Untangling the role of tau in Alzheimer’s disease: A unifying hypothesis
Tóm tắt
Recent investigations into the etiology and pathogenesis of Alzheimer’s disease (AD) in the past few years have expanded to include previously unexplored and/or disconnected aspects of AD and related conditions at both the cellular and systemic levels of organization. These include how AD-associated abnormalities affect the cell cycle and neuronal differentiation state and how they recruit signal transduction, membrane trafficking and protein transcytosis mechanisms to produce a neurotoxic syndrome capable of spreading itself throughout the brain. The recent expansion of AD research into intercellular and new aspects of cellular degenerative mechanisms is causing a systemic re-evaluation of AD pathogenesis, including the roles played by well-studied elements, such as the generation of Aβ and tau protein aggregates. It is also changing our view of neurodegenerative diseases as a whole. Here we propose a conceptual framework to account for some of the emerging aspects of the role of tau in AD pathogenesis.
Tài liệu tham khảo
Alzheimer A., Über eine eigenartige Erkrankung der Hirnrinde, Allg. Z. Psychiatr., 1907, 64, 146–148
Lowenberg K., Waggoner R., Familial organic psychosis (Alzheimer’s type), Arch. Neurol., 1934, 31, 737–754
Blessed G., Tomlinson B.E., Roth M., The association between quantitative measures of dementia and of senile change in the cerebral grey matter of elderly subjects, Br. J. Psychiatry, 1968, 114, 797–811
Olson M.I., Shaw C.M., Presenile dementia and Alzheimer’s disease in mongolism, Brain, 1969, 92, 147–156
Cook R., Ward B., Austin J., Studies in aging of the brain: IV. Familial Alzheimer’s disease: relationship to transmissible dementia, aneuploidy and microtubular defects, Neurology, 1979, 29, 1402–1412
Buckton K.E., Whalley L.J., Lee M., Christie J.E., Chromosome changes in Alzheimer’s presenile dementia, J. Med. Genet., 1983, 20, 46–51
Bird T.D., Sumi S.M., Nemens E.J., Nochlin D., Schellenberg G., Lampe T.H., et al., Phenotypic heterogeneity in familial Alzheimer’s disease: a study of 24 kindreds, Ann. Neurol., 1989, 25, 12–25
Gambetti P., Autilio-Gambetti L., Perry G., Shecket G., Crane R.C., Antibodies to neurofibrillary tangles of Alzheimer’s disease raised from human and animal neurofilament fractions, Lab. Invest., 1983, 49, 430–435
Hyman B.T., Van Hoesen G.W., Damasio A.R., Barnes C.L., Alzheimer’s disease: cell-specific pathology isolates the hippocampal formation, Science, 1984, 225, 1168–1170
Kidd M., Paired helical filaments in electron microscopy of Alzheimer’s disease, Nature, 1963, 197, 192–193
Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., DeLong M.R., Alzheimer’s disease and senile dementia: loss of neurons in the basal forebrain, Science, 1982, 215, 1237–1239
Drachman D.A., Leavitt J., Human memory and the cholinergic system: a relationship to aging?, Arch. Neurol., 1974, 30, 113–121
Glenner G.G., Wong C.W., Alzheimer’s disease and Down’s syndrome: sharing of a unique cerebrovascular amyloid fibril protein, Biochem. Biophys. Res. Commun., 1984, 122, 1131–1135
Grundke-Iqbal I., Iqbal K., Tung Y.C., Quinlan M., Wisniewski H.M., Binder L.I., Abnormal phosphorylation of the microtubuleassociated protein tau in Alzheimer cytoskeletal pathology, Proc. Natl. Acad. Sci. USA, 1986, 83, 4913–4917
Kosik K.S., Joachim C.L., Selkoe D.J., Microtubule associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease, Proc. Natl. Acad. Sci. USA 83, 1986, 4044–4048
Bancher C., Brunner C., Lassman H., Budka H., Jellinger K., Wiche G., et al., Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer’s disease, Brain Res., 1989, 477, 90–99
McKee A.C., Kowall N.W., Kosik K.S., Microtubular reorganization and dendritic growth response in Alzheimer’s disease, Ann. Neurol., 1989, 26, 652–659
Braak H., Braak E., Neuropathological staging of Alzheimer-related changes, Acta Neuropathol., 1991, 82, 239–259
Yamaguchi H., Nakazato Y., Shoji M., Ihara Y., Hirai S., Ultrastructure of the neuropil threads in the Alzheimer brain: their dendritic origin and accumulation in the senile plaques, Acta Neuropathol., 1990, 80, 368–374
St. George-Hyslop P.H., Tanzi R.E., Polinsky R.J., Haines J.L., Nee L., Watkins P.C., et al. The genetic defect causing familial Alzheimer’s disease maps on chromosome 21, Science, 1987, 235, 885–890
Chartier-Harlin M.C., Crawford F., Houlden H., Warren A., Hughes D., Fidani L., et al., Early-onset Alzheimer’s disease caused by mutations at codon 717 of the beta-amyloid precursor protein gene, Nature, 1991, 353, 844–846
Goate A., Chartier-Hardin M.C., Mullan M., Brown J., Crawford F., Fidani L., et al., Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer’s Disease, Nature, 1991, 349, 704–706
Murrel J. M., Farlow B., Ghetti B., Benson M.D., A mutation in the amyloid precursor protein associated with hereditary Alzheimer’s disease, Science, 1991, 254, 97–99
Selkoe D.J., The molecular pathology of Alzheimer’s disease, Neuron, 1991, 6, 487–498
Hardy J.A., Higgins G.A., Alzheimer’s disease: the amyloid cascade hypothesis, Science, 1992, 256, 184–185
Wallace W.C., Bragin V., Robakis N.K., Sambamurti K., VanderPutten D., Merril C.R., et al., Increased biosynthesis of Alzheimer amyloid precursor protein the in cerebral cortex of rats with lesions of the nucleus basalis of Meynert, Mol. Brain Res., 1991, 10, 173–178
Strittmatter W.J., Saunders A.M., Schmechel D., Pericak-Vance M., Enghild J., Salvesen G.S., et al., Apolipoprotein E: high-avidity binding to betaamyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease, Proc. Natl. Acad. Sci. USA, 1993, 90, 1977–1981
Wisniewski T., Frangione B., Apolipoprotein E: a pathological chaperone protein in patients with cerebral and systemic amyloid, Neurosci. Lett., 1992, 135:235–238
Gentleman S.M., Nash M.J., Sweeting C.J., Graham D.I., Roberts G.W., β-Amyloid precursor protein (βAPP) as a marker for axonal injury after head injury, Neurosci. Lett., 1993, 160, 139–144
