Pathology of neurodegenerative diseases

Cold Spring Harbor Perspectives in Biology

Volumn 9, Issue 7, 2017, Pages

  Dugger, Brittany N ^a   Dickson, Dennis W ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN AGGREGATE;

CLASSIFICATION; DEGENERATIVE DISEASE; HUMAN; PATHOLOGY; PROTEIN CONFORMATION;

HUMANS; NEURODEGENERATIVE DISEASES; PROTEIN AGGREGATES; PROTEIN CONFORMATION;

EID: 85018863504     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a028035     Document Type: Review

References (157)

1. Adler CH, Connor DJ, Hentz JG, Sabbagh MN, Caviness JN, Shill HA, Noble B, Beach TG. 2010. Incidental Lewy body disease: Clinical comparison to a control cohort. Mov Disord 25: 642–646.
2. Adler CH, Beach TG, Hentz JG, Shill HA, Caviness JN, Driver-Dunckley E, Sabbagh MN, Sue LI, Jacobson SA, Belden CM, et al. 2014. Low clinical diagnostic accuracy of early vs. advanced Parkinson disease: Clinicopatholog-ic study. Neurology 83: 406–412.
3. Alafuzoff I, Ince PG, Arzberger T, Al-Sarraj S, Bell J, Bodi I, Bogdanovic N, Bugiani O, Ferrer I, Gelpi E, et al. 2009a. Staging/typing of Lewy body related α-synuclein pathology: A study of the BrainNet Europe Consortium. Acta Neuropathol 117: 635–652.
4. Alafuzoff I, Thal DR, Arzberger T, Bogdanovic N, Al-Sarraj S, Bodi I, Boluda S, Bugiani O, Duyckaerts C, Gelpi E, et al. 2009b. Assessment of β-amyloid deposits in human brain: A study of the BrainNet Europe Consortium. Acta Neuropathol 117: 309–320.
5. Alafuzoff I, Pikkarainen M, Neumann M, Arzberger T, Al-Sarraj S, Bodi I, Bogdanovic N, Bugiani O, Ferrer I, Gelpi E, et al. 2015. Neuropathological assessments of the pathology in frontotemporal lobar degeneration with TDP43-positive inclusions: An inter-laboratory study by the BrainNet Europe consortium. J Neural Transm (Vienna) 122: 957–972.
6. Alonso AC, Li B, Grundke-Iqbal I, Iqbal K. 2008. Mechanism of tau-induced neurodegeneration in Alzheimer disease and related tauopathies. Curr Alzheimer Res 5: 375–384.
7. Amador-Ortiz C, Lin WL, Ahmed Z, Personett D, Davies P, Duara R, Graff-Radford NR, Hutton ML, Dickson DW. 2007. TDP-43 immunoreactivity in hippocampal sclerosis and Alzheimer’s disease. Ann Neurol 61: 435– 445.
8. Andreadis A. 2005. Tau gene alternative splicing: Expression patterns, regulation and modulation of function in nor- mal brain and neurodegenerative diseases. Biochim Biophys Acta 1739: 91–103.
9. Arai T, Ikeda K, Akiyama H, Nonaka T, Hasegawa M, Ishi-guro K, Iritani S, Tsuchiya K, Iseki E, Yagishita S, et al. 2004. Identification of amino-terminally cleaved tau fragments that distinguish progressive supranuclear palsy from corticobasal degeneration. Ann Neurol 55: 72–79.
10. Armstrong RA, Lantos PL, Cairns NJ. 2005. Overlap between neurodegenerative disorders. Neuropathology 25: 111–124.
11. Armstrong MJ, Litvan I, Lang AE, Bak TH, Bhatia KP, Bor-roni B, Boxer AL, Dickson DW, Grossman M, Hallett M, et al. 2013. Criteria for the diagnosis of corticobasal degeneration. Neurology 80: 496–503.
12. Arnold SJ, Dugger BN, Beach TG. 2013. TDP-43 deposition in prospectively followed, cognitively normal elderly individuals: Correlation with argyrophilic grains but not other concomitant pathologies. Acta Neuropathol 126: 51–57.
13. Bang J, Spina S, Miller BL. 2015. Frontotemporal dementia. Lancet 386: 1672–1682.
14. Beach TG, Adler CH, Lue L, Sue LI, Bachalakuri J, Henry-Watson J, Sasse J, Boyer S, Shirohi S, Brooks R, et al. 2009. Unified staging system for Lewy body disorders: Correlation with nigrostriatal degeneration, cognitive impairment and motor dysfunction. Acta Neuropathol 117: 613–634.
