{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T18:32:06Z","timestamp":1786991526895,"version":"build-2736575974"},"reference-count":45,"publisher":"Elsevier BV","issue":"6","license":[{"start":{"date-parts":[[2025,6,1]],"date-time":"2025-06-01T00:00:00Z","timestamp":1748736000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2025,6,1]],"date-time":"2025-06-01T00:00:00Z","timestamp":1748736000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2025,5,20]],"date-time":"2025-05-20T00:00:00Z","timestamp":1747699200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"publisher","award":["178282"],"award-info":[{"award-number":["178282"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100023695","name":"Metabolomics Innovation Centre","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100023695","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000190","name":"University of Alberta","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000190","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["2022-03638"],"award-info":[{"award-number":["2022-03638"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["2019-04967"],"award-info":[{"award-number":["2019-04967"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["jbc.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Journal of Biological Chemistry"],"published-print":{"date-parts":[[2025,6]]},"DOI":"10.1016\/j.jbc.2025.110262","type":"journal-article","created":{"date-parts":[[2025,5,21]],"date-time":"2025-05-21T19:35:45Z","timestamp":1747856145000},"page":"110262","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":4,"title":["Symmetric stimulation of Hsp90 catalyzed ATP hydrolysis through enhanced active site gate dynamics"],"prefix":"10.1016","volume":"301","author":[{"given":"Breanna","family":"Magnan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Dumont","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Suad","family":"Rashid","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"LaPointe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leo","family":"Spyracopoulos","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.jbc.2025.110262_bib1","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1038\/nrm.2017.20","article-title":"The HSP90 chaperone machinery","volume":"18","author":"Schopf","year":"2017","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.jbc.2025.110262_bib2","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1002\/bip.22835","article-title":"Review: the HSP90 molecular chaperone\u2014an enigmatic ATPase","volume":"105","author":"Pearl","year":"2016","journal-title":"Biopolymers"},{"key":"10.1016\/j.jbc.2025.110262_bib3","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1038\/nature10317","article-title":"Molecular chaperones in protein folding and proteostasis","volume":"475","author":"Hartl","year":"2011","journal-title":"Nature"},{"key":"10.1016\/j.jbc.2025.110262_bib4","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a034017","article-title":"Structure, function, and regulation of the Hsp90 machinery","volume":"11","author":"Biebl","year":"2019","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"10.1016\/j.jbc.2025.110262_bib5","doi-asserted-by":"crossref","first-page":"39303","DOI":"10.1074\/jbc.M305751200","article-title":"Dissection of the contribution of individual domains to the ATPase mechanism of Hsp90","volume":"278","author":"Wegele","year":"2003","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.jbc.2025.110262_bib6","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1038\/nsmb.1565","article-title":"Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90","volume":"16","author":"Hessling","year":"2009","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.jbc.2025.110262_bib7","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1016\/j.bbamcr.2011.07.020","article-title":"The \u2018active life\u2019 of Hsp90 complexes","volume":"1823","author":"Prodromou","year":"2012","journal-title":"Biochim. Biophys. Acta Mol. Cell Res."},{"key":"10.1016\/j.jbc.2025.110262_bib8","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1017\/S0033583510000314","article-title":"Conformational dynamics of the molecular chaperone Hsp90","volume":"44","author":"Krukenberg","year":"2011","journal-title":"Q. Rev. Biophys."},{"key":"10.1016\/j.jbc.2025.110262_bib9","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1093\/abbs\/gms001","article-title":"Structure insights into mechanisms of ATP hydrolysis and the activation of human heat-shock protein 90","volume":"44","author":"Li","year":"2012","journal-title":"Acta Biochim. Biophys. Sin. (Shanghai)."},{"key":"10.1016\/j.jbc.2025.110262_bib10","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1038\/nature04716","article-title":"Crystal structure of an Hsp90\u2013nucleotide\u2013p23\/Sba1 closed chaperone complex","volume":"440","author":"Ali","year":"2006","journal-title":"Nature"},{"key":"10.1016\/j.jbc.2025.110262_bib11","doi-asserted-by":"crossref","first-page":"33689","DOI":"10.1074\/jbc.M103832200","article-title":"Coordinated ATP hydrolysis by the Hsp90 dimer","volume":"276","author":"Richter","year":"2001","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.jbc.2025.110262_bib12","doi-asserted-by":"crossref","first-page":"1375","DOI":"10.1016\/j.bpj.2016.08.023","article-title":"Single-molecule analysis beyond dwell times: demonstration and assessment in and out of equilibrium","volume":"111","author":"Schmid","year":"2016","journal-title":"Biophys. J."