Invited review: Neuropathology of tauopathies: Principles and practice

Neuropathology and Applied Neurobiology

Volumn 41, Issue 1, 2015, Pages 3-23

  Kovacs, Gabor G ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Argyrophilic grain disease; Corticobasal degeneration; Globular glial tauopathy; Neurofibrillary tangle dementia; Pick's disease; Primary age related tauopathy; Progressive supranuclear palsy; Tau astrogliopathy in the elderly; Tauopathy

Indexed keywords

ALPHA SYNUCLEIN; APOLIPOPROTEIN E; PRION PROTEIN; TAR DNA BINDING PROTEIN; TAU PROTEIN; MAPT PROTEIN, HUMAN;

ACETYLATION; AGING; ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ARGYROPHILIA; ARGYROPHILIC GRAIN DISEASE; ASTROCYTE; CARBOXY TERMINAL SEQUENCE; CEREBELLAR ATAXIA; CHROMOSOME 17; CHRONIC TRAUMATIC ENCEPHALOPATHY; COILED BODY; CORTICOBASAL DEGENERATION; CYTOPATHOLOGY; DEAMINATION; DENTATE GYRUS; ELECTRON MICROSCOPY; EXON; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; GENETIC ANALYSIS; GENETIC RISK; GENOTYPE; GLOBULAR GLIAL TAUOPATHY; GLYCOSYLATION; GRANULE CELL; HAPLOTYPE; HIPPOCAMPAL SCLEROSIS; HIPPOCAMPUS; HISTOPATHOLOGY; HUMAN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MICROSCOPY; MICROTUBULE; NERVE FIBER TRANSPORT; NEUROFIBRILLARY TANGLE ONLY DEMENTIA; NEUROPATHOLOGY; NOMENCLATURE; OLIGODENDROGLIA; PARKINSONISM; PHENOTYPE; PICK PRESENILE DEMENTIA; PRIMARY AGE RELATED TAUOPATHY; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SENILE PLAQUE; SILVER STAINING; TANDEM REPEAT; TAUOPATHY; TRAUMATIC BRAIN INJURY; BRAIN; GENETICS; METABOLISM; MUTATION; PATHOLOGY; TAUOPATHIES;

BRAIN; HUMANS; MUTATION; TAU PROTEINS; TAUOPATHIES;

EID: 84923006997     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12208     Document Type: Review

References (123)

1. Cairns NJ, Bigio EH, Mackenzie IR, Neumann M, Lee VM, Hatanpaa KJ, White CL 3rd, Schneider JA, Grinberg LT, Halliday G, Duyckaerts C, Lowe JS, Holm IE, Tolnay M, Okamoto K, Yokoo H, Murayama S, Woulfe J, Munoz DG, Dickson DW, Ince PG, Trojanowski JQ, Mann DM. Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 2007; 114: 5-22
2. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW. A protein factor essential for microtubule assembly. Proc Natl Acad Sci U S A 1975; 72: 1858-1862
3. Lee G, Leugers CJ. Tau and tauopathies. Prog Mol Biol Transl Sci 2012; 107: 263-293
4. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989; 3: 519-526
5. Spillantini MG, Goedert M. Tau pathology and neurodegeneration. Lancet Neurol 2013; 12: 609-622
6. Cruts M, Theuns J, Van Broeckhoven C. Locus-specific mutation databases for neurodegenerative brain diseases. Hum Mutat 2012; 33: 1340-1344
7. Sergeant N, Delacourte A, Buee L. Tau protein as a differential biomarker of tauopathies. Biochim Biophys Acta 2005; 1739: 179-197
8. Iqbal K, Liu F, Gong CX, Alonso Adel C, Grundke-Iqbal I. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol 2009; 118: 53-69
9. Noble W, Hanger DP, Miller CC, Lovestone S. The importance of tau phosphorylation for neurodegenerative diseases. Front Neurol 2013; 4: 83
10. Kovacs GG, Botond G, Budka H. Protein coding of neurodegenerative dementias: the neuropathological basis of biomarker diagnostics. Acta Neuropathol 2010; 119: 389-408
11. Grinberg LT, Wang X, Wang C, Sohn PD, Theofilas P, Sidhu M, Arevalo JB, Heinsen H, Huang EJ, Rosen H, Miller BL, Gan L, Seeley WW. Argyrophilic grain disease differs from other tauopathies by lacking tau acetylation. Acta Neuropathol 2013; 125: 581-593
