Invited review: Neuropathology of tauopathies: principles and practice

Kovacs, G. G.

doi:10.1111/nan.12208

Cited by 492Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchAmyotrophic Lateral Sclerosis Research

Invited review: Neuropathology of tauopathies: principles and practice

Kovacs, G. G.·2015·Neuropathology and Applied Neurobiology

DOI 10.1111/nan.12208

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Abstract

Tauopathies are clinically, morphologically and biochemically heterogeneous neurodegenerative diseases characterized by the deposition of abnormal tau protein in the brain. The neuropathological phenotypes are distinguished based on the involvement of different anatomical areas, cell types and presence of distinct isoforms of tau in the pathological deposits. The nomenclature of primary tauopathies overlaps with the modern classification of frontotemporal lobar degeneration. Neuropathological phenotypes comprise Pick's disease, progressive supranuclear palsy, corticobasal degeneration, argyrophilic grain disease, primary age‐related tauopathy, formerly called also as neurofibrillary tangle‐only dementia, and a recently characterized entity called globular glial tauopathy. Mutations in the gene encoding the microtubule‐associated protein tau are associated with frontotemporal dementia and parkinsonism linked to chromosome 17. In addition, further neurodegenerative conditions with diverse aetiologies may be associated with tau pathologies. Thus, the spectrum of tau pathologies and tauopathy entities expands beyond the traditionally discussed disease forms. Detailed multidisciplinary studies are still required to understand their significance.

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The pathological diagnosis of tauopathy relies on the presence of particular tau inclusions with cell- or brain-region-specific distributions.
“The pathological diagnosis of tauopathy relies on the presence of particular tau inclusions with cell/brain-region-specific distributions [30].”
From Role of Tau Protein in Neurodegenerative Diseases and Development of Its Targeted Drugs: A Literature Review (2024) · cites this paper as [30]
Aggregated hyperphosphorylated tau is a well-described pathological hallmark of several non-AD disorders, such as frontotemporal lobar degeneration.
“Furthermore, aggregated hyperphosphorylated tau is a well-described pathological hallmark of several other non-AD disorders, such as frontotemporal lobar degeneration (FTLD) [45].”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [45]

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Kovács, G. G., Molnár, K., László, L., Ströbel, T., Botond, G., Hönigschnabl, S., Reiner‐Concin, A., Palkovits, M., Fischer, P. A., & Budka, H. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0819-x · Cited by 90 · see citing works
Hippocampal Sclerosis Dementia with Tauopathy
Beach, T. G., Sue, L. I., Scott, S., Layne, K. J., Newell, A., Walker, D. G., Baker, M., Sahara, N., Yen, S.-H. C., Hutton, M. L., et al. (2003) · Brain Pathology · doi:10.1111/j.1750-3639.2003.tb00027.x · Cited by 89 · see citing works
Current concepts of neuropathological diagnostics in practice: neurodegenerative diseases
Kovács, G. G., & Budka, H. (2010) · Clinical Neuropathology · doi:10.5414/npp29271 · Cited by 85 · see citing works
The MAPT H1 haplotype is associated with tangle-predominant dementia
Santa‐María, I., Haggiagi, A. M., Liu, X., Wasserscheid, J., Nelson, P. T., Dewar, K., Clark, L. N., & Crary, J. F. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-1017-1 · Cited by 83 · see citing works
Enduring involvement of tau, β-amyloid, α-synuclein, ubiquitin and TDP-43 pathology in the amyotrophic lateral sclerosis/parkinsonism–dementia complex of Guam (ALS/PDC)
