{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,26]],"date-time":"2025-12-26T01:23:57Z","timestamp":1766712237758,"version":"build-2065373602"},"reference-count":58,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2021,4,28]],"date-time":"2021-04-28T00:00:00Z","timestamp":1619568000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP25291041","JP15H01359","JP16H04787","JP16H01317","JP18K19347","JP17K07397"],"award-info":[{"award-number":["JP25291041","JP15H01359","JP16H04787","JP16H01317","JP18K19347","JP17K07397"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100018732","name":"Ohsumi Frontier Science Foundation","doi-asserted-by":"publisher","award":["N\/A"],"award-info":[{"award-number":["N\/A"]}],"id":[{"id":"10.13039\/501100018732","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008732","name":"Uehara Memorial Foundation","doi-asserted-by":"publisher","award":["N\/A"],"award-info":[{"award-number":["N\/A"]}],"id":[{"id":"10.13039\/100008732","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005927","name":"Daiichi Sankyo Foundation of Life Science","doi-asserted-by":"publisher","award":["N\/A"],"award-info":[{"award-number":["N\/A"]}],"id":[{"id":"10.13039\/501100005927","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007802","name":"Institute for Fermentation, Osaka","doi-asserted-by":"publisher","award":["N\/A"],"award-info":[{"award-number":["N\/A"]}],"id":[{"id":"10.13039\/100007802","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004423","name":"Waseda University","doi-asserted-by":"publisher","award":["2017B-242, 2017B-243, 2018B-222, 2019C-570, 2020R-038, 2021C-227, 2018S-139, 2019C-571"],"award-info":[{"award-number":["2017B-242, 2017B-243, 2018B-222, 2019C-570, 2020R-038, 2021C-227, 2018S-139, 2019C-571"]}],"id":[{"id":"10.13039\/501100004423","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>The cytoskeleton microtubule consists of polymerized \u03b1\u03b2-tubulin dimers and plays essential roles in many cellular events. Reagents that inhibit microtubule behaviors have been developed as antifungal, antiparasitic, and anticancer drugs. Benzimidazole compounds, including thiabendazole (TBZ), carbendazim (MBC), and nocodazole, are prevailing microtubule poisons that target \u03b2-tubulin and inhibit microtubule polymerization. The molecular basis, however, as to how the drug acts on \u03b2-tubulin remains controversial. Here, we characterize the S. pombe \u03b2-tubulin mutant nda3-TB101, which was previously isolated as a mutant resistance to benzimidazole. The mutation site tyrosine at position 50 is located in the interface of two lateral \u03b2-tubulin proteins and at the gate of a putative binging pocket for benzimidazole. Our observation revealed two properties of the mutant tubulin. First, the dynamics of cellular microtubules comprising the mutant \u03b2-tubulin were stabilized in the absence of benzimidazole. Second, the mutant protein reduced the affinity to benzimidazole in vitro. We therefore conclude that the mutant \u03b2-tubulin Nda3-TB101 exerts a dual effect on microtubule behaviors: the mutant \u03b2-tubulin stabilizes microtubules and is insensitive to benzimidazole drugs. This notion fine-tunes the current elusive molecular model regarding binding of benzimidazole to \u03b2-tubulin.<\/jats:p>","DOI":"10.3390\/cells10051042","type":"journal-article","created":{"date-parts":[[2021,4,28]],"date-time":"2021-04-28T10:41:58Z","timestamp":1619606518000},"page":"1042","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Dual Impact of a Benzimidazole Resistant \u03b2-Tubulin on Microtubule Behavior in Fission Yeast"],"prefix":"10.3390","volume":"10","author":[{"given":"Mamika","family":"Minagawa","sequence":"first","affiliation":[{"name":"Laboratory of Cytoskeletal Logistics, Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Minamo","family":"Shirato","sequence":"additional","affiliation":[{"name":"Laboratory of Cytoskeletal Logistics, Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mika","family":"Toya","sequence":"additional","affiliation":[{"name":"Laboratory of Cytoskeletal Logistics, Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan"},{"name":"Faculty of Science and Engineering, Global Center for Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan"},{"name":"Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7974-4157","authenticated-orcid":false,"given":"Masamitsu","family":"Sato","sequence":"additional","affiliation":[{"name":"Laboratory of Cytoskeletal Logistics, Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan"},{"name":"Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan"},{"name":"Institute for Medical-Oriented Structural Biology, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1038\/34465","article-title":"Structure of the \u03b1\u03b2 tubulin dimer by electron crystallography","volume":"391","author":"Nogales","year":"1998","journal-title":"Nature"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1038\/nrm.2016.45","article-title":"microtubules: 50 years on from the discovery of