Automated NMR assignment and protein structure determination using sparse dipolar coupling constraints

Progress in Nuclear Magnetic Resonance Spectroscopy

Volumn 55, Issue 2, 2009, Pages 101-127

  Donald, Bruce R ^a   Martin, Jeffrey ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 67650473269     PISSN: 00796565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnmrs.2008.12.001     Document Type: Review

References (176)

1. Eiso A.B., Pugh D.J.R., Kaptein R., Boelens R., and Bonvin A.M.J.J. Direct use of unassigned resonances in NMR structure calculations with proxy residues. J. Am. Chem. Soc. 128 23 (2006) 7566-7571
2. Al-Hashimi H.M., Bolon P.J., and Prestegard J.H. Molecular symmetry as an aid to geometry determination in ligand protein complexes. J. Magn. Reson. 142 (2000) 153-158
3. Al-Hashimi H.M., Gorin A., Majumdar A., Gosser Y., and Patel D.J. Towards structural genomics of RNA: rapid NMR resonance assignment and simultaneous RNA tertiary structure determination using residual dipolar couplings. J. Mol. Biol. 318 (2002) 637-649
4. Al-Hashimi H.M., and Patel D.J. Residual dipolar couplings: synergy between NMR and structural genomics. J. Biomol. NMR 22 1 (2002) 1-8
5. Anderson A.C. Two crystal structures of dihydrofolate reductase-thymidylate synthase from Cryptosporidium hominis reveal protein-ligand interactions including a structural basis for observed antifolate resistance. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61 Pt. 3 (2005) 258-262
6. Andrec M., Du P., and Levy R.M. Protein backbone structure determination using only residual dipolar couplings from one ordering medium. J. Biomol. NMR 21 4 (2001) 335-347
7. Annila A., Aitio H., Thulin E., and Drakenberg T. Recognition of protein folds via dipolar couplings. J. Biomol. NMR 14 (1999) 223-230
8. Apaydin S., Conitzer V., and Donald B.R. Structure-based protein NMR assignments using native structural ensembles. J. Biomol. NMR 40 (2008) 263-276
9. Artymiuk P.J., Blake C.C.F., Rice D.W., and Wilson K.S. The structures of the monoclinic and orthorhombic forms of hen egg-white lysozyme at 6 angstroms resolution. Acta Crystallogr. B Biol. Crystallogr. 38 (1982) 778
10. Babu C.R., Flynn P.F., and Wand A.J. Validation of protein structure from preparations of encapsulated proteins dissolved in low viscosity fluids. J. Am. Chem. Soc. 123 (2001) 2691
11. C. Bailey-Kellogg, J.J. Kelley III, R. Lilien, B.R. Donald, Physical geometric algorithms for structural molecular biology, in: The Special Session on Computational Biology & Chemistry, Proceedings IEEE International Conference on Robotics and Automation (ICRA-2001), May 2001, pp. 940-947.
12. Bailey-Kellogg C., Widge A., Kelley III J.J., Berardi M.J., Bushweller J.H., and Donald B.R. The NOESY jigsaw: automated protein secondary structure and main-chain assignment from sparse, unassigned NMR data. J. Comp. Biol. 3-4 7 (2000) 537-558
13. Coggins B.E., and Zhou P. Sampling of the NMR time domain along concentric rings. J. Magn. Reson. 184 2 (2007) 207-221
14. Berger B., Kleinberg J., and Leighton F.T. Reconstructing a three-dimensional model with arbitrary errors. J. ACM 46 2 (1999) 212-235
15. Brünger A.T. XPLOR: A System for X-ray Crystallography and NMR (1993), Yale University Press, New Haven
16. Cavanaugh J., Fairbrother W.J., Palmer III A.G., and Skelton N.J. Protein NMR Spectroscopy: Principles and Practice (1995), Academic Press
17. Cavasotto C.N., Kovacs J.A., and Abagyan R.A. Representing receptor flexibility in ligand docking through relevant normal modes. J. Am. Chem. Soc. 127 26 (2005) 9632-9640
18. Chen Y., Reizer J., Saier Jr. M.H., Fairbrother W.J., and Wright P.E. Mapping of the binding interfaces of the proteins of the bacterial phosphotransferase system, HPr and IIAglc. Biochemistry 32 1 (1993) 32-37
19. Chou J.J., Li S., and Bax A. Study of conformational rearrangement and refinement of structural homology models by the use of heteronuclear dipolar couplings. J. Biomol. NMR 18 (2000) 217-227
