Protein loop closure using orientational restraints from NMR data

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 2, 2012, Pages 433-453

  Tripathy, Chittaranjan ^a   Zeng, Jianyang ^a   Zhou, Pei ^b   Donald, Bruce Randall ^a,b  

^a Duke University   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Algorithms; Inverse kinematics; Loop closure; Nuclear magnetic resonance; Protein loops; Residual dipolar couplings; Sphero conic; Structural biology

Indexed keywords

HIGH MOBILITY GROUP B3 PROTEIN; UBIQUITIN; BACTERIAL PROTEIN; CARRIER PROTEIN; DINI PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; IMMUNOGLOBULIN G-BINDING PROTEIN, STREPTOCOCCUS SUIS TYPE 2; PROTEIN;

ACCURACY; ALGORITHM; ARTICLE; HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; NUCLEAR MAGNETIC RESONANCE; PROTEIN DATABASE;

ALGORITHMS; BACTERIAL PROTEINS; CARRIER PROTEINS; DATABASES, PROTEIN; ESCHERICHIA COLI PROTEINS; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS; UBIQUITIN;

EID: 84855701877     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23207     Document Type: Article

References (123)

1. Pesce S, Benezara R. The loop region of the helix-loop-helix protein Id1 is critical for its dominant negative activity. Mol Cell Biol 1993;13:7874-7880.
2. Buchbinder JL, Fletterick RJ. Role of the active site gate of glycogen phosphorylase in allosteric inhibition and substrate binding.J Biol Chem 1996;271:22305-22309.
3. Greenwald J, Le V, Butler SL, Bushman FD, Choe S. The mobility of an HIV-1 integrase active site loop is correlated with catalytic activity. Biochemistry 1999;38:8892-8898.
4. 2 receptor lines the binding-site crevice. Proc Natl Acad Sci USA 2004;101:440-445.
5. Gorczynski MJ, Grembecka J, Zhou Y, Kong Y, Roudaia L, Douvas MG, Newman M, Bielnicka I, Baber G, Corpora T, Shi J, Sridharan M, Lilien R, Donald BR, Speck NA, Brown ML, Bushweller JH. Allosteric inhibition of the protein-protein interaction between the leukemia-associated proteins Runx1 and CBFβ. Chemistry & Biology 2007;14:1186-1197.
6. Velloso LM, Bhaskaran SS, Schuch R, Fischetti VA, Stebbins CE.A structural basis for the allosteric regulation of non-hydrolysing UDP-GlcNAc 2-epimerases. EMBO Rep 2008;9:199-205.
7. Santiago C, Celma ML, Stehle T, Casasnovas JM. Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat Struct Mol Biol 2010;17:124-129.
8. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourn PE. The protein data bank. Nucleic Acids Res 2000;28:235-242.
9. Gō N, Scheraga HA. Ring closure and local conformational deformations of chain molecules. Macromolecules 1970;3:178-187.
10. Xiang Z, Soto CS, Honig B. Evaluating conformational free energies: the colony energy and its application to the problem of loop prediction. Proc Natl Acad Sci USA 2002;99:7432-7437.
11. Wang C, Bradley P, Baker D. Protein-protein docking with backbone flexibility.J Mol Biol 2007;373:503-519.
12. Hu X, Wang H, Ke H, Kuhlman B. High-resolution design of a protein loop. Proc Natl Acad Sci USA 2007;104:17668-17673.
13. Mandell DJ, Coutsias EA, Kortemme T. Sub-angstrom accuracy in protein loop reconstruction by robotics-inspired conformational sampling. Nat Methods 2009;6:551-552.
14. Rufino SD, Donate LE, Canard LHJ, Blundell TL. Predicting the conformational class of short and medium size loops connecting regular secondary structures: application to comparative modelling.J Mol Biol 1997;267:352-367.
