Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Translational Neuroscience

Editor-in-Chief: David, Olivier

1 Issue per year

IMPACT FACTOR 2017: 0.833
5-year IMPACT FACTOR: 1.247

CiteScore 2017: 1.00

SCImago Journal Rank (SJR) 2017: 0.428
Source Normalized Impact per Paper (SNIP) 2017: 0.244

Open Access
See all formats and pricing
More options …

Tau-mediated synaptic damage in Alzheimer’s disease

Santosh Jadhav
  • Institute of Neuroimmunology, Slovak Academy of Sciences, Centre of Excellence for Alzheimer’s Disease and Related Disorders, Dubravska 9, 845 10 Bratislava, Slovak Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Veronika Cubinkova
  • Institute of Neuroimmunology, Slovak Academy of Sciences, Centre of Excellence for Alzheimer’s Disease and Related Disorders, Dubravska 9, 845 10 Bratislava, Slovak Republic
  • Axon Neuroscience SE, Grosslingova 45, Bratislava, Slovak Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Ivana Zimova
  • Institute of Neuroimmunology, Slovak Academy of Sciences, Centre of Excellence for Alzheimer’s Disease and Related Disorders, Dubravska 9, 845 10 Bratislava, Slovak Republic
  • Axon Neuroscience SE, Grosslingova 45, Bratislava, Slovak Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Veronika Brezovakova
  • Institute of Neuroimmunology, Slovak Academy of Sciences, Centre of Excellence for Alzheimer’s Disease and Related Disorders, Dubravska 9, 845 10 Bratislava, Slovak Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Aladar Madari
  • Small animal clinic, University of Veterinary Medicine and Pharmacy, Komenskeho 73, Kosice, Slovak Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Viera Cigankova
  • Department of Anatomy, Histology and Physiology, University of Veterinary Medicine and Pharmacy, Komenskeho 73, 041 81 Kosice, Slovak Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Norbert Zilka
  • Institute of Neuroimmunology, Slovak Academy of Sciences, Centre of Excellence for Alzheimer’s Disease and Related Disorders, Dubravska 9, 845 10 Bratislava, Slovak Republic
  • Axon Neuroscience SE, Grosslingova 45, Bratislava, Slovak Republic
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2015-10-23 | DOI: https://doi.org/10.1515/tnsci-2015-0023


Synapses are the principal sites for chemical communication between neurons and are essential for performing the dynamic functions of the brain. In Alzheimer’s disease and related tauopathies, synapses are exposed to disease modified protein tau, which may cause the loss of synaptic contacts that culminate in dementia. In recent decades, structural, transcriptomic and proteomic studies suggest that Alzheimer’s disease represents a synaptic disorder. Tau neurofibrillary pathology and synaptic loss correlate well with cognitive impairment in these disorders. Moreover, regional distribution and the load of neurofibrillary lesions parallel the distribution of the synaptic loss. Several transgenic models of tauopathy expressing various forms of tau protein exhibit structural synaptic deficits. The pathological tau proteins cause the dysregulation of synaptic proteome and lead to the functional abnormalities of synaptic transmission. A large body of evidence suggests that tau protein plays a key role in the synaptic impairment of human tauopathies.

Keywords: Alzheimer’s disease; Synaptic loss; Tau protein; Neurofibrillary degeneration; Tauopathies; Tau mislocalization; Transgenic models


  • [1] Bliss T.V.P., Collingridge G.L., A synaptic model of memory: long-term potentiation in the hippocampus, Nature, 1993, 361, 31-39 Google Scholar

  • [2] Honer W.G., Dickson D.W., Gleeson J., Davies P., Regional synaptic pathology in Alzheimer’s disease, Neurobiol. Aging, 1992,13, 375-382 CrossrefGoogle Scholar

  • [3] Danysz W., Parsons C.G., Alzheimer’s disease, β-amyloid, glutamate, NMDA receptors and memantine - searching for the connections, Br. J. Pharmacol., 2012, 167, 324-352 Google Scholar

  • [4] Anstey K.J., Cherbuin N., Herath P.M., Development of a new method for assessing global risk of Alzheimer’s disease for use in population health approaches to prevention, Prev. Sci., 2013, 14, 411-421 CrossrefGoogle Scholar

  • [5] Mosconi L, McHugh P.F., Let food be thy medicine: diet, nutrition, and biomarkers’ risk of Alzheimer’s disease, Curr. Nutr. Rep., 2015, 4, 126- 135 CrossrefGoogle Scholar

  • [6] Braak H., Braak E., Neuropathological stageing of Alzheimer-related changes, Acta Neuropathol., 1991, 82, 239-259 CrossrefGoogle Scholar

  • [7] Hardy J., Selkoe D.J., The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics, Science, 2002, 297, 353-356 Google Scholar

  • [8] Sepulveda-Falla D., Barrera-Ocampo A., Hagel C., Korwitz A., Vinueza- Veloz M.F., Zhou K., et al., Familial Alzheimer’s disease-associated presenilin-1 alters cerebellar activity and calcium homeostasis, J. Clin. Invest., 2014, 124, 1552-1567 CrossrefGoogle Scholar

  • [9] Gatz M., Reynolds C.A., Fratiglioni L., Johansson B., Mortimer J.A., Berg S., et al., Role of genes and environments for explaining Alzheimer disease, Arch. Gen. Psychiatry, 2006, 63, 168-174 CrossrefGoogle Scholar

  • [10] Schneider L.S., Mangialasche F., Andreasen N., Feldman H., Giacobini E., Jones R., et al., Clinical trials and late-stage drug development for Alzheimer’s disease: an appraisal from 1984 to 2014, J. Intern. Med., 2014, 275, 251-283 Google Scholar

  • [11] Mallucci G.R., Prion neurodegeneration: starts and stops at the synapse, Prion, 2009, 3, 195-201 CrossrefGoogle Scholar

  • [12] DeKosky S.T., Scheff S.W., Synapse loss in frontal cortex biopsies in Alzheimer’s disease: correlation with cognitive severity, Ann. Neurol., 1990, 27, 457-464 CrossrefGoogle Scholar

