2dcr Citations

Automated protein structure determination from NMR spectra.

J. Am. Chem. Soc. 128 13112-22 (2006)
Related entries: 2dcq, 2dcp, 1wqu

Cited: 77 times
EuropePMC logo PMID: 17017791


Fully automated structure determination of proteins in solution (FLYA) yields, without human intervention, three-dimensional protein structures starting from a set of multidimensional NMR spectra. Integrating existing and new software, automated peak picking over all spectra is followed by peak list filtering, the generation of an ensemble of initial chemical shift assignments, the determination of consensus chemical shift assignments for all (1)H, (13)C, and (15)N nuclei, the assignment of NOESY cross-peaks, the generation of distance restraints, and the calculation of the three-dimensional structure by torsion angle dynamics. The resulting, preliminary structure serves as additional input to the second stage of the procedure, in which a new ensemble of chemical shift assignments and a refined structure are calculated. The three-dimensional structures of three 12-16 kDa proteins computed with the FLYA algorithm coincided closely with the conventionally determined structures. Deviations were below 0.95 A for the backbone atom positions, excluding the flexible chain termini. 96-97% of all backbone and side-chain chemical shifts in the structured regions were assigned to the correct residues. The purely computational FLYA method is suitable for substituting all manual spectra analysis and thus overcomes a main efficiency limitation of the NMR method for protein structure determination.

Reviews citing this publication (9)

  1. NMR-based Stable Isotope Resolved Metabolomics in systems biochemistry. Lane AN, Fan TW. Arch. Biochem. Biophys. 628 123-131 (2017)
  2. NMR-based automated protein structure determination. Würz JM, Kazemi S, Schmidt E, Bagaria A, Güntert P. Arch. Biochem. Biophys. 628 24-32 (2017)
  3. NMR solution structure determination of large RNA-protein complexes. Yadav DK, Lukavsky PJ. Prog Nucl Magn Reson Spectrosc 97 57-81 (2016)
  4. An overview of tools for the validation of protein NMR structures. Vuister GW, Fogh RH, Hendrickx PM, Doreleijers JF, Gutmanas A. J. Biomol. NMR 58 259-285 (2014)
  5. Recent advances in computational methods for nuclear magnetic resonance data processing. Gao X. Genomics Proteomics Bioinformatics 11 29-33 (2013)
  6. Synergistic applications of MD and NMR for the study of biological systems. Fisette O, Lagüe P, Gagné S, Morin S. J. Biomed. Biotechnol. 2012 254208 (2012)
  7. Advances in automated NMR protein structure determination. Guerry P, Herrmann T. Q. Rev. Biophys. 44 257-309 (2011)
  8. Automated structure determination from NMR spectra. Güntert P. Eur. Biophys. J. 38 129-143 (2009)
  9. Structural proteomics by NMR spectroscopy. Shin J, Lee W, Lee W. Expert Rev Proteomics 5 589-601 (2008)

Articles citing this publication (68)

