{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,6]],"date-time":"2026-05-06T08:49:50Z","timestamp":1778057390311,"version":"3.51.4"},"reference-count":47,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2015,6,1]],"date-time":"2015-06-01T00:00:00Z","timestamp":1433116800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"DOI":"10.1371\/journal.pcbi.1004313","type":"journal-article","created":{"date-parts":[[2015,6,2]],"date-time":"2015-06-02T00:51:07Z","timestamp":1433206267000},"page":"e1004313","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":23,"title":["Detailed Per-residue Energetic Analysis Explains the Driving Force for Microtubule Disassembly"],"prefix":"10.1371","volume":"11","author":[{"given":"Ahmed T.","family":"Ayoub","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mariusz","family":"Klobukowski","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jack A.","family":"Tuszynski","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2015,6,1]]},"reference":[{"key":"ref1","article-title":"Microtubules","author":"JS Hyams","year":"1993"},{"issue":"3","key":"ref2","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1083\/jcb.111.3.1039","article-title":"Kinetochores capture astral microtubules during chromosome attachment to the mitotic spindle: direct visualization in live newt lung cells","volume":"111","author":"JH Hayden","year":"1990","journal-title":"The Journal of Cell Biology"},{"issue":"10","key":"ref3","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1038\/nrd3253","article-title":"Microtubule-binding agents: a dynamic field of cancer therapeutics","volume":"9","author":"C Dumontet","year":"2010","journal-title":"Nature Reviews Drug Discovery"},{"issue":"4054","key":"ref4","doi-asserted-by":"crossref","first-page":"1104","DOI":"10.1126\/science.177.4054.1104","article-title":"Microtubule Formation in vitro in Solutions Containing Low Calcium Concentrations","volume":"177","author":"RC Weisenberg","year":"1972","journal-title":"Science"},{"key":"ref5","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-642-69652-7","article-title":"Microtubules","author":"P Dustin","year":"1984"},{"issue":"4","key":"ref6","doi-asserted-by":"crossref","first-page":"1437","DOI":"10.1083\/jcb.107.4.1437","article-title":"Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies","volume":"107","author":"RA Walker","year":"1988","journal-title":"The Journal of Cell Biology"},{"issue":"5124","key":"ref7","doi-asserted-by":"crossref","first-page":"1044","DOI":"10.1126\/science.8102497","article-title":"Localization of an exchangeable GTP binding site at the plus end of microtubules","volume":"261","author":"T Mitchison","year":"1993","journal-title":"Science"},{"issue":"7","key":"ref8","doi-asserted-by":"crossref","first-page":"1918","DOI":"10.1021\/bi00510a030","article-title":"Kinetic analysis of guanosine 5\u2019-triphosphate hydrolysis associated with tubulin polymerization","volume":"20","author":"MF Carlier","year":"1981","journal-title":"Biochemistry"},{"issue":"5991","key":"ref9","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1038\/312237a0","article-title":"Dynamic instability of microtubule growth","volume":"312","author":"T Mitchison","year":"1984","journal-title":"Nature"},{"issue":"3","key":"ref10","doi-asserted-by":"crossref","first-page":"1561","DOI":"10.1073\/pnas.77.3.1561","article-title":"Taxol stabilizes microtubules in mouse fibroblast cells","volume":"77","author":"PB Schiff","year":"1980","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"5","key":"ref11","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1083\/jcb.114.5.977","article-title":"Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study","volume":"114","author":"EM Mandelkow","year":"1991","journal-title":"The Journal of Cell Biology"},{"issue":"1","key":"ref12","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1083\/jcb.128.1.117","article-title":"Structural changes accompanying GTP hydrolysis in microtubules: information from a slowly hydrolyzable analogue guanylyl-(alpha,beta)-methylene-diphosphonate","volume":"128","author":"AA Hyman","year":"1995","journal-title":"The Journal of Cell Biology"},{"issue":"2","key":"ref13","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.sbi.2006.03.005","article-title":"Structural mechanisms underlying nucleotide-dependent self-assembly of tubulin and its relatives","volume":"16","author":"E Nogales","year":"2006","journal-title":"Current Opinion in Structural Biology"},{"issue":"41","key":"ref14","doi-asserted-by":"crossref","first-page":"31672","DOI":"10.1074\/jbc.M110.141929","article-title":"Stathmin and interfacial microtubule inhibitors recognize a naturally curved conformation of tubulin dimers","volume":"285","author":"P Barbier","year":"2010","journal-title":"Journal of Biological Chemistry"},{"issue":"5","key":"ref15","doi-asserted-by":"crossref","first-page":"1117","DOI":"10.1016\/j.cell.2014.03.053","article-title":"High-resolution microtubule structures reveal the structural transitions in <italic>\u03b1\u03b2<\/italic>-tubulin upon GTP hydrolysis","volume":"157","author":"G Alushin","year":"2014","journal-title":"Cell"},{"issue":"5","key":"ref16","doi-asserted-by":"crossref","first-page":"1008","DOI":"10.1016\/j.cell.2014.05.001","article-title":"The Engine of Microtubule Dynamics Comes into Focus","volume":"157","author":"TJ Mitchison","year":"2014","journal-title":"Cell"},{"issue":"2","key":"ref17","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/S0006-3495(81)84850-3","article-title":"The role of subunit entropy in cooperative assembly. Nucleation of microtubules and other two\u2013dimensional polymers","volume":"34","author":"HP Erickson","year":"1981","journal-title":"Biophysical Journal"},{"issue":"9","key":"ref18","doi-asserted-by":"crossref","first-page":"6035","DOI":"10.1073\/pnas.092504999","article-title":"Estimates of lateral and longitudinal bond energies within the microtubule lattice","volume":"99","author":"V VanBuren","year":"2002","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"10","key":"ref19","doi-asserted-by":"crossref","first-page":"2257","DOI":"10.1110\/ps.03187503","article-title":"The physical basis of microtubule structure and stability","volume":"12","author":"D Sept","year":"2003","journal-title":"Protein Science"},{"issue":"2","key":"ref20","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1529\/biophysj.106.089987","article-title":"Microtubule stability studied by three-dimensional molecular theory of solvation","volume":"92","author":"P Drabik","year":"2007","journal-title":"Biophysical Journal"},{"issue":"4","key":"ref21","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1007\/s10822-012-9566-x","article-title":"The state of the guanosine nucleotide allosterically affects the interfaces of tubulin in protofilament","volume":"26","author":"J Andr\u00e9","year":"2012","journal-title":"Journal of Computer-Aided Molecular Design"},{"issue":"49","key":"ref22","doi-asserted-by":"crossref","first-page":"17036","DOI":"10.1021\/ja506385p","article-title":"Tubulin Bond Energies and Microtubule Biomechanics Determined from Nanoindentation in Silico","volume":"136","author":"O Kononova","year":"2014","journal-title":"Journal of the American Chemical Society"},{"issue":"3","key":"ref23","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1016\/j.bpj.2014.05.047","article-title":"Analysis of the Strength of Interfacial Hydrogen Bonds between Tubulin Dimers Using Quantum Theory of Atoms in Molecules","volume":"107","author":"AT Ayoub","year":"2014","journal-title":"Biophysical Journal"},{"issue":"2","key":"ref24","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/j.bpj.2010.04.038","article-title":"Mechanical properties of a complete microtubule revealed through molecular dynamics simulation","volume":"99","author":"DB Wells","year":"2010","journal-title":"Biophysical Journal"},{"issue":"10","key":"ref25","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1016\/S0969-2126(02)00827-4","article-title":"Microtubule structure at 8 \u00c5 resolution","volume":"10","author":"H Li","year":"2002","journal-title":"Structure"},{"issue":"5","key":"ref26","first-page":"1045","article-title":"Downing KH","volume":"313","author":"J L\u00f6we","year":"2001","journal-title":"Journal of Molecular Biology"},{"issue":"1","key":"ref27","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1021\/ci100275a","article-title":"Assessing the Performance of the MM\/PBSA and MM\/GBSA Methods. 1. The Accuracy of Binding Free Energy Calculations Based on Molecular Dynamics Simulations","volume":"51","author":"T Hou","year":"2011","journal-title":"Journal of Chemical Information and Modeling"},{"issue":"1","key":"ref28","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/S0092-8674(00)80961-7","article-title":"High-Resolution Model of the Microtubule","volume":"96","author":"E Nogales","year":"1999","journal-title":"Cell"},{"issue":"9","key":"ref29","doi-asserted-by":"crossref","first-page":"5312","DOI":"10.1073\/pnas.051309398","article-title":"The binding conformation of Taxol in <italic>\u03b2<\/italic>-tubulin: A model based on electron crystallographic density","volume":"98","author":"JP Snyder","year":"2001","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"36","key":"ref30","doi-asserted-by":"crossref","first-page":"17278","DOI":"10.1016\/S0021-9258(18)45374-4","article-title":"Mg<sup>2+<\/sup> dependence of guanine nucleotide binding to tubulin","volume":"262","author":"JJ Correia","year":"1987","journal-title":"Journal of Biological Chemistry"},{"issue":"21","key":"ref31","doi-asserted-by":"crossref","first-page":"4567","DOI":"10.1021\/bi00692a002","article-title":"Magnesium-induced self-association of calf brain tubulin. II","volume":"14","author":"RP Frigon","year":"1975","journal-title":"Thermodynamics. Biochemistry"},{"issue":"3","key":"ref32","doi-asserted-by":"crossref","first-page":"1464","DOI":"10.1016\/S0006-291X(88)81306-8","article-title":"Fast disassembly of microtubules induced by Mg<sup>2+<\/sup> or Ca<sup>2+<\/sup>","volume":"155","author":"V Gal","year":"1988","journal-title":"Biochemical and Biophysical Research Communications"},{"issue":"28","key":"ref33","doi-asserted-by":"crossref","first-page":"6648","DOI":"10.1021\/bi00480a014","article-title":"Effects of magnesium on the dynamic instability of individual microtubules","volume":"29","author":"ET O\u2019Brien","year":"1990","journal-title":"Biochemistry"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1038\/ncomms4094","article-title":"Ectopic A-lattice seams destabilize microtubules","volume":"5","author":"M Katsuki","year":"2014","journal-title":"Nature Communications"},{"key":"ref35","unstructured":"Molecular Operating Environment (MOE); 2012. Chemical Computing Group Inc., 1010 Sherbooke St. West, Suite #910, Montreal, QC, Canada, H3A 2R7."},{"issue":"6681","key":"ref36","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1038\/30288","article-title":"Structure of the alpha beta tubulin dimer by electron crystallography","volume":"393","author":"E Nogales","year":"1998","journal-title":"Nature"},{"key":"ref37","article-title":"AMBER 12","author":"D Case","year":"2012"},{"issue":"19","key":"ref38","doi-asserted-by":"crossref","first-page":"5179","DOI":"10.1021\/ja00124a002","article-title":"A second generation force field for the simulation of proteins, nucleic acids, and organic molecules","volume":"117","author":"WD Cornell","year":"1995","journal-title":"Journal of the American Chemical Society"},{"issue":"3","key":"ref39","doi-asserted-by":"crossref","first-page":"712","DOI":"10.1002\/prot.21123","article-title":"Comparison of multiple Amber force fields and development of improved protein backbone parameters","volume":"65","author":"V Hornak","year":"2006","journal-title":"Proteins: Structure, Function, and Bioinformatics"},{"issue":"9","key":"ref40","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1002\/jcc.10262","article-title":"Development of polyphosphate parameters for use with the AMBER force field","volume":"24","author":"KL Meagher","year":"2003","journal-title":"Journal of Computational Chemistry"},{"issue":"9","key":"ref41","doi-asserted-by":"crossref","first-page":"3878","DOI":"10.1021\/ct400314y","article-title":"Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit solvent Particle Mesh Ewald","volume":"9","author":"R Salomon-Ferrer","year":"2013","journal-title":"Journal of Chemical Theory and Computation"},{"issue":"5","key":"ref42","doi-asserted-by":"crossref","first-page":"1542","DOI":"10.1021\/ct200909j","article-title":"Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 1. Generalized Born","volume":"8","author":"AW G\u00f6tz","year":"2012","journal-title":"Journal of Chemical Theory and Computation"},{"issue":"2","key":"ref43","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1016\/j.cpc.2012.09.022","article-title":"SPFP: Speed without compromise\u2014A mixed precision model for GPU accelerated molecular dynamics simulations","volume":"184","author":"SL Grand","year":"2013","journal-title":"Computer Physics Communications"},{"issue":"7","key":"ref44","doi-asserted-by":"crossref","first-page":"3084","DOI":"10.1021\/ct400341p","article-title":"PTRAJ and CPPTRAJ: Software for Processing and Analysis of Molecular Dynamics Trajectory Data","volume":"9","author":"DR Roe","year":"2013","journal-title":"Journal of Chemical Theory and Computation"},{"issue":"9","key":"ref45","doi-asserted-by":"crossref","first-page":"3314","DOI":"10.1021\/ct300418h","article-title":"MMPBSA.py: An Efficient Program for End-State Free Energy Calculations","volume":"8","author":"BR Miller","year":"2012","journal-title":"Journal of Chemical Theory and Computation"},{"issue":"1","key":"ref46","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/0263-7855(96)00018-5","article-title":"VMD: Visual molecular dynamics","volume":"14","author":"W Humphrey","year":"1996","journal-title":"Journal of Molecular Graphics"},{"issue":"12","key":"ref47","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1021\/ar000033j","article-title":"Calculating Structures and Free Energies of Complex Molecules: Combining Molecular Mechanics and Continuum Models","volume":"33","author":"PA Kollman","year":"2000","journal-title":"Accounts of Chemical Research"}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pcbi.1004313","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,10]],"date-time":"2022-05-10T13:26:59Z","timestamp":1652189219000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1004313"}},"subtitle":[],"editor":[{"given":"James M.","family":"Briggs","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2015,6,1]]},"references-count":47,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2015,6,1]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1004313","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,6,1]]}}}