Hoozemans JJM, Van Haastert ES, Nijholt DAT, Rozemuller AJM, Eikelenboom P, Scheper W. The unfolded protein response is activated in pretangle neurons in Alzheimer’s disease hippocampus. Am J Pathol. 2009;174:1241–51. https://doi.org/10.2353/ajpath.2009.080814.
Article
CAS
Google Scholar
Köhler C. Granulovacuolar degeneration: a neurodegenerative change that accompanies tau pathology. Acta Neuropathol. 2016;132:339–59. https://doi.org/10.1007/s00401-016-1562-0.
Article
CAS
Google Scholar
Nijholt DAT, Van Haastert ES, Rozemuller AJM, Scheper W, Hoozemans JJM. The unfolded protein response is associated with early tau pathology in the hippocampus of tauopathies. J Pathol. 2012;226:693–702. https://doi.org/10.1002/PATH.3969.
Article
CAS
Google Scholar
Yamazaki Y, Matsubara T, Takahashi T, Kurashige T, Dohi E, Hiji M, et al. Granulovacuolar degenerations appear in relation to hippocampal phosphorylated tau accumulation in various neurodegenerative disorders. PLoS One. 2011;6. https://doi.org/10.1371/journal.pone.0026996.
Ball MJ. Topographic distribution of neurofibrillary tangles and granulovacuolar degeneration in hippocampal cortex of aging and demented patients. A quantitative study. Acta Neuropathol. 1978:73–80. https://doi.org/10.1007/BF00690970.
Ball MJ, Lo P. Granulovacuolar degeneration in the ageing brain and in dementia. J Neuropathol Exp Neurol. 1977;36:474–87.
Xu M, Shibayama H, Kobayashi H, Yamada K, Ishihara R, Zhao P, et al. Granulovacuolar degeneration in the hippocampal cortex of aging and demented patients - a quantitative study. Acta Neuropathol. 1992;85:1–9. https://doi.org/10.1007/BF00304627.
Article
CAS
Google Scholar
Nasreddine ZS, Loginov M, Clark LN, Lamarche J, Miller BL, Lamontagne A, et al. From genotype to phenotype: a clinical, pathological, and biochemical investigation of frontotemporal dementia and parkinsonism (FTDP-17) caused by the P301L tau mutation. Ann Neurol. 1999;45:704–15. https://doi.org/10.1002/1531-8249(199906)45:6<704::AID-ANA4>3.0.CO;2-X.
Wiersma VI, van Ziel AM, Vazquez-Sanchez S, Nölle A, Berenjeno-Correa E, Bonaterra-Pastra A, et al. Granulovacuolar degeneration bodies are neuron-selective lysosomal structures induced by intracellular tau pathology. Acta Neuropathol. 2019;138:943–70.
Wiersma VI, Hoozemans JJM, Scheper W. Untangling the origin and function of granulovacuolar degeneration bodies in neurodegenerative proteinopathies. Acta Neuropathol Commun. 2020;8:1–21. https://doi.org/10.1186/s40478-020-00996-5.
Article
Google Scholar
Thal DR, Del Tredici K, Ludolph AC, Hoozemans JJM, Rozemuller AJ, Braak H, et al. Stages of granulovacuolar degeneration: their relation to Alzheimer’s disease and chronic stress response. Acta Neuropathol. 2011;122:577–89. https://doi.org/10.1007/s00401-011-0871-6.
Article
CAS
Google Scholar
Puladi B, Dinekov M, Arzberger T, Taubert M, Köhler C. The relation between tau pathology and granulovacuolar degeneration of neurons. Neurobiol Dis. 2021;147:105138. https://doi.org/10.1016/j.nbd.2020.105138.
Article
CAS
Google Scholar
Aubry S, Shin W, Crary JF, Lefort R, Qureshi YH, Lefebvre C, et al. Assembly and interrogation of Alzheimer’s disease genetic networks reveal novel regulators of progression. PLoS One. 2015;10:1–25. https://doi.org/10.1371/journal.pone.0120352.
Article
CAS
Google Scholar
Stadelmann C, Deckwerth TL, Srinivasan A, Bancher C, Brück W, Jellinger K, et al. Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer’s disease: evidence for apoptotic cell death. Am J Pathol. 1999;155:1459–66. https://doi.org/10.1016/S0002-9440(10)65460-0.
