Argyrophilic grain disease
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1 Argyrophilic grain disease Prof. Isidro Ferrer, Institut Neuropatologia, Servei Anatomia Patològica, IDIELLHospital Universitari de ellvitge, Universitat de arcelona, IERNED, Hospitalet de LLobregat; Spain
2 AGD at first: a neuropathological finding in some patients with dementia A D E F Argyrophilic grains (AGs) Neurons with pretangles Astrocytes with argyrophilia oiled bodies in oligodendrocytes allooned neurons in amygdala AGD: Gallyas
3 AGs and pretangles are recognized with several phosphospecific antitau antibodies
4 ARGYROPHILI GRAIN DISEASE: DEMENTIA WITH GRAINS Delineation of a process versus definition of a disease raak H. raak E. Argyrophilic grains haracteristic pathology of cerebral cortex in cases of adult onset dementia without Alzheimer changes. Neurosci Lett 1987; raak H. raak E. ortical and subcortical argyrophilic grains characterize A disease associated withadult onset dementia. Neuropathol Appl Neurobiol 1989;15:1326 Ikeda K, Akiyama H. Kondo H. Haga. A study of dementia with argyrophilic grains. Possible cytoskeletal abnormality in dendrospinal portion of neurons and oligodendrocytes. Acta Neuropathol 1995;89: Tolnay M, Spillantini MG, Goedert M, Ulrich J, angui D, Probst A. Argyrophilic Grain disease: Widespread hyperphosphorylation of tau protein in limbic neurons. Acta Neuropathol 1997;93: Tolnay M, Probst A. allooned neurons expressing alpha crystallin as a constant feature of the amygdala in argyrophilic grain disease. Neurosci Lett 1998;246: AGD: A novel tauopathy Togo T, Sahara N, Yen SH, ookson N, Ishizara T, Hutton M, de Silva R, Lees A, Dickson DW. Argyrophilic grain disease is a sporadic 4repeat tauopaty. J Neuropathol Exp Neurol 2002;61: Tolnay M, Sergeant N, Ghestem A, halbot S, de Vos RAI, Jansen Steur ENH, Probst A, Delacourte A. Argyrophilic grain disease and Alzheimer s disease are distinguished by their different distribution of tau protein isoforms. Acta Neuropathol 2002;104: Ferrer I, arrachina M, Tolnay M, Rey MJ, Vidal N, armona M, lanco R, Puig. Phosphorylated protein kinases associated with neuronal and glial tau deposits in argyrophilic grain disease. rain Pathol 2003;13:6278. Molecular pathology of AGD Ferrer I, Santpere G, van Leeuwen FW. Argyrophilic grain disease. rain 2008; 131:
5 A D E F Grains: Golgi method
6 A D AGD. A: A1, AT8; : laterotuberal, AT8; : A1, 4R; D: entorhinal cortex, 4R
7 A D E F G H I J K L AGD. A: A1; : dentate gyrus; : entorhinal cortex; D: amygdala; E: accumbens; F: septum; G: putamen; H: substantia nigra; I: white matter; J: A1 tau4r; K: E tau4r; I: amyg, αcrystallin
8 A D AGD cortical. A: A1; : amygdala; : entorhinal cortex; D: frontal cortex
9 Argyrophilic grain (AG) staging Stage I: anterior entorhinal cortex; mild involvement of the cortical and basolateral nuclei of the amygdala; mild involvement of the hypothalamic lateral tuberal nucleus. Stage II: entorhinal cortex; anterior A1; transentorhinal cortex; cortical and basolateral nuclei of the amygdala; presubiculum; hypothalamic lateral tuberal nucleus; dentate gyrus. Stage III: entorhinal cortex; A1; perirhinal cortex; presubiculum; amygdala; dentate gyrus; hypothalamic lateral tuberal nucleus; mild involvement of A2 and A3; mild involvement of the subiculum; mild involvement of other nuclei of the hypothalamus (i.e. mammillary bodies); mild involvement of the anterior temporal cortex, insular cortex, anterior cingulated gyrus, orbitofrontal cortex, nucleus accumbens, septal nuclei; rare grains in the midbrain. Stage IV: moderate to severe additional involvement of the neocortex and brainstem
10 linical symptoms ognitive decline and dementia ehavioural abnormalities, personality changes and emotional and mood imbalance Episodic memory loss Amnesia, irritability and agitation, followed by delusions, dysphoria and apathy Mild amnestic cognitive impairment is not uncommon as an initial manifestation of AGD A small number of patients present with progressive transcortical sensory aphasia, prominent abnormal behaviour and aggression, and moderate to severe cognitive impairment consistent with frontotemporal dementia The presence of AGD plus mildmoderate ADtype pathology is, probably, the cause of dementia and not just the presence of AGD. The age of onset is around 70 years old. The duration of the disease is between 4 and 8 years
11 ARGYROPHILI GRAIN DISEASE: DEMENTIA WITH GRAINS Genetics The disease appears to be sporadic Not known genetic factors, but for a single hereditary case: Kovacs GG, Pittman A, Revesz T, Luk, Lees A, Kiss E, Tariska P, Laszlo L, Molnár K, Molnar MJ, Tolnay M, de Silva R. MAPT S305I mutation: implications for agryrophilic grain disease. Acta Neuropathol 116: (2008) The frequency of apolipoprotein E ε4 (ApoE ε4) allele in AGD is similar to that of the general population. Yet the frequency of ApoE ε2 is higher than that observed in AD and controls Association of AGD with tau H1 haplotype is confusing, with both positive and negative results (Togo et al., 2002; Miserez et al., 2003).