15. Beach TG, Monsell SE, Phillips LE, Kukull W. 2012. Accuracy of the clinical diagnosis of Alzheimer disease at National Institute on Aging Alzheimer Disease Centers, 2005–2010. J Neuropathol Exp Neurol 71: 266–273.
16. Bieniek KF, Ross OA, Cormier KA, Walton RL, Soto-Ortolaza A, Johnston AE, DeSaro P, Boylan KB, Graff-Radford NR, Wszolek ZK, et al. 2015. Chronic traumatic encephalopathy pathology in a neurodegenerative disorders brain bank. Acta Neuropathol 130: 877–889.
17. Binder LI, Frankfurter A, Rebhun LI. 1985. The distribution of tau in the mammalian central nervous system. J Cell Biol 101: 1371–1378.
18. Braak H, Braak E. 1987. Argyrophilic grains: Characteristic pathology of cerebral cortex in cases of adult onset dementia without Alzheimer changes. Neurosci Lett 76: 124–127.
19. Braak H, Braak E. 1991. Neuropathological stageing of Alz-heimer-related changes. Acta Neuropathol 82: 239–259.
20. Braak H, Braak E, Grundke-Iqbal I, Iqbal K. 1986. Occurrence of neuropil threads in the senile human brain and in Alzheimer’s disease: A third location of paired helical filaments outside of neurofibrillary tangles and neuritic plaques. Neurosci Lett 65: 351–355.
21. Braak H, Del Tredici K. 2016. Potential pathways of abnormal tau and α-synuclein dissemination in sporadic Alzheimer’s and Parkinson’s diseases. Cold Spring Harb Perspect Biol 8: a023630.
22. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E. 2003. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24: 197– 211.
23. Braak H, Thal DR, Ghebremedhin E, Del Tredici K. 2011. Stages of the pathologic process in Alzheimer disease: Age categories from 1 to 100 years. J Neuropathol Exp Neurol 70: 960–969.
24. Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, Suh E, Van Deerlin VM, Wood EM, Baek Y, et al. 2013. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol 74: 20–38.
25. Brettschneider J, Del Tredici K, Irwin DJ, Grossman M, Robinson JL, Toledo JB, Lee EB, Fang L, Van Deerlin VM, Ludolph AC, et al. 2014. Sequential distribution of pTDP-43 pathology in behavioral variant frontotemporal dementia (bvFTD). Acta Neuropathol 127: 423–439.
26. Budka H, Aguzzi A, Brown P, Brucher JM, Bugiani O, Gul-lotta F, Haltia M, Hauw JJ, Ironside JW, Jellinger K, et al. 1995. Neuropathological diagnostic criteria for Creutz-feldt–Jakob disease (CJD) and other human spongiform encephalopathies (prion diseases). Brain Pathol 5: 459– 466.
27. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR. 2000. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33: 95–130.
28. Constantinidis J, Richard J, Tissot R. 1974. Pick’s disease. Histological and clinical correlations. Eur Neurol 11: 208–217.
29. Cook C, Stankowski JN, Carlomagno Y, Stetler C, Petrucelli L. 2014. Acetylation: A new key to unlock tau’s role in neurodegeneration. Alzheimers Res Ther 6: 29.
30. Crary JF, Trojanowski JQ, Schneider JA, Abisambra JF, Abner EL, Alafuzoff I, Arnold SE, Attems J, Beach TG, Bigio EH, et al. 2014. Primary age-related tauopathy (PART): A common pathology associated with human aging. Acta Neuropathol 128: 755–766.
31. Cykowski MD, Coon EA, Powell SZ, Jenkins SM, Benarroch EE, Low PA, Schmeichel AM, Parisi JE. 2015. Expanding the spectrum of neuronal pathology in multiple system atrophy. Brain 138: 2293–2309.
32. DeJesus-Hernandez M, Mackenzie IR, Boeve B, Boxer Al, Baker M, Rutherford NJ, Nicholson AM, Finch NA, Flynn H, Adamson J, et al. 2011. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72: 245–256.
33. Dickson DW. 1997. The pathogenesis of senile plaques. J Neuropathol Exp Neurol 56: 321–339.
34. Dickson DW. 1998. Pick’s disease: A modern approach. Brain Pathol 8: 339–354.
35. Dickson DW. 2001. α-Synuclein and the Lewy body disorders. Curr Opin Neurol 14: 423–432.
36. Dickson DW, Bergeron C, Chin SS, Duyckaerts C, Horou-pian D, Ikeda K, Jellinger K, Lantos PL, Lippa CF, Mirra SS, et al. 2002. Office of Rare Diseases neuropathologic criteria for corticobasal degeneration. J Neuropathol Exp Neurol 61: 935–946.
