Cited by 333Alzheimer's disease research and treatmentsAdvanced Glycation End Products researchDementia and Cognitive Impairment Research

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Analysis of microtubule-associated protein tau glycation in paired helical filaments.

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Ledesma, M.D., Bonay, P., Colaço, C., Avila, J.·1994·Journal of Biological Chemistry

DOI 10.1016/s0021-9258(17)31849-5

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Abstract

Alzheimer's disease is typified by the characteristic histopathological lesions of neurofibrillar plaques and tangles. The latter are composed of paired helical filaments (PHFs), the major components of which are modified forms of the microtubule-associated protein tau. The exact nature of these modifications remains unknown, although the presence of hyperphosphorylated tau in PHFs argues strongly that phosphorylation is one of the modifications that result in the polymerization of tau into PHFs. However, hyperphosphorylation alone is insufficient to explain the formation of PHFs. In an attempt to characterize other post-translational modifications of PHF-tau, we have analyzed its glycation. A fraction of PHF-tau seems to be glycated in vivo, whereas soluble tau from either Alzheimer's disease or non-demented human brain is not glycated at all. Purified tau from bovine brain can be efficiently glycated in vitro. Tau glycation is accompanied by a decrease in the tau binding to tubulin. These results support the view that glycation may be one of the modifications hampering the binding of tau to tubulin in Alzheimer's disease, thus facilitating tau aggregation into PHFs.