Article
CAS
Google Scholar
Unterberger U, Höftberger R, Gelpi E, Flicker H, Budka H, Voigtländer T. Endoplasmic reticulum stress features are prominent in Alzheimer disease but not in prion diseases in vivo. J Neuropathol Exp Neurol. 2006;65:348–57. https://doi.org/10.1097/01.JNEN.0000218445.30535.6F.
Article
CAS
Google Scholar
Lund H, Gustafsson E, Svensson A, Nilsson M, Berg M, Sunnemark D, et al. MARK4 and MARK3 associate with early tau phosphorylation in Alzheimer’s disease granulovacuolar degeneration bodies. Acta Neuropathol Commun. 2014;2:1–15. https://doi.org/10.1186/2051-5960-2-22.
Article
Google Scholar
Midani-Kurçak JS, Dinekov M, Puladi B, Arzberger T, Köhler C. Effect of tau-pathology on charged multivesicular body protein 2b (CHMP2B). Brain Res. 2019;1706:224–36. https://doi.org/10.1016/J.BRAINRES.2018.11.008.
Article
Google Scholar
Köhler C, Dinekov M, Götz J. Granulovacuolar degeneration and unfolded protein response in mouse models of tauopathy and Aβ amyloidosis. Neurobiol Dis. 2014:169–79. https://doi.org/10.1016/j.nbd.2014.07.006.
Andrés-Benito P, Carmona M, Pirla MJ, Torrejón-Escribano B, del Rio JA, Ferrer I. Dysregulated protein phosphorylation as main contributor of granulovacuolar degeneration at the first stages of neurofibrillary tangles pathology. Neuroscience. 2021. https://doi.org/10.1016/j.neuroscience.2021.10.023.
Barranco N, Plá V, Alcolea D, Sánchez-Domínguez I, Fischer-Colbrie R, Ferrer I, et al. Dense core vesicle markers in CSF and cortical tissues of patients with Alzheimer’s disease. Transl Neurodegener. 2021;10:1–15. https://doi.org/10.1186/S40035-021-00263-0/FIGURES/7.
Article
Google Scholar
Hou X, Watzlawik JO, Cook C, Liu CC, Kang SS, Lin WL, et al. Mitophagy alterations in Alzheimer’s disease are associated with granulovacuolar degeneration and early tau pathology. Alzheimer’s Dement. 2021;17:417–30. https://doi.org/10.1002/ALZ.12198.
Article
CAS
Google Scholar
Koper MJ, Van Schoor E, Ospitalieri S, Vandenberghe R, Vandenbulcke M, von Arnim CAF, et al. Necrosome complex detected in granulovacuolar degeneration is associated with neuronal loss in Alzheimer’s disease. Acta Neuropathol. 2020;139:463–84. https://doi.org/10.1007/s00401-019-02103-y.
Article
CAS
Google Scholar
Nishikawa T, Takahashi T, Nakamori M, Hosomi N, Maruyama H, Miyazaki Y, et al. The identification of raft-derived tau-associated vesicles that are incorporated into immature tangles and paired helical filaments. Neuropathol Appl Neurobiol. 2016;42:639–53. https://doi.org/10.1111/NAN.12288.
Article
CAS
Google Scholar
Siedlak SL, Jiang Y, Huntley ML, Wang L, Gao J, Xie F, et al. TMEM230 accumulation in granulovacuolar degeneration bodies and dystrophic neurites of Alzheimer’s disease. J Alzheimer’s Dis. 2017;58:1027–33.
Stutzbach LD, Xie SX, Naj AC, Albin R, Gilman S, Lee VMY, et al. The unfolded protein response is activated in disease-affected brain regions in progressive supranuclear palsy and Alzheimer’s disease. Acta Neuropathol Commun. 2013;2:1–13. https://doi.org/10.1186/2051-5960-1-31/COMMENTS.
Article
Google Scholar
Heman-Ackah SM, Manzano R, Hoozemans JJM, Scheper W, Flynn R, Haerty W, et al. Alpha-synuclein induces the unfolded protein response in Parkinson’s disease SNCA triplication iPSC-derived neurons. Hum Mol Genet. 2017;26:4441–50. https://doi.org/10.1093/hmg/ddx331.
