{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,24]],"date-time":"2026-01-24T23:51:02Z","timestamp":1769298662403,"version":"3.49.0"},"reference-count":61,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2019,1,16]],"date-time":"2019-01-16T00:00:00Z","timestamp":1547596800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"},{"start":{"date-parts":[[2020,1,16]],"date-time":"2020-01-16T00:00:00Z","timestamp":1579132800000},"content-version":"am","delay-in-days":365,"URL":"http:\/\/rsc.li\/journals-terms-of-use"}],"funder":[{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T34 GM083688"],"award-info":[{"award-number":["T34 GM083688"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"crossref","award":["T34 GM083688"],"award-info":[{"award-number":["T34 GM083688"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["rsc.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2019,5,22]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Here, we report the preparation and photo-physical characterization of hexa-coordinated vertebrate globins, human neuroglobin (hNgb) and cytoglobin (hCygb), with the native iron protoporphyrin IX (FePPIX) cofactor replaced by a fluorescent isostructural analogue, zinc protoporphyrin IX (ZnPPIX). To facilitate insertion of ZnPPIX into hexa-coordinated globins, apoproteins prepared via butanone extraction were unfolded by the addition of GuHCl and subsequently slowly refolded in the presence of ZnPPIX. The absorption\/emission spectra of ZnPPIX reconstituted hCygb are similar to those observed for ZnPPIX reconstituted myoglobin whereas the absorption and emission spectra of ZnPPIX reconstituted hNgb are blue shifted by \u223c2 nm. Different steady state absorption and emission properties of ZnPPIX incorporated in hCygb and hNgb are consistent with distinct hydrogen bonding interactions between ZnPPIX and the globin matrix. The fluorescence lifetime of ZnPPIX in hexa-coordinated globins is bimodal pointing towards increased heterogeneity of the heme binding cavity in hCygb and hNgb. ZnPPIX reconstituted Ngb binds to cytochrome c with the same affinity as reported for the native protein, suggesting that fluorescent analogues of Cygb and Ngb can be readily employed to monitor interactions between vertebrate hexa-coordinated globins and other proteins.<\/jats:p>","DOI":"10.1039\/c8mt00332g","type":"journal-article","created":{"date-parts":[[2019,1,16]],"date-time":"2019-01-16T18:34:21Z","timestamp":1547663661000},"page":"906-913","update-policy":"https:\/\/doi.org\/10.1039\/rsc_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Utility of fluorescent heme analogue ZnPPIX to monitor conformational heterogeneity in vertebrate hexa-coordinated globins"],"prefix":"10.1093","volume":"11","author":[{"given":"Antonija","family":"Tangar","sequence":"first","affiliation":[{"name":"Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Val\u00e9rie","family":"Derrien","sequence":"additional","affiliation":[{"name":"Laboratoire de Chimie-Physique, CNRS, Universite Paris-Sud, Universit\u00e9 Paris Saclay, 91405 Orsay, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ruipeng","family":"Lei","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria Jose","family":"Santiago Estevez","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pierre","family":"Sebban","sequence":"additional","affiliation":[{"name":"Laboratoire de Chimie-Physique, CNRS, Universite Paris-Sud, Universit\u00e9 Paris Saclay, 91405 Orsay, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sophie","family":"Bernad","sequence":"additional","affiliation":[{"name":"Laboratoire de Chimie-Physique, CNRS, Universite Paris-Sud, Universit\u00e9 Paris Saclay, 91405 Orsay, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0385-9457","authenticated-orcid":false,"given":"Jaroslava","family":"Miksovska","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA"},{"name":"Biomolecular Sciences Institute, Florida International University, Miami, Florida 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2019,1,16]]},"reference":[{"key":"2021121516072922700_cit1","first-page":"146","volume":"7","author":"Baez","year":"2016","journal-title":"Front. Neurol. Neurosci."},{"key":"2021121516072922700_cit2","doi-asserted-by":"crossref","first-page":"6995","DOI":"10.3390\/ijms13066995","volume":"13","author":"Yu","year":"2012","journal-title":"Int. J. Mol. Sci."