Distribution patterns of tau pathology in progressive supranuclear palsy.
Coiled body
Neurofibrillary tangle
Progressive supranuclear palsy
Propagation
Richardson syndrome
Sequential involvement
Stage
Tau
Tauopathy
Tufted astrocyte
Journal
Acta neuropathologica
ISSN: 1432-0533
Titre abrégé: Acta Neuropathol
Pays: Germany
ID NLM: 0412041
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
20
12
2019
accepted:
11
04
2020
revised:
16
03
2020
pubmed:
10
5
2020
medline:
3
8
2021
entrez:
9
5
2020
Statut:
ppublish
Résumé
Progressive supranuclear palsy (PSP) is a 4R-tauopathy predominated by subcortical pathology in neurons, astrocytes, and oligodendroglia associated with various clinical phenotypes. In the present international study, we addressed the question of whether or not sequential distribution patterns can be recognized for PSP pathology. We evaluated heat maps and distribution patterns of neuronal, astroglial, and oligodendroglial tau pathologies and their combinations in different clinical subtypes of PSP in postmortem brains. We used conditional probability and logistic regression to model the sequential distribution of tau pathologies across different brain regions. Tau pathology uniformly predominates in the neurons of the pallido-nigro-luysian axis in different clinical subtypes. However, clinical subtypes are distinguished not only by total tau load but rather cell-type (neuronal versus glial) specific vulnerability patterns of brain regions suggesting distinct dynamics or circuit-specific segregation of propagation of tau pathologies. For Richardson syndrome (n = 81) we recognize six sequential steps of involvement of brain regions by the combination of cellular tau pathologies. This is translated to six stages for the practical neuropathological diagnosis by the evaluation of the subthalamic nucleus, globus pallidus, striatum, cerebellum with dentate nucleus, and frontal and occipital cortices. This system can be applied to further clinical subtypes by emphasizing whether they show caudal (cerebellum/dentate nucleus) or rostral (cortical) predominant, or both types of pattern. Defining cell-specific stages of tau pathology helps to identify preclinical or early-stage cases for the better understanding of early pathogenic events, has implications for understanding the clinical subtype-specific dynamics of disease-propagation, and informs tau-neuroimaging on distribution patterns.
Identifiants
pubmed: 32383020
doi: 10.1007/s00401-020-02158-2
pii: 10.1007/s00401-020-02158-2
pmc: PMC7360645
doi:
Substances chimiques
MAPT protein, human
0
tau Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
99-119Subventions
Organisme : NIA NIH HHS
ID : P30 AG010124
Pays : United States
Organisme : NIA NIH HHS
ID : P01 AG017586
Pays : United States
Organisme : Medical Research Council
ID : MR/L016397/1
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : P01 AG066597
Pays : United States
Organisme : NIA NIH HHS
ID : U19 AG062418
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS109260
Pays : United States
Organisme : NCATS NIH HHS
ID : TL1 TR001880
Pays : United States
Organisme : NINDS NIH HHS
ID : K23 NS088341
Pays : United States
Références
