{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T22:24:56Z","timestamp":1791239096938,"version":"4.1.0"},"reference-count":41,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2024,5,30]],"date-time":"2024-05-30T00:00:00Z","timestamp":1717027200000},"content-version":"vor","delay-in-days":1,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000038","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"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,6,4]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Red blood cells (RBCs) constitute \u223c50% of the bloodstream and represent an important target for environmental pollutants and bacterial\/viral infections, which can result in their rupture. In addition, diseases such as sickle cell anaemia and paroxysmal nocturnal haemoglobinuria can also result in the rupture of RBCs, which can be potentially life-threatening. With regard to the release of cytosolic metalloproteins from RBCs into the blood-organ system, the biochemical fate of haemoglobin is rather well understood, while comparatively little is known about another highly abundant Zn-metalloprotein, carbonic anhydrase (CA I). To gain insight into the interaction of CA I with human blood plasma constituents, we have employed a metallomics tool comprised of size-exclusion chromatography (SEC) coupled online with an inductively coupled plasma atomic emission spectrometer (ICP-AES), which allows to simultaneously observe all Cu, Fe, and Zn-metalloproteins. After the addition of CA I to human blood plasma incubated at 37\u00b0C, the SEC-ICP-AES analysis using phosphate buffered saline (pH 7.4) after 5\u00a0min, 1\u00a0h, and 2\u00a0h revealed that CA I eluted after all endogenous Zn-metalloproteins in the 30\u00a0kDa range. Matrix-assisted laser desorption-time of flight mass spectrometry analysis of the collected Zn-peak confirmed that CA I eluted from the column intact. Our in vitro results suggest that CA I released from RBCs to plasma remains free and may be actively involved in health-relevant adverse processes that unfold at the bloodstream-endothelial interface, including atherosclerosis and vision loss.<\/jats:p>","DOI":"10.1093\/mtomcs\/mfae028","type":"journal-article","created":{"date-parts":[[2024,5,30]],"date-time":"2024-05-30T01:01:13Z","timestamp":1717030873000},"source":"Crossref","is-referenced-by-count":4,"title":["Interaction of carbonic anhydrase I released from red blood cells with human plasma in vitro"],"prefix":"10.1093","volume":"16","author":[{"given":"Maryam","family":"Doroudian","sequence":"first","affiliation":[{"name":"Department of Chemistry, University of Calgary , 2500 University Drive NW, Calgary, AB T2N 1N4 , Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00fcrgen","family":"Gailer","sequence":"additional","affiliation":[{"name":"Department of Chemistry, University of Calgary , 2500 University Drive NW, Calgary, AB T2N 1N4 , Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,5,29]]},"reference":[{"issue":"11","key":"2024062013154633800_bib1","doi-asserted-by":"crossref","first-page":"9687","DOI":"10.3390\/ijms24119687","article-title":"Carbonic anhydrase and biomarker research: new insights","volume":"24","author":"Lionetto","year":"2023","journal-title":"Int. J. Mol. Sci."},{"issue":"1","key":"2024062013154633800_bib2","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1146\/annurev.ph.58.030196.002515","article-title":"Multiple roles of carbonic anhydrase in cellular transport and metabolism","volume":"58","author":"Henry","year":"1996","journal-title":"Annu. Rev. Physiol."},{"issue":"2","key":"2024062013154633800_bib3","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.ucl.2023.01.009","article-title":"Biomarkers for the detection and surveillance of renal cancer","volume":"50","author":"Nolazco","year":"2023","journal-title":"Urol. Clin. North Am."},{"key":"2024062013154633800_bib4","doi-asserted-by":"crossref","DOI":"10.1142\/p1044","volume-title":"Metallomics. A Primer of Integrated Biometal Sciences","author":"Maret","year":"2016"},{"issue":"6","key":"2024062013154633800_bib5","doi-asserted-by":"crossref","first-page":"596","DOI":"10.1002\/mas.20178","article-title":"The proteominer and the fortyniners: searching for gold nuggest in the proteomic arena","volume":"27","author":"Righetti","year":"2008","journal-title":"Mass Spectrom. Rev."},{"issue":"1","key":"2024062013154633800_bib6","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1039\/C5MT00186B","article-title":"Investigating the adduct formation of organic mercury species with carbonic anhydrase and hemoglobin from human blood cell hemolysate by means of LC\/ESI-TOF-MS and LC\/ICP-MS","volume":"8","author":"Hogeback","year":"2016","journal-title":"Metallomics"},{"issue":"1","key":"2024062013154633800_bib7","doi-asserted-by":"crossref","first-page":"e0262160","DOI":"10.1371\/journal.pone.0262160","article-title":"Quantification of human plasma metalloproteins in multiple sclerosis, ischemic stroke and health controls reveals an association of haptoglobin-hemoglobin complexes with age","volume":"17","author":"Sarpong-Kumankomah","year":"2022","journal-title":"PLoS One"},{"issue":"3","key":"2024062013154633800_bib8","doi-asserted-by":"crossref","first-page":"670","DOI":"10.1111\/j.1432-1033.1997.00670.x","article-title":"The malaria parasite supplies glutathione to its host cell","volume":"250","author":"Atamna","year":"1997","journal-title":"Eur. J. Biochem."},{"issue":"1","key":"2024062013154633800_bib9","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/0300-483X(90)90065-O","article-title":"Evidence for oxidative damage to red blood cells in mice by arsine gas","volume":"63","author":"Blair","year":"1990","journal-title":"Toxicology"},{"issue":"2","key":"2024062013154633800_bib10","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1159\/000430137","article-title":"Enhanced suicidal erythrocyte death contributing to anaemia in the elderly","volume":"36","author":"Lupescu","year":"2015","journal-title":"Cell. Physiol. Biochem."},{"issue":"5","key":"2024062013154633800_bib11","doi-asserted-by":"crossref","first-page":"L765","DOI":"10.1152\/ajplung.00269.2018","article-title":"Depletion of haptoglobin and hemopexin promote hemoglobin-mediated lipoprotein oxidation in sickle cell disease","volume":"315","author":"Yalamanoglu","year":"2018","journal-title":"Am. J. Physiol-Lung Cell Mol. Physiol."},{"key":"2024062013154633800_bib12","first-page":"924","article-title":"Rapid flow cytometric test for the diagnosis of membrane cytosleleton-associated haemolytic anaemia","volume":"111","author":"King","year":"2000","journal-title":"Br. J. Haematol."},{"issue":"1","key":"2024062013154633800_bib13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/nrdp.2017.28","article-title":"Paroxysmal nocturnal haemoglobinuria","volume":"3","author":"Hill","year":"2017","journal-title":"Nat. Rev. Dis. Primers"},{"key":"2024062013154633800_bib14","doi-asserted-by":"crossref","first-page":"110802","DOI":"10.1016\/j.jinorgbio.2019.110802","article-title":"Identification of a haptoglobin-hemoglobin complex in human blood plasma","volume":"201","author":"Sarpong-Kumankomah","year":"2019","journal-title":"J. Inorg. Biochem."},{"issue":"13","key":"2024062013154633800_bib15","doi-asserted-by":"crossref","first-page":"3292","DOI":"10.1002\/pmic.200401228","article-title":"Depletion of multiple high-abundance proteins improves protein profiling capacities of human serum and plasma","volume":"5","author":"Echan","year":"2005","journal-title":"Proteomics"},{"issue":"6","key":"2024062013154633800_bib16","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1039\/c1mt00037c","article-title":"Liquid chromatography-inductively coupled plasma-based metallomic approaches to probe health-relevant interactions between xenobiotics and mammalian organisms","volume":"3","author":"Gomez-Ariza","year":"2011","journal-title":"Metallomics"},{"issue":"3","key":"2024062013154633800_bib17","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1586\/epr.09.44","article-title":"Analysis of the plasma metalloproteome by SEC-ICP-AES: bridging proteomics and metabolomics","volume":"6","author":"Manley","year":"2009","journal-title":"Expert Rev. Proteom."},{"issue":"5","key":"2024062013154633800_bib18","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1039\/b903681d","article-title":"Probing the interaction of arsenobetaine with blood plasma constituents in vitro: an SEC-ICP-AES study","volume":"1","author":"Pei","year":"2009","journal-title":"Metallomics"},{"issue":"1","key":"2024062013154633800_bib19","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1007\/s00775-008-0424-1","article-title":"Simultaneous Cu-, Fe-, and Zn-specific detection of metalloproteins contained in rabbit plasma by size-exclusion chromatography-inductively coupled plasma atomic emission spectroscopy","volume":"14","author":"Manley","year":"2009","journal-title":"J. Biol. Inorg. Chem."},{"issue":"7","key":"2024062013154633800_bib20","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1039\/c003321a","article-title":"Remarkable effect of mobile phase buffer on the SEC-ICP-AES derived Cu, Fe and Zn-metalloproteome pattern of rabbit blood plasma","volume":"2","author":"Jahromi","year":"2010","journal-title":"Metallomics"},{"issue":"13","key":"2024062013154633800_bib21","doi-asserted-by":"crossref","first-page":"5258","DOI":"10.1021\/bi048135v","article-title":"Thermodynamic stability of carbonic anhydrase: measurements of binding affinity and stoichiometry using ThermoFluor","volume":"44","author":"Matulis","year":"2005","journal-title":"Biochemistry"},{"key":"2024062013154633800_bib22","doi-asserted-by":"crossref","first-page":"122147","DOI":"10.1016\/j.jchromb.2020.122147","article-title":"Sample preparation of blood plasma enables baseline separation of iron metalloproteins by SEC-GFAAS","volume":"1147","author":"Miller","year":"2020","journal-title":"J. Chromatogr. B"},{"issue":"1","key":"2024062013154633800_bib23","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.aogh.2016.01.005","article-title":"Health consequences of environmental exposures: changing global patterns of exposure and disease","volume":"82","author":"Landrigan","year":"2016","journal-title":"Ann. Global Health"},{"issue":"9","key":"2024062013154633800_bib24","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1002\/ajim.22336","article-title":"Occupational cadmium exposure-associated oxidative stress and erythrocyte fragility among jewelry workers in India","volume":"57","author":"Moitra","year":"2014","journal-title":"Am. J. Industr. Med."},{"key":"2024062013154633800_bib25","article-title":"Fourth national report on human exposure to environmental chemicals","author":"Centers of Disease Control and Prevention A, GA, USA"},{"issue":"1-2","key":"2024062013154633800_bib26","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/BF02919103","article-title":"Synergistic toxicity between arsenic and methylated selenium compounds","volume":"20","author":"Kraus","year":"1989","journal-title":"Biol. Trace Elem. Res."},{"issue":"13","key":"2024062013154633800_bib27","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1001\/jama.293.13.1653","article-title":"The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin","volume":"293","author":"Rother","year":"2005","journal-title":"JAMA"},{"issue":"10","key":"2024062013154633800_bib28","doi-asserted-by":"crossref","first-page":"3311","DOI":"10.1007\/s00216-012-5743-y","article-title":"Protein fractionation and detection for metalloproteomics: challenges and approaches","volume":"402","author":"Barnett","year":"2012","journal-title":"Anal. Bioanal. Chem."},{"issue":"4","key":"2024062013154633800_bib29","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1039\/b713633c","article-title":"Metallomics: the concept and methodology","volume":"38","author":"Mounicou","year":"2009","journal-title":"Chem. Soc. Rev."},{"issue":"4","key":"2024062013154633800_bib30","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1152\/physrev.1967.47.4.595","article-title":"Carbonic anhydrase: chemistry, physiology, and inhibition","volume":"47","author":"Maren","year":"1967","journal-title":"Physiol. Rev."},{"issue":"5","key":"2024062013154633800_bib31","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1093\/jalm\/jfaa051","article-title":"Detection of intravascular hemolysis in newborn infants using urinary carbonic anhydrase I immunoreactivity","volume":"5","author":"Hulikova","year":"2020","journal-title":"J. Appl. Lab. Med."},{"issue":"1","key":"2024062013154633800_bib32","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1186\/s12885-015-1707-x","article-title":"CA1 contributes to microcalcification and tumorigenesis in breast cancer","volume":"15","author":"Zheng","year":"2015","journal-title":"BMC Cancer"},{"issue":"2","key":"2024062013154633800_bib33","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/S0014-5793(00)02260-2","article-title":"Effects of homocysteine on the binding of extracellular-superoxide dismutase to the endothelial cell surface","volume":"486","author":"Yamamoto","year":"2000","journal-title":"FEBS Lett."},{"key":"2024062013154633800_bib34","doi-asserted-by":"crossref","first-page":"379","DOI":"10.3389\/fphys.2014.00379","article-title":"Red blood cell, hemoglobin and heme in the progression of atherosclerosis","volume":"5","author":"Jeney","year":"2014","journal-title":"Front. Physiol."},{"issue":"10","key":"2024062013154633800_bib35","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.3390\/biom12101358","article-title":"Investigating the role of zinc in atherosclerosis: a review","volume":"12","author":"Shen","year":"2022","journal-title":"Biomolecules"},{"key":"2024062013154633800_bib36","first-page":"766","article-title":"Carbonic anhydrase 1-mediated calcification is associated with atherosclerosis, and methalzolamide alleviates its pathogenesis","volume":"10","author":"Yuan","year":"2019","journal-title":"Front Physiol"},{"issue":"1","key":"2024062013154633800_bib37","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1146\/annurev.biochem.78.081307.110540","article-title":"Mechanisms of endocytosis","volume":"78","author":"Doherty","year":"2009","journal-title":"Annu. Rev. Biochem."},{"issue":"2","key":"2024062013154633800_bib38","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1038\/nm1534","article-title":"Extracellular carbonic anhydrase mediates hemorrhagic retinal and cerebral vascular permeability through prekallikrein activation","volume":"13","author":"Gao","year":"2007","journal-title":"Nat. Med."},{"issue":"3","key":"2024062013154633800_bib39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1177\/1759091416651511","article-title":"Zinc in multiple sclerosis: a systematic review and meta-analysis","volume":"8","author":"Bredholt","year":"2016","journal-title":"ASN Neuro."},{"issue":"2","key":"2024062013154633800_bib40","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1136\/jcp.3.2.142","article-title":"Urinary excretion of carbonic anhydrase","volume":"3","author":"Robinson","year":"1950","journal-title":"J. Clin. Pathol."},{"issue":"11","key":"2024062013154633800_bib41","doi-asserted-by":"crossref","first-page":"200","DOI":"10.3390\/inorganics10110200","article-title":"Integrative metallomics studies of toxic metal(loid) substances at the blood plasma-red blood cell-organ\/tumor nexus","volume":"10","author":"Doroudian","year":"2022","journal-title":"Inorganics"}],"container-title":["Metallomics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/metallomics\/advance-article-pdf\/doi\/10.1093\/mtomcs\/mfae028\/57987099\/mfae028.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/metallomics\/article-pdf\/16\/6\/mfae028\/58288395\/mfae028.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/metallomics\/article-pdf\/16\/6\/mfae028\/58288395\/mfae028.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,20]],"date-time":"2024-06-20T13:17:43Z","timestamp":1718889463000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/metallomics\/article\/doi\/10.1093\/mtomcs\/mfae028\/7685028"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,29]]},"references-count":41,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2024,6,4]]}},"URL":"https:\/\/doi.org\/10.1093\/mtomcs\/mfae028","relation":{},"ISSN":["1756-591X"],"issn-type":[{"value":"1756-591X","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,6]]},"published":{"date-parts":[[2024,5,29]]},"article-number":"mfae028"}}