Quality assessment of protein NMR structures

Current Opinion in Structural Biology

Volumn 23, Issue 5, 2013, Pages 715-724

  Rosato, Antonio ^a   Tejero, Roberto ^b   Montelione, Gaetano T ^c,d  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF VALENCIA   (Spain)

^c RUTGERS UNIVERSITY   (United States)

^d RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL PARAMETERS; ATOMIC PACKING; DIHEDRAL ANGLE DISTRIBUTION; ENERGY REFINEMENT; FREE R FACTOR; HUMAN; HYDROGEN BOND; KNOWLEDGE BASED MEASURE; MEASUREMENT ACCURACY; METRIC SYSTEM; MODEL VERSUS DATA METRIC; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE RESTRAINT ANALYSIS; NUCLEAR OVERHAUSER EFFECT; ONLINE SYSTEM; PARAMAGNETIC RESONANCE ENHANCEMENT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DATABASE; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; QUALITY CONTROL; RESIDUAL DIPOLAR COUPLING; REVIEW; SCALAR COUPLING; SMALL ANGLE SCATTERING; STATISTICAL ANALYSIS; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

DATABASES, PROTEIN; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS; REPRODUCIBILITY OF RESULTS; RESEARCH;

EID: 84885857075     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.08.005     Document Type: Review

References (76)