15. van Vlijmen HWT, Karplus M. PDB-based protein loop prediction: parameters for selection and methods for optimization.J Mol Biol 1997;267:975-1001.
16. Tosatto SCE, Eckart Bindewald JH, Männer R.A divide and conquer approach to fast loop modeling. Protein Eng 2002;15:279-286.
17. Du P, Andrec M, Levy RM. Have we seen all structures corresponding to short protein fragments in the protein data bank? An update. Protein Eng 2003;16:407-414.
18. Soto CS, Fasnacht M, Zhu J, Forrest L, Honig B. Loop modeling: sampling, filtering, and scoring. Proteins: Struct Funct Bioinform 2008;70:834-843.
19. Fiser A, Do RKG, Sali A. Modeling of loops in protein structures. Protein Sci 2000;9:1753-1773.
20. Shenkin PS, Yarmush DL, Fine RM, Wang H, Levinthal C. Predicting antobody hypervariable loop conformation. I. Ensembles of random conformations for ringlike structures. Biopolymers 1987; 26:2053-2085.
21. Koehl P, Delarue M.A self consistent mean field approach to simultaneous gap closure and side-chain positioning in homology modelling. Nat Struct Biol 1995;2:163-170.
22. Wang L-CT, Chen CC.A combined optimization method for solving the inverse kinematics problem of mechanical manipulators. IEEE Trans Rob Autom 1991;7:489-499.
23. Cortés J, Siméon T, Remaud-Siméon M, Tran V. Geometric algorithms for the conformational analysis of long protein loops.J Comput Chem 2004;25:956-967.
24. Milgram RJ, Liu G, Latombe J-C. On the structure of the inverse kinematics map of a fragment of protein backbone.J Comput Chem 2008;29:50-68.
25. Wedemeyer WJ, Scheraga HA. Exact analytical loop closure in proteins using polynomial equations.J Comput Chem 1999;20:819-844.
26. Coutsias EA, Seok C, Jacobson MP, Dill KA.A kinematic view of loop closure.J Comput Chem 2004;25:510-528.
27. Coutsias EA, Seok C, Wester MJ, Dill KA. Resultants and loop closure. Int J Quantum Chem 2006;106:176-189.
28. Canutescu AA, Dunbrack RL, Jr. Cyclic coordinate descent: a robotics algorithm for protein loop closure. Protein Sci 2003; 12:963-972.
29. Al-Nasr K, He J. An effective convergence independent loop closure method using forward-backward cyclic coordinate descent. Int J Data Min Bioin 2009;3:346-361.
30. Yao P, Dhanik A, Marz N, Propper R, Kou C, Liu G, van den Bedem H, Latombe J-C, Halperin-Landsberg I, Altman RB. Efficient algorithms to explore conformation spaces of flexible protein loops. IEEE/ACM Trans Comput Bioinform 2008;5:534-545.
31. Kolodny R, Guibas L, Levitt M, Koehl P. Inverse kinematics in biology: the protein loop closure problem. Int J Rob Res 2005; 24:151-163.
32. Lee J, Lee D, Park H, Coutsias EA, Seok C. Protein loop modeling by using fragment assembly and analytical loop closure. Proteins Struct Funct Bioinform 2010;78:3428-3436.
33. i dimer database. Protein Sci 1995; 4:1412-1420.
34. Janardhan A, Vajda S. Selecting near-native conformations in homology modeling: the role of molecular mechanics and solvation terms. Protein Sci 1998;7:1772-1780.
35. Chothia C, Lesk AM. Canonical structures for the hypervariable regions of immunoglobulins.J Mol Biol 1987;196:901-917.
36. Martin ACR, Thornton JM. Structural families in loops of homologous proteins: automatic classification, modeling, and application to antibodies.J Mol Biol 1996;263:800-815.
