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Because they transport oxygen, red blood cells (RBCs) may play a role in the severity of hypoxemia in COVID-19 patients. The present study combines state-of-the-art metabolomics, proteomics, and lipidomics approaches to investigate the impact of COVID-19 on RBCs from 23 healthy subjects and 29 molecularly diagnosed COVID-19 patients. RBCs from COVID-19 patients had increased levels of glycolytic intermediates, accompanied by oxidation and fragmentation of ankyrin, spectrin beta, and the N-terminal cytosolic domain of band 3 (AE1). Significantly altered lipid metabolism was also observed, in particular, short- and medium-chain saturated fatty acids, acyl-carnitines, and sphingolipids. Nonetheless, there were no alterations of clinical hematological parameters, such as RBC count, hematocrit, or mean corpuscular hemoglobin concentration, with only minor increases in mean corpuscular volume. Taken together, these results suggest a significant impact of SARS-CoV-2 infection on RBC structural membrane homeostasis at the protein and lipid levels. Increases in RBC glycolytic metabolites are consistent with a theoretically improved capacity of hemoglobin to off-load oxygen as a function of allosteric modulation by high-energy phosphate compounds, perhaps to counteract COVID-19-induced hypoxia. Conversely, because the N-terminus of AE1 stabilizes deoxyhemoglobin and finely tunes oxygen off-loading and metabolic rewiring toward the hexose monophosphate shunt, RBCs from COVID-19 patients may be less capable of responding to environmental variations in hemoglobin oxygen saturation\/oxidant stress when traveling from the lungs to peripheral capillaries and vice versa.<\/jats:p>","DOI":"10.1021\/acs.jproteome.0c00606","type":"journal-article","created":{"date-parts":[[2020,10,26]],"date-time":"2020-10-26T10:10:40Z","timestamp":1603707040000},"page":"4455-4469","source":"Crossref","is-referenced-by-count":239,"title":["Evidence of Structural\nProtein Damage and Membrane\nLipid Remodeling in Red Blood Cells from COVID-19 Patients"],"prefix":"10.1021","volume":"19","author":[{"given":"Tiffany","family":"Thomas","sequence":"first","affiliation":[{"name":"Columbia University , , , ,","place":["New York, New York, United States, 10032"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Davide","family":"Stefanoni","sequence":"additional","affiliation":[{"name":"University of Colorado Denver \u2212 Anschutz Medical Campus , , , ,","place":["Aurora, Colorado, United States, 80045"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monika","family":"Dzieciatkowska","sequence":"additional","affiliation":[{"name":"University of Colorado Denver \u2212 Anschutz Medical Campus , , , ,","place":["Aurora, Colorado, United States, 80045"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aaron","family":"Issaian","sequence":"additional","affiliation":[{"name":"University of Colorado Denver \u2212 Anschutz Medical Campus , , , ,","place":["Aurora, Colorado, United States, 80045"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Travis","family":"Nemkov","sequence":"additional","affiliation":[{"name":"University of Colorado Denver \u2212 Anschutz Medical Campus , , , ,","place":["Aurora, Colorado, United States, 80045"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryan C.","family":"Hill","sequence":"additional","affiliation":[{"name":"University of Colorado Denver \u2212 Anschutz Medical Campus , , , ,","place":["Aurora, Colorado, United States, 80045"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard O.","family":"Francis","sequence":"additional","affiliation":[{"name":"Columbia University , , , ,","place":["New York, New York, United States, 10032"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Krystalyn E.","family":"Hudson","sequence":"additional","affiliation":[{"name":"Columbia University , , , ,","place":["New York, New York, United States, 10032"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul W.","family":"Buehler","sequence":"additional","affiliation":[{"name":"University of Maryland , , , ,","place":["Baltimore, Maryland, United States, 21201"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James C.","family":"Zimring","sequence":"additional","affiliation":[{"name":"University of Virginia , , , ,","place":["Charlottesville, Virginia, United States, 22903"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eldad A.","family":"Hod","sequence":"additional","affiliation":[{"name":"Columbia University , , , ,","place":["New York, New York, United States, 10032"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kirk C.","family":"Hansen","sequence":"additional","affiliation":[{"name":"University of Colorado Denver \u2212 Anschutz Medical Campus , , , ,","place":["Aurora, Colorado, United States, 80045"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven L.","family":"Spitalnik","sequence":"additional","affiliation":[{"name":"Columbia University , , , ,","place":["New York, New York, United States, 10032"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2258-6490","authenticated-orcid":true,"given":"Angelo","family":"D\u2019Alessandro","sequence":"additional","affiliation":[{"name":"University of Colorado Denver \u2212 Anschutz Medical Campus , , , ,","place":["Aurora, Colorado, United States, 80045"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,10,26]]},"reference":[{"issue":"7798","key":"2026081714252228000_cit1","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1038\/s41586-020-2008-3","article-title":"A New Coronavirus\nAssociated with Human Respiratory\nDisease in China","volume":"579","author":"Wu","year":"2020","journal-title":"Nature"},{"issue":"4","key":"2026081714252228000_cit2","doi-asserted-by":"publisher","first-page":"450","DOI":"10.1038\/s41591-020-0820-9","article-title":"The Proximal\nOrigin of SARS-CoV-2","volume":"26","author":"Andersen","year":"2020","journal-title":"Nat. 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How Deep Omics Characterization of the Most Abundant\nCell in the Human Body Highlights Other Systemic Metabolic Functions\nbeyond Oxygen Transport","volume":"15","author":"Nemkov","year":"2018","journal-title":"Expert Rev. 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Virol."},{"issue":"1","key":"2026081714252228000_cit36","doi-asserted-by":"publisher","first-page":"73","DOI":"10.3390\/v11010073","article-title":"Characterization of the Lipidomic Profile of Human\nCoronavirus-Infected Cells: Implications for Lipid Metabolism Remodeling\nupon Coronavirus Replication","volume":"11","author":"Yan","year":"2019","journal-title":"Viruses"},{"key":"2026081714252228000_cit37","doi-asserted-by":"publisher","DOI":"10.1101\/2020.05.14.20102491","article-title":"COVID-19 Infection\nResults in Alterations of the Kynurenine Pathway and Fatty Acid Metabolism\nThat Correlate with IL-6 Levels and Renal Status","author":"Thomas","year":"2020","journal-title":"MedRxiv"},{"issue":"7","key":"2026081714252228000_cit38","doi-asserted-by":"publisher","first-page":"1132","DOI":"10.1194\/jlr.R082578","article-title":"The Phospholipase\nA2 Activity of Peroxiredoxin 6","volume":"59","author":"Fisher","year":"2018","journal-title":"J. Lipid Res."},{"issue":"2","key":"2026081714252228000_cit39","doi-asserted-by":"publisher","first-page":"130","DOI":"10.2450\/2020.0256-19","article-title":"Decoding the\nMetabolic Landscape of Pathophysiological Stress-Induced Cell Death\nin Anucleate Red Blood Cells","volume":"18","author":"Nemkov","year":"2020","journal-title":"Blood Transfus."},{"issue":"4","key":"2026081714252228000_cit40","first-page":"315","article-title":"Red Cell Vesiculation--a\nCommon Membrane Physiologic Event","volume":"108","author":"Wagner","year":"1986","journal-title":"J. Lab. Clin.\nMed."},{"key":"2026081714252228000_cit41","doi-asserted-by":"publisher","first-page":"29637","DOI":"10.1038\/srep29637","article-title":"Hypoxia-Mediated Impaired\nErythrocyte\nLands\u2019 Cycle Is Pathogenic for Sickle Cell Disease","volume":"6","author":"Wu","year":"2016","journal-title":"Sci. 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