{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T11:20:47Z","timestamp":1792668047452,"version":"4.5.0"},"reference-count":52,"publisher":"American Chemical Society (ACS)","issue":"14","license":[{"start":{"date-parts":[[2020,11,25]],"date-time":"2020-11-25T00:00:00Z","timestamp":1606262400000},"content-version":"vor","delay-in-days":160,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_ccby_termsofuse.html"}],"funder":[{"DOI":"10.13039\/100010661","name":"Horizon 2020 Framework Programme","doi-asserted-by":"publisher","award":["731005"],"award-info":[{"award-number":["731005"]}],"id":[{"id":"10.13039\/100010661","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010661","name":"Horizon 2020 Framework Programme","doi-asserted-by":"publisher","award":["871037"],"award-info":[{"award-number":["871037"]}],"id":[{"id":"10.13039\/100010661","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/na","name":"Ministero dell'Istruzione, dell'Universit\u00e0 e della Ricerca","doi-asserted-by":"publisher","award":["20177XJCHX"],"award-info":[{"award-number":["20177XJCHX"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,7,21]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>In-cell NMR can investigate protein conformational changes at atomic resolution, such as those changes induced by drug binding or chemical modifications, directly in living human cells, and therefore has great potential in the context of drug development as it can provide an early assessment of drug potency. NMR bioreactors can greatly improve the cell sample stability over time and, more importantly, allow for recording in-cell NMR data in real time to monitor the evolution of intracellular processes, thus providing unique insights into the kinetics of drug-target interactions. However, current implementations are limited by low cell viability at &amp;gt;24 h times, the reduced sensitivity compared to \u201cstatic\u201d experiments and the lack of protocols for automated and quantitative analysis of large amounts of data. Here, we report an improved bioreactor design which maintains human cells alive and metabolically active for up to 72 h, and a semiautomated workflow for quantitative analysis of real-time in-cell NMR data relying on Multivariate Curve Resolution. We apply this setup to monitor protein\u2013ligand interactions and protein oxidation in real time. High-quality concentration profiles can be obtained from noisy 1D and 2D NMR data with high temporal resolution, allowing further analysis by fitting with kinetic models. This unique approach can therefore be applied to investigate complex kinetic behaviors of macromolecules in a cellular setting, and could be extended in principle to any real-time NMR application in live cells.<\/jats:p>","DOI":"10.1021\/acs.analchem.0c01677","type":"journal-article","created":{"date-parts":[[2020,6,18]],"date-time":"2020-06-18T15:34:51Z","timestamp":1592494491000},"page":"9997-10006","source":"Crossref","is-referenced-by-count":63,"title":["Real-Time Quantitative In-Cell NMR: Ligand Binding\nand Protein Oxidation Monitored in Human Cells Using Multivariate\nCurve Resolution"],"prefix":"10.1021","volume":"92","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4183-4311","authenticated-orcid":true,"given":"Enrico","family":"Luchinat","sequence":"first","affiliation":[{"name":"University of Florence , , Via Luigi Sacconi 6 , ,","place":["Sesto Fiorentino, Florence, Italy, 50019"]},{"name":"Center for Colloids and Surface Science \u2212 CSGI , Via della Lastruccia 3 , ,","place":["Sesto Fiorentino, Florence, Italy, 50019"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Letizia","family":"Barbieri","sequence":"additional","affiliation":[{"name":"University of Florence , , Via Luigi Sacconi 6 , ,","place":["Sesto Fiorentino, Florence, Italy, 50019"]},{"name":"Interuniversity Consortium for Magnetic Resonance of Metalloproteins \u2212 CIRMMP , Via Luigi Sacconi 6 , ,","place":["Sesto Fiorentino, Florence, Italy, 50019"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Timothy F.","family":"Campbell","sequence":"additional","affiliation":[{"name":"University of Florence , , Via Luigi