37. Fine RM, Wang H, Shenkin PS, Yarmush DL, Levinthal C. Predicting antibody hypervariable loop conformations. II: Minimization and molecular dynamics studies of MCPC603 from many randomly generated loop conformations. Proteins Struct Funct Bioinform 1986;1:342-362.
38. Bruccoleri RE, Karplus M. Conformational sampling using high temperature molecular dynamics. Macromolecules 1990;29:1847-1862.
39. Cheng X, Wang H, Grant B, Sine SM, McCammon JA. Targeted molecular dynamics study of C-loop closure and channel gating in nicotinic receptors. PLoS Comput Biol 2006;2:e134.
40. Collura V, Higo J, Garnier J. Modeling of protein loops by simulated annealing. Protein Sci 1993;2:1502-1510.
41. Rosenbach D, Rosenfeld R. Simultaneous modeling of multiple loops in proteins. Protein Sci 1995;4:496-505.
42. Jiang H, Blouin C. Ab initio construction of all-atom loop conformations.J Mol Model 2006;12:221-228.
43. Donald BR. Algorithms in structural molecular biology. Cambridge, MA:The MIT Press;2011.
44. Manocha D, Canny JF. Efficient inverse kinematics for general 6r manipulators. IEEE Trans Rob Autom 1994;10:648-657.
45. Chirikjian GS. General methods for computing hyper-redundant manipulator inverse kinematics. In: Proceedings of the 1993 IEEE/RSJ international conference on intelligent robots and systems, Yokohama, Japan, vol. 2, 1993. pp 1067-1073.
46. van den Bedem H, Lotan I, Latombe J-C, Deacona AM. Real-space protein-model completion: an inverse-kinematics approach. Acta Crystallogr D Biol Crystallogr 2005;61:2-13.
47. Shehu A, Clementi C, Kavraki LE. Modeling protein conformational ensembles: from missing loops to equilibrium fluctuations. Proteins Struct Funct Bioinform 2006;65:164-179.
48. Saxe JB. Embeddability of weighted graphs in k-space is strongly NP-hard. In: Proceedings of the 17th Allerton conference on communications, control, and computing, Monticello, IL, USA.1979, pp 480-489.
49. Clore GM, Gronenborn AM, Tjandra N. Direct structure refinement against residual dipolar couplings in the presence of rhombicity of unknown magnitude.J Magn Reson 1998;131:159-162.
50. Güntert P. Automated NMR protein structure determination. Prog Nucl Magn Reson Spectrosc 2003;43:105-125.
51. Mumenthaler C, Güntert P, Braun W, Wüthrich K. Automated combined assignment of NOESY spectra and three-dimensional protein structure determination.J Biomol NMR 1997;10:351-362.
52. Kuszewski J, Schwieters CD, Garrett DS, Byrd RA, Tjandra N, Clore GM. Completely automated, highly error-tolerant macromolecular structure determination from multidimensional nuclear overhauser enhancement spectra and chemical shift assignments.J Am Chem Soc 2004;126:6258-6273.
53. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM. The Xplor-NIH NMR molecular structure determination package.J Magn Reson 2003;160:65-73.
54. Brünger AT.X-PLOR, version 3.1. A system for X-ray crystallography and NMR. New Haven, CT:Yale University Press;1992.
55. Delaglio F, Kontaxis G, Bax A. Protein structure determination using molecular fragment replacement and NMR dipolar couplings.J Am Chem Soc 2000;122:2142-2143.
56. Rohl CA, Baker D. De novo determination of protein backbone structure from residual dipolar couplings using rosetta.J Am Chem Soc 2002;124:2723-2729.
57. Bouvignies G, Meier S, Grzesiek S, Blackledge M. Ultrahigh-resolution backbone structure of perdeuterated protein GB1 using residual dipolar couplings from two alignment media. Angew Chem Int Ed Engl 2006;118:8346-8349.
58. Tian F, Valafar H, Prestegard JH.A dipolar coupling based strategyfor simultaneous resonance assignment and structure determination of protein backbones.J Am Chem Soc 2001;123: 11791-11796.
