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

Ledesma, M.D.; Bonay, P.; Colaço, C.; Avila, J.

doi:10.1016/s0021-9258(17)31849-5

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

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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Glycated tau is only detected in PHF-tau isolated from AD brain samples, but not in soluble tau from AD or normal brain samples.
“Glycated tau is only detected in PHF-tau isolated from AD brain samples, but not in soluble tau from AD or normal brain samples [177, 179].”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [177]
Tau is preferentially glycated at Lys residues within the microtubule-binding domain, where advanced glycation end products are generated.
“Tau is preferentially glycated at Lys residues within the microtubule-binding domain, where advanced glycation end products are generated [177–179].”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [177]

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Background
Tau and neurodegenerative disease: the story so far
Iqbal, K., Liu, F., & Gong, C.-X. (2016) · Nature Reviews Neurology · doi:10.1038/nrneurol.2015.225 · Cited by 806 · see citing works
The Role of Advanced Glycation End Products in Aging and Metabolic Diseases: Bridging Association and Causality
Chaudhuri, J., Bains, Y., Guha, S., Kahn, A., Hall, D., Bose, N., Gugliucci, A., & Kapahi, P. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.08.014 · Cited by 669 · see citing works
Tau and tauopathies
Arendt, T., Stieler, J. T., & Holzer, M. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.08.018 · Cited by 609 · see citing works
Post-translational modifications of tau protein: Implications for Alzheimer's disease
Martin, L., Latypova, X., & Terro, F. (2011) · Neurochemistry International · doi:10.1016/j.neuint.2010.12.023 · Cited by 645 · see citing works
“Tau truncation in AD might later cause glycation (Ledesma et al., 1994) and ubiquitination (Morishima-Kawashima et al., 1993; Perry et al., 1987).”
Type 2 diabetes mellitus, cognitive impairment and dementia
Stewart, R., & Liolitsa, D. (1999) · Diabetic Medicine · doi:10.1046/j.1464-5491.1999.00027.x · Cited by 562 · see citing works
Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer’s disease: possible relation to oxidative stress.
Deibel, M. A., Ehmann, W. D., & Markesbery, W. R. (1996) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(96)00203-1 · Cited by 540 · see citing works
In Situ Oxidative Catalysis by Neurofibrillary Tangles and Senile Plaques in Alzheimer’s Disease
Sayre, L. M., Perry, G. L., Harris, P. L. R., Liu, Y. A., Schubert, K. A., & Smith, M. A. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0740270.x · Cited by 538 · see citing works
Advanced glycation endproducts and their receptor RAGE in Alzheimer's disease
Srikanth, V., Maczurek, A., Phan, T., Steele, M., Westcott, B., Juskiw, D., & Münch, G. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.04.016 · Cited by 524 · see citing works
Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI
den Heijer, T., Vermeer, S. E., van Dijk, E. J., Prins, N. D., Koudstaal, P. J., Albert Hofman, D., & Breteler, M. M. B. (2003) · Diabetologia · doi:10.1007/s00125-003-1235-0 · Cited by 512 · see citing works
Protein oxidation in the brain in Alzheimer's disease
Aksenov, M. Y., Aksenova, M. V., Butterfield, D. A., Geddes, J. W., & Markesbery, W. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00580-7 · Cited by 503 · see citing works
“Ledesma et al.(24) demonstrated the presence of AGEs in tau in a fraction of PHF in AD, whereas soluble tau from either AD or non-”
Background
Oxidative Stress in Neurodegenerative Diseases: From a Mitochondrial Point of View
Cenini, G., Lloret, A., & Cascella, R. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/2105607 · Cited by 435 · see citing works
“Several papers published in the early nineties suggested an important role of glycation in the formation of neurofibrillary tangles and senile plaques [103, 104].”
Background
How does diabetes accelerate Alzheimer disease pathology?
Sims-Robinson, C., Kim, B., Rosko, A., & Feldman, E. L. (2010) · Nature Reviews Neurology · doi:10.1038/nrneurol.2010.130 · Cited by 492 · see citing works
Radical AGEing in Alzheimer's disease
Smith, M. A., Sayre, L. M., Monnier, V. M., & Perry, G. L. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93897-7 · Cited by 462 · see citing works
Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration.
