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International Journal of Alzheimer's Disease
Volume 2012 (2012), Article ID 752894, 10 pages
doi:10.1155/2012/752894
Review Article
Lysosomal Fusion Dysfunction as a Unifying Hypothesis for Alzheimer's Disease Pathology
Department of Molecular and Cellular Biochemistry, The Ohio State University College of Medicine, Columbus, OH 43210, USA
Received 2 June 2012; Revised 1 August 2012; Accepted 2 August 2012
Academic Editor: Wiep Scheper
Copyright © 2012 Kristen E. Funk and Jeff Kuret. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Linked References
- D. J. Selkoe, “The cell biology β-amyloid precursor protein and presenilin in Alzheimer's disease,” Trends in Cell Biology, vol. 8, no. 11, pp. 447–453, 1998. View at Publisher · View at Google Scholar · View at Scopus
- M. Goedert, “Tau protein and the neurofibrillary pathology of Alzheimer's disease,” Trends in Neurosciences, vol. 16, no. 11, pp. 460–465, 1993. View at Scopus
- M. J. Ball and P. Lo, “Granulovacuolar degeneration in the ageing brain and in dementia,” Journal of Neuropathology and Experimental Neurology, vol. 36, no. 3, pp. 474–487, 1977. View at Scopus
- D. M. Holtzman, “CSF biomarkers for Alzheimer's disease: current utility and potential future use,” Neurobiology of Aging, vol. 32, supplement 1, pp. S4–S9, 2011.
- A. Goate, M. C. Chartier-Harlin, M. Mullan et al., “Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease,” Nature, vol. 349, no. 6311, pp. 704–706, 1991. View at Publisher · View at Google Scholar · View at Scopus
- M. A. Smith, G. Perry, P. L. Richey et al., “Oxidative damage in Alzheimer's,” Nature, vol. 382, no. 6587, pp. 120–121, 1996. View at Scopus
- T. Hasegawa, “Prolonged stress will induce Alzheimer's disease in elderly people by increased release of homocysteic acid,” Medical Hypotheses, vol. 69, no. 5, pp. 1135–1139, 2007. View at Publisher · View at Google Scholar · View at Scopus
- I. Mellman, “Membranes and sorting,” Current Opinion in Cell Biology, vol. 8, no. 4, pp. 497–498, 1996. View at Publisher · View at Google Scholar · View at Scopus
- A. V. Vieira, C. Lamaze, and S. L. Schmid, “Control of EGF receptor signaling by clathrin-mediated endocytosis,” Science, vol. 274, no. 5295, pp. 2086–2089, 1996. View at Publisher · View at Google Scholar · View at Scopus
- P. A. Vanlandingham and B. P. Ceresa, “Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration,” The Journal of Biological Chemistry, vol. 284, no. 18, pp. 12110–12124, 2009. View at Publisher · View at Google Scholar · View at Scopus
- J. H. Hurley, “ESCRT complexes and the biogenesis of multivesicular bodies,” Current Opinion in Cell Biology, vol. 20, no. 1, pp. 4–11, 2008. View at Publisher · View at Google Scholar · View at Scopus
- S. Saksena, J. Sun, T. Chu, and S. D. Emr, “ESCRTing proteins in the endocytic pathway,” Trends in Biochemical Sciences, vol. 32, no. 12, pp. 561–573, 2007. View at Publisher · View at Google Scholar · View at Scopus
- R. L. Williams and S. Urbé, “The emerging shape of the ESCRT machinery,” Nature Reviews Molecular Cell Biology, vol. 8, no. 5, pp. 355–368, 2007. View at Publisher · View at Google Scholar · View at Scopus
- R. M. Johnstone, A. Mathew, A. B. Mason, and K. Teng, “Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins,” Journal of Cellular Physiology, vol. 147, no. 1, pp. 27–36, 1991. View at Scopus
- C. Théry, L. Zitvogel, and S. Amigorena, “Exosomes: composition, biogenesis and function,” Nature Reviews Immunology, vol. 2, no. 8, pp. 569–579, 2002. View at Scopus
- C. M. Fader and M. I. Colombo, “Autophagy and multivesicular bodies: two closely related partners,” Cell Death and Differentiation, vol. 16, no. 1, pp. 70–78, 2009. View at Publisher · View at Google Scholar · View at Scopus