McKenzie J.E., Gentleman S.M., Roberts G.W., Graham D.I., Royston M.C., Increased numbers of βAPP-immunoreactive neurones in the entorhinal cortex after head injury, Neuroreport, 1994, 6, 161–164
Yankner B.A., Dawes L.R., Fisher S., Villa-Komaroff L., Oster-Granite M.L., Neve R.L., Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer’s disease, Science, 1989, 245, 417–420
Busciglio J., Lorenzo A., Yeh J., Yankner B.A., Amyloid fibrils induce tau phosphorylation and loss of microtubule binding, Neuron, 1995, 14, 879–888
Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., et al., Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein, Nature, 1995, 373, 523–527
Wolfe M.S., Xia W., Ostaszewski B.L., Diehl T.S., Kimberly W.T., Selkoe D.J., Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity, Nature, 1999, 398, 513–517
Kowall N.W., Kosik K.S., Axonal disruption and aberrant localization of tau protein characterize the neuropil pathology of Alzheimer’s disease, Ann. Neurol., 1987, 22, 639–643
Weingarten M.D., Lockwood A.H., Hwo S.Y., Kirschner M.W., A protein factor essential for microtubule assembly, Proc. Natl. Acad. Sci. USA, 1975, 72, 1858–1862
Cleveland D.W., Hwo S.Y., Kirschner M.W., Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly, J. Mol. Biol., 1977, 116, 227–247
Greenberg S.G., Davies P., A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis, Proc. Natl. Acad. Sci. USA, 1990, 87, 5827–5831
Binder L.I., Frankfurter A., Rebhun L.I., The distribution of tau polypeptides in the mammalian central nervous system, J. Cell Biol., 1985, 101, 1371–1378
Lindwall G., Cole R.D., Phosphorylation affects the ability of tau protein to promote microtubule assembly, J. Biol. Chem., 1984, 259, 5301–5305
Lee G., Cowan N., Kirschner M. The primary structure and heterogeneity of tau protein from mouse brain, Science, 1998, 239, 285–288
Goedert M., Wischik C.M., Crowther R.A., Walker J.E., Klug A., Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau, Proc. Natl. Acad. Sci. USA, 85, 1998, 4051–4055
Ksiezak-Reding H., Yen S.H., Structural stability of paired helical filaments requires microtubule-binding domains of tau: a model for self-association, Neuron, 1991, 6, 717–728
Novak M., Jakes R., Edwards P.C., Milstein C., Wischik C.M., Difference between the tau protein of Alzheimer paired helical filament core and normal tau revealed by epitope analysis of monoclonal antibodies 423 and 7.51, Proc. Natl. Acad. Sci. USA, 1991, 88, 5837–5841
Crowther R.A., Olesen O.F., Jakes R., Goedert M., The microtubule binding repeats of tau protein assemble into filaments like those found in Alzheimer’s disease, FEBS Lett., 1992, 309, 199–202
Arriagada P.A., Growdon J.H., Hedley-White E.T., Hyman B.T., Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer’s Disease, Neurology, 1992, 42, 631–639
Armstrong R.A., Myers D., Smith C.U.M., The spatial patterns of plaques and tangles in Alzheimer’s disease do not support the ‘cascade hypothesis’, Dementia, 1993, 4, 16–20
Baum L., Seger R., Woodgett J.R., Kawabata S., Maruyama K., Koyama M., Silver J., Saitoh T., Overexpressed tau protein in cultured cells is phosphorylated without formation of PHF: implication of phosphoprotein phosphatase involvement, Mol. Brain Res., 1995, 34, 1–17
Levy-Lahad E., Wasco W., Poorkaj P., Romano D.M., Oshima J., Pettingell W.H., et al., Candidate gene for the chromosome 1 familial Alzheimer’s disease locus, Science, 1995, 269, 973–977
Sherrington R., Rogaev E.I., Liang Y., et al., Cloning of a gene bearing missense mutations in early-onset familial Alzheimer’s disease, Nature, 1995, 375, 754–760
Spillantini M.G., Murrell J.R., Goedert M., Farlow M.R., Klug A., Ghetti B., Mutation in the tau gene in familial multiple system tauopathy with presenile dementia, Proc. Natl. Acad. Sci. USA, 1998, 95, 7737–7741
Hall G.F., Yao J., Lee G., Tau overexpressed in identified lamprey neurons in situ is spatially segregated by phosphorylation state, forms hyperphosphorylated, dense aggregations and induces neurodegeneration, Proc. Natl. Acad. Sci. USA, 1997, 94, 4733–4738
Ishihara T., Hong M., Zhang B., Nakagawa Y., Lee M.K., Trojanowski J.Q., et al., Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform, Neuron, 1999, 24, 751–762
Spittaels K., Van den Haute C., Van Dorpe J., Bruynseels K., Vandezande K., Laenen I., et al., Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein, Am. J. Pathol., 1999, 155, 2153–2165
Götz J., Chen F., Barmettler R., Nitsch R.M., Tau filament formation in transgenic mice expressing P301L tau, J. Biol. Chem., 2001, 276, 529–534
Lewis J., McGowan E., Rockwood J., Melrose H., Nacharaju P., Van Slegtenhorst M., et al., Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein, Nat. Genet., 2000, 25, 402–405
Buee L., Delacourte A., Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, FTDP-17 and Pick’s disease, Brain Pathol., 1999, 9, 681–693
Hasegawa M., Smith M.J., Goedert M., Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly, FEBS Lett., 1998, 437, 207–210
Arawaka S., Usami M., Sahara N., Schellenberg G.D., Lee G., Mori H., The tau mutation (val337met) disrupts cytoskeletal networks of microtubules, Neuroreport, 2000, 10, 993–997
Goedert M., Jakes R., Crowther R.A., Effects of frontotemporal dementia FTDP-17 mutations on heparin-induced assembly of tau filaments, FEBS Lett., 1999, 450, 306–311
Nacharaju P., Lewis J., Easson C., Yen S., Hackett J., Hutton M., et al., Accelerated filament formation from tau protein with specific FTDP-17 missense mutations, FEBS Lett., 1999, 447, 195–199
Goedert M., Satumtira S., Jakes R., Smith M.J., Kamibayashi C., White C.L.3rd, et al., Reduced binding of protein phosphatase 2A to tau protein with frontotemporal dementia and parkinsonism linked to chromosome 17 mutations, J. Neurochem., 2000, 75, 2155–2162
Alonso A.D., Grundke-Iqbal I., Barra H.S., Iqbal K., Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubuleassociated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau, Proc. Natl. Acad. Sci. USA, 94, 1997, 298–303