12. Irwin DJ, Cohen TJ, Grossman M, Arnold SE, Xie SX, Lee VM, Trojanowski JQ. Acetylated tau, a novel pathological signature in Alzheimer's disease and other tauopathies. Brain 2012; 135: 807-818
13. Baborie A, Griffiths TD, Jaros E, McKeith IG, Burn DJ, Richardson A, Ferrari R, Moreno J, Momeni P, Duplessis D, Pal P, Rollinson S, Pickering-Brown S, Thompson JC, Neary D, Snowden JS, Perry R, Mann DM. Pathological correlates of frontotemporal lobar degeneration in the elderly. Acta Neuropathol 2011; 121: 365-371
14. Dugger BN, Hentz JG, Adler CH, Sabbagh MN, Shill HA, Jacobson S, Caviness JN, Belden C, Driver-Dunckley E, Davis KJ, Sue LI, Beach TG. Clinicopathological outcomes of prospectively followed normal elderly brain bank volunteers. J Neuropathol Exp Neurol 2014; 73: 244-252
15. Evidente VG, Adler CH, Sabbagh MN, Connor DJ, Hentz JG, Caviness JN, Sue LI, Beach TG. Neuropathological findings of PSP in the elderly without clinical PSP: possible incidental PSP? Parkinsonism Relat Disord 2011; 17: 365-371
16. Kovacs GG, Milenkovic I, Wohrer A, Hoftberger R, Gelpi E, Haberler C, Honigschnabl S, Reiner-Concin A, Heinzl H, Jungwirth S, Krampla W, Fischer P, Budka H. Non-Alzheimer neurodegenerative pathologies and their combinations are more frequent than commonly believed in the elderly brain: a community-based autopsy series. Acta Neuropathol 2013; 126: 365-384
17. Kovacs GG, Rozemuller AJ, van Swieten JC, Gelpi E, Majtenyi K, Al-Sarraj S, Troakes C, Bodi I, King A, Hortobagyi T, Esiri MM, Ansorge O, Giaccone G, Ferrer I, Arzberger T, Bogdanovic N, Nilsson T, Leisser I, Alafuzoff I, Ironside JW, Kretzschmar H, Budka H. Neuropathology of the hippocampus in FTLD-Tau with Pick bodies: a study of the BrainNet Europe Consortium. Neuropathol Appl Neurobiol 2013; 39: 166-178
18. Gelpi E, Cullel F, Navarro-Otano J, Llado A. Globular glial-like inclusions in a patient with advanced Alzheimer's disease. Acta Neuropathol 2013; 126: 155-157
19. Williams DR, Lees AJ. Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol 2009; 8: 270-279
20. Dickson DW, Ahmed Z, Algom AA, Tsuboi Y, Josephs KA. Neuropathology of variants of progressive supranuclear palsy. Curr Opin Neurol 2010; 23: 394-400
21. Williams DR, Holton JL, Strand K, Revesz T, Lees AJ. Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov Disord 2007; 22: 2235-2241
22. Kouri N, Whitwell JL, Josephs KA, Rademakers R, Dickson DW. Corticobasal degeneration: a pathologically distinct 4R tauopathy. Nat Rev Neurol 2011; 7: 263-272
23. Kouri N, Oshima K, Takahashi M, Murray ME, Ahmed Z, Parisi JE, Yen SH, Dickson DW. Corticobasal degeneration with olivopontocerebellar atrophy and TDP-43 pathology: an unusual clinicopathologic variant of CBD. Acta Neuropathol 2013; 125: 741-752
24. Piguet O, Halliday GM, Reid WG, Casey B, Carman R, Huang Y, Xuereb JH, Hodges JR, Kril JJ. Clinical phenotypes in autopsy-confirmed Pick disease. Neurology 2011; 76: 253-259
25. Tolnay M, Probst A. Argyrophilic grain disease. Handb Clin Neurol 2008; 89: 553-563
26. Ishihara K, Araki S, Ihori N, Shiota J, Kawamura M, Yoshida M, Hashizume Y, Nakano I. Argyrophilic grain disease presenting with frontotemporal dementia: a neuropsychological and pathological study of an autopsied case with presenile onset. Neuropathology 2005; 25: 165-170
27. Tsuchiya K, Mitani K, Arai T, Yamada S, Komiya T, Esaki Y, Haga C, Yamanouchi H, Ikeda K. 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. Acta Neuropathol 2001; 102: 195-199
28. Jellinger KA, Attems J. Neurofibrillary tangle-predominant dementia: comparison with classical Alzheimer disease. Acta Neuropathol 2007; 113: 107-117