1. Rosato A., Aramini J.M., Arrowsmith C., Bagaria A., Baker D., Cavalli A., Doreleijers J.F., Eletsky A., Giachetti A., Guerry P., Gutmanas A., et al. Blind testing of routine, fully automated determination of protein structures from NMR data. Structure 2012, 20:227-236.
2. Rosato A., Bagaria A., Baker D., Bardiaux B., Cavalli A., Doreleijers J.F., Giachetti A., Guerry P., Guntert P., Herrmann T., Huang Y.J., et al. CASD-NMR: critical assessment of automated structure determination by NMR. Nat Methods 2009, 6:625-626.
3. Mao B., Guan R., Montelione G.T. Improved technologies now routinely provide protein NMR structures useful for molecular replacement. Structure 2011, 19:757-766.
4. Lange O.F., Rossi P., Sgourakis N.G., Song Y., Lee H.W., Aramini J.M., Ertekin A., Xiao R., Acton T.B., Montelione G.T., Baker D. Determination of solution structures of proteins up to 40kDa using cs-rosetta with sparse NMR data from deuterated samples. Proc Natl Acad Sci USA 2012, 109:10873-10878.
5. Raman S., Lange O.F., Rossi P., Tyka M., Wang X., Aramini J., Liu G., Ramelot T.A., Eletsky A., Szyperski T., Kennedy M.A., et al. NMR structure determination for larger proteins using backbone-only data. Science 2010, 327:1014-1018.
6. Hiller S., Wagner G. The role of solution NMR in the structure determinations of vdac-1 and other membrane proteins. Curr Opin Struct Biol 2009, 19:396-401.
7. Hiller S., Garces R.G., Malia T.J., Orekhov V.Y., Colombini M., Wagner G. Solution structure of the integral human membrane protein vdac-1 in detergent micelles. Science 2008, 321:1206-1210.
8. Read R.J., Adams P.D., Arendall W.B., Brunger A.T., Emsley P., Joosten R.P., Kleywegt G.J., Krissinel E.B., Lutteke T., Otwinowski Z., Perrakis A., et al. A new generation of crystallographic validation tools for the protein data bank. Structure 2011, 19:1395-1412.
9. Montelione G.T., Nilges M., Bax A., Güntert P., Herrmann T., Richardson J.S., Schwieters C.D., Vranken W.F., Vuister G.W., Wishart D.S., Berman H.M., et al. Recommendations of the wwpdb NMR validation task force. Structure 2013, 21:1563-1570.
10. Bhattacharya A., Tejero R., Montelione G.T. Evaluating protein structures determined by structural genomics consortia. Proteins 2007, 66:778-795.
11. Chen V.B., Arendall W.B., Headd J.J., Keedy D.A., Immormino R.M., Kapral G.J., Murray L.W., Richardson J.S., Richardson D.C. Molprobity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. Sect. D, Biol. Crystallogr. 2010, 66(Pt 1):12-21.
12. Sippl M.J. Recognition of errors in three-dimensional structures of proteins. Proteins 1993, 17:355-362.
13. Luthy R., Bowie J.U., Eisenberg D. Assessment of protein models with three-dimensional profiles. Nature 1992, 356:83-85.
14. Bhattacharya A., Wunderlich Z., Monleon D., Tejero R., Montelione G.T. Assessing model accuracy using the homology modeling automatically software. Proteins 2008, 70:105-118.
15. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., Thornton J.M. Aqua and procheck-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 1996, 8:477-486.
16. Arendall W.B., Tempel W., Richardson J.S., Zhou W., Wang S., Davis I.W., Liu Z.J., Rose J.P., Carson W.M., Luo M., Richardson D.C. A test of enhancing model accuracy in high-throughput crystallography. J Struct Funct Genomics 2005, 6:1-11.
17. Sheffler W., Baker D. Rosettaholes: rapid assessment of protein core packing for structure prediction, refinement, design, and validation. Protein Sci Publ Protein Soc 2009, 18:229-239.
18. van der Schot G., Zhang Z., Vernon R., Shen Y., Vranken W.F., Baker D., Bonvin A.M., Lange O.F. Improving 3D structure prediction from chemical shift data. J Biomol NMR 2013, 57:27-35.
19. Shen Y., Lange O., Delaglio F., Rossi P., Aramini J.M., Liu G., Eletsky A., Wu Y., Singarapu K.K., Lemak A., Ignatchenko A., et al. Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci U S A 2008, 105:4685-4690.
20. Tejero R., Snyder D., Mao B., Aramini J.M., Montelione G.T. PDBStat: a universal restraint converter and restraint analysis software package for protein NMR. J Biomol NMR 2013, 56:337-351.
21. Ramelot T.A., Raman S., Kuzin A.P., Xiao R., Ma L.C., Acton T.B., Hunt J.F., Montelione G.T., Baker D., Kennedy M.A. Improving NMR protein structure quality by rosetta refinement: a molecular replacement study. Proteins 2009, 75:147-167.
22. Bertini I., Case D.A., Ferella L., Giachetti A., Rosato A. A grid-enabled web portal for NMR structure refinement with amber. Bioinformatics 2011, 27:2384-2390.
23. Nederveen A.J., Doreleijers J.F., Vranken W., Miller Z., Spronk C.A., Nabuurs S.B., Guntert P., Livny M., Markley J.L., Nilges M., Ulrich E.L., et al. Recoord: a recalculated coordinate database of 500+ proteins from the pdb using restraints from the biomagresbank. Proteins 2005, 59:662-672.
24. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., Llinas M., Ulrich E.L., Markley J.L., Ionides J., Laue E.D. The ccpn data model for NMR spectroscopy: development of a software pipeline. Proteins 2005, 59:687-696.
25. Doreleijers J.F., Raves M.L., Rullmann T., Kaptein R. Completeness of nodes in protein structure: a statistical analysis of NMR. J Biomol NMR 1999, 14:123-132.
26. Borgias B.A., James T.L. Two-dimensional nuclear overhauser effect: complete relaxation matrix analysis. Methods Enzymol 1989, 176:169-183.
27. Gronwald W., Kirchhofer R., Gorler A., Kremer W., Ganslmeier B., Neidig K.P., Kalbitzer H.R. Rfac, a program for automated NMR r-factor estimation. J Biomol NMR 2000, 17:137-151.
28. Zhu L., Dyson H.J., Wright P.E. A noesy-hsqc simulation program, spirit. J Biomol NMR 1998, 11:17-29.
29. Huang Y.J., Powers R., Montelione G.T. Protein NMR recall, precision, and F measure scores (RPF scores): structure quality assessment measures based on information retrieval statistics. J Am Chem Soc 2005, 127:1665-1674.
30. Huang Y.J., Rosato A., Singh G., Montelione G.T. Rpf: a quality assessment tool for protein NMR structures. Nucleic Acids Res 2012, 40(Web Server issue):W542-W546.
31. Bagaria A., Jaravine V., Huang Y.J., Montelione G.T., Guntert P. Protein structure validation by generalized linear model root-mean-square deviation prediction. Protein Sci Publ Protein Soc 2012, 21:229-238.
32. Clore G.M., Robien M.A., Gronenborn A.M. Exploring the limits of precision and accuracy of protein structures determined by nuclear magnetic resonance spectroscopy. J Mol Biol 1993, 231:82-102.
33. Valafar H., Prestegard J.H. Redcat: a residual dipolar coupling analysis tool. J Magn Reson 2004, 167:228-241.
34. Bryson M., Tian F., Prestegard J.H., Valafar H. Redcraft: a tool for simultaneous characterization of protein backbone structure and motion from rdc data. J Magn Reson 2008, 191:322-334.
35. Cornilescu G., Marquardt J.L., 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.
36. Grishaev A., Wu J., Trewhella J., Bax A. Refinement of multidomain protein structures by combination of solution small-angle X-ray scattering and NMR data. J Am Chem Soc 2005, 127:16621-16628.
37. Clore G.M., Schwieters C.D. 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 2004, 126:2923-2938.
38. 1H couplings. Chembiochem 2013, 14:684-688.
39. Brunger A.T., Clore G.M., Gronenborn A.M., Saffrich R., Nilges M. Assessing the quality of solution nuclear magnetic resonance structures by complete cross-validation. Science 1993, 261:328-331.
40. Willard L., Ranjan A., Zhang H., Monzavi H., Boyko R.F., Sykes B.D., Wishart D.S. Vadar: a web server for quantitative evaluation of protein structure quality. Nucleic Acids Res 2003, 31:3316-3319.
41. Berjanskii M., Tang P., Liang J., Cruz J.A., Zhou J., Zhou Y., Bassett E., MacDonell C., Lu P., Lin G., Wishart D.S. GeNMR: a web server for rapid NMR-based protein structure determination. Nucleic Acids Res 2009, 37(Web Server issue):W670-W677.
42. Berjanskii M., Liang Y., Zhou J., Tang P., Stothard P., Zhou Y., Cruz J., MacDonell C., Lin G., Lu P., Wishart D.S. Process: a protein structure evaluation suite and server. Nucleic Acids Res 2010, 38(Web Server issue):W633-W640.
43. Berjanskii M., Zhou J., Liang Y., Lin G., Wishart D.S. Resolution-by-proxy: a simple measure for assessing and comparing the overall quality of NMR protein structures. J Biomol NMR 2012, 53:167-180.
44. Vila J.A., Aramini J.M., Rossi P., Kuzin A., Su M., Seetharaman J., Xiao R., Tong L., Montelione G.T., Scheraga H.A. Quantum chemical 13c(alpha) chemical shift calculations for protein NMR structure determination, refinement, and validation. Proc Natl Acad Sci USA 2008, 105:14389-14394.
45. Martin O.A., Villegas M.E., Vila J.A., Scheraga H.A. Analysis of 13calpha and 13cbeta chemical shifts of cysteine and cystine residues in proteins: a quantum chemical approach. J Biomol NMR 2010, 46:217-225.
46. Vila J.A., Serrano P., Wuthrich K., Scheraga H.A. Sequential nearest-neighbor effects on computed 13calpha chemical shifts. J Biomol NMR 2010, 48:23-30.
47. Martin O.A., Vila J.A., Scheraga H.A. Cheshift-2: graphic validation of protein structures. Bioinformatics 2012, 28:1538-1539.
48. Shen Y., Bax A. Sparta+: a modest improvement in empirical NMR chemical shift prediction by means of an artificial neural network. J Biomol NMR 2010, 48:13-22.
49. Han B., Liu Y., Ginzinger S.W., Wishart D.S. Shiftx2: significantly improved protein chemical shift prediction. J Biomol NMR 2011, 50:43-57.
50. Wang B., Wang Y., Wishart D.S. A probabilistic approach for validating protein NMR chemical shift assignments. J Biomol NMR 2010, 47:85-99.
51. Sahakyan A.B., Vranken W.F., Cavalli A., Vendruscolo M. Using side-chain aromatic proton chemical shifts for a quantitative analysis of protein structures. Angew Chem Int Ed Engl 2011, 50:9620-9623.
