Soc 135:16595-16609
13. Bernadò P, Mylonas E, Petoukhov MV, Blackledge M, Svergun DI (2007) Structural characterization of flexible proteins using small-angle X-ray scattering. J Am Chem Soc 129:5656-5664
14. 9k. J Biomol NMR 21:85-98
15. Bertini I, Janik MBL, Lee Y-M, Luchinat C, Rosato A (2001b) Magnetic susceptibility tensor anisotropies for a lanthanide Ion series in a fixed protein matrix. J Am Chem Soc 123:4181-4188
16. Bertini I, Janik MBL, Liu G, Luchinat C, Rosato A (2001c) Solution structure calculations through self-orientation in a magnetic field of cerium (III) substituted calcium-binding protein. J Magn Reson 148:23-30
17. Bertini I, Longinetti M, Luchinat C, Parigi G, Sgheri L (2002a) Efficiency of paramagnetism-based constraints to determine the spatial arrangement of α-helical secondary structure elements. J Biomol NMR 22:123-136
18. Bertini I, Luchinat C, Parigi G (2002b) Magnetic susceptibility in paramagnetic NMR. Prog NMR Spectrosc 40:249-273
19. Bertini I, Gelis I, Katsaros N, Luchinat C, Provenzani A (2003) Tuning the affinity for lanthanides of calcium binding proteins. Biochemistry 42:8011-8021
20. Bertini I, Del Bianco C, Gelis I, Katsaros N, Luchinat C, Parigi G, Peana M, Provenzani A, Zoroddu MA (2004a) Experimentally exploring the conformational space sampled by domain reorientation in calmodulin. Proc Natl Acad Sci USA 101:6841-6846
21. II matrix metalloproteinase 12. Angew Chem Int Ed 43:2254-2256
22. Bertini I, Luchinat C, Parigi G, Pierattelli R (2005) NMR of paramagnetic metalloproteins. ChemBioChem 6:1536-1549
23. Bertini I, Gupta YK, Luchinat C, Parigi G, Peana M, Sgheri L, Yuan J (2007) Paramagnetism-based NMR restraints provide maximum allowed probabilities for the different conformations of partially independent protein domains. J Am Chem Soc 129:12786-12794
24. Bertini I, Luchinat C, Parigi G, Pierattelli R (2008) Perspectives in NMR of paramagnetic proteins. Dalton Trans 2008:3782-3790
25. Bertini I, Kursula P, Luchinat C, Parigi G, Vahokoski J, Willmans M, Yuan J (2009) Accurate solution structures of proteins from X-ray data and minimal set of NMR data: calmodulin peptide complexes as examples. J Am Chem Soc 131:5134-5144
26. Bertini I, Bhaumik A, De Paepe G, Griffin RG, Lelli M, Lewandowski JR, Luchinat C (2010a) High-resolution solidstate NMR structure of a 17.6 kDa protein. J Am Chem Soc 132:1032-1040
27. Bertini I, Giachetti A, Luchinat C, Parigi G, Petoukhov MV, Pierattelli R, Ravera E, Svergun DI (2010b) Conformational space of flexible biological macromolecules from average data. J Am Chem Soc 132:13553-13558
28. Bertini I, Calderone V, Cerofolini L, Fragai M, Geraldes CFGC, Hermann P, Luchinat C, Parigi G, Teixeira JMC (2012a) The catalytic domain of MMP-1 studied through tagged lanthanides. Dedicated to Prof. A.V. Xavier. FEBS Lett 586:557-567
29. Bertini I, Ferella L, Luchinat C, Parigi G, Petoukhov MV, Ravera E, Rosato A, Svergun DI (2012b) MaxOcc: a web portal for maximum occurence analysis. J Biomol NMR 53:271-280
30. Bertini I, Luchinat C, Nagulapalli M, Parigi G, Ravera E (2012c) Paramagnetic relaxation enhancements for the characterization of the conformational heterogeneity in two-domain proteins. Phys Chem Chem Phys 14:9149-9156
31. Blackledge M (2005) Recent progress in the study of biomolecular structure and dynamics in solution from residual dipolar couplings. Prog NMR Spectrosc 46:23-61
32. Boehr DD, McElheny D, Dyson HJ, Wright PE (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313:1638-1642
33. Boehr DD, Nussinov R, Wright PE (2009) The role of dynamic conformational ensembles in biomolecular recognition (vol 5, pg 789, 2009).