},{"key":"2021121516072922700_cit3","doi-asserted-by":"crossref","first-page":"15306","DOI":"10.1073\/pnas.251466698","volume":"98","author":"Sun","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2021121516072922700_cit4","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/978-0-387-75434-5_13","volume":"618","author":"Burmester","year":"2007","journal-title":"Adv. Exp. Med. Biol."},{"key":"2021121516072922700_cit5","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1124\/mol.112.083634","volume":"83","author":"Zhang","year":"2013","journal-title":"Mol. Pharmacol."},{"key":"2021121516072922700_cit6","doi-asserted-by":"crossref","first-page":"3869","DOI":"10.1007\/s00018-011-0764-9","volume":"68","author":"Oleksiewicz","year":"2011","journal-title":"Cell. Mol. Life Sci."},{"key":"2021121516072922700_cit7","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.niox.2017.11.004","volume":"72","author":"Reeder","year":"2018","journal-title":"Nitric oxide"},{"key":"2021121516072922700_cit8","doi-asserted-by":"crossref","first-page":"24990","DOI":"10.1038\/srep24990","volume":"6","author":"Thuyle","year":"2016","journal-title":"Sci. Rep."},{"key":"2021121516072922700_cit9","doi-asserted-by":"crossref","first-page":"18959","DOI":"10.1074\/jbc.M116.730176","volume":"291","author":"Trashin","year":"2016","journal-title":"J. Biol. Chem."},{"key":"2021121516072922700_cit10","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.niox.2013.03.008","volume":"32","author":"Singh","year":"2013","journal-title":"Nitric oxide"},{"key":"2021121516072922700_cit11","doi-asserted-by":"crossref","first-page":"51713","DOI":"10.1074\/jbc.M309396200","volume":"278","author":"Hamdane","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2021121516072922700_cit12","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.jinorgbio.2013.08.006","volume":"129","author":"Astudillo","year":"2013","journal-title":"J. Inorg. Biochem."},{"key":"2021121516072922700_cit13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jinorgbio.2017.11.003","volume":"179","author":"Hanai","year":"2018","journal-title":"J. Inorg. Biochem."},{"key":"2021121516072922700_cit14","doi-asserted-by":"crossref","first-page":"9735","DOI":"10.1021\/bi060716s","volume":"45","author":"Smagghe","year":"2006","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit15","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1002\/iub.446","volume":"63","author":"Merlino","year":"2011","journal-title":"IUBMB Life"},{"key":"2021121516072922700_cit16","doi-asserted-by":"crossref","first-page":"17351","DOI":"10.1073\/pnas.0407633101","volume":"101","author":"Vallone","year":"2004","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2021121516072922700_cit17","doi-asserted-by":"crossref","first-page":"9984","DOI":"10.1021\/bi301016u","volume":"51","author":"Astudillo","year":"2012","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit18","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1080\/15216540500037711","volume":"56","author":"Kiger","year":"2004","journal-title":"IUBMB Life"},{"key":"2021121516072922700_cit19","doi-asserted-by":"crossref","first-page":"5133","DOI":"10.1021\/bi027067e","volume":"42","author":"Sawai","year":"2003","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit20","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1002\/chem.201603421","volume":"23","author":"Vitagliano","year":"2017","journal-title":"Chemistry"},{"key":"2021121516072922700_cit21","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/0006-3002(59)90407-X","volume":"35","author":"Teale","year":"1959","journal-title":"Biochim. Biophys. Acta"},{"key":"2021121516072922700_cit22","doi-asserted-by":"crossref","first-page":"4573","DOI":"10.1016\/S0021-9258(18)93664-1","volume":"244","author":"Asakura","year":"1969","journal-title":"J. Biol. Chem."},{"key":"2021121516072922700_cit23","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1016\/j.jinorgbio.2007.03.009","volume":"101","author":"Belogortseva","year":"2007","journal-title":"J. Inorg. Biochem."},{"key":"2021121516072922700_cit24","doi-asserted-by":"crossref","first-page":"11138","DOI":"10.1039\/C5CC02680F","volume":"51","author":"Oohora","year":"2015","journal-title":"Chem. Commun."},{"key":"2021121516072922700_cit25","doi-asserted-by":"crossref","DOI":"10.1201\/b16502","volume-title":"Introduction to fluorescence","author":"Jameson","year":"2014","edition":"1st"},{"key":"2021121516072922700_cit26","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1111\/j.1432-1033.1987.tb10558.x","volume":"162","author":"Albani","year":"1987","journal-title":"Eur. J. Biochem."