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Background
Lipid peroxidation and advanced glycation end products in the brain in normal aging and in Alzheimer's disease
Dei, R., Takeda, A., Niwa, H., Li, M., Nakagomi, Y., Watanabe, M., Inagaki, T., Washimi, Y., Yasuda, Y., Horie, K., et al. (2002) · Acta Neuropathologica · doi:10.1007/s00401-002-0523-y · Cited by 179
Vitamin C and Vitamin E for Alzheimer's Disease
Boothby, L. A., & Doering, P. L. (2005) · Annals of Pharmacotherapy · doi:10.1345/aph.1e495 · Cited by 176
“9 years of treatment and included all of the following: (1) MMSE, (2) animal category, (3) letter fluency, (4) logical memory part 1, (5) logical memory part 2, (6) immediate recall, (7) word list, and (8) digits backwards.”
Background
Influence of advanced glycation end-products and AGE-inhibitors on nucleation-dependent polymerization of β-amyloid peptide
Münch, G. W., Mayer, S., Michaelis, J., Hipkiss, A. R., Riederer, P. F., Müller, R., Neumann, A., Schinzel, R., & Cunningham, A. M. (1997) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/s0925-4439(96)00062-2 · Cited by 174
Inflammation and NF-κB in Alzheimer's Disease and Diabetes
Granic, I., Dolga, A. M., Nijholt, I. M., van Dijk, G., & Eisel, U. L. M. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-0976 · Cited by 178
“Furthermore, glycation of A β enhances its aggregation in vitro [75], and glycated tau, in addition to hyperphosphorylation, appears to enhance the formation of paired helical ﬁlaments (PHFs) [76,77].”
The sour side of neurodegenerative disorders: the effects of protein glycation
Miranda, H. V., & Outeiro, T. F. (2009) · The Journal of Pathology · doi:10.1002/path.2682 · Cited by 172
“Tau glycation enhances the formation of paired helical filaments in AD and reduces its ability to bind microtubules in vitro [68].”
Background
Mitochondrial involvement in Alzheimer’s disease
Bonilla, E., Tanji, K., Hirano, M., Vu, T., DiMauro, S., & Schon, E. A. (1999) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00165-0 · Cited by 165
Glycation—a sweet tempter for neuronal death
Kikuchi, S. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00273-4 · Cited by 169
BACE1 is at the crossroad of a toxic vicious cycle involving cellular stress and β-amyloid production in Alzheimer’s disease
Chami, L., & Checler, F. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-52 · Cited by 168
AGEs/RAGE complex upregulates BACE1 via NF-κB pathway activation
Guglielmotto, M., Aragno, M., Tamagno, E., Vercellinatto, I., Visentin, S., Medana, C., Catalano, M. G., Smith, M. A., Perry, G. L., Danni, O., et al. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.05.026 · Cited by 163
“The involvement of AGEs in brain aging and in AD was reported more than 10 years ago, in studies that demonstrated that the microtubule associated tau protein as well as A are substrates for glycation (Ledesma et al., 1994; Smith et al., 1994; Vitek et al., 1994; Yan et al., 1994, 1995).”
Amyloidogenesis of Tau protein
Niżyński, B., Dzwolak, W., & Nieznański, K. (2017) · Protein Science · doi:10.1002/pro.3275 · Cited by 166
Interaction of Tau Isoforms with Alzheimer's Disease Abnormally Hyperphosphorylated Tau and in VitroPhosphorylation into the Disease-like Protein
Alonso, A. D. C., Zaidi, T., Novák, M., Barra, H. S., Grundke, I., & Iqbal, K. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105365200 · Cited by 160
Mitochondrial ATP-synthase in the entorhinal cortex is a target of oxidative stress at stages I/II of Alzheimer’s disease pathology
Terni, B., Boada, J., Portero‐Otin, M., Pamplona, R., & Ferrer, I. (2010) · Brain Pathology · doi:10.1111/j.1750-3639.2009.00266.x · Cited by 159
“Increased levels of glycation end products and lipid peroxidation markers have been observed in brains of patients with AD in association with NFTs and Ab deposits (23, 47, 56).”
Background
Active site-directed antibodies identify calpain II as an early-appearing and pervasive component of neurofibrillary pathology in Alzheimer's disease
Grynspan, F., Griffin, W. R., Cataldo, A. M., Katayama, S., & Nixon, R. A. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00384-3 · Cited by 156
Role for glyoxalase I in Alzheimer's disease
Chen, F., Wollmer, M. A., Hoerndli, F. J., Münch, G. W., Kuhla, B., Rogaev, E. I., Tsolaki, M., Papassotiropoulos, A., & Götz, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402338101 · Cited by 151
Tau protein is phosphorylated by cyclic AMP-dependent protein kinase and calcium/calmodulin-dependent protein kinase II within its microtubule-binding domains at Ser-262 and Ser-356
Litersky, J. M., Johnson, G. V. W., Jakes, R., Goedert, M., Lee, M., & Seubert, P. A. (1996) · Biochemical Journal · doi:10.1042/bj3160655 · Cited by 150
Advanced glycation end products and diabetic complications
Stitt, A. W., Jenkins, A. J., & Cooper, M. E. (2002) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.11.9.1205 · Cited by 152
Advanced Maillard Reaction End Products, Free Radicals, and Protein Oxidation in Alzheimer's Diseasea
Smith, M. A., Richey, P. L., Taneda, S., Kutty, R. K., Lm, S., Monnier, V. M., & Perry, G. L. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb21836.x · Cited by 146
Hyperphosphorylated tau proteins differentiate corticobasal degeneration and Pick's disease
Buée‐Scherrer, V., Hof, P. R., Buée, L., Leveugle, B., Vermersch, P., Perl, D. P., Olanow, C. W., & Delacourte, A. (1996) · Acta Neuropathologica · doi:10.1007/s004010050436 · Cited by 150
O-GlcNAc Modification of tau Directly Inhibits Its Aggregation without Perturbing the Conformational Properties of tau Monomers
Yuzwa, S. A., Cheung, A. H., Okon, M., McIntosh, L. P., & Vocadlo, D. J. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.01.004 · Cited by 152
“Tau, however, is also subject to a number of other post-translational modifications including, for example, proteolysis [10–12], acetylation [13], glycation [14,15], and O-glycosylation by O-linked N-acetyl-D-glucosamine (O-GlcNAc) [16].”
Background
G lycation in P arkinson's disease and Alzheimer's disease
Miranda, H. V., El‐Agnaf, O. M. A., & Outeiro, T. F. (2016) · Movement Disorders · doi:10.1002/mds.26566 · Cited by 146
Role of Hydrogen Peroxide in the Aetiology of Alzheimer??s Disease
Milton, N. G. N. (2004) · Drugs & Aging · doi:10.2165/00002512-200421020-00002 · Cited by 141
Normal and Pathological Tau Proteins as Factors for Microtubule Assembly
Delacourte, A., & Buée, L. (1997) · International review of cytology · doi:10.1016/s0074-7696(08)62588-7 · Cited by 145
Oxidative stress: A bridge between Down's syndrome and Alzheimer's disease
Zana, M., Janka, Z., & Kalman, J. L. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.03.008 · Cited by 140
Lysine-Directed Post-translational Modifications of Tau Protein in Alzheimer's Disease and Related Tauopathies
Kontaxi, C., Piccardo, P., & Gill, A. C. (2017) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2017.00056 · Cited by 138
“…occurs preferentially at the MBD of PHF-tau (Ledesma and Avila, 1995); lysines present at the R3 repeat were initially identified to be glycated in vitro (Ledesma et al., 1994), but later studies confirmed immunologically that glycation takes place in vivo within the MBD (Ledesma and Avila, 1995).”
BackgroundInfluential
Pseudophosphorylation and Glycation of Tau Protein Enhance but Do Not Trigger Fibrillization in Vitro
Necula, M., & Kuret, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405527200 · Cited by 140
Expression of 8-oxoguanine DNA glycosylase is reduced and associated with neurofibrillary tangles in Alzheimer's disease brain
Iida, T., Furuta, A., Nishioka, K., Nakabeppu, Y., & Iwaki, T. (2001) · Acta Neuropathologica · doi:10.1007/s004010100418 · Cited by 135
Metal ions and oxidative protein modification in neurological disease.
Sayre, L. M., Moreira, P. I., Smith, M. A., & Perry, G. L. (2005) · PubMed · Cited by 135
Oxidative stress mediates the pathogenic effect of different Alzheimer’s disease risk factors
Guglielmotto, M. (2010) · Frontiers in Aging Neuroscience · doi:10.3389/neuro.24.003.2010 · Cited by 135
“The involvement of AGEs in brain aging and in AD was reported more than 10 years ago, in studies showing that the microtubule associated protein tau and Aβ, were substrates for glycation (Ledesma et al., 1994; Smith et al., 1994; Vitek et al., 1994; Yan et al., 1994, 1995).”
Toxic Advanced Glycation End Products (TAGE) Theory in Alzheimer’s Disease
Sato, T., Shimogaito, N., Wu, X., Kikuchi, S., Yamagishi, S., & Takeuchi, M. (2006) · American Journal of Alzheimer s Disease & Other Dementias® · doi:10.1177/1533317506289277 · Cited by 133
Advanced glycation endproducts and their pathogenic roles in neurological disorders
Münch, G. W., Westcott, B., Menini, T., & Gugliucci, A. (2010) · Amino Acids · doi:10.1007/s00726-010-0777-y · Cited by 133
“3) (Ledesma et al. 1994).”
Tauopathy: A common mechanism for neurodegeneration and brain aging
Saha, P., & Sen, N. (2019) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2019.01.007 · Cited by 134
“Prion‐Like” Templated Misfolding in Tauopathies
Clavaguera, F., Lavenir, I., Falcon, B., Frank, S., Goedert, M., & Tolnay, M. (2013) · Brain Pathology · doi:10.1111/bpa.12044 · Cited by 133
“They include tau acetylation (20, 51, 67), glycation (61, 87), O-GlcNAcylation (5), nitration (79), ubiquitination (21, 68), sumoylation (28), prolyl isomerization (65) and truncation (34, 104).”
Background
Free radical damage, iron, and Alzheimer's disease
Smith, M. A., & Perry, G. L. (1995) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(95)00213-l · Cited by 130