Sacconi 6 , ,","place":["Sesto Fiorentino, Florence, Italy, 50019"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0562-5774","authenticated-orcid":true,"given":"Lucia","family":"Banci","sequence":"additional","affiliation":[{"name":"University of Florence , , Via Luigi Sacconi 6 , ,","place":["Sesto Fiorentino, Florence, Italy, 50019"]},{"name":"University of Florence , , Via Luigi Sacconi 6 , ,","place":["Sesto Fiorentino, Florence, Italy, 50019"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,6,18]]},"reference":[{"issue":"7234","key":"2026090117044439300_cit1","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1038\/nature07839","article-title":"High-Resolution Multi-Dimensional\nNMR Spectroscopy of Proteins in Human Cells","volume":"458","author":"Inomata","year":"2009","journal-title":"Nature"},{"issue":"2","key":"2026090117044439300_cit2","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1107\/S2052252516020625","article-title":"In-Cell NMR: A Topical Review","volume":"4","author":"Luchinat","year":"2017","journal-title":"IUCrJ"},{"issue":"8","key":"2026090117044439300_cit3","doi-asserted-by":"publisher","first-page":"2165","DOI":"10.1002\/anie.201712284","article-title":"Evaluation\nof the Stability of DNA I-Motifs in the Nuclei of Living Mammalian\nCells","volume":"57","author":"Dzatko","year":"2018","journal-title":"Angew. Chem., Int. Ed."},{"issue":"6","key":"2026090117044439300_cit4","doi-asserted-by":"publisher","first-page":"1550","DOI":"10.1021\/acs.accounts.8b00147","article-title":"In-Cell NMR in Human Cells: Direct Protein Expression Allows Structural\nStudies of Protein Folding and Maturation","volume":"51","author":"Luchinat","year":"2018","journal-title":"Acc.\nChem. Res."},{"issue":"22","key":"2026090117044439300_cit5","doi-asserted-by":"publisher","first-page":"7284","DOI":"10.1002\/anie.201900840","article-title":"High-Resolution Protein\n3D Structure Determination in Living Eukaryotic Cells","volume":"58","author":"Tanaka","year":"2019","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090117044439300_cit6","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1016\/j.jmr.2019.07.018","article-title":"Cells, Drugs and NMR","volume":"306","author":"Siegal","year":"2019","journal-title":"J. Magn.\nReson."},{"issue":"5","key":"2026090117044439300_cit7","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1038\/nchembio.1202","article-title":"Atomic-Resolution Monitoring of Protein\nMaturation in Live Human Cells by NMR","volume":"9","author":"Banci","year":"2013","journal-title":"Nat.\nChem. Biol."},{"key":"2026090117044439300_cit8","doi-asserted-by":"publisher","first-page":"5502","DOI":"10.1038\/ncomms6502","article-title":"In-Cell NMR Reveals Potential Precursor of Toxic Species from SOD1\nFALS Mutants","volume":"5","author":"Luchinat","year":"2014","journal-title":"Nat. Commun."},{"issue":"7588","key":"2026090117044439300_cit9","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1038\/nature16531","article-title":"Structural Disorder\nof Monomeric \u03b1-Synuclein Persists in Mammalian Cells","volume":"530","author":"Theillet","year":"2016","journal-title":"Nature"},{"issue":"1","key":"2026090117044439300_cit10","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1007\/s00775-017-1509-5","article-title":"Intracellular\nMetal Binding and Redox\nBehavior of Human DJ-1","volume":"23","author":"Barbieri","year":"2018","journal-title":"JBIC, J. Biol. Inorg.\nChem."},{"issue":"6","key":"2026090117044439300_cit11","doi-asserted-by":"publisher","first-page":"747","DOI":"10.1016\/j.chembiol.2013.05.007","article-title":"Visualization\nof Redox-Controlled\nProtein Fold in Living Cells","volume":"20","author":"Banci","year":"2013","journal-title":"Chem. 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Res. Commun."},{"issue":"2","key":"2026090117044439300_cit18","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1016\/j.jmr.2009.10.008","article-title":"A Bioreactor\nfor In-Cell Protein NMR","volume":"202","author":"Sharaf","year":"2010","journal-title":"J. Magn. Reson."