34. Nat Chem Biol 5:954
35. Bonvin AM, Brunger AT (1996) Do NOE distances contain enough information to assess the relative populations of multi-conformer structures? J Biomol NMR 7:72-76
36. Bothe JR, Nikolova EN, Eichhorn CD, Chugh J, Hansen AL, Al Hashimi HM (2011) Characterizing RNA dynamics at atomic resolution using solution-state NMR spectroscopy. Nat Methods 8:919-931
37. Burgi R, Pitera J, Van Gunsteren WF (2001) Assessing the effect of conformational averaging on the measured values of observables. J Biomol NMR 19:305-320
38. Camilloni C, Vendruscolo M (2015) A tensor-free method for the structural and dynamical refinement of proteins using residual dipolar couplings. J Phys Chem B 119:653-661
39. Cerofolini L, Fields GB, Fragai M, Geraldes CFGC, Luchinat C, Parigi G, Ravera E, Svergun DI, Teixeira JMC (2013) Examination of matrix metalloproteinase-1 (MMP-1) in solution: a preference for the pre-collagenolysis state. J Biol Chem 288:30659-30671
40. Chen Y, Campbell SL, Dokholyan NV (2007) Deciphering protein dynamics from NMR data using explicit structure sampling and selection. Biophys J 93:2300-2306
41. 2+ calmodulin reveals flexible hand-like properties of its domains. Nat Struct Biol 8:990-997
42. Choy W-Y, Forman-Kay JD (2001) Calculation of ensembles of structures representing the unfolded state of an SH3 domain. J Mol Biol 308:1011-1032
43. Chuang GY, Mehra-Chaudhary R, Ngan CH, Zerbe BS, Kozakov D, Vajda S, Beamer LJ (2010) Domain motion and interdomain hot spots in a multidomain enzyme. Protein Sci 19:1662-1672
44. Clore GM, Schwieters CD (2004) How much backbone motion in ubiquitin is required to account for dipolar coupling data measured in multiple alignment media as assessed by independent cross-validation? J Am Chem Soc 126:2923-2938
45. Das Gupta S, Hu X, Keizers PHJ, Liu W-M, Luchinat C, Nagulapalli M, Overhand M, Parigi G, Sgheri L, Ubbink M (2011) Narrowing the conformational space sampled by two-domain proteins with paramagnetic probes in both domains. J Biomol NMR 51:253-263
46. Diaz-Moreno I, Diaz-Quintana A, De la Rosa MA, Ubbink M (2005) Structure of the complex between plastocyanin and cytochrome f from the cyanobacterium nostoc Sp. PCC 7119 as determined by paramagnetic NMR. J Biol Chem 280:18908-18915
47. Fisher CK, Stultz CM (2011) Constructing ensembles for instrinsically disordered proteins. Curr Opin Struct Biol 21:426-431
48. Fisher CK, Huang A, Stultz CM (2010) Modeling intrinsically disordered proteins with bayesian statistics. J Am Chem Soc 132:14919-14927
49. Fragai M, Luchinat C, Parigi G (2006) "Four-dimensional" protein structures: examples from metalloproteins. Acc Chem Res 39:909-917
50. Gaponenko V, Sarma SP, Altieri AS, Horita DA, Li J, Byrd RA (2004) Improving the accuracy of NMR structures of large proteins using pseudocontact shifts as long/range restraints. J Biomol NMR 28:205-212
51. Gardner RJ, Longinetti M, Sgheri L (2005) Reconstruction of orientations of a moving protein domain from paramagnetic data. Inverse Probl 21:879-898
52. Gempf KL, Butler SJ, Funk AM, Parker D (2013) Direct and selective tagging of cysteine residues in peptides and proteins with 4-nitropyridyl lanthanide complexes. Chem Commun (Camb) 49:9104-9106
53. Gochin M, Roder H (1995a) Protein structure refinement based on paramagnetic NMR shifts: applications to wild-type and mutants forms of cytochrome c. Protein Sci 4:296-305