20. Clore G.M., Omichinski J.G., Sakaguchi K., Zambrano N., Sakamoto H., Appella E., and Gronenborn A.M. Interhelical angles in the solution structure of the oligomerization domain of p53: correction. Science 267 5203 (1995) 1515-1516
21. 3 - NH NOESY spectrum on a 29 kDa protein. J. Am. Chem. Soc. 127 33 (2005) 11562-11563
22. Coggins B.E., and Zhou P. PACES: protein sequential assignment by computer-assisted exhaustive search. J. Biomol. NMR 26 2 (2003) 93-111
23. Coggins B.E., and Zhou P. Polar Fourier transforms of radially sampled NMR data. J. Magn. Reson. 182 1 (2006) 84-95
24. HC′ in a perdeuterated protein. J. Magn. Reson. 40 2 (1999) 510-512
25. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
26. Coutsias E.A., Seok C., Jacobson M.P., and Dill K.A. A kinematic view of loop closure. J. Comput. Chem. 25 4 (2004) 510-528
27. Coutsias E.A., Seok C., Wester M.J., and Dill K.A. Resultants and loop closure. Int. J. Quant. Chem. 106 1 (2006) 176-189
28. Crippen G. Chemical distance geometry: current realization and future projection. J. Math. Chem. 6 (1991) 307-324
29. Crippen G.M., and Havel T.F. Distance Geometry and Molecular Conformations (1988), Wiley
30. Cross A.D.J., and Hancock E.R. Graph matching with a dual-step EM algorithm. IEEE Trans. Pattern Anal. Mach. Intell. 20 11 (1998) 1236-1253
31. del Rio-Portílla F., Blechta V., and Freeman R. Measurement of poorly-resolved splittings by J-doubling in the frequency domain. J. Magn. Reson. 111a (1994) 132-135
32. Delaglio F., Kontaxis G., and Bax A. Protein structure determination using molecular fragment replacement and NMR dipolar couplings. J. Am. Chem. Soc. 122 9 (2000) 2142-2143
33. Dempster A., Laird N., and Rubin D. Maximum likelihood from incomplete data via the EM algorithm. J. R. Stat. Soc. Ser. B 39 1 (1977) 1-38
34. Desmet J., DeMaeyer M., Hazes B., and Lasters I. The dead-end elimination theorem and its use in protein side chain positioning. Nature 356 (1992) 539-542
35. Diamond R. Real-space refinement of the structure of hen egg-white lysozyme. J. Mol. Biol. 82 (1974) 371-391
36. Donald B.R. Plenary lecture: algorithmic challenges in structural molecular biology and proteomics. In: Erdmann M., Overmars M., Hsu D., and van der Stappen A.F. (Eds). Proceedings of the Sixth International Workshop on the Algorithmic Foundations of Robotics (WAFR), pp 1-10, Utrecht/Zeist, The Netherlands, July 2004. University of Utrecht. Algorithmic Foundations of Robotics VI, Springer Tracts in Advanced Robotics vol. 17 (2005), Springer, Berlin 1-10
37. Donald B.R., Kapur D., and Mundy J. Symbolic and Numerical Computation for Artificial Intelligence (1992), Academic Press, Harcourt Jovanovich, London
38. Fowler A.C., Tian F., Al-Hashimi H.M., and Prestegard J.H. Rapid determination of protein folds using residual dipolar couplings. J. Mol. Biol. 304 3 (2000) 447-460
39. Gallagher T., Alexander P., Bryan P., and Gilliland G.L. Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR. Biochemistry 33 (1994) 4721-4729
40. 1 H - δ 1 methyl) isoleucine into proteins for multidimensional NMR studies. J. Am. Chem. Soc. 119 32 (1997) 7599-7600
41. Gemmecker G., Jahnke W., and Kessler H. Measurement of fast proton exchange rates in isotopically labelled compounds. J. Am. Chem. Soc. 115 24 (1993) 11620-11621
42. Georgiev I., and Donald B.R. Dead-end elimination with backbone flexibility. Bioinformatics 23 13 (2007) (special issue on papers from the International Conference on Intelligent Sys. for Mol. Biol. (ISMB 2007), Vienna, Austria, July 21-25, 2007)
43. Georgiev I., Keedy D., Richardson J., Richardson D., and Donald B.R. Algorithm for backrub motions in protein design. Bioinformatics 22 (2008) e174-e183 (special issue on papers from International Conference on Intelligent Sys. for Mol. Biol. (ISMB 2008) Toronto, CA, July, 2008)
44. Georgiev I., Lilien R., and Donald B.R. Improved pruning algorithms and divide-and-conquer strategies for dead-end elimination, with application to protein design. Bioinformatics 22 14 (2006) e174-e183 (special issue on papers from the Int'l Conf. on Intelligent Sys. Mol. Biol. (ISMB 2006), Fortaleza, Brazil)