Article
CAS
Google Scholar
Hoozemans JJM, van Haastert ES, Eikelenboom P, de Vos RAI, Rozemuller JM, Scheper W. Activation of the unfolded protein response in Parkinson’s disease. Biochem Biophys Res Commun. 2007;354:707–11. https://doi.org/10.1016/j.bbrc.2007.01.043.
Article
CAS
Google Scholar
Hou X, Fiesel FC, Truban D, Castanedes Casey M, Lin WL, Soto AI, et al. Age- and disease-dependent increase of the mitophagy marker phospho-ubiquitin in normal aging and Lewy body disease. Autophagy. 2018;14:1404–18. https://doi.org/10.1080/15548627.2018.1461294.
Article
CAS
Google Scholar
Mamais A, Manzoni C, Nazish I, Arber C, Sonustun B, Wray S, et al. Analysis of macroautophagy related proteins in G2019S LRRK2 Parkinson’s disease brains with Lewy body pathology. Brain Res. 2018;1701:75–84. https://doi.org/10.1016/j.brainres.2018.07.023.
Article
CAS
Google Scholar
Nagamine S, Yamazaki T, Makioka K, Fujita Y, Ikeda M, Takatama M, et al. Hypersialylation is a common feature of neurofibrillary tangles and granulovacuolar degenerations in Alzheimer’s disease and tauopathy brains. Neuropathology. 2016;36:333–45. https://doi.org/10.1111/neup.12277.
Article
CAS
Google Scholar
Mizutani T, Innose T, Nakajima S, Kakimi S, Uchigata M, Ikeda K, et al. Familial parkinsonism and dementia with ballooned neurons, argyrophilic neuronal inclusions, atypical neurofibrillary tangles, tau-negative astrocytic fibrillary tangles, and Lewy bodies. Acta Neuropathol. 1998;95:15–27.
Article
CAS
Google Scholar
Makioka K, Yamazaki T, Fujita Y, Takatama M, Nakazato Y, Okamoto K. Involvement of endoplasmic reticulum stress defined by activated unfolded protein response in multiple system atrophy. J Neurol Sci. 2010;297:60–5. https://doi.org/10.1016/j.jns.2010.06.019.
Article
CAS
Google Scholar
Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, Gage FH, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science (80- ). 1996;272:263–7.
Article
CAS
Google Scholar
Li X, Koudstaal W, Fletcher L, Costa M, van Winsen M, Siregar B, et al. Naturally occurring antibodies isolated from PD patients inhibit synuclein seeding in vitro and recognize Lewy pathology. Acta Neuropathol. 2019;137:825–36. https://doi.org/10.1007/s00401-019-01974-5.
Article
CAS
Google Scholar
Chen JJ, Nathaniel DL, Raghavan P, Nelson M, Tian R, Tse E, et al. Compromised function of the ESCRT pathway promotes endolysosomal escape of tau seeds and propagation of tau aggregation. J Biol Chem. 2019;294:18952–66. https://doi.org/10.1074/jbc.RA119.009432.
Article
CAS
Google Scholar
Flavin WP, Bousset L, Green ZC, Chu Y, Skarpathiotis S, Chaney MJ, et al. Endocytic vesicle rupture is a conserved mechanism of cellular invasion by amyloid proteins. Acta Neuropathol. 2017;134:629–53. https://doi.org/10.1007/s00401-017-1722-x.
Article
CAS
Google Scholar
Jia J, Claude-Taupin A, Gu Y, Choi SW, Peters R, Bissa B, et al. Galectin-3 coordinates a cellular system for lysosomal repair and removal. Dev Cell. 2020;52:69–87.e8. https://doi.org/10.1016/j.devcel.2019.10.025.
Article
CAS
Google Scholar
Papadopoulos C, Kirchner P, Bug M, Grum D, Koerver L, Schulze N, et al. VCP /p97 cooperates with YOD 1, UBXD 1 and PLAA to drive clearance of ruptured lysosomes by autophagy. EMBO J. 2017;36:135–50. https://doi.org/10.15252/embj.201695148.
Article
CAS
Google Scholar
Strang KH, Croft CL, Sorrentino ZA, Chakrabarty P, Golde TE, Giasson BI. Distinct differences in prion-like seeding and aggregation between Tau protein variants provide mechanistic insights into tauopathies. J Biol Chem. 2018;293:2408–21. https://doi.org/10.1074/jbc.M117.815357.