},{"issue":"4","key":"2026090117044439300_cit19","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.1002\/anie.201207243","article-title":"A Gel-Encapsulated Bioreactor System for NMR Studies\nof Protein-Protein Interactions in Living Mammalian Cells","volume":"52","author":"Kubo","year":"2013","journal-title":"Angew. Chem., Int. Ed."},{"issue":"81","key":"2026090117044439300_cit20","doi-asserted-by":"publisher","first-page":"11245","DOI":"10.1039\/C7CC06004A","article-title":"Impact of\nCellular Health Conditions on the Protein Folding State in Mammalian\nCells","volume":"53","author":"Inomata","year":"2017","journal-title":"Chem. 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Chem."},{"issue":"2","key":"2026090117044439300_cit29","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1038\/nrd2467","article-title":"Carbonic\nAnhydrases: Novel Therapeutic Applications for Inhibitors and Activators","volume":"7","author":"Supuran","year":"2008","journal-title":"Nat. Rev. Drug Discovery"},{"issue":"10","key":"2026090117044439300_cit30","doi-asserted-by":"publisher","first-page":"767","DOI":"10.1038\/nrd3554","article-title":"Interfering with\nPH Regulation in Tumours as a Therapeutic\nStrategy","volume":"10","author":"Neri","year":"2011","journal-title":"Nat. Rev. Drug Discovery"},{"issue":"8","key":"2026090117044439300_cit31","doi-asserted-by":"publisher","first-page":"4421","DOI":"10.1021\/cr200176r","article-title":"Multiple Binding\nModes of Inhibitors to Carbonic Anhydrases: How to Design Specific\nDrugs Targeting 15 Different Isoforms?","volume":"112","author":"Alterio","year":"2012","journal-title":"Chem.\nRev."},{"issue":"8","key":"2026090117044439300_cit32","doi-asserted-by":"publisher","first-page":"4865","DOI":"10.1007\/s11033-014-3417-x","article-title":"Ebselen, a Promising Antioxidant Drug: Mechanisms of\nAction and Targets of Biological Pathways","volume":"41","author":"Azad","year":"2014","journal-title":"Mol.\nBiol. Rep."},{"key":"2026090117044439300_cit33","doi-asserted-by":"publisher","DOI":"10.1002\/anie.202000451","article-title":"Superoxide\nDismutase 1 in Health and Disease: How a Front-Line Antioxidant Becomes\nNeurotoxic","author":"Trist","year":"2020","journal-title":"Angew. Chem., Int. Ed."},{"issue":"34","key":"2026090117044439300_cit34","doi-asserted-by":"publisher","first-page":"13555","DOI":"10.1073\/pnas.1207493109","article-title":"Human Superoxide Dismutase\n1 (HSOD1) Maturation through Interaction with Human Copper Chaperone\nfor SOD1 (HCCS)","volume":"109","author":"Banci","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U. S.\nA."},{"issue":"29","key":"2026090117044439300_cit35","doi-asserted-by":"publisher","first-page":"12025","DOI":"10.1074\/jbc.M117.775981","article-title":"Copper-Zinc\nSuperoxide Dismutase Is Activated through a Sulfenic Acid Intermediate\nat a Copper Ion Entry Site","volume":"292","author":"Fetherolf","year":"2017","journal-title":"J. Biol. Chem."},{"issue":"2","key":"2026090117044439300_cit36","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.3000141","article-title":"Molecular\nRecognition and Maturation of SOD1 by Its Evolutionarily Destabilised\nCognate Chaperone HCCS","volume":"17","author":"Sala","year":"2019","journal-title":"PLoS Biol."},{"issue":"40","key":"2026090117044439300_cit37","doi-asserted-by":"publisher","first-page":"12402","DOI":"10.1073\/pnas.1511308112","article-title":"Thermodynamics of Protein Destabilization in Live Cells","volume":"112","author":"Danielsson","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"issue":"1","key":"2026090117044439300_cit38","doi-asserted-by":"publisher","first-page":"17433","DOI":"10.1038\/s41598-017-17815-y","article-title":"A Molecular\nChaperone Activity of\nCCS Restores the Maturation of SOD1 FALS Mutants","volume":"7","author":"Luchinat","year":"2017","journal-title":"Sci. Rep."},{"key":"2026090117044439300_cit39","doi-asserted-by":"publisher","first-page":"101102","DOI":"10.1016\/j.redox.2019.101102","article-title":"Cadmium Effects\non Superoxide Dismutase 1 in Human Cells Revealed by NMR","volume":"21","author":"Polykretis","year":"2019","journal-title":"Redox Biol."