Judith Miklossy, A., Steele, J. C., Yu, S. Y., McCall, S. A., Sandberg, G. D., McGeer, E. G., & McGeer, P. L. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0439-2 · Cited by 81 · see citing works
Clinicopathological Outcomes of Prospectively Followed Normal Elderly Brain Bank Volunteers
Dugger, B. N., Hentz, J. G., Adler, C. H., Sabbagh, M. N., Shill, H. A., Jacobson, S. A., Caviness, J. N., Belden, C. M., Driver‐Dunckley, E. D., Davis, K. J., et al. (2014) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000046 · Cited by 80 · see citing works
Pathological correlates of frontotemporal lobar degeneration in the elderly
Baborie, A., Griffiths, T. D., Jaros, E., McKeith, I. G., Burn, D. J., Richardson, A. M. T., Ferrari, R., Moreno, J. H., Momeni, P., DuPlessis, D., et al. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0765-z · Cited by 78 · see citing works
Argyrophilic thorny astrocyte clusters in association with Alzheimer’s disease pathology in possible primary progressive aphasia
Muñoz, D. G., Woulfe, J., & KERTESZ, A. E. (2007) · Acta Neuropathologica · doi:10.1007/s00401-007-0266-x · Cited by 77 · see citing works
Mixed tau, TDP-43 and p62 pathology in FTLD associated with a C9ORF72 repeat expansion and p.Ala239Thr MAPT (tau) variant
King, A., Al‐Sarraj, S., Troakes, C., Smith, B. N., Maekawa, S., Iovino, M., Spillantini, M. G., & Shaw, C. E. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-1050-0 · Cited by 76 · see citing works
Globular glial tauopathies (GGT) presenting with motor neuron disease or frontotemporal dementia: an emerging group of 4-repeat tauopathies
Ahmed, Z., Doherty, K. A., Silveira‐Moriyama, L., Bandopadhyay, R., Lashley, T., Mamais, A., Hondhamuni, G., Wray, S., Newcombe, J., O’Sullivan, S. S., et al. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0857-4 · Cited by 74 · see citing works
Neuropathology of the hippocampus in FTLD‐Tau with Pick bodies: a study of the BrainNet Europe Consortium
Kovács, G. G., Rozemüller, A. J. M., Swieten, J. C. V., Gelpí, E., Majtényi, K., Al‐Sarraj, S., Troakes, C., Bódi, I., King, A., Hortobágyi, T., et al. (2012) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01272.x · Cited by 72 · see citing works
Pathological τ proteins in postencephalitic parkinsonism: Comparison with Alzheimer's disease and other neurodegenerative disorders
Buée‐Scherrer, V., Buée, L., Leveugle, B., Perl, D. P., Vermersch, P., Hof, P. R., & Delacourte, A. (1997) · Annals of Neurology · doi:10.1002/ana.410420312 · Cited by 71 · see citing works
Selective Neurofibrillary Degeneration of the Hippocampal CA2 Sector Is Associated with Four-Repeat Tauopathies
Ishizawa, T., Ko, L., Cookson, N., Davies, P., Espinoza, M., & Dickson, D. W. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.12.1040 · Cited by 71 · see citing works
The Effect of Prolonged Fixation Time on Immunohistochemical Staining of Common Neurodegenerative Disease Markers
Pikkarainen, M., MARTIKAINEN, P. M., & Alafuzoff, I. I. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181c6c13d · Cited by 68 · see citing works
Plaque biogenesis in brain aging and Alzheimer's disease. II. Progressive transformation and developmental sequence of dystrophic neurites
Su, J. H., Cummings, B. J., & Cotman, C. W. (1998) · Acta Neuropathologica · doi:10.1007/s004010050920 · Cited by 67 · see citing works
Hereditary prion protein amyloidoses
Ghetti, B. F., Tagliavini, F., Takao, M., et al. (2003) · Clinics in Laboratory Medicine · doi:10.1016/s0272-2712(02)00064-1 · Cited by 65 · see citing works
Lewy Bodies in Progressive Supranuclear Palsy Represent an Independent Disease Process
Uchikado, H., DelleDonne, A., Ahmed, Z., & Dickson, D. W. (2006) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/01.jnen.0000218449.17073.43 · Cited by 65 · see citing works
Non-Alzheimer non-Pick dementia with Fahr's syndrome.