},{"key":"2021121516072922700_cit27","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/S0006-3495(90)82363-8","volume":"58","author":"Papp","year":"1990","journal-title":"Biophys. J."},{"key":"2021121516072922700_cit28","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/s00775-007-0309-8","volume":"13","author":"Takashima","year":"2008","journal-title":"J. Biol. Inorg. Chem."},{"key":"2021121516072922700_cit29","doi-asserted-by":"crossref","first-page":"1460","DOI":"10.1021\/bi00704a022","volume":"13","author":"Leonard","year":"1974","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit30","doi-asserted-by":"crossref","first-page":"16297","DOI":"10.1021\/ja0656806","volume":"128","author":"Komatsu","year":"2006","journal-title":"J. Am. Chem. Soc."},{"key":"2021121516072922700_cit31","doi-asserted-by":"crossref","first-page":"1864","DOI":"10.1021\/jp501615h","volume":"118","author":"Lepeshkevich","year":"2014","journal-title":"J. Phys. Chem. A"},{"key":"2021121516072922700_cit32","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1021\/j100274a013","volume":"90","author":"Feitelson","year":"1986","journal-title":"J. Phys. Chem."},{"key":"2021121516072922700_cit33","doi-asserted-by":"crossref","first-page":"10708","DOI":"10.1021\/j100027a006","volume":"99","author":"Maiti","year":"1995","journal-title":"J. Phys. Chem."},{"key":"2021121516072922700_cit34","doi-asserted-by":"crossref","first-page":"1192","DOI":"10.1021\/ja00395a033","volume":"103","author":"Zemel","year":"1981","journal-title":"J. Am. Chem. Soc."},{"key":"2021121516072922700_cit35","doi-asserted-by":"crossref","first-page":"4884","DOI":"10.1016\/j.febslet.2006.08.003","volume":"580","author":"Fago","year":"2006","journal-title":"FEBS Lett."},{"key":"2021121516072922700_cit36","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.inoche.2015.10.010","volume":"62","author":"Tiwari","year":"2015","journal-title":"Inorg. Chem. Commun."},{"key":"2021121516072922700_cit37","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/j.ijbiomac.2008.07.003","volume":"43","author":"B\u00f8nding","year":"2008","journal-title":"Int. J. Biol. Macromol."},{"key":"2021121516072922700_cit38","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1006\/jmbi.1999.3124","volume":"292","author":"Miyazaki","year":"1999","journal-title":"J. Mol. Biol."},{"key":"2021121516072922700_cit39","doi-asserted-by":"crossref","first-page":"7843","DOI":"10.1021\/bi030263g","volume":"43","author":"Hui","year":"2004","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit40","doi-asserted-by":"crossref","first-page":"11256","DOI":"10.1021\/ja982009v","volume":"120","author":"Naito","year":"1998","journal-title":"J. Am. Chem. Soc."},{"key":"2021121516072922700_cit41","doi-asserted-by":"crossref","first-page":"7533","DOI":"10.1021\/ja00258a049","volume":"109","author":"Gingrich","year":"1987","journal-title":"J. Am. Chem. Soc."},{"key":"2021121516072922700_cit42","doi-asserted-by":"crossref","first-page":"2417","DOI":"10.1002\/anie.201308431","volume":"53","author":"Chakraborty","year":"2014","journal-title":"Angew. Chem."},{"key":"2021121516072922700_cit43","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1006\/jmbi.1996.0123","volume":"256","author":"Yang","year":"1996","journal-title":"J. Mol. Biol."},{"key":"2021121516072922700_cit44","doi-asserted-by":"crossref","first-page":"11901","DOI":"10.1021\/bi9608976","volume":"35","author":"Lloyd","year":"1996","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit45","doi-asserted-by":"crossref","first-page":"14986","DOI":"10.1021\/bi00254a006","volume":"33","author":"Shiro","year":"1994","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit46","doi-asserted-by":"crossref","first-page":"5132","DOI":"10.1021\/bi00070a023","volume":"32","author":"Smerdon","year":"1993","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit47","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1021\/ic00226a028","volume":"25","author":"Feitelson","year":"1986","journal-title":"Inorg. Chem."},{"key":"2021121516072922700_cit48","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/0162-0134(86)80094-0","volume":"28","author":"Dalvit","year":"1986","journal-title":"J. Inorg. Biochem."