37. Dickson DW, Ahmed Z, Algom AA, Tsuboi Y, Josephs KA. 2010. Neuropathology of variants of progressive supranuclear palsy. Curr Opin Neurol 23: 394–400.
38. Dickson DW, Kouri N, Murray ME, Josephs KA. 2011. Neuropathology of frontotemporal lobar degeneration-tau (FTLD-tau). J Mol Neurosci 45: 384–389.
39. Dugger BN, Dickson DW. 2010. Cell type specific sequestration of choline acetyltransferase and tyrosine hydroxylase within Lewy bodies. Acta Neuropathol 120: 633–639.
40. Dugger BN, Serrano GE, Sue LI, Walker DG, Adler CH, Shill HA, Sabbagh MN, Caviness JN, Hidalgo J, Saxon-Labelle M, et al. 2012. Presence of striatal amyloid plaques in Parkinson’s disease dementia predicts concomitant Alzheimer’s disease: Usefulness for amyloid imaging. J Par-kinsons Dis 2: 57–65.
41. Dugger BN, Adler CH, Shill HA, Caviness J, Jacobson S, Driver-Dunckley E, Beach TG. 2014a. Concomitant pathologies among a spectrum of parkinsonian disorders. Parkinsonism Relat Disord 20: 525–529.
42. Dugger BN, Clark CM, Serrano G, Mariner M, Bedell BJ, Coleman RE, Doraiswamy PM, Lu M, Fleisher AS, Reiman EM, et al. 2014b. Neuropathologic heterogeneity does not impair florbetapir-positron emission tomography postmortem correlates. J Neuropathol Exp Neurol 73: 72–80.
43. Dugger BN, Hentz JG, Adler CH, Sabbagh MN, Shill HA, Jacobson S, Caviness JN, Belden C, Driver-Dunckley E, Davis KJ, et al. 2014c. Clinicopathological outcomes of prospectively followed normal elderly brain bank volunteers. J Neuropathol Exp Neurol 73: 244–252.
44. Ellison D. 2013. Neuropathology: A reference text of CNS pathology. Mosby, Edinburgh.
45. Espinoza M, de Silva R, Dickson DW, Davies P. 2008. Differential incorporation of tau isoforms in Alzheimer’s disease. J Alzheimers Dis 14: 1–16.
46. Evidente VG, Adler CH, Sabbagh MN, Connor DJ, Hentz JG, Caviness JN, Sue LI, Beach TG. 2011. Neuropathological findings of PSP in the elderly without clinical PSP: Possible incidental PSP? Parkinsonism Relat Disord 17: 365–371.
47. Feany MB, Dickson DW. 1995. Widespread cytoskeletal pathology characterizes corticobasal degeneration. Am J Pathol 146: 1388–1396.
48. Frigerio R, Fujishiro H, Ahn TB, Josephs KA, Maraganore DM, DelleDonne A, Parisi JE, Klos KJ, Boeve BF, Dickson DW, et al. 2011. Incidental Lewy body disease: Do some cases represent a preclinical stage of dementia with Lewy bodies? Neurobiol Aging 32: 857–863.
49. Fujishiro H, Uchikado H, Arai T, Hasegawa M, Akiyama H, Yokota O, Tsuchiya K, Togo T, Iseki E, Hirayasu Y. 2009. Accumulation of phosphorylated TDP-43 in brains of patients with argyrophilic grain disease. Acta Neuropathol 117: 151–158.
50. Fukumoto H, Asami-Odaka A, Suzuki N, Iwatsubo T. 1996. Association of Aβ 40-positive senile plaques with micro-glial cells in the brains of patients with Alzheimer’s disease and in non-demented aged individuals. Neurodegeneration 5: 13–17.
51. Galvin JE, Lee VM, Baba M, Mann DM, Dickson DW, Yamaguchi H, Schmidt ML, Iwatsubo T, Trojanowski JQ. 1997. Monoclonal antibodies to purified cortical Lewy bodies recognize the mid-size neurofilament subunit. Ann Neurol 42: 595–603.
52. Ghasemi M, Brown R. 2016. Genetics of amyotrophic lateral sclerosis. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a024125.
53. Ghetti B, Dlouhy SR, Giaccone G, Bugiani O, Frangione B, Farlow MR, Tagliavini F. 1995. Gerstmann–Sträussler– Scheinker disease and the Indiana kindred. Brain Pathol 5: 61–75.