},{"issue":"1","key":"2026090117044439300_cit40","doi-asserted-by":"publisher","first-page":"1693","DOI":"10.1038\/s41467-018-04114-x","article-title":"The Cysteine-Reactive\nSmall Molecule Ebselen Facilitates Effective SOD1Maturation","volume":"9","author":"Capper","year":"2018","journal-title":"Nat. Commun."},{"issue":"42","key":"2026090117044439300_cit41","doi-asserted-by":"publisher","first-page":"39456","DOI":"10.1074\/jbc.M206452200","article-title":"A Novel Antioxidant Mechanism of\nEbselen Involving\nEbselen Diselenide, a Substrate of Mammalian Thioredoxin and Thioredoxin\nReductase","volume":"277","author":"Zhao","year":"2002","journal-title":"J. Biol. Chem."},{"issue":"6","key":"2026090117044439300_cit42","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1038\/nprot.2016.061","article-title":"Characterization\nof Proteins by In-Cell\nNMR Spectroscopy in Cultured Mammalian Cells","volume":"11","author":"Barbieri","year":"2016","journal-title":"Nat. Protoc."},{"issue":"24","key":"2026090117044439300_cit43","doi-asserted-by":"publisher","first-page":"12008","DOI":"10.1021\/ac502300q","article-title":"NMR Flow Tube for\nOnline NMR Reaction Monitoring","volume":"86","author":"Foley","year":"2014","journal-title":"Anal. Chem."},{"issue":"6","key":"2026090117044439300_cit44","doi-asserted-by":"publisher","first-page":"661","DOI":"10.1007\/BF02192855","article-title":"Gradient-Tailored\nExcitation for\nSingle-Quantum NMR Spectroscopy of Aqueous Solutions","volume":"2","author":"Piotto","year":"1992","journal-title":"J. Biomol. 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Chem."},{"issue":"3","key":"2026090117044439300_cit48","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1021\/ac00130a035","article-title":"Evolving Factor\nAnalysis for the Resolution of Overlapping Chromatographic Peaks","volume":"59","author":"Maeder","year":"1987","journal-title":"Anal. Chem."},{"issue":"5","key":"2026090117044439300_cit49","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1002\/(SICI)1099-128X(199709\/10)11:5&lt;393::AID-CEM483&gt;3.0.CO;2-L","article-title":"A Fast Non-Negativity-Constrained Least Squares Algorithm","volume":"11","author":"Bro","year":"1997","journal-title":"J. Chemom."},{"key":"2026090117044439300_cit50","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1016\/j.vascn.2018.11.004","article-title":"Development of a Bioreactor\nSystem for Cytotoxic Evaluation of Pharmacological Compounds in Living\nCells Using NMR Spectroscopy","volume":"95","author":"Carvalho","year":"2019","journal-title":"J. Pharmacol.\nToxicol. Methods"},{"issue":"6","key":"2026090117044439300_cit51","doi-asserted-by":"publisher","first-page":"2304","DOI":"10.1002\/anie.201912919","article-title":"Real\u25a1Time NMR\nSpectroscopy\nfor Studying Metabolism","volume":"59","author":"Alshamleh","year":"2020","journal-title":"Angew. Chem., Int.\nEd."},{"issue":"10","key":"2026090117044439300_cit52","doi-asserted-by":"publisher","first-page":"3886","DOI":"10.1002\/anie.201913585","article-title":"NMR Characterization of Surface Receptor Protein Interactions\nin Live Cells Using Methylcellulose Hydrogels","volume":"59","author":"Mateos","year":"2020","journal-title":"Angew. Chem., Int. Ed."}],"container-title":["Analytical Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.analchem.0c01677","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/ancham\/article-pdf\/92\/14\/9997\/67523353\/acs.analchem.0c01677.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/ancham\/article-pdf\/92\/14\/9997\/67523353\/acs.analchem.0c01677.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T21:04:48Z","timestamp":1788296688000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/ancham\/article\/92\/14\/9997\/826819\/Real-Time-Quantitative-In-Cell-NMR-Ligand-Binding"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,18]]},"references-count":52,"journal-issue":{"issue":"14","published-online":{"date-parts":[[2020,6,18]]},"published-print":{"date-parts":[[2020,7,21]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.analchem.0c01677","relation":{},"ISSN":["0003-2700","1520-6882"],"issn-type":[{"value":"0003-2700","type":"print"},{"value":"1520-6882","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,6,18]]}}}