},{"key":"2021121516072922700_cit49","doi-asserted-by":"crossref","first-page":"1585","DOI":"10.1016\/j.jinorgbio.2005.04.018","volume":"99","author":"Lecomte","year":"2005","journal-title":"J. Inorg. Biochem."},{"key":"2021121516072922700_cit50","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/0009-2614(93)85724-3","volume":"215","author":"Ahn","year":"1993","journal-title":"Chem. Phys. Lett."},{"key":"2021121516072922700_cit51","doi-asserted-by":"crossref","first-page":"12820","DOI":"10.1021\/bi960895l","volume":"35","author":"Reddy","year":"1996","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit52","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1002\/1097-0282(2000)57:5<291::AID-BIP60>3.0.CO;2-O","volume":"57","author":"Sanfratello","year":"2000","journal-title":"Biopolymers"},{"key":"2021121516072922700_cit53","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1016\/S0006-3495(01)76080-8","volume":"80","author":"Shibata","year":"2001","journal-title":"Biophys. J."},{"key":"2021121516072922700_cit54","doi-asserted-by":"crossref","first-page":"10270","DOI":"10.1039\/c003606b","volume":"12","author":"Esquerra","year":"2010","journal-title":"Phys. Chem. Chem. Phys."},{"key":"2021121516072922700_cit55","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1107\/S1399004714000078","volume":"70","author":"Guimaraes","year":"2014","journal-title":"Acta Crystallogr., Sect. D: Biol. Crystallogr."},{"key":"2021121516072922700_cit56","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1016\/S0969-2126(03)00166-7","volume":"11","author":"Pesce","year":"2003","journal-title":"Structure"},{"key":"2021121516072922700_cit57","doi-asserted-by":"crossref","first-page":"1217","DOI":"10.1016\/j.bbrc.2004.03.007","volume":"316","author":"De Sanctis","year":"2004","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"2021121516072922700_cit58","doi-asserted-by":"crossref","first-page":"8080","DOI":"10.1021\/ja034584r","volume":"125","author":"Du","year":"2003","journal-title":"J. Am. Chem. Soc."},{"key":"2021121516072922700_cit59","doi-asserted-by":"crossref","first-page":"12988","DOI":"10.1021\/ja063330d","volume":"128","author":"Bondarenko","year":"2006","journal-title":"J. Am. Chem. Soc."},{"key":"2021121516072922700_cit60","doi-asserted-by":"crossref","first-page":"13257","DOI":"10.1021\/bi050997o","volume":"44","author":"Sawai","year":"2005","journal-title":"Biochemistry"},{"key":"2021121516072922700_cit61","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1002\/prot.22872","volume":"79","author":"Xu","year":"2011","journal-title":"Proteins"}],"container-title":["Metallomics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/metallomics\/article-pdf\/11\/5\/906\/41774561\/c8mt00332g.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/metallomics\/article-pdf\/11\/5\/906\/41774561\/c8mt00332g.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,12,15]],"date-time":"2021-12-15T16:26:48Z","timestamp":1639585608000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/metallomics\/article\/11\/5\/906\/5962186"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,1,16]]},"references-count":61,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2019,5,22]]}},"URL":"https:\/\/doi.org\/10.1039\/c8mt00332g","relation":{},"ISSN":["1756-5901","1756-591X"],"issn-type":[{"value":"1756-5901","type":"print"},{"value":"1756-591X","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,5]]},"published":{"date-parts":[[2019,1,16]]},"assertion":[{"value":"This document is Similarity Check deposited","name":"similarity_check","explanation":{"URL":"https:\/\/www.crossref.org\/services\/similarity-check\/"},"group":{"name":"similarity_check","label":"SIMILARITY CHECK"}},{"value":"Supplementary Information","URL":"https:\/\/doi.org\/10.1039\/C8MT00332G","name":"related_data","group":{"name":"related_data","label":"RELATED DATA"}},{"value":"Jaroslava Miksovska (ORCID)","URL":"http:\/\/orcid.org\/0000-0002-0385-9457","name":"identifier","group":{"name":"author_identifiers","label":"IDENTIFIERS"}},{"value":"Single-blind","order":2,"name":"peer_review_method","group":{"name":"peer_review_method","label":"PEER REVIEW METHOD"}},{"value":"Received 15 November 2018; Accepted 16 January 2019;  Accepted Manuscript published 16 January 2019;  Advance Article published 8 February 2019;  Version of Record published 22 May 2019","order":1,"name":"history","group":{"name":"publication_history","label":"PUBLICATION HISTORY"}}]}}