45. Georgiev I., Lilien R., and Donald B.R. The minimized dead-end elimination criterion and its application to protein redesign in a hybrid scoring and search algorithm for computing partition functions over molecular ensembles. J. Comput. Chem. 29 10 (2008) 1527-1542
46. Giesen A.W., Homans S.W., and Brown J.M. Determination of protein global folds using backbone residual dipolar coupling and long-range NOE restraints. J. Biomol. NMR 25 (2003) 63-71
47. Girard E., Chantalat L., Vicat J., and Kahn R. Gd-HPDO3A, a complex to obtain high-phasing-power heavy atom derivatives for SAD and MAD experiments: results with tetragonal hen egg-white lysozyme. Acta Crystallogr. D Biol. Crystallogr. 58 (2001) 1-9
48. Goldstein R. Efficient rotamer elimination applied to protein side-chains and related spin glasses. Biophys. J. 66 (1994) 1335-1340
49. Gorczynski M.J., Grembecka J., Zhou Y., Kong Y., Roudaiya L., Douvas M.G., Newman M., Bielnicka I., Baber G., Corpora T., Shi J., Sridharan M., Lilien R., Donald B.R., Speck N.A., Brown M.L., and Bushweller J.H. Allosteric inhibition of the protein-protein interaction between the leukemia-associated proteins RUNX1 and CBF β. Chem. Biol. 14 10 (2007)
50. Gronenborn A.M., Filpula D.R., Essig N.Z., Achari A., Whitlow M., Wingfield P.T., and Clore G.M. A novel highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science 253 (1991) 657
51. Grzesiek S., and Bax A. Measurement of amide proton exchange rates and NOEs with water in 13C/15N-enriched calcineurin B. J. Biomol. NMR 3 6 (1993) 627-638
52. Güntert P., Mumenthaler C., and Wüthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273 (1997) 283-298
53. Guntert P. Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278 (2004) 353-378
54. Hajduk P.J., Meadows R.P., and Fesik S.W. Drug design: discovering high-affinity ligands for proteins. Science 278 (1997) 497-499
55. Hendrickson B. Conditions for unique graph realizations. SIAM J. Comput. 21 (1992) 65-84
56. Hendrickson B. The molecule problem: exploiting structures in global optimization. SIAM J. Optimization 5 (1995) 835-857
57. Herrmann T., Güntert P., and Wüthrich K. Protein NMR structure determination with automated noe assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319 (2002) 209-227
58. K. Hinsen, Normal mode theory and harmonic potential approximations, Course and Lecture Notes. http://dirac.cnrs-orleans.fr/~hinsen/, Centre de Biophysique Molculaire (CNRS), Orleans, France, 2000.
59. Huang Y.J., Swapna G.V., Rajan P.K., Ke H., Xia B., Shukla K., Inouye M., and Montelione G.T. Solution NMR structure of ribosome-binding factor a (RbfA), a coldshock adaptation protein from Escherichia coli. J. Mol. Biol. 327 (2003) 521-536
60. Huang Y.J., Tejero R., Powers R., and Montelione G.T. A topology-constrained distance network algorithm for protein structure determination from NOESY data. Proteins 62 3 (2006) 587-603
61. Hus J.-C., Marion D., and Blackledge M. De novo determination of protein structure by NMR using orientational and long-range order restraints. J. Mol. Biol. 298 5 (2000) 927-936
62. Hus J.C., Marion D., and Blackledge M. Determination of protein backbone using only residual dipolar couplings. J. Am. Chem. Soc. 123 (2001) 1541-1542
63. Hus J.C., Prompers J., and Brüschweiler R. Assignment strategy for proteins of known structure. J. Magn. Reson. 157 (2002) 119-125
64. Korukottu J., Bayrhuber M., Montaville P., Vijayan V., Jung Y.S., Becker S., and Zweckstetter M. Fast high-resolution protein structure determination by using unassigned NMR data. Angew. Chem. Int. Ed. Engl. 46 (2007) 1176-1179
65. Jacobs D.J., Rader A.J., Kuhn L.A., and Thorpe M.F. Protein flexibility predictions using graph theory. Proteins 44 2 (2001) 150-165
66. Johnson E.C., Lazar G.A., Desjarlais J.R., and Handel T.M. Solution structure and dynamics of a designed hydrophobic core variant of ubiquitin. Struct. Fold Des. 7 (1999) 967-976
67. Jung Y.S., and Zweckstetter M. Backbone assignment of proteins with known structure using residual dipolar couplings. J. Biomol. NMR 30 1 (2004) 25-35