- S. Pankiv, T. H. Clausen, T. Lamark et al., “p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy,” The Journal of Biological Chemistry, vol. 282, no. 33, pp. 24131–24145, 2007. View at Publisher · View at Google Scholar · View at Scopus
- Y. Kabeya, N. Mizushima, T. Ueno et al., “LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing,” EMBO Journal, vol. 19, no. 21, pp. 5720–5728, 2000. View at Scopus
- W. A. Dunn Jr., “Studies on the mechanisms of autophagy: maturation of the autophagic vacuole,” Journal of Cell Biology, vol. 110, no. 6, pp. 1935–1945, 1990. View at Publisher · View at Google Scholar · View at Scopus
- E. L. Eskelinen, “Maturation of autophagic vacuoles in Mammalian cells,” Autophagy, vol. 1, no. 1, pp. 1–10, 2005. View at Scopus
- R. A. Nixon and A. M. Cataldo, “Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 9, no. 3, supplement, pp. 277–289, 2006. View at Scopus
- R. A. Nixon, P. M. Mathews, and A. M. Cataldo, “The neuronal endosomal-lysosomal system in Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 3, no. 1, pp. 97–107, 2001. View at Scopus
- S. D. Ginsberg, M. J. Alldred, S. E. Counts et al., “Microarray analysis of hippocampal CA1 neurons implicates early endosomal dysfunction during Alzheimer's disease progression,” Biological Psychiatry, vol. 68, no. 10, pp. 885–893, 2010. View at Publisher · View at Google Scholar · View at Scopus
- S. D. Ginsberg, E. J. Mufson, S. E. Counts et al., “Regional selectivity of rab5 and rab7 protein upregulation in mild cognitive impairment and Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 22, no. 2, pp. 631–639, 2010. View at Publisher · View at Google Scholar · View at Scopus
- S. D. Ginsberg, E. J. Mufson, M. J. Alldred et al., “Upregulation of select rab GTPases in cholinergic basal forebrain neurons in mild cognitive impairment and Alzheimer's disease,” Journal of Chemical Neuroanatomy, vol. 42, no. 2, pp. 102–110, 2011. View at Publisher · View at Google Scholar · View at Scopus
- A. M. Cataldo, P. M. Mathews, A. B. Boiteau et al., “Down syndrome fibroblast model of Alzheimer-related endosome pathology: accelerated endocytosis promotes late endocytic defects,” American Journal of Pathology, vol. 173, no. 2, pp. 370–384, 2008. View at Publisher · View at Google Scholar · View at Scopus
- A. M. Cataldo, C. M. Peterhoff, J. C. Troncoso, T. Gomez-Isla, B. T. Hyman, and R. A. Nixon, “Endocytic pathway abnormalities precede amyloid β deposition in sporadic Alzheimer's disease and down syndrome: differential effects of APOE genotype and presenilin mutations,” American Journal of Pathology, vol. 157, no. 1, pp. 277–286, 2000. View at Scopus
- Y. W. Zhang, R. Thompson, H. Zhang, and H. Xu, “APP processing in Alzheimer's disease,” Molecular Brain, vol. 4, no. 1, article 3, 2011. View at Publisher · View at Google Scholar · View at Scopus
- V. Hook, T. Toneff, M. Bogyo et al., “Inhibition of cathepsin B reduces β-amyloid production in regulated secretory vesicles of neuronal chromaffin cells: evidence for cathepsin B as a candidate β-secretase of Alzheimer's disease,” Biological Chemistry, vol. 386, no. 9, pp. 931–940, 2005. View at Publisher · View at Google Scholar · View at Scopus
- V. Y. H. Hook, M. Kindy, T. Reinheckel, C. Peters, and G. Hook, “Genetic cathepsin B deficiency reduces β-amyloid in transgenic mice expressing human wild-type amyloid precursor protein,” Biochemical and Biophysical Research Communications, vol. 386, no. 2, pp. 284–288, 2009. View at Publisher · View at Google Scholar · View at Scopus
- I. Benilova, E. Karran, and B. De Strooper, “The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes,” Nature Neuroscience, vol. 15, no. 3, pp. 349–357, 2012.