tubulin","volume":"17","author":"Borisy","year":"2016","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1146\/annurev.cellbio.13.1.83","article-title":"Microtubule polymerization dynamics","volume":"13","author":"Desai","year":"1997","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/S0074-7696(04)41002-X","article-title":"Microtubule-associated proteins and their essential roles during mitosis","volume":"241","author":"Maiato","year":"2004","journal-title":"Int. Rev. Cytol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3988","DOI":"10.1073\/pnas.1014758108","article-title":"GTP\u03b3S microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs)","volume":"108","author":"Maurer","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/j.cell.2012.02.049","article-title":"EBs recognize a nucleotide-dependent structural cap at growing microtubule ends","volume":"149","author":"Maurer","year":"2012","journal-title":"Cell"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.cell.2007.11.043","article-title":"XMAP215 is a processive microtubule polymerase","volume":"132","author":"Brouhard","year":"2008","journal-title":"Cell"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.1101\/gad.9.13.1572","article-title":"P93dis1, which is required for sister chromatid separation, is a novel microtubule and spindle pole body-associating protein phosphorylated at the Cdc2 target sites","volume":"9","author":"Nabeshima","year":"1995","journal-title":"Genes Dev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1016\/S0960-9822(01)00155-5","article-title":"M phase-specific kinetochore proteins in fission yeast: Microtu-bule-associating Dis1 and Mtc1 display rapid separation and segregation during anaphase","volume":"11","author":"Nakaseko","year":"2001","journal-title":"Curr. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/emboj\/20.13.3389","article-title":"Fission yeast ch-TOG\/XMAP215 homologue Alp14 connects mitotic spindles with the kinetochore and is a component of the Mad2-dependent spindle checkpoint","volume":"20","author":"Garcia","year":"2001","journal-title":"EMBO J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2878","DOI":"10.1091\/mbc.e12-03-0205","article-title":"Fission yeast Alp14 is a dose-dependent plus end\u2013tracking microtubule polymerase","volume":"23","author":"Kim","year":"2012","journal-title":"Mol. Biol. Cell"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/S0092-8674(00)80991-5","article-title":"XKCM1: A xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly","volume":"84","author":"Walczak","year":"1996","journal-title":"Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/S0092-8674(00)80960-5","article-title":"Kin I kinesins are microtubule-destabilizing enzymes","volume":"96","author":"Desai","year":"1999","journal-title":"Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.ceb.2006.12.009","article-title":"Microtubule polymerases and depolymerases","volume":"19","author":"Howard","year":"2007","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3919","DOI":"10.1091\/mbc.12.12.3919","article-title":"Two related kinesins, klp5+andklp6+, foster microtubule disassembly and are required for meiosis in fission yeast","volume":"12","author":"West","year":"2001","journal-title":"Mol. Biol. Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1016\/S0960-9822(02)00761-3","article-title":"Two kinesin-like kin I family proteins in fission yeast regulate the establishment of metaphase and the onset of anaphase A","volume":"12","author":"Garcia","year":"2002","journal-title":"Curr. Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1091\/mbc.e08-09-0979","article-title":"Kinesin-8 from fission yeast: A hetero-dimeric, plus-end-directed motor that can couple microtubule depolymerization to cargo movement","volume":"20","author":"Grissom","year":"2009","journal-title":"Mol. Biol. Cell"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1146\/annurev.py.24.090186.000355","article-title":"Benzimidazole fungicides: Mechanism of action and biological impact","volume":"24","author":"Davidse","year":"1986","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1002\/med.2610130205","article-title":"Antimitotic agents: Chemistry and recognition of tubulin molecule","volume":"13","author":"Iwasaki","year":"1993","journal-title":"Med. Res. Rev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1002\/cm.970170204","article-title":"Identification of an amino acid substitution in the benA, \u03b2-tubulin gene of Aspergillus nidulans that confers thiabendazole resistance and benomyl supersensitivity","volume":"17","author":"Jung","year":"1990","journal-title":"Cell Motil. Cytoskelet."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1002\/cm.970220304","article-title":"Amino acid alterations in the benA (\u03b2-tubulin) gene of Aspergillus nidulans that confer benomyl resistance","volume":"22","author":"Jung","year":"1992","journal-title":"Cell Motil. Cytoskelet."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1007\/BF00351701","article-title":"A single amino-acid substitution in the beta-tubulin gene of Neurospora confers both carbendazim resistance and diethofencarb sensitivity","volume":"21","author":"Fujimura","year":"1992","journal-title":"Curr. Genet."