59. Giesen AW, Homans SW, Brown JM. Determination of protein global folds using backbone residual dipolar coupling and long-range NOE restraints.J Biomol NMR 2003;25:63-71.
60. Andrec M, Du P, Levy RM. Protein backbone structure determination using only residual dipolar couplings from one ordering medium.J Biomol NMR 2004;21:335-347.
61. Wang L, Donald BR. 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 2004; 29:223-242.
62. Wang L, Mettu RR, Donald BR.A polynomial-time algorithm for de novo protein backbone structure determination from NMR data.J Comput Biol 2006;13:1276-1288.
63. Donald BR, Martin J. Automated NMR assignment and protein structure determination using sparse dipolar coupling constraints. Prog Nucl Magn Reson Spectrosc 2009;55:101-127.
64. Yershova A, Tripathy C, Zhou P, Donald BR. Algorithms and analytic solutions using sparse residual dipolar couplings for high-resolution automated protein backbone structure determination by NMR. Presented at the The Ninth International Workshop on the Algorithmic Foundations of Robotics, Singapore.2010. pp 355-372.
65. Frey KM, Georgiev I, Donald BR, Anderson AC. Predicting resistance mutations using protein design algorithms. Proc Natl Acad Sci USA 2010;107:13707-13712.
66. Chen C-Y, Georgiev I, Anderson AC, Donald BR. Computational structure-based redesign of enzyme activity. Proc Natl Acad Sci USA 2009;106:3764-3769.
67. Georgiev I, Lilien RH, Donald BR. 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 2008;29:1527-1542.
68. Lilien RH, Stevens BW, Anderson AC, Donald BR.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 2005;12:740-761.
69. Martin JW, Yan AK, Bailey-Kellogg C, Zhou P, Donald BR.A graphical method for analyzing distance restraints using residual dipolar couplings for structure determination of symmetric protein homo-oligomers. Protein Sci 2011;20:970-985.
70. Zeng J, Zhou P, Donald BR. Protein side-chain resonance assignment and NOE assignment using RDC-defined backbones without TOCSY data.J Biomol NMR 2011;50:371-395.
71. Zeng J, Boyles J, Tripathy C, Wang L, Yan A, Zhou P, Donald BR. High-resolution protein structure determination starting with a global fold calculated from exact solutions to the RDC equations. JBiomol NMR 2009;45:265-281.
72. Wang L, Donald BR. An efficient and accurate algorithm for assigning nuclear overhauser effect restraints using a rotamer library ensemble and residual dipolar couplings. Presented at the IEEE Computational Systems Bioinformatics Conference, Stanford, CA.2005. pp. 189-202.
73. Zeng J, Tripathy C, Zhou P, Donald BR. A Hausdorff-based NOE assignment algorithm using protein backbone determined from residual dipolar couplings and rotamer Patterns. In Proceedings of the 7th annual international conference on computational systems bioinformatics, Stanford CA, USA2008. pp. 169-181.
74. Higman VA, Boyd J, Smith LJ, Redfield C. Residual dipolar couplings: are multiple independent alignments always possible?J Biomol NMR 2011;49:53-60.
75. Shen Y, Lange O, Delaglio F, Rossi P, Aramini JM, Liu G, Eletsky A, Wu Y, Singarapu KK, Lemak A, Ignatchenko A, Arrowsmith CH, Szyperski T, Montelione GT, Baker D, Bax A. Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci USA 2008;105:4685-4690.
76. Cornilescu G, Delaglio F, Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology.J Biomol NMR 1999;13:289-302.
77. Shen Y, Delaglio F, Cornilescu G, Bax A. TALOS+: A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts.J Biomol NMR 2009;44:213-223.
78. Liu P, Zhu F, Rassokhin DN, Agrafiotis DK.A self-organizing algorithm for modeling protein loops. PLoS Comput Biol 2009; 5:e1000478, 08.