- D. Prvulovic and H. Hampel, “Amyloid β (Aβ) and phospho-tau (p-tau) as diagnostic biomarkers in Alzheimer's disease,” Clinical Chemistry and Laboratory Medicine, vol. 49, no. 3, pp. 367–374, 2011. View at Publisher · View at Google Scholar · View at Scopus
- A. M. Cataldo, J. L. Barnett, C. Pieroni, and R. A. Nixon, “Increased neuronal endocytosis and protease delivery to early endosomes in sporadic Alzheimer's disease: neuropathologic evidence for a mechanism of increased β-amyloidogenesis,” Journal of Neuroscience, vol. 17, no. 16, pp. 6142–6151, 1997. View at Scopus
- A. M. Cataldo, S. Petanceska, N. B. Terio et al., “Aβ localization in abnormal endosomes: association with earliest Aβ elevations in AD and Down syndrome,” Neurobiology of Aging, vol. 25, no. 10, pp. 1263–1272, 2004. View at Publisher · View at Google Scholar · View at Scopus
- O. M. Grbovic, P. M. Mathews, Y. Jiang et al., “Rab5-stimulated up-regulation of the endocytic pathway increases intracellular β-cleaved amyloid precursor protein carboxyl-terminal fragment levels and Aβ production,” The Journal of Biological Chemistry, vol. 278, no. 33, pp. 31261–31268, 2003. View at Publisher · View at Google Scholar · View at Scopus
- P. M. Mathews, C. B. Guerra, Y. Jiang et al., “Alzheimer's disease-related overexpression of the cation-dependent mannose 6-phosphate receptor increases Aβ secretion: role for altered lysosomal hydrolase distribution in β-amyloidogenesis,” The Journal of Biological Chemistry, vol. 277, no. 7, pp. 5299–5307, 2002. View at Publisher · View at Google Scholar · View at Scopus
- R. A. Nixon, A. M. Cataldo, and P. M. Mathews, “The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review,” Neurochemical Research, vol. 25, no. 9-10, pp. 1161–1172, 2000. View at Scopus
- W. H. Yu, A. M. Cuervo, A. Kumar et al., “Macroautophagy—a novel β-amyloid peptide-generating pathway activated in Alzheimer's disease,” Journal of Cell Biology, vol. 171, no. 1, pp. 87–98, 2005. View at Publisher · View at Google Scholar · View at Scopus
- M. Arbel, I. Yacoby, and B. Solomon, “Inhibition of amyloid precursor protein processing by β-secretase through site-directed antibodies,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 21, pp. 7718–7723, 2005. View at Publisher · View at Google Scholar · View at Scopus
- J. T. Huse, D. S. Pijak, G. J. Leslie, V. M. Y. Lee, and R. W. Doms, “Maturation and endosomal targeting of β-site amyloid precursor protein-cleaving enzyme. The Alzheimer's disease β-secretase,” The Journal of Biological Chemistry, vol. 275, no. 43, pp. 33729–33737, 2000. View at Publisher · View at Google Scholar · View at Scopus
- S. Kametaka, M. Shibata, K. Moroe et al., “Identification of phospholipid scramblase 1 as a novel interacting molecule with β-secretase (β-site amyloid precursor protein (APP) cleaving enzyme (BACE)),” The Journal of Biological Chemistry, vol. 278, no. 17, pp. 15239–15245, 2003. View at Publisher · View at Google Scholar · View at Scopus
- A. Kinoshita, H. Fukumoto, T. Shah, C. M. Whelan, M. C. Irizarry, and B. T. Hyman, “Demonstration by FRET of BACE interaction with the amyloid precursor protein at the cell surface and in early endosomes,” Journal of Cell Science, vol. 116, part 16, pp. 3339–3346, 2003. View at Publisher · View at Google Scholar · View at Scopus
- Y. H. Koh, C. A. F. von Arnim, B. T. Hyman, R. E. Tanzi, and G. Tesco, “BACE is degraded via the lysosomal pathway,” The Journal of Biological Chemistry, vol. 280, no. 37, pp. 32499–32504, 2005. View at Publisher · View at Google Scholar · View at Scopus
- R. P. Friedrich, K. Tepper, R. Rönicke et al., “Mechanism of amyloid plaque formation suggests an intracellular basis of Aβ pathogenicity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 5, pp. 1942–1947, 2010. View at Publisher · View at Google Scholar · View at Scopus
- E. H. Koo and S. L. Squazzo, “Evidence that production and release of amyloid β-protein involves the endocytic pathway,” The Journal of Biological Chemistry, vol. 269, no. 26, pp. 17386–17389, 1994. View at Scopus
- L. McConlogue, F. Castellano, C. deWit, D. Schenk, and W. A. Maltese, “Differential effects of a Rab6 mutant on secretory versus amyloidogenic processing of Alzheimer's β-amyloid precursor protein,” The Journal of Biological Chemistry, vol. 271, no. 3, pp. 1343–1348, 1996. View at Publisher · View at Google Scholar · View at Scopus
- G. D. Schellenberg and T. J. Montine, “The genetics and neuropathology of Alzheimer's disease,” Acta Neuropathologica, vol. 124, no. 3, pp. 305–323, 2012.