Alonso A.C., Zaidi T., Novak M., Grundke-Iqbal I., Iqbal K., Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments and straight filaments, Proc. Natl. Acad. Sci. USA, 2001, 98, 6923–6928
Lee V.M., Goedert M., Trojanowski J.Q., Neurodegenerative tauopathies, Annu. Rev. Neurosci., 2001, 24, 1121–1159
Binder L.I., Guillozet-Bongaarts A.L., Garcia-Sierra F., Berry R.W., Tau, tangles, and Alzheimer’s disease, Biochim. Biophys. Acta, 2005, 1739, 216–223
Iqbal K.C., Alonso A., Chen S., Chohan M.O., El-Akkad E., Gong C.X., et al., Tau pathology in Alzheimer disease and other tauopathies, Biochim. Biophys. Acta, 2005, 1739, 198–210
Avila J., Tau phosphorylation and aggregation in Alzheimer’s disease pathology, FEBS Lett., 2006, 580, 2922–2927
Stoothoff W., Johnson G.V., Tau phosphorylation: physiological and pathological consequences, Biochim. Biophys. Acta, 2005, 1739, 280–297
Delacourte A., Sergeant N., Wattez A., Gauvreau D., Robitaille Y., Vulnerable neuronal subsets in Alzheimer’s and Pick’s disease are distinguished by their tau isoform distribution and phosphorylation, Ann. Neurol., 1998, 43, 193–204
Sergeant N., Wattez A., Delacourte A., Neurofibrillary degeneration in progressive supranuclear palsy and corticobasal degeneration: tau pathologies with exclusive “exon 10” isoforms, J. Neurochem., 1999, 72, 1243–1249
Hutton M., Lewis J., Dickson D., Yen S.H., McGowan E., Analysis of tauopathies with transgenic mice, Trends Mol. Med., 2001, 7, 467–470
Jakes R., Novak M., Davison M., Wischik C.M., Identification of 3- and 4-repeat tau isoforms within the PHF in Alzheimer’s disease, EMBO J., 1991, 10, 2725–2729
Crowther R.A., Olesen O.F., Smith M.J., Jakes R., Goedert M., Assembly of Alzheimer-like filaments from full-length tau protein, FEBS Lett., 1994, 337, 135–138
Brandt R., Leger J., Lee G., Interaction of tau with the neural plasma membrane mediated by tau’s amino-terminal projection domain, J. Cell Biol., 1995, 131, 1327–1340
Lee G., Newman S.T., Gard D.L., Band H., Panchamoorthy G., Tau interacts with src-family non-receptor tyrosine kinases, J. Cell Sci., 1998, 111, 3167–3177
Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., et al., Diffusible, nonfibrillar ligands derived from Abeta1–42 are potent central nervous system neurotoxins, Proc. Natl. Acad. Sci. USA, 1998, 95, 6448–6453
Lee G., Thangavel R., Sharma V.M., Litersky J.M., Bhaskar K., Fang S.M., et al., Phosphorylation of tau by fyn: implications for Alzheimer’s disease, J. Neurosci., 2004, 24, 2304–2312
Ho G.J., Hashimoto M., Adame A., Izu M., Alford M.F., Thal L.J., et al., Altered p59Fyn kinase expression accompanies disease progression in Alzheimer’s disease: implications for its functional role, Neurobiol. Aging, 2005, 26, 625–635
Arendt T., Holzer M., Grossmann A., Zedlick D., Bruckner M.K., Increased expression and subcellular translocation of the mitogen activated protein kinase kinase and mitogen-activated protein kinase in Alzheimer’s disease, Neuroscience, 1995, 68, 5–18
Vincent I., Jicha G., Rosado M., Dickson D.W., Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer’s disease brain, J. Neurosci., 1997, 17, 3588–3598
Vincent I., Zheng J., Dickson D.W., Kress Y., Davies P., Mitotic phosphoepitopes precede paired helical filaments in Alzheimer’s disease, Neurobiol. Aging, 1998, 19, 287–296
Yang Y., Mufson E.J., Herrup K., Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer’s disease, J. Neurosci., 2003, 23, 2557–2563
Nixon, R.A., Cataldo A.M., Paskevitch P. A., Hamilton D.J., Wheelock T.R., Kanaley-Andrews L., The lysosomal system in neurons: involvement at multiple stages in Alzheimer’s disease pathogenesis, Ann. NY Acad. Sci., 1992, 674, 65–88
Cataldo A.M., Barnett J.L., Berman S.A., Li J., Quarless S., Bursztajn S., et al., Gene expression and cellular content of cathepsin D in Alzheimer’s disease brain: evidence for early up-regulation of the endosomal-lysosomal system, Neuron, 1995, 14, 671–680
Yasojima K., Kuret J., DeMaggio A.J., McGeer E., McGeer P.L., Casein kinase 1 delta mRNA is upregulated in Alzheimer disease brain, Brain Res., 2000, 865, 116–120
Baumann K., Mandelkowa E.M., Biernata J., Piwnica-Wormsb H., Mandelkow E., Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin dependent kinases Cdk2 and Cdk5, FEBS Lett., 1993, 336, 417–424
Drewes G., Ebneth A., Preuss U., Mandelkow E.M., Mandelkow E., MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption, Cell, 1997, 89, 297–308
Yoshida H., Watanabe A., Ihara Y., Collapsin response mediator protein-2 is associated with neurofibrillary tangles in Alzheimer’s disease, J. Biol. Chem., 1998, 273, 9761–9768
de la Monte S.M., Ng S.C., Hsu D.W., Aberrant GAP-43 gene expression in Alzheimer’s disease, Am. J. Pathol., 1995, 147, 934–946
Caceres A., Kosik K.S., Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons, Nature, 1990, 343, 461–463
Mandell J., Banker G.A., A spatial gradient of tau protein phosphorylation in nascent axons, J. Neurosci., 1996, 16, 5727–5740
Biernat J., Mandelkow E.M., The development of cell processes induced by tau protein requires phosphorylation of Serine 262 and 356 in the repeat domain and is inhibited by phosphorylation in the proline-rich domains, Mol. Biol. Cell, 1999, 10, 727–740
Biernat J., Wu Y.Z., Timm T., Zheng-Fischöfer Q., Mandelkow E., Meijer L., et al., Protein kinase MARK/PAR-1 is required for neurite outgrowth and establishment of neuronal polarity, Mol. Biol. Cell, 2002, 13, 4013–4028
Belkadi A., LoPresti P., Truncated tau with the Fyn-binding domain and without the microtubule-binding domain hinders the myelinating capacity of an oligodendrocyte cell line, J. Neurochem., 2008, 107, 351–360
Takei Y., Teng J., Harada A., Hirokawa N., Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes, J. Cell Biol., 2000, 150, 989–1000
Corsellis J.A., Brierley J.B., Observations on the pathology of insidious dementia following head injury, J. Ment. Sci., 1959, 105, 714–720
