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Aberrations in tau-MT binding are linked to several neurodegenerative diseases. Little is known about how regions outside the four canonical MT-binding repeat regions of tau protein (R1\u2013R4) are involved in MT binding. Here, we synthesize a tau protein fragment (tau368\u2013412, R\u2019 domain), a flanking domain downstream of the R4 domain, without and with fluorine labels incorporated at its aromatic (Phe378, Tyr394) and proline (Pro397, Pro405, with 2S,4R stereochemistry) residues. The 1H and 13C chemical shift data point to slight secondary structural propensities in tau peptide and confirm that its predominantly disordered structure is largely preserved after fluorination. The NMR chemical shift and NOESY data detect and quantify cis-Pro at Pro397 and Pro405 positions, and the MD simulation data suggest that the cis\/trans isomerization of these two prolines could alter the conformational ensemble of the tau peptide. Through combined 1H and 13C NMR chemical shift and 19F chemical shift, relaxation, and dark-state exchange saturation transfer (DEST) analyses, we reveal a rapid exchange process between free tau peptide and a lowly populated MT-bound state that occurs on a submillisecond time scale (\u03c4ex \u223c 500 \u03bcs). The 19F DEST data also demonstrate that the MT binding predominantly occurs at the N-terminal region of the tau peptide adjacent to the canonical R4 domain and that it retains a large level of side-chain dynamics in the MT-bound state. Our study provides mechanistic insight into tau-MT binding and exemplifies how novel 19F NMR-based methods enable investigating proteins in the context of challenging large systems.<\/jats:p>","DOI":"10.1021\/acs.jpcb.6c04549","type":"journal-article","created":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T17:02:05Z","timestamp":1790010125000},"page":"10206-10221","source":"Crossref","is-referenced-by-count":0,"title":["Microtubule Binding\nof a Tau Peptide Monitored through\nFluorine NMR Probes"],"prefix":"10.1021","volume":"130","author":[{"given":"Kalyan S.","family":"Chakrabarti","sequence":"first","affiliation":[{"name":"Krea University , , , ,","place":["Sri City, Andhra Pradesh, India, 517646"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luigi","family":"Russo","sequence":"additional","affiliation":[{"name":"University of Campania-Luigi Vanvitelli , , Viale Abramo Lincoln 5 , ,","place":["Caserta, Italy, 81100"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dipendu","family":"Dhar","sequence":"additional","affiliation":[{"name":"Leibniz Institute of Plant Biochemistry , , Weinberg 3 , ,","place":["Halle, Germany, 06120"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kerstin","family":"Overkamp","sequence":"additional","affiliation":[{"name":"Max Planck Institute for Multidisciplinary Sciences , , Am Fa\u00dfberg 11 , ,","place":["Go\u0308ttingen, Germany, 37077"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0089-7156","authenticated-orcid":true,"given":"Mehdi D.","family":"Davari","sequence":"additional","affiliation":[{"name":"Leibniz Institute of Plant Biochemistry , , Weinberg 3 , ,","place":["Halle, Germany, 06120"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6935-6564","authenticated-orcid":true,"given":"Nasrollah","family":"Rezaei-Ghaleh","sequence":"additional","affiliation":[{"name":"University of Pavia , , Via Ferrata 9 , ,","place":["Pavia, Italy, 27100"]},{"name":"Heinrich Heine University (HHU) Du\u0308sseldorf , , Universita\u0308tsstra\u00dfe 1 , ,","place":["Du\u0308sseldorf, Germany, 40225"]},{"name":"Ju\u0308lich Forschungszentrum , , ,","place":["Ju\u0308lich, Germany, 52428"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,9,21]]},"reference":[{"issue":"17","key":"2026100109062418900_cit1","doi-asserted-by":"publisher","DOI":"10.1002\/chem.202203493","article-title":"Fast Motions\nDominate Dynamics of Intrinsically Disordered Tau Protein at High\nTemperatures","volume":"29","author":"Abyzov","year":"2023","journal-title":"Chemistry"},{"issue":"3","key":"2026100109062418900_cit2","doi-asserted-by":"publisher","first-page":"235","DOI":"10.2174\/092986606775338461","article-title":"Studying the natively\nunfolded neuronal Tau protein by solution NMR spectroscopy","volume":"13","author":"Lippens","year":"2006","journal-title":"Protein Pept. Lett."