29. Murray ME, Graff-Radford NR, Ross OA, Petersen RC, Duara R, Dickson DW. Neuropathologically defined subtypes of Alzheimer's disease with distinct clinical characteristics: a retrospective study. Lancet Neurol 2011; 10: 785-796
30. Janocko NJ, Brodersen KA, Soto-Ortolaza AI, Ross OA, Liesinger AM, Duara R, Graff-Radford NR, Dickson DW, Murray ME. Neuropathologically defined subtypes of Alzheimer's disease differ significantly from neurofibrillary tangle-predominant dementia. Acta Neuropathol 2012; 124: 681-692
31. Fu YJ, Nishihira Y, Kuroda S, Toyoshima Y, Ishihara T, Shinozaki M, Miyashita A, Piao YS, Tan CF, Tani T, Koike R, Iwanaga K, Tsujihata M, Onodera O, Kuwano R, Nishizawa M, Kakita A, Ikeuchi T, Takahashi H. Sporadic four-repeat tauopathy with frontotemporal lobar degeneration, Parkinsonism, and motor neuron disease: a distinct clinicopathological and biochemical disease entity. Acta Neuropathol 2010; 120: 21-32
32. Josephs KA, Katsuse O, Beccano-Kelly DA, Lin WL, Uitti RJ, Fujino Y, Boeve BF, Hutton ML, Baker MC, Dickson DW. Atypical progressive supranuclear palsy with corticospinal tract degeneration. J Neuropathol Exp Neurol 2006; 65: 396-405
33. Ahmed Z, Bigio EH, Budka H, Dickson DW, Ferrer I, Ghetti B, Giaccone G, Hatanpaa KJ, Holton JL, Josephs KA, Powers J, Spina S, Takahashi H, White CL 3rd, Revesz T, Kovacs GG. Globular glial tauopathies (GGT): consensus recommendations. Acta Neuropathol 2013; 126: 537-544
34. Dickson DW, Rademakers R, Hutton ML. Progressive supranuclear palsy: pathology and genetics. Brain Pathol 2007; 17: 74-82
35. Russ C, Lovestone S, Baker M, Pickering-Brown SM, Andersen PM, Furlong R, Mann D, Powell JF. The extended haplotype of the microtubule associated protein tau gene is not associated with Pick's disease. Neurosci Lett 2001; 299: 156-158
36. Togo T, Sahara N, Yen SH, Cookson N, Ishizawa T, Hutton M, de Silva R, Lees A, Dickson DW. Argyrophilic grain disease is a sporadic 4-repeat tauopathy. J Neuropathol Exp Neurol 2002; 61: 547-556
37. Santa-Maria I, Haggiagi A, Liu X, Wasserscheid J, Nelson PT, Dewar K, Clark LN, Crary JF. The MAPT H1 haplotype is associated with tangle-predominant dementia. Acta Neuropathol 2012; 124: 693-704
38. Kovacs GG, Majtenyi K, Spina S, Murrell JR, Gelpi E, Hoftberger R, Fraser G, Crowther RA, Goedert M, Budka H, Ghetti B. White matter tauopathy with globular glial inclusions: a distinct sporadic frontotemporal lobar degeneration. J Neuropathol Exp Neurol 2008; 67: 963-975
39. Braak E, Braak H, Mandelkow EM. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 1994; 87: 554-567
40. Luna-Munoz J, Chavez-Macias L, Garcia-Sierra F, Mena R. Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phospho-dependent tau epitopes in Alzheimer's disease. J Alzheimers Dis 2007; 12: 365-375
41. de Silva R, Lashley T, Gibb G, Hanger D, Hope A, Reid A, Bandopadhyay R, Utton M, Strand C, Jowett T, Khan N, Anderton B, Wood N, Holton J, Revesz T, Lees A. Pathological inclusion bodies in tauopathies contain distinct complements of tau with three or four microtubule-binding repeat domains as demonstrated by new specific monoclonal antibodies. Neuropathol Appl Neurobiol 2003; 29: 288-302
42. Uchihara T. Silver diagnosis in neuropathology: principles, practice and revised interpretation. Acta Neuropathol 2007; 113: 483-499
43. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, Fraser G, Stalder AK, Beibel M, Staufenbiel M, Jucker M, Goedert M, Tolnay M. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 2009; 11: 909-913
