Cited by 501Alzheimer's disease research and treatmentsMicrotubule and mitosis dynamicsNeuroinflammation and Neurodegeneration Mechanisms

The DOI matches its Crossref record; 64 of the 66 references it cites were found in a registry or an index.

The microtubule binding domain of tau protein

Lee, Gloria, Neve, Rachael L., Kosik, Kenneth S.·1989·Neuron

DOI 10.1016/0896-6273(89)90050-0

Open this paper in CoChat — free account

Abstract

Tau protein is a microtubule-associated protein implicated in the spatial and temporal specification of microtubules and has been found in the neurofibrillary tangles of Alzheimer's disease. Determination of tau protein structure has revealed three 18 amino acid repeated sequences hypothesized to be tubulin binding sites. Using tau cDNA clones from human fetal brain, we employed E. coli expression systems to synthesize tau protein and fragments of tau protein in order to identify the microtubule binding site. A fragment containing the three repeated sequences binds microtubules, while the amino-terminal half of the protein does not bind. Fragments containing two or one repeat are also capable of binding, indicating that the basic tubulin interacting unit is one repeat.

Integrity signals

Registry

Crossref · 10.1016/0896-6273(89)90050-0

Cites

64 of 64 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589
DNA sequencing with chain-terminating inhibitors
Sanger, F., Nicklen, S., & Coulson, A. R. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.12.5463 · Cited by 68,572
A new method for sequencing DNA.
Maxam, A. M., & Gilbert, W. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.2.560 · Cited by 7,929
A protein factor essential for microtubule assembly
Weingarten, M. D., Lockwood, A. H., Hwo, S. Y., & Kirschner, M. W. (1975) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.72.5.1858 · Cited by 3,089
Ultrasensitive Stain for Proteins in Polyacrylamide Gels Shows Regional Variation in Cerebrospinal Fluid Proteins
Merril, C. R., Goldman, D. A., Sedman, S. A., & Ebert, M. H. (1981) · Science · doi:10.1126/science.6162199 · Cited by 2,933
Microtubule-associated protein tau. A component of Alzheimer paired helical filaments.
Grundke, I., Iqbal, K., Quinlan, M., Tung, Y. C., Zaidi, M. S., & Wisniewski, H. M. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)38495-8 · Cited by 1,780
The distribution of tau in the mammalian central nervous system.
Binder, L. I., Frankfurter, A., & Rebhun, L. I. (1985) · The Journal of cell biology · doi:10.1083/jcb.101.4.1371 · Cited by 1,588
Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease.
Kosik, K. S., Joachim, C. L., & Selkoe, D. J. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.11.4044 · Cited by 1,491
Self-citation
Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau
Goedert, M., Wischik, C. M., Crowther, R. A., Walker, J. E., & Klug, A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.11.4051 · Cited by 1,134
A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: Application to sequencing the corn mitochondrial 18 S rDNA
Dale, R. M. K., McClure, B., & Houchins, J. P. (1985) · Plasmid · doi:10.1016/0147-619x(85)90053-8 · Cited by 1,043
Cloning and sequencing of the cDNA encoding an isoform of microtubule‐associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain.
Goedert, M., Spillantini, M. G., Potier, M. C., Ulrich, J., & Crowther, R. A. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03390.x · Cited by 1,037
Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease.
Wischik, C. M., Novak, M., Thøgersen, H. C., Edwards, P. C., Runswick, M. J., Jakes, R., Walker, J. E., Milstein, C., Roth, M., & Klug, A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.12.4506 · Cited by 939
Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin
Cleveland, D. W., Hwo, S.-Y., & Kirschner, M. W. (1977) · Journal of Molecular Biology · doi:10.1016/0022-2836(77)90213-3 · Cited by 915
Phosphorylation affects the ability of tau protein to promote microtubule assembly.
Lindwall, G., & Cole, R. D. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42989-9 · Cited by 901
Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly
Cleveland, D. W., Hwo, S. Y., & Kirschner, M. W. (1977) · Journal of Molecular Biology · doi:10.1016/0022-2836(77)90214-5 · Cited by 881
Tau protein function in living cells.
Drubin, D. G., & Kirschner, M. W. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.103.6.2739 · Cited by 766
Neurofibrillary tangles of Alzheimer disease share antigenic determinants with the axonal microtubule-associated protein tau (tau)
Wood, J. G., Mirra, S. S., Pollock, N. J., & Binder, L. I. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.11.4040 · Cited by 763
IN VITRO SYNTHESIS OF PROTEIN IN MICROBIAL SYSTEMS
Zubay, G. (1973) · Annual Review of Genetics · doi:10.1146/annurev.ge.07.120173.001411 · Cited by 699