54. Gochin M, Roder H (1995b) Use of pseudocontact shifts as a structural constraint for macromolecules in solution. Bull Magn Reson 17:1-4
55. Guerry P, Salmon L, Mollica L, Ortega Roldan JL, Markwick P, van Nuland NA, McCammon JA, Blackledge M (2013) Mapping the population of protein conformational energy sub-states from NMR dipolar couplings. Angew Chem Int Ed Engl 52:3181-3185
56. Hansen MR, Mueller L, Pardi A (1998) Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat Struct Biol 5:1065-1074
57. Hass MAS, Keizers PHJ, Blok A, Hiruma Y, Ubbink M (2010) Validation of a lanthanide tag for the analysis of protein dynamics by paramagnetic NMR spectroscopy. J Am Chem Soc 132:9952-9953
58. Häussinger D, Huang J, Grzesiek S (2009) DOTA-M8: an extremely rigid, high-affinity lanthanide chelating tag for PCS NMR spectroscopy. J Am Chem Soc 131:14761-14767
59. Huang J, Grzesiek S (2010) Ensemble calculations of unstructured proteins constrained by RDC and PRE data: a case study of urea-denatured ubiquitin. J Am Chem Soc 132:694-705
60. Hulsker R, Baranova MV, Bullerjahn GS, Ubbink M (2008) Dynamics in the transient complex of plastocyanin-cytochrome f from Prochlorothrix hollandica. J Am Chem Soc 130:1985-1991
61. Iwahara J, Schwieters CD, Clore GM (2004) Ensemble approach for NMR structure refinement against H-1 paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule. J Am Chem Soc 126:5879-5896
62. Jensen MR, Hansen DF, Ayna U, Dagil R, Hass MA, Christensen HE, Led JJ (2006) On the use of pseudocontact shifts in the structure determination of metalloproteins. Magn Reson Chem 44:294-301
63. John M, Otting G (2007) Strategies for measurements of pseudocontact shifts in protein NMR spectroscopy. ChemPhysChem 8:2309-2313
64. Jones E, Oliphant E, Peterson P et al (2001) SciPy: Open source scientific tools for Python
65. Keizers PHJ, Saragliadis A, Hiruma Y, Overhand M, Ubbink M (2008) Design, synthesis, and evaluation of a lanthanide chelating protein probe: CLaNP-5 yields predictable paramagnetic effects independent of environment. J Am Chem Soc 130:14802-14812
66. Kobashigawa Y, Saio T, Ushio M, Sekiguchi M, Yokochi M, Ogura K, Inagaki F (2012) Convenient method for resolving degeneracies due to symmetry of the magnetic susceptibility tensor and its application to pseudo contact shift-based protein-protein complex structure determination. J Biomol NMR 53:53-63
67. Korzhnev DM, Kay LE (2008) Probing invisible, low-populated states of protein molecules by relaxation dispersion NMR spectroscopy: an application to protein folding. Acc Chem Res 41:442-451
68. Kuffner JJ (2004) Effective sampling and distance metrics for 3D rigid body path planning. In: Proceedings IEEE international conference on Robotics and Automation (ICRA), vol 4, p 3993
69. Kukic P, Camilloni C, Cavalli A, Vendruscolo M (2014) Determination of the individual roles of the linker residues in the interdomain motions of calmodulin using NMR chemical shifts. J Mol Biol 426:1826-1838
70. Kurland RJ, McGarvey BR (1970) Isotropic NMR shifts in transition metal complexes: calculation of the Fermi contact and pseudocontact terms. J Magn Reson 2:286-301
71. Lakomek NA, Walter KF, Fares C, Lange OF, de Groot BL, Grubmuller H, Bruschweiler R, Munk A, Becker S, Meiler J, Griesinger C (2008) Self-consistent residual dipolar coupling based model-free analysis for the robust determination of nanosecond to microsecond protein dynamics. J Biomol NMR 41:139-155