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.funbio.2013.12.001","article-title":"The Podosphaera fusca TUB2 gene, a molecular \u201cSwiss Army knife\u201d with multiple applications inpowdery mildew research","volume":"118","year":"2014","journal-title":"Fungal Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1478","DOI":"10.1094\/Phyto-83-1478","article-title":"Mutations leading to substitutions at amino acids 198 and 200 of beta-tubulin that correlate with be-nomyl-resistance phenotypes of field strains of Botrytis cinerea","volume":"83","author":"Yarden","year":"1993","journal-title":"Phytopathology"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1091\/mbc.5.1.29","article-title":"Systematic mutational analysis of the yeast \u03b2-tubulin gene","volume":"5","author":"Reijo","year":"1994","journal-title":"Mol. Biol. Cell"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1006\/pest.1999.2406","article-title":"Mutations of the \u03b2-Tubulin gene associated with different phenotypes of benzimidazole resistance in the cereal eyespot fungi Tapesia yallundae and Tapesia acuformis","volume":"64","author":"Albertini","year":"1999","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/0166-6851(94)90066-3","article-title":"Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in \u03b2-tubulin isotype 1","volume":"63","author":"Kwa","year":"1994","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/S1471-4922(01)01983-3","article-title":"Genetic variability following selection of Haemonchus contortus with anthelmintics","volume":"17","author":"Prichard","year":"2001","journal-title":"Trends Parasitol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/0092-8674(84)90319-2","article-title":"Identification of the pleiotropic cell division cycle gene NDA2 as one of two different \u03b1-tubulin genes in schizosaccharomyces pombe","volume":"37","author":"Toda","year":"1984","journal-title":"Cell"},{"key":"ref_30","first-page":"2168","article-title":"Differential expressions of essential and nonessential \u03b1-tubulin genes in Schiz-osaccharomyces pombe","volume":"6","author":"Adachi","year":"1986","journal-title":"Mol. Cell Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/0092-8674(84)90013-8","article-title":"The NDA3 gene of fission yeast encodes \u03b2-tubulin: A cold-sensitive nda3 mutation re-versibly blocks spindle formation and chromosome movement in mitosis","volume":"39","author":"Hiraoka","year":"1984","journal-title":"Cell"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1007\/BF00267375","article-title":"Genetic analysis of resistant mutants to antimitotic benzimidazole compounds in Schizosaccharomyces pombe","volume":"180","author":"Yamamoto","year":"1980","journal-title":"Mol. Genet. Genom."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/S0022-2836(83)80018-7","article-title":"Two cell division cycle genes NDA2 and NDA3 of the fission yeast Schiz-osaccharomyces pombe control microtubular organization and sensitivity to anti-mitotic benzimidazole compounds","volume":"168","author":"Umesono","year":"1983","journal-title":"J. Mol. Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"7161","DOI":"10.1038\/s41598-018-25336-5","article-title":"Analysis of \u03b2-tubulin-carbendazim interaction reveals that binding site for MBC fungicides does not include residues involved in fungicide resistance","volume":"8","author":"Romero","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1016\/0076-6879(91)94059-L","article-title":"[56] Molecular genetic analysis of fission yeast Schizosaccharomyces pombe","volume":"194","author":"Moreno","year":"1991","journal-title":"Methods Enzymol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1002\/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y","article-title":"Heter-ologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe","volume":"14","author":"Wu","year":"1998","journal-title":"Yeast"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1002\/yea.1233","article-title":"New drug-resistant cassettes for gene disruption and epitope tagging inSchizosaccharomyces pombe","volume":"22","author":"Sato","year":"2005","journal-title":"Yeast"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1007\/978-1-60327-993-2_11","article-title":"Visualization of fluorescence-tagged proteins in fission yeast: The analysis of mitotic spindle dynamics using GFP-tubulin under the native promoter","volume":"545","author":"Sato","year":"2009","journal-title":"Methods Mol. Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1038\/nprot.2009.2","article-title":"Protein structure prediction on the Web: A case study using the Phyre server","volume":"4","author":"Kelley","year":"2009","journal-title":"Nat. Protoc."