44. Alafuzoff I, Pikkarainen M, Al-Sarraj S, Arzberger T, Bell J, Bodi I, Bogdanovic N, Budka H, Bugiani O, Ferrer I, Gelpi E, Giaccone G, Graeber MB, Hauw JJ, Kamphorst W, King A, Kopp N, Korkolopoulou P, Kovacs GG, Meyronet D, Parchi P, Patsouris E, Preusser M, Ravid R, Roggendorf W, Seilhean D, Streichenberger N, Thal DR, Kretzschmar H. Interlaboratory comparison of assessments of Alzheimer disease-related lesions: a study of the BrainNet Europe Consortium. J Neuropathol Exp Neurol 2006; 65: 740-757
45. Kuusisto E, Kauppinen T, Alafuzoff I. Use of p62/SQSTM1 antibodies for neuropathological diagnosis. Neuropathol Appl Neurobiol 2008; 34: 169-180
46. Pikkarainen M, Martikainen P, Alafuzoff I. The effect of prolonged fixation time on immunohistochemical staining of common neurodegenerative disease markers. J Neuropathol Exp Neurol 2010; 69: 40-52
47. Uchihara T, Nakamura A, Shibuya K, Yagishita S. Specific detection of pathological three-repeat tau after pretreatment with potassium permanganate and oxalic acid in PSP/CBD brains. Brain Pathol 2011; 21: 180-188
48. Wischik CM, Novak M, Edwards PC, Klug A, Tichelaar W, Crowther RA. Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci U S A 1988; 85: 4884-4888
49. Lee VM, Goedert M, Trojanowski JQ. Neurodegenerative tauopathies. Annu Rev Neurosci 2001; 24: 1121-1159
50. Arai T, Ikeda K, Akiyama H, Nonaka T, Hasegawa M, Ishiguro K, Iritani S, Tsuchiya K, Iseki E, Yagishita S, Oda T, Mochizuki A. Identification of amino-terminally cleaved tau fragments that distinguish progressive supranuclear palsy from corticobasal degeneration. Ann Neurol 2004; 55: 72-79
51. Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Wiche G, Seitelberger F, Grundke-Iqbal I, Iqbal K, Wisniewski HM. Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res 1989; 477: 90-99
52. Dickson DW. The pathogenesis of senile plaques. J Neuropathol Exp Neurol 1997; 56: 321-339
53. Su JH, Cummings BJ, Cotman CW. Plaque biogenesis in brain aging and Alzheimer's disease. II. Progressive transformation and developmental sequence of dystrophic neurites. Acta Neuropathol 1998; 96: 463-471
54. Wang D, Munoz DG. Qualitative and quantitative differences in senile plaque dystrophic neurites of Alzheimer's disease and normal aged brain. J Neuropathol Exp Neurol 1995; 54: 548-556
55. Dickson DW, Wertkin A, Kress Y, Ksiezak-Reding H, Yen SH. Ubiquitin immunoreactive structures in normal human brains. Distribution and developmental aspects. Lab Invest 1990; 63: 87-99
56. Ahmed Z, Doherty KM, Silveira-Moriyama L, Bandopadhyay R, Lashley T, Mamais A, Hondhamuni G, Wray S, Newcombe J, O'Sullivan SS, Wroe S, de Silva R, Holton JL, Lees AJ, Revesz T. Globular glial tauopathies (GGT) presenting with motor neuron disease or frontotemporal dementia: an emerging group of 4-repeat tauopathies. Acta Neuropathol 2011; 122: 415-428
57. Botez G, Probst A, Ipsen S, Tolnay M. Astrocytes expressing hyperphosphorylated tau protein without glial fibrillary tangles in argyrophilic grain disease. Acta Neuropathol 1999; 98: 251-256
58. Kovacs GG, Molnar K, Laszlo L, Strobel T, Botond G, Honigschnabl S, Reiner-Concin A, Palkovits M, Fischer P, Budka H. A peculiar constellation of tau pathology defines a subset of dementia in the elderly. Acta Neuropathol 2011; 122: 205-222
59. Santpere G, Ferrer I. Delineation of early changes in cases with progressive supranuclear palsy-like pathology. Astrocytes in striatum are primary targets of tau phosphorylation and GFAP oxidation. Brain Pathol 2009; 19: 177-187