72. Lange OF, Lakomek N-A, Farès C, Schröder GF, Walter KFA, Becker S, Meiler J, Grubmüller H, Griesinger C, de Groot BL (2008) Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320:1471-1475
73. Latham MP, Hanson P, Brown DJ, Pardi A (2008) Comparison of alignment tensors generated for native tRNA(Val) using magnetic fields and liquid crystalline media. J Biomol NMR 40:83-94
74. Lindorff-Larsen K, Best RB, DePristo MA, Dobson CM, Vendruscolo M (2005) Simultaneous determination of protein structure and dynamics. Nature 433:128-132
75. Liu WM, Keizers PH, Hass MA, Blok A, Timmer M, Sarris AJ, Overhand M, Ubbink M (2012) A pH-sensitive, colorful, lanthanide-chelating paramagnetic NMR probe. J Am Chem Soc 134:17306-17313
76. Loh CT, Ozawa K, Tuck KL, Barlow N, Huber T, Otting G, Graham B (2013) Lanthanide tags for site-specific ligation to an unnatural amino acid and generation of pseudocontact shifts in proteins. Bioconjug Chem 24:260-268
77. Lohman JAB, Maclean C (1978) Alignment effects on high resolution NMR spectra induced by the magnetic field. Chem Phys 35:269-274
78. Longinetti M, Luchinat C, Parigi G, Sgheri L (2006) Efficient determination of the most favored orientations of protein domains from paramagnetic NMR data. Inverse Probl 22:1485-1502
79. Losonczi JA, Prestegard JH (1998) Improved dilute bicelle solutions for high-resolution NMR of biological macromolecules. J Biomol NMR 12:447-451
80. Losonczi JA, Andrec M, Fischer MW, Prestegard JH (1999) Order matrix analysis of residual dipolar couplings using singular value decomposition. J Magn Reson 138:334-342
81. Luchinat C, Nagulapalli M, Parigi G, Sgheri L (2012a) Maximum occurence analysis of protein conformations for different distributions of paramagnetic metal ions within flexible twodomain proteins. J Magn Reson 215:85-93
82. Luchinat C, Parigi G, Ravera E, Rinaldelli M (2012b) Solid state NMR crystallography through paramagnetic restraints. J Am Chem Soc 134:5006-5009
83. Maltsev AS, Grishaev A, Roche J, Zasloff M, Bax A (2014) Improved cross validation of a static ubiquitin structure derived from high precision residual dipolar couplings measured in a drug-based liquid crystalline phase. J Am Chem Soc 136:3752-3755
84. Man B, Su XC, Liang H, Simonsen S, Huber T, Messerle BA, Otting G (2010) 3-Mercapto-2,6-pyridinedicarboxylic acid: a small lanthanide-binding tag for protein studies by NMR spectroscopy. Chem Eur J 16:3827-3832
85. Montalvao R, Camilloni C, De SA, Vendruscolo M (2014) New opportunities for tensor-free calculations of residual dipolar couplings for the study of protein dynamics. J Biomol NMR 58:233-238
86. Musiani F, Rossetti G, Capece L, Gerger TM, Micheletti C, Varani G, Carloni P (2014) Molecular dynamics simulations identify time scale of conformational changes responsible for conformational selection in molecular recognition of HIV-1 transactivation responsive RNA. J Am Chem Soc 136:15631-15637
87. Nesterov Y (2012) Efficiency of coordinate descent methods on huge-scale optimization problems. SIAM J Optim 22:341-362
88. Nodet L, Salmon L, Ozenne V, Meier S, Jensen MR, Blackledge M (2009) Quantitative description of backbone conformational sampling of unfolded proteins at amino acid resolution from NMR residual dipolar couplings. J Am Chem Soc 131:17908-17918
