A topology‐constrained distance network algorithm for protein structure determination from NOESY data

This article formulates the multidimensional nuclear Overhauser effect spectroscopy (NOESY) interpretation problem using graph theory and presents a novel, bottom‐up, topology‐constrained distance network analysis algorithm for NOESY cross peak interpretation using assigned resonances. AutoStructure is a software suite that implements this topology‐constrained distance network analysis algorithm and iteratively generates structures using the three‐dimensional (3D) protein structure calculation programs XPLOR/CNS or DYANA. The minimum input for AutoStructure includes the amino acid sequence, a list of resonance assignments, and lists of 2D, 3D, and/or 4D‐NOESY cross peaks. AutoStructure can also analyze homodimeric proteins when X‐filtered NOESY experiments are available. The quality of input data and final 3D structures is evaluated using recall, precision, and F‐measure (RPF) scores, a statistical measure of goodness of fit with the input data. AutoStructure has been tested on three protein NMR data sets for which high‐quality structures have previously been solved by an expert, and yields comparable high‐quality distance constraint lists and 3D protein structures in hours. We also compare several protein structures determined using AutoStructure with corresponding homologous proteins determined with other independent methods. The program has been used in more than two dozen protein structure determinations, several of which have already been published. Proteins 2006. © 2005 Wiley‐Liss, Inc.

[1]  Peter Norvig,et al.  Artificial Intelligence: A Modern Approach , 1995 .

[2]  Timothy F. Havel,et al.  The combinatorial distance geometry method for the calculation of molecular conformation. I. A new approach to an old problem. , 1983, Journal of theoretical biology.

[3]  Werner Braun,et al.  Automated combined assignment of NOESY spectra and three-dimensional protein structure determination , 1997, Journal of biomolecular NMR.

[4]  M Adler.  Modified genetic algorithm resolves ambiguous NOE restraints and reduces unsightly NOE violations , 2000, Proteins.

[5]  C. Chothia.  Principles that determine the structure of proteins. , 1984, Annual review of biochemistry.

[6]  Angela M. Gronenborn,et al.  The Impact of Direct Refinement against 13Cα and 13Cβ Chemical Shifts on Protein Structure Determination by NMR , 1995 .

[7]  K. Wüthrich.  NMR of proteins and nucleic acids , 1988 .

[8]  K. W. Lo,et al.  Structure of the Monomeric 8-kDa Dynein Light Chain and Mechanism of the Domain-swapped Dimer Assembly* , 2003, Journal of Biological Chemistry.

[9]  Gaetano T Montelione,et al.  Solution NMR structure of ribosome-binding factor A (RbfA), a cold-shock adaptation protein from Escherichia coli. , 2003, Journal of molecular biology.

[10]  D. Rees,et al.  Three-dimensional structures of acidic and basic fibroblast growth factors. , 1993, Science.

[11]  C. Bewley,et al.  Impact of Residual Dipolar Couplings on the Accuracy of NMR Structures Determined from a Minimal Number of NOE Restraints , 1999 .

[12]  Kurt Wüthrich,et al.  Determination of the Three-dimensional Structure of the Antennapedia Homeodomain from Drosophila in Solution by 1H Nuclear Magnetic Resonance Spectroscopy , 1993 .

[13]  D. Richardson,et al.  Exploring steric constraints on protein mutations using MAGE/PROBE , 2000, Protein science : a publication of the Protein Society.

[14]  Robert Powers,et al.  Protein NMR recall, precision, and F-measure scores (RPF scores): structure quality assessment measures based on information retrieval statistics. , 2005, Journal of the American Chemical Society.

[15]  G T Montelione,et al.  HYPER: A hierarchical algorithm for automatic determination of protein dihedral-angle constraints and stereospecific CβH2 resonance assignments from NMR data , 1999, Journal of biomolecular NMR.

[16]  A. Gronenborn,et al.  Improving the quality of NMR and crystallographic protein structures by means of a conformational database potential derived from structure databases , 1996, Protein science : a publication of the Protein Society.

[17]  Peter Güntert,et al.  Influence of the completeness of chemical shift assignments on NMR structures obtained with automated NOE assignment , 2004, Journal of Structural and Functional Genomics.

[18]  A. Bax,et al.  Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. , 1997, Science.

[19]  K Wüthrich,et al.  Sequential resonance assignments in protein 1H nuclear magnetic resonance spectra. Computation of sterically allowed proton-proton distances and statistical analysis of proton-proton distances in single crystal protein conformations. , 1982, Journal of molecular biology.