Billingsley, M., & Kincaid, R. (1997) · Biochemical Journal · doi:10.1042/bj3230577 · Cited by 469 · see citing works
The role of tau in neurodegeneration
Gendron, T. F., & Petrucelli, L. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-13 · Cited by 478 · see citing works
Elevated 4-Hydroxynonenal in Ventricular Fluid in Alzheimer’s Disease
Lovell, M. A., Ehmann, W. D., Mattson, M. P., & Markesbery, W. R. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00108-5 · Cited by 413 · see citing works
Advanced Glycation End Products in Alzheimer's Disease and Other Neurodegenerative Diseases
Sasaki, N., Fukatsu, R., Tsuzuki, K., Hayashi, Y., Yoshida, T., Fujii, N., Koike, T., WAKAYAMA, I., Yanagihara, R. T., Garruto, R. M., et al. (1998) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65659-3 · Cited by 411 · see citing works
Non-enzymatically glycated tau in Alzheimer's disease induces neuronal oxidant stress resulting in cytokine gene expression and release of amyloid β-peptide
Yan, S. D., Yan, S. F., Chen, X., Fu, J., Chen, M., Kuppusamy, P., Smith, M. A., Perry, G., Godman, G. C., Nawroth, P., et al. (1995) · Nature Medicine · doi:10.1038/nm0795-693 · Cited by 406 · see citing works
Tau Protein Modifications and Interactions: Their Role in Function and Dysfunction
Mietelska‐Porowska, A., Wasik, U., Goras, M., Filipek, A., & Niewiadomska, G. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms15034671 · Cited by 407 · see citing works
“It is modified by serine, threonine and tyrosine phosphorylation [63], isomerization [64], glycation [65], nitration [66], O-GlcNAcylation [67], acetylation [68], oxidation [69], polyamination [70], sumoylation [71], ubiquitination [72] and proteolytic cleavage (truncation) [73].”
Background
Rapid Assembly of Alzheimer-like Paired Helical Filaments from Microtubule-Associated Protein Tau Monitored by Fluorescence in Solution
Friedhoff, P., Schneider, A., Mandelkow, E., & Mandelkow�, E. (1998) · Biochemistry · doi:10.1021/bi980537d · Cited by 401 · see citing works
Microtubule-associated protein tau in development, degeneration and protection of neurons
Wang, J., & Liu, F. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.03.002 · Cited by 395 · see citing works
An intracellular protein that binds amyloid-β peptide and mediates neurotoxicity in Alzheimer's disease
Du Yan, S., Fu, J., Soto, C., Chen, X., Zhu, H., Al-Mohanna, F., Collison, K., Zhu, A., Stern, E., Saido, T., et al. (1997) · Nature · doi:10.1038/39522 · Cited by 379 · see citing works
Oxidative injury in diseases of the central nervous system: focus on alzheimer’s disease
Praticò, D., & Delanty, N. (2000) · The American Journal of Medicine · doi:10.1016/s0002-9343(00)00547-7 · Cited by 378 · see citing works
New Phosphorylation Sites Identified in Hyperphosphorylated Tau (Paired Helical Filament‐Tau) from Alzheimer's Disease Brain Using Nanoelectrospray Mass Spectrometry
Hanger, D. P., Betts, J. C., Loviny, T. L. F., Blackstock, W. P., & Anderton, B. H. (1998) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1998.71062465.x · Cited by 378 · see citing works
Common pathological processes in Alzheimer disease and type 2 diabetes: A review
Li, L., & Hölscher, C. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.09.001 · Cited by 367 · see citing works
“AGEs are involved in the production of the pathologic hallmarks of AD: accumulation of Aβ is increased by Aβ glycation, and formation of NFTs from phosphorylated tau is accelerated by glycation of tau protein (Ledesma et al., 1994).”