  1. BioMagResBank. 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, Kent Wenger R, Yao H, Markley JL. Nucleic Acids Res. 36 D402-8 (2008)
  2. Probabilistic interaction network of evidence algorithm and its application to complete labeling of peak lists from protein NMR spectroscopy. Bahrami A, Assadi AH, Markley JL, Eghbalnia HR. PLoS Comput. Biol. 5 e1000307 (2009)
  3. Blind testing of routine, fully automated determination of protein structures from NMR data. Rosato A, Aramini JM, Arrowsmith C, Bagaria A, Baker D, Cavalli A, Doreleijers JF, Eletsky A, Giachetti A, Guerry P, Gutmanas A, Güntert P, He Y, Herrmann T, Huang YJ, Jaravine V, Jonker HR, Kennedy MA, Lange OF, Liu G, Malliavin TE, Mani R, Mao B, Montelione GT, Nilges M, Rossi P, van der Schot G, Schwalbe H, Szyperski TA, Vendruscolo M, Vernon R, Vranken WF, Vries Sd, Vuister GW, Wu B, Yang Y, Bonvin AM. Structure 20 227-236 (2012)
  4. Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis. Berry JL, Phelan MM, Collins RF, Adomavicius T, Tønjum T, Frye SA, Bird L, Owens R, Ford RC, Lian LY, Derrick JP. PLoS Pathog. 8 e1002923 (2012)
  5. Nucleosomal DNA binding drives the recognition of H3K36-methylated nucleosomes by the PSIP1-PWWP domain. van Nuland R, van Schaik FM, Simonis M, van Heesch S, Cuppen E, Boelens R, Timmers HM, van Ingen H. Epigenetics Chromatin 6 12 (2013)
  6. Structural biology by NMR: structure, dynamics, and interactions. Markwick PR, Malliavin T, Nilges M. PLoS Comput. Biol. 4 e1000168 (2008)
  7. Polynomially scaling spin dynamics simulation algorithm based on adaptive state-space restriction. Kuprov I, Wagner-Rundell N, Hore PJ. J. Magn. Reson. 189 241-250 (2007)
  8. Probing the relationship between Gram-negative and Gram-positive S1 proteins by sequence analysis. Salah P, Bisaglia M, Aliprandi P, Uzan M, Sizun C, Bontems F. Nucleic Acids Res. 37 5578-5588 (2009)
  9. Automated protein structure calculation from NMR data. Williamson MP, Craven CJ. J. Biomol. NMR 43 131-143 (2009)
  10. Synthesis of xanthones, thioxanthones, and acridones by the coupling of arynes and substituted benzoates. Zhao J, Larock RC. J. Org. Chem. 72 583-588 (2007)
  11. Combined automated NOE assignment and structure calculation with CYANA. Güntert P, Buchner L. J. Biomol. NMR 62 453-471 (2015)
  12. Experimental conversion of a defensin into a neurotoxin: implications for origin of toxic function. Zhu S, Peigneur S, Gao B, Umetsu Y, Ohki S, Tytgat J. Mol. Biol. Evol. 31 546-559 (2014)
  13. Objective identification of residue ranges for the superposition of protein structures. Kirchner DK, Güntert P. BMC Bioinformatics 12 170 (2011)
  14. Automated structure determination of proteins with the SAIL-FLYA NMR method. Takeda M, Ikeya T, Güntert P, Kainosho M. Nat Protoc 2 2896-2902 (2007)
  15. Binding site identification and structure determination of protein-ligand complexes by NMR a semiautomated approach. Ziarek JJ, Peterson FC, Lytle BL, Volkman BF. Meth. Enzymol. 493 241-275 (2011)
  16. Open-channel structures of the human glycine receptor α1 full-length transmembrane domain. Mowrey DD, Cui T, Jia Y, Ma D, Makhov AM, Zhang P, Tang P, Xu Y. Structure 21 1897-1904 (2013)
  17. Automated assignment of NMR chemical shifts using peak-particle dynamics simulation with the DYNASSIGN algorithm. Schmucki R, Yokoyama S, Güntert P. J. Biomol. NMR 43 97-109 (2009)
  18. Structure of the Cdt1 C-terminal domain: conservation of the winged helix fold in replication licensing factors. Khayrutdinov BI, Bae WJ, Yun YM, Lee JH, Tsuyama T, Kim JJ, Hwang E, Ryu KS, Cheong HK, Cheong C, Ko JS, Enomoto T, Karplus PA, Güntert P, Tada S, Jeon YH, Cho Y. Protein Sci. 18 2252-2264 (2009)