52. Sahakyan A.B., Vranken W.F., Cavalli A., Vendruscolo M. Structure-based prediction of methyl chemical shifts in proteins. J Biomol NMR 2011, 50:331-346.
53. Vila J.A., Sue S.C., Fraser J.S., Scheraga H.A., Dyson H.J. Cheshift-2 resolves a local inconsistency between two X-ray crystal structures. J Biomol NMR 2012, 54:193-198.
54. Vila J.A., Arnautova Y.A., Vorobjev Y., Scheraga H.A. Assessing the fractions of tautomeric forms of the imidazole ring of histidine in proteins as a function of ph. Proc Natl Acad Sci USA 2011, 108:5602-5607.
55. Hyberts S.G., Goldberg M.S., Havel T.F., Wagner G. The solution structure of eglin c based on measurements of many nodes and coupling constants and its comparison with X-ray structures. Protein Sci 1992, 1:736-751.
56. Kirchner D.K., Guntert P. Objective identification of residue ranges for the superposition of protein structures. BMC Bioinformatics 2011, 12:170.
57. Vuister G.W., Fogh R.H., Hendrickx P.M., Doreleijers J.F., Gutmanas A. An overview of tools for the validation of protein NMR structures. J Biomol NMR 2013.
58. Snyder D.A., Montelione G.T. Clustering algorithms for identifying core atom sets and for assessing the precision of protein structure ensembles. Proteins 2005, 59:673-686.
59. Andrec M., Snyder D.A., Zhou Z., Young J., Montelione G.T., Levy R.M. A large data set comparison of protein structures determined by crystallography and NMR: statistical test for structural differences and the effect of crystal packing. Proteins 2007, 69:449-465.
60. Tejero R., Bassolino-Klimas D., Bruccoleri R.E., Montelione G.T. Simulated annealing with restrained molecular dynamics using congen: energy refinement of the NMR solution structures of epidermal and type-alpha transforming growth factors. Protein Sci 1996, 5:578-592.
61. Doreleijers J.F., Sousa da Silva A.W., Krieger E., Nabuurs S.B., Spronk C.A., Stevens T.J., Vranken W.F., Vriend G., Vuister G.W. CiNG: an integrated residue-based structure validation program suite. J Biomol NMR 2012, 54:267-283.
62. Doreleijers J.F., Vranken W.F., Schulte C., Markley J.L., Ulrich E.L., Vriend G., Vuister G.W. NRG-CiNG: integrated validation reports of remediated experimental biomolecular NMR data and coordinates in wwpdb. Nucleic Acids Res 2012, 40(Database issue):519-524.
63. Hendrickx P.M., Gutmanas A., Kleywegt G.J. Vivaldi: visualization and validation of biomacromolecular NMR structures from the pdb. Proteins 2013, 81:583-591.
64. Bagaria A., Jaravine V., Guntert P. Estimating structure quality trends in the protein data bank by equivalent resolution. Comput Biol Chem 2013, 46C:8-15.
65. Lindorff-Larsen K., Best R.B., Depristo M.A., Dobson C.M., Vendruscolo M. Simultaneous determination of protein structure and dynamics. Nature 2005, 433:128-132.
66. Aramini J.M., Petrey D., Lee D.Y., Janjua H., Xiao R., Acton T.B., Everett J.K., Montelione G.T. Solution NMR structure of alr2454 from nostoc sp Pcc 7120, the first structural representative of pfam domain family pf11267. J Struct Funct Genomics 2012, 13:171-176.
67. Moseley H.N., Sahota G., Montelione G.T. Assignment validation software suite for the evaluation and presentation of protein resonance assignment data. J Biomol NMR 2004, 28:341-355.
68. Doreleijers J.F., Sousa da Silva A.W., Krieger E., Nabuurs S.B., Spronk C.A., Stevens T.J., Vranken W.F., Vriend G., Vuister GW: Cing: An integrated residue-based structure validation program suite. J Biomol NMR 2012.
69. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22:2577-2637.
70. Joosten R.P., te Beek T.A., Krieger E., Hekkelman M.L., Hooft R.W., Schneider R., Sander C., Vriend G. A series of pdb related databases for everyday needs. Nucleic Acids Res 2011, 39(Database issue):D411-D419.
71. Vriend G. What if: a molecular modeling and drug design program. J Mol Graph 1990, 8:52-56. 29.
72. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. Procheck: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993, 26:283-291.
73. Rieping W., Vranken W.F. Validation of archived chemical shifts through atomic coordinates. Proteins 2010, 78:2482-2489.
74. Block J.N., Zielinski D.J., Chen V.B., Davis I.W., Vinson E.C., Brady R., Richardso J.S., Richardson D.C. Kinimmerse: macromolecular vr for NMR ensembles. Source Code Biol Med 2009, 4:3.
75. Wang L., Eghbalnia H.R., Bahrami A., Markley J.L. Linear analysis of carbon-13 chemical shift differences and its application to the detection and correction of errors in referencing and spin system identifications. J Biomol NMR 2005, 32:13-22.
76. Kelley L.A., Gardner S.P., Sutcliffe M.J. An automated approach for defining core atoms and domains in an ensemble of NMR-derived protein structures. Protein Eng 1997, 10:737-741.