- N. Takasugi, T. Tomita, I. Hayashi et al., “The role of presenilin cofactors in the γ-secratase complex,” Nature, vol. 422, no. 6930, pp. 438–441, 2003. View at Publisher · View at Google Scholar · View at Scopus
- W. T. Kimberly, M. J. LaVoie, B. L. Ostaszewski, W. Ye, M. S. Wolfe, and D. J. Selkoe, “γ-Secretase is a membrane protein complex comprised of presenilin, nicastrin, aph-1, and pen-2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 11, pp. 6382–6387, 2003. View at Publisher · View at Google Scholar · View at Scopus
- P. Cupers, M. Bentahir, K. Craessaerts et al., “The discrepancy between presenilin subcellular localization and γ-secretase processing of amyloid precursor protein,” Journal of Cell Biology, vol. 154, no. 4, pp. 731–740, 2001. View at Publisher · View at Google Scholar · View at Scopus
- D. M. Kovacs, H. J. Fausett, K. J. Page et al., “Alzheimer-associated presenilins 1 and 2: neuronal expression in brain and localization to intracellular membranes in mammalian cells,” Nature Medicine, vol. 2, no. 2, pp. 224–229, 1996. View at Publisher · View at Google Scholar · View at Scopus
- D. Scheuner, C. Eckman, M. Jensen et al., “Secreted amyloid β-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease,” Nature Medicine, vol. 2, no. 8, pp. 864–870, 1996. View at Publisher · View at Google Scholar · View at Scopus
- D. R. Borchelt, G. Thinakaran, C. B. Eckman et al., “Familial Alzheimer's disease-linked presenilin I variants elevate aβ1- 42/1-40 ratio in vitro and in vivo,” Neuron, vol. 17, no. 5, pp. 1005–1013, 1996. View at Publisher · View at Google Scholar · View at Scopus
- D. Cai, J. Y. Leem, J. P. Greenfield et al., “Presenilin-1 regulates intracellular trafficking and cell surface delivery of β-amyloid precursor protein,” The Journal of Biological Chemistry, vol. 278, no. 5, pp. 3446–3454, 2003. View at Publisher · View at Google Scholar · View at Scopus
- C. Dumanchin, C. Czech, D. Campion et al., “Presenilins interact with Rab11, a small GTPase involved in the regulation of vesicular transport,” Human Molecular Genetics, vol. 8, no. 7, pp. 1263–1269, 1999. View at Publisher · View at Google Scholar · View at Scopus
- W. Scheper, R. Zwart, and F. Baas, “Rab6 membrane association is dependent of Presenilin 1 and cellular phosphorylation events,” Molecular Brain Research, vol. 122, no. 1, pp. 17–23, 2004. View at Publisher · View at Google Scholar · View at Scopus
- W. Scheper, R. Zwart, P. van der Sluijs, W. Annaert, W. A. van Gool, and F. Baas, “Alzheimer's presenilin 1 is a putative membrane receptor for rab GDP dissociation inhibitor,” Human Molecular Genetics, vol. 9, no. 2, pp. 303–310, 2000. View at Scopus
- J. H. Lee, W. H. Yu, A. Kumar et al., “Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations,” Cell, vol. 141, no. 7, pp. 1146–1158, 2010. View at Publisher · View at Google Scholar · View at Scopus
- A. Yamamoto, Y. Tagawa, T. Yoshimori, Y. Moriyama, R. Masaki, and Y. Tashiro, “Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells,” Cell Structure and Function, vol. 23, no. 1, pp. 33–42, 1998. View at Scopus
- X. Zhang, K. Garbett, K. Veeraraghavalu, et al., “A role for presenilins in autophagy revisited: normal acidification of Lysosomes in cells lacking PSEN1 and PSEN2,” Journal of Neuroscience, vol. 32, no. 25, pp. 8633–8648, 2012.
- K. Coen, R. S. Flannagan, S. Baron, et al., “Lysosomal calcium homeostasis defects, not proton pump defects, cause endo-lysosomal dysfunction in PSEN-deficient cells,” Journal of Cell Biology, vol. 198, no. 1, pp. 23–35, 2012.
- P. R. Pryor, B. M. Mullock, N. A. Bright, S. R. Gray, and J. P. Luzio, “The role of intraorganellar Ca2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles,” Journal of Cell Biology, vol. 149, no. 5, pp. 1053–1062, 2000. View at Publisher · View at Google Scholar · View at Scopus
- A. J. Morgan, F. M. Platt, E. Lloyd-Evans, and A. Galione, “Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease,” Biochemical Journal, vol. 439, no. 3, pp. 349–374, 2011.
- D. Harold, R. Abraham, P. Hollingworth, et al., “Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease,” Nature Genetics, vol. 41, no. 10, pp. 1088–1093, 2009. View at Scopus
- J. C. Lambert, S. Heath, G. Even, et al., “Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease,” Nature Genetics, vol. 41, no. 10, pp. 1094–1099, 2009.