68. Juszewski K., Schwieters C.D.S., 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
69. Ruan K., Briggman K.B., and Tolman J.R. De novo determination of internuclear vector orientations from residual dipolar couplings measured in three independent alignment media. J. Biomol. NMR 41 2 (2008) 61-76
70. Kamisetty H., Bailey-Kellogg C., and Pandurangan G. An efficient randomized algorithm for contact-based NMR backbone resonance assignment. Bioinformatics 22 2 (2006) 172-180
71. Kay L.E. Protein dynamics from NMR. Nat. Struct. Biol. 5 (1998) 513-517
72. Kemple M.D., Ray B.D., Lipkowitz K.B., Prendergast F.G., and Rao B.D. The use of lanthanides for solution structure determination of biomolecules by NMR: evaluation of the methodology with EDTA derivatives as model systems. J. Am. Chem. Soc. 110 25 (1988) 8275-8287
73. Kim D.E., Chivian D., and Baker D. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 32 Web Server issue (2004) 526-531
74. Kolodny R., Guibas L., Levitt M., and Koehl P. Inverse kinematics in biology: the protein loop closure problem. Int. J. Robotics Res. 24 (2005) 151-163
75. 2+-selective channels in lipid bilayers. J. Biol. Chem. 263 (1988) 18364-18368
76. Kuhn H.W. Hungarian method for the assignment problem. Nav. Res. Logist. Q. 2 (1955) 83-97
77. Kurinov I.V., and Harrison R.W. The influence of temperature on lysozyme crystals - structure and dynamics of protein and water. Acta Crystallogr. D Biol. Crystallogr. 51 (1995) 98-109
78. C. Langmead, B.R. Donald, 3D structural homology detection via unassigned residual dipolar couplings, in: Proceedings of the IEEE Computer Society Bioinformatics Conference (CSB), Stanford, August 2003, pp. 209-217, PMID: 16452795.
79. Langmead C., and Donald B.R. An expectation/maximization nuclear vector replacement algorithm for automated NMR resonance assignments. J. Biomol. NMR 29 2 (2004) 111-138
80. C. Langmead, B.R. Donald, High-throughput 3D structural homology detection via NMR resonance assignment, in: Proceedings of the IEEE Computational Systems Bioinformatics Conference (CSB), Stanford, CA, August 2004, pp. 278-289, PMID: 16448021.
81. C. Langmead, C.R. McClung, B.R. Donald, A maximum entropy algorithm for rhythmic analysis of genome-wide expression patterns, in: Proceedings of the IEEE Computer Society Bioinformatics Conference (IEEE CSB), August 2002, pp. 237-245, PMID: 15838140.
82. Langmead C., Yan A., Lilien R., Wang L., and Donald B.R. A polynomial-time nuclear vector replacement algorithm for automated NMR resonance assignments. Proceedings of the Seventh Annual International Conference on Research in Computational Molecular Biology (RECOMB), pp. 176-187, Berlin, Germany (April, 2003), ACM Press
83. Langmead C., Yan A., Lilien R., Wang L., and Donald B.R. A polynomial-time nuclear vector replacement algorithm for automated NMR resonance assignments. J. Comput. Biol. 11 2-3 (2004) 277-298
84. Langmead C., Yan A., McClung C.R., and Donald B.R. Phase-independent rhythmic analysis of genome-wide expression patterns. J. Comput. Biol. 10 3-4 (2003) 521-536
85. Lasters I., and Desmet J. The fuzzy-end elimination theorem: correctly implementing the side chain placement algorithm based on the dead-end elimination theorem. Protein Eng. 6 (1993) 717-722
86. Li M., Phatnani H.P., Guan Z., Sage H., Greenleaf A.L., and Zhou P. Solution structure of the Set2-Rpb1 interacting domain of human Set2 and its interaction with the hyperphosphorylated C-terminal domain of Rpb1. Proc. Natl. Acad. Sci. USA 102 49 (2005) 17636-17641
87. Lilien R., Farid H., and Donald B.R. Probabilistic disease classification of expression-dependent proteomic data from mass spectrometry of human serum. J. Comput. Biol. 10 6 (2003) 925-946
88. Lilien R., Stevens B., Anderson A., and Donald B.R. A novel ensemble-based scoring and search algorithm for protein redesign, and its application to modify the substrate specificity of the gramicidin synthetase A phenylalanine adenylation enzyme. J. Comput. Biol. 12 6-7 (2005) 740-761