  • [13] Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., et al., Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment, Ann. Neurol., 1991, 30, 572-580 CrossrefGoogle Scholar

  • [14] Selkoe D.J., Alzheimer’s disease is a synaptic failure, Science, 2002, 298, 789-791 Google Scholar

  • [15] Davies C.A., Mann D.M., Sumpter P.Q., Yates P.O., A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer’s disease, J. Neurol. Sci., 1987, 78, 151-164 CrossrefGoogle Scholar

  • [16] Scheff S.W., Price D.A., Alzheimer’s disease-related synapse loss in the cingulate cortex, J. Alzheimers Dis., 2001, 3, 495-505 Google Scholar

  • [17] Masliah E., Mallory M., Alford M., DeTeresa R., Hansen L.A., McKeel D.W., et al., Altered expression of synaptic proteins occurs early during progression of Alzheimer’s disease, Neurology, 2001, 56, 127-129 CrossrefGoogle Scholar

  • [18] Scheff S.W., Price D.A., Schmitt F.A., DeKosky S.T., Mufson E.J., Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment, Neurology, 2007, 68, 1501-1508 CrossrefGoogle Scholar

  • [19] Falke E., Nissanov J., Mitchell T.W., Bennett D.A., Trojanowski J.Q., Arnold S.E., Subicular dendritic arborization in Alzheimer’s disease correlates with neurofibrillary tangle density, Am. J. Pathol., 2003, 163, 1615-1621 Google Scholar

  • [20] Ingelsson M., Fukumoto H., Newell K.L., Growdon J.H., Hedley-Whyte E.T., Frosch M.P., et al., Early Aβ accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain, Neurology, 2004, 62, 925-931 CrossrefGoogle Scholar

  • [21] Serrano-Pozo A., Frosch M.P., Masliah E., Hyman B.T., Neuropathological alterations in Alzheimer disease, Cold Spring Harb. Perspect. Med., 2011, 1, a006189 Google Scholar

  • [22] Lansdall C.J., An effective treatment for Alzheimer’s disease must consider both amyloid and tau, Biosci. Horiz., 2014, 7, hzu002 Google Scholar

  • [23] Buée L., Bussière T., Buée-Scherrer V., Delacourte A., Hof P.R., Tau protein isoforms, phosphorylation and role in neurodegenerative disorders, Brain Res. Rev., 2000, 33, 95-130 CrossrefGoogle Scholar

  • [24] Ihara Y., Nukina N., Miura R., Ogawara M., Phosphorylated tau protein is integrated into paired helical filaments in Alzheimer’s disease, J. Biochem., 1986, 99, 1807-1810 Google Scholar

  • [25] Goedert M., Spillantini M.G., Jakes R., Rutherford D., Crowther R.A., Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer’s disease, Neuron, 1989, 3, 519-526 CrossrefGoogle Scholar

  • [26] Goedert M., Spillantini M.G., Potier M.C., Ulrich J., Crowther R.A., Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain, EMBO J., 1989, 8, 393-399 Google Scholar

  • [27] Preuss U., Biernat J., Mandelkow E.M., Mandelkow E., The ‘jaws’ model of tau-microtubule interaction examined in CHO cells, J. Cell Sci., 1997, 110, 789-800 Google Scholar

  • [28] Dixit R., Ross J.L., Goldman Y.E., Holzbaur EL., Differential regulation of dynein and kinesin motor proteins by tau, Science, 2008, 319, 1086- 1089 Google Scholar

  • [29] Matus A., Stiff microtubules and neuronal morphology, Trends Neurosci., 1994, 17, 19-22 CrossrefGoogle Scholar

  • [30] Hwang S.C., Jhon D.Y., Bae Y.S., Kim J.H., Rhee S.G., Activation of phospholipase C-γ by the concerted action of tau proteins and arachidonic acid, J. Biol. Chem., 1996, 271, 18342-18349 Google Scholar

  • [31] Mattsson N., Savman K., Osterlundh G., Blennow K., Zetterberg H., Converging molecular pathways in human neural development and degeneration, Neurosci. Res., 2010, 66, 330-332 CrossrefGoogle Scholar

  • [32] Lee G., Kwei S.L., Newman S.T., Lu M., Liu Y., A new molecular interactor for tau protein, Soc. Neurosci. Abstr., 1996, 22, 975 Google Scholar

  • [33] Stieler J.T., Bullmann T., Kohl F., Tøien Ø., Brückner M.K., Härtig W., et al., The physiological link between metabolic rate depression and tau phosphorylation in mammalian hibernation, PLoS One, 2011, 6, e14530 Google Scholar

  • [34] Ahmed T., Van der Jeugd A., Blum D., Galas MC., D’Hooge R., Buée L., Cognition and hippocampal synaptic plasticity in mice with a homozygous tau deletion, Neurobiol. Aging, 2014, 35, 2474-2478 CrossrefGoogle Scholar

  • [35] Kimura T., Whitcomb D.J., Jo J., Regan P., Piers T., Heo S., et al., Microtubule-associated protein tau is essential for long-term depression in the hippocampus, Philos. Trans. R. Soc. B, 2014, 369, 20130144 Google Scholar

  • [36] Regan P., Piers T., Yi J.H., Kim D.H., Huh S., Park S.J., et al., Tau phosphorylation at serine 396 residue is required for hippocampal LTD, J. Neurosci., 2015, 35, 4804-4812 CrossrefGoogle Scholar

  • [37] 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 Google Scholar

  • [38] Mondragón-Rodríguez S., Trillaud-Doppia E., Dudilot A., Bourgeois C., Lauzon M., Leclerc N., et al., Interaction of endogenous tau protein with synaptic proteins is regulated by N-methyl-D-aspartate receptor-dependent tau phosphorylation, J. Biol. Chem., 2012, 287, 32040-32053 Google Scholar

  • [39] Klein C., Kramer E.M., Cardine A.M., Schraven B., Brandt R., Trotter J., Process outgrowth of oligodendrocytes is promoted by interaction of fyn kinase with the cytoskeletal protein tau, J. Neurosci., 2002, 22, 698-707 Google Scholar