[20]  Axel T. Brunger,et al.  X-PLOR Version 3.1: A System for X-ray Crystallography and NMR , 1992 .

[21]  Robert Powers,et al.  An integrated platform for automated analysis of protein NMR structures. , 2005, Methods in enzymology.

[22]  D. Wishart,et al.  The 13C Chemical-Shift Index: A simple method for the identification of protein secondary structure using 13C chemical-shift data , 1994, Journal of biomolecular NMR.

[23]  A. Gronenborn,et al.  Three-dimensional structure of interleukin 8 in solution. , 1991, Biochemistry.

[24]  F J Moy,et al.  High-resolution solution structure of basic fibroblast growth factor determined by multidimensional heteronuclear magnetic resonance spectroscopy. , 1996, Biochemistry.

[25]  G. Marius Clore,et al.  Improving the Packing and Accuracy of NMR Structures with a Pseudopotential for the Radius of Gyration , 1999 .

[26]  Charles D Schwieters,et al.  The Xplor-NIH NMR molecular structure determination package. , 2003, Journal of magnetic resonance.

[27]  K. Wüthrich,et al.  Torsion angle dynamics for NMR structure calculation with the new program DYANA. , 1997, Journal of molecular biology.

[28]  G W Vuister,et al.  The impact of direct refinement against three-bond HN-C alpha H coupling constants on protein structure determination by NMR. , 1994, Journal of magnetic resonance. Series B.

[29]  R J Read,et al.  Crystallography & NMR system: A new software suite for macromolecular structure determination. , 1998, Acta crystallographica. Section D, Biological crystallography.

[30]  Roberto Tejero,et al.  Simulated annealing with restrained molecular dynamics using a flexible restraint potential: Theory and evaluation with simulated NMR constraints , 1996, Protein science : a publication of the Protein Society.

[31]  P. Kraulis,et al.  Three-dimensional NMR spectroscopy of a protein in solution , 1988, Nature.

[32]  A. Gronenborn,et al.  Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2. , 1988, Protein engineering.

[33]  William R. Taylor,et al.  Analysis and prediction of the packing of α-helices against a β-sheet in the tertiary structure of globular proteins , 1982 .

[34]  G. Montelione,et al.  The structure of the carboxyl terminus of striated alpha-tropomyosin in solution reveals an unusual parallel arrangement of interacting alpha-helices. , 2003, Biochemistry.

[35]  H Oschkinat,et al.  Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from beta-spectrin. , 1997, Journal of molecular biology.

[36]  Gaetano T Montelione,et al.  Automated analysis of protein NMR assignments and structures. , 2004, Chemical reviews.

[37]  G. Wagner,et al.  NMR spectroscopy: a multifaceted approach to macromolecular structure , 2000, Quarterly Reviews of Biophysics.

[38]  J. Thornton,et al.  AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR , 1996, Journal of biomolecular NMR.

[39]  G. Montelione,et al.  The solution structure of the pH‐induced monomer of dynein light‐chain LC8 from Drosophila , 2004, Protein science : a publication of the Protein Society.

[40]  D. Wemmer,et al.  Solution structure of a putative ribosome binding protein from Mycoplasma pneumoniae and comparison to a distant homolog , 2003, Journal of Structural and Functional Genomics.

[41]  Kuo-Chen Chou,et al.  Interactions between an α-helix and a β-sheet: Energetics of αβ packing in proteins☆ , 1985 .

[42]  Cyrus Chothia,et al.  Packing of α-Helices onto β-Pleated sheets and the anatomy of αβ proteins☆ , 1980 .

[43]  E. Eisenmesser,et al.  Solution structure of interleukin-13 and insights into receptor engagement. , 2001, Journal of molecular biology.

[44]  A. Gronenborn,et al.  Multidimensional heteronuclear nuclear magnetic resonance of proteins. , 1994, Methods in enzymology.

[45]  S. Grzesiek,et al.  Measurement of homo- and heteronuclear J couplings from quantitative J correlation. , 1994, Methods in enzymology.

[46]  Charles D Schwieters,et al.  Completely automated, highly error-tolerant macromolecular structure determination from multidimensional nuclear overhauser enhancement spectra and chemical shift assignments. , 2004, Journal of the American Chemical Society.

[47]  R. Powers,et al.  High-resolution solution structure of the inhibitor-free catalytic fragment of human fibroblast collagenase determined by multidimensional NMR. , 1998, Biochemistry.