54. Gibb WR, Lees AJ. 1988. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51: 745–752.
55. Gibb WR, Luthert PJ, Marsden CD. 1989. Corticobasal degeneration. Brain 112: 1171–1192.
56. Gijselinck I, Cruts M, Van Broeckhoven C. 2016. The genetics of C9orf72 expansions. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a026757.
57. Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, et al. 2008. Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71: 670–676.
58. Goedert M, Klug A, Crowther RA. 2006. Tau protein, the paired helical filament and Alzheimer’s disease. J Alzheimers Dis 9: 195–207.
59. Goldfarb LG, Brown P, McCombie WR, Goldgaber D, Swer-gold GD, Wills PR, Cervenakova L, Baron H, Gibbs CJ Jr, Gajdusek DC. 1991. Transmissible familial Creutzfeldt– Jakob disease associated with five, seven, and eight extra octapeptide coding repeats in the PRNP gene. Proc Natl Acad Sci 88: 10926–10930.
60. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM. 1986. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 261: 6084–6089.
61. Halliday G, Hely M, Reid W, Morris J. 2008. The progression of pathology in longitudinally followed patients with Parkinson’s disease. Acta Neuropathol 115: 409–415.
62. Halliday GM, Holton JL, Revesz T, Dickson DW. 2011. Neuropathology underlying clinical variability in patients with synucleinopathies. Acta Neuropathol 122: 187–204.
63. Hardy J, Duff K, Hardy KG, Perez-Tur J, Hutton M. 1998. Genetic dissection of Alzheimer’s disease and related de-mentias: amyloid and its relationship to tau. Nat Neurosci 1: 355–358.
64. Hassan A, Whitwell JL, Boeve BF, Jack CR Jr, Parisi JE, Dickson DW, Josephs KA. 2010. Symmetric corticobasal degeneration (S-CBD). Parkinsonism Relat Disord 16: 208– 214.
65. Hinz FI, Geschwind DH. 2016. Molecular genetics of neuro-degerative dementia. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a023705.
66. Hof PR, Bouras C, Buee L, Delacourte A, Perl DP, Morrison JH. 1992. Differential distribution of neurofibrillary tangles in the cerebral cortex of dementia pugilistica and Alzheimer’s disease cases. Acta Neuropathol 85: 23–30.
67. Holton JL, Ghiso J, Lashley T, Rostagno A, Guerin CJ, Gibb G, Houlden H, Ayling H, Martinian L, Anderton BH, et al. 2001. Regional distribution of amyloid-Bri deposition and its association with neurofibrillary degeneration in familial British dementia. Am J Pathol 158: 515–526.
68. Hsiao KK, Cass C, Schellenberg GD, Bird T, Devine-Gage E, Wisniewski H, Prusiner SB. 1991. A prion protein variant in a family with the telencephalic form of Gerstmann– Straussler–Scheinker syndrome. Neurology 41: 681–684.
69. Hu WT, Josephs KA, Knopman DS, Boeve BF, Dickson DW, Petersen RC, Parisi JE. 2008. Temporal lobar predominance of TDP-43 neuronal cytoplasmic inclusions in Alzheimer disease. Acta Neuropathol 116: 215–220.
70. Hughes AJ, Daniel SE, Kilford L, Lees AJ. 1992. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: A clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55: 181–184.
71. 0 -splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393: 702–705.
72. Hyman BT, Trojanowski JQ. 1997. Consensus recommendations for the postmortem diagnosis of Alzheimer disease from the National Institute on Aging and the Reagan Institute Working Group on diagnostic criteria for the neuropathological assessment of Alzheimer disease. J Neuropathol Exp Neurol 56: 1095–1097.
73. Ikeda K, Akiyama H, Haga C, Kondo H, Arima K, Oda T. 1994. Argyrophilic thread-like structure in corticobasal degeneration and supranuclear palsy. Neurosci Lett 174: 157–159.
74. Ince PG, Highley JR, Kirby J, Wharton SB, Takahashi H, Strong MJ, Shaw PJ. 2011. Molecular pathology and genetic advances in amyotrophic lateral sclerosis: An emerging molecular pathway and the significance of glial pathology. Acta Neuropathol 122: 657–671.
75. Irizarry MC, Growdon W, Gomez-Isla T, Newell K, George JM, Clayton DF, Hyman BT. 1998. Nigral and cortical Lewy bodies and dystrophic nigral neurites in Parkinson’s disease and cortical Lewy body disease contain α-synuclein immunoreactivity. J Neuropathol Exp Neurol 57: 334–337.