  • [40] Amihăesei I.C., Cojocarut E., Mungiu O.C., Alzheimer - certitudes and hypotheses, Rev. Med. Chir. Soc. Med. Nat. Iasi., 2013, 117, 119-126 Google Scholar

  • [41] Kidd M., Paired helical filaments in electron microscopy of Alzheimer’s disease, Nature, 1963, 197, 192-193 Google Scholar

  • [42] Crowther R.A, Wischik C.M., Image reconstruction of the Alzheimer paired helical filament, EMBO J., 1985, 4, 3661-3665 Google Scholar

  • [43] Ksiezak-Reding H., Morgan K., Mattiace L.A., Davies P., Liu W.K., Yen S.H, et al., Ultrastructure and biochemical composition of paired helical filaments in corticobasal degeneration, Am. J. Pathol., 1994, 145, 1496-1508 Google Scholar

  • [44] Brion J.P., Couck A.M., Passareiro H., Flament-Durand J., Neurofibrillary tangles of Alzheimer’s disease: an immunohistochemical and immunoelectron study, J. Submicrosc. Cytol., 1985, 17, 89-96 Google Scholar

  • [45] Kosik K.S., Joachim C.L., Selkoe D.J., Microtubule-associated protein tau (τ) is a major antigenic component of paired helical filaments in Alzheimer disease, Proc. Natl. Acad. Sci. USA, 1986, 83, 4044-4048 CrossrefGoogle Scholar

  • [46] Grundke-Iqbal I., Iqbal K., Tung Y.C., Quinlan M., Wisniewski H.M., Binder L.I., Abnormal phosphorylation of the microtubule-associated protein tau (τ) in Alzheimer cytoskeletal pathology, Proc. Natl. Acad. Sci. USA, 1986, 83, 4913-4917 CrossrefGoogle Scholar

  • [47] Grundke-Iqbal I., Iqbal K.., Quinlan M, Tung Y.C., Zaidi M.S., Wisniewski H.M., Microtubule-associated protein tau. A component of Alzheimer paired helical filaments, J. Biol. Chem., 1986, 261, 6084-6089 Google Scholar

  • [48] Wischik C.M., Novak M., Thøgersen H.C., Edwards P.C., Runswick M.J., Jakes R., et al., Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease, Proc. Natl. Acad. Sci. USA, 1988, 85, 4506-4510 CrossrefGoogle Scholar

  • [49] Wischik C.M., Novak M., Edwards P.C., Klug A., Tichelaar W., Crowther R.A., Structural characterization of the core of the paired helical filament of Alzheimer disease, Proc. Natl. Acad. Sci. USA, 1988, 85, 4884-4888 CrossrefGoogle Scholar

  • [50] Skrabana R., Skrabanova M., Csokova N., Sevcik J., Novak M., Intrinsically disordered tau protein in Alzheimer’s tangles: a coincidence or a rule?, Bratisl. Lek. Listy, 2006, 107, 354-358 Google Scholar

  • [51] Gong C.X., Liu F., Grundke-Iqbal I., Iqbal K., Post-translational modifications of tau protein in Alzheimer’s disease, J. Neural Transm., 2005, 112, 813-838 CrossrefGoogle Scholar

  • [52] Pevalova M., Filipcik P., Novak M., Avila J., Iqbal K., Post-translational modifications of tau protein, Bratisl. Lek. Listy, 2006, 107, 346-353 Google Scholar

  • [53] Martin L., Latypova X., Terro F., Post-translational modifications of tau protein: implications for Alzheimer’s disease. Neurochem. Int., 2011, 58, 458-471 CrossrefGoogle Scholar

  • [54] Ksiezak-Reding H., Liu W.K., Yen S.H., Phosphate analysis and dephosphorylation of modified tau associated with paired helical filaments, Brain Res., 1992, 597, 209-219 Google Scholar

  • [55] Köpke E., Tung Y.C., Shaikh S., Alonso A.C., Iqbal K., Grundke-Iqbal I., Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease, J. Biol. Chem., 1993, 268, 24374-24384 Google Scholar

  • [56] Augustinack J.C., Schneider A., Mandelkow E.M., Hyman B.T., Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer’s disease, Acta Neuropathol., 200, 103, 26-35 Google Scholar

  • [57] Biernat J., Gustke N., Drewes G., Mandelkow E.M., Mandelkow E., Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding, Neuron, 1993, 11, 153-163 CrossrefGoogle Scholar

  • [58] Goedert M., Jakes R., Crowther R. A., Cohen P., Vanmechelen E., Vandermeeren M. , et al., Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer’s disease: identification of phosphorylation sites in tau protein, Biochem. J., 1994, 301, 871-877 Google Scholar

  • [59] Zheng-Fischhöfer Q., Biernat J., Mandelkow E.M., Illenberger S., Godemann R., Mandelkow E., Sequential phosphorylation of Tau by glycogen synthase kinase-3b and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical-filament-like conformation, Eur. J. Biochem., 1998, 252, 542-552 Google Scholar

  • [60] von Bergen M., Barghorn S., Li L., Marx A., Biernat J., Mandelkow E.M., et al., Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local b-structure, J. Biol. Chem., 2001, 276, 48165-48174 Google Scholar

  • [61] Goux W.J., The conformations of filamentous and soluble tau associated with Alzheimer paired helical filaments, Biochemistry, 2002, 41, 13798-13806 CrossrefGoogle Scholar

  • [62] Hiraoka S., Yao T.M., Minoura K., Tomoo K., Sumida M., Taniguchi T., Ishida T., Conformational transition state is responsible for assembly of microtubule-binding domain of tau protein, Biochem. Biophys. Res. Commun., 2004, 315, 659-663 Google Scholar

  • [63] Kovacech B., Skrabana R., Novak M., Transition of tau protein from disordered to misordered in Alzheimer’s disease, Neurodegener. Dis., 2010, 7, 24-27 CrossrefGoogle Scholar

  • [64] Novak M., Wischik C.M., Edwards P.C., Panell R., Milstein C., Characterization of the first monoclonal antibody against the pronase resistant core of the Alzheimer PHF, Prog. Clin. Biol. Res., 1989, 317, 755-761 Google Scholar