Corsellis J.A., Bruton C.J., Freeman-Browne D., The aftermath of boxing, Psychol. Med., 1973, 3, 270–303
McKee A.C., Cantu R.C., Nowinski C.J., Hedley-Whyte E.T., Gavett B.E., Budson A.E., et al., Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury, J. Neuropathol. Exp. Neurol., 2009, 68, 709–735
Rapoport M., Dawson H.N., Binder L.I., Vitek M.P., Ferreira A., Tau is essential to beta-amyloid-induced neurotoxicity, Proc. Natl. Acad. Sci. USA, 2002, 99, 6364–6369
King M.E., Kan H., Baas P.W., Erisir A., Glabe C., Bloom G.S., Taudependent microtubule disassembly initiated by prefibrillar betaamyloid, J. Cell Biol., 2006, 175, 541–546
Götz J., Probst A., Spillatini M.G., Schäfer T., Jakes R., Bürki K., et al., Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform, EMBO J., 1995, 14, 1304–1313
Brion J.P., Tremp G., Octave J.N., Transgenic expression of the shortest human tau affects its compartmentalization and its phosphorylation as in the pretangle stage of Alzheimer’s disease, Am. J. Pathol., 1999, 54, 255–270
Hong M., Zhukareva V., Vogelsberg-Ragaglia V., Wszolek Z., Reed L., Miller B.I., et al., Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17, Science, 1998, 282, 1914–1917
DeTure M., Ko L.W., Yen S., Nacharaju P., Easson C., Lewis J., et al., Missense tau mutations identified in FTDP-17 have a small effect on tau-microtubule interactions, Brain Res., 2000, 853, 5–14
Harada A., Oguchi K., Okabe S., Kuno J., Terada S., Ohshima T., et al., Altered microtubule organization in small-calibre axons of mice lacking tau protein, Nature, 1994, 369, 488–491
Tint I., Slaughter T., Fischer I., Black M.M., Acute inactivation of tau has no effect on dynamics of microtubules in growing axons of cultured sympathetic neurons, J. Neurosci., 1998, 18, 8660–8673
Amadoro G., Serafino A.L., Barbato C., Ciotti M.T., Sacco A., Calissano P., et al., Role of N-terminal tau domain integrity on the survival of cerebellar granule neurons, Cell. Death Differ., 2004, 11, 217–230
Amadoro G., Ciotti M.T., Costanzi M., Cestari V., Calissano P., Canu N., NMDA receptor mediates tau-induced neurotoxicity by calpain and ERK/MAPK activation, Proc. Natl. Acad. Sci. USA, 2006, 103, 2892–2897
Corsetti V., Amadoro G., Gentile A., Capsoni S., Ciotti M.T., Cencioni M.T., et al., Identification of a caspase-derived N-terminal tau fragment in cellular and animal Alzheimer’s disease models, Mol. Cell. Neurosci., 2008, 38, 381–392
Horowitz P.M., LaPointe N., Guillozet-Bongaarts A.L., Berry R.W., Binder L.I., N-terminal fragments of tau inhibit full-length tau polymerization in vitro, Biochemistry, 2006, 45, 12859–12866
Gamblin T.C., Berry R.W., Binder L.I., Tau polymerization: role of the amino terminus, Biochemistry, 2003, 42, 2252–2257
Yin H., Kuret J., C-terminal truncation modulates both nucleation and extension phases of tau fibrillization, FEBS Lett., 2006, 580, 211–215
Zilka N., Filipcik P., Koson P., Fialova L., Skrabana R., Zilkova M., et al., Truncated tau from sporadic Alzheimer’s disease suffices to drive neurofibrillary degeneration in vivo, FEBS Lett., 2006, 580, 3582–3588
Abraha A., Ghoshal N., Gamblin T. C., Cryns V., Berry R.W., Kuret J., et al., C-terminal inhibition of tau assembly in vitro and in Alzheimer’s disease, J. Cell Sci., 2000, 113, 3737–3745
Wang Y.P., Biernat J., Pickhardt M., Mandelkow E., Mandelkow E.M., Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model, Proc. Natl. Acad. Sci. USA, 2007, 104, 10252–10257
Guillozet-Bongaarts A.L., Garcia-Sierra F., Reynolds M.R., Horowitz P.M., Fu Y., Wang T., et al., Tau truncation during neurofibrillary tangle evolution in Alzheimer’s disease, Neurobiol. Aging, 2005, 26, 1015–22
Roberson E.D., Scearce-Levie K., Palop J.J., Yan F., Cheng I.H., Wu T., et al., Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer’s disease mouse model, Science, 2007, 316, 750–754
Folwell J., Cowan C.M., Ubhi K.K., Shiabh H., Newman T.A., Shepherd D., et al., Aβ exacerbates the neuronal dysfunction caused by human tau expression in a Drosophila model of Alzheimer’s disease, Exp. Neurol., 2009, 223, 401–409
Mudher A., Lovestone S., Alzheimer’s disease-do tauists and baptists finally shake hands?, Trends Neurosci., 2002, 25, 22–26
He H.J., Wang X.S., Pan R., Wang D.L., Liu M.N., He R.Q., The proline rich domain of tau plays a role in interactions with actin, BMC Cell Biol., 2009, 10, 81–93
Perez M., Valpuesta J.M., Medina M., Montejo de Garcini E., J. Avila, Polymerization of tau into filaments in the presence of heparin: the minimal sequence required for tau-tau interaction, J. Neurochem., 1996, 67, 1183–1190
Magnani E., Fan J., Gasparini L., Golding M., Williams M., Schiavo G., et al., Interaction of tau protein with the dynactin complex, EMBO J., 2007, 26, 4546–4554
Fulga T.A., Elson-Schwab I., Khurana V., Steinhilb M.L., Spires T.L., Hyman B.T., et al., Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo, Nat. Cell Biol., 2007, 9, 139–148
Blard O., Feuillette S., Bou J., Chaumette B., Frebourg T., Campion D., et al., Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila, Hum. Mol. Genet., 2007, 16, 555–566
Lee G., Tau and src family tyrosine kinases, Biochim. Biophys. Acta, 2005, 1739, 323–330
Lu P.J., Wulf G., Zhou X.Z., Davies P., Lu K.P., The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein, Nature, 1999, 399, 784–788
Dickey C.A., Yue M., Lin W.L., Dickson D.W., Dunmore J.H., Lee W.C., et al., Deletion of the ubiquitin ligase CHIP leads to the accumulation, but not the aggregation, of both endogenous phospho- and caspase-3-cleaved tau species, J. Neurosci., 2006, 26, 6985–6996
Sarkar M., Kuret J., Lee G., Two motifs within the tau microtubule binding domain mediate its association with the hsc70 molecular chaperone, J. Neurosci. Res., 2008, 86, 2763–2773
Makrides V., Shen T.E., Bhatia R., Smith B.L., Thimm, J., Lal, R., et al., Microtubule-dependent oligomerization of tau, Implications for physiological tau function and tauopathies, J. Biol. Chem., 2003, 278, 33298–33304