- R. W. Mahley and S. C. Rall Jr., “Apolipoprotein E: far more than a lipid transport protein,” Annual Review of Genomics and Human Genetics, vol. 1, no. 2000, pp. 507–537, 2000. View at Scopus
- R. W. Mahley, K. H. Weisgraber, and Y. Huang, “Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS,” Journal of Lipid Research, vol. 50, supplement, pp. S183–S188, 2009. View at Publisher · View at Google Scholar · View at Scopus
- E. Rogaeva, Y. Meng, J. H. Lee et al., “The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease,” Nature Genetics, vol. 39, no. 2, pp. 168–177, 2007. View at Publisher · View at Google Scholar · View at Scopus
- S. Seshadri, A. L. Fitzpatrick, M. A. Ikram, et al., “Genome-wide analysis of genetic loci associated with Alzheimer disease,” The Journal of the American Medical Association, vol. 303, no. 18, pp. 1832–1840, 2010.
- L. Jones, D. Harold, and J. Williams, “Genetic evidence for the involvement of lipid metabolism in Alzheimer's disease,” Biochimica et Biophysica Acta, vol. 1801, no. 8, pp. 754–761, 2010. View at Publisher · View at Google Scholar · View at Scopus
- T. Nuutinen, T. Suuronen, A. Kauppinen, and A. Salminen, “Clusterin: a forgotten player in Alzheimer's disease,” Brain Research Reviews, vol. 61, no. 2, pp. 89–104, 2009. View at Publisher · View at Google Scholar · View at Scopus
- W. Kim, S. Lee, and G. F. Hall, “Secretion of human tau fragments resembling CSF-tau in Alzheimer's disease is modulated by the presence of the exon 2 insert,” FEBS Letters, vol. 584, no. 14, pp. 3085–3088, 2010. View at Publisher · View at Google Scholar · View at Scopus
- W. Kim, S. Lee, C. Jung, A. Ahmed, G. Lee, and G. F. Hall, “Interneuronal transfer of human tau between lamprey central neurons in situ,” Journal of Alzheimer's Disease, vol. 19, no. 2, pp. 647–664, 2010. View at Publisher · View at Google Scholar · View at Scopus
- E. Emmanouilidou, K. Melachroinou, T. Roumeliotis et al., “Cell-produced α-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival,” Journal of Neuroscience, vol. 30, no. 20, pp. 6838–6851, 2010. View at Publisher · View at Google Scholar · View at Scopus
- B. Fevrier, D. Vilette, F. Archer et al., “Cells release prions in association with exosomes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 26, pp. 9683–9688, 2004. View at Publisher · View at Google Scholar · View at Scopus
- L. Rajendran, M. Honsho, T. R. Zahn et al., “Alzheimer's disease β-amyloid peptides are released in association with exosomes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 30, pp. 11172–11177, 2006. View at Publisher · View at Google Scholar · View at Scopus
- S. Saman, W. Kim, M. Raya, et al., “Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease,” The Journal of Biological Chemistry, vol. 287, no. 6, pp. 3842–3849, 2012.
- H. Braak, I. Alafuzoff, T. Arzberger, H. Kretzschmar, and K. Del Tredici, “Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry,” Acta Neuropathologica, vol. 112, no. 4, pp. 389–404, 2006. View at Publisher · View at Google Scholar · View at Scopus
- S. Lee, W. Kim, Z. Li, and G. F. Hall, “Accumulation of vesicle-associated human tau in distal dendrites drives degeneration and tau secretion in an in situ cellular tauopathy model,” International Journal of Alzheimer's Disease, vol. 2012, Article ID 172837, 16 pages, 2012. View at Publisher · View at Google Scholar
- M. Sverdlov, A. N. Shajahan, and R. D. Minshall, “Tyrosine phosphorylation-dependence of caveolae-mediated endocytosis,” Journal of Cellular and Molecular Medicine, vol. 11, no. 6, pp. 1239–1250, 2007. View at Publisher · View at Google Scholar · View at Scopus
- W. Nickel, “Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells,” Traffic, vol. 6, no. 8, pp. 607–614, 2005. View at Publisher · View at Google Scholar · View at Scopus