12 ARGYROPHILI GRAIN DISEASE: DEMENTIA WITH GRAINS Association of AGD with Alzheimer disease, progressive supranuclear palsy, orticobasal degeneration and αsynucleinopathies MartinezLage P, Muñoz DG. Prevalence and disease associations of argyrophilic grains of raak. J Neuropathol Exp Neurol 1997;56: raak H, raak E. Argyrophylic grain disease: Frequency of occurrence in different age categories and neuropthological diagnostic criteria. J Neural Transm 1998;105: Ikeda K, Akiyama H, Arai T, Matsushita M, Tsuchiya K, Miyazaki H. linical aspects of argyrophilic grain disease. lin Neuropathol 2000;19: Tolnay M, Monsch AU, Probst A. Argyrophilic grain disease. A frequent dementing disorder in old patients. Adv Exp Med iol 2001;487:3958 Togo T, ookson N, Dickson DW. Argyrophilic grain disease: Neuropathology, frequency in a dementia brain bank and lack of relationship with apolipoprotein E. rain Pathol 2002;12:4552
13 A D E F G H I AGD+PSP. A: s. nigra; : nucleus of the vagus nerve; : reticular formation; D: A1; E: subiculum; F: entorhinal cortex; G: dentate gyrus; H: dentate gyrus; I: amygdala
14 A D E F G H I AGD+PSP. A: septum; : accumbens; : caudate; D: medial putamen; E: mammillary bodies; F: basal forebrain; G: frontal cortex; I: amygdala (tufted)
15 A D AGD+ astrocytic plaques: A: A1; : entorhinal cortex; : amygdala; D: temporal cortex
16 ARGYROPHILI GRAIN DISEASE: DEMENTIA WITH GRAINS AGD and neurotransmitters Practically nothing known, excepting Yamada T, McGeer PL, McGeer EG. Some immunohistochemical features of argyrophilic grain dementia with normal cortical choline acetyltransferase levels but extensive subcortical pathology and markedly reduced dopamine. J Geriatr Psychiatry Neurol 5: 313 (1992) Perezuira S, arrachina M, Rodriguez A, Albasanz JL, Martin M, Ferrer I. Expression levels of adenosine receptors in hippocampus and frontal cortex in argyrophilic grain disease. Neurosci Lett 423: (2007)
17 Adenosine receptors in the frontal cortex and hippocampus in AGD A Frontal ortex AGD A1R (37 KDa) A Frontal ortex AGD AI (120 KDa) βactin (45 KDa) βactin (45 KDa) A1R protein levels (AU) 2,5 1,5 0,5 AI protein levels (AU) 2,5 1,5 0,5 AGD AGD Hippocampus AGD A1R (37 KDa) Hippocampus AGD AI (120 KDa) βactin (45 KDa) βactin (45 KDa) 2,5 * A1R protein levels (AU) 1,8 1,4 1,0 0,6 0,2 * AI protein levels (AU) 1,5 0,5 AGD AGD
18 AGD is a tauopathy with tau phosphorylated at different threonine and serine sites A D E F G H I antitau phosphospecific antibodies Thr181 (A), Ser214 (), Ser396 (), Ser199 (D), Ser231 (E), Ser422 (F), Ser202 (G) and Ser262 (H), and antibody 7.51 (I)
19 AGD is a 4R tauopathy tau 7.51 Thr 181 Ser 262 Ser SIF Total SIF Total SIF Total SIF Total 4R immunohistochemistry
20 Several taukinases are localized in neurons with pretangles and in grains A Active stress kinases: SAPK/JNKP and p38p, and GSK3β
21 taukinases colocalize with taup in neurons with pretangles and in grains
22 Tau 422 MEK1 ERK2 JNK1 amkii SIF Total SIF Total SIF Total SIF Total SIF Total GSK3α/β MAPK/ERKP SAPKJNKP p38p GSK3βP SIF Total SIF Total SIF Total SIF Total SIF Total Tau kinases in sarkosyl insoluble fractions and in total homogenates in AGD