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1799","DOI":"10.1091\/mbc.e11-11-0951","article-title":"Spindle pole body components are reorganized during fission yeast meiosis","volume":"23","author":"Ohta","year":"2012","journal-title":"Mol. Biol. Cell"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An open-source platform for bio-logical-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.4161\/cc.28294","article-title":"Dissecting the first and the second meiotic divisions using a marker-less drug-hypersensitive fission yeast","volume":"13","author":"Aoi","year":"2014","journal-title":"Cell Cycle"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"S3947","DOI":"10.1016\/j.arabjc.2014.06.001","article-title":"Interaction of anthelmintic drug (thiabendazole) with DNA: Spectroscopic and molecular modeling studies","volume":"10","author":"Jalali","year":"2017","journal-title":"Arab. J. Chem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/S0092-8674(00)80961-7","article-title":"High-Resolution Model of the Microtubule","volume":"96","author":"Nogales","year":"1999","journal-title":"Cell"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1022","DOI":"10.1016\/j.str.2010.05.010","article-title":"Structural basis of interprotofilament interaction and lateral deformation of microtubules","volume":"18","author":"Sui","year":"2010","journal-title":"Structure"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1016\/j.cell.2015.07.012","article-title":"Mechanistic origin of microtubule dynamic instability and its modulation by eb proteins","volume":"162","author":"Zhang","year":"2015","journal-title":"Cell"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.jmgm.2004.08.001","article-title":"A possible model of benzimidazole binding to \u03b2-tubulin disclosed by invoking an inter-domain movement","volume":"23","author":"Robinson","year":"2004","journal-title":"J. Mol. Graph. Model."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1242\/jcs.00925","article-title":"Role of microtubules and tea1p in establishment and maintenance of fission yeast cell polarity","volume":"117","author":"Sawin","year":"2004","journal-title":"J. Cell Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1016\/j.chembiol.2012.06.008","article-title":"Analyzing Fission Yeast Multidrug Resistance Mechanisms to Develop a Genetically Tractable Model System for Chemical Biology","volume":"19","author":"Kawashima","year":"2012","journal-title":"Chem. Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1083\/jcb.153.2.397","article-title":"A Mechanism for nuclear positioning in fission yeast based on microtubule pushing","volume":"153","author":"Tran","year":"2001","journal-title":"J. Cell Biol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/j.cub.2004.03.029","article-title":"The microtubule plus end-tracking proteins mal3p and tip1p cooperate for cell-end targeting of interphase microtubules","volume":"14","author":"Busch","year":"2004","journal-title":"Curr. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1083\/jcb.139.3.717","article-title":"Mal3, the fission yeast homologue of the human APC-interacting protein EB-1 is required for microtubule integrity and the maintenance of cell form","volume":"139","author":"Beinhauer","year":"1997","journal-title":"J. Cell Biol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1965","DOI":"10.1083\/jcb.127.6.1965","article-title":"Direct visualization of the microtubule lattice seam both in vitro and in vivo","volume":"127","author":"Kikkawa","year":"1994","journal-title":"J. Cell Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"15205","DOI":"10.1016\/S0021-9258(18)68165-7","article-title":"The GTP-binding peptide of \u03b2-tubulin. Localization by direct photoaffinity labeling and com-parison with nucleotide-binding proteins","volume":"263","author":"Linse","year":"1988","journal-title":"J. Biol. Chem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1038\/nsmb.1482","article-title":"Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice","volume":"15","author":"Katsuki","year":"2008","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Zanic, M., Stear, J.H., Hyman, A.A., and Howard, J. (2009). EB1 recognizes the nucleotide state of tubulin in the microtubule lattice. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0007585"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1517\/14728222.4.2.219","article-title":"Structural basis for the action of drugs that affect microtubule dynamics","volume":"4","author":"Downing","year":"2000","journal-title":"Emerg. Ther. Targets"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1002\/cmdc.201700530","article-title":"Effects of the Protonation State of Titratable Residues and the Presence of Water Molecules on Nocodazole Binding to \u03b2-Tubulin","volume":"13","author":"Castillo","year":"2018","journal-title":"Chem. Med. Chem."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/10\/5\/1042\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:54:42Z","timestamp":1760162082000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/10\/5\/1042"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,28]]},"references-count":58,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["cells10051042"],"URL":"https:\/\/doi.org\/10.3390\/cells10051042","relation":{},"ISSN":["2073-4409"],"issn-type":[{"type":"electronic","value":"2073-4409"}],"subject":[],"published":{"date-parts":[[2021,4,28]]}}}