Wang J.Z., Grundke-Iqbal I., Iqbal K., Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration, Eur. J. Neurosci., 2007, 25, 59–68
Samsonov A., Yu J.Z., Rasenick M., Popov S.V., Tau interaction with microtubules in vivo, J. Cell Sci., 2004, 117,25, 6129–6141
Mocanu M.M., Nissen A., Eckermann K., Khlistunova I., Biernat J., Drexler D., et al., The potential for beta-structure in the repeat domain of tau protein determines aggregation, synaptic decay, neuronal loss, and coassembly with endogenous Tau in inducible mouse models of tauopathy, J. Neurosci., 2008, 28, 737–748
Nixon, R.A., Endosome function and dysfunction in Alzheimer’s disease and other neurodegenerative diseases, Neurobiol. Aging, 2005, 26, 373–382
Nixon R.A., Wegiel J., Kumar A., Yu W.H., Peterhoff C., Cataldo A., et al., Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study, J. Neuropathol. Exp. Neurol., 2005, 64, 120–122
Boland B.A., Kumar A., Lee F.M., Platt J., Wegiel J., Yu W.H., et al., Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer’s disease, J. Neurosci., 2008, 28, 6926–6937
Park S.Y., Ferreira A., The generation of a 17 kDa neurotoxic fragment: an alternative mechanism by which tau mediates beta-amyloidinduced neurodegeneration, J. Neurosci., 2005, 25, 5365–5375
Gomez-Ramos A., Diaz-Hernandez M., Cuadros R., Hernandez F., Avila J., Extracellular tau is toxic to neuronal cells, FEBS Lett., 2006, 580, 4842–4850
Gómez-Ramos A., Díaz-Hernández M., Rubio A., Miras-Portugal M.T., Avila J., Extracellular tau promotes intracellular calcium increase through M1 and M3 muscarinic receptors in neuronal cells, Mol. Cell. Neurosci., 2008, 37, 673–681
Braak E., Braak H., Mandelkow E.M., A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads, Acta Neuropathol., 1994, 87, 554–567
Santacruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., et al., Tau suppression in a neurodegenerative mouse model improves memory function, Science, 2005, 309, 476–481
Berger Z., Roder H., Hanna A., Carlson A., Rangachari V., Yue M., et al., Accumulation of pathological tau species and memory loss in a conditional model of tauopathy, J. Neurosci., 2007, 27, 3650–3662
Hall G.F., Chu B., Lee G., Yao J., Human tau filaments induce microtubule and synapse loss in vertebrate central neurons, J. Cell Sci., 2000, 120, 1373–1387
Wittmann C.W., Wszolek M.F., Shulman J.M., Salvaterra P.M., Lewis J., Hutton M., et al., Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles, Science, 2001, 293, 5530, 711–714
Lee S., Jung C., Lee G, Hall G.F., Tauopathy mutants P301L, G272V, R406W and V337M accelerate neurodegeneration in the lamprey in situ cellular tauopathy model, J. Alzheimers Dis., 2009, 16, 99–111
Yeh P., Chang C., Phosphorylation alters tau distribution and elongates life span in Drosophila, J. Alzheimers Dis., 2010, 21, 543–556
Chatterjee S., Sang T.K., Lawless G.M., Jackson G.R., Dissociation of tau toxicity and phosphorylation: role of GSK-3beta, MARK and Cdk5 in a Drosophila model, Hum. Mol. Genet., 2009, 18, 164–177
Maeda S., Sahara N., Saito Y., Murayama M., Yoshiike Y., Kim H., et al., Granular tau oligomers as intermediates of tau filaments, Biochemistry, 46, 3856–3861
Maeda S., Sahara N., Saito Y., Murayama S., Ikai A., Takashima A., Increased levels of granular tau oligomers: an early sign of brain aging and Alzheimer’s disease, Neurosci. Res., 2006, 54, 197–201
Sahara N., Maeda S., Takashima A., Tau oligomerization: a role for tau aggregation intermediates linked to neurodegeneration, Curr. Alz. Res., 2008, 5, 591–598
Bretteville A., Planel E., Tau aggregates: toxic, inert, or protective species?, J. Alzheimers Dis., 2008, 14, 431–436
Patterson K.C., Remmer Y., Fu S., Brooker N., Kanaan L., Vana S., et al., Characterization of prefibrillar tau oligomers in vitro and in Alzheimer disease, J. Biol. Chem., 2011, 286, 23063–23076
Iliev A.I., Ganesan S., Bunt G., Wouters F.S., Removal of patternbreaking sequences in microtubule binding repeats produces instantaneous tau aggregation and toxicity, J. Biol. Chem., 2006, 281, 37195–37204
Lasagna-Reeves C.A., Castillo-Carranza D.L., Guerrero-Muoz M.J., Jackson G.R., Kayed R., Preparation and characterization of neurotoxic tau oligomers, Biochemistry, 2010, 49, 10039–10041
Andorfer C., Acker C.M., Kress Y., Hof P.R., Duff K., Davies P., Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms, J. Neurosci., 2005, 225, 5446–5545
Ambegaokar S., Jackson G., Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation, Hum. Mol. Genet., 2011, 20, 4947–4977
Pei J.J., Grundke-Iqbal I., Iqbal K., Bogdanovic N., Winblad B., Cowburn R.F., Accumulation of cyclin-dependent kinase 5 (cdk5) in neurons with early stages of Alzheimer’s disease neurofibrillary degeneration, Brain Res., 1998, 797, 267–277
Stone J.G., Siedlak S.L., Tabaton M., Hirano A., Castellani R.J., Santocanale C., et al., The cell cycle regulator phosphorylated retinoblastoma protein is associated with tau pathology in several tauopathies, J. Neuropathol. Exp. Neurol., 2011, 70, 578–587
Morsch R., Simon W., Coleman P.D., Neurons may live for decades with neurofibrillary tangles, J. Neuropathol. Exp. Neurol., 1999, 58, 188–197
Bobinski M., Wegiel J., Tarnawski M., Bobinski M., Reisberg B., de Leon M.J., et al., Relationships between regional neuronal loss and neurofibrillary changes in the hippocampal formation and duration and severity of Alzheimer disease, J. Neuropathol. Exp. Neurol., 1997, 56, 414–420
Müller W., Eckert A., Kurz C., Eckert G., Leuner K., Mitochondrial dysfunction: common final pathway in brain aging and Alzheimer’s disease — therapeutic aspects, Mol. Neurobiol., 2010, 41, 159–171
Swerdlow R.H., Khan S.M., A “mitochondrial cascade hypothesis” for sporadic Alzheimer’s disease, Med. Hypotheses, 2004, 63, 8–20
Fang Y., Wu N., Gan X., Yan W., Morrell J. C., Gould, S.J., Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes, PLoS Biol., 2007, 5, e158