76. Ishizawa T, Mattila P, Davies P, Wang D, Dickson DW. 2003. Colocalization of tau and α-synuclein epitopes in Lewy bodies. J Neuropathol Exp Neurol 62: 389–397.
77. Janocko NJ, Brodersen KA, Soto-Ortolaza AI, Ross OA, Lie-singer AM, Duara R, Graff-Radford NR, Dickson DW, Murray ME. 2012. Neuropathologically defined subtypes of Alzheimer’s disease differ significantly from neurofibrillary tangle-predominant dementia. Acta Neuropathol 124: 681–692.
78. Josephs KA, Dickson DW. 2003. Diagnostic accuracy of progressive supranuclear palsy in the Society for Progressive Supranuclear Palsy brain bank. Mov Disord 18: 1018– 1026.
79. Josephs KA, Tsuboi Y, Cookson N, Watt H, Dickson DW. 2004. Apolipoprotein E epsilon 4 is a determinant for Alzheimer-type pathologic features in tauopathies, synucleinopathies, and frontotemporal degeneration. Arch Neurol 61: 1579–1584.
80. Josephs KA, Lin WL, Ahmed Z, Stroh DA, Graff-Radford NR, Dickson DW. 2008a. Frontotemporal lobar degeneration with ubiquitin-positive, but TDP-43-negative inclusions. Acta Neuropathol 116: 159–167.
81. Josephs KA, Whitwell JL, Ahmed Z, Shiung MM, Weigand SD, Knopman DS, Boeve BF, Parisi JE, Petersen RC, Dickson DW, et al. 2008b. β-Amyloid burden is not associated with rates of brain atrophy. Ann Neurol 63: 204–212.
82. Josephs KA, Whitwell JL, Parisi JE, Knopman DS, Boeve BF, Geda YE, Jack CR Jr, Petersen RC, Dickson DW. 2008c. Argyrophilic grains: A distinct disease or an additive pathology? Neurobiol Aging 29: 566–573.
83. Josephs KA, Murray ME, Whitwell JL, Parisi JE, Petrucelli L, Jack CR, Petersen RC, Dickson DW. 2014. Staging TDP- 43 pathology in Alzheimer’s disease. Acta Neuropathol 127: 441–450.
84. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, Multhaup G, Beyreuther K, Muller-Hill B. 1987. The precursor of Alzheimer’s disease amyloid A4 protein resembles a cell-surface receptor. Nature 325: 733–736.
85. Kertesz A, Hudson L, Mackenzie IR, Munoz DG. 1994. The pathology and nosology of primary progressive aphasia. Neurology 44: 2065–2072.
86. Kolb HC, Andrés JI. 2016. Tau positron emission tomography imaging. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a023721.
87. Kosaka K, Yoshimura M, Ikeda K, Budka H. 1984. Diffuse type of Lewy body disease: Progressive dementia with abundant cortical Lewy bodies and senile changes of varying degree—A new disease? Clin Neuropathol 3: 185–192.
88. Kouri N, Whitwell JL, Josephs KA, Rademakers R, Dickson DW. 2011. Corticobasal degeneration: A pathologically distinct 4R tauopathy. Nat Rev Neurol 7: 263–272.
89. Kovacs GG. 2015. Invited review: Neuropathology of tauopathies: Principles and practice. Neuropathol Appl Neurobiol 41: 3–23.
90. Kovacs GG, Ferrer I, Grinberg LT, Alafuzoff I, Attems J, Budka H, Cairns NJ, Crary JF, Duyckaerts C, Ghetti B, et al. 2016. Aging-related tau astrogliopathy (ARTAG): Harmonized evaluation strategy. Acta Neuropathol 131: 87–102.
91. Kuo YM, Kokjohn TA, Beach TG, Sue LI, Brune D, Lopez JC, Kalback WM, Abramowski D, Sturchler-Pierrat C, Stau-fenbiel M, et al. 2001. Comparative analysis of amyloid-β chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer’s disease brains. J Biol Chem 276: 12991–12998.
92. Kuusisto E, Parkkinen L, Alafuzoff I. 2003. Morphogenesis of Lewy bodies: Dissimilar incorporation of α-synuclein, ubiquitin, and p62. J Neuropathol Exp Neurol 62: 1241– 1253.
93. Lantos PL. 1998. The definition of multiple system atrophy: A review of recent developments. J Neuropathol Exp Neurol 57: 1099–1111.
94. Lee VM, Goedert M, Trojanowski JQ. 2001. Neurodegenerative tauopathies. Annu Rev Neurosci 24: 1121–1159.
95. Leverenz JB, Umar I, Wang Q, Montine TJ, McMillan PJ, Tsuang DW, Jin J, Pan C, Shin J, Zhu D, et al. 2007. Proteomic identification of novel proteins in cortical lewy bodies. Brain Pathol 17: 139–145.
