{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T05:14:46Z","timestamp":1789103686875,"version":"build-2803163510"},"reference-count":48,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2020,6,1]],"date-time":"2020-06-01T00:00:00Z","timestamp":1590969600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2020,6,1]],"date-time":"2020-06-01T00:00:00Z","timestamp":1590969600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"funder":[{"DOI":"10.13039\/501100005010","name":"Associazione Italiana per la Ricerca sul Cancro","doi-asserted-by":"publisher","award":["IG20719"],"award-info":[{"award-number":["IG20719"]}],"id":[{"id":"10.13039\/501100005010","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001732","name":"Danmarks Grundforskningsfond","doi-asserted-by":"publisher","award":["DNRF125"],"award-info":[{"award-number":["DNRF125"]}],"id":[{"id":"10.13039\/501100001732","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001943","name":"Partnership for Advanced Computing in Europe AISBL","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001943","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Biochemical Pharmacology"],"published-print":{"date-parts":[[2020,6]]},"DOI":"10.1016\/j.bcp.2020.113869","type":"journal-article","created":{"date-parts":[[2020,2,21]],"date-time":"2020-02-21T02:29:38Z","timestamp":1582252178000},"page":"113869","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":32,"special_numbering":"C","title":["S-nitrosylation affects TRAP1 structure and ATPase activity and modulates cell response to apoptotic stimuli"],"prefix":"10.1016","volume":"176","author":[{"given":"Fiorella","family":"Faienza","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matteo","family":"Lambrughi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Salvatore","family":"Rizza","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Pecorari","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paola","family":"Giglio","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan","family":"Salamanca Viloria","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Francesca","family":"Allega","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giovanni","family":"Chiappetta","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jo\u00eblle","family":"Vinh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesca","family":"Pacello","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea","family":"Battistoni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea","family":"Rasola","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena","family":"Papaleo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppe","family":"Filomeni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.bcp.2020.113869_b0005","doi-asserted-by":"crossref","first-page":"3574","DOI":"10.1074\/jbc.270.8.3574","article-title":"Identification of a protein with homology to hsp90 that binds the type 1 tumor necrosis factor receptor","volume":"270","author":"Song","year":"1995","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.bcp.2020.113869_b0010","doi-asserted-by":"crossref","first-page":"11677","DOI":"10.1074\/jbc.M709516200","article-title":"The ATPase cycle of the mitochondrial Hsp90 analog Trap1 *","volume":"283","author":"Leskovar","year":"2008","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.bcp.2020.113869_b0015","doi-asserted-by":"crossref","first-page":"1","DOI":"10.5483\/BMBRep.2012.45.1.1","article-title":"TRAP1 regulation of mitochondrial life or death decision in cancer cells and mitochondria-targeted TRAP1 inhibitors","volume":"45","author":"Kang","year":"2012","journal-title":"BMB Rep."},{"key":"10.1016\/j.bcp.2020.113869_b0020","article-title":"The mitochondrial HSP90 paralog TRAP1 forms an OXPHOS-regulated tetramer and is involved in maintaining mitochondrial metabolic homeostasis","volume":"679431","author":"Joshi","year":"2019","journal-title":"BioRxiv"},{"key":"10.1016\/j.bcp.2020.113869_b0025","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/j.molcel.2013.12.023","article-title":"Structural asymmetry in the closed state of mitochondrial Hsp90 (TRAP1) supports a two-step ATP hydrolysis mechanism","volume":"53","author":"Lavery","year":"2014","journal-title":"Mol. Cell."},{"key":"10.1016\/j.bcp.2020.113869_b0030","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fonc.2017.00058","article-title":"The chaperone TRAP1 as a modulator of the mitochondrial adaptations in cancer cells","volume":"7","author":"Masgras","year":"2017","journal-title":"Front. Oncol."