89. O'Leary DP (2009) Scientific computing with case studies. SIAM, Bangkok
90. Pickford AR, Campbell ID (2004) NMR studies of modular protein structures and their interactions. Chem Rev 104:3557-3566
91. Pintacuda G, John M, Su XC, Otting G (2007) NMR structure determination of protein-ligand complexes by lanthanide labeling. Acc Chem Res 40:206-212
92. Prestegard JH, Al-Hashimi HM, Tolman JR (2000) NMR structures of biomolecules using field oriented media and residual dipolar couplings. Q Rev Biophys 33:371-424
93. Ramirez BE, Bax A (1998) Modulation of the alignment tensor of macromolecules dissolved in a dilute liquid crystalline medium. J Am Chem Soc 120:9106-9107
94. Ravera E, Salmon L, Fragai M, Parigi G, Al-Hashimi HM, Luchinat C (2014) Insights into domain-domain motions in proteins and RNA from solution NMR. Acc Chem Res 47:3118-3126
95. Rinnenthal J, Buck J, Ferner J, Wacker A, Furtig B, Schwalbe H (2011) Mapping the landscape of RNA dynamics with NMR spectroscopy. Acc Chem Res 44:1292-1301
96. Rodriguez-Castañeda F, Haberz P, Leonov A, Griesinger C (2006) Paramagnetic tagging of diamagnetic proteins for solution NMR. Magn Reson Chem 44:S10-S16
97. Russo L, Maestre-Martinez M, Wolff S, Becker S, Griesinger C (2013) Interdomain dynamics explored by paramagnetic NMR. J Am Chem Soc 135:17111-17120
98. Ryabov YE, Fushman D (2006) Analysis of interdomain dynamics in a two-domain protein using residual dipolar couplings together with 15 N relaxation data. Magn Reson Chem 44:S143-S151
99. Ryabov YE, Fushman D (2007) A model of Interdomain mobility in a multidomain protein. J Am Chem Soc 129:3315-3327
100. Saio T, Ogura K, Shimizu K, Yokochi M, Burke TR Jr, Inagaki F (2011) An NMR strategy for fragment-based ligand screening utilizing a paramagnetic lanthanide probe. J Biomol NMR 51:395-408
101. Schmitz C, Vernon R, Otting G, Baker D, Huber T (2012) Protein structure determination from pseudocontact shifts using ROSETTA. J Mol Biol 416:668-677
102. Schroeder R, Barta A, Semrad K (2004) Strategies for RNA folding and assembly. Nat Rev Mol Cell Biol 5:908-919
103. Sgheri L (2010a) Conformational freedom of proteins and the maximal probability of sets of orientations. Inverse Probl 26:035003-1-035003-19
104. Sgheri L (2010b) Joining RDC data from flexible protein domains. Inverse Probl 26:1150211-11502112
105. Sicheri F, Kuriyan J (1997) Structures of Src-family tyrosine kinases. Curr Opin Struct Biol 7:777-785
106. Simin M, Irausquin S, Cole CA, Valafar H (2014) Improvements to REDCRAFT: a software tool for simultaneous characterization of protein backbone structure and dynamics from residual dipolar couplings. J Biomol NMR 60:241-264
107. Stelzer AC, Frank AT, Bailor MH, Andricioaei I, Al Hashimi HM (2009) Constructing atomic-resolution RNA structural ensembles using MD and motionally decoupled NMR RDCs. Methods 49:167-173
108. Su XC, Otting G (2010) Paramagnetic labelling of proteins and oligonucleotides for NMR. J Biomol NMR 46:101-112
109. Su XC, Huber T, Dixon NE, Otting G (2006) Site-specific labelling of proteins with a rigid lanthanide-binding tag. ChemBioChem 7:1599-1604
110. Su XC, Man B, Beeren S, Liang H, Simonsen S, Schmitz C, Huber T, Messerle BA, Otting G (2008a) A dipicolinic acid tag for rigid lanthanide tagging of proteins and paramagnetic NMR spectroscopy. J Am Chem Soc 130:10486-10487