  • [65] Novak M., Kabat J., Wischik C.M., Molecular characterization of the minimal protease resistant tau unit of the Alzheimer’s disease paired helical filament, EMBO J., 1993, 12, 365-370 Google Scholar

  • [66] 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 Google Scholar

  • [67] Ghoshal N., García-Sierra F., Fu Y., Beckett L.A., Mufson E.J., Kuret J., et al., Tau-66: evidence for a novel tau conformation in Alzheimer’s disease, J. Neurochem., 2001, 77, 1372-1385 CrossrefGoogle Scholar

  • [68] Basurto-Islas G., Luna-Muñoz J., Guillozet-Bongaarts A.L., Binder L.I., Mena R., García-Sierra F., Accumulation of aspartic acid 421- and glutamic acid 391-cleaved tau in neurofibrillary tangles correlates with progression in Alzheimer disease, J. Neuropathol. Exp. Neurol., 2008, 67, 470-483 Google Scholar

  • [69] Bondareff W., Mountjoy C.Q., Roth M., Hauser D.L., Neurofibrillary degeneration and neuronal loss in Alzheimer’s disease, Neurobiol. Aging, 1989, 10, 709-715 CrossrefGoogle Scholar

  • [70] Sergeant N., Delacourte A., Buee L., Tau protein as a differential biomarker of tauopathies, Biochem. Biophys. Acta, 2005, 1739, 179- 219 Google Scholar

  • [71] Williams D.R., Tauopathies: classification and clinical update on neurodegenerative diseases associated with microtubule-associated protein tau, Intern. Med. J., 2006, 36, 652-660 CrossrefGoogle Scholar

  • [72] Buée 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 CrossrefGoogle Scholar

  • [73] Fu Y.J., Nishihira Y., Kuroda S., Toyoshima Y., Ishihara T., Shinozaki M., et al., Sporadic four-repeat tauopathy with frontotemporal lobar degeneration, Parkinsonism, and motor neuron disease: a distinct clinicopathological and biochemical disease entity, Acta Neuropathol., 2010, 120, 21-32 CrossrefGoogle Scholar

  • [74] Binder L.I., Frankfurter A., Rebhun L.I., The distribution of tau in the mammalian central nervous system, J. Cell Biol., 1985, 101, 1371-1378 CrossrefGoogle Scholar

  • [75] Aronov S., Aranda G., Behar L., Ginzburg I., Axonal tau mRNA localization coincides with tau protein in living neuronal cells and depends on axonal targeting signal, J. Neurosci., 2001, 21, 6577-6587 Google Scholar

  • [76] Sultan A., Nesslany F., Violet M., Bégard S., Loyens A., Talahari S., et al., Nuclear tau, a key player in neuronal DNA protection, J. Biol. Chem., 2011, 286, 4566-4575 Google Scholar

  • [77] Hoover B.R., Reed M.N., Jianjun Su., Penrod R.D., Kotilinek L.A., Grant M.K., et al., Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration, Neuron, 2010, 68, 1067-1081 CrossrefGoogle Scholar

  • [78] Jadhav S., Katina S., Kovac A., Kazmerova Z., Novak M., Zilka N., Truncated tau deregulates synaptic markers in rat model for human tauopathy, Front. Cell. Neurosci., 2015, 9, 24 Google Scholar

  • [79] Frandemiche M.L., De Seranno S., Rush T., Borel E., Elie A., Arnal I., et al., Activity-dependent tau protein translocation to excitatory synapse is disrupted by exposure to amyloid-b oligomers, J. Neurosci., 2014, 34, 6084-6097 CrossrefGoogle Scholar

  • [80] Zmuda J.F., Rivas R.J., Actin disruption alters the localization of tau in the growth cones of cerebellar granule neurons, J. Cell Sci., 2000, 113, 2797-2809 Google Scholar

  • [81] DiTella M., Feiguin F., Morfini G., Cáceres A., Microfilament-associated growth cone component depends upon tau for its intracellular localization, Cell Motil. Cytoskeleton, 1994, 29, 117-130 CrossrefGoogle Scholar

  • [82] Chen Q., Zhou Z., Zhang L., Wang Y., Zhang Y.W., Zhong M., et al., Tau protein is involved in morphological plasticity in hippocampal neurons in response to BDNF, Neurochem. Int., 2012, 60, 233-242 CrossrefGoogle Scholar

  • [83] Arriagada P.V., Growdon J.H., Hedley-Whyte E.T., Hyman B.T., Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer’s disease, Neurology, 1992, 42, 631-639 CrossrefGoogle Scholar

  • [84] Blennow K., Bogdanovic N., Alafuzoff I., Ekman R., Davidsson P., Synaptic pathology in Alzheimer’s disease: relation to severity of dementia, but not to senile plaques, neurofibrillary tangles, or the ApoE4 allele, J. Neural Transm., 1996, 103, 603-618 Google Scholar

  • [85] Callahan L.M., Vaules W.A., Coleman P.D., Progressive reduction of synaptophysin message in single neurons in Alzheimer disease, J. Neuropathol. Exp. Neurol., 2002, 61, 384-395 Google Scholar

  • [86] Rapoport S.I., In vivo PET imaging and postmortem studies suggest potentially reversible and irreversible stages of brain metabolic failure in Alzheimer’s disease, Eur. Arch. Psychiatry Clin. Neurosci., 1999, 249, S46-S55 Google Scholar

  • [87] 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 CrossrefGoogle Scholar

  • [88] 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 CrossrefGoogle Scholar

  • [89] Penzes P., Vanleeuwen J.E., Impaired regulation of synaptic actin cytoskeleton in Alzheimer’s disease, Brain Res. Rev., 2011, 67, 184-192 CrossrefGoogle Scholar

  • [90] Masliah E., Terry R.D., Alford M., DeTeresa R., Hansen L.A., Cortical and subcortical patterns of synaptophysinlike immunoreactivity in Alzheimer’s disease, Am. J. Pathol., 1991, 138, 235-246 Google Scholar