- Y. Fang, N. Wu, X. Gan, W. Yan, J. C. Morrell, and S. J. Gould, “Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes,” PLoS Biology, vol. 5, no. 6, article e158, 2007. View at Publisher · View at Google Scholar · View at Scopus
- P. J. Dolan and G. V. W. Johnson, “A caspase cleaved form of tau is preferentially degraded through the autophagy pathway,” The Journal of Biological Chemistry, vol. 285, no. 29, pp. 21978–21987, 2010. View at Publisher · View at Google Scholar · View at Scopus
- R. A. Armstrong, N. J. Cairns, and P. L. Lantos, “Clustering of Pick bodies in patients with Pick's disease,” Neuroscience Letters, vol. 242, no. 2, pp. 81–84, 1998. View at Publisher · View at Google Scholar · View at Scopus
- R. A. Armstrong, N. J. Cairns, and P. L. Lantos, “Clustering of cerebral cortical lesions in patients with corticobasal degeneration,” Neuroscience Letters, vol. 268, no. 1, pp. 5–8, 1999. View at Publisher · View at Google Scholar · View at Scopus
- H. Braak and E. Braak, “Neuropathological stageing of Alzheimer-related changes,” Acta Neuropathologica, vol. 82, no. 4, pp. 239–259, 1991. View at Scopus
- A. Gómez-Ramos, M. Díaz-Hernández, R. Cuadros, F. Hernández, and J. Avila, “Extracellular tau is toxic to neuronal cells,” FEBS Letters, vol. 580, no. 20, pp. 4842–4850, 2006. View at Publisher · View at Google Scholar · View at Scopus
- A. Gómez-Ramos, M. Díaz-Hernández, A. Rubio, M. T. Miras-Portugal, and J. Avila, “Extracellular tau promotes intracellular calcium increase through M1 and M3 muscarinic receptors in neuronal cells,” Molecular and Cellular Neuroscience, vol. 37, no. 4, pp. 673–681, 2008. View at Publisher · View at Google Scholar · View at Scopus
- K. Strauss, C. Goebel, H. Runz et al., “Exosome secretion ameliorates lysosomal storage of cholesterol in Niemann-Pick type C disease,” The Journal of Biological Chemistry, vol. 285, no. 34, pp. 26279–26288, 2010. View at Publisher · View at Google Scholar · View at Scopus
- E. Bednarski and G. Lynch, “Cytosolic proteolysis of τ by cathepsin D in hippocampus following suppression of cathepsins B and L,” Journal of Neurochemistry, vol. 67, no. 5, pp. 1846–1855, 1996. View at Scopus
- A. Kenessey, P. Nacharaju, L. W. Ko, and S. H. Yen, “Degradation of tau by lysosomal enzyme cathepsin D: implication for Alzheimer neurofibrillary degeneration,” Journal of Neurochemistry, vol. 69, no. 5, pp. 2026–2038, 1997. View at Scopus
- J. Bendiske and B. A. Bahr, “Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis—an approach for slowing Alzheimer disease?” Journal of Neuropathology and Experimental Neurology, vol. 62, no. 5, pp. 451–463, 2003. View at Scopus
- K. Ii, H. Ito, E. Kominami, and A. Hirano, “Abnormal distribution of cathepsin proteinases and endogenous inhibitors (cystatins) in the hippocampus of patients with Alzheimer's disease, parkinsonism-dementia complex on Guam, and senile dementia and in the aged,” Virchows Archiv A, vol. 423, no. 3, pp. 185–194, 1993. View at Scopus
- K. Ikeda, H. Akiyama, T. Arai et al., “Alz-50/Gallyas-positive lysosome-like intraneuronal granules in Alzheimer's disease and control brains,” Neuroscience Letters, vol. 258, no. 2, pp. 113–116, 1998. View at Publisher · View at Google Scholar · View at Scopus
- E. E. Congdon, S. Kim, J. Bonchak, T. Songrug, A. Matzavinos, and J. Kuret, “Nucleation-dependent tau filament formation: the importance of dimerization and an estimation of elementary rate constants,” The Journal of Biological Chemistry, vol. 283, no. 20, pp. 13806–13816, 2008. View at Publisher · View at Google Scholar · View at Scopus
- Q. Zhong, E. E. Congdon, H. N. Nagaraja, and J. Kuret, “Tau isoform composition influences rate and extent of filament formation,” The Journal of Biological Chemistry, vol. 287, no. 24, pp. 20711–20719, 2012.