60. Ferrer I, Lopez-Gonzalez I, Carmona M, Arregui L, Dalfo E, Torrejon-Escribano B, Diehl R, Kovacs GG. Glial and neuronal tau pathology in tauopathies: characterization of disease-specific phenotypes and tau pathology progression. J Neuropathol Exp Neurol 2014; 73: 81-97
61. Arima K. Ultrastructural characteristics of tau filaments in tauopathies: immuno-electron microscopic demonstration of tau filaments in tauopathies. Neuropathology 2006; 26: 475-483
62. Dickson DW. Pick's disease: a modern approach. Brain Pathol 1998; 8: 339-354
63. Zhukareva V, Mann D, Pickering-Brown S, Uryu K, Shuck T, Shah K, Grossman M, Miller BL, Hulette CM, Feinstein SC, Trojanowski JQ, Lee VM. Sporadic Pick's disease: a tauopathy characterized by a spectrum of pathological tau isoforms in gray and white matter. Ann Neurol 2002; 51: 730-739
64. Williams DR, Holton JL, Strand C, Pittman A, de Silva R, Lees AJ, Revesz T. Pathological tau burden and distribution distinguishes progressive supranuclear palsy-parkinsonism from Richardson's syndrome. Brain 2007; 130: 1566-1576
65. Dickson DW, Bergeron C, Chin SS, Duyckaerts C, Horoupian D, Ikeda K, Jellinger K, Lantos PL, Lippa CF, Mirra SS, Tabaton M, Vonsattel JP, Wakabayashi K, Litvan I. Office of rare diseases neuropathologic criteria for corticobasal degeneration. J Neuropathol Exp Neurol 2002; 61: 935-946
66. Dickson DW. Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration. J Neurol 1999; 246 (Suppl. 2): II6-15
67. Clavaguera F, Akatsu H, Fraser G, Crowther RA, Frank S, Hench J, Probst A, Winkler DT, Reichwald J, Staufenbiel M, Ghetti B, Goedert M, Tolnay M. Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci U S A 2013; 110: 9535-9540
68. Tolnay M, Clavaguera F. Argyrophilic grain disease: a late-onset dementia with distinctive features among tauopathies. Neuropathology 2004; 24: 269-283
69. Braak H, Braak E. Argyrophilic grains: characteristic pathology of cerebral cortex in cases of adult onset dementia without Alzheimer changes. Neurosci Lett 1987; 76: 124-127
70. Dickson DW, Crystal HA, Mattiace LA, Masur DM, Blau AD, Davies P, Yen SH, Aronson MK. Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol Aging 1992; 13: 179-189
71. Ferrer I, Santpere G, van Leeuwen FW. Argyrophilic grain disease. Brain 2008; 131: 1416-1432
72. Saito Y, Ruberu NN, Sawabe M, Arai T, Tanaka N, Kakuta Y, Yamanouchi H, Murayama S. Staging of argyrophilic grains: an age-associated tauopathy. J Neuropathol Exp Neurol 2004; 63: 911-918
73. Josephs KA, Whitwell JL, Parisi JE, Knopman DS, Boeve BF, Geda YE, Jack CR Jr, Petersen RC, Dickson DW. Argyrophilic grains: a distinct disease or an additive pathology? Neurobiol Aging 2008; 29: 566-573
74. Crary JF, Trojanowski JQ, Schneider JA, Abisambra JF, Abner EL, Alafuzoff I, Arnold SE, Attems J, Beach TG, Bigio EH, Cairns NJ, Dickson DW, Gearing M, Grinberg LT, Hof PR, Hyman BT, Jellinger K, Jicha GA, Kovacs GG, Knopman DS, Kofler J, Kukull WA, Mackenzie IR, Masliah E, McKee A, Montine TJ, Murray ME, Neltner JH, Santa-Maria I, Seeley WW, Serrano-Pozo A, Shelanski ML, Stein T, Takao M, Thal DR, Toledo JB, Troncoso JC, Vonsattel JP, White CL 3rd, Wisniewski T, Woltjer RL, Yamada M, Nelson PT. Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol 2014; 128: 755-766
75. Kawakami I, Hasegawa M, Arai T, Ikeda K, Oshima K, Niizato K, Aoki N, Omi K, Higashi S, Hosokawa M, Hirayasu Y, Akiyama H. Tau accumulation in the nucleus accumbens in tangle-predominant dementia. Acta Neuropathol Commun 2014; 2: 40