},{"key":"10.1016\/j.bcp.2020.113869_b0035","first-page":"1","article-title":"A novel N-terminal extension in mitochondrial TRAP1 serves as a thermal regulator of chaperone activity","author":"Partridge","year":"2014","journal-title":"Elife"},{"key":"10.1016\/j.bcp.2020.113869_b0040","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/j.molcel.2013.12.023","article-title":"Article structural asymmetry in the closed state a two-step ATP hydrolysis mechanism","volume":"53","author":"Lavery","year":"2014","journal-title":"Mol. Cell."},{"key":"10.1016\/j.bcp.2020.113869_b0045","doi-asserted-by":"crossref","first-page":"2952","DOI":"10.1073\/pnas.1516167113","article-title":"Mitochondrial Hsp90 is a ligand-activated molecular chaperone coupling ATP binding to dimer closure through a coiled-coil intermediate","volume":"113","author":"Sung","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.bcp.2020.113869_b0050","doi-asserted-by":"crossref","first-page":"e25235","DOI":"10.7554\/eLife.25235","article-title":"Symmetry broken and rebroken during the ATP hydrolysis cycle of the mitochondrial Hsp90 TRAP1","volume":"6","author":"Elnatan","year":"2017","journal-title":"Elife"},{"key":"10.1016\/j.bcp.2020.113869_b0055","doi-asserted-by":"crossref","first-page":"E1604","DOI":"10.1073\/pnas.1220659110","article-title":"Molecular chaperone TRAP1 regulates a metabolic switch between mitochondrial respiration and aerobic glycolysis","volume":"110","author":"Yoshida","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.bcp.2020.113869_b0060","doi-asserted-by":"crossref","first-page":"969","DOI":"10.3892\/ijo.2014.2530","article-title":"TRAP1 revisited: novel localizations and functions of a \u201cnext-generation\u201d biomarker (Review)","volume":"45","author":"Amoroso","year":"2014","journal-title":"Int. J. Oncol."},{"key":"10.1016\/j.bcp.2020.113869_b0065","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1016\/j.tcb.2014.03.005","article-title":"Mitochondrial oxidative phosphorylation TRAP(1)ped in tumor cells","volume":"24","author":"Rasola","year":"2014","journal-title":"Trends Cell Biol."},{"key":"10.1016\/j.bcp.2020.113869_b0070","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1016\/j.ccr.2012.07.015","article-title":"Control of tumor bioenergetics and survival stress signaling by mitochondrial HSP90s","volume":"22","author":"Chae","year":"2012","journal-title":"Cancer Cell."},{"key":"10.1016\/j.bcp.2020.113869_b0075","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.canlet.2009.01.018","article-title":"TRAP1, a novel mitochondrial chaperone responsible for multi-drug resistance and protection from apoptotis in human colorectal carcinoma cells","volume":"279","author":"Costantino","year":"2009","journal-title":"Cancer Lett."},{"key":"10.1016\/j.bcp.2020.113869_b0080","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.cell.2007.08.028","article-title":"Regulation of tumor cell mitochondrial homeostasis by an organelle-specific Hsp90 chaperone network","volume":"131","author":"Kang","year":"2007","journal-title":"Cell."},{"key":"10.1016\/j.bcp.2020.113869_b0085","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1016\/j.cmet.2013.04.019","article-title":"The mitochondrial chaperone TRAP1 promotes neoplastic growth by inhibiting succinate dehydrogenase","volume":"17","author":"Sciacovelli","year":"2013","journal-title":"Cell Metab."},{"key":"10.1016\/j.bcp.2020.113869_b0090","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.ccr.2004.11.022","article-title":"Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-\u03b1 prolyl hydroxylase","volume":"7","author":"Selak","year":"2005","journal-title":"Cancer Cell."},{"key":"10.1016\/j.bcp.2020.113869_b0095","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1371\/journal.pbio.0050172","article-title":"PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1","volume":"5","author":"Pridgeon","year":"2007","journal-title":"PLoS Biol."},{"key":"10.1016\/j.bcp.2020.113869_b0100","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1016\/j.celrep.2016.12.056","article-title":"Absence of neurofibromin induces an oncogenic metabolic switch via mitochondrial ERK-mediated phosphorylation of the chaperone TRAP1","volume":"18","author":"Masgras","year":"2017","journal-title":"Cell Rep."},{"key":"10.1016\/j.bcp.2020.113869_b0105","doi-asserted-by":"crossref","first-page":"1369","DOI":"10.1158\/0008-5472.CAN-18-2558","article-title":"Interplay between TRAP1 and sirtuin-3 modulates mitochondrial respiration and oxidative stress to maintain stemness of glioma stem cells","volume":"79","author":"Park","year":"2019","journal-title":"Cancer Res."