111. Su XC, McAndrew K, Huber T, Otting G (2008b) Lanthanide-binding peptides for NMR measurements of residual dipolar couplings and paramagnetic effects from multiple angles. J Am Chem Soc 130:1681-1687
112. Svergun DI, Petoukhov MV, Koch MHJ (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys J 80:2946-2953
113. Swarbrick JD, Ung P, Chhabra S, Graham B (2011a) An iminodiacetic acid based lanthanide binding tag for paramagnetic exchange NMR spectroscopy. Angew Chem Int Ed Engl 50:4403-4406
114. Swarbrick JD, Ung P, Su XC, Maleckis A, Chhabra S, Huber T, Otting G, Graham B (2011b) Engineering of a bis-chelator motif into a protein alpha-helix for rigid lanthanide binding and paramagnetic NMR spectroscopy. Chem Commun (Camb) 47:7368-7370
115. Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a diluite liquid crystalline medium. Science 278:1111-1114
116. 15N-NMR relaxation measurements. Eur J Biochem 230:1014-1024
117. Tolman JR (2001) Dipolar couplings as a probe of molecular dynamics and structure in solution. Curr Opin Struct Biol 11:532-539
118. Tolman JR, Ruan K (2006) NMR residual dipolar couplings as probes of biomolecular dynamics. Chem Rev 106:1720-1736
119. Tolman JR, Flanagan JM, Kennedy MA, Prestegard JH (1995) Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution. Proc Natl Acad Sci USA 92:9279-9283
120. Tonks NK (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7:833-846
121. Torchia DA (2015) NMR studies of dynamic biomolecular conformational ensembles. Prog Nucl Magn Reson Spectrosc 84-85:14-32
122. Valafar H, Prestegard JH (2004) REDCAT: a residual dipolar coupling analysis tool. J Magn Reson 167:228-241
123. Wang H, Eberstadt M, Olejniczak ET, Meadows RP, Fesik SW (1998) A liquid crystalline medium for measuring residual dipolar couplings over a wide range of temperatures. J Biomol NMR 12:443-446
124. Wöhnert J, Franz KJ, Nitz M, Imperiali B, Schwalbe H (2003) Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings. J Am Chem Soc 125:13338-13339
125. Yagi H, Maleckis A, Otting G (2013a) A systematic study of labelling an alpha-helix in a protein with a lanthanide using IDA-SH or NTA-SH tags. J Biomol NMR 55:157-166
126. Yagi H, Pilla KB, Maleckis A, Graham B, Huber T, Otting G (2013b) Three-dimensional protein fold determination from backbone amide pseudocontact shifts generated by lanthanide tags at multiple sites. Structure 21:883-890
127. Zhang Y, Zuiderweg ER (2004) The 70-kDa heat shock protein chaperone nucleotide-binding domain in solution unveiled as a molecular machine that can reorient its functional subdomains. Proc Natl Acad Sci USA 101:10272-10277
128. Zhang Q, Throolin R, Pitt SW, Serganov A, Al Hashimi HM (2003) Probing motions between equivalent RNA domains using magnetic field induced residual dipolar couplings: accounting for correlations between motions and alignment. J Am Chem Soc 125:10530-10531
129. Zhuang T, Lee HS, Imperiali B, Prestegard JH (2008) Structure determination of a Galectin-3-carbohydrate complex using paramagnetism-based NMR constraints. Protein Sci 17:1220-1231
130. Zweckstetter M (2008) NMR: prediction of molecular alignment from structure using the PALES software. Nat Protoc 3:679-690
131. Zweckstetter M, 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
132. Zweckstetter M, Bax A (2001) Characterization of molecular alignment in aqueous suspensions of Pf1 bacteriophage. J Biomol NMR 20:365-377