Vega I.E., Cui L., Propst J.A., Hutton M.L., Lee G., Yen S.H., Increase in tau tyrosine phosphorylation correlates with the formation of tau aggregates, Mol. Brain Res., 2005, 138, 135–144
Sverdlov M., Shajahan A.N., Minshall R.D., Tyrosine phosphorylationdependence of caveolae-mediated endocytosis, J. Cell. Mol. Med., 2007, 11, 1239–1250
Saman S., Kim W., Raya M., Visnick Y., Miro S., Saman S., et al., Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease, J. Biol. Chem., 2012, 287, 3842–3849
Zehe C., Engling A., Wegehingel S., Schäfer T., Nickel W., Cell-surface heparan sulfate proteoglycans are essential components of the unconventional export machinery of FGF-2, Proc. Natl. Acad. Sci. USA, 2006, 103, 15479–15484
Goedert M., Jakes R., Spillantini M.G., Hasegawa M., Smith M.J., Crowther R.A., Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans, Nature, 1996, 383, 550–553
Gray E.G., Paula-Barbosa M., Roher A., Alzheimer’s disease: paired helical filaments and cytomembranes, Neuropathol. Appl. Neurobiol., 1987, 13, 91–110
Fath T., Eidenmüller J., Brandt R., Tau-mediated cytotoxicity in a pseudohyperphosphorylation model of Alzheimer’s disease, J. Neurosci., 2002, 22, 9733–9741
Barré P., Eliezer D., Folding of the repeat domain of tau upon binding to lipid surfaces, J. Mol. Biol., 2006, 362, 312–326
Wilson D.M., Binder, L.I., Free fatty acids stimulate the polymerization of tau and amyloid beta peptides, Am. J. Pathol., 1997, 161, 2321–2335
Chirita C.N., Necula M., Kuret J., Anionic micelles and vesicles induce tau fibrillization in vitro, J. Biol. Chem., 2003, 278, 25644–25650
Kampers T., Friedhoff P., Biernat J., Mandelkow E.M., RNA stimulates aggregation of microtubule-associated protein-tau into Alzheimerlike paired helical filaments, FEBS Lett., 1997, 399, 344–349
Hall G.F., What is the common link between protein aggregation and interneuronal lesion propagation in neurodegenerative disease?, In: Chang R. (Ed.) Neurodegenerative diseases — processes, prevention, protection and monitoring, InTech, 2011, 1–17
Farah C.A., Perreault S., Liazoghli D., Desjardins M., Anton A., Lauzon M., et al., Tau interacts with Golgi membranes and mediates their association with microtubules, Cell Motil. Cytoskeleton, 2006, 63, 710–724
Liazoghli D., Perreault S., Micheva K.D., Desjardins M., Leclerc N., Fragmentation of the Golgi apparatus induced by overexpression of WT and mutant human tau forms in neurons, Am. J. Pathol., 2005, 166, 1499–1514
Kim W., Lee S., Hall G.F., Secretion of human tau fragments resembling CSF-tau in Alzheimer’s disease is modulated by the presence of the exon 2 insert, FEBS Lett., 2010, 584, 3085–3088
Lee S., Kim W., Li Z., Hall G.F., Accumulation of vesicle-associated human tau in distal dendrites drives degeneration and tau secretion in an in situ cellular tauopathy model, Int. J. Alzheimers Dis., 2012, 172837
Hamano T., Gendron T.F., Causevic E., Yen S.H., Lin W.L., Isidoro C., et al., Autophagic-lysosomal perturbation enhances tau aggregation in transfectants with induced wild-type tau expression, Eur. J. Neurosci., 2008, 27, 1119–11130
Abrahamsen H., Stenmark H., Protein secretion: unconventional exit by exophagy, Curr. Biol., 2011, 20, R415–R418
Funk K., Kuret J., Lysosomal fusion dysfunction as a unifying hypothesis for Alzheimer’s disease pathology, Int. J. Alzheimers Dis., 2012, 752894
Clavaguera F., Bolmont T., Crowther R.A., Abramowski D., Frank S., Probst A., et al., Transmission and spreading of tauopathy in transgenic mouse brain, Nat. Cell Biol., 2009, 11, 909–913
Liu L., Drouet V., Wu J.W., Witter M.P., Small S.A., Clell C., et al., Trans-synaptic spread of tau pathology in vivo, PloS One, 2012, 7, e31302
deCalignon A., Polydoro M., Suárez-Calvet M., William C., Adamowicz D.H., Kopeikina K.J., et al., Propagation of tau pathology in a model of early Alzheimer’s disease, Neuron, 2012, 73, 685–697
Morrison J.H., Hof P.R. Selective vulnerability of corticocortical and hippocampal circuits in aging and Alzheimer’s disease, Prog. Brain Res., 2002, 136, 467–486
Ko L.W., Rush T., Sahara N., Kersh J.S., Easson C., Deture M., et al., Assembly of filamentous tau aggregates in human neuronal cells, J. Alzheimers Dis., 2004, 6, 605–622
http://www.alzgene.org/
Jensen L.J., Kuhn M., Stark M., Chaffron S., Creevey C. Muller J., et al., STRING 8 — a global view on proteins and their functional interactions in 630 organisms, Nucleic Acids Res., 2009, 37(Database issue), D412–D416
Mathivanan S., Fahner C.J., Reid G.E., Simpson R.J., ExoCarta, 2012, database of exosomal proteins, RNA and lipids, Nucleic Acids Res., 2012, 40(Database issue), D1241–1244
Hall G.F., Lee S., Yao J., Neurofibrillary degeneration can be arrested in an in vivo cellular model of human tauopathy by application of a compound which inhibits tau filament formation in vitro, J. Mol. Neurosci., 2002, 19, 253–260
Kim W., Lee S., Jung C., Ahmed A., Lee G., Hall G.F., Interneuronal transfer of human tau between lamprey central neurons in situ, J. Alzheimers Dis., 2010, 19, 647–664
Le M.N., Kim W., Lee S., McKee A.C., Hall G.F., Multiple mechanisms of extracellular tau spreading in a non-transgenic tauopathy model, Am. J. Neurodegener. Dis., 2012, 1, 316–333
Hall G.F., Saman S., Secretion or death? What is the significance of elevated CSF-tau in early AD?, Comm. Integr. Biol., 2012, 5, 1–4
Frost B., Jacks R.L., Diamond M.I., Propagation of tau misfolding from the outside to the inside of a cell, J. Biol. Chem., 2009, 284, 12845–12852
Honson N.S., Jensen J.R., Abraha A., Hall G.F., Kuret J., Small-molecule mediated neuroprotection in an in situ model of tauopathy, Neurotox. Res., 2009, 15, 274–283
Rajendran L., Honsho M., Zahn T.R., Keller P., Geiger K.D., Verkade P., et al., Alzheimer’s disease beta-amyloid peptides are released in association with exosomes, Proc. Natl. Acad. Sci. USA, 2006, 103, 11242–11247