76. Ishizawa T, Ko LW, Cookson N, Davias P, Espinoza M, Dickson DW. Selective neurofibrillary degeneration of the hippocampal CA2 sector is associated with four-repeat tauopathies. J Neuropathol Exp Neurol 2002; 61: 1040-1047
77. Milenkovic I, Petrov T, Kovacs GG. Patterns of hippocampal tau pathology differentiate neurodegenerative dementias. Dement Geriatr Cogn Disord 2014; 38: 375-388
78. Hishikawa N, Hashizume Y, Yoshida M, Niwa J, Tanaka F, Sobue G. Tuft-shaped astrocytes in Lewy body disease. Acta Neuropathol 2005; 109: 373-380
79. Duda JE, Giasson BI, Mabon ME, Miller DC, Golbe LI, Lee VM, Trojanowski JQ. Concurrence of alpha-synuclein and tau brain pathology in the Contursi kindred. Acta Neuropathol 2002; 104: 7-11
80. Kiely AP, Asi YT, Kara E, Limousin P, Ling H, Lewis P, Proukakis C, Quinn N, Lees AJ, Hardy J, Revesz T, Houlden H, Holton JL. Alpha-synucleinopathy associated with G51D SNCA mutation: a link between Parkinson's disease and multiple system atrophy? Acta Neuropathol 2013; 125: 753-769
81. Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, Lincoln S, Kachergus J, Hulihan M, Uitti RJ, Calne DB, Stoessl AJ, Pfeiffer RF, Patenge N, Carbajal IC, Vieregge P, Asmus F, Muller-Myhsok B, Dickson DW, Meitinger T, Strom TM, Wszolek ZK, Gasser T. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 2004; 44: 601-607
82. Bieniek KF, Murray ME, Rutherford NJ, Castanedes-Casey M, DeJesus-Hernandez M, Liesinger AM, Baker MC, Boylan KB, Rademakers R, Dickson DW. Tau pathology in frontotemporal lobar degeneration with C9ORF72 hexanucleotide repeat expansion. Acta Neuropathol 2013; 125: 289-302
83. King A, Al-Sarraj S, Troakes C, Smith BN, Maekawa S, Iovino M, Spillantini MG, Shaw CE. Mixed tau, TDP-43 and p62 pathology in FTLD associated with a C9ORF72 repeat expansion and p.Ala239Thr MAPT (tau) variant. Acta Neuropathol 2013; 125: 303-310
84. Kovacs GG, Budka H. The spectrum of tau pathology in human prion disease. In Prions and Diseases. Eds W-Q Zou, P Gambetti. New York: Springer, 2013; 103-119
85. Ghetti B, Tagliavini F, Takao M, Bugiani O, Piccardo P. Hereditary prion protein amyloidoses. Clin Lab Med 2003; 23: 65-85, viii
86. Kovacs GG, Seguin J, Quadrio I, Hoftberger R, Kapas I, Streichenberger N, Biacabe AG, Meyronet D, Sciot R, Vandenberghe R, Majtenyi K, Laszlo L, Strobel T, Budka H, Perret-Liaudet A. Genetic Creutzfeldt-Jakob disease associated with the E200K mutation: characterization of a complex proteinopathy. Acta Neuropathol 2011; 121: 39-57
87. Kosaka K. Diffuse neurofibrillary tangles with calcification: a new presenile dementia. J Neurol Neurosurg Psychiatry 1994; 57: 594-596
88. Shibayama H, Kobayashi H, Nakagawa M, Yamada K, Iwata H, Iwai K, Takeuchi T, Mu-Qune X, Ishihara R, Iwase S. Non-Alzheimer non-Pick dementia with Fahr's syndrome. Clin Neuropathol 1992; 11: 237-250
89. Hashimoto N, Takeuchi T, Ishihara R, Ukai K, Kobayashi H, Iwata H, Iwai K, Mizuno Y, Yamaguchi H, Shibayama H. Glial fibrillary tangles in diffuse neurofibrillary tangles with calcification. Acta Neuropathol 2003; 106: 150-156
90. Habuchi C, Iritani S, Sekiguchi H, Torii Y, Ishihara R, Arai T, Hasegawa M, Tsuchiya K, Akiyama H, Shibayama H, Ozaki N. Clinicopathological study of diffuse neurofibrillary tangles with calcification. With special reference to TDP-43 proteinopathy and alpha-synucleinopathy. J Neurol Sci 2011; 301: 77-85
91. Holton JL, Ghiso J, Lashley T, Rostagno A, Guerin CJ, Gibb G, Houlden H, Ayling H, Martinian L, Anderton BH, Wood NW, Vidal R, Plant G, Frangione B, Revesz T. Regional distribution of amyloid-Bri deposition and its association with neurofibrillary degeneration in familial British dementia. Am J Pathol 2001; 158: 515-526