- C. A. Dickey, A. Kamal, K. Lundgren et al., “The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins,” The Journal of Clinical Investigation, vol. 117, no. 3, pp. 648–658, 2007. View at Publisher · View at Google Scholar · View at Scopus
- W. Luo, F. Dou, A. Rodina et al., “Roles of heat-shock protein 90 in maintaining and facilitating the neurodegenerative phenotype in tauopathies,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 22, pp. 9511–9516, 2007. View at Publisher · View at Google Scholar · View at Scopus
- Y. Wang, M. Martinez-Vicente, U. Krüger et al., “Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing,” Human Molecular Genetics, vol. 18, no. 21, pp. 4153–4170, 2009. View at Publisher · View at Google Scholar · View at Scopus
- Y. P. Wang, J. Biernat, M. Pickhardt, E. Mandelkow, and E. M. Mandelkow, “Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 24, pp. 10252–10257, 2007. View at Publisher · View at Google Scholar · View at Scopus
- A. Samsonov, J. Z. Yu, M. Rasenick, and S. V. Popov, “Tau interaction with microtubules in vivo,” Journal of Cell Science, vol. 117, part 25, pp. 6129–6141, 2004. View at Publisher · View at Google Scholar · View at Scopus
- R. Dixit, J. L. Ross, Y. E. Goldman, and E. L. F. Holzbaur, “Differential regulation of dynein and kinesin motor proteins by tau,” Science, vol. 319, no. 5866, pp. 1086–1089, 2008. View at Publisher · View at Google Scholar · View at Scopus
- L. C. Kapitein, M. A. Schlager, M. Kuijpers et al., “Mixed microtubules steer dynein-driven cargo transport into dendrites,” Current Biology, vol. 20, no. 4, pp. 290–299, 2010. View at Publisher · View at Google Scholar · View at Scopus
- S. Love, L. R. Bridges, and C. P. Case, “Neurofibrillary tangles in Niemann-Pick disease type C,” Brain, vol. 118, part 1, pp. 119–129, 1995. View at Scopus
- P. Z. Almos, S. Horvath, A. Czibula, et al., “H1 tau haplotype-related genomic variation at 17q21.3 as an Asian heritage of the European Gypsy population,” Heredity, vol. 101, no. 5, pp. 416–419, 2008. View at Publisher · View at Google Scholar · View at Scopus
- R. L. Neve, P. Harris, K. S. Kosik, D. M. Kurnit, and T. A. Donlon, “Identification of cDNA clones for the human microtubule-associated protein tau and chromosomal localization of the genes for tau and microtubule-associated protein 2,” Brain Research, vol. 387, no. 3, pp. 271–280, 1986. View at Scopus
- R. Brandt, J. Léger, and G. Lee, “Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain,” Journal of Cell Biology, vol. 131, no. 5, pp. 1327–1340, 1995. View at Publisher · View at Google Scholar · View at Scopus
- A. Abraha, N. Ghoshal, T. C. Gamblin et al., “C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease,” Journal of Cell Science, vol. 113, part 21, pp. 3737–3745, 2000. View at Scopus
- C. Haase, J. T. Stieler, T. Arendt, and M. Holzer, “Pseudophosphorylation of tau protein alters its ability for self-aggregation,” Journal of Neurochemistry, vol. 88, no. 6, pp. 1509–1520, 2004. View at Scopus
- F. Liu, B. Li, E. J. Tung, I. Grundke-Iqbal, K. Iqbal, and C. X. Gong, “Site-specific effects of tau phosphorylation on its microtubule assembly activity and self-aggregation,” European Journal of Neuroscience, vol. 26, no. 12, pp. 3429–3436, 2007. View at Publisher · View at Google Scholar · View at Scopus
- H. Vanderstichele, K. De Vreese, K. Blennow et al., “Analytical performance and clinical utility of the INNOTEST PHOSPHO-TAU(181P) assay for discrimination between Alzheimer's disease and dementia with Lewy bodies,” Clinical Chemistry and Laboratory Medicine, vol. 44, no. 12, pp. 1472–1480, 2006. View at Publisher · View at Google Scholar · View at Scopus
- D. H. Smith, D. F. Meaney, and W. H. Shull, “Diffuse axonal injury in head trauma,” Journal of Head Trauma Rehabilitation, vol. 18, no. 4, pp. 307–316, 2003. View at Scopus
- L. Buée, T. Bussière, V. Buée-Scherrer, A. Delacourte, and P. R. Hof, “Tau protein isoforms, phosphorylation and role in neurodegenerative disorders,” Brain Research Reviews, vol. 33, no. 1, pp. 95–130, 2000. View at Publisher · View at Google Scholar · View at Scopus
- L. Martin, X. Latypova, and F. Terro, “Post-translational modifications of tau protein: implications for Alzheimer's disease,” Neurochemistry International, vol. 58, no. 4, pp. 458–471, 2011. View at Publisher · View at Google Scholar · View at Scopus
- M. Morishima-Kawashima, M. Hasegawa, K. Takio, M. Suzuki, K. Titani, and Y. Ihara, “Ubiquitin is conjugated with amino-terminally processed tau in paired helical filaments,” Neuron, vol. 10, no. 6, pp. 1151–1160, 1993. View at Publisher · View at Google Scholar · View at Scopus
- D. Cripps, S. N. Thomas, Y. Jeng, F. Yang, P. Davies, and A. J. Yang, “Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation,” The Journal of Biological Chemistry, vol. 281, no. 16, pp. 10825–10838, 2006. View at Publisher · View at Google Scholar · View at Scopus
- S. N. Thomas, K. E. Funk, Y. Wan, et al., “Dual modification of Alzheimer's disease PHF-tau protein by lysine methylation and ubiquitylation: a mass spectrometry approach,” Acta Neuropathologica, vol. 123, no. 1, pp. 105–117, 2012.