[48]  Gaohua Liu,et al.  NMR data collection and analysis protocol for high-throughput protein structure determination. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Chris Bailey-Kellogg,et al.  The NOESY Jigsaw: Automated Protein Secondary Structure and Main-Chain Assignment from Sparse, Unassigned NMR Data , 2000, J. Comput. Biol..

[50]  K Wüthrich,et al.  Polypeptide secondary structure determination by nuclear magnetic resonance observation of short proton-proton distances. , 1984, Journal of molecular biology.

[51]  Torsten Herrmann,et al.  Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. , 2002, Journal of molecular biology.

[52]  P E Bourne,et al.  Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. , 1998, Protein engineering.

[53]  E. Campbell,et al.  1H, 15N, 13C and 13CO assignments and secondary structure determination of basic fibroblast growth factor using 3D heteronuclear NMR spectroscopy , 1995, Journal of biomolecular NMR.

[54]  M. Nilges,et al.  Refinement of protein structures in explicit solvent , 2003, Proteins.

[55]  G. Montelione,et al.  Structure of antibacterial peptide microcin J25: a 21-residue lariat protoknot. , 2003, Journal of the American Chemical Society.

[56]  B. Honig,et al.  Solution structure of Vibrio cholerae protein VC0424: A variation of the ferredoxin‐like fold , 2003, Protein science : a publication of the Protein Society.

[57]  A. Bax,et al.  Protein backbone angle restraints from searching a database for chemical shift and sequence homology , 1999, Journal of biomolecular NMR.

[58]  G. Montelione,et al.  Solution NMR structure and folding dynamics of the N terminus of a rat non-muscle alpha-tropomyosin in an engineered chimeric protein. , 2001, Journal of molecular biology.

[59]  W. Braun,et al.  Automated assignment of simulated and experimental NOESY spectra of proteins by feedback filtering and self-correcting distance geometry. , 1995, Journal of molecular biology.

[60]  R. Powers,et al.  Assignments, secondary structure and dynamics of the inhibitor-free catalytic fragment of human fibroblast collagenase , 1997, Journal of biomolecular NMR.

[61]  B. Rost,et al.  Solution NMR structure of the 30S ribosomal protein S28E from Pyrococcus horikoshii , 2003, Protein science : a publication of the Protein Society.

[62]  H. Scheraga,et al.  Solution of the embedding problem and decomposition of symmetric matrices. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[63]  K Wüthrich,et al.  Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance constraints with nuclear magnetic resonance. , 1983, Journal of molecular biology.

[64]  H A Scheraga,et al.  Visualization of the nature of protein folding by a study of a distance constraint approach in two‐dimensional models , 1982, Biopolymers.

[65]  R. Powers,et al.  Solution structure of human IL-13 and implication for receptor binding. , 2001, Journal of molecular biology.

[66]  A M Gronenborn,et al.  Improvements and extensions in the conformational database potential for the refinement of NMR and X-ray structures of proteins and nucleic acids. , 1997, Journal of magnetic resonance.

[67]  Thomas Szyperski,et al.  Protein NMR spectroscopy in structural genomics , 2000, Nature Structural Biology.

[68]  C. Chothia,et al.  Helix to helix packing in proteins. , 1981, Journal of molecular biology.

[69]  Gaetano T Montelione,et al.  Automated protein fold determination using a minimal NMR constraint strategy , 2003, Protein science : a publication of the Protein Society.

[70]  R. Wahl,et al.  1.56 Å structure of mature truncated human fibroblast collagenase , 1994, Proteins.

[71]  J. Augsburger,et al.  A new approach to an old problem. , 1999, Survey of ophthalmology.

[72]  W. Gronwald,et al.  Automated assignment of NOESY NMR spectra using a knowledge based method (KNOWNOE) , 2002, Journal of biomolecular NMR.

[73]  Bin Wu,et al.  Solution structure of ribosomal protein S28E from Methanobacterium thermoautotrophicum , 2003, Protein science : a publication of the Protein Society.

[74]  W R Taylor,et al.  Analysis and prediction of the packing of alpha-helices against a beta-sheet in the tertiary structure of globular proteins. , 1982, Journal of Molecular Biology.

[75]  Ronald L. Rivest,et al.  Introduction to Algorithms , 1990 .

[76]  Alexander Grishaev,et al.  CLOUDS, a protocol for deriving a molecular proton density via NMR , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[77]  M Nilges,et al.  Calculation of protein structures with ambiguous distance restraints. Automated assignment of ambiguous NOE crosspeaks and disulphide connectivities. , 1995, Journal of molecular biology.