The Primary Structure and Heterogeneity of Tau Protein from Mouse Brain
Lee, G. S., Cowan, N. J., & Kirschner, M. W. (1988) · Science · doi:10.1126/science.3122323 · Cited by 680
Self-citation
Developmentally regulated expression of specific tau sequences
Kosik, K. S., Orecchio, L. D., Bakalis, S., & Neve, R. L. (1989) · Neuron · doi:10.1016/0896-6273(89)90077-9 · Cited by 598
Self-citation
Identification of cDNA clones for the human microtubule-associated protein tau and chromosomal localization of the genes for tau and microtubule-associated protein 2
Neve, R. L., Harris, P. K. W., Kosik, K. S., Kurnit, D. M., & Donlon, T. A. (1986) · Molecular Brain Research · doi:10.1016/0169-328x(86)90033-1 · Cited by 565
Self-citation
Tau Consists of a Set of Proteins with Repeated C-Terminal Microtubule-Binding Domains and Variable N-Terminal Domains
Himmler, A., Drechsel, D. N., Kirschner, M. W., & Martin, D. W. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.4.1381-1388.1989 · Cited by 555
A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs).
Vallee, R. B. (1982) · The Journal of cell biology · doi:10.1083/jcb.92.2.435 · Cited by 551
The periodic association of MAP2 with brain microtubules in vitro.
Kim, H., Binder, L. I., & Rosenbaum, J. L. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.80.2.266 · Cited by 512
Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors.
Drubin, D. G., Feinstein, S. C., Shooter, E. M., & Kirschner, M. W. (1985) · The Journal of Cell Biology · doi:10.1083/jcb.101.5.1799 · Cited by 510
Microtubule-Associated Protein MAP2 Shares a Microtubule Binding Motif with Tau Protein
Lewis, S. A., Wang, D. H., & Cowan, N. J. (1988) · Science · doi:10.1126/science.3142041 · Cited by 483
Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22
Hultmark, D. (1986) · Cell · doi:10.1016/0092-8674(86)90464-2 · Cited by 455
‘ATG vectors’ for regulated high-level expression of cloned genes in Escherichia coli
Amann, E. P., & Brosius, J. (1985) · Gene · doi:10.1016/0378-1119(85)90041-1 · Cited by 391
Tau proteins: the molecular structure and mode of binding on microtubules.
Hirokawa, N., Shiomura, Y., & Okabe, S. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.107.4.1449 · Cited by 389
MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: an immunocytochemical study of cultured rat cerebrum
Kosik, K., & Finch, E. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-10-03142.1987 · Cited by 368
Self-citation
The car☐yl third of tau is tightly bound to paired helical filaments
Kondo, J., Honda, T., Mori, H., Hamada, Y., Miura, R., OGAWARA, M., & Ihara, Y. (1988) · Neuron · doi:10.1016/0896-6273(88)90130-4 · Cited by 357
A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end.
Gard, D. L., & Kirschner, M. W. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.5.2203 · Cited by 354
Microtubule Assembly in vitro. Purification of Assembly-Promoting Factors
Fellous, A., Francon, J., Lennon, A. M., & Nunez, J. (1977) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1977.tb11726.x · Cited by 339
One of the Antigenic Determinants of Paired Helical Filaments Is Related to Tau Protein1
Nukina, N., & Ihara, Y. (1986) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a135625 · Cited by 338
Fractionation of Brain Microtubule‐Associated Proteins
HERZOG, W., & Weber, K. K. (1978) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1978.tb12716.x · Cited by 311
The preferential translation of Drosophila hsp70 mRNA requires sequences in the untranslated leader
McGarry, T. J., & Lindquist, S. L. (1985) · Cell · doi:10.1016/0092-8674(85)90286-7 · Cited by 289
Enhanced translation of chimaeric messenger RNAs containing a plant viral untranslated leader sequence
Jobling, S. A., & Gehrke, L. (1987) · Nature · doi:10.1038/325622a0 · Cited by 283
Biochemical and immunological analyses of cytoskeletal domains of neurons.
Peng, I., Binder, L. I., & Black, M. M. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.102.1.252 · Cited by 230
Maximizing Gene Expression
(1986) · Elsevier eBooks · doi:10.1016/c2013-0-01063-8 · Cited by 219
Common and distinct tubulin binding sites for microtubule-associated proteins.
Littauer, U. Z., Giveon, D., Thierauf, M., Ginzburg, I., & Ponstingl, H. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.19.7162 · Cited by 217
Mise en évidence immunologique de la protéine tau au niveau des lésions de dégénérescence neurofibrillaire de la maladie d'Alzheimer
Brion, J., Passareiro, H., Nunez, J., & Durand, J. F. (1985) · Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) · Cited by 197
Identity and polymerization-stimulatory activity of the nontubulin proteins associated with microtubules
Murphy, D. B., Vallee, R. B., & Borisy, G. G. (1977) · Biochemistry · doi:10.1021/bi00631a004 · Cited by 186
Studies on the expression of the microtubule-associated protein, tau, during mouse brain development, with newly isolated complementary DNA probes.