Article
CAS
Google Scholar
Koller EJ, Gonzalez De La Cruz E, MacHula T, Ibanez KR, Lin WL, Williams T, et al. Combining P301L and S320F tau variants produces a novel accelerated model of tauopathy. Hum Mol Genet. 2019;28:3255–69. https://doi.org/10.1093/hmg/ddz151.
Article
CAS
Google Scholar
Croft CL, Cruz PE, Ryu DH, Ceballos-Diaz C, Strang KH, Woody BM, et al. rAAV-based brain slice culture models of Alzheimer’s and Parkinson’s disease inclusion pathologies. J Exp Med. 2019;216:539–55. https://doi.org/10.1084/jem.20182184.
Article
CAS
Google Scholar
Ishizawa T, Sahara N, Ishiguro K, Kersh J, McGowan E, Lewis J, et al. Co-localization of glycogen synthase kinase-3 with neurofibrillary tangles and granulovacuolar degeneration in transgenic mice. Am J Pathol. 2003;163:1057–67. https://doi.org/10.1016/S0002-9440(10)63465-7.
Article
CAS
Google Scholar
Köhler C, Dinekov M, Götz J. Active glycogen synthase kinase-3 and tau pathology-related tyrosine phosphorylation in pR5 human tau transgenic mice. Neurobiol Aging. 2013;34:1369–79. https://doi.org/10.1016/j.neurobiolaging.2012.11.010.
Article
CAS
Google Scholar
Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, et al. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science (80- ). 2001;293:1487–91. https://doi.org/10.1126/science.1058189.
Article
CAS
Google Scholar
Yamoah A, Tripathi P, Sechi A, Köhler C, Guo H, Chandrasekar A, et al. Aggregates of RNA binding proteins and ER chaperones linked to exosomes in granulovacuolar degeneration of the Alzheimer’s disease brain. J Alzheimer’s Dis. 2020;75:139–56. https://doi.org/10.3233/jad-190722.
Article
CAS
Google Scholar
Aragão Gomes L, Uytterhoeven V, Lopez-Sanmartin D, Tomé SO, Tousseyn T, Vandenberghe R, et al. Maturation of neuronal AD-tau pathology involves site-specific phosphorylation of cytoplasmic and synaptic tau preceding conformational change and fibril formation. Acta Neuropathol. 2021;141:173–92. https://doi.org/10.1007/s00401-020-02251-6.
Article
CAS
Google Scholar
Volpicelli-Daley LA, Luk KC, Lee VM-Y. Addition of exogenous α-synuclein preformed fibrils to primary neuronal cultures to seed recruitment of endogenous α-synuclein to Lewy body and Lewy neurite-like aggregates. Nat Protoc. 2014;9:2135–46. https://doi.org/10.1038/nprot.2014.143.
Article
CAS
Google Scholar
Morris M, Knudsen GM, Maeda S, Trinidad JC, Ioanoviciu A, Burlingame AL, et al. Tau post-translational modifications in wild-type and human amyloid precursor protein transgenic mice. Nat Neurosci. 2015;18:1183–9. https://doi.org/10.1038/nn.4067.
Article
CAS
Google Scholar
Funk KE, Thomas SN, Schafer KN, Cooper GL, Liao Z, Clark DJ, et al. Lysine methylation is an endogenous post-translational modification of tau protein in human brain and a modulator of aggregation propensity. Biochem J. 2014;462:77–88. https://doi.org/10.1042/BJ20140372.
Article
CAS
Google Scholar
Wennström M, Janelidze S, Nilsson KPR, Serrano GE, Beach TG, Dage JL, et al. Cellular localization of p-tau217 in brain and its association with p-tau217 plasma levels. Acta Neuropathol Commun. 2022;10:1–12. https://doi.org/10.1186/s40478-021-01307-2.
Article
CAS
Google Scholar
Matsuo ES, Shin RW, Billingsley ML, Van deVoorde A, O’Connor M, Trojanowski JQ, et al. Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer’s disease paired helical filament tau. Neuron. 1994;13:989–1002. https://doi.org/10.1016/0896-6273(94)90264-X.