},{"issue":"2","key":"2026100109062418900_cit3","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1000034","article-title":"Structural polymorphism of 441-residue\ntau at single\nresidue resolution","volume":"7","author":"Mukrasch","year":"2009","journal-title":"PLoS Biol."},{"issue":"11","key":"2026100109062418900_cit4","doi-asserted-by":"publisher","first-page":"845","DOI":"10.1038\/s41580-024-00753-9","article-title":"Cellular and pathological\nfunctions of tau","volume":"25","author":"Parra Bravo","year":"2024","journal-title":"Nat. Rev. Mol. Cell Biol."},{"issue":"12","key":"2026100109062418900_cit5","doi-asserted-by":"publisher","first-page":"1887","DOI":"10.1091\/mbc.6.12.1887","article-title":"Domains of tau protein, differential phosphorylation,\nand dynamic instability of microtubules","volume":"6","author":"Trinczek","year":"1995","journal-title":"Mol.\nBiol. Cell"},{"key":"2026100109062418900_cit6","doi-asserted-by":"publisher","first-page":"1121","DOI":"10.1146\/annurev.neuro.24.1.1121","article-title":"Neurodegenerative tauopathies","volume":"24","author":"Lee","year":"2001","journal-title":"Annu. Rev. Neurosci."},{"key":"2026100109062418900_cit7","doi-asserted-by":"publisher","DOI":"10.1016\/j.pneurobio.2019.101644","article-title":"Four-repeat\ntauopathies","volume":"180","author":"Ro\u0308sler","year":"2019","journal-title":"Prog. Neurobiol."},{"issue":"1","key":"2026100109062418900_cit8","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1038\/nrn.2015.1","article-title":"Tau in physiology\nand pathology","volume":"17","author":"Wang","year":"2016","journal-title":"Nat. Rev. Neurosci."},{"key":"2026100109062418900_cit9","doi-asserted-by":"publisher","DOI":"10.3389\/fneur.2020.595532","article-title":"Tau Post-translational\nModifications:\nDynamic Transformers of Tau Function, Degradation, and Aggregation","volume":"11","author":"Alquezar","year":"2021","journal-title":"Front. Neurol."},{"issue":"52","key":"2026100109062418900_cit10","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2414176121","article-title":"GSK3\u03b2 phosphorylation catalyzes\nthe aggregation of tau into Alzheimer\u2019s disease-like filaments","volume":"121","author":"Chakraborty","year":"2024","journal-title":"Proc. Natl. Acad. Sci. 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Ed."},{"key":"2026100109062418900_cit13","doi-asserted-by":"publisher","DOI":"10.1016\/j.bpc.2023.107155","article-title":"Magnetic resonance investigation of conformational\nresponses of tau protein to specific phosphorylation","volume":"305","author":"Lasorsa","year":"2024","journal-title":"Biophys. Chem."},{"issue":"28","key":"2026100109062418900_cit14","doi-asserted-by":"publisher","DOI":"10.1002\/anie.202504292","article-title":"Multiple and\nAlternative Sites Make Tau Protein an Adaptable Sticky Surface for\nthe SH3 Domain of Fyn Kinase","volume":"64","author":"Tira","year":"2025","journal-title":"Angew. Chem.,\nInt. Ed."},{"issue":"22","key":"2026100109062418900_cit15","doi-asserted-by":"publisher","DOI":"10.1002\/cbic.202400566","article-title":"Untangling\nthe Complexity and Impact of Tau Protein Ubiquitination","volume":"25","author":"Trivellato","year":"2024","journal-title":"ChemBioChem"},{"issue":"32","key":"2026100109062418900_cit16","doi-asserted-by":"publisher","first-page":"9511","DOI":"10.1021\/bi00198a017","article-title":"Domains of tau protein and interactions\nwith microtubules","volume":"33","author":"Gustke","year":"1994","journal-title":"Biochemistry"},{"issue":"12","key":"2026100109062418900_cit17","doi-asserted-by":"publisher","first-page":"3246","DOI":"10.1002\/anie.201712089","article-title":"The Binding\nMode of a Tau Peptide with Tubulin","volume":"57","author":"Kadavath","year":"2018","journal-title":"Angew. Chem.,\nInt. 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Lett."},{"issue":"82","key":"2026100109062418900_cit29","doi-asserted-by":"publisher","first-page":"12404","DOI":"10.1039\/C9CC06124J","article-title":"A facile oxygen-17\nNMR method to determine effective viscosity in dilute, molecularly\ncrowded and confined aqueous media","volume":"55","author":"Rezaei-Ghaleh","year":"2019","journal-title":"Chem. Commun."},{"issue":"3","key":"2026100109062418900_cit30","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1007\/BF00197809","article-title":"NMRPipe: a multidimensional spectral\nprocessing system based on UNIX\npipes","volume":"6","author":"Delaglio","year":"1995","journal-title":"J. Biomol. 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Chem.\nSoc."},{"key":"2026100109062418900_cit37","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.104778","article-title":"Twelve phosphomimetic mutations induce\nthe assembly of recombinant full-length human tau into paired helical\nfilaments","volume":"14","author":"Lo\u0308vestam","year":"2026","journal-title":"eLife"},{"issue":"6","key":"2026100109062418900_cit38","doi-asserted-by":"publisher","first-page":"787","DOI":"10.1002\/cphc.200301051","article-title":"Approximate solutions\nof the Bloch-McConnell equations\nfor two-site chemical exchange","volume":"5","author":"Abergel","year":"2004","journal-title":"ChemPhysChem"},{"issue":"1","key":"2026100109062418900_cit39","doi-asserted-by":"publisher","first-page":"421","DOI":"10.5194\/mr-2-421-2021","article-title":"Extended Bloch-McConnell equations\nfor mechanistic analysis of hyperpolarized","volume":"2","author":"Eykyn","year":"2021","journal-title":"Magn. Reson."},{"key":"2026100109062418900_cit40","unstructured":"Molecular Operating\nEnvironment (MOE), version 02, 2022."},{"issue":"2","key":"2026100109062418900_cit41","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.softx.2015.06.001","article-title":"GROMACS: High performance\nmolecular simulations through multi-level parallelism from laptops\nto supercomputers","volume":"1\u20132","author":"Abraham","year":"2015","journal-title":"SoftwareX"},{"issue":"21","key":"2026100109062418900_cit42","doi-asserted-by":"publisher","first-page":"E4758","DOI":"10.1073\/pnas.1800690115","article-title":"Developing\na molecular dynamics force\nfield for both folded and disordered protein states","volume":"115","author":"Robustelli","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"issue":"23","key":"2026100109062418900_cit43","doi-asserted-by":"publisher","DOI":"10.1063\/1.2121687","article-title":"A general purpose model\nfor the condensed phases of\nwater: TIP4P\/2005","volume":"123","author":"Abascal","year":"2005","journal-title":"J. Chem. Phys."},{"issue":"19","key":"2026100109062418900_cit44","doi-asserted-by":"publisher","first-page":"8577","DOI":"10.1063\/1.470117","article-title":"A smooth particle\nmesh Ewald method","volume":"103","author":"Essmann","year":"1995","journal-title":"J. Chem. Phys."},{"issue":"12","key":"2026100109062418900_cit45","doi-asserted-by":"publisher","first-page":"1463","DOI":"10.1002\/(SICI)1096-987X(199709)18:12&lt;1463::AID-JCC4&gt;3.0.CO;2-H","article-title":"LINCS: A linear\nconstraint solver for molecular simulations","volume":"18","author":"Hess","year":"1997","journal-title":"J. Comput. Chem."},{"key":"2026100109062418900_cit46","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1080\/08927029108022142","article-title":"Generalized Verlet\nAlgorithm for Efficient Molecular Dynamics Simulations with Long-range\nInteractions","volume":"6","author":"Grubmu\u0308ller","year":"1991","journal-title":"Mol. Simul."},{"issue":"8","key":"2026100109062418900_cit47","doi-asserted-by":"publisher","first-page":"3684","DOI":"10.1063\/1.448118","article-title":"Molecular\ndynamics with coupling to an external bath","volume":"81","author":"Berendsen","year":"1984","journal-title":"J. Chem. Phys."},{"issue":"12","key":"2026100109062418900_cit48","doi-asserted-by":"publisher","first-page":"7182","DOI":"10.1063\/1.328693","article-title":"Polymorphic transitions\nin single crystals: A new molecular\ndynamics method","volume":"52","author":"Parrinello","year":"1981","journal-title":"J. Appl. Phys."},{"key":"2026100109062418900_cit49","doi-asserted-by":"crossref","unstructured":"Gowers, R. J.; Linke, M.; Barnoud, J.; Reddy, T.; Melo, M. N.; Seyler, S. L.; Domanski, J. J.; Dotson, D. L.; Buchoux, S.; Kenney, I. M.; Beckstein, O.\n          MDAnalysis: A\nPython Package\nfor the Rapid Analysis of Molecular Dynamics Simulations, 2016.","DOI":"10.25080\/Majora-629e541a-00e"},{"issue":"8","key":"2026100109062418900_cit50","doi-asserted-by":"publisher","first-page":"1528","DOI":"10.1016\/j.bpj.2015.08.015","article-title":"MDTraj:\nA Modern Open Library for the Analysis of Molecular\nDynamics Trajectories","volume":"109","author":"McGibbon","year":"2015","journal-title":"Biophys. J."},{"issue":"1","key":"2026100109062418900_cit51","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/0263-7855(96)00018-5","article-title":"VMD: Visual molecular dynamics","volume":"14","author":"Humphrey","year":"1996","journal-title":"J. Mol. 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