Shibayama, H., Kobayashi, H., Nakagawa, M., et al. (1992) · PubMed · Cited by 62 · see citing works
Qualitative and Quantitative Differences in Senile Plaque Dystrophie Neurites of Alzheimerʼs Disease and Normal Aged Brain
WANG, D., & Muñoz, D. G. (1995) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199507000-00009 · Cited by 62 · see citing works
Pantothenate kinase‐associated neurodegeneration is not a synucleinopathy
Li, A. S. M., Paudel, R., Johnson, R. M., et al. (2012) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01269.x · Cited by 56 · see citing works
Delineation of Early Changes in Cases with Progressive Supranuclear Palsy‐Like Pathology. Astrocytes in Striatum are Primary Targets of Tau Phosphorylation and GFAP Oxidation
Santpere, G., & Ferrer, I. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2008.00173.x · Cited by 56 · see citing works
TARDBP mutation p. I le383 V al associated with semantic dementia and complex proteinopathy
Gelpí, E., van der Zee, J., Estrada, A. T., Broeckhoven, C. V., & Sánchez‐Valle, R. (2013) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12063 · Cited by 56 · see citing works
Sporadic four-repeat tauopathy with frontotemporal lobar degeneration, Parkinsonism, and motor neuron disease: a distinct clinicopathological and biochemical disease entity
Fu, Y., Nishihira, Y., Kuroda, S., Toyoshima, Y., Ishihara, T., Shinozaki, M., Miyashita, A., Piao, Y.-S., Tan, C., Tani, T., et al. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0649-2 · Cited by 55 · see citing works
Neuropathological findings of PSP in the elderly without clinical PSP: Possible incidental PSP?
Evidente, V. G. H., Adler, C. H., Sabbagh, M. N., Connor, D. J., Hentz, J. G., Caviness, J. N., Sue, L. I., & Beach, T. G. (2011) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2011.02.017 · Cited by 52 · see citing works
Mesial Temporal Astrocyte Tau Pathology in the MRC-CFAS Ageing Brain Cohort
Lace, G., Ince, P. G., Brayne, C., Savva, G. M., Matthews, F. E., de Silva, R., Simpson, J. E., & Wharton, S. B. (2012) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000341581 · Cited by 52 · see citing works
Argyrophilic grain disease presenting with frontotemporal dementia: A neuropsychological and pathological study of an autopsied case with presenile onset
Ishihara, K., Araki, S., Ihori, N., Shiota, J., Kawamura, M., Yoshida, M., Hashizume, Y., & Nakano, I. (2005) · Neuropathology · doi:10.1111/j.1440-1789.2005.00598.x · Cited by 52 · see citing works
Numerous glial fibrillary tangles in oligodendroglia in cases of subacute sclerosing panencephalitis with neurofibrillary tangles
Iked, K., Akiyama, H., Kondo, H., et al. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)11713-7 · Cited by 51 · see citing works
Absence of α-synuclein pathology in postencephalitic parkinsonism
Jellinger, K. A. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0537-9 · Cited by 49 · see citing works
Clinical phenotypes in autopsy-confirmed Pick disease
Piguet, O., Halliday, G. M., Reid, W., Casey, B. J., Carman, R., Huang, Y. M., Xuereb, J. H., Hodges, J. R., & Kril, J. J. (2011) · Neurology · doi:10.1212/wnl.0b013e318207b1ce · Cited by 47 · see citing works
Argyrophilic grain disease mimicking temporal Pick's disease: a clinical, radiological, and pathological study of an autopsy case with a clinical course of 15 years