Background
Oxidative Stress and Neurodegeneration
Moreira, P. I., Smith, M. A., Zhu, X., Nunomura, A., Castellani, R. J., & Perry, G. L. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1333.062 · Cited by 366 · see citing works
The Microtubule-associated Protein Tau Is Extensively Modified with O-linked N-acetylglucosamine
Arnold, C. S., Johnson, G. W., Cole, R. N., Dong, D. L.-Y., Lee, M., & Hart, G. W. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.46.28741 · Cited by 361 · see citing works
Glycosylation of microtubule–associated protein tau: An abnormal posttranslational modification in Alzheimer's disease
Wang, J.-Z., Grundke-Iqbal, I., & Iqbal, K. (1996) · Nature Medicine · doi:10.1038/nm0896-871 · Cited by 360 · see citing works
Free fatty acids stimulate the polymerization of tau and amyloid beta peptides. In vitro evidence for a common effector of pathogenesis in Alzheimer's disease.
(1997) · Europe PMC (PubMed Central) · Cited by 354 · see citing works
Iron (III) induces aggregation of hyperphosphorylated τ and its reduction to iron (II) reverses the aggregation: implications in the formation of neurofibrillary tangles of Alzheimer's disease
Yamamoto, A., Shin, R., Hasegawa, K., Naiki, H., Sato, H., Yoshimasu, F., & Kitamoto, T. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.t01-1-01061.x · Cited by 313 · see citing works
Advanced glycation: an important pathological event in diabetic and age related ocular disease
Stitt, A. W. (2001) · British Journal of Ophthalmology · doi:10.1136/bjo.85.6.746 · Cited by 305 · see citing works
Alzheimer's disease – synergistic effects of glucose deficit, oxidative stress and advanced glycation endproducts
Münch, G. W., Schinzel, R., Loske, C., Wong, A. O., Durany, N., Li, J. J., Vlassara, H., Smith, M. A., Perry, G. L., & Riederer, P. F. (1998) · Journal of Neural Transmission · doi:10.1007/s007020050069 · Cited by 302 · see citing works
“Furthermore, glycated tau found in neurons in AD (Smith et al., 1994b; Yan et al., 1994; Ledesma et al., 1994) causes an oxidative response in neuroblastoma cells including induction of heme oxygenase-1, translocation of NFκB and peroxidation of membrane lipids (Yan et al., 1994, 1995).”
Background
Is oxidative damage the fundamental pathogenic mechanism of Alzheimer’s and other neurodegenerative diseases?
Perry, G. L., Nunomura, A., Hirai, K., Zhu, X., Prez, M. D. F., Ávila, J., Castellani, R. J., Atwood, C., Aliev, G., Sayre, L. M., et al. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)01113-9 · Cited by 297 · see citing works
Microtubule-Associated Protein Tau
Yen, S.-H. C., Nacharaju, P., Ko, L., Kenessey, Á., & Liu, W.-K. (1998) · Elsevier eBooks · doi:10.1016/b978-012734610-6/50012-9 · Cited by 284 · see citing works
The relationship between oxidative/nitrative stress and pathological inclusions in Alzheimer’s and Parkinson’s diseases1,2 11Guest Editors: Mark A. Smith and George Perry 22This article is part of a series of reviews on “Causes and Consequences of Oxidative Stress in Alzheimer’s Disease.” The full list of papers may be found on the homepage of the journal.
Giasson, B. I., Ischiropoulos, H., Lee, V. M. ‐., & Trojanowski, J. Q. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00804-3 · Cited by 281 · see citing works
Vitamin E and Alzheimer disease: the basis for additional clinical trials
Grundman, M. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.2.630s · Cited by 267 · see citing works
Iron (III) induces aggregation of hyperphosphorylated τ and its reduction to iron (II) reverses the aggregation: implications in the formation of neurofibrillary tangles of Alzheimer's disease
Yamamoto, A., Shin, R., Hasegawa, K., Naiki, H., Sato, H., YOSHIMASU, F., & Kitamoto, T. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01061.x · Cited by 246 · see citing works
Tau phosphorylation in Alzheimer's disease: pathogen or protector?