Emmanouilidou E., Melachroinou K., Roumeliotis T., Garbis S.D., Ntzouni M., Margaritis L.H., et al., Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival, J. Neurosci., 2010, 30, 6838–6851
Fevrier B., Vilette D., Archer F., Loew D., Faigle W., Vidal M., et al., Cells release prions in association with exosomes, Proc. Natl. Acad. Sci. USA, 2004, 101, 9683–9688
Soto C., Estrada L., Protein misfolding and neurodegeneration, Arch. Neurol., 2008, 65, 184–189
Aguzzi A., Sigurdson C., Heikenwaelder M., Molecular mechanisms of prion pathogenesis, Annu. Rev. Pathol., 3, 11–40
Novak P., Prcina M., Kontsekova E., Tauons and prions: infamous cousins?, J. Alzheimers Dis., 2011, 26, 413–430
Su J.H., Deng G., Cotman C.W., Transneuronal degeneration in the spread of Alzheimer’s disease pathology: immunohistochemical evidence for the transmission of tau hyperphosphorylation, Neurobiol. Dis., 1997, 4, 365–375
Armstrong R.A., Cairns N.J., Lantos P.L., Clustering of cerebral cortical lesions in patients with corticobasal degeneration, Neurosci. Lett., 1999, 268, 5–8
Armstrong R.A., Cairns N.J., Lantos P.L., Clustering of Pick bodies in Pick’s disease, Neurosci. Lett., 1998, 242, 81–84
Armstrong R.A., Cairns N.J., Lantos P.L., What does the study of spatial patterns tell us about the pathogenesis of neurodegenerative disorders?, Neuropathology, 2001, 21, 1–12
McKee A.C., Stern R.A., Nowinski C., Stein T., Alvarez V.E., Daneshvar D., et al., The spectrum of disease in chronic traumatic encephalopathy, Brain, 2013, 136, 43–64
Guo J.L., Lee V.M.Y., Seeding of normal tau by pathological tau conformers drives pathogenesis of Alzheimer-like tangles, J. Biol. Chem., 2011, 286, 15317–15331
Kfoury N., Holmes B.B., Jiang H., Holtzman D.M., Diamond M.I., Transcellular propagation of tau aggregation by fibrillar species, J. Biol. Chem., 2012, 287, 19440–19451
Wu J.W., Herman M., Liu L., Simoes S., Acker C.M., Figueroa H., et al., Small misfolded tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons, J. Biol. Chem., 2013, 288, 1856–1870
Iba M., Guo J.L., McBride J.D., Zhang B., Trojanowski J.Q., Lee V.M., Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer’s-like tauopathy, J. Neurosci., 2013, 33, 1024–1037
Lasagna-Reeves C.A., Castillo-Carranza D.L., Sengupta U., Guerrero-Munoz M.J., Kiritoshi T., Neugebauer V., et al., Alzheimer brainderived tau oligomers propagate pathology from endogenous tau, Sci. Rep., 2012, 2, 700
Hall G.F., Patuto B.A., Is tau now ready for admission to the prion club?, Prion, 2012, 6, 223–233
Canu N., Filesi I., Pristerà A., Ciotti M.T., Biocca S., Altered intracellular distribution of PrPC and impairment of proteasome activity in tau overexpressing cortical neurons, J. Alzheimers Dis., 2011, 27, 603–613
Litman P., Barg J., Rindzoonski L., Ginzburg I., Subcellular localization of tau mRNA in differentiating neuronal cell culture: Implications for neuronal polarity, Neuron, 1993, 10, 627–638
Aronov S., Aranda G., Behar L., Ginzberg I., Axonal tau mRNA localization coincides with tau protein in living neuronal cells and depends on axonal targetting signal, J. Neurosci., 2001, 21, 6577–6587
Schraen-Maschke S., Dhaenens C.M., Delacourte A., Sablonniere B., Microtubule-associated protein tau gene: a risk factor in human neurodegenerative diseases, Neurobiol. Dis., 2004, 15, 449–460
Caffrey T, Joachim C., Wade-Martins R., Haplotype-specific expression of the N-terminal exons 2 and 3 at the human MAPT locus, Neurobiol. Aging, 2008, 29, 1923–1929
Wegiel J., Gong C.X., Hwang Y.W., The role of DYRK1A in neurodegenerative diseases, FEBS J., 2011, 278, 236–245
McNaughton D., et al., Duplication of amyloid precursor protein (APP), but not prion protein (PRNP) gene is a significant cause of early onset dementia in a large UK series, Neurobiol. Aging, 2012, 33, 426.e13–e21
Mac Donald C.L., Johnson A.M., Cooper D., Nelson E.C., Werner N.J., Shimony J.S, et al., Detection of blast-related traumatic brain injury in U.S. military personnel, N. Engl. J. Med., 2011, 364, 2091–2100
Hall G.F., Poulos A., Cohen M.J., Sprouts emerging from the dendrites of axotomized lamprey central neurons have axonlike ultrastructure, J. Neurosci., 1989, 9, 588–599
Hall G.F., Yao J., Selzer M., Kosik K.S., Cytoskeletal correlates to cell polarity loss following axotomy of lamprey central neurons, J. Neurocytol., 1997, 26, 733–753
Rose P.K., MacDermid V., Joshi M., Neuber-Hess M., Emergence of axons from distal dendrites of adult mammalian neurons following a permanent axotomy, Eur. J. Neurosci., 2001, 13, 1166–1176
Singleton R.H., Zhu J., Stone J.R., Povlishock J.T., Traumatically induced axotomy adjacent to the soma does not result in acute neuronal death, J. Neurosci., 2002, 22, 791–802
Amadoro G., Corsetti V., Stringaro A., Colone M., D’Aguanno S., Meli G., et al., A NH2 tau fragment targets neuronal mitochondria at AD synapses: possible implications for neurodegeneration, J. Alzheimers Dis., 2010, 21, 445–470
Thies E., Mandelkow E.M., Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1, J. Neurosci., 2007, 27, 2896–2907
Kins S., Crameri A., Evans D.R., Hemmings B.A., Nitsch R.M., Götz J., Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice, J. Biol. Chem., 2001, 276, 38193–38200
Lazarov O., Lee M., Peterson D.A., Sisodia S.S.,Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice, J. Neurosci., 2002, 22, 9785–9793
Klein W.L., Synaptic targeting by Abeta oligomers (ADDLS) as a basis for memory loss in early Alzheimer’s disease, Alzheimers Dement., 2006, 2, 43–55
Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., et al., Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo, Nature, 2002, 416, 535–539
Tsai J., Grutzendler J., Duff K., Gan W.B., Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches, Nat. Neurosci., 2004, 7, 1181–1183
Boekhoorn K., Terwel D., Biemans B., Borghgraef P., Wiegert O., Ramakers G.J., et al., Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy, J. Neurosci., 2006, 26, 3514–3523
Zempel H., Thies E., Mandelkow E., Mandelkow E.M., A beta oligomers cause localized Ca2+ elevation, missorting of endogenous tau into dendrites, tau phosphorylation, and endogenous tau into dendrites, tau phosphorylation, and destruction of microtubules and spines, J. Neurosci., 2010, 30, 11938–11950
Ittner L.M., Ke Y.D., Delerue F., Bi M., Gladbach A., van Eersel J., et al., Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer’s disease mouse models, Cell, 2010, 142, 387–397
Tackenberg C., Brandt R., Divergent pathways mediate spine alterations and cell death induced by amyloid-beta, wild-type tau, and R406W tau, J. Neurosci., 2009, 29, 14439–14450
Luebke J.I., Weaver C.M., Rocher A.B., Rodriguez A., Crimins J.L., Dickstein D.L., et al., Dendritic vulnerability in neurodegenerative disease: insights from analyses of cortical pyramidal neurons in transgenic mouse models, Brain Struct. Funct., 2010, 214, 181–199
Boekhoorn K., Joels M., Lucassen P.J., Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus, Neurobiol. Dis., 24, 1–14, 2006
Hu W.T., Holtzman D.M., Fagan A.M., Shaw L.M., Perrin R., Arnold S.E., et al., Plasma multianalyte profiling in mild cognitive impairment and Alzheimer disease, Neurology, 2012, 79, 897–905
Clinton L.K., Blurton-Jones M., Myczek K., Trojanowski J.Q., LaFerla F.M., Synergistic interactions between Abeta, tau, and alphasynuclein: acceleration of neuropathology and cognitive decline, J. Neurosci., 2010, 30, 7281–7289
Perry G., Kawai M., Tabaton M., Onorato M., Mulvihill P., Richey P., et al., Neuropil threads of Alzheimer’s disease show a marked alteration of the normal cytoskeleton, J. Neurosci., 1991, 11, 1748–1755
Ihara Y., Massive somatodendritic sprouting of cortical neurons in Alzheimer’s Disease, Brain Res., 1988, 459, 138–144
Uchida Y., Ohshima T., Sasaki Y., Suzuki H., Yanai S., Yamashita N., et al., Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer’s disease, Genes Cells, 2005, 10, 165–179
Arimura N., Kaibuchi K., Neuronal polarity: from extracellular signals to intracellular mechanisms, Nat. Rev. Neurosci., 2007, 8, 194–205
Leugers C.J., Lee G., Tau potentiates nerve growth factor-induced mitogen-activated protein kinase signaling and neurite initiation without a requirement for microtubule binding, J. Biol. Chem., 2010, 285, 19125–19134
Cowan C.M., Shepherd D., Mudher A., Insights from Drosophila models of Alzheimer’s disease, Biochem. Soc. Trans., 2010, 38,4, 988–992
Mudher A., Shepherd D., Newman T.A., Mildren P., Jukes J.P., Squire A., et al., GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila, Mol. Psychiatry, 2004, 9, 522–530
Khurana V., Feany M.B., Connecting cell-cycle activation to neurodegeneration in Drosophila, Biochim. Biophys. Acta, 2007, 1772, 446–456
Hall G.F., The biology and pathobiology of tau protein, In: Kavallaris M. (Ed.), The cytoskeleton and human disease, Springer, 2012, 285–313
Tian A.G., Deng W.M., Par-1 and tau regulate the anterior-posterior gradient of microtubules in Drosophila oocytes, Dev. Biol., 2009, 327, 458–464
Li S., Mallory M., Alford M., Tanaka S., Masliah E., Glutamate transporter alterations in Alzheimer disease are possibly associated with abnormal APP expression, J. Neuropathol. Exp. Neurol., 1997, 56, 901–911
Gorlovoy P., Larionov S., Pham T.T.H., Neumann H., Accumulation of tau induced in neurites by microglial proinflammatory mediators, FASEB J., 2009, 23, 2502–2513
Maxwell W.L., McCreath B.J., Graham D.I., Gennarelli T.A., Cytochemical evidence for redistribution of membrane pump calcium-ATPase and ecto-Ca-ATPase activity, and calcium influx in myelinated nerve fibres of the optic nerve after stretch injury, J. Neurocytol., 1995, 24, 925–42
Jafari S.S., Maxwell W.L., Neilson M., Graham D.I., Axonal cytoskeletal changes after non-disruptive axonal injury, J. Neurocytol., 1997, 26, 207–221
Uryu K., Chen X.H., Martinez D., Browne K.D., Johnson V.E., Graham D.I., et al., Multiple proteins implicated in neurodegenerative diseases accumulate in axons after brain trauma in humans, Exp. Neurol., 2007, 208, 185–192
Goldstein L.G., Fisher A., Tagge C., Wojnarowicz M.W., Zhang X.L., Sullivan J.S., et al., Blast exposure induces chronic traumatic encephalopathy and persistent defects in axonal conduction, synaptic plasticity, and hippocampal memory, Sci. Transl. Med., 2012, 4, 134ra60
Iijima-Ando K., Sekiya M., Maruko-Otake A., Ohtake Y., Suzuki E., Lu B., et al., Loss of axonal mitochondria promotes taumediated neurodegeneration and Alzheimer’s diseaserelated tau phosphorylation via PAR-1, PLoS Genet., 2012, 8, e1002918
Craig A.M., Graf E.R., Linhoff M.W., How to build a central synapse: clues from cell culture, Trends Neurosci., 2006, 29, 8–20
Perez M.R., Zheng H., Lex H., Van der Ploeg T., Koo E., The betaamyloid precursor protein of Alzheimer’s disease enhances neuron viability and modulates neuronal polarity, J. Neurosci., 1997, 17, 9407–9414
LaPointe N.E., Morfini G., Pigino G., Gaisina I.N., Kozikowski A.P., Binder L.I., et al., The amino terminus of tau inhibits kinesin dependent axonal transport: implications for filament toxicity, J. Neurosci. Res., 2009, 87, 440–451
Pérez M., Cuadros R., Benítez M.J., Jiménez J.S., Interaction of Alzheimer’s disease amyloid ß peptide fragment 25–35 with tau protein, and with a tau peptide containing the microtubule binding domain, J. Alzheimers Dis., 2004, 6, 461–467
Rank K.B., Pauley A.M., Bhattacharya K., Wang Z., Evans D.B., Fleck T.J., et al., Direct interaction of soluble human recombinant tau protein with Abeta 1–42 results in tau aggregation and hyperphosphorylation by tau protein kinase II, FEBS Lett., 2002, 514, 263–268
Guo J.T., Arai J., Miklossy J., McGeer P., Tau forms soluble complexes that may promote self aggregation of both into the insoluble forms observed in Alzheimer’s disease, Proc. Natl. Acad. Sci. USA, 2006, 103, 1953–1958
Funk K.E., Mrak R.E., Kuret J., Granulovacuolar degeneration (GVD) bodies of Alzheimer’s disease (AD) resemble late-stage autophagic organelles, Neuropathol. Appl. Neurobiol., 2011, 37, 295–306