  • [91] Honer W.G, Pathology of presynaptic proteins in Alzheimer’s disease: more than simple loss of terminals, Neurobiol. Aging, 2003, 24, 1047- 1062 CrossrefGoogle Scholar

  • [92] Sze C.I., Bi H., Kleinschmidt-DeMasters B.K., Filley C.M., Martin L.J., Selective regional loss of exocytotic presynaptic vesicle proteins in Alzheimer’s disease brains, J. Neurol. Sci., 2000, 175, 81-90 Google Scholar

  • [93] Masliah E., Mallory M., Alford M., DeTeresa R., Hansen L.A., McKeel D.W., et al., Altered expression of synaptic proteins occurs early during progression of Alzheimer’s disease, Neurology, 2001, 56, 127- 129 CrossrefGoogle Scholar

  • [94] Reddy P.H., Mani G., Park B.S., Jacques J., Murdoch G., Whetsell W. Jr., Kaye J., Manczak M., Differential loss of synaptic proteins in Alzheimer’s disease: implications for synaptic dysfunction, J. Alzheimers Dis., 2005, 7, 103-117 Google Scholar

  • [95] Counts S.E., Nadeem M., Lad S.P., Wuu J., Mufson E.J., Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment, J. Neuropathol. Exp. Neurol., 2006, 65, 592-601 Google Scholar

  • [96] DeKosky S.T., Ikonomovic M.D., Styren S.D., Beckett L., Wisniewski S., Bennett D.A., et al. Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment, Ann. Neurol., 2002, 51, 145-155 CrossrefGoogle Scholar

  • [97] Bell K.F.S., Bennett D.A., Cuello A.C., Paradoxical upregulation of glutamatergic presynaptic boutons during mild cognitive impairment, J. Neurosci., 2007, 27, 10810-10817 CrossrefGoogle Scholar

  • [98] Scheff S.W., Price D.A., Schmitt F.A., Mufson E.J., Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment, Neurobiol. Aging, 2006, 27, 1372-1384 CrossrefGoogle Scholar

  • [99] Bertoni-Freddari C., Fattoretti P., Solazzi M., Giorgetti B., Di Stefano G., Casoli T., et al., Neuronal death versus synaptic pathology in Alzheimer’s disease, Ann. NY Acad. Sci., 2003, 1010, 635-638 Google Scholar

  • [100] Hof P., Morrison J., The cellular basis of cortical disconnection and related dementing conditions, In: Terry R., Katzman R., Bick K. (Eds), Alzheimer’s disease, Raven Press, New York, USA, 1994, 197-230 Google Scholar

  • [101] Scheff S.W., DeKosky S.T., Price D.A., Quantitative assessment of cortical synaptic density in Alzheimer’s disease, Neurobiol. Aging, 1990, 11, 29-37 CrossrefGoogle Scholar

  • [102] Masliah E., Mallory M., Hansen L., DeTeresa R., Alford M., Terry R., Synaptic and neuritic alterations during the progression of Alzheimer’s disease, Neurosci. Lett., 1994, 174, 67-72 Google Scholar

  • [103] Scheff S.W., Sparks L., Price D.A., Quantitative assessment of synaptic density in the entorhinal cortex in Alzheimer’s disease, Ann. Neurol., 1993, 34, 356-361 CrossrefGoogle Scholar

  • [104] Wakabayashi K., Honer W.G., Masliah E., Synapse alterations in the hippocampal-entorhinal formation in Alzheimer’s disease with and without Lewy body disease, Brain Res., 1994, 667, 24-32 Google Scholar

  • [105] Masliah E., Alford M., DeTeresa R., Mallory M., Hansen L., Deficient glutamate transport is associated with neurodegeneration in Alzheimer’s disease, Ann. Neurol., 1996, 40, 759-766 CrossrefGoogle Scholar

  • [106] Masliah E., Hansen L., Albright T., Mallory M., Terry R.D., lmmunoelectron microscopic study of synaptic pathology in Alzheimer’s disease, Acta Neuropathol., 1991, 81, 428-433 CrossrefGoogle Scholar

  • [107] Masliah E., Mallory M., Hansen L., DeTeresa R., Terry R.D., Quantitative synaptic alterations in the human neocortex during normal aging, Neurology, 1993, 43, 192-197 CrossrefGoogle Scholar

  • [108] Gonatas N.K., Anderson W.W., Evangelista I., The contribution of altered synapses in the senile plaque: an electron microscopic study in Alzheimer’s disease, J. Neuropathol. Exp. Neurol., 1967, 26, 25-39 Google Scholar

  • [109] Masliah E., Mallory M., Deerinck T., DeTeresa R., Lamont S., Miller A., et al., Re-evaluation of the structural organization of neuritic plaques in Alzheimer’s disease, J. Neuropathol. Exp. Neurol., 1993, 52, 135-142 Google Scholar

  • [110] Gylys K.H., Fein J.A., Yang F., Wiley D.J., Miller C.A., Cole G.M., Synaptic changes in Alzheimer’s disease: increased amyloid-β and gliosis in surviving terminals is accompanied by decreased PSD-95 fluorescence, Am. J. Pathol., 2004, 165, 1809-1817 Google Scholar

  • [111] Masliah E., Terry R., The role of synaptic proteins in the pathogenesis of disorders of the central nervous system, Brain Pathol., 1993, 3, 77- 85 CrossrefGoogle Scholar

  • [112] Callahan L.M., Vaules W.A., Coleman P.D., Quantitative decrease in synaptophysin message expression and increase in cathepsin D message expression in Alzheimer disease neurons containing neurofibrillary tangles, J. Neuropathol. Exp. Neurol., 1999, 58, 275-287 Google Scholar

  • [113] Louneva N., Cohen J.W., Han L.Y., Talbot K., Wilson R.S., Bennett D.A., et al., Caspase-3 is enriched in postsynaptic densities and increased in Alzheimer’s disease, Am. J. Pathol., 2008, 173, 1488-1495 Google Scholar