Authors: Ledesma, M. D., Bonay, P., Colaço, C., & Avila, J.
Affiliations: Consejo Superior de Investigaciones Científicas (ES)
ORCID: Ledesma, M.D.
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 1994-08
Volume: 269
Issue: 34
Pages: 21614-21619
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1016/s0021-9258(17)31849-5
OpenAlex: W1577069180
Semantic Scholar: 68928334bcb2a45f531ceaeaa8ef0e1a72308735
Cited by: 333
References: 72
Citations by year: 2026: 1 · 2025: 2 · 2024: 7 · 2023: 6 · 2022: 4 · 2021: 8 · 2020: 2 · 2019: 12 · 2018: 13 · 2017: 7 · 2016: 10 · 2015: 5 · 2014: 13 · 2013: 11 · 2012: 13
FWCI: 11.84
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 9581 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
PubMed (publishedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Keywords: tau protein, glycation, paired helical filaments, Alzheimer's disease, post-translational modification, tau aggregation, neurofibrillary tangles, hyperphosphorylation
MeSH terms: Aged, Aged, 80 and over, Alzheimer Disease, Amino Acid Sequence, Animals, Brain Chemistry, Cattle, Diabetes Mellitus, Humans, Lysine, Microtubules, Molecular Sequence Data, Protein Binding, Neurofibrillary Tangles, tau Proteins, Glycation End Products, Advanced, Diabetes Complications

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Analysis of microtubule-associated protein tau glycation in paired helical filaments.

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