89. Lilien R.H., Bailey-Kellogg C., Anderson A.C., and Donald B.R. A subgroup algorithm to identify cross-rotation peaks consistent with non-crystallographic symmetry. Acta Crystallogr. D Biol. Crystallogr. 60 6 (2004) 1057-1067
90. Lim K., Nadarajah A., Forsythe E.L., and Pusey M.L. Locations of bromide ions in tetragonal lysozyme crystals. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 899-904
91. Lopez-Mendez B., and Guntert P. Automated protein structure determination from NMR spectra. J. Am. Chem. Soc. 128 40 (2006) 13112-13122
92. Losonczi J.A., Andrec M., Fischer M.W., and Prestegard J.H. Order matrix analysis of residual dipolar couplings using singular value decomposition. J. Magn. Reson. 138 2 (1999) 334-342
93. Bryson M., Tian F., Prestegard J.H., and Valafar H. REDCRAFT: a tool for simultaneous characterization of protein backbone structure and motion from RDC data. J. Magn. Reson. 191 2 (2008) 322-334
94. Marin A., Malliavin T.E., Nicolas P., and Delsuc M.A. From NMR chemical shifts to amino acid types: investigation of the predictive power carried by nuclei. J. Biomol. NMR 30 1 (2004) 47-60
95. Meiler J., Blomberg N., Nilges M., and Griesinger C. A new approach for applying residual dipolar couplings as restraints in structure elucidation. J. Biomol. NMR 16 (2000) 245-252
96. Meiler J., Peti W., and Griesinger C. DipoCoup: a versatile program for 3D-structure homology comparison based on residual dipolar couplings and pseudocontact shifts. J. Biomol. NMR 17 (2000) 283-294
97. Meiler J., and Baker D. Rapid protein fold determination using unassigned NMR data. Proc. Natl. Acad. Sci. USA 100 26 (2003) 15404-15409
98. Meiler J., and Baker D. The fumarate sensor DcuS: progress in rapid protein fold elucidation by combining protein structure prediction methods with NMR spectroscopy. J. Magn. Reson. 173 2 (2005) 310-316
99. Mettu R., Lilien R., and Donald B.R. High-throughput inference of protein-protein interfaces from unassigned NMR data. Bioinformatics 21 Suppl. 1 (2005) i292-i301
100. Mueller G.A., Choy W.Y., Yang D., Forman-Kay J.D., Venters R.A., and Kay L.E. Global folds of proteins with low densities of NOEs using residual dipolar couplings: application to the 370-residue maltodextrin-binding protein. J. Mol. Biol. 300 1 (2000) 197-212
101. 15N chemical shifts. J. Biomol. NMR 26 (2003) 215-240
102. Nilges M. A calculation strategy for the structure determination of symmetric dimers by 1H NMR. Proteins 17 3 (1993) 297-309
103. Nilges M., Macias M., Odonoghue S., and Oschkinat H. Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from β-spectrin. J. Mol. Biol. 269 (1997) 408-422
104. Noonan K., O'Brien D., and Snoeyink J. Probik: protein backbone motion by inverse kinematics. Int. J. Robotics Res. 24 11 (2005) 971-982
105. Vitek O., Bailey-Kellogg C., Craig B., and Vitek J. Inferential backbone assignment for sparse data. J. Biomol. NMR 35 3 (2006) 187-208
106. Oki H., Matsuura Y., Komatsu H., and Chernov A.A. Refined structure of orthorhombic lysozyme crystallized at high temperature: correlation between morphology and intermolecular contacts. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 114
107. Okorokov A.L., Sherman M.B., Plisson C., Grinkevich V., Sigmundsson K., Selivanova G., Milner J., and Orlova E.V. The structure of p53 tumour suppressor protein reveals the basis for its functional plasticity. EMBO J. 25 21 (2006) 5191-5200
108. 13C resonances of proteins. J. Biomol. NMR 2 6 (1992) 655-659
109. O'Neil R., Lilien R., Donald B.R., Stroud R., and Anderson A. The crystal structure of dihydrofolate reductase-thymidylate synthase from Cryptosporidium hominis reveals a novel architecture for the bifunctional enzyme. J. Eukaryot. Microbiol. 50 6 (2003) 555-556
110. O'Neil R., Lilien R., Donald B.R., Stroud R., and Anderson A. Phylogenetic classification of protozoa based on the structure of the linker domain in the bifunctional enzyme, dihydrofolate reductase-thymidylate synthase. J. Biol. Chem. 278 52 (2003) 52980-52987
