{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,11]],"date-time":"2026-03-11T23:50:18Z","timestamp":1773273018852,"version":"3.50.1"},"reference-count":35,"publisher":"Oxford University Press (OUP)","issue":"22","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2009,11,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Summary: Protein structures can be viewed as networks of contacts (edges) between amino-acid residues (nodes). Here we dissect proteins into sub-graphs consisting of six nodes and their corresponding edges, with an edge being either a backbone hydrogen bond (H-bond) or a covalent interaction. Six thousand three hundred and twenty-two such sub-graphs were found in a large non-redundant dataset of high-resolution structures, from which 35 occur much more frequently than in a random model. Many of these significant sub-graphs (also called network motifs) correspond to sub-structures of \u03b1 helices and \u03b2-sheets, as expected. However, others correspond to more exotic sub-structures such as 310 helix, Schellman motif and motifs that were not defined previously. This topological characterization of patterns is very useful for producing a detailed differences map to compare protein structures. Here we analyzed in details the differences between NMR, molecular dynamics (MD) simulations and X-ray structures for Lysozyme, SH3 and the lambda repressor. In these cases, the same structures solved by NMR and simulated by MD showed small but consistent differences in their motif composition from the crystal structures, despite a very small root mean square deviation (RMSD) between them. This may be due to differences in the pair-wise energy functions used and the dynamic nature of these proteins.<\/jats:p>\n                  <jats:p>Availability: A web-based tool to calculate network motifs is available at http:\/\/bioinfo.weizmann.ac.il\/protmot\/.<\/jats:p>\n                  <jats:p>Contact: \u00a0gideon.schreiber@weizmann.ac.il; koby.levy@weizmann.ac.il<\/jats:p>\n                  <jats:p>Supplementary information: \u00a0Supplementary data are available at Bioinformatics online.<\/jats:p>","DOI":"10.1093\/bioinformatics\/btp541","type":"journal-article","created":{"date-parts":[[2009,9,18]],"date-time":"2009-09-18T20:15:24Z","timestamp":1253304924000},"page":"2921-2928","source":"Crossref","is-referenced-by-count":19,"title":["Understanding hydrogen-bond patterns in proteins using network motifs"],"prefix":"10.1093","volume":"25","author":[{"given":"Ofer","family":"Rahat","sequence":"first","affiliation":[{"name":"1 Department of Biological Chemistry, 2Department of Molecular Cell Biology and 3Department of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Uri","family":"Alon","sequence":"additional","affiliation":[{"name":"1 Department of Biological Chemistry, 2Department of Molecular Cell Biology and 3Department of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yaakov","family":"Levy","sequence":"additional","affiliation":[{"name":"1 Department of Biological Chemistry, 2Department of Molecular Cell Biology and 3Department of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gideon","family":"Schreiber","sequence":"additional","affiliation":[{"name":"1 Department of Biological Chemistry, 2Department of Molecular Cell Biology and 3Department of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2009,9,18]]},"reference":[{"key":"2023013112152641400_B1","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1002\/pro.5560070103","article-title":"Helix capping","volume":"7","author":"Aurora","year":"1998","journal-title":"Protein Sci."},{"key":"2023013112152641400_B2","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/nchembio766","article-title":"Dissecting the energetics of protein alpha-helix C-cap termination through chemical protein synthesis","volume":"2","author":"Bang","year":"2006","journal-title":"Nat. Chem. Biol."},{"key":"2023013112152641400_B3","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1093\/nar\/28.1.235","article-title":"The Protein Data Bank","volume":"28","author":"Berman","year":"2000","journal-title":"Nucleic Acids Res."},{"key":"2023013112152641400_B4","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1002\/1097-0134(20001115)41:3<271::AID-PROT10>3.0.CO;2-Z","article-title":"Bayesian probabilistic approach for predicting backbone structures in terms of protein blocks","volume":"41","author":"de Brevern","year":"2000","journal-title":"Proteins"},{"key":"2023013112152641400_B5","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1002\/jcc.540040211","article-title":"CHARMM: a program for macromolecular energy, minimization and dynamic calculation","volume":"4","author":"Brooks","year":"1983","journal-title":"J. Comp. Chem."