96. Lomen-Hoerth C, Anderson T, Miller B. 2002. The overlap of amyotrophic lateral sclerosis and frontotemporal dementia. Neurology 59: 1077–1079.
97. Mackenzie IRA, Neumann M. 2016. Fused in sarcoma neuropathology in neurodegenerative disease. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a024299.
98. Mackenzie IR, Baborie A, Pickering-Brown S, Du Plessis D, Jaros E, Perry RH, Neary D, Snowden JS, Mann DM. 2006. Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration: Classification and relation to clinical phenotype. Acta Neuropathol 112: 539–549.
99. Mackenzie IR, Neumann M, Bigio EH, Cairns NJ, Alafuzoff I, Kril J, Kovacs GG, Ghetti B, Halliday G, Holm IE, et al. 2010. Nomenclature and nosology for neuropathologic subtypes of frontotemporal lobar degeneration: An update. Acta Neuropathol 119: 1–4.
100. Mackenzie IR, Neumann M, Baborie A, Sampathu DM, Du Plessis D, Jaros E, Perry RH, Trojanowski JQ, Mann DM, Lee VM. 2011. A harmonized classification system for FTLD-TDP pathology. Acta Neuropathol 122: 111–113.
101. Mandelkow EM, Mandelkow E. 2012. Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb Perspect Med 2: a006247.
102. Martin L, Latypova X, Terro F. 2011. Post-translational modifications of tau protein: implications for Alzheimer’s disease. Neurochem Int 58: 458–471.
103. Masters CL, Simms G, Weinman NA, Multhaup G, Mc-Donald BL, Beyreuther K. 1985. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci 82: 4245–4249.
104. McKee AC, Cantu RC, Nowinski CJ, Hedley-Whyte ET, Gav-ett BE, Budson AE, Santini VE, Lee HS, Kubilus CA, Stern RA. 2009. Chronic traumatic encephalopathy in athletes: Progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 68: 709–735.
105. McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH, Lee HS, Wojtowicz SM, Hall G, Baugh CM, et al. 2013. The spectrum of disease in chronic traumatic encephalopathy. Brain 136: 43–64.
106. McKee AC, Cairns NJ, Dickson DW, Folkerth RD, Dirk Keene C, Litvan I, Perl DP, Stein TD, Vonsattel JP, Stewart W, et al. 2015. The first NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. Acta Neuropathol 131: 75–86.
107. McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, et al. 2005. Diagnosis and management of dementia with Lewy bodies: Third report of the DLB Consortium. Neurology 65: 1863–1872.
108. Milenkovic I, Kovacs GG. 2013. Incidental corticobasal degeneration in a 76-year-old woman. Clin Neuropathol 32: 69–72.
109. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brown-lee LM, Vogel FS, Hughes JP, van Belle G, Berg L. 1991. The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part II: Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41: 479–486.
110. Montenigro PH, Corp DT, Stein TD, Cantu RC, Stern RA. 2015. Chronic traumatic encephalopathy: Historical origins and current perspective. Annu Rev Clin Psychol 11: 309–330.
111. Montine TJ, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Dickson DW, Duyckaerts C, Frosch MP, Masliah E, Mirra SS, et al. 2012. National Institute on Aging-Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer’s disease: A practical approach. Acta Neuropathol 123: 1–11.
112. Morishima M, Ihara Y. 1994. Posttranslational modifications of tau in paired helical filaments. Dementia 5: 282–288.
113. Murray ME, Graff-Radford NR, Ross OA, Petersen RC, Duara R, Dickson DW. 2011. Neuropathologically defined subtypes of Alzheimer’s disease with distinct clin- ical characteristics: A retrospective study. Lancet Neurol 10: 785–796.
114. Neumann M, Sampathu DM, Kwong LK, Truax AC, Mic-senyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, et al. 2006. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314: 130–133.
115. Neumann M, Mackenzie IR, Cairns NJ, Boyer PJ, Markesbery WR, Smith CD, Taylor JP, Kretzschmar HA, Kimonis VE, Forman MS. 2007. TDP-43 in the ubiquitin pathology of frontotemporal dementia with VCP gene mutations. J Neuropathol Exp Neurol 66: 152–157.
116. Petersen RC, Parisi JE, Dickson DW, Johnson KA, Knopman DS, Boeve BF, Jicha GA, Ivnik RJ, Smith GE, Tangalos EG, et al. 2006. Neuropathologic features of amnestic mild cognitive impairment. Arch Neurol 63: 665–672.
117. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, et al. 1997. Mutation in the α-synuclein gene identified in families with Parkinson’s disease. Science 276: 2045– 2047.
118. Prusiner SB. 1982. Novel proteinaceous infectious particles cause scrapie. Science 216: 136–144.
119. Prusiner SB. 1998. Prions. Proc Natl Acad Sci 95: 13363– 13383.
120. Prusiner SB, Woerman AL, Rampersaud R, Watts JC, Berry DB, Patel S, Oehler A, Lowe JK, Kravitz SN, Geschwind DH, et al. 2015. Evidence for α-synuclein prions causing multiple system atrophy in humans with signs of Parkinson’s disease. Proc Natl Acad Sci 112: E5308–E5317.
121. Ratti A, Buratti E. 2016. Physiological Functions and Patho-biology of TDP-43 and FUS/TLS proteins. J Neurochem 138: 95–111.
122. Rebeiz JJ, Kolodny EH, Richardson EP Jr. 1968. Cortico-dentatonigral degeneration with neuronal achromasia. Arch Neurol 18: 20–33.
123. Renton AE, Majounie E, Waite A, Símon-Sánchez J, Rol-linson S, Gibbs JR, Schymick JC, Laaksovirta H, van Swieten JC, Myllykangas L, et al. 2011. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72: 257–268.
124. Roberts GW. 1988. Immunocytochemistry of neurofibrillary tangles in dementia pugilistica and Alzheimer’s disease: Evidence for common genesis. Lancet 2: 1456– 1458.
125. Sampathu DM, Neumann M, Kwong LK, Chou TT, Micse-nyi M, Truax A, Bruce J, Grossman M, Trojanowski JQ, Lee VM. 2006. Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohistochemistry and novel monoclonal antibodies. Am J Pathol 169: 1343–1352.
126. Schmidt ML, Zhukareva V, Newell KL, Lee VM, Trojanowski JQ. 2001. Tau isoform profile and phosphorylation state in dementia pugilistica recapitulate Alzheimer’s disease. Acta Neuropathol 101: 518–524.
127. Schmitt FA, Davis DG, Wekstein DR, Smith CD, Ashford JW, Markesbery WR. 2000. “Preclinical” AD revisited: Neuropathology of cognitively normal older adults. Neurology 55: 370–376.
128. Schultz C, Ghebremedhin E, Del Tredici K, Rub U, Braak H. 2004. High prevalence of thorn-shaped astrocytes in the aged human medial temporal lobe. Neurobiol Aging 25: 397–405.
129. Seeley WW. 2016. Mapping neurodegenerative disease onset and progression. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a023622.
130. Selikhova M, Williams DR, Kempster PA, Holton JL, Revesz T, Lees AJ. 2009. A clinico-pathological study of subtypes in Parkinson’s disease. Brain 132: 2947–2957.
131. Sherzai A, Edland SD, Masliah E, Hansen L, Pizzo DP, Co-rey-Bloom J. 2013. Spongiform change in dementia with Lewy bodies and Alzheimer disease. Alzheimer Dis Assoc Disord 27: 157–161.
132. Sparks DL, Danner FW, Davis DG, Hackney C, Landers T, Coyne CM. 1994. Neurochemical and histopathologic alterations characteristic of Pick’s disease in a non-demented individual. J Neuropathol Exp Neurol 53: 37–42.
133. Spillantini MG, Goedert M. 2013. Tau pathology and neurodegeneration. Lancet Neurol 12: 609–622.
134. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. 1997. α-Synuclein in Lewy bodies. Nature 388: 839–840.
135. Stern RA, Daneshvar DH, Baugh CM, Seichepine DR, Montenigro PH, Riley DO, Fritts NG, Stamm JM, Robbins CA, McHale L, et al. 2013. Clinical presentation of chronic traumatic encephalopathy. Neurology 81: 1122–1129.
136. Sudhof TC, Rizo J. 2011. Synaptic vesicle exocytosis. Cold Spring Harb Perspect Biol 3: a005637.
137. Tagliavini F, Giaccone G, Frangione B, Bugiani O. 1988. Preamyloid deposits in the cerebral cortex of patients with Alzheimer’s disease and nondemented individuals. Neurosci Lett 93: 191–196.
138. TCW J, Goate AM. 2016. Genetics of β-amyloid precursor protein in Alzheimer’s disease. Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a024539.
139. Thal DR, Rub U, Orantes M, Braak H. 2002. Phases of A β-deposition in the human brain and its relevance for the development of AD. Neurology 58: 1791–1800.