  19. Protein-small molecule interactions in neocarzinostatin, the prototypical enediyne chromoprotein antibiotic. Baker JR, Woolfson DN, Muskett FW, Stoneman RG, Urbaniak MD, Caddick S. Chembiochem 8 704-717 (2007)
  20. PONDEROSA, an automated 3D-NOESY peak picking program, enables automated protein structure determination. Lee W, Kim JH, Westler WM, Markley JL. Bioinformatics 27 1727-1728 (2011)
  21. A universal expression tag for structural and functional studies of proteins. Rogov VV, Rozenknop A, Rogova NY, Löhr F, Tikole S, Jaravine V, Güntert P, Dikic I, Dötsch V. Chembiochem 13 959-963 (2012)
  22. Comparison of structure determination methods for intrinsically disordered amyloid-β peptides. Ball KA, Wemmer DE, Head-Gordon T. J Phys Chem B 118 6405-6416 (2014)
  23. Modeling of NMR processing, toward efficient unattended processing of NMR experiments. Tramesel D, Catherinot V, Delsuc MA. J. Magn. Reson. 188 56-67 (2007)
  24. Automated and assisted RNA resonance assignment using NMR chemical shift statistics. Aeschbacher T, Schmidt E, Blatter M, Maris C, Duss O, Allain FH, Güntert P, Schubert M. Nucleic Acids Res. 41 e172 (2013)
  25. Automated NMR Assignment and Protein Structure Determination using Sparse Dipolar Coupling Constraints. Donald BR, Martin J. Prog Nucl Magn Reson Spectrosc 55 101-127 (2009)
  26. Automated NMR structure determination of stereo-array isotope labeled ubiquitin from minimal sets of spectra using the SAIL-FLYA system. Ikeya T, Takeda M, Yoshida H, Terauchi T, Jee JG, Kainosho M, Güntert P. J. Biomol. NMR 44 261-272 (2009)
  27. Exclusively NOESY-based automated NMR assignment and structure determination of proteins. Ikeya T, Jee JG, Shigemitsu Y, Hamatsu J, Mishima M, Ito Y, Kainosho M, Güntert P. J. Biomol. NMR 50 137-146 (2011)
  28. The apo-structure of the low molecular weight protein-tyrosine phosphatase A (MptpA) from Mycobacterium tuberculosis allows for better target-specific drug development. Stehle T, Sreeramulu S, Löhr F, Richter C, Saxena K, Jonker HR, Schwalbe H. J. Biol. Chem. 287 34569-34582 (2012)
  29. The insect defensin lucifensin from Lucilia sericata. Nygaard MK, Andersen AS, Kristensen HH, Krogfelt KA, Fojan P, Wimmer R. J. Biomol. NMR 52 277-282 (2012)
  30. Finding Our Way in the Dark Proteome. Bhowmick A, Brookes DH, Yost SR, Dyson HJ, Forman-Kay JD, Gunter D, Head-Gordon M, Hura GL, Pande VS, Wemmer DE, Wright PE, Head-Gordon T. J. Am. Chem. Soc. 138 9730-9742 (2016)
  31. Reliability of exclusively NOESY-based automated resonance assignment and structure determination of proteins. Schmidt E, Güntert P. J. Biomol. NMR 57 193-204 (2013)
  32. Robust, integrated computational control of NMR experiments to achieve optimal assignment by ADAPT-NMR. Bahrami A, Tonelli M, Sahu SC, Singarapu KK, Eghbalnia HR, Markley JL. PLoS ONE 7 e33173 (2012)
  33. Advances in Nuclear Magnetic Resonance for Drug Discovery. Powers R. Expert Opin Drug Discov 4 1077-1098 (2009)
  34. Structure of the putative 32 kDa myrosinase-binding protein from Arabidopsis (At3g16450.1) determined by SAIL-NMR. Takeda M, Sugimori N, Torizawa T, Terauchi T, Ono AM, Yagi H, Yamaguchi Y, Kato K, Ikeya T, Jee J, Güntert P, Aceti DJ, Markley JL, Kainosho M. FEBS J. 275 5873-5884 (2008)
  35. CcpNmr AnalysisAssign: a flexible platform for integrated NMR analysis. Skinner SP, Fogh RH, Boucher W, Ragan TJ, Mureddu LG, Vuister GW. J. Biomol. NMR 66 111-124 (2016)