Lee, H., Perry, G. L., Moreira, P. I., Garrett, M. R., Liu, Q., Zhu, X., Takeda, A., Nunomura, A., & Smith, M. A. (2005) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2005.02.008 · Cited by 240 · see citing works
Longitudinal association of vascular and Alzheimer’s dementias, diabetes, and glucose tolerance
Curb, J. D., Rodríguez, B. L., Abbott, R. D., Petrovitch, H., Ross, G. W., Masaki, K., Foley, D. J., Blanchette, P. L., Harris, T. B., Chen, R., et al. (1999) · Neurology · doi:10.1212/wnl.52.5.971 · Cited by 231 · see citing works
Tau Cleavage and Dephosphorylation in Cerebellar Granule Neurons Undergoing Apoptosis
Canu, N., Dus, L., Barbato, C., Ciotti, M. T., Brancolini, C., Rinaldi, A. M., Novak, M., Cattaneo, A., Bradbury, A., & Calissano, P. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07061.1998 · Cited by 232 · see citing works
“…posttranslational changes, including physiological phosphorylation and glycosylation (Lovestone and Reynolds, 1997), as well as pathological phosphorylation (Grundke-Iqbal et al., 1986a), glycosylation (Wang et al., 1996), glycation (Ledesma et al., 1994), and truncation (Novak et al., 1993) in AD.”
Background
Demonstrating the case that AD is a vascular disease: epidemiologic evidence
Launer, L. J. (2002) · Ageing Research Reviews · doi:10.1016/s0047-6374(01)00364-5 · Cited by 227 · see citing works
Inhibition of tau phosphorylating protein kinase cdk5 prevents β‐amyloid‐induced neuronal death
Alvarez, A. R., Toro, R., Cáceres, A., & Maccioni, R. B. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01279-x · Cited by 228 · see citing works
Four-repeat tauopathies
Rösler, T. W., Marvian, A. T., Brendel, M., Nykänen, N.-P., Höllerhage, M., Schwarz, S. C., Hopfner, F., Koeglsperger, T., Respondek, G., Schweyer, K., et al. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.101644 · Cited by 219 · see citing works
Cytochemical Demonstration of Oxidative Damage in Alzheimer Disease by Immunochemical Enhancement of the Carbonyl Reaction with 2,4-Dinitrophenylhydrazine
Smith, M. A., Sayre, L. M., Anderson, V. E., Harris, P. L. R., Beal, M. F., Kowall, N. W., & Perry, G. L. (1998) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215549804600605 · Cited by 222 · see citing works
“It is tempting to speculate that neuronal damage involves not only the cytoskeletal proteins that bear glycoxidative (Ledesma et al. 1994; Yan et al. 1995) and lipoxidative (Smith et al., unpublished observation) adducts but also nuclear components.”
Background
Immunohistochemical detection of 4-hydroxy-2-nonenal adducts in Alzheimer's disease is associated with inheritance of APOE4.
Montine, K. S., Olson, S. J., Amarnath, K., Whetsell, W. O., Graham, D. G., & Montine, T. J. (1997) · Europe PMC (PubMed Central) · Cited by 220 · see citing works
Nitration of Tau Protein Is Linked to Neurodegeneration in Tauopathies
Horiguchi, T., Uryu, K., Giasson, B. I., Ischiropoulos, H., Lightfoot, R. T., Bellmann, C., Richter‐Landsberg, C., Lee, V. M. ‐., & Trojanowski, J. Q. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63462-1 · Cited by 220 · see citing works
Evidence of a balance between phosphorylation and O-GlcNAc glycosylation of Tau proteins—a role in nuclear localization
Lefebvre, T., Ferreira, S., Dupont-Wallois, L., Bussière, T., Dupire, M.-J., Delacourte, A., Michalski, J., & Caillet‐Boudin, M. (2003) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(02)00477-4 · Cited by 209 · see citing works
Updates in Alzheimer's disease: from basic research to diagnosis and therapies
Liu, E., Zhang, Y., & Wang, J. (2024) · Translational Neurodegeneration · doi:10.1186/s40035-024-00432-x · Cited by 220 · see citing works
“In addition, tau protein in the AD brains undergoes abnormal glycation [416, 417].”