140. Thenganatt MA, Jankovic J. 2014. Parkinson disease subtypes. JAMA Neurol 71: 499–504.
141. Togo T, Cookson N, Dickson DW. 2002a. Argyrophilic grain disease: Neuropathology, frequency in a dementia brain bank and lack of relationship with apolipoprotein E. Brain Pathol 12: 45–52.
142. Togo T, Sahara N, Yen SH, Cookson N, Ishizawa T, Hutton M, de Silva R, Lees A, Dickson DW. 2002b. Argyrophilic grain disease is a sporadic 4-repeat tauopathy. J Neuropathol Exp Neurol 61: 547–556.
143. Toledo JB, Gopal P, Raible K, Irwin DJ, Brettschneider J, Sedor S, Waits K, Boluda S, Grossman M, Van Deerlin VM, et al. 2016. Pathological α-synuclein distribution in subjects with coincident Alzheimer’s and Lewy body pathology. Acta Neuropathol 131: 393–409.
144. Tolnay M, Clavaguera F. 2004. Argyrophilic grain disease: A late-onset dementia with distinctive features among tauopathies. Neuropathology 24: 269–283.
145. Tolnay M, Probst A. 1998. Ballooned neurons expressing αB-crystallin as a constant feature of the amygdala in argyrophilic grain disease. Neurosci Lett 246: 165–168.
146. Uchihara T, Tsuchiya K, Nakamura A, Akiyama H. 2005. Silver staining profiles distinguish Pick bodies from neurofibrillary tangles of Alzheimer type: Comparison between Gallyas and Campbell –Switzer methods. Acta Neuropathol 109: 483–489.
147. Uchikado H, DelleDonne A, Ahmed Z, Dickson DW. 2006a. Lewy bodies in progressive supranuclear palsy represent an independent disease process. J Neuropathol Exp Neurol 65: 387–395.
148. Uchikado H, Lin WL, DeLucia MW, Dickson DW. 2006b. Alzheimer disease with amygdala Lewy bodies: A distinct form of α-synucleinopathy. J Neuropathol Exp Neurol 65: 685–697.
149. Ueda K, Fukushima H, Masliah E, Xia Y, Iwai A, Yoshimoto M, Otero DA, Kondo J, Ihara Y, Saitoh T. 1993. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc Natl Acad Sci 90: 11282–11286.
150. Vidal R, Frangione B, Rostagno A, Mead S, Revesz T, Plant G, Ghiso J. 1999. A stop-codon mutation in the BRI gene associated with familial British dementia. Nature 399: 776–781.
151. 0 region of the BRI gene originates an amyloid peptide that is associated with dementia in a Danish kindred. Proc Natl Acad Sci 97: 4920–4925.
152. Watts JC, Giles K, Oehler A, Middleton L, Dexter DT, Gentleman SM, DeArmond SJ, Prusiner SB. 2013. Transmission of multiple system atrophy prions to transgenic mice. Proc Natl Acad Sci 110: 19555–19560.
153. Weihl CC, Temiz P, Miller SE, Watts G, Smith C, Forman M, Hanson PI, Kimonis V, Pestronk A. 2008. TDP-43 accumulation in inclusion body myopathy muscle suggests a common pathogenic mechanism with frontotemporal dementia. J Neurol Neurosurg Psychiatry 79: 1186–1189.
154. Westermark P, Benson MD, Buxbaum JN, Cohen AS, Frangione B, Ikeda S, Masters CL, Merlini G, Saraiva MJ, Sipe JD. 2005. Amyloid: Toward terminology clarification. Report from the Nomenclature Committee of the International Society of Amyloidosis. Amyloid 12: 1–4.
155. Whitwell JL, Josephs KA, Murray ME, Kantarci K, Przybelski SA, Weigand SD, Vemuri P, Senjem ML, Parisi JE, Knopman DS, et al. 2008. MRI correlates of neurofibrillary tangle pathology at autopsy: Avoxel-based morphometry study. Neurology 71: 743–749.
156. Williams DR, Lees AJ. 2009. Progressive supranuclear palsy: Clinicopathological concepts and diagnostic challenges. Lancet Neurol 8: 270–279.
157. Woerman AL, Aoyagi A, Patel S, Kazmi SA, Lobach I, Grinberg LT, McKee AC, Seeley WW, Olson SH, Prusiner SB. 2016. Tau prions from Alzheimer’s disease and chronic traumatic encephalopathy patients propagate in cultured cells. Proc Natl Acad Sci doi: 10.1073/pnas.1616344113.