Ahmed Z, Josephs KA, Gonzalez J, DelleDonne A, Dickson DW (2008) Clinical and neuropathologic features of progressive supranuclear palsy with severe pallido-nigro-luysial degeneration and axonal dystrophy. Brain 131:460–472. https://doi.org/10.1093/brain/awm301
doi: 10.1093/brain/awm301
pubmed: 18158316
Allen M, Wang X, Serie DJ, Strickland SL, Burgess JD, Koga S et al (2018) Divergent brain gene expression patterns associate with distinct cell-specific tau neuropathology traits in progressive supranuclear palsy. Acta Neuropathol 136:709–727. https://doi.org/10.1007/s00401-018-1900-5
doi: 10.1007/s00401-018-1900-5
pubmed: 30136084
pmcid: 6208732
Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259
doi: 10.1007/BF00308809
pubmed: 1759558
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
doi: 10.1016/S0197-4580(02)00065-9
pubmed: 12498954
Dickson DW (1999) Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration. J Neurol 246(2):6–15. https://doi.org/10.1007/bf03161076
doi: 10.1007/bf03161076
Dickson DW, Ahmed Z, Algom AA, Tsuboi Y, Josephs KA (2010) Neuropathology of variants of progressive supranuclear palsy. Curr Opin Neurol 23:394–400. https://doi.org/10.1097/WCO.0b013e32833be924
doi: 10.1097/WCO.0b013e32833be924
pubmed: 20610990
Dugger BN, Hentz JG, Adler CH, Sabbagh MN, Shill HA, Jacobson S et al (2014) Clinicopathological outcomes of prospectively followed normal elderly brain bank volunteers. J Neuropathol Exp Neurol 73:244–252. https://doi.org/10.1097/NEN.0000000000000046
doi: 10.1097/NEN.0000000000000046
pubmed: 24487796
Evidente VG, Adler CH, Sabbagh MN, Connor DJ, Hentz JG, Caviness JN et al (2011) Neuropathological findings of PSP in the elderly without clinical PSP: possible incidental PSP? Parkinsonism Relat Disord 17:365–371. https://doi.org/10.1016/j.parkreldis.2011.02.017
doi: 10.1016/j.parkreldis.2011.02.017
pubmed: 21420891
pmcid: 3109165
Forrest SL, Kril JJ, Halliday GM (2019) Cellular and regional vulnerability in frontotemporal tauopathies. Acta Neuropathol 138:705–727. https://doi.org/10.1007/s00401-019-02035-7
doi: 10.1007/s00401-019-02035-7
pubmed: 31203391
Gardner RC, Boxer AL, Trujillo A, Mirsky JB, Guo CC, Gennatas ED et al (2013) Intrinsic connectivity network disruption in progressive supranuclear palsy. Ann Neurol 73:603–616. https://doi.org/10.1002/ana.23844
doi: 10.1002/ana.23844
pubmed: 23536287
pmcid: 3732833
Gibbons GS, Lee VMY, Trojanowski JQ (2019) Mechanisms of cell-to-cell transmission of pathological tau: a review. JAMA Neurol 76:101–108. https://doi.org/10.1001/jamaneurol.2018.2505
doi: 10.1001/jamaneurol.2018.2505
pubmed: 30193298
pmcid: 6382549
Halliday GM, Macdonald V, Henderson JM (2005) A comparison of degeneration in motor thalamus and cortex between progressive supranuclear palsy and Parkinson's disease. Brain 128:2272–2280. https://doi.org/10.1093/brain/awh596
doi: 10.1093/brain/awh596
pubmed: 16014651
Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL et al (1994) Preliminary NINDS neuropathologic criteria for Steele–Richardson–Olszewski syndrome (progressive supranuclear palsy). Neurology 44:2015–2019. https://doi.org/10.1212/wnl.44.11.2015
doi: 10.1212/wnl.44.11.2015
pubmed: 7969952
Hoglinger GU, Respondek G, Stamelou M, Kurz C, Josephs KA, Lang AE et al (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 32:853–864. https://doi.org/10.1002/mds.26987
doi: 10.1002/mds.26987
pubmed: 28467028
pmcid: 5516529
Irwin DJ, Brettschneider J, McMillan CT, Cooper F, Olm C, Arnold SE et al (2016) Deep clinical and neuropathological phenotyping of Pick disease. Ann Neurol 79:272–287. https://doi.org/10.1002/ana.24559
doi: 10.1002/ana.24559
pubmed: 26583316
Jadhav S, Avila J, Scholl M, Kovacs GG, Kovari E, Skrabana R et al (2019) A walk through tau therapeutic strategies. Acta Neuropathol Commun 7:22. https://doi.org/10.1186/s40478-019-0664-z
doi: 10.1186/s40478-019-0664-z
pubmed: 30767766
pmcid: 6376692
Koga S, Parks A, Kasanuki K, Sanchez-Contreras M, Baker MC, Josephs KA et al (2017) Cognitive impairment in progressive supranuclear palsy is associated with tau burden. Mov Disord 32:1772–1779. https://doi.org/10.1002/mds.27198
doi: 10.1002/mds.27198
pubmed: 29082658
pmcid: 5732021
Kovacs GG (2015) Invited review: neuropathology of tauopathies: principles and practice. Neuropathol Appl Neurobiol 41:3–23. https://doi.org/10.1111/nan.12208
doi: 10.1111/nan.12208
pubmed: 25495175
Kovacs GG (2019) Molecular pathology of neurodegenerative diseases: principles and practice. J Clin Pathol 72:725–735. https://doi.org/10.1136/jclinpath-2019-205952
doi: 10.1136/jclinpath-2019-205952
pubmed: 31395625
Kovacs GG, Lee VM, Trojanowski JQ (2017) Protein astrogliopathies in human neurodegenerative diseases and aging. Brain Pathol 27:675–690. https://doi.org/10.1111/bpa.12536
doi: 10.1111/bpa.12536
pubmed: 28805003
pmcid: 5578412
Kovacs GG, Milenkovic I, Wohrer A, Hoftberger R, Gelpi E, Haberler C et al (2013) Non-Alzheimer neurodegenerative pathologies and their combinations are more frequent than commonly believed in the elderly brain: a community-based autopsy series. Acta Neuropathol 126:365–384. https://doi.org/10.1007/s00401-013-1157-y
doi: 10.1007/s00401-013-1157-y
pubmed: 23900711
Kovacs GG, Robinson JL, Xie SX, Lee EB, Grossman M, Wolk DA et al (2017) Evaluating the patterns of aging-related tau astrogliopathy unravels novel insights into brain aging and neurodegenerative diseases. J Neuropathol Exp Neurol 76:270–288. https://doi.org/10.1093/jnen/nlx007
doi: 10.1093/jnen/nlx007
pubmed: 28340083
pmcid: 6251691
Kovacs GG, Xie SX, Lee EB, Robinson JL, Caswell C, Irwin DJ et al (2017) Multisite assessment of aging-related tau astrogliopathy (ARTAG). J Neuropathol Exp Neurol 76:605–619. https://doi.org/10.1093/jnen/nlx041
doi: 10.1093/jnen/nlx041
pubmed: 28591867
pmcid: 6251511
Kovacs GG, Xie SX, Robinson JL, Lee EB, Smith DH, Schuck T et al (2018) Sequential stages and distribution patterns of aging-related tau astrogliopathy (ARTAG) in the human brain. Acta Neuropathol Commun 6:50. https://doi.org/10.1186/s40478-018-0552-y
doi: 10.1186/s40478-018-0552-y
pubmed: 29891013
pmcid: 5996526
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174
doi: 10.2307/2529310
pubmed: 843571
Lantos PL (1994) The neuropathology of progressive supranuclear palsy. J Neural Transm Suppl 42:137–152. https://doi.org/10.1007/978-3-7091-6641-3_11
doi: 10.1007/978-3-7091-6641-3_11
pubmed: 7964683
Ling H, de Silva R, Massey LA, Courtney R, Hondhamuni G, Bajaj N et al (2014) Characteristics of progressive supranuclear palsy presenting with corticobasal syndrome: a cortical variant. Neuropathol Appl Neurobiol 40:149–163. https://doi.org/10.1111/nan.12037
doi: 10.1111/nan.12037
pubmed: 23432126
pmcid: 4260147
Ling H, Kovacs GG, Vonsattel JP, Davey K, Mok KY, Hardy J et al (2016) Astrogliopathy predominates the earliest stage of corticobasal degeneration pathology. Brain 139:3237–3252. https://doi.org/10.1093/brain/aww256
doi: 10.1093/brain/aww256
pubmed: 27797812
Milenkovic I, Petrov T, Kovacs GG (2014) Patterns of hippocampal tau pathology differentiate neurodegenerative dementias. Dement Geriatr Cogn Disord 38:375–388. https://doi.org/10.1159/000365548
doi: 10.1159/000365548
pubmed: 25195847
Nogami A, Yamazaki M, Saito Y, Hatsuta H, Sakiyama Y, Takao M et al (2015) Early stage of progressive supranuclear palsy: a neuropathological study of 324 consecutive autopsy cases. J Nippon Med Sch 82:266–273. https://doi.org/10.1272/jnms.82.266
doi: 10.1272/jnms.82.266
pubmed: 26823029
Respondek G, Grimm MJ, Piot I, Arzberger T, Compta Y, Englund E et al (2019) Validation of the movement disorder society criteria for the diagnosis of 4-repeat tauopathies. Mov Disord. https://doi.org/10.1002/mds.27872
doi: 10.1002/mds.27872
pubmed: 31571273
pmcid: 7993399
Respondek G, Stamelou M, Kurz C, Ferguson LW, Rajput A, Chiu WZ et al (2014) The phenotypic spectrum of progressive supranuclear palsy: a retrospective multicenter study of 100 definite cases. Mov Disord 29:1758–1766. https://doi.org/10.1002/mds.26054
doi: 10.1002/mds.26054
pubmed: 25370486
Robinson JL, Lee EB, Xie SX, Rennert L, Suh E, Bredenberg C et al (2018) Neurodegenerative disease concomitant proteinopathies are prevalent, age-related and APOE4-associated. Brain 141:2181–2193. https://doi.org/10.1093/brain/awy146
doi: 10.1093/brain/awy146
pubmed: 29878075
pmcid: 6022546
Rösler TW, Tayaranian Marvian A, Brendel M, Nykanen NP, Hollerhage M, Schwarz SC et al (2019) Four-repeat tauopathies. Prog Neurobiol 180:101644. https://doi.org/10.1016/j.pneurobio.2019.101644
doi: 10.1016/j.pneurobio.2019.101644
pubmed: 31238088
Saito Y, Ruberu NN, Sawabe M, Arai T, Tanaka N, Kakuta Y et al (2004) Staging of argyrophilic grains: an age-associated tauopathy. J Neuropathol Exp Neurol 63:911–918
doi: 10.1093/jnen/63.9.911
pubmed: 15453090
Sakae N, Josephs KA, Litvan I, Murray ME, Duara R, Uitti RJ et al (2019) Neuropathologic basis of frontotemporal dementia in progressive supranuclear palsy. Mov Disord 34:1655–1662. https://doi.org/10.1002/mds.27816
doi: 10.1002/mds.27816
pubmed: 31433871
pmcid: 6899964
Sakae N, Josephs KA, Litvan I, Murray ME, Duara R, Uitti RJ et al (2019) Neuropathologic basis of frontotemporal dementia in progressive supranuclear palsy. Mov Disord. https://doi.org/10.1002/mds.27816
doi: 10.1002/mds.27816
pubmed: 31433871
pmcid: 6899964
Sakai K, Yamada M (2011) Early-stage progressive supranuclear palsy with degenerative lesions confined to the subthalamic nucleus and substantia nigra. Neuropathology 31:77–81. https://doi.org/10.1111/j.1440-1789.2010.01134.x
doi: 10.1111/j.1440-1789.2010.01134.x
pubmed: 20573028
Schofield EC, Hodges JR, Bak TH, Xuereb JH, Halliday GM (2012) The relationship between clinical and pathological variables in Richardson's syndrome. J Neurol 259:482–490. https://doi.org/10.1007/s00415-011-6205-8
doi: 10.1007/s00415-011-6205-8
pubmed: 21837549
Schonhaut DR, McMillan CT, Spina S, Dickerson BC, Siderowf A, Devous MD Sr et al (2017) (18) F-flortaucipir tau positron emission tomography distinguishes established progressive supranuclear palsy from controls and Parkinson disease: A multicenter study. Ann Neurol 82:622–634. https://doi.org/10.1002/ana.25060
doi: 10.1002/ana.25060
pubmed: 28980714
pmcid: 5665658
Shoeibi A, Litvan I, Tolosa E, Ser TD, Lee E, Investigators T (2019) Progression of two progressive supranuclear palsy phenotypes with comparable initial disability. Parkinsonism Relat Disord 66:87–93. https://doi.org/10.1016/j.parkreldis.2019.07.010
doi: 10.1016/j.parkreldis.2019.07.010
pubmed: 31307919
Smith R, Scholl M, Honer M, Nilsson CF, Englund E, Hansson O (2017) Tau neuropathology correlates with FDG-PET, but not AV-1451-PET, in progressive supranuclear palsy. Acta Neuropathol 133:149–151. https://doi.org/10.1007/s00401-016-1650-1
doi: 10.1007/s00401-016-1650-1
pubmed: 27900460
Steele JC (2014) Historical perspectives and memories of progressive supranuclear palsy. Semin Neurol 34:121–128. https://doi.org/10.1055/s-0034-1381740
doi: 10.1055/s-0034-1381740
pubmed: 24963672
Toledo JB, Van Deerlin VM, Lee EB, Suh E, Baek Y, Robinson JL et al (2014) A platform for discovery: the University of Pennsylvania integrated neurodegenerative disease Biobank. Alzheimers Dement 10(477–484):e471. https://doi.org/10.1016/j.jalz.2013.06.003
doi: 10.1016/j.jalz.2013.06.003
Tsuboi Y, Josephs KA, Boeve BF, Litvan I, Caselli RJ, Caviness JN et al (2005) Increased tau burden in the cortices of progressive supranuclear palsy presenting with corticobasal syndrome. Mov Disord 20:982–988. https://doi.org/10.1002/mds.20478
doi: 10.1002/mds.20478
pubmed: 15834857
Walker Z, Gandolfo F, Orini S, Garibotto V, Agosta F, Arbizu J et al (2018) Clinical utility of FDG PET in Parkinson's disease and atypical parkinsonism associated with dementia. Eur J Nucl Med Mol Imaging 45:1534–1545. https://doi.org/10.1007/s00259-018-4031-2
doi: 10.1007/s00259-018-4031-2
pubmed: 29779045
pmcid: 6061481
Williams DR, de Silva R, Paviour DC, Pittman A, Watt HC, Kilford L et al (2005) Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson's syndrome and PSP-parkinsonism. Brain 128:1247–1258. https://doi.org/10.1093/brain/awh488
doi: 10.1093/brain/awh488
pubmed: 15788542
Williams DR, Holton JL, Strand C, Pittman A, de Silva R, Lees AJ et al (2007) Pathological tau burden and distribution distinguishes progressive supranuclear palsy-parkinsonism from Richardson's syndrome. Brain 130:1566–1576. https://doi.org/10.1093/brain/awm104
doi: 10.1093/brain/awm104
pubmed: 17525140
Yokoyama Y, Toyoshima Y, Shiga A, Tada M, Kitamura H, Hasegawa K et al (2016) Pathological and clinical spectrum of progressive supranuclear palsy: with special reference to astrocytic tau pathology. Brain Pathol 26:155–166. https://doi.org/10.1111/bpa.12265
doi: 10.1111/bpa.12265
pubmed: 25974705
Yoshida K, Hata Y, Kinoshita K, Takashima S, Tanaka K, Nishida N (2017) Incipient progressive supranuclear palsy is more common than expected and may comprise clinicopathological subtypes: a forensic autopsy series. Acta Neuropathol 133:809–823. https://doi.org/10.1007/s00401-016-1665-7
doi: 10.1007/s00401-016-1665-7
pubmed: 28064358