},{"key":"10.1016\/j.bcp.2020.113869_b0110","doi-asserted-by":"crossref","first-page":"4170","DOI":"10.1158\/0008-5472.CAN-15-2637","article-title":"S-nitrosylation of the mitochondrial chaperone TRAP1 sensitizes hepatocellular carcinoma cells to inhibitors of succinate dehydrogenase","volume":"76","author":"Rizza","year":"2016","journal-title":"Cancer Res."},{"key":"10.1016\/j.bcp.2020.113869_b0115","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1021\/acs.jctc.7b00766","article-title":"The structural asymmetry of mitochondrial Hsp90 (Trap1) determines fine tuning of functional dynamics","volume":"14","author":"Moroni","year":"2018","journal-title":"J. Chem. Theory Comput."},{"key":"10.1016\/j.bcp.2020.113869_b0120","first-page":"5.6.1","article-title":"Comparative protein structure modeling using modeller","volume":"54","author":"Webb","year":"2016","journal-title":"Curr. Protoc. Bioinforma."},{"key":"10.1016\/j.bcp.2020.113869_b0125","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1038\/nature04105","article-title":"Intrinsic dynamics of an enzyme underlies catalysis","volume":"438","author":"Eisenmesser","year":"2005","journal-title":"Nature"},{"key":"10.1016\/j.bcp.2020.113869_b0130","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1038\/nchembio.2212","article-title":"Conformational footprints","volume":"12","author":"Ma","year":"2016","journal-title":"Nat. Chem. Biol."},{"key":"10.1016\/j.bcp.2020.113869_b0135","doi-asserted-by":"crossref","first-page":"W422","DOI":"10.1093\/nar\/gkt416","article-title":"Vienna-PTM web server: a toolkit for MD simulations of protein post-translational modifications","volume":"41","author":"Margreitter","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.bcp.2020.113869_b0140","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1021\/ct700301q","article-title":"GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation","volume":"4","author":"Hess","year":"2008","journal-title":"J. Chem. Theory Comput."},{"key":"10.1016\/j.bcp.2020.113869_b0145","first-page":"LP-E4766","article-title":"Developing a molecular dynamics force field for both folded and disordered protein states","volume":"E4758","author":"Robustelli","year":"2018","journal-title":"Proc. Natl. Acad. Sci. 115"},{"key":"10.1016\/j.bcp.2020.113869_b0150","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1007\/s00249-011-0700-9","article-title":"Definition and testing of the GROMOS force-field versions 54A7 and 54B7","volume":"40","author":"Schmid","year":"2011","journal-title":"Eur. Biophys. J."},{"key":"10.1016\/j.bcp.2020.113869_b0155","doi-asserted-by":"crossref","first-page":"e1003154","DOI":"10.1371\/journal.pcbi.1003154","article-title":"A Systematic framework for molecular dynamics simulations of protein post-translational modifications","volume":"9","author":"Petrov","year":"2013","journal-title":"PLOS Comput. Biol."},{"key":"10.1016\/j.bcp.2020.113869_b0160","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1016\/j.bbrc.2008.10.017","article-title":"Force field parameters for S-nitrosocysteine and molecular dynamics simulations of S-nitrosated thioredoxin","volume":"377","author":"Han","year":"2008","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"10.1016\/j.bcp.2020.113869_b0165","doi-asserted-by":"crossref","first-page":"W522","DOI":"10.1093\/nar\/gkm276","article-title":"PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations","volume":"35","author":"Dolinsky","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.bcp.2020.113869_b0170","doi-asserted-by":"crossref","first-page":"1537","DOI":"10.1021\/ci400639r","article-title":"PyInteraph: a framework for the analysis of interaction networks in structural ensembles of Proteins","volume":"54","author":"Tiberti","year":"2014","journal-title":"J. Chem. Inf. Model."},{"key":"10.1016\/j.bcp.2020.113869_b0175","article-title":"An optimal distance cutoff for contact-based protein structure networks using side-chain centers of mass","volume":"2838","author":"Salamanca Viloria","year":"2017","journal-title":"Sci. Rep. 7"},{"key":"10.1016\/j.bcp.2020.113869_b0180","doi-asserted-by":"crossref","first-page":"28","DOI":"10.3389\/fmolb.2015.00028","article-title":"Integrating atomistic molecular dynamics simulations, experiments, and network analysis to study protein dynamics: strength in unity","volume":"2","author":"Papaleo","year":"2015","journal-title":"Front. Mol. Biosci."},{"key":"10.1016\/j.bcp.2020.113869_b0185","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/S0022-2836(02)00442-4","article-title":"Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations","volume":"320","author":"Guerois","year":"2002","journal-title":"J. Mol. Biol."},{"key":"10.1016\/j.bcp.2020.113869_b0190","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1002\/prot.340170408","article-title":"Essential dynamics of proteins","volume":"17","author":"Amadei","year":"1993","journal-title":"Proteins Struct. Funct. Bioinforma."