Tsuchiya, K., Mitani, K., Arai, T., Yamada, S., Komiya, T., Esaki, Y., Haga, C., Yamanouchi, H., & Ikeda, K. (2001) · Acta Neuropathologica · doi:10.1007/s004010100365 · Cited by 46 · see citing works
Corticobasal degeneration with olivopontocerebellar atrophy and TDP-43 pathology: an unusual clinicopathologic variant of CBD
Kouri, N., Oshima, K., Takahashi, M., Murray, M. E., Ahmed, Z., Parisi, J. E., Yen, S. H., & Dickson, D. W. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1087-8 · Cited by 44 · see citing works
Tau accumulation in the nucleus accumbens in tangle-predominant dementia
Kawakami, I., Hasegawa, M., Arai, T., Ikeda, K., Oshima, K., Niizato, K., Aoki, N., Omi, K., Higashi, S., Hosokawa, M., et al. (2014) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-2-40 · Cited by 42 · see citing works
Argyrophilic grain disease
Tolnay, M., & Probst, A. (2008) · Handbook of clinical neurology · doi:10.1016/s0072-9752(07)01251-1 · Cited by 41 · see citing works
Patterns of Hippocampal Tau Pathology Differentiate Neurodegenerative Dementias
Milenković, I., Petrov, T., & Kovács, G. G. (2014) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000365548 · Cited by 36 · see citing works
The extended haplotype of the microtubule associated protein tau gene is not associated with Pick's disease
Russ, C., Lovestone, S., Baker, M. C., et al. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01785-7 · Cited by 35 · see citing works
Specific Detection of Pathological Three‐repeat Tau after Pretreatment with Potassium Permanganate and Oxalic Acid in PSP/CBD Brains
Uchihara, T., Nakamura, A., Shibuya, K., et al. (2010) · Brain Pathology · doi:10.1111/j.1750-3639.2010.00433.x · Cited by 33 · see citing works
Glial fibrillary tangles and argyrophilic threads: Classification and disease specificity
Ikeda, K. (1996) · Neuropathology · doi:10.1111/j.1440-1789.1996.tb00158.x · Cited by 31 · see citing works
Hippocampal sclerosis with four-repeat tau-positive round inclusions in the dentate gyrus: a new type of four-repeat tauopathy
Miki, Y., Mori, F., Hori, E., Kaimori, M., & Wakabayashi, K. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0531-2 · Cited by 29 · see citing works
Concomitant progressive supranuclear palsy and chronic traumatic encephalopathy in a boxer
Ling, H., Kara, E., Revesz, T., Lees, A. J., Plant, G. T., Martino, D., Houlden, H., Hardy, J., & Holton, J. L. (2014) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-2-24 · Cited by 27 · see citing works
Tuft-shaped astrocytes in Lewy body disease
Hishikawa, N., Hashizume, Y., Yoshida, M., Niwa, J.-I., Tanaka, F., & Sobue, G. (2005) · Acta Neuropathologica · doi:10.1007/s00401-004-0967-3 · Cited by 26 · see citing works
Corticobasal degeneration with focal, massive tau accumulation in the subcortical white matter astrocytes
Sakai, K., Piao, Y.-S., Kikugawa, K., Ohara, S., Hasegawa, M., Takano, H., Fukase, M., Nishizawa, M., Kakita, A., & Takahashi, H. (2006) · Acta Neuropathologica · doi:10.1007/s00401-006-0093-5 · Cited by 26 · see citing works
Glial fibrillary tangles in diffuse neurofibrillary tangles with calcification
Hashimoto, N., Takeuchi, T., Ishihara, R., et al. (2003) · Acta Neuropathologica · doi:10.1007/s00401-003-0715-0 · Cited by 23 · see citing works
Concomitant progressive supranuclear palsy and multiple system atrophy: More than a simple twist of fate?