Background
Molecular links between Alzheimer’s disease and diabetes mellitus
Yang, Y., & Song, W. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.009 · Cited by 201 · see citing works
Alzheimer Disease
Smith, M. A. (1998) · International review of neurobiology · doi:10.1016/s0074-7742(08)60607-8 · Cited by 201 · see citing works
Active glycation in neurofibrillary pathology of Alzheimer disease: Nε-(Carboxymethyl) lysine and hexitol-lysine
Castellani, R. J., Harris, P. L. R., Sayre, L. M., Fujii, J., Taniguchi, N., Vitek, M. P., Founds, H., Atwood, C., Perry, G. L., & Smith, M. A. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00570-6 · Cited by 198 · see citing works
Neurotoxicity of Advanced Glycation End-Products for Cultured Cortical Neurons
Takeuchi, M., Bucala, R., Suzuki, T., Ohkubo, T., Yamazaki, M., Koike, T., Kameda, Y., & Makita, Z. (2000) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/59.12.1094 · Cited by 198 · see citing works
Insulin signaling, glucose metabolism and mitochondria: Major players in Alzheimer's disease and diabetes interrelation
Correia, S. C., Santos, R. X., Carvalho, C., Cardoso, S., Candeias, E., Santos, M. S., Oliveira, C. R., & Moreira, P. I. (2012) · Brain Research · doi:10.1016/j.brainres.2011.12.063 · Cited by 195 · see citing works
It’s all about tau
Tapia‐Rojas, C., Cabezas-Opazo, F., Deaton, C. A., Vergara, E. H., Johnson, G. V. W., & Quintanilla, R. A. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.12.005 · Cited by 195 · see citing works
“, 1998), indicating that glycated tau likely is more prone to aggregate (Ledesma et al., 1994).”
Background
Carbonyl Toxicology and Alzheimer's Disease
Picklo, M. J. (2002) · Toxicology and Applied Pharmacology · doi:10.1006/taap.2002.9506 · Cited by 194 · see citing works
Tau oligomers and aggregation in Alzheimer’s disease
Meraz‐Ríos, M. A., León, K. I. L.-D., Campos‐Peña, V., Anda-Hernández, M. A. D., & Mena‐López, R. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06511.x · Cited by 193 · see citing works
Reactive Oxygen Species Mediate Cellular Damage in Alzheimer Disease
Perry, G. L., Castellani, R. J., Hirai, K., & Smith, M. A. (1998) · Journal of Alzheimer s Disease · doi:10.3233/jad-1998-1103 · Cited by 184 · see citing works
“Nonetheless, the overall result is damage including advanced glycation end products (53,102,123,126), nitration (29,109), lipid peroxidation adduction products (63,86) as well as carbonyl-modified neurofilament protein and free carbonyls (99,105,107) with the involvement extending beyond the lesions to neurons not dis…”
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 · see citing works
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 175 · see citing works
“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 · see citing works
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 174 · see citing works
“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 168 · see citing works
“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 · see citing works
Glycation—a sweet tempter for neuronal death
Kikuchi, S. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00273-4 · Cited by 169 · see citing works
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 · see citing works
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 162 · see citing works
“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 157 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 150 · see citing works
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 · see citing works
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 144 · see citing works
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 143 · see citing works
“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 142 · see citing works
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 · see citing works
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 136 · see citing works
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 137 · see citing works
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 · see citing works
“…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 136 · see citing works
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Iida, T., Furuta, A., Nishioka, K., Nakabeppu, Y., & Iwaki, T. (2001) · Acta Neuropathologica · doi:10.1007/s004010100418 · Cited by 135 · see citing works
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 · see citing works
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 133 · see citing works
“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 · see citing works
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 132 · see citing works
“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 128 · see citing works
“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 129 · see citing works
“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 · see citing works

Microtubule-Stabilizing Activity of Microtubule-Associated Proteins (MAPs) Is Due to Increase in Frequency of Rescue in Dynamic Instability: Shortening Length Decreases with Binding of MAPs onto Microtubules.
Itoh, T. J., & Hotani, H. (1994) · Cell Structure and Function · doi:10.1247/csf.19.279 · Cited by 59 · see citing works
Microtubule‐binding property of microtubule‐associated protein 2 differs from that of microtubule‐associated protein 4 and tau
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MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments
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Effects of three microtubule-associated proteins (MAP2, MAP4, and Tau) on microtubules’ physical properties and neurite morphology
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Modulation of microtubule shape in vitro by high molecular weight microtubule associated proteins MAP1A, MAP1B, and MAP2
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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: Health Sciences › Medicine › Physiology › 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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