- C. Raiborg, T. E. Rusten, and H. Stenmark, “Protein sorting into multivesicular endosomes,” Current Opinion in Cell Biology, vol. 15, no. 4, pp. 446–455, 2003. View at Publisher · View at Google Scholar · View at Scopus
- V. Chau, J. W. Tobias, A. Bachmair et al., “A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein,” Science, vol. 243, no. 4898, pp. 1576–1583, 1989. View at Scopus
- T. J. Cohen, J. L. Guo, D. E. Hurtado et al., “The acetylation of tau inhibits its function and promotes pathological tau aggregation,” Nature Communications, vol. 2, no. 1, article 252, 2011. View at Publisher · View at Google Scholar · View at Scopus
- S. W. Min, S. H. Cho, Y. Zhou et al., “Acetylation of tau inhibits its degradation and contributes to tauopathy,” Neuron, vol. 67, no. 6, pp. 953–966, 2010. View at Publisher · View at Google Scholar · View at Scopus
- J. A. Latham and S. Y. R. Dent, “Cross-regulation of histone modifications,” Nature Structural and Molecular Biology, vol. 14, no. 11, pp. 1017–1024, 2007. View at Publisher · View at Google Scholar · View at Scopus
- M. J. Ball, “Neuronal loss, neurofibrillary tangles and granulovacuolar degeneration in the hippocampus with ageing and dementia. A quantitative study,” Acta Neuropathologica, vol. 37, no. 2, pp. 111–118, 1977. View at Scopus
- N. Ghoshal, F. García-Sierra, J. Wuu et al., “Tau conformational changes correspond to impairments of episodic memory in mild cognitive impairment and Alzheimer's disease,” Experimental Neurology, vol. 177, no. 2, pp. 475–493, 2002. View at Publisher · View at Google Scholar · View at Scopus
- K. Okamoto, S. Hirai, T. Iizuka, T. Yanagisawa, and M. Watanabe, “Reexamination of granulovacuolar degeneration,” Acta Neuropathologica, vol. 82, no. 5, pp. 340–345, 1991. View at Publisher · View at Google Scholar · View at Scopus
- K. E. Funk, R. E. Mrak, and J. Kuret, “Granulovacuolar degeneration (GVD) bodies of Alzheimer's disease (AD) resemble late-stage autophagic organelles,” Neuropathology and Applied Neurobiology, vol. 37, no. 3, pp. 295–306, 2011. View at Publisher · View at Google Scholar · View at Scopus
- Y. Yamazaki, T. Takahashi, M. Hiji et al., “Immunopositivity for ESCRT-III subunit CHMP2B in granulovacuolar degeneration of neurons in the Alzheimer's disease hippocampus,” Neuroscience Letters, vol. 477, no. 2, pp. 86–90, 2010. View at Publisher · View at Google Scholar · View at Scopus
- B. Boland, A. Kumar, S. Lee et al., “Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease,” Journal of Neuroscience, vol. 28, no. 27, pp. 6926–6937, 2008. View at Publisher · View at Google Scholar · View at Scopus
- L. Q. Chen, J. S. Wei, Z. N. Lei, L. M. Zhang, Y. Liu, and F. Y. Sun, “Induction of Bcl-2 and Bax was related to hyperphosphorylation of tau and neuronal death induced by okadaic acid in rat brain,” Anatomical Record A, vol. 287, no. 2, pp. 1236–1245, 2005. View at Publisher · View at Google Scholar · View at Scopus
- S. Díaz-Troya, M. E. Pérez-Pérez, F. J. Florencio, and J. L. Crespo, “The role of TOR in autophagy regulation from yeast to plants and mammals,” Autophagy, vol. 4, no. 7, pp. 851–865, 2008. View at Scopus
- G. A. Soliman, H. A. Acosta-Jaquez, E. A. Dunlop et al., “mTOR Ser-2481 autophosphorylation monitors mTORC-specific catalytic activity and clarifies rapamycin mechanism of action,” The Journal of Biological Chemistry, vol. 285, no. 11, pp. 7866–7879, 2010. View at Publisher · View at Google Scholar · View at Scopus