Silveira‐Moriyama, L., Gonzalez, A. M. D., O’Sullivan, S. S., Williams, D. R., Massey, L. A., Parkkinen, L., Ahmed, Z., de Silva, R., Chacón, J., Révész, T., et al. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.10.036 · Cited by 22 · see citing works
Cerebrotendinous xanthomatosis with the c.379 C > T (p. R 127 W ) mutation in the CYP27A1 gene associated with premature age‐associated limbic tauopathy
Kapás, I., Katkó, M., Harangi, M., et al. (2013) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12058 · Cited by 17 · see citing works
Tau accumulation in the nucleus accumbens in tangle-predominant dementia
河上緒 (2014) · Cited by 16 · see citing works
Clinicopathological study of diffuse neurofibrillary tangles with calcification
Habuchi, C., Iritani, S., Sekiguchi, H., et al. (2010) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2010.10.021 · Cited by 10 · see citing works
Globular glial-like inclusions in a patient with advanced Alzheimer’s disease
Gelpí, E., Cullel, F., Navarro‐Otano, J., et al. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1131-8 · Cited by 10 · see citing works
The Spectrum of Tau Pathology in Human Prion Disease
Kovács, G. G., & Budka, H. (2012) · Springer eBooks · doi:10.1007/978-1-4614-5338-3_7 · Cited by 9 · see citing works
Pick's pathology in Parkinson's disease with dementia
Vilas, D., Martí, M. J., Botta‐Orfila, T., et al. (2012) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01287.x · Cited by 3 · see citing works
Frequency and Relation of Argyrophilic Grain Disease and Thorn-Shaped Astrocytes in Alzheimer’s Disease
Uchikado, H., Fujino, Y., Lin, W., & Dickson, D. W. (2007) · Springer eBooks · doi:10.1007/978-0-387-72076-0_39 · Cited by 2 · see citing works

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Pathology of Neurodegenerative Diseases
Dugger, B. N., & Dickson, D. W. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028035 · Cited by 1,665 · 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
Aging-related tau astrogliopathy (ARTAG): Harmonized evaluation strategy
Kovacs, G. G., Ferrer, I., Grinberg, L. T., Alafuzoff, I., Attems, J., Budka, H., Cairns, N. J., Crary, J. F., Duyckaerts, C., Ghetti, B., et al. (2016) · Acta Neuropathologica · doi:10.1007/s00401-015-1509-x · Cited by 532 · see citing works
“Finally, tufted astrocytes in PSP, astrocytic plaques in CBD, globular astrocytic inclusions in GGT, and ramified astrocytes in PiD are distinct from tau-immunoreactive astrocytes in the gray matter in ARTAG (see Table 1).”
Influential
Distribution patterns of tau pathology in progressive supranuclear palsy
Kovacs, G. G., Lukic, M. J., Irwin, D. J., Arzberger, T., Respondek, G., Lee, E. B., Coughlin, D., Giese, A., Grossman, M., Kurz, C., et al. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02158-2 · Cited by 483 · see citing works
Self-citation
Tau molecular diversity contributes to clinical heterogeneity in Alzheimer’s disease
Dujardin, S., Commins, C., Lathuiliere, A., Beerepoot, P., Fernandes, A. R., Kamath, T. V., De Los Santos, M. B., Klickstein, N., Corjuc, D. L., Corjuc, B. T., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-0938-9 · Cited by 438 · see citing works
What is the evidence that tau pathology spreads through prion-like propagation?
Mudher, A., Colin, M., Dujardin, S., Medina, M., Dewachter, I., Alavi Naini, S. M., Mandelkow, E.-M., Mandelkow, E., Buée, L., Goedert, M., et al. (2017) · Acta Neuropathologica Communications · doi:10.1186/s40478-017-0488-7 · Cited by 384 · see citing works
Mechanisms of secretion and spreading of pathological tau protein
Brunello, C. A., Merezhko, M., Uronen, R.-L., & Huttunen, H. J. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03349-1 · Cited by 304 · see citing works
Tau seeding activity begins in the transentorhinal/entorhinal regions and anticipates phospho-tau pathology in Alzheimer’s disease and PART
Kaufman, S. K., Del Tredici, K., Thomas, T. L., Braak, H., & Diamond, M. I. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1855-6 · Cited by 259 · see citing works
Review: Astrocytes in Alzheimer's disease and other age‐associated dementias: a supporting player with a central role
Garwood, C. J., Ratcliffe, L. E., Simpson, J. E., Heath, P. R., Ince, P. G., & Wharton, S. B. (2017) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12338 · Cited by 233 · see citing works
Tauopathies.