  • [114] Jacob C.P., Koutsilieri E., Bartl J., Neuen-Jacob E., Arzberger T., Zander N., et al. Alterations in expression of glutamatergic transporters and receptors in sporadic Alzheimer’s disease, J. Alzheimers Dis., 2007, 11, 97-116 Google Scholar

  • [115] Masliah E., Mallory M., Alford M., DeTeresa R., Iwai A., Saitoh T., Molecular mechanisms of synaptic disconnection in Alzheimer’s disease, In: Hyman B.T., Duyckaerts C. (Eds.), Connections, cognition and Alzheimer’s disease, Springer, Berlin, Germany, 1997, 121-140 Google Scholar

  • [116] Delacourte A., Sergeant N., Champain D., Wattez A., Maurage C.A., Lebert F., et al., Nonoverlapping but synergetic tau and APP pathologies in sporadic Alzheimer’s disease, Neurology, 2002, 59, 398-407 CrossrefGoogle Scholar

  • [117] Tanzi R.E., Bertram L., Twenty years of the Alzheimer’s disease amyloid hypothesis: a genetic perspective, Cell, 2005, 120, 545- 555 CrossrefGoogle Scholar

  • [118] Sadigh-Eteghad S., Sabermarouf B., Majdi A., Talebi M., Farhoudi M., Mahmoudi J., Amyloid-beta: a crucial factor in Alzheimer’s disease, Med. Princ. Pract., 2015, 24, 1-10 CrossrefGoogle Scholar

  • [119] Carter J., Lippa C. F., Beta-amyloid, neuronal death and Alzheimer’s disease, Curr. Mol. Med., 2001, 1, 733-737 Google Scholar

  • [120] Musiek E.S., Holtzman D.M., Three dimensions of the amyloid hypothesis: time, space and ‘wingmen’, Nat. Neurosci., 2015, 18, 800-806 CrossrefGoogle Scholar

  • [121] Delacourte A., Tauopathies: recent insights into old diseases, Folia Neuropathol., 2005, 43, 244-257 Google Scholar

  • [122] Masliah E., Ellisman M., Carragher B., Mallory M., Young S., Hansen L., et al., Three-dimensional analysis of the relationship between synaptic pathology and neuropil threads in Alzheimer disease, J. Neuropathol. Exp. Neurol., 1992, 51, 404-414 Google Scholar

  • [123] Callahan L.M., Coleman P.D., Neurons bearing neurofibrillary tangles are responsible for selected synaptic deficits in Alzheimer’s disease, Neurobiol. Aging, 1995, 16, 311-314 CrossrefGoogle Scholar

  • [124] Brun A., Liu X., Erikson C., Synapse loss and gliosis in the molecular layer of the cerebral cortex in Alzheimer’s disease and in frontal lobe degeneration, Neurodegeneration, 1995, 4, 171-177 CrossrefGoogle Scholar

  • [125] Liu X., Brun A., Regional and laminar synaptic pathology in frontal lobe degeneration of non-Alzheimer type, Int. J. Geriatr. Psychiatry, 1996, 11, 47-55 CrossrefGoogle Scholar

  • [126] Bigio E.H., Vono M.B., Satumtira S., Adamson J., Sontag E., Hynan L.S., et al., Cortical synapse loss in progressive supranuclear palsy, J. Neuropathol. Exp. Neurol., 2001, 60, 403-410 Google Scholar

  • [127] Suzuki K., Parker C.C., Pentchev P.G., Katz D., Ghetti B., D’Agostino A.N., et al., Neurofibrillary tangles in Niemann-Pick disease type C, Acta Neuropathol., 1995, 89, 227-238 CrossrefGoogle Scholar

  • [128] Suzuki M., Desmond T.J., Albin R.L., Frey K.A., Cholinergic vesicular transporters in progressive supranuclear palsy, Neurology, 2002, 58, 1013-1018 CrossrefGoogle Scholar

  • [129] Picciotto M.R., Wickman K., Using knockout and transgenic mice to study neurophysiology and behavior, Physiol. Rev., 1998, 78, 1131-1163 Google Scholar

  • [130] Zilka N., Korenova M., Novak M., Misfolded tau protein and disease modifying pathways in transgenic rodent models of human tauopathies, Acta Neuropathol., 2009, 118, 71-86 CrossrefGoogle Scholar

  • [131] Probst A., Gotz J., Wiederhold K.H., Tolnay M., Mistl C., Jaton A.L., et al., Axonopathy and amyotrophy in mice transgenic for human fourrepeat tau protein, Acta Neuropathol., 2000, 99, 469-481 CrossrefGoogle Scholar

  • [132] Mocanu M.M., Nissen A., Eckermann K., Khlistunova I., Biernat J., Drexler D., et al., The potential for β-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 CrossrefGoogle Scholar

  • [133] Kimura T., Yamashita S., Fukuda T., Park J.M., Murayama M., Mizoroki T., et al., Hyperphosphorylated tau in parahippocampal cortex impairs place learning in aged mice expressing wild-type human tau, EMBO J., 2007, 26, 5143-5152 CrossrefGoogle Scholar

  • [134] Kremer A., Maurin H., Demedts D., Devijver H., Borghgraef P., Van Leuven F., Early improved and late defective cognition is reflected by dendritic spines in Tau.P301L mice, J. Neurosci., 2011, 31, 18036- 18047 Google Scholar

  • [135] Dickstein D.L., Brautigam H., Stockton S.D., Schmeidler J., Hof P.R., Changes in dendritic complexity and spine morphology in transgenic mice expressing human wild-type tau, Brain Struct. Funct., 2010, 214, 161-179 Google Scholar

  • [136] Polydoro M., Acker C.M., Duff K., Castillo P.E., Davies P., Agedependent impairment of cognitive and synaptic function in the htau mouse model of tau pathology, J. Neurosci., 2009, 29, 10741- 10749 CrossrefGoogle Scholar

  • [137] 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 Google Scholar

  • [138] Yoshiyama Y., Higuchi M., Zhang B., Huang S.M., Iwata N., Saido T.C., et al., Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model, Neuron, 2007, 53, 337-351 Google Scholar