},{"key":"2023013112152641400_B6","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1006\/jmbi.1998.1943","article-title":"Prediction of local structure in proteins usinag a library of sequence-structure motifs","volume":"281","author":"Bystroff","year":"1998","journal-title":"J. Mol. Biol."},{"key":"2023013112152641400_B7","first-page":"468","volume-title":"Probability and Statistics","author":"DeGroot","year":"1975"},{"key":"2023013112152641400_B8","doi-asserted-by":"crossref","first-page":"8637","DOI":"10.1073\/pnas.122076099","article-title":"Topological determinants of protein folding","volume":"99","author":"Dokholyan","year":"2002","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023013112152641400_B9","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1002\/prot.20601","article-title":"An assessment of the accuracy of methods for predicting hydrogen positions in protein structures","volume":"61","author":"Forrest","year":"2005","journal-title":"Proteins"},{"key":"2023013112152641400_B10","doi-asserted-by":"crossref","first-page":"6648","DOI":"10.1073\/pnas.0408036102","article-title":"Ab initio quantum chemistry: methodology and applications","volume":"102","author":"Friesner","year":"2005","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023013112152641400_B11","doi-asserted-by":"crossref","first-page":"10167","DOI":"10.1073\/pnas.93.19.10167","article-title":"Packing at the protein-water interface","volume":"93","author":"Gerstein","year":"1996","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023013112152641400_B12","doi-asserted-by":"crossref","first-page":"7605","DOI":"10.1021\/bi00081a001","article-title":"Helix stop signals in proteins and peptides: the capping box","volume":"32","author":"Harper","year":"1993","journal-title":"Biochemistry"},{"key":"2023013112152641400_B13","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1145\/974614.974655","article-title":"Mining protein family specific residue packing patterns from protein structure graphs","author":"Huan","year":"2004","journal-title":"RECOMB'04"},{"key":"2023013112152641400_B14","first-page":"227","article-title":"Distance-based identification of structure motifs in proteins using constrained frequent subgraph mining","author":"Huan","year":"2006","journal-title":"Proc. LSS Comp. Sys. Bioinfor. Conf. CSB"},{"key":"2023013112152641400_B15","doi-asserted-by":"crossref","first-page":"2577","DOI":"10.1002\/bip.360221211","article-title":"Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features","volume":"22","author":"Kabsch","year":"1983","journal-title":"Biopolymers"},{"key":"2023013112152641400_B16","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/S0022-2836(02)00942-7","article-title":"Small libraries of protein fragments model native protein structures accurately","volume":"323","author":"Kolodny","year":"2002","journal-title":"J. Mol. Biol."},{"key":"2023013112152641400_B17","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1002\/1097-0134(20000901)40:4<662::AID-PROT90>3.0.CO;2-F","article-title":"Recurrent oligomers in proteins: an optimal scheme reconciling accurate and concise backbone representations in automated folding and design studies","volume":"40","author":"Micheletti","year":"2000","journal-title":"Proteins"},{"key":"2023013112152641400_B18","doi-asserted-by":"crossref","first-page":"1538","DOI":"10.1126\/science.1089167","article-title":"Superfamilies of evolved and designed networks","volume":"303","author":"Milo","year":"2004","journal-title":"Science"},{"key":"2023013112152641400_B19","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1038\/380730a0","article-title":"Context-dependent secondary structure formation of a designed protein sequence","volume":"380","author":"Minor","year":"1996","journal-title":"Nature"},{"key":"2023013112152641400_B20","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1002\/prot.340120407","article-title":"Stereochemical quality of protein structure coordinates","volume":"12","author":"Morris","year":"1992","journal-title":"Proteins"},{"key":"2023013112152641400_B21","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/0014-5793(93)80625-5","article-title":"Termination of right handed helices in proteins by residues in left handed helical conformations","volume":"321","author":"Nagarajaram","year":"1993","journal-title":"FEBS Lett."},{"issue":"Suppl. 