(2018) · Handbook of Clinical Neurology · doi:10.1016/b978-0-12-802395-2.00025-0 · Cited by 225 · see citing works
Self-citation
Altered Proteins in the Aging Brain
Elobeid, A., Libard, S., Leino, M., Popova, S. N., & Alafuzoff, I. (2016) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlw002 · Cited by 202 · see citing works
YKL-40 (Chitinase 3-like I) is expressed in a subset of astrocytes in Alzheimer’s disease and other tauopathies
Querol-Vilaseca, M., Colom-Cadena, M., Pegueroles, J., San Martín-Paniello, C., Clarimon, J., Belbin, O., Fortea, J., & Lleó, A. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0893-7 · Cited by 158 · see citing works
Identification of evolutionarily conserved gene networks mediating neurodegenerative dementia
Swarup, V., Hinz, F. I., Rexach, J. E., Noguchi, K.-I., Toyoshiba, H., Oda, A., Hirai, K., Sarkar, A., Seyfried, N. T., Cheng, C., et al. (2019) · Nature Medicine · doi:10.1038/s41591-018-0223-3 · Cited by 136 · see citing works
Chronic traumatic encephalopathy is a common co-morbidity, but less frequent primary dementia in former soccer and rugby players
Lee, E. B., Kinch, K., Johnson, V. E., Trojanowski, J. Q., Smith, D. H., & Stewart, W. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-02030-y · Cited by 157 · see citing works
Review: neuropathology of non-tau frontotemporal lobar degeneration
Neumann, M., & Mackenzie, I. R. A. (2019) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12526 · Cited by 144 · see citing works
Evaluating the Patterns of Aging-Related Tau Astrogliopathy Unravels Novel Insights Into Brain Aging and Neurodegenerative Diseases
Kovacs, G. G., Robinson, J. L., Xie, S. X., Lee, E. B., Grossman, M., Wolk, D. A., Irwin, D. J., Weintraub, D., Kim, C. F., Schuck, T., et al. (2017) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlx007 · Cited by 132 · see citing works
Self-citation
Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau
Rayaprolu, S., Higginbotham, L., Bagchi, P., Watson, C. M., Zhang, T., Levey, A. I., Rangaraju, S., & Seyfried, N. T. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-020-00840-3 · Cited by 118 · see citing works
A comprehensive resource for induced pluripotent stem cells from patients with primary tauopathies
Karch, C. M., Kao, A. W., Karydas, A., Onanuga, K., Martinez, R., Argouarch, A., Wang, C., Huang, C., Sohn, P. D., Bowles, K. R., et al. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.09.006 · Cited by 119 · see citing works
In vivo retention of <sup>18</sup> F-AV-1451 in corticobasal syndrome
Smith, R., Schöll, M., Widner, H., van Westen, D., Svenningsson, P., Hägerström, D., Ohlsson, T., Jögi, J., Nilsson, C., & Hansson, O. (2017) · Neurology · doi:10.1212/wnl.0000000000004264 · Cited by 117 · see citing works
Astroglia and Tau: New Perspectives
Kovacs, G. G. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00096 · Cited by 115 · see citing works
Self-citation
Tau biology, tauopathy, traumatic brain injury, and diagnostic challenges
Castellani, R. J., & Perry, G. (2019) · Journal of Alzheimer’s Disease · doi:10.3233/jad-180721 · Cited by 110 · see citing works
Shared genetic risk between corticobasal degeneration, progressive supranuclear palsy, and frontotemporal dementia
International FTD-Genomics Consortium (IFGC), Yokoyama, J. S., Karch, C. M., Fan, C. C., Bonham, L. W., Kouri, N., Ross, O. A., Rademakers, R., Kim, J., Wang, Y., et al. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1693-y · Cited by 99 · see citing works
“Approximately half of bvFTD clinical syndromes result from underlying Pick’s disease, which is characterized by predominantly 3R tau inclusions (Pick bodies) in the frontal, temporal and insular cortical gray matter [25].”