  • [139] Crescenzi R., DeBrosse C., Nanga R.P., Reddy S., Haris M., Hariharan H., et al., In vivo measurement of glutamate loss is associated with synapse loss in a mouse model of tauopathy, Neuroimage, 2014, 101, 185-192 CrossrefGoogle Scholar

  • [140] Hoffmann N.A., Dorostkar M.M., Blumenstock S., Goedert M., Herms J., Impaired plasticity of cortical dendritic spines in P301S tau transgenic mice, Acta Neuropathol. Commun., 2013, 1, 82 Google Scholar

  • [141] Kopeikina K.J., Polydoro M., Tai H.C., Yaeger E., Carlson G.A., Pitstick R., et al., Synaptic alterations in the rTg4510 mouse model of tauopathy, J. Comp. Neurol., 2013, 521, 1334-1353 Google Scholar

  • [142] Kopeikina K.J., Wegmann S., Pitstick R., Carlson G.A., Bacskai B.J., Betensky R.A., et al., Tau causes synapse loss without disrupting calcium homeostasis in the rTg4510 model of tauopathy, PLoS One, 2013, 8, e80834 Google Scholar

  • [143] 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 Google Scholar

  • [144] Rocher A.B., Crimins J.L., Amatrudo J.M., Kinson M.S., Todd-Brown M.A., Lewis J., et al., Structural and functional changes in tau mutant mice neurons are not linked to the presence of NFTs, Exp. Neurol., 2010, 223, 385-393 Google Scholar

  • [145] Crimins J.L., Rocher A.B., Peters A., Shultz P., Lewis J., Luebke J.I., Homeostatic responses by surviving cortical pyramidal cells in neurodegenerative tauopathy, Acta Neuropathol., 2011, 122, 551- 564 CrossrefGoogle Scholar

  • [146] Crimins J.L., Rocher A.B., Luebke J.I., Electrophysiological changes precede morphological changes to frontal cortical pyramidal neurons in the rTg4510 mouse model of progressive tauopathy, Acta Neuropathol., 2012, 124, 777-795 CrossrefGoogle Scholar

  • [147] Katsuse O., Lin W.L., Lewis J., Hutton M.L., Dickson D.W., Neurofibrillary tangle-related synaptic alterations of spinal motor neurons of P301L tau transgenic mice, Neurosci. Lett., 2006, 409, 95-99 Google Scholar

  • [148] Levenga J., Krishnamurthy P., Rajamohamedsait H., Wong H., Franke T.F., Cain P., et al., Tau pathology induces loss of GABAergic interneurons leading to altered synaptic plasticity and behavioral impairments, Acta Neuropathol. Commun., 2013, 1, 34 Google Scholar

  • [149] Harris J.A., Koyama A., Maeda S., Ho K., Devidze N., Dubal D.B., et al., Human P301L-mutant tau expression in mouse entorhinalhippocampal network causes tau aggregation and presynaptic pathology but no cognitive deficits, PLoS One, 2012, 7, e45881 Google Scholar

  • [150] Polydoro M., Dzhala V.I., Pooler A.M., Nicholls S.B., McKinney A.P., Sanchez L., Soluble pathological tau in the entorhinal cortex leads to presynaptic deficits in an early Alzheimer’s disease model, Acta Neuropathol., 2014, 127, 257-270 CrossrefGoogle Scholar

  • [151] Hunsberger H.C., Rudy C.C., Batten S.R., Gerhardt G.A., Reed M.N., P301L tau expression affects glutamate release and clearance in the hippocampal trisynaptic pathway, J. Neurochem., 2015, 132, 169- 182 Google Scholar

  • [152] Van der Jeugd A., Ahmed T., Burnouf S., Belarbi K., Hamdame M., Grosjean M.E., et al., Hippocampal tauopathy in tau transgenic mice coincides with impaired hippocampus-dependent learning and memory, and attenuated late-phase long-term depression of synaptic transmission, Neurobiol. Learn. Mem., 2011, 95, 296-304 Google Scholar

  • [153] Schindowski K., Bretteville A., Leroy K., Bégard S., Brion J.P., Hamdane M., et al., Alzheimer’s disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits, Am. J. Pathol., 2006, 169, 599-616 Google Scholar

  • [154] Burnouf S., Martire A., Derisbourg M., Laurent C., Belarbi K., Leboucher A., et al., NMDA receptor dysfunction contributes to impaired brain-derived neurotrophic factor-induced facilitation of hippocampal synaptic transmission in a tau transgenic model, Aging Cell, 2013, 12, 11-23 CrossrefGoogle Scholar

  • [155] Rosenmann H., Grigoriadis N., Eldar-Levy H., Avital A., Rozenstein L., Touloumi O., et al., A novel transgenic mouse expressing double mutant tau driven by its natural promoter exhibits tauopathy characteristics, Exp. Neurol., 2008, 212, 71-84 Google Scholar

  • [156] Sydow A., Van der Jeugd A., Zheng F., Ahmed T., Balschun D., Petrova O., et al., Tau-induced defects in synaptic plasticity, learning, and memory are reversible in transgenic mice after switching off the toxic tau mutant, J. Neurosci., 2011, 31, 2511-2525 CrossrefGoogle Scholar

  • [157] Eckermann K., Mocanu M.M., Khlistunova I., Biernat J., Nissen A., Hofmann A., et al., The beta-propensity of tau determines aggregation and synaptic loss in inducible mouse models of tauopathy, J. Biol. Chem., 2007, 282, 31755-31765 Google Scholar

  • [158] Decker J.M., Krüger L., Sydow A., Zhao S., Frotscher M., Mandelkow E., et al., Pro-aggregant tau impairs mossy fiber plasticity due to structural changes and Ca++ dysregulation, Acta Neuropathol. Commun., 2015, 3, 23 Google Scholar

  • [159] Messing L., Decker J.M., Joseph M., Mandelkow E., Mandelkow E.M., Cascade of tau toxicity in inducible hippocampal brain slices and prevention by aggregation inhibitors, Neurobiol. Aging, 2013, 34, 1343-1354 CrossrefGoogle Scholar