79. Baker D, Sali A. Protein structure prediction and structural genomics. Science 2001;294:93-96.
80. Langmead CJ, Donald BR. 3D structural homology detection via unassigned residual dipolar couplings. In: Procedings of 2003 IEEE computational systems bioinformatics conference, Stanford, CA, USA2003. pp 209-217.
81. Langmead CJ, Donald BR. High-throughput 3D structural homology detection via NMR resonance assignment. In Procedings of 2004 IEEE computational systems bioinformatics conference, Stanford, CA, USA2004. pp 278-289.
82. Losonczi JA, Andrec M, Fischer MWF, Prestegard JH. Order matrix analysis of residual dipolar couplings using singular value decomposition.J Magn Reson 1999;138:334-342.
83. Saupe A. Recent results in the field of liquid crystals. Angew Chem 1968;7:97-112.
84. Tjandra N, Bax A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 1997;278:1111-1114.
85. Tolman JR, Flanagan JM, Kennedy MA, Prestegard JH. Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution. Proc Natl Acad Sci USA 1995;92:9279-9283.
86. Prestegard JH, Bougault CM, Kishore AI. Residual dipolar couplings in structure determination of biomolecules. Chem Rev 2004;104:3519-3540.
87. Ramirez BE, Bax A. Modulation of the alignment tensor of macromolecules dissolved in a dilute liquid crystalline medium.J Am Chem Soc 1998;120:9106-9107.
88. Casey J. On cyclides and sphero-quartics. Proc R Soc Lond 1871;XIX:495-497.
89. Salmon G.A treatise on the analytic geometry of three dimensions, 5th ed. London:Longmans, Green and Company;1912.
90. Salmon G.A treatise on conic sections, 6th ed. New York:Chelsea Publishing Company;1960.
91. Yoshikawa T. Foundations of robotics: analysis and control. Cambridge, MA:The MIT Press;1990.
92. Chirikjian GS, Burdick JW.A hyper-redundant manipulator. IEEE Rob Autom Mag 1994;1(4):22-29.
93. Lovell SC, Davis IW, Arendall WB, III, de Bakker PIW, Word JM, Prisant MG, Richardson JS, Richardson DC. Structure Validation by Cα Geometry: φ{symbol}, ψ, and Cβ deviation. Proteins: Struct Funct Genet 2003;50:437-450.
94. Word JM, Lovell SC, LaBean TH, Taylor HC, Zalis ME, Presley BK, Richardson JS, Richardson DC. Visualizing and quantifying molecular goodness-of-fit: small-probe contact dots with explicit hydrogen atoms.J Mol Biol 1999;285:1711-1733.
95. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes.J Biomol NMR 1995;6:277-293.
96. Johnson BA, Blevins RA. NMRView: a computer program for the visualization and analysis of NMR data.J Biomol NMR 1994; 4:603-614.
97. Bartels C, Xia T, Billeter M, Güntert P, Wüthrich K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules.J Biomol NMR 1995;6:1-10.
98. Coggins BE, Zhou P. PACES: protein sequential assignment by computer-assisted exhaustive search.J Biomol NMR 2003;26:93-111.
99. Ottiger M, Delaglio F, Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra.J Mag Reson 1998;131:373-378.
100. α spins.J Magn Reson 2006;180:127-136.
101. 2H)-labeled proteins.J Biomol NMR 2000;17:43-54.
102. Cornilescu G, Marquardt JL, Ottiger M, Bax A. Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase.J Am Chem Soc 1998;120:6836-6837.
103. Ramirez BE, Voloshin ON, Camerini-Otero RD, Bax A. Solution structure of DinI provides insight into its mode of RecA inactivation. Protein Sci 2000;9:2161-2169.
104. Ulmer TS, Ramirez BE, Delaglio F, Bax A. Evaluation of backbone proton positions and dynamics in a small protein by liquid crystal NMR spectroscopy.J Am Chem Soc 2003;125:9179-9191.
105. Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, Lin J, Livny M, Mading S, Maziuk D, Miller Z, Nakatani E, Schulte CF, Tolmie DE, Wenger RK, Yao H, Markley JL. BioMagResBank. Nucleic Acids Res 2008;36(Database issue):D402-D408.
106. Shen Y, Vernon R, Baker D, Bax A. De novo protein structure generation from incomplete chemical shift assignments.J Biomol NMR 2007;43:63-78.
107. Raman S, Lange OF, Rossi P, Tyka M, Wang X, Aramini J, Liu G, Ramelot TA, Eletsky A, Szyperski T, Kennedy MA, Prestegard J, Montelione GT, Baker D. NMR structure determination for larger proteins using backbone-only data. Science 2010;327:1014-1018.
108. Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, Jacak R, Kaufman K, Renfrew PD, Smith CA, Sheffler W, Davis IW, Cooper S, Treuille A, Mandell DJ, Richter F, Ban YEA, Fleishman SJ, Corn JE, Kim DE, Lyskov S, Berrondo M, Mentzer S, Popovic Z, Havranek JJ, Karanicolas J, Das R, Meiler J, Kortemme T, Gray JJ, Kuhlman B, Baker D, Bradley P. ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol 2011;487:545-574.
109. Han B, Liu Y, Ginzinger S, Wishart D. SHIFTX2: significantly improved protein chemical shift prediction.J Biomol NMR 2011; 50:43-57.
110. Schueler-Furman O, Wang C, Bradley P, Misura K, Baker D. Progress in modeling of protein structures and interactions. Science 2005;310:638-642.
111. Zweckstetter M, Bax A. Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR.J Am Chem Soc 2000;122:3791-3792.
112. Zweckstetter M. NMR: prediction of molecular alignment from structure using the PALES software. Nat Protoc 2008;3:679-690.
113. Sellers BD, Zhu K, Zhao S, Friesner RA, Jacobson MP. Toward better refinement of comparative models: predicting loops in inexact environments. Proteins Struct Funct Bioinform 2008;72: 959-971.
114. Tolman JR, Flanagan JM, Kennedy MA, Prestegard JH. NMR evidence for slow collective motions in cyanometmyoglobin. Nat Struct Biol 1997;4:292-297.
115. Markwick PRL, Bouvignies G, Salmon L, McCammon JA, Nilges M, Blackledge M. Toward a unified representation of protein structural dynamics in solution.J Am Chem Soc 2009;131:16968-16975.
116. Salmon L, Bouvignies G, Markwick P, Lakomek N, Showalter S, Li D-W, Walter K, Griesinger C, Brüschweiler R, Blackledge M. Protein conformational flexibility from structure-free analysis of NMR dipolar couplings: quantitative and absolute determination of backbone motion in ubiquitin. Angew Chem Int Ed Engl 2009; 48:4154-4157.
117. Lange OF, Lakomek N-A, Fares C, Schroder GF, Walter KFA, Becker S, Meiler J, Grubmuller H, Griesinger C, de Groot BL. Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 2008;320:1471-1475.
118. Wlodarski T, Zagrovic B. Conformational selection and induced fit mechanism underlie specificity in noncovalent interactions with ubiquitin. Proc Natl Acad Sci USA 2009;106:19346-19351.
119. Long D, Brüschweiler R. In silico elucidation of the recognition dynamics of ubiquitin. PLoS Comput Biol 2011;7:e1002035.
120. Tolman JR, Ruan K. NMR residual dipolar couplings as probes of biomolecular dynamics. Chem Rev 2006;106:1720-1736.
121. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010;66:12-21.
122. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, III, Snoeyink J, Richardson JS, Richardson DC. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 2007:35(Web Server issue);W375-W383.
123. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Laura WM, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010;66:12-21.