Background
Neuroinflammation and Tau Colocalize in vivo in Progressive Supranuclear Palsy
Malpetti, M., Passamonti, L., Rittman, T., Jones, P. S., Vázquez Rodríguez, P., Bevan‐Jones, W. R., Hong, Y. T., Fryer, T. D., Aigbirhio, F. I., O'Brien, J. T., et al. (2020) · Annals of Neurology · doi:10.1002/ana.25911 · Cited by 83 · see citing works
Identification of Conserved Proteomic Networks in Neurodegenerative Dementia
Swarup, V., Chang, T. S., Duong, D. M., Dammer, E. B., Dai, J., Lah, J. J., Johnson, E. C. B., Seyfried, N. T., Levey, A. I., & Geschwind, D. H. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107807 · Cited by 78 · see citing works
Identification of conserved proteomic networks in neurodegenerative dementia
Swarup, V., Chang, T. S., Duong, D. M., Dammer, E. B., Lah, J. J., Johnson, E. E. C. B., Seyfried, N. T., Levey, A. I., & Geschwind, D. H. (2019) · doi:10.1101/825802 · Cited by 78 · see citing works
Microglia: Friend and foe in tauopathy
Odfalk, K. F., Bieniek, K. F., & Hopp, S. C. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102306 · Cited by 60 · see citing works
Role of Tau Protein in Neurodegenerative Diseases and Development of Its Targeted Drugs: A Literature Review
Yang, J., Zhi, W., & Wang, L. (2024) · Molecules · doi:10.3390/molecules29122812 · Cited by 63 · see citing works
“The pathological diagnosis of tauopathy relies on the presence of particular tau inclusions with cell/brain-region-speciﬁc distributions [30].”
Background
New classification of tauopathies
Höglinger, G. U., Respondek, G., & Kovacs, G. G. (2018) · Revue Neurologique · doi:10.1016/j.neurol.2018.07.001 · Cited by 57 · see citing works
Individual regional associations between Aβ-, tau- and neurodegeneration (ATN) with microglial activation in patients with primary and secondary tauopathies
Finze, A., Biechele, G., Rauchmann, B.-S., Franzmeier, N., Palleis, C., Katzdobler, S., Weidinger, E., Guersel, S., Schuster, S., Harris, S., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02188-8 · Cited by 40 · see citing works
The right temporal variant of frontotemporal dementia is not genetically sporadic: a case series
Ulugut Erkoyun, H., van der Lee, S. J., Nijmeijer, B., van Spaendonk, R., Nelissen, A., Scarioni, M., Dijkstra, A., Samancı, B., Gürvit, H., Yıldırım, Z., et al. (2021) · Journal of Alzheimer’s Disease · doi:10.3233/jad-201191 · Cited by 24 · see citing works
Tau liquid–liquid phase separation: At the crossroads of tau physiology and tauopathy
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Authors: Kovacs, G. G.
Affiliations: Institute of Neurology Medical University of Vienna Vienna Austria
Venue: Neuropathology and Applied Neurobiology
Publisher: Wiley
Published: 2015-01-29
Volume: 41
Issue: 1
Pages: 3-23
ISSN: 0305-1846 (ISSN-L)
1365-2990
DOI: 10.1111/nan.12208
OpenAlex: W1902303720
Cited by: 492
References: 124
Citations by year: 2026: 15 · 2025: 29 · 2024: 29 · 2023: 38 · 2022: 63 · 2021: 79 · 2020: 42 · 2019: 54 · 2018: 48 · 2017: 41 · 2016: 37 · 2015: 17
FWCI: 3.72
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Neuropathology and Applied Neurobiology (publishedVersion)
PubMed (publishedVersion)
Funders: European Commission's 7th Framework Programme (GA No 278486, DEVELAGE)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
Keywords: tauopathy, tau protein, neurodegenerative diseases, frontotemporal lobar degeneration, Pick's disease, progressive supranuclear palsy, corticobasal degeneration, argyrophilic grain disease, primary age-related tauopathy, globular glial tauopathy, tau isoforms, tau mutations, nomenclature
MeSH terms: Brain, Humans, Mutation, tau Proteins, Tauopathies

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