Drubin, D. G., Caput, D., & Kirschner, M. W. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.98.3.1090 · Cited by 164
Changes in composition and activity of microtubule-associated proteins during brain development
Mareck, A., Fellous, A., Francon, J., & Nunez, J. (1980) · Nature · doi:10.1038/284353a0 · Cited by 160
Regulation of microtubule protein levels during cellular morphogenesis in nerve growth factor-treated PC12 cells.
Drubin, D. G., Kobayashi, S., Kellogg, D. R., & Kirschner, M. W. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.106.5.1583 · Cited by 160
Heterogeneity of Microtubule‐Associated Proteins and Brain Development
Francon, J., Lennon, A. M., Fellous, A., Mareck, A., Pierre, M., & Nunez, J. (1982) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1982.tb07072.x · Cited by 155
Highly conserved sequencim in the 3′ untranslated region of mRNAs coding for homologous proteins in distantly related species
Yaffe, D., Nudel, U., Mayer, Y., & Neuman, S. (1985) · Nucleic Acids Research · doi:10.1093/nar/13.10.3723 · Cited by 153
Localization of the tubulin binding site for tau protein
Serrano, L. G., de Garcini, E. M., HERNÁNDEZ, M. A., & Ávila, J. (1985) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1985.tb09342.x · Cited by 136
Polycation-induced assembly of purified tubulin.
Erickson, H., & Voter, W. A. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.8.2813 · Cited by 129
Identification of three coated vesicle components as alpha- and beta-tubulin linked to a phosphorylated 50,000-dalton polypeptide.
Pfeffer, S. R., Drubin, D. G., & Kelly, R. B. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.97.1.40 · Cited by 129
Tau Epitopes are Incorporated into a Range of Lesions in Alzheimerʼs Disease
Joachim, C. L., Morris, J. H., Selkoe, D. J., & Kosik, K. S. (1987) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-198711000-00001 · Cited by 100
Self-citation
DNA-directed peptide synthesis. II. The synthesis of the alpha-fragment of the enzyme beta-galactosidase.
DeVries, J. K., & Zubay, G. (1967) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.57.4.1010 · Cited by 93
Association of Tau Protein with Microtubules in Living Cells
Drubin, D. G., KOBAYASHI, S., & Kirschner, M. W. (1986) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1986.tb38398.x · Cited by 91
In vitro reconstitution of calf brain microtubules: effects of macromolecules
Lee, J. C., Tweedy, N. B., & Timasheff, S. N. (1978) · Biochemistry · doi:10.1021/bi00607a013 · Cited by 90
[11] Purification of brain microtubules and microtubule-associated protein 1 using taxol
Vallee, R. B. (1986) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(86)34079-5 · Cited by 84
Cell-free synthesis of proteins coding for mobilisation functions of ColE1 and transposition functions of Tn3
Collins, J. F. (1979) · Gene · doi:10.1016/0378-1119(79)90083-0 · Cited by 79
Temperature-dependent reversible assembly of taxol-treated microtubules.
Collins, C. A., & Vallee, R. B. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.6.2847 · Cited by 65
Microtubule-binding domain of tau proteins.
Aizawa, H., Kawasaki, H., Murofushi, H., Kotani, S., Suzuki, K., & Sakai, H. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)68555-2 · Cited by 63
Microtubule‐associated protein MAP1 promotes microtubule assembly in vitro
Kuznetsov, S., Rodionov, V., Gelfand, V. I., & Rosenblat, V. A. (1981) · FEBS Letters · doi:10.1016/0014-5793(81)80791-0 · Cited by 61
High-level expression of a proteolytically sensitive diphtheria toxin fragment in Escherichia coli
Bishai, W. R., Rappuoli, R., & Murphy, J. R. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.11.5140-5151.1987 · Cited by 56
A comparative study of the in vitro polymerization of tubulin in the presence of the microtubule-associated proteins MAP2 and tau.
Sandoval, I. V., & Vandekerckhove, J. S. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)68915-5 · Cited by 52
A distinct form of tau is selectively incorporated into Alzheimer's paired helical filaments
Mori, H., Hamada, Y., Kawaguchi, M., Honda, T., Kondo, J., & Ihara, Y. (1989) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(89)92240-7 · Cited by 50
Gamma-actin: unusual mRNA 3'-untranslated sequence conservation and amino acid substitutions that may be cancer related.
Chou, C. C., Davis, R. C., Fuller, M. L., Slovin, J. P., Wong, A., WRIGHT, J. M., Kania, S. A., Shaked, R., Gatti, R. A., & Salser, W. A. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.9.2575 · Cited by 39
Optional exon in the 5'-untranslated region of 3-hydroxy-3-methylglutaryl coenzyme A synthase gene: conserved sequence and splicing pattern in humans and hamsters.
Gil, G., Smith, J. R., Goldstein, J. L., & Brown, M. S. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.7.1863 · Cited by 35