Article
CAS
Google Scholar
Santpere G, Puig B, Ferrer I. Low molecular weight species of tau in Alzheimer’s disease are dependent on tau phosphorylation sites but not on delayed post-mortem delay in tissue processing. Neurosci Lett. 2006;399:106–10. https://doi.org/10.1016/j.neulet.2006.01.036.
Article
CAS
Google Scholar
Moors TE, Maat CA, Niedieker D, Mona D, Petersen D, Timmermans-Huisman E, et al. The subcellular arrangement of alpha-synuclein proteoforms in the Parkinson’s disease brain as revealed by multicolor STED microscopy. Acta Neuropathol. 2021;142:423–48. https://doi.org/10.1007/s00401-021-02329-9.
Article
CAS
Google Scholar
DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, et al. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science (80- ). 1997;277:1990–3. https://doi.org/10.1126/science.277.5334.1990.
Article
CAS
Google Scholar
Wiersma VI, van Hecke W, Scheper W, van Osch MAJ, Hermsen WJM, Rozemuller AJM, et al. Activation of the unfolded protein response and granulovacuolar degeneration are not common features of human prion pathology. Acta Neuropathol Commun. 2016;4:113. https://doi.org/10.1186/s40478-016-0383-7.
Article
CAS
Google Scholar
Scheres SH, Zhang W, Falcon B, Goedert M. Cryo-EM structures of tau filaments. Curr Opin Struct Biol. 2020;64:17–25. https://doi.org/10.1016/j.sbi.2020.05.011.
Article
CAS
Google Scholar
Riku Y, Duyckaerts C, Boluda S, Plu I, Le Ber I, Millecamps S, et al. Increased prevalence of granulovacuolar degeneration in C9orf72 mutation. Acta Neuropathol. 2019;138:783–93. https://doi.org/10.1007/s00401-019-02028-6.
Article
CAS
Google Scholar
Van Schoor E, Koper MJ, Ospitalieri S, Dedeene L, Tomé SO, Vandenberghe R, et al. Necrosome-positive granulovacuolar degeneration is associated with TDP-43 pathological lesions in the hippocampus of ALS/FTLD cases. Neuropathol Appl Neurobiol. 2021;47:328–45. https://doi.org/10.1111/nan.12668.
Article
CAS
Google Scholar
Gami-Patel P, van Dijken I, Meeter LH, Melhem S, Morrema THJ, Scheper W, et al. Unfolded protein response activation in C9orf72 frontotemporal dementia is associated with dipeptide pathology and granulovacuolar degeneration in granule cells. Brain Pathol. 2021;31:163–73. https://doi.org/10.1111/bpa.12894.
Article
CAS
Google Scholar
Barthélemy NR, Bateman RJ, Hirtz C, Marin P, Becher F, Sato C, et al. Cerebrospinal fluid phospho-tau T217 outperforms T181 as a biomarker for the differential diagnosis of Alzheimer’s disease and PET amyloid-positive patient identification. Alzheimer’s Res Ther. 2020;12:1–11. https://doi.org/10.1186/s13195-020-00596-4.
Article
CAS
Google Scholar
Janelidze S, Stomrud E, Smith R, Palmqvist S, Mattsson N, Airey DC, et al. Cerebrospinal fluid p-tau217 performs better than p-tau181 as a biomarker of Alzheimer’s disease. Nat Commun. 2020;11:1–12. https://doi.org/10.1038/s41467-020-15436-0.
Article
CAS
Google Scholar
Palmqvist S, Janelidze S, Quiroz YT, Zetterberg H, Lopera F, Stomrud E, et al. Discriminative accuracy of plasma phospho-tau217 for Alzheimer disease vs other neurodegenerative disorders. JAMA. 2020;324:772–81. https://doi.org/10.1001/jama.2020.12134.
Article
CAS
Google Scholar
Cortes CJ, La Spada AR. TFEB dysregulation as a driver of autophagy dysfunction in neurodegenerative disease: molecular mechanisms, cellular processes, and emerging therapeutic opportunities. Neurobiol Dis. 2019;122:83–93. https://doi.org/10.1016/j.nbd.2018.05.012.
Article
CAS
Google Scholar
Cabukusta B, Neefjes J. Mechanisms of lysosomal positioning and movement. Traffic. 2018;19:761–9. https://doi.org/10.1111/tra.12587.
Article
CAS
Google Scholar