111. Oxenoid K., and Chou J.J. The structure of phospholamban pentamer reveals a channel-like architecture in membranes. PNAS 102 (2005) 10870-10875
112. Palmer A.G. Probing molecular motion by NMR. Curr. Opin. Struct. Biol. 7 (1997) 732-737
113. Palmer A.G., Williams J., and McDermott A. Nuclear magnetic resonance studies of biopolymer dynamics. J. Phys. Chem. 100 (1996) 13293-13310
114. Pearlman D.A., Case D.A., Caldwell J.W., Ross W.S., Cheatham T.E., DeBolt S., Ferguson D., Seibel G., and Kollman P. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structures and energies of molecules. Comp. Phys. Commun. 91 (1995) 1-41
115. Pierce N., Spriet J., Desmet J., and Mayo S. Conformational splitting: a more powerful criterion for dead-end elimination. J. Comput. Chem. 21 (2000) 999-1009
116. Popov V.M., Chan D.C.M., Fillingham Y.A., Yee W.A., Wright D.L., and Anderson A.C. Analysis of complexes of inhibitors with Cryptosporidium hominis DHFR leads to a new trimethoprim derivative. Bioorg. Med. Chem. Lett. 16 16 (2006) 4366-4370
117. Potluri S., Yan A., Chou J.J., Donald B.R., and Bailey-Kellogg C. Structure determination of symmetric homo-oligomers by a complete search of symmetry configuration space using NMR restraints and van der Waals packing. Proteins: Struct. Funct. Bioinform. 65 1 (2006) 203-219
118. Potluri S., Yan A., Donald B.R., and Bailey-Kellogg C. A complete algorithm to resolve ambiguity for inter-subunit NOE assignment in structure determination of symmetric homo-oligomers. Protein Sci. 16 1 (2006)
119. Prestegard J.H. New techniques in structural NMR - anisotropic interactions. Nat. Struct. Biol. (1998) 517-522
120. Prestegard J.H., Bougault C.M., and Kishore A.I. Residual dipolar couplings in structure determination of biomolecules. Chem. Rev. 104 8 (2004) 3519-3540
121. Qu Y., Guo J.T., Olman V., and Xu Y. Protein fold recognition through application of residual dipolar coupling data. Pac. Symp. Biocomput. (2004) 459-470
122. Bertram R., Quine J.R., Chapman M.S., and Cross T.A. Atomic refinement using orientational restraints from solid-state NMR. J. Magn. Reson. 147 (2000) 9-16
123. Ramage R., Green J., Muir T.W., Ogunjobi O.M., Love S., and Shaw K. Synthetic, structural and biological studies of the ubiquitin system: the total chemical synthesis of ubiquitin. J. Biochem. 299 (1994) 151-158
124. Rieping W., Habeck M., and Nilges M. Inferential structure determination. Science 209 5732 (2005) 303-306
125. Rohl C.A., and Baker D. De Novo determination of protein backbone structure from residual dipolar couplings using Rosetta. J. Am. Chem. Soc. 124 11 (2002) 2723-2729
126. Rohl C.A. Protein structure estimation from minimal restraints using Rosetta. Methods Enzymol. 394 (2005) 244-260
127. Ruan K., and Tolman J.R. Composite alignment media for the measurement of independent sets of NMR residual dipolar couplings. J. Am. Chem. Soc. 127 43 (2005) 15032-15033
128. Bansal S., Miao X., Adams M.W., Prestegard J.H., and Valafar H. Rapid classification of protein structure models using unassigned backbone RDCs and probability density profile analysis (PDPA). J. Magn. Reson. 192 1 (2008) 60-68
129. Rumpel S., Becker S., and Zweckstetter M. High-resolution structure determination of the CylR2 homodimer using paramagnetic relaxation enhancement and structure-based prediction of molecular alignment. J. Biomol. NMR 40 1 (2008) 1-13
130. Saupe A. Recent results in the field of liquid crystals. Angew. Chem. 7 (1968) 97-112
131. J.B. Saxe, Embeddability of weighted graphs in k-space is strongly NP-hard, in: Proceedings of the 17th Allerton Conference on Communications, Control, and Computing, 1979, pp. 480-489.
132. Seavey B.R., Farr E.A., Westler W.M., and Markley J.L. A relational database for sequence-specific protein NMR data. J. Biomol. NMR 1 (1991) 217-236
133. Shuker S.B., Hajduk P.J., Meadows R.P., and Fesik S.W. Discovering high-affinity ligands for proteins: SAR by NMR. Science 274 (1996) 1531-1534
134. R. Singh, B. Berger, ChainTweak: sampling from the neighbourhood of a protein conformation, in: Pacific Symposium on Biocomputing 2005, pp. 54-65.