Sorted by citations

The molecular pathology of Alzheimer's disease
Selkoe, D. J. (1991) · Neuron · doi:10.1016/0896-6273(91)90052-2 · Cited by 2,708
Neurodegenerative Tauopathies
Lee, V. M.-Y., Goedert, M., & Trojanowski, J. Q. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1121 · Cited by 2,480
Tau-mediated neurodegeneration in Alzheimer’s disease and related disorders
Ballatore, C., Lee, V. M.-Y., & Trojanowski, J. Q. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2194 · Cited by 2,174
Tau protein isoforms, phosphorylation and role in neurodegenerative disorders11These authors contributed equally to this work.
Buée, L., Bussière, T., Buée‐Scherrer, V., Delacourte, A., & Hof, P. R. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(00)00019-9 · Cited by 2,142
A68: a Major Subunit of Paired Helical Filaments and Derivatized Forms of Normal Tau
Lee, V. M.-Y., Balin, B. J., Otvos, L., & Trojanowski, J. Q. (1991) · Science · doi:10.1126/science.1899488 · Cited by 1,418

See all 501

Authors: Lee, G., Neve, R. L., & Kosik, K. S.
Affiliations: Brigham and Women's Hospital (US)
Boston Children's Hospital (US)
ORCID: Lee, Gloria
Neve, Rachael L.
Kosik, Kenneth S.
Venue: Neuron
Publisher: Elsevier BV
Published: 1989-06
Volume: 2
Issue: 6
Pages: 1615-1624
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/0896-6273(89)90050-0
OpenAlex: W1972355725
Cited by: 500
References: 66
Citations by year: 2026: 8 · 2025: 13 · 2024: 13 · 2023: 19 · 2022: 12 · 2021: 19 · 2020: 14 · 2019: 17 · 2018: 13 · 2017: 13 · 2016: 8 · 2015: 12 · 2014: 13 · 2013: 13 · 2012: 13
FWCI: 14.86
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r29gm039300-05, 5r01ag006601-13)
National Institute on Aging (R01 AG06601-01)
National Institute of General Medical Sciences (R29 GM39300-01)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: tau protein, microtubule-binding site, microtubule-associated proteins, tubulin binding, neurofibrillary tangles, Alzheimer's disease, protein structure
MeSH terms: Amino Acid Sequence, Base Sequence, Binding Sites, DNA, Humans, Microtubule-Associated Proteins, Microtubules, Molecular Sequence Data, Protein Binding, Recombinant Fusion Proteins, Repetitive Sequences, Nucleic Acid, Sequence Homology, Nucleic Acid, Tubulin, tau Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

The microtubule binding domain of tau protein

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks