Tauopathies Alzheimer s disease Down s syndrome Dementia with only tangles (tangle only dementia) Pick s disease Progressive supranuclear palsy
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1 Tauopathies Prof. Isidro Ferrer, Institut Neuropatologia, Servei Anatomia Patològica, IDIBELL-Hospital Universitari de Bellvitge, Universitat de Barcelona, CIBERNED, Hospitalet de LLobregat; Spain
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3 Tauopathies Alzheimer s disease Down s syndrome Dementia with only tangles (tangle only dementia) Pick s disease Progressive supranuclear palsy Corticobasal degeneration Argyrophilic grain disease Frontotemporal lobar degeneration (and parkinsonism) due to mutations in MAPT (tau gene) Parkinson-dementia-ALS complex guamanian and non-guamanian Dementia pugilistica Myotonic dystrophy Rare tauopathies: tau panencephalopathy, AD-like with astrocytes, Niemann-Pick disease type C, certain prion diseases (GSS with tau), mutations in LRRK2, familial British dementia, Hallervorden-Spatz disease, postencephalitic parkinsonism Hyperphosphorylated tau in muscular diseases: sporadic Inclusion body myositis (sibm), myofibrillar myopathies (MFM)
4 Post-translational modifications of tau 1. O-Glycosylation: O-linked N-Acetylglucosamine (O-GlcNAc) 2. Phosphorylation: 2a.- Sites: about 79 putative sites, 30 described; most of them localized outside the microtubulebinding domains; most of them on the Ser-Pro and Thr-Pro motives. 2b.- Kinases: mitogen-activated protein kinase (MAPK) extracellular-regulated kinase (MAPK/ERK); glycogen synthase kinase (GSK3); tau-tubulin kinase; cyclin-dependent kinases cdk2 and cdk5; stress-activated protein kinases (SAPK/JNKs), stress-kinase of 38 kda (p38); microtubule-affinity regulating kinase (MARK): calcium/calmodulin-dependent protein kinase II (CaMPK II), cyclic- AMP-dependent kinase (PKA); and casein kinase II. 2c.- Phosphatases: Ser/Thr phosphatase proteins 1, 2A, 2B (calcineurin) and 2C.
5 0N 1N 2N 3R MBDs 2N 1N 0N 4R Exon 2 Exon 3 Exon 10 Tau isoforms expressed in the brain result from alternative splicing; 3Rtau contain 3 repeats, whereas 4Rtau contain four repeats. Big tau (about 120 kda) is expressed in the peripheral nervous system and muscle.
6 Pick disease Atrophy of the anterior temporal and frontal lobes, the orbital frontal lobe and the medial temporal lobes ( knife-edge atrophy). Severe degeneration in the hippocampus and amygdala. Degeneration in the corpus striatum, pallidum and substantia nigra may be detected. Neuron loss, vacuolation of the neuropil, astrocytic gliosis in the affected regions. Loss of dendritic spines and pre-synaptic markers. NF-P (+), tau (-) ballooned neurons (swollen chromatolytic neurons or Pick cells) in cerebral cortex. Pick bodies, NF-P (+), tau-p (+), in cerebral cortex (cingulate, insular, inferior temporal, inferior parietal and fusiform), hippocampal complex (pyramidal neurons of the hippocampus, granule cells of the dentate gyrus). tau-positive (ramified) inclusions in astrocytes. tau-positive coiled bodies and threads in oligodendrocytes.
7 Pick disease A B C Atrophy of the frontal and temporal lobes, and caudate (A). Pick bodies (arrow), silver stain (B) and electron microscopy (C). Pick bodies, antiphosphorylated tau antibodies (D) D
8 Pick disease A B C D E F G H I Pick bodies and tau-immunoreactive inclusions (AT8 antibody) in the hilus of the hippocampus (A), dentate gyrus (B), CA1 area (C), subiculum (D), entorhinal cortex (E), temporal cortex (F), amygdala (G), reticular nuclei of the brain stem (H)
9 Pick disease A B C D E F G H I Atypical Pick disease: Pick bodies, tau-immunoreactive astrocytes astrocytes (F) and coiled bodies (I) (E) a few of them reminiscent of tufted
10 Band pattern of phospho-tau as revealed by several anphospho-specific anti-tau antibodies. Bands of 64 and 60 kda PiD 64 KDa 60 KDa Thr 181 Ser 202 Ser 214 Ser 396 Ser 422 Ser 262 Tau kinases in sarkosyl insoluble fractions Tau-Thr 181 MAPK/ERK-P SAPK/JNK-P p38- P CAMKβ-II 64 KDa 60 KDa Immunoprecipitation (IP) of p38-p from Pick sarkosyl-insoluble fractions p38-p kinase assay of Pick IP. ATF-2 phosphorylation 38 kda 45 kda p38 P C C PiD PiD CT CT - ATF-2 +ATF-2 -ATF-2 +ATF-2 ATF-2 +ATF-2
11 Progressive supranuclear palsy (PSP) Neuron loss and astrocytosis are consistently found in the brainstem, cerebellum, pallidum, subthalamic nucleus and thalamus. Cortical involvement may be detected in patients who had suffered from cognitive decline. PSP subgroups: Cortical type Subcortical type tau (+) globose neurofibrillary tangles (NFTs) and neuropil threads in the basal ganglia, nucleus basalis of Meynert, brainstem and dentate nucleus. NFTs may be observed in small pyramidal neurons of the cerebral neocortex and pyramidal cells of the hippocampus (but distribution differs from that in AD). tau (+) inclusions in astrocytes: astrocytic tufts (star-like tufts), thorn-shaped inclusions. tau (+) oligodendrocytic inclusions: coiled bodies and threads.
12 Progressive supranuclear palsy (PSP) Neurofibrillary tangles and threads in locus ceruleus (lc) and cerebral cortex (cc) (A-D). Astrocytes and tufted astrocytes stained with anti-p-tau antibodies (right panel) P-tau-immunoreactive bands in the pons (p) and white matter (wm) in sarkosyl-insoluble fraction in PSP p tau Ser 214 p tau Ser kda 68 kda 66 kda 62 kda triplet at 37 kda 33 kda P WM P WM
13 Progressive supranuclear palsy A B C D E F G H Neuron loss in the globus pallidus (A), subthalamus (B) and substantia nigra (C); neurofibrillary tangle (arrow) in locus ceruleus (D). Hyperphosphorylated tau in the striatum (E, F), superior colliculus (G) and locus ceruleus (H). Positive astrocytes and oligodendrocytes (coiled bodies) are seen in addition to tau-immunorecative neurons.
14 Progressive supranuclear palsy A B C D E F G H Neuronal involvement in PSP (A-C). Entorhinal cortex (D); pons (E); locus ceruleus (F); lateral reticular formation (G); dentate nucleus (H)
15 Progressive supranuclear palsy A B C D E F G H Hyperphosphorylated-tau-immunoreactive inclusions in astrocytes (A-E) and oligodendrocytes: coiled bodies (F-H). C-E: tufted astrocytes
16 Progressive supranuclear palsy A B C D E F G H Expression of active tau-kinases in PSP. A-D: SAPK/JNK-P; E-G: p38-p; H: GSK-3β-P
17 PSP A B C D Early PSP, pre-clinical stage. A, B: caudate; C,: globus pallidus; D: subthalamus. A, GFAP; B-D: AT8
18 PSP A B C D Early PSP, pre-clinical stage. A: caudate; B: amygdala; C: CA1; D: DG
19 PSP A B C D E F G H I J PSP, intermediate stages. A: putamen; B: caudate; C: amygdala; D: CA1; E: dentate gyrus; F: Meynert nucleus; G: pons; H, midbrain (tufted astrocyte); I: locus ceruleus; J: gyrus cinguli
20 PSP A B C D E F G H I PSP; AT8. A: caudate; B: amygdala; C: pallidus; D: dorsomedial thalamus; E: subthalamus; F: superior colliculus; G: pons; H: frontal cortex; I: CA1 area of the hippocampus.
21 PSP CASE 1 CASE 2 CASE 3 CASE 4 CASE 5 p-tau Ser p-tau Thr p-tau Ser FC S P WM FC S P WM FC S P WM FC S P WM FC CP P WM
22 PSP CASE 1 CASE 2 CASE 3 CASE 4 CASE 5 p-tau Ser p-tau Ser FC S P WM FC S P WM FC S P WM FC S P WM FC S P WM Band patterns of phospho-tau, as seen with different phospho-specific anti-tau antibodies in the frontal cortex (FC), striatum (S), pons (P) and white matter (WM) in five PSP cases. Note the two bands of 68 and 64 kda practically in all cases and regions, and the different bands of lower molecular weight in the different regions and different cases.
23 A B C D Loss of neurons and spongiosis in the upper cortical layers (A) together with ballooned neurons filled willed with phosphorylated neurofilaments and αb-crystallin (C, D) can be seen in cortical type PSP. (B): locus ceruleus with neurofibrillary tangles (arrow)
24 Corticobasal degeneration (CBD) (Corticodentatonigral degeneration with neuronal achromasia, corticobasal ganglionic degeneration, corticonigral degeneration with neuronal achromasia). Cortical atrophy (frontal lobe > temporal lobe > parietal lobe), often asymmetrical. Moderate atrophy of the striatum. Degeneration in the substantia nigra. Neuron loss, vacuolation of the neuropil, astrocytic gliosis in the cerebral cortex, striatum, pallidum, dorsomedial nucleus of the thalamus, amygdala and substantia nigra. Mild gliosis in the dentate nucleus. Large numbers of NF-P (+), tau (-) huge ballooned neurons (achromatic neurons in Nissl stains) in cerebral cortex, also containing a B crystallin. tau (+) intraneuronal inclusions (pre-tangles), granular deposits, rarely neurofibrillary tangles. tau (+) neuropil threads. tau (+) astrocytic inclusions: astrocytic plaques; tau (+) astrocytic end-feet in subependymal, subpial and perivascular areas. tau (+) oligodendrocytic inclusions: coiled bodies and threads.
25 Corticobasal degeneration Atrophy of the cerebral cortex and enlargemenmt of the lateral ventricle. Swollen cortical neeurons (achromatic neurons), as seen with haematoxylin and eosin, are filled with phosphorylated neurofilaments Hyper-phosphorylated tau is found in neurons (horizontal arrowheads), globose neurons in the brain stem, and in astrocytic plaques (vertical arrowheads)
26 Corticobasal degeneration Ballooned neurons (arrows) contain phosphorylated neurofilaments
27 Corticobasal degeneration Ballooned neurons contain phosphorylated αb-crystallin A, B: frontal cortex; C, D: AD, amygdala. Ballooned neurons. A, C: αb-crystallin; B, D: phosphorylated αbcrystallin
28 Corticobasal degeneration A B C D A E F G H I Ballooned neurons contain αb-crystallin that co-localizes with hsp-27 (A-C) and phosphorylatyed neurofilaments (D- F). Negative controls (G-I)
29 Corticobasal degeneration A B C D E F G H I A: frontal cortex: espongiosis in the upper layers (left); B: balloooned neurons in the cortex stained with anti B- crystallin antibodies; C: frontal cortex; D: striatum; E: CA1 region of the hippocampus; F: Dentate gyrus; G: amygdala; H: substantia nigra; I: medial reticular nucleus, medulla oblongata. C-I: phospho-tau (AT8 antibody)
30 Corticobasal degeneration Astrocytic plaques in cerebral cortex
31 Corticobasal degeneration Frontotemporal atrophy. Band pattern of phospho-tau in PHF fractions reveals two bands of 68 and 64 kda
32 Corticobasal degeneration A B C D E F G H A, B: Ballooned neurons in the cerebral cortex, NF-P; αb-crystallin; C: frontal cortex; D: hippocampus; E: caudate; F, G: astrocytic plaques; H: coiled body in the white matter. C-H: AT8 antibody
33 Phospho-tau bands, as visualized with different phospho-specific anti-tau antibodies, in fractions enriched with abnormal aggregates of filaments in Alzheimer disease (AD), progressive supranuclear palsy (PSP), Pick disease (PiD) and corticobasal degeneration (CBD). AD is characterized by four bands of 73, 68, 64 and 60 kda; PSP and CBD by two bands of 68 and 64 kda, and PiD by two bands of about 64 and 60 kda
34 Rare tauopathies: Mixed tauopathy with incomplete PSP and CBD characteristics
35 Rare tauopathies: Mixed tauopathy with incomplete PSP and CBD characteristics A B C D E F G H Ballooned neurons in cerebral cortex (A and B: αb-crystallin). C-H: hyperphosphorylated tau in striatum (C), white matter (D), motor ocular nucleus (E), pons (F), ventral reticular (G), and lateral reticular (H).
36 Rare tauopathies: Multiple system tauopathy A B C D Tau-immunoreactive inclusions in neurons and glial cells as revealed with several phospho-specific anti-tau antibodies Ser422 (A), Ser202 (C), Ser396 (D) and with the phosphorylation-independent tau antibody 7.51 (B).
37 Argyrophilic grain disease Argyrophilic grains may be the only alteration in rare demented individuals, but they are also found in some cognitive normal subjects over age 65 years Association with AD stages I-IV of Braak, common. Argyrophilic grains may be found in Progressive supranuclear palsy, Corticobasal Degeneration, Pick disease, Diffuse lewy body disease, Multiple system atrophy, Parkinson disease and Motoneuron disease Neuropathology Dendritic-derived, irregulary shaped structures with filiform or knobby appendages (grains). Electron microscopy: 9-19 nm straight filaments or smooth tubules. Immunohistochemistry: phosphorylated tau tau-positive coiled bodies in oligodendrocytes in deep cortical layers and subcortical white matter.
38 AGD A AGD, Gallyas stain. Pretangles, tangles and grains (A, B). Ballooned neurons in amygdala; Gallyas-positive astrocytes (D); coiled bodies (oligodendrocytes) (E, F) B 4R tau CA1 (A), entorhinal cortex (B) Ballooned neurons in the amygdala contain phosphorylated neurofilaments and αb-crystallin (A-C), and are stained with antibodies to active tau kinases; MAPK/ERK, SAPK/JNK, p38, GSK-3β 73 KDa 68 KDa 64 KDa 60 KDa AD AGD Ser 262 Thr 181 Ser 202 Ser 214 Ser 396 Ser 422 AGD, bands of 68 and 64 kda of phospho-tau
39 AGD AGD AD Grains: Golgi method Band pattern of phospho-tau in PHF fractions in AD and AGD. Note in AGD the upper bands of the 68 and 64 kda and the lower bands which differ from those found in AD
40 AGD A B C D Argyrophilic grains in CA1 (A), entorhinal cortex (B), nucleus tuberalis (C), mammilllary bodies (D). AT8 antibody
41 AGD A B C D E F Argyrophilic grains in CA1 (A), subiculum (B), amygdala (C), Meynert nucleus (D), cingular cortex (E), locus ceruleus (F). AT8 antibody
42 AGD AGD. A: CA1; B:dentate gyrus; C: entorhinal cortex; D: amygdala; E: accumbens; F: septum; G: putamen; H: substantia nigra; I: white matter; J: CA1 tau4r; K: EC tau4r; I: amyg, αb-crystallin
43 AGD AGD. A-C: αb-crystallin in ballooned neurons in amygdala; D-F: phosphorylated αb-crystallin in ballooned neurons in amygdala; G: αb-crystallin in reactive astrocytes in the temporal white matter (these cells do not contain phosphorylated B-crystallinB; H: α B-crystallin in cortical oligodendroglia; I: phosphorylated αbcrystallin is absent in cortical oligodendroglia.
44 Dementia with only tangles A B C D E F G H Hyper-phosphorylated tau (AT8 antibody. A: entorhinal cortex; B: CA1 area of the hippocampus; C: putamen; D: Meynert nucleus; E: superior colliculus; F: locus ceruleus; G: motor ocular III; H: lateral reticular nucleus of the brain stem
45 Frontotemporal lobar degeneration (dementia) with mutations in the tau gene: familial tauopathies (FTLD-tau) N279K N296N R5H R5L L266V K257T G372V ΔN296 N296H S305S S305N 10 Intronic mutations S320F V337M S352L G389R R406W 1 9 L284L P301L P301S K369I L315R E342V I260V Splicing Pick-like Tangle predominant Other patterns
46 Mechanisms of MAPT mutations 1. Splicing mutations: Alterations in the 3R:4R ratio a. In intron following exon 10 b. In exon 10 i. Pure (silent) L284L, S305S, N296N ii. Mixed splicing and structural ΔN296, N296H, N279K, S305N 2. Mutations affecting the structure of the tau protein a. In exon 10 P301L, P301S b. In exons 1, 9, 11, 12, or 13 i. With neurofibrillary tangles: V337M, R406W ii. With Pick bodies: K257, L266V, G272V, L315R, S320F, 336R, E342V, K369I, G389R iii. With other patterns R5H, R5L, I260V, S352L11
47 FTLD-tau P301L A B C D Frontotemporal atrophy. Loss of neurons and spongiosis in the upper layers (A) with occasional ballooned neurons (B) in the cerebral cortex (CC). Inclusions are also seen in the dentate gyrus (arrow, DG, C) Hyperphosphorylated tau deposits in neurons and glial cells
48 FTLD-tau P301L Intraneuronal inclusions are stained with phospho-specific anti-tau antibodies (214, 396), and with antibodies directed against active forms of tau-kinases JNK, p38 and GSK-3
49 FTLD-tau P301L Two different cases. Left pannel: intraneuronal inclusions as revealed with different phospho-specific anti-tau antibodies, tubulin (tub) and ubiquitin (ubi). Right pannel; different regions: cc: cerebral cortex; EC: entorhinal cortex; CA1 area of the hippocampus; Str: striatum; DG: dentate gyrus; Mey: Meynert nucleus; As: astrocytes; WM: coiled bodies in the white matter
50 FTLD deln296 A B C D E F Widespread neuronal and glial hyperphosphorylated tau deposits Frontotemporal atrophy, atrophy of the mesencephalon and pons
51 FTLD deln296 Tangles Astrocytes Coiled bodies Thr Ser Ser Ser Ser MAPK/ERK-P SAPK/JNK-P P38-P GSK-3β-P tau-kinases associated with tau phosphorylation in FTLD del296: MAPK-ERK-P; SAPK-JNK-P; p38-p; GSK-3β-P
52 FTLD K317M A B C Frontotemporal atrophy D E F Marked spongiosis in the upper layers of the cerebral cortex (A). Widespread neuronal and glial hyperphorylated tau-immunoreactive deposits (B-F). Tufted astrocytes, fibrous astrocytes, globose oligodendoglial inclusions and coiled bodies are common.
53 FTLD K317M Generalized neuronal and glial hyperphosphorylated tau deposits in the cerebral cortex (cc), thalamus (thal), striatum (str), mammillary bodies (mam) and cerebral white matter (wm). Deposits in astrocytes are reminiscent of tufted astrocytes and fibrous astrocytes, and inclusions in oligodendrocytes are globose or coiled.
54 Identification of phospho-tau-immunoreactive bands in sarkosyl-insoluble fractions in FTDP P-tau Ser Case Region FC FC Hip FC Tau mutation P301L P301L R406W Phospho-tau bands in P301L mutation differ from those in R406W mutation
55 Myotonic dystrophy A B C D E F G H I A: parietal cortex; B: temporal cortex; C: cingulate cortex; D: insula; E: CA1; F: mammillary body; G: locus ceruleus; H, I: entorhinal cortex. A-G: AT8; H: 3Rtau; I: 4Rtau
56 Myotonic dystrophy A B C D tau deposits in the entorhinal cortex, A, B: AT8; C: 3R tau; D: 4Rtau
57 Myotonic dystrophy 50 kda 50 kda 50 kda 37 kda 37 kda 37 kda 25 kda 25 kda 25 kda AD MD1 MD2 MD3 AD MD1 MD2 MD3 AD AD AD MD1 MD2 MD3 Band pattern of 3R (left) 4R (middle) and phosphorylated tau (Ser214) (right) in fractions enriched in filaments in three cases of myotonic dystrophy (MD1, MD2, MD3) compared with Alzheimer disease (AD). AD is characterized by three bands of 68, 64 and 60 kda, whereas myotonic dystrophy shows bands of 50 kda and lower which are not found in any other tauopathy.
58 Prion diseases PRNP P102L-129V PRNP P102L-129V. Cerebral cortex; b: cerebellum, HE; C: cerebellum, PAS; D, E: PrP cortex; F: striatum; G: thalamus; H: cerebellum; I: spinal cord
59 Prion diseases PRNP P102L-129V PRNP P102L-129V. A: PrP; B: GFAP; C: CD68; D: αb-crystallin; E: AT8; F: AT8; G: tau3r; H: tau4r; I: ubiquitin
60 Prion diseases PRNP P102L-129V PRNP P102L-129V. Confocal microscopy PrP deposition (left column, green), phospho-tau (Thr181) (mid column, red), merge (right column). Hyperphosphorylated tau is accumulkated in cell processes surrrounding PrP deposits.
61 Prion diseases 75 kda 75 kda 75 kda 50 kda 50 kda 50 kda 37 kda 37 kda 37 kda 25 kda 25 kda 25 kda AD AD AD GSS1 GSS2 AD AD AD GSS1 GSS2 AD AD AD GSS 1 GSS2 Band pattern of 3Rtau (left), 4Rtau (middle) and phospho-tau (Ser214; right) in PHF fractions in two cases of Gerstmann- Straüssler-Scheinker (GSS) syndrome and in Alzheimer disease (AD) GSS1: PRNP Y218N 129V GSS2: PRNP P102L-129V
62 Myofibrillar myopathies(mfm): myotilinopathies and desminopathies sarcolemma integrins MLP myotilin Filamin C actin zyxin α-actinin telethonin calsarcin titin CapZ ZASP MLP nebulin αb-crystallin myopalladin desmin mink Myotilinopaty Z-line Z-line Thick filaments Thin filaments I band A band I band Desminopathy
63 sibm and MFM sibm. Positive fibers immunoreactive for A: 4Rtau; B: 3Rtau; C: P-tau Thr 181; D: Alz50; E: AT8; F: P-tau Ser422; G: AKT-P; H: MAPK/ERK-P; I: SAPK/JNK-P; J: p38-p; K: GSK-3βTyr; L: GSK-3βSer9; : J: p38-p; K: GSK-3βTyr; L: GSK-3βSer9
64 sibm and MFM Myotilinopathy. Positive fibers immunoreactive for A: 3Rtau; B: 4Rtau; C: P-tau Thr181; D: Alz50; E: P-tau Ser422; F: AT8; G: 3Rtau; H: P-tau Ser396; I: P-tau-Thr181.
65 sibm and MFM Myotilinopathy. Positive fibers immunoreactive for A: AKT-P: B: MAPK/ERK-P; C: SAPK/JNK-P; D: p38-p; E: GSK-3βTyr; F: GSK-3βSer9
66 sibm and MFM Desminopathy. Positive fibers immunoreactive fo A: 3Rtau; B: 4Rtau; C: Alz50; D. P-tau Thr181; E: P-tau Ser 422; F: P-tau-Ser 396; G: SAPK/JNK-P; H: p38-p; I: GSK-3βSer9
67 sibm and MFM. Big tau (about 120 kda) and GSK-3α/β levels. Myoblastic C2C12 line used as a control
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