92. Li A, Paudel R, Johnson R, Courtney R, Lees AJ, Holton JL, Hardy J, Revesz T, Houlden H. Pantothenate kinase-associated neurodegeneration is not a synucleinopathy. Neuropathol Appl Neurobiol 2012; 39: 121-131
93. Paisan-Ruiz C, Li A, Schneider SA, Holton JL, Johnson R, Kidd D, Chataway J, Bhatia KP, Lees AJ, Hardy J, Revesz T, Houlden H. Widespread Lewy body and tau accumulation in childhood and adult onset dystonia-parkinsonism cases with PLA2G6 mutations. Neurobiol Aging 2012; 33: 814-823
94. Distl R, Treiber-Held S, Albert F, Meske V, Harzer K, Ohm TG. Cholesterol storage and tau pathology in Niemann-Pick type C disease in the brain. J Pathol 2003; 200: 104-111
95. Jellinger KA. Absence of alpha-synuclein pathology in postencephalitic parkinsonism. Acta Neuropathol 2009; 118: 371-379
96. Buee-Scherrer V, Buee L, Leveugle B, Perl DP, Vermersch P, Hof PR, Delacourte A. Pathological tau proteins in postencephalitic parkinsonism: comparison with Alzheimer's disease and other neurodegenerative disorders. Ann Neurol 1997; 42: 356-359
97. Miklossy J, Steele JC, Yu S, McCall S, Sandberg G, McGeer EG, McGeer PL. Enduring involvement of tau, beta-amyloid, alpha-synuclein, ubiquitin and TDP-43 pathology in the amyotrophic lateral sclerosis/parkinsonism-dementia complex of Guam (ALS/PDC). Acta Neuropathol 2008; 116: 625-637
98. Ikeda K, Akiyama H, Kondo H, Arai T, Arai N, Yagishita S. Numerous glial fibrillary tangles in oligodendroglia in cases of subacute sclerosing panencephalitis with neurofibrillary tangles. Neurosci Lett 1995; 194: 133-135
99. Garbern JY, Neumann M, Trojanowski JQ, Lee VM, Feldman G, Norris JW, Friez MJ, Schwartz CE, Stevenson R, Sima AA. A mutation affecting the sodium/proton exchanger, SLC9A6, causes mental retardation with tau deposition. Brain 2010; 133: 1391-1402
100. Kapas I, Katko M, Harangi M, Paragh G, Balogh I, Koczi Z, Regelsberger G, Molnar MJ, Kovacs GG. Cerebrotendinous xanthomatosis with the c.379C>T (p.R127W) mutation in the CYP27A1 gene associated with premature age-associated limbic tauopathy. Neuropathol Appl Neurobiol 2014; 40: 345-350
101. Gelpi E, van der Zee J, Turon Estrada A, Van Broeckhoven C, Sanchez-Valle R. TARDBP mutation p.Ile383Val associated with semantic dementia and complex proteinopathy. Neuropathol Appl Neurobiol 2014; 40: 225-230
102. Miki Y, Mori F, Hori E, Kaimori M, Wakabayashi K. Hippocampal sclerosis with four-repeat tau-positive round inclusions in the dentate gyrus: a new type of four-repeat tauopathy. Acta Neuropathol 2009; 117: 713-718
103. McKee AC, Cantu RC, Nowinski CJ, Hedley-Whyte ET, Gavett BE, Budson AE, Santini VE, Lee HS, Kubilus CA, Stern RA. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 2009; 68: 709-735
104. Schmidt ML, Zhukareva V, Newell KL, Lee VM, Trojanowski JQ. Tau isoform profile and phosphorylation state in dementia pugilistica recapitulate Alzheimer's disease. Acta Neuropathol 2001; 101: 518-524
105. Stein TD, Alvarez VE, McKee AC. Chronic traumatic encephalopathy: a spectrum of neuropathological changes following repetitive brain trauma in athletes and military personnel. Alzheimers Res Ther 2014; 6: 4
106. McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH, Lee HS, Wojtowicz SM, Hall G, Baugh CM, Riley DO, Kubilus CA, Cormier KA, Jacobs MA, Martin BR, Abraham CR, Ikezu T, Reichard RR, Wolozin BL, Budson AE, Goldstein LE, Kowall NW, Cantu RC. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013; 136: 43-64