  • [160] Sydow A., Van der Jeugd A., Zheng F., Ahmed T., Balschun D., Petrova O., et al., Reversibility of tau-related cognitive defects in a regulatable FTD mouse model, J. Mol. Neurosci., 2011, 45, 432- 437 CrossrefGoogle Scholar

  • [161] Heffernan J.M., Eastwood S.L., Nagy Z., Sanders M.W., McDonald B., Harrison P.J., Temporal cortex synaptophysin mRNA is reduced in Alzheimer’s disease and is negatively correlated with the severity of dementia, Exp. Neurol., 1998, 150, 235-239 Google Scholar

  • [162] Coleman P.D., Yao P.J., Synaptic slaughter in Alzheimer’s disease, Neurobiol. Aging, 2003, 24, 1023-1027 CrossrefGoogle Scholar

  • [163] Lassmann H., Weiler R., Fischer P., Bancher C., Jellinger K., Floor E., et al. Synaptic pathology in Alzheimer’s disease: immunological data for markers of synaptic and large dense-core vesicles, Neuroscience, 1992, 46, 1-8 CrossrefGoogle Scholar

  • [164] Lassmann H., Fischer P., Jellinger K., Synaptic pathology of Alzheimer’s disease, Ann. NY Acad. Sci., 1993, 695, 59-64 Google Scholar

  • [165] Hatanpää K., Isaacs K.R., Shirao T., Brady D.R., Rapoport S.I., Loss of proteins regulating synaptic plasticity in normal aging of the human brain and in Alzheimer disease, J. Neuropathol. Exp. Neurol., 1999, 58, 637-643 Google Scholar

  • [166] Tai H.C., Serrano-Pozo A., Hashimoto T., Frosch M.P., Spires-Jones T.L., Hyman B.T., The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system, Am. J. Pathol., 2012, 181, 1426-1435 Google Scholar

  • [167] Yamada K., Holth J.K., Liao F., Stewart F.R., Mahan T.E., Jiang H., et al., Neuronal activity regulates extracellular tau in vivo, J. Exp. Med., 2014, 211, 387-393 Google Scholar

  • [168] Sokolow S., Henkins K.M., Bilousova T., Gonzalez B., Vinters H.V., Miller C.A., et al., Pre-synaptic C-terminal truncated tau is released from cortical synapses in Alzheimer’s disease, J. Neurochem., 2015, 133, 368-379 Google Scholar

  • [169] McMillan P., Korvatska E., Poorkaj P., Evstafjeva Z., Robinson L., Greenup L., et al., Tau isoform regulation is region- and cell-specific in mouse brain, J. Comp. Neurol., 2008, 511,788-803 Google Scholar

  • [170] 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 Google Scholar

  • [171] Filipcik P., Zilka N., Bugos O., Kucerak J., Koson P., Novak P., Novak M., First transgenic rat model developing progressive cortical neurofibrillary tangles, Neurobiol. Aging, 2012, 33, 1448-1456 CrossrefGoogle Scholar

  • [172] Hanes J., Zilka N., Bartkova M., Caletkova M., Dobrota D., Novak M., Rat tau proteome consists of six tau isoforms: implication for animal models of human tauopathies, J. Neurochem., 2009, 108, 1167-1176 CrossrefGoogle Scholar

  • [173] Alldred M.J., Duff K.E., Ginsberg S.D., Microarray analysis of CA1 pyramidal neurons in a mouse model of tauopathy reveals progressive synaptic dysfunction, Neurobiol. Dis., 2012, 45, 751-762 CrossrefGoogle Scholar

  • [174] Van der Jeugd A., Hochgräfe K., Ahmed T., Decker J.M., Sydow A., Hofmann A., et al., Cognitive defects are reversible in inducible mice expressing pro-aggregant full-length human tau, Acta Neuropathol., 2012, 123, 787-805 Google Scholar

About the article

Received: 2015-07-31

Accepted: 2015-10-04

Published Online: 2015-10-23

Citation Information: Translational Neuroscience, Volume 6, Issue 1, ISSN (Online) 2081-6936, DOI: https://doi.org/10.1515/tnsci-2015-0023.

Export Citation

©2015 Santosh Jadhav et al.. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Yan Shi, Ying-Yan Fang, Yu-Ping Wei, Qian Jiang, Peng Zeng, Na Tang, Youming Lu, Qing Tian, and Ling-Qiang Zhu
Journal of Alzheimer's Disease, 2018, Page 1
A. Borreca, V. Latina, V. Corsetti, S. Middei, S. Piccinin, F. Della Valle, R. Bussani, M. Ammassari-Teule, R. Nisticò, P. Calissano, and G. Amadoro
Molecular Neurobiology, 2018
Jaume Folch, Oriol Busquets, Miren Ettcheto, Elena Sánchez-López, Ruben Dario Castro-Torres, Ester Verdaguer, Maria Luisa Garcia, Jordi Olloquequi, Gemma Casadesús, Carlos Beas-Zarate, Carme Pelegri, Jordi Vilaplana, Carme Auladell, and Antoni Camins
Journal of Alzheimer's Disease, 2017, Page 1
E Lauretti, J-G Li, A Di Meco, and D Praticò
Translational Psychiatry, 2017, Volume 7, Number 1, Page e1020
Thomas Arendt, Jens T. Stieler, and Max Holzer
Brain Research Bulletin, 2016, Volume 126, Page 238
Goran Šimić, Mirjana Babić Leko, Selina Wray, Charles R. Harrington, Ivana Delalle, Nataša Jovanov-Milošević, Danira Bažadona, Luc Buée, Rohan de Silva, Giuseppe Di Giovanni, Claude M. Wischik, and Patrick R. Hof
Progress in Neurobiology, 2017, Volume 151, Page 101
Goran Šimić, Mirjana Babić Leko, Selina Wray, Charles Harrington, Ivana Delalle, Nataša Jovanov-Milošević, Danira Bažadona, Luc Buée, Rohan de Silva, Giuseppe Di Giovanni, Claude Wischik, and Patrick Hof
Biomolecules, 2016, Volume 6, Number 1, Page 6

Comments (0)

Please log in or register to comment.
Log in