},{"key":"10.1016\/j.bcp.2020.113869_b0195","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0021-9258(19)52451-6","article-title":"Protein measurement with the folin phenol reagent","volume":"193","author":"Lowry","year":"1951","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.bcp.2020.113869_b0200","doi-asserted-by":"crossref","first-page":"e49138","DOI":"10.7554\/eLife.49138","article-title":"Computational and cellular studies reveal structural destabilization and degradation of MLH1 variants in Lynch syndrome","volume":"8","author":"Abildgaard","year":"2019","journal-title":"Elife"},{"key":"10.1016\/j.bcp.2020.113869_b0205","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1002\/humu.23707","article-title":"Toward mechanistic models for genotype\u2013phenotype correlations in phenylketonuria using protein stability calculations","volume":"40","author":"Scheller","year":"2019","journal-title":"Hum. Mutat."},{"key":"10.1016\/j.bcp.2020.113869_b0210","doi-asserted-by":"crossref","first-page":"e1006739","DOI":"10.1371\/journal.pgen.1006739","article-title":"Predicting the impact of Lynch syndrome-causing missense mutations from structural calculations","volume":"13","author":"Nielsen","year":"2017","journal-title":"PLOS Genet."},{"key":"10.1016\/j.bcp.2020.113869_b0215","doi-asserted-by":"crossref","first-page":"6577","DOI":"10.1158\/0008-5472.CAN-10-1256","article-title":"Mitochondrial chaperone trap1 and the calcium binding protein sorcin interact and protect cells against apoptosis induced by antiblastic agents","volume":"70","author":"Landriscina","year":"2010","journal-title":"Cancer Res."},{"key":"10.1016\/j.bcp.2020.113869_b0220","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s40001-019-0365-x","article-title":"Staurosporine induces apoptosis in pancreatic carcinoma cells PaTu 8988t and Panc-1 via the intrinsic signaling pathway","volume":"24","author":"Malsy","year":"2019","journal-title":"Eur. J. Med. Res."},{"key":"10.1016\/j.bcp.2020.113869_b0225","doi-asserted-by":"crossref","first-page":"3250","DOI":"10.1096\/fj.10-177527","article-title":"Triggering of a novel intrinsic apoptosis pathway by the kinase inhibitor staurosporine: activation of caspase-9 in the absence of Apaf-1","volume":"25","author":"Manns","year":"2011","journal-title":"FASEB J."},{"key":"10.1016\/j.bcp.2020.113869_b0230","first-page":"899","article-title":"Dynamics-based community analysis and perturbation response scanning of allosteric interaction networks in the TRAP1 chaperone structures dissect molecular linkage between conformational asymmetry and sequential ATP hydrolysis","volume":"2018","author":"Verkhivker","year":"1866","journal-title":"Biochim. Biophys. Acta - Proteins Proteomics"},{"key":"10.1016\/j.bcp.2020.113869_b0235","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1089\/ars.2017.7403","article-title":"Protein S-nitrosylation: determinants of specificity and enzymatic regulation of S-nitrosothiol-based signaling","volume":"30","author":"Stomberski","year":"2019","journal-title":"Antioxid. Redox Signal."},{"issue":"6080","key":"10.1016\/j.bcp.2020.113869_b0240","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1126\/science.1215643","article-title":"Endogenous protein S-nitrosylation in E. coli: regulation by OxyR","volume":"336","author":"Seth","year":"2012","journal-title":"Science"}],"container-title":["Biochemical Pharmacology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0006295220300976?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0006295220300976?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,11,2]],"date-time":"2025-11-02T15:05:33Z","timestamp":1762095933000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0006295220300976"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6]]},"references-count":48,"alternative-id":["S0006295220300976"],"URL":"https:\/\/doi.org\/10.1016\/j.bcp.2020.113869","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/859629","asserted-by":"object"}]},"ISSN":["0006-2952"],"issn-type":[{"value":"0006-2952","type":"print"}],"subject":[],"published":{"date-parts":[[2020,6]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"S-nitrosylation affects TRAP1 structure and ATPase activity and modulates cell response to apoptotic stimuli","name":"articletitle","label":"Article Title"},{"value":"Biochemical Pharmacology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.bcp.2020.113869","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2020 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}],"article-number":"113869"}}