107. Ling H, Kara E, Revesz T, Lees AJ, Plant GT, Martino D, Houlden H, Hardy J, Holton JL. Concomitant progressive supranuclear palsy and chronic traumatic encephalopathy in a boxer. Acta Neuropathol Commun 2014; 2: 24
108. Ikeda K. Glial fibrillary tangles and argyrophilic threads: classification and disease specificity. Neuropathology 1996; 16: 71-77
109. Schultz C, Ghebremedhin E, Del Tredici K, Rub U, Braak H. High prevalence of thorn-shaped astrocytes in the aged human medial temporal lobe. Neurobiol Aging 2004; 25: 397-405
110. Uchikado H, Fujino Y, Lin W, Dickson D. Frequency and relation of argyrophilic grain disease and Thorn-shaped astrocytes in Alzheimer's disease. In Advances in Alzheimer's and Parkinsons Disease. Eds A Fisher, M Memo, F Stocchi, I Hanin. New York, USA: Springer, 2008; 375-379
111. Munoz DG, Woulfe J, Kertesz A. Argyrophilic thorny astrocyte clusters in association with Alzheimer's disease pathology in possible primary progressive aphasia. Acta Neuropathol 2007; 114: 347-357
112. Sakai K, Piao YS, Kikugawa K, Ohara S, Hasegawa M, Takano H, Fukase M, Nishizawa M, Kakita A, Takahashi H. Corticobasal degeneration with focal, massive tau accumulation in the subcortical white matter astrocytes. Acta Neuropathol 2006; 112: 341-348
113. Lace G, Ince PG, Brayne C, Savva GM, Matthews FE, de Silva R, Simpson JE, Wharton SB. Mesial temporal astrocyte tau pathology in the MRC-CFAS ageing brain cohort. Dement Geriatr Cogn Disord 2012; 34: 15-24
114. Beach TG, Sue L, Scott S, Layne K, Newell A, Walker D, Baker M, Sahara N, Yen SH, Hutton M, Caselli R, Adler C, Connor D, Sabbagh M. Hippocampal sclerosis dementia with tauopathy. Brain Pathol 2003; 13: 263-278
115. Kovacs GG, Budka H. Current concepts of neuropathological diagnostics in practice: neurodegenerative diseases. Clin Neuropathol 2010; 29: 271-288
116. Uryu K, Nakashima-Yasuda H, Forman MS, Kwong LK, Clark CM, Grossman M, Miller BL, Kretzschmar HA, Lee VM, Trojanowski JQ, Neumann M. Concomitant TAR-DNA-binding protein 43 pathology is present in Alzheimer disease and corticobasal degeneration but not in other tauopathies. J Neuropathol Exp Neurol 2008; 67: 555-564
117. Fujishiro H, Uchikado H, Arai T, Hasegawa M, Akiyama H, Yokota O, Tsuchiya K, Togo T, Iseki E, Hirayasu Y. Accumulation of phosphorylated TDP-43 in brains of patients with argyrophilic grain disease. Acta Neuropathol 2009; 117: 151-158
118. Popescu A, Lippa CF, Lee VM, Trojanowski JQ. Lewy bodies in the amygdala: increase of alpha-synuclein aggregates in neurodegenerative diseases with tau-based inclusions. Arch Neurol 2004; 61: 1915-1919
119. Uchikado H, DelleDonne A, Ahmed Z, Dickson DW. Lewy bodies in progressive supranuclear palsy represent an independent disease process. J Neuropathol Exp Neurol 2006; 65: 387-395
120. Fujishiro H, Tsuboi Y, Lin WL, Uchikado H, Dickson DW. Co-localization of tau and alpha-synuclein in the olfactory bulb in Alzheimer's disease with amygdala Lewy bodies. Acta Neuropathol 2008; 116: 17-24
121. Silveira-Moriyama L, Gonzalez AM, O'Sullivan SS, Williams DR, Massey L, Parkkinen L, Ahmed Z, de Silva R, Chacon JR, Revesz T, Lees AJ, Holton JL. Concomitant progressive supranuclear palsy and multiple system atrophy: more than a simple twist of fate? Neurosci Lett 2009; 467: 208-211
122. Vilas D, Marti MJ, Botta-Orfila T, Colom-Cadena M, Gelpi E. Pick's pathology in Parkinson's disease with dementia. Neuropathol Appl Neurobiol 2012; 38: 737-743
123. Guo JL, Lee VM. Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases. Nat Med 2014; 20: 130-138