135. Skrynnikov N.R., and Kay L.E. Assessment of molecular structure using frame-independent orientational restraints derived from residual dipolar couplings. J. Biomol. NMR 18 3 (2000) 239-252
136. Stevens B., Lilien R., Georgiev I., Donald B.R., and Anderson A. Redesigning the PheA domain of gramicidin synthetase leads to a new understanding of the enzyme's mechanism and selectivity. Biochemistry 45 51 (2006) 15495-15504
137. Suhre K., and Sanejouand Y.H. ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res. 32 Web Server issue (2004) 610-614
138. Suhre K., and Sanejouand Y.H. On the potential of normal-mode analysis for solving difficult molecular-replacement problems. Acta Crystallogr. D Biol. Crystallogr. 60 Pt. 4 (2004) 796-799
139. Tian F., Valafar H., and Prestegard J.H. A dipolar coupling based strategy for simultaneous resonance assignment and structure determination of protein backbones. J. Am. Chem. Soc. 123 47 (2001) 11791-11796
140. Tjandra N., and Bax A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278 (1997) 1111-1114
141. Tobi D., and Bahar I. Structural changes involved in protein binding correlate with intrinsic motions of proteins in the unbound state. Proc. Natl. Acad. Sci. USA 102 52 (2005) 18908-18913
142. Tolman J.R., Flanagan J.M., Kennedy M.A., and Prestegard J.H. Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution. Proc. Natl. Acad. Sci. USA 92 (1995) 9279-9283
143. Tugarinov V., Choy W.Y., Orekhov V.Y., and Kay L.E. Solution NMR-derived global fold of a monomeric 82-kDa enzyme. Proc. Natl. Acad. Sci. USA 102 3 (2005) 622-627
144. Tugarinov V., Muhandiram R., Ayed A., and Kay L.E. Four-dimensional NMR spectroscopy of a 723-residue protein: chemical shift assignments and secondary structure of malate synthase g. J. Am. Chem. Soc. 124 34 (2002) 10025-10035
145. Valafar H., and Prestegard J.H. Rapid classification of a protein fold family using a statistical analysis of dipolar couplings. Bioinformatics 19 12 (2003) 1549-1555
146. Vaney M.C., Maignan S., Ries-Kautt M., and Ducruix A. High-resolution structure (1.33 angstrom) of a HEW lysozyme tetragonal crystal grown in the APCF apparatus. Data and structural comparison with a crystal grown under microgravity from SpaceHab-01 mission. Acta Crystallogr. D Biol. Crystallogr. 52 (1996) 505-517
147. Vijay-Kumar S., Bugg C.E., and Cook W.J. Structure of ubiquitin refined at 1.8 Å resolution. J. Mol. Biol. 194 (1987) 531-544
148. Vitek O., Bailey-Kellogg C., Craig B., Kuliniewicz P., and Vitek J. Reconsidering complete search algorithms for protein backbone NMR assignment. Bioinformatics 21 Suppl. 2 (2005) ii230-ii236
149. Vitek O., Vitek J., Craig B., and Bailey-Kellogg C. Model-based assignment and inference of protein backbone Nuclear Magnetic Resonances. Stat. Appl. Genet. Mol. Biol. 3 1 (2004)
150. Wang C.E., Pérez T.L., and Tidor B. AMBIPACK: a systematic algorithm for packing of macromolecular structures with ambiguous distance constraints. Proteins: Struct. Funct. Genet. 32 (1998) 26-42
151. L. Wang, B.R. Donald, Analysis of a systematic search-based algorithm for determining protein backbone structure from a minimal number of residual dipolar couplings, in: Proceedings of the IEEE Computational Systems Bioinformatics Conference (CSB), Stanford, CA, August 2004, pp. 319-330, PMID: 16448025.
152. Wang L., and Donald B.R. Exact solutions for internuclear vectors and backbone dihedral angles from NH residual dipolar couplings in two media, and their application in a systematic search algorithm for determining protein backbone structure. J. Biomol. NMR 29 3 (2004) 223-242
153. L. Wang, B.R. Donald, An efficient and accurate algorithm for assigning nuclear Overhauser effect restraints using a rotamer library ensemble and residual dipolar couplings, in: Proceedings of the IEEE Computational Systems Bioinformatics Conference (CSB), Stanford, CA, August 2005, pp. 189-202, PMID: 16447976.
154. L. Wang, B.R. Donald, A data-driven, systematic search algorithm for structure determination of denatured or disordered proteins, in: Proceedings of the LSS Computational Systems Bioinformatics Conference (CSB), Stanford, CA, August 2006, pp. 68-78, PMID: 17369626.
155. L. Wang, R. Mettu, B.R. Donald, An algebraic geometry approach to protein backbone structure determination from NMR data, in: Proceedings of the IEEE Computational Systems Bioinformatics Conference (CSB),, Stanford, CA, August 2005, pp. 235-246, PMID: 16447981.
156. Wang L., Mettu R., and Donald B.R. A polynomial-time algorithm for de novo protein backbone structure determination from NMR data. J. Comput. Biol. 13 7 (2006) 1276-1288
157. Wang Y.X., Jacob J., Cordier F., Wingfield P., Stahl S.J., Lee-Huang S., Torchia D., Grzesiek S., and Bax A. Measurement of 3hJNC' connectivities across hydrogen bonds in a 30 kDa protein. J. Biomol. NMR 14 2 (1999) 181-184
158. 13C′ dipolar couplings in a perdeuterated 30 kDa protein dissolved in a dilute liquid crystalline phase. J. Am. Chem. Soc. 120 29 (1998) 7385-7386
159. Wedemeyer W.J., Rohl C.A., and Scheraga H.A. Exact solutions for chemical bond orientations from residual dipolar couplings. J. Biomol. NMR 22 (2002) 137-151
160. Weidong H., and Wang L. Residual dipolar couplings: measurements and applications to biomolecular studies. Annu. Rep. NMR Spectrosc. 58 (2006) 231-303
161. Wells S., Menor S., Hespenheide B., and Thorpe M.F. Constrained geometric simulation of diffusive motion in proteins. Phys. Biol. 2 4 (2005) 127-136
162. Wikipedia, NP-completeness, Wikipedia, the Free Encyclopedia, September 2008. Available online: http://en.wikipedia.org/wiki/NP-complete.
163. 13C chemical shift data. J. Biomol. NMR 4 (1994) 171-180
164. Wishart D.S., Sykes B.D., and Richards F.M. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222 2 (1991) 311-333
165. 13C chemical shift data. Biochemistry 31 6 (1992) 1647-1651
166. Wuthrich K. Protein recognition by NMR. Nat. Struct. Biol. 7 3 (2000) 188-189
167. Choy W.Y., Tollinger M., Mueller G.A., and Kay L.E. Direct structure refinement of high molecular weight proteins against residual dipolar couplings and carbonyl chemical shift changes upon alignment: an application to maltose binding protein. J. Biomol. NMR 21 1 (2001) 31-40
168. Wang X., Bansal S., Jiang M., and Prestegard J.H. RDC-assisted modeling of symmetric protein homo-oligomers. Protein Sci. 17 5 (2008) 899-907
169. 13C′ chemical shifts in proteins using a density functional database. J. Biomol. NMR 21 (2001) 321-333
170. Xu Y., Zheng Y., Fan J.S., and Yang D. A new strategy for structure determination of large proteins in solution without deuteration. Nat. Methods 3 11 (2006) 931-937
171. Yan A., Langmead C., and Donald B.R. A probability-based similarity measure for Saupe alignment tensors with applications to residual dipolar couplings in NMR structural biology. Int. J. Robotics Res. 24 2-3 (2005) 165-182 (special issue on Robotics Techniques Applied to Computational Biology)
172. Zamoon J., Mascioni A., Thomas D.D., and Veglia G. NMR solution structure and topological orientation of monomeric phospholamban in dodecylphosphocholine micelles. Biophys. J. 85 4 (2003) 2589-2598
173. Zavodszky M.I., Lei M., Thorpe M.F., Day A.R., and Kuhn L.A. Modeling correlated main-chain motions in proteins for flexible molecular recognition. Proteins 57 2 (2004) 243-261
174. J. Zeng, C. Tripathy, P. Zhou, B.R. Donald, A Hausdorff-based NOE assignment algorithm using protein backbone determined from residual dipolar couplings and rotamer patterns, in: Proceedings of the LSS Computational Systems Bioinformatics Conference (CSB), Stanford, CA, Aug 2008, pp. 169-181, PMID: 19122773.
175. Zweckstetter M. Determination of molecular alignment tensors without backbone resonance assignment: aid to rapid analysis of protein-protein interactions. J. Biomol. NMR 27 1 (2003) 41-56
176. Zweckstetter M., and Bax A. Single-step determination of protein substructures using dipolar couplings: aid to structural genomics. J. Am. Chem. Soc. 123 38 (2001) 9490-9491