23 Tau kinases and phosphotau are also present in ballooned neurons in the entorhinal cortex and amygdala NF tau SAPK/JNKP + tau SAPK/JNKP + tau p38p + tau αcrystallin, phosphorylated neurofilaments, phosphotau and taukinases in ballooned neurons in the amygdala
24 GSK3βP p P38P p SAPK/JNKP d + + MAPK/ERKP GSK3β JNK1 ERK MEK d Ser p Ser396 + ± ++ d Ser p Ser p Thr181 oiled bodies Astrocyt allooned neuron Tangles Pretangles Grain
25 αcrystallin is phosphorylated in ballooned neurons
26 Specific tau truncated forms are usually encountered in AGD and they differ from those seen in AD AGD AGD AD
27 Thrombin is a strong candidate as a causative protease of truncated tau A A D E F G H I thrombin calpain 2 caspase 3
28 The ubiquitinproteasome system (UPS) in AGD A p62 D ubiquitin
29 Ubiquitin colocalizes with tau in AGs A D E F Ubiquitin + AT8
30 Human AGDUbiquitin marker ctls AGDpat. band N; density type of sample ctl AGDpatol Human AGDUbiquitin 40 lot Ab: antiubi density p< p<0.005 * * ctl AGD 20 0 band1 band2 band3 band4 type of sample Increased ubiquitination in selected protein bands in AGD hippocampus
31 A D E Mutant ubiquitin
32 A TL AGD TL AGD AntiML TL AGD A K 20 lot Ab: AntiDNP 20 lot Ab: AntiEL 0 GSA AASA 30 ontrol TL * AGD F R S L H O G Q E 20 lot Ab: AntiML 20 lot Ab: AntiMDAL TL 25 0 EL ML MDAL 30 AGD density adjusted to actin * DNP EL ML MDAL * AGD Increased expression of oxidative damage as revealed with different markers Oxidative stress and oxidative damage in AGD
33 Oxidative stress responses in AGD RAGE: receptor of advanced glycation end products A D A, : control, D: AGD
34 Oxidative stress responses in AGD Superoxide dismutase 1 and 2: SOD1 and SOD2 A D A SOD1: A, : control;, D: AGD. A, : A1;, D: E SOD2: A: control, : AGD. A1
35 Mitochondrial respiratory complexes and AIF in AGD hippocampus A TL AGD 30 TL AGD lot Ab: AntiNDUFS3 lot Ab: AntiSDHA lot Ab: AntiUQR2 density adjusted to porin 1,4 1,2 1 0,8 0,6 0,4 0,2 * * ** 36 lot Ab: AntiMTO1 0 NDUFS3 SDHA UQR2 MTO1 UP4 AIF lot Ab: AntiUP4 57 lot Ab: AntiAIF 31 lot Ab: AntiPorin 48 Decreased expression of proteins of mitochondrial complexes, and increased AIF lot Ab: AntiβActin Actin
36 taup+ mitochondrial porin. No porin localization in grains
37 Increased expression of endoplasmic reticulum stress markers in AGD hippocampus A TL AGD TL AGD 36 lot Ab: AntipEif2α lot Ab: AntiGRP 78 lot Ab: AntiEif2α lot Ab: AntiIRE1 lot Ab: AntiGRP lot Ab: AntiATF6 lot Ab: AntiATF6 cleaved lot Ab: AntiPDI lot Ab: AntiKDEL lot Ab: AntiXP1 lot Ab: AntiβActin Actin 48 lot Ab: AntiβActin Actin
38 aging mitochondrial anomalies oxidative stress oxidative responses RAGE SOD1 SOD2 activation of stress kinases SAPK/JNK and p38 tau4r tau hyperphosphorylation activation of other kinases: i.e. GSK3β p62 hyperphosphorylated tau aggregation ubiquitin AGs tau ubiquination pretangles mrna misreading: U +1 tangles truncated tau Endoplasmic reticulum stress tau/u +1 trombin in AGs and tangles Abnormal protein folding impaired UPS function AGs tangles tau Sequestration of active stress kinases and GSK3β
39
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