  36. Systematic evaluation of combined automated NOE assignment and structure calculation with CYANA. Buchner L, Güntert P. J. Biomol. NMR 62 81-95 (2015)
  37. Automated NMR resonance assignment strategy for RNA via the phosphodiester backbone based on high-dimensional through-bond APSY experiments. Krähenbühl B, El Bakkali I, Schmidt E, Güntert P, Wider G. J. Biomol. NMR 59 87-93 (2014)
  38. Automated solid-state NMR resonance assignment of protein microcrystals and amyloids. Schmidt E, Gath J, Habenstein B, Ravotti F, Székely K, Huber M, Buchner L, Böckmann A, Meier BH, Güntert P. J. Biomol. NMR 56 243-254 (2013)
  39. Rapid synthesis of the indole-indolone scaffold via [3+2] annulation of arynes by methyl indole-2-carboxylates. Rogness DC, Larock RC. Tetrahedron Lett. 50 4003-4008 (2009)
  40. Error tolerant NMR backbone resonance assignment and automated structure generation. Alipanahi B, Gao X, Karakoc E, Li SC, Balbach F, Feng G, Donaldson L, Li M. J Bioinform Comput Biol 9 15-41 (2011)
  41. Computer vision-based automated peak picking applied to protein NMR spectra. Klukowski P, Walczak MJ, Gonczarek A, Boudet J, Wider G. Bioinformatics 31 2981-2988 (2015)
  42. Rational design of alpha-helical antimicrobial peptides: do's and don'ts. Uggerhøj LE, Poulsen TJ, Munk JK, Fredborg M, Sondergaard TE, Frimodt-Moller N, Hansen PR, Wimmer R. Chembiochem 16 242-253 (2015)
  43. Mesomartoxin, a new K(v)1.2-selective scorpion toxin interacting with the channel selectivity filter. Wang X, Umetsu Y, Gao B, Ohki S, Zhu S. Biochem. Pharmacol. 93 232-239 (2015)
  44. Effects of NMR spectral resolution on protein structure calculation. Tikole S, Jaravine V, Orekhov VY, Güntert P. PLoS ONE 8 e68567 (2013)
  45. Simultaneous single-structure and bundle representation of protein NMR structures in torsion angle space. Gottstein D, Kirchner DK, Güntert P. J. Biomol. NMR 52 351-364 (2012)
  46. Peakmatch: a simple and robust method for peak list matching. Buchner L, Schmidt E, Güntert P. J. Biomol. NMR 55 267-277 (2013)
  47. Strategy for automated NMR resonance assignment of RNA: application to 48-nucleotide K10. Krähenbühl B, Lukavsky P, Wider G. J. Biomol. NMR 59 231-240 (2014)
  48. Solution NMR refinement of a metal ion bound protein using metal ion inclusive restrained molecular dynamics methods. Chakravorty DK, Wang B, Lee CW, Guerra AJ, Giedroc DP, Merz KM. J. Biomol. NMR 56 125-137 (2013)
  49. Fast automated NMR spectroscopy of short-lived biological samples. Tikole S, Jaravine V, Rogov VV, Rozenknop A, Schmöe K, Löhr F, Dötsch V, Güntert P. Chembiochem 13 964-967 (2012)
  50. Peak picking multidimensional NMR spectra with the contour geometry based algorithm CYPICK. Würz JM, Güntert P. J. Biomol. NMR 67 63-76 (2017)
  51. Structure/Function Analysis of Protein-Protein Interactions Developed by the Yeast Pih1 Platform Protein and Its Partners in Box C/D snoRNP Assembly. Quinternet M, Rothé B, Barbier M, Bobo C, Saliou JM, Jacquemin C, Back R, Chagot ME, Cianférani S, Meyer P, Branlant C, Charpentier B, Manival X. J. Mol. Biol. 427 2816-2839 (2015)
  52. NMRFAM-SDF: a protein structure determination framework. Dashti H, Lee W, Tonelli M, Cornilescu CC, Cornilescu G, Assadi-Porter FM, Westler WM, Eghbalnia HR, Markley JL. J. Biomol. NMR 62 481-495 (2015)
  53. Automatic phase correction of 2D NMR spectra by a whitening method. Balacco G, Cobas C. Magn Reson Chem 47 322-327 (2009)