},{"key":"10.1016\/j.jbc.2025.110262_bib13","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1038\/nchembio.2111","article-title":"Cooperation of local motions in the Hsp90 molecular chaperone ATPase mechanism","volume":"12","author":"Schulze","year":"2016","journal-title":"Nat. Chem. Biol."},{"key":"10.1016\/j.jbc.2025.110262_bib14","doi-asserted-by":"crossref","first-page":"1869","DOI":"10.1021\/acs.biochem.9b00144","article-title":"The Hsp90 chaperone: 1H and 19F dynamic nuclear magnetic resonance spectroscopy reveals a perfect enzyme","volume":"58","author":"Lee","year":"2019","journal-title":"Biochemistry"},{"key":"10.1016\/j.jbc.2025.110262_bib15","doi-asserted-by":"crossref","first-page":"8388","DOI":"10.1021\/acs.jpcb.4c03363","article-title":"Asymmetric dynamics drive catalytic activation of the Hsp90 chaperone","volume":"128","author":"Magnan","year":"2024","journal-title":"J. Phys. Chem. B."},{"key":"10.1016\/j.jbc.2025.110262_bib16","doi-asserted-by":"crossref","first-page":"44905","DOI":"10.1074\/jbc.M208457200","article-title":"N-terminal residues regulate the catalytic efficiency of the Hsp90 ATPase cycle","volume":"277","author":"Richter","year":"2002","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.jbc.2025.110262_bib17","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.molcel.2010.01.006","article-title":"Asymmetric activation of the Hsp90 dimer by its cochaperone Aha1","volume":"37","author":"Retzlaff","year":"2010","journal-title":"Mol. Cell."},{"key":"10.1016\/j.jbc.2025.110262_bib18","doi-asserted-by":"crossref","first-page":"21170","DOI":"10.1074\/jbc.M800046200","article-title":"Intra- and intermonomer interactions are required to synergistically facilitate ATP hydrolysis in Hsp90","volume":"283","author":"Cunningham","year":"2008","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.jbc.2025.110262_bib19","doi-asserted-by":"crossref","first-page":"4383","DOI":"10.1093\/emboj\/19.16.4383","article-title":"The ATPase cycle of Hsp90 drives a molecular clamp\u2019 via transient dimerization of the N-terminal domains","volume":"19","author":"Prodromou","year":"2000","journal-title":"EMBO J."},{"key":"10.1016\/j.jbc.2025.110262_bib20","doi-asserted-by":"crossref","DOI":"10.1002\/pro.5255","article-title":"Ordered ATP hydrolysis in the Hsp90 chaperone is regulated by Aha1 and a conserved post-translational modification","volume":"34","author":"Amoah","year":"2025","journal-title":"Protein Sci."},{"key":"10.1016\/j.jbc.2025.110262_bib21","doi-asserted-by":"crossref","first-page":"11301","DOI":"10.1074\/jbc.M510142200","article-title":"Intrinsic inhibition of the Hsp90 ATPase activity","volume":"281","author":"Richter","year":"2006","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.jbc.2025.110262_bib22","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1038\/nsb0697-477","article-title":"A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone","volume":"4","author":"Prodromou","year":"1997","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.jbc.2025.110262_bib23","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-019-09299-3","article-title":"The conserved NxNNWHW motif in Aha-type co-chaperones modulates the kinetics of Hsp90 ATPase stimulation","volume":"10","author":"Mercier","year":"2019","journal-title":"Nat. Commun."},{"key":"10.1016\/j.jbc.2025.110262_bib24","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1083\/jcb.143.4.901","article-title":"In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis","volume":"143","author":"Obermann","year":"1998","journal-title":"J. Cell Biol."},{"key":"10.1016\/j.jbc.2025.110262_bib25","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1016\/S1097-2765(02)00785-2","article-title":"Activation of the ATPase activity of Hsp90 by the stress-regulated cochaperone Aha1","volume":"10","author":"Panaretou","year":"2002","journal-title":"Mol. Cell."},{"key":"10.1016\/j.jbc.2025.110262_bib26","article-title":"Cryo-EM structures reveal a multistep mechanism of Hsp90 activation by co-chaperone Aha1","author":"Liu","year":"2020","journal-title":"bioRxiv"},{"key":"10.1016\/j.jbc.2025.110262_bib27","doi-asserted-by":"crossref","first-page":"1402","DOI":"10.1038\/sj.emboj.7600141","article-title":"Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery","volume":"23","author":"Meyer","year":"2004","journal-title":"EMBO J."},{"key":"10.1016\/j.jbc.2025.110262_bib28","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/S0065-3233(08)60460-X","article-title":"Stability of proteins small globular proteins","volume":"33","author":"Privalov","year":"1979","journal-title":"Adv. Protein Chem."},{"key":"10.1016\/j.jbc.2025.110262_bib29","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/S0065-3233(08)60548-3","article-title":"Energetics of protein structure","volume":"47","author":"Makhatadze","year":"1995","journal-title":"Adv. Protein Chem."},{"key":"10.1016\/j.jbc.2025.110262_bib30","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/0014-5793(93)81405-O","article-title":"Protein folding and stability: the pathway of folding of barnase","volume":"325","author":"Fersht","year":"1993","journal-title":"FEBS Lett."},{"key":"10.1016\/j.jbc.2025.110262_bib31","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/j.molcel.2010.01.005","article-title":"Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function","volume":"37","author":"Mollapour","year":"2010","journal-title":"Mol. Cell."},{"key":"10.1016\/j.jbc.2025.110262_bib32","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1016\/j.molcel.2011.02.011","article-title":"Threonine 22 phosphorylation attenuates Hsp90 interaction with cochaperones and affects its chaperone activity","volume":"41","author":"Mollapour","year":"2011","journal-title":"Mol. Cell"},{"key":"10.1016\/j.jbc.2025.110262_bib33","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1016\/j.molcel.2012.05.015","article-title":"Dynamic tyrosine phosphorylation modulates cycling of the HSP90-P50CDC37-AHA1 chaperone machine","volume":"47","author":"Xu","year":"2012","journal-title":"Mol. Cell"},{"key":"10.1016\/j.jbc.2025.110262_bib34","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/j.molcel.2013.12.007","article-title":"Asymmetric Hsp90 N domain SUMOylation recruits Aha1 and ATP-competitive inhibitors","volume":"53","author":"Mollapour","year":"2014","journal-title":"Mol. Cell"},{"key":"10.1016\/j.jbc.2025.110262_bib35","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1515\/hsz-2018-0251","article-title":"A novel method for site-specific chemical SUMOylation: SUMOylation of Hsp90 modulates co-chaperone binding in vitro","volume":"400","author":"Wolmarans","year":"2019","journal-title":"Biol. Chem."},{"key":"10.1016\/j.jbc.2025.110262_bib36","doi-asserted-by":"crossref","first-page":"2984","DOI":"10.1021\/acs.jpcb.0c00626","article-title":"Nucleotide binding and active site gate dynamics for the Hsp90 chaperone ATPase domain from benchtop and high field 19F NMR spectroscopy","volume":"124","author":"Rashid","year":"2020","journal-title":"J. Phys. Chem. B."},{"key":"10.1016\/j.jbc.2025.110262_bib37","doi-asserted-by":"crossref","first-page":"3665","DOI":"10.1021\/acs.jpcb.9b01741","article-title":"Side-chain dynamics of the trifluoroacetone cysteine derivative characterized by 19F NMR relaxation and molecular dynamics simulations","volume":"123","author":"Rashid","year":"2019","journal-title":"J. Phys. Chem. B."},{"key":"10.1016\/j.jbc.2025.110262_bib38","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1007\/BF00197809","article-title":"NMRPipe: a multidimensional spectral processing system based on UNIX pipes","volume":"6","author":"Delaglio","year":"1995","journal-title":"J. Biomol. NMR"},{"key":"10.1016\/j.jbc.2025.110262_bib39","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1063\/1.1734254","article-title":"Nuclear magnetic resonance study of the protolysis of trimethylammonium ion in aqueous solution\u2014order of the reaction with respect to solvent","volume":"39","author":"Luz","year":"1963","journal-title":"J. Chem. Phys."},{"key":"10.1016\/j.jbc.2025.110262_bib40","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1103\/PhysRev.70.460","article-title":"Nuclear induction","volume":"70","author":"Bloch","year":"1946","journal-title":"Phys. Rev."},{"key":"10.1016\/j.jbc.2025.110262_bib41","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1063\/1.1744152","article-title":"Reaction rates by nuclear magnetic resonance","volume":"28","author":"McConnell","year":"1958","journal-title":"J. Chem. Phys."},{"key":"10.1016\/j.jbc.2025.110262_bib42","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1002\/9780470147122.ch2","article-title":"The study of intramolecular rate processes by dynamic nuclear magnetic resonance","volume":"3","author":"Binsch","year":"1968","journal-title":"Top. Stereochem."},{"key":"10.1016\/j.jbc.2025.110262_bib43","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":"Cornell","year":"1995","journal-title":"J. Am. Chem. Soc."},{"key":"10.1016\/j.jbc.2025.110262_bib44","doi-asserted-by":"crossref","first-page":"3863","DOI":"10.1021\/jz501780a","article-title":"Building water models: a different approach","volume":"5","author":"Izadi","year":"2014","journal-title":"J. Phys. Chem. Lett."},{"key":"10.1016\/j.jbc.2025.110262_bib45","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1006\/jmbi.1995.0514","article-title":"Fluctuation and cross-correlation analysis of protein motions observed in nanosecond molecular dynamics simulations","volume":"252","author":"H\u00fcnenberger","year":"1995","journal-title":"J. Mol. Biol."}],"container-title":["Journal of Biological Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S002192582502112X?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S002192582502112X?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,30]],"date-time":"2025-10-30T16:24:35Z","timestamp":1761841475000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S002192582502112X"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6]]},"references-count":45,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2025,6]]}},"alternative-id":["S002192582502112X"],"URL":"https:\/\/doi.org\/10.1016\/j.jbc.2025.110262","relation":{},"ISSN":["0021-9258"],"issn-type":[{"value":"0021-9258","type":"print"}],"subject":[],"published":{"date-parts":[[2025,6]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Symmetric stimulation of Hsp90 catalyzed ATP hydrolysis through enhanced active site gate dynamics","name":"articletitle","label":"Article Title"},{"value":"Journal of Biological Chemistry","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.jbc.2025.110262","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2025 The Authors. Published by Elsevier Inc on behalf of American Society for Biochemistry and Molecular Biology\u00e9","name":"copyright","label":"Copyright"}],"article-number":"110262"}}