1","key":"2023013112152641400_B22","first-page":"396","article-title":"Neutron protein crystallography in JAERI","volume":"70","author":"Niimura","year":"2001","journal-title":"J. Phys. Soc. Jpn."},{"key":"2023013112152641400_B23","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1006\/jmbi.1996.0819","article-title":"An automated classification of the structure of protein loops","volume":"266","author":"Oliva","year":"1997","journal-title":"J. Mol. Biol."},{"key":"2023013112152641400_B24","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1002\/prot.21749","article-title":"Cluster conservation as a novel tool for studying protein-protein interactions evolution","volume":"71","author":"Rahat","year":"2008","journal-title":"Proteins"},{"key":"2023013112152641400_B25","doi-asserted-by":"crossref","first-page":"e163","DOI":"10.1093\/bioinformatics\/btl290","article-title":"Rediscovering secondary structures as network motifs-an unsupervised learning approach","volume":"23","author":"Raveh","year":"2007","journal-title":"Bioinformatics"},{"key":"2023013112152641400_B26","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1073\/pnas.0407280102","article-title":"The modular architecture of protein-protein binding interfaces","volume":"102","author":"Reichmann","year":"2005","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023013112152641400_B27","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.1126\/science.3381086","article-title":"Amino acid preferences for specific locations at the ends of alpha helices","volume":"240","author":"Richardson","year":"1988","journal-title":"Science"},{"key":"2023013112152641400_B28","first-page":"167","article-title":"The anatomy and taxonomy of protein structure","volume-title":"Advances in Protein Chemistry","author":"Richardson","year":"1981"},{"key":"2023013112152641400_B29","first-page":"53","article-title":"The \u03b1L conformation at the ends of helices","volume-title":"Protein Folding.","author":"Schellman","year":"1980"},{"key":"2023013112152641400_B30","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1002\/prot.340050410","article-title":"A 3D building blocks approach to analyzing and predicting structure of proteins","volume":"5","author":"Unger","year":"1989","journal-title":"Proteins"},{"key":"2023013112152641400_B31","doi-asserted-by":"crossref","first-page":"1589","DOI":"10.1093\/bioinformatics\/btg224","article-title":"PISCES: a protein sequence culling server","volume":"19","author":"Wang","year":"2003","journal-title":"Bioinformatics"},{"key":"2023013112152641400_B32","first-page":"31","article-title":"Mining RNA tertiary motifs with structure graphs","author":"Wang","year":"2007","journal-title":"Nineteenth International Conference on Science and Statistical Database Management (SSDBM 2007)"},{"key":"2023013112152641400_B33","doi-asserted-by":"crossref","first-page":"1152","DOI":"10.1093\/bioinformatics\/btl038","article-title":"FANMOD: a tool for fast network motif detection","volume":"22","author":"Wernicke","year":"2006","journal-title":"Bioinformatics"},{"key":"2023013112152641400_B34","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1006\/jmbi.1996.0020","article-title":"Automatic classification and analysis of alpha alpha-turn motifs in proteins","volume":"255","author":"Wintjens","year":"1996","journal-title":"J. Mol. Biol."},{"key":"2023013112152641400_B35","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1006\/jmbi.1998.2400","article-title":"Visualizing and quantifying molecular goodness-of-fit: small-probe contact dots with explicit hydrogen atoms","volume":"285","author":"Word","year":"1999","journal-title":"J. Mol. Biol."}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/25\/22\/2921\/48997230\/bioinformatics_25_22_2921.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/25\/22\/2921\/48997230\/bioinformatics_25_22_2921.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,31]],"date-time":"2023-01-31T16:51:37Z","timestamp":1675183897000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/25\/22\/2921\/180785"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,9,18]]},"references-count":35,"journal-issue":{"issue":"22","published-print":{"date-parts":[[2009,11,15]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btp541","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.1255959.911054","asserted-by":"object"},{"id-type":"doi","id":"10.3410\/f.1255959.723058","asserted-by":"object"}]},"ISSN":["1367-4811","1367-4803"],"issn-type":[{"value":"1367-4811","type":"electronic"},{"value":"1367-4803","type":"print"}],"subject":[],"published-other":{"date-parts":[[2009,11,15]]},"published":{"date-parts":[[2009,9,18]]}}}