  54. Structural Basis of the High Affinity Interaction between the Alphavirus Nonstructural Protein-3 (nsP3) and the SH3 Domain of Amphiphysin-2. Tossavainen H, Aitio O, Hellman M, Saksela K, Permi P. J. Biol. Chem. 291 16307-16317 (2016)
  55. NMR structure calculation for all small molecule ligands and non-standard residues from the PDB Chemical Component Dictionary. Yilmaz EM, Güntert P. J. Biomol. NMR 63 21-37 (2015)
  56. NMR Structure of Francisella tularensis Virulence Determinant Reveals Structural Homology to Bet v1 Allergen Proteins. Zook J, Mo G, Sisco NJ, Craciunescu FM, Hansen DT, Baravati B, Cherry BR, Sykes K, Wachter R, Van Horn WD, Fromme P. Structure 23 1116-1122 (2015)
  57. An algorithm to enumerate all possible protein conformations verifying a set of distance constraints. Cassioli A, Bardiaux B, Bouvier G, Mucherino A, Alves R, Liberti L, Nilges M, Lavor C, Malliavin TE. BMC Bioinformatics 16 23 (2015)
  58. Structural features of peptoid-peptide hybrids in lipid-water interfaces. Uggerhøj LE, Munk JK, Hansen PR, Güntert P, Wimmer R. FEBS Lett. 588 3291-3297 (2014)
  59. A new model for mapping the peptide backbone: predicting proton chemical shifts in proteins. Barneto JL, Avalos M, Babiano R, Cintas P, Jiménez JL, Palacios JC. Org. Biomol. Chem. 8 857-863 (2010)
  60. Prediction of peak overlap in NMR spectra. Hefke F, Schmucki R, Güntert P. J. Biomol. NMR 56 113-123 (2013)
  61. MOTOR: model assisted software for NMR structure determination. Schieborr U, Sreeramulu S, Elshorst B, Maurer M, Saxena K, Stehle T, Kudlinzki D, Gande SL, Schwalbe H. Proteins 81 2007-2022 (2013)
  62. Chimeric Avidin--NMR structure and dynamics of a 56 kDa homotetrameric thermostable protein. Tossavainen H, Kukkurainen S, Määttä JA, Kähkönen N, Pihlajamaa T, Hytönen VP, Kulomaa MS, Permi P. PLoS ONE 9 e100564 (2014)
  63. Exploiting image registration for automated resonance assignment in NMR. Strickland M, Stephens T, Liu J, Tjandra N. J. Biomol. NMR 62 143-156 (2015)
  64. Redox-dependent disulfide bond formation in SAP30L corepressor protein: Implications for structure and function. Laitaoja M, Tossavainen H, Pihlajamaa T, Valjakka J, Viiri K, Lohi O, Permi P, Jänis J. Protein Sci. 25 572-586 (2016)
  65. Lipopolysaccharide-bound structure of the antimicrobial peptide cecropin P1 determined by nuclear magnetic resonance spectroscopy. Baek MH, Kamiya M, Kushibiki T, Nakazumi T, Tomisawa S, Abe C, Kumaki Y, Kikukawa T, Demura M, Kawano K, Aizawa T. J. Pept. Sci. 22 214-221 (2016)
  66. NmPin from the marine thaumarchaeote Nitrosopumilus maritimus is an active membrane associated prolyl isomerase. Hoppstock L, Trusch F, Lederer C, van West P, Koenneke M, Bayer P. BMC Biol. 14 53 (2016)
  67. INFOS: spectrum fitting software for NMR analysis. Smith AA. J. Biomol. NMR 67 77-94 (2017)
  68. Identification and structural characterization of LytU, a unique peptidoglycan endopeptidase from the lysostaphin family. Raulinaitis V, Tossavainen H, Aitio O, Juuti JT, Hiramatsu K, Kontinen V, Permi P. Sci Rep 7 6020 (2017)

Related citations provided by authors (2)

  1. Solution structure of the Src homology 2 domain from the human feline sarcoma oncogene Fes.. Scott A, Pantoja-Uceda D, Koshiba S, Inoue M, Kigawa T, Terada T, Shirouzu M, Tanaka A, Sugano S, Yokoyama S, Güntert P J. Biomol. NMR 31 357-61 (2005)
  2. NMR assignment of the SH2 domain from the human feline sarcoma oncogene FES.. Scott A, Pantoja-Uceda D, Koshiba S, Inoue M, Kigawa T, Terada T, Shirouzu M, Tanaka A, Sugano S, Yokoyama S, Güntert P J. Biomol. NMR 30 463-4 (2004)