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Propagation of Tau Pathology in a Model of Early Alzheimer's Disease

Open access
de Calignon, Alix, Polydoro, Manuela, Suárez-Calvet, Marc, William, Christopher, Adamowicz, David H., Kopeikina, Kathy J., Pitstick, Rose, Sahara, Naruhiko +4 more·2012·Neuron

Abstract

Summary Neurofibrillary tangles advance from layer II of the entorhinal cortex (EC-II) toward limbic and association cortices as Alzheimer disease (AD) evolves. However, the mechanism involved in this hierarchical pattern of disease progression is unknown. We describe a transgenic mouse model in which overexpression of human tau P301L is restricted to EC-II. Tau pathology progresses from EC transgene-expressing neurons to neurons without detectable transgene expression, first to EC neighboring cells, followed by propagation to neurons downstream in the synaptic circuit such as the dentate gyrus, CA fields of the hippocampus, and cingulate cortex. Human tau protein spreads to these regions and co-aggregates with endogenous mouse tau. With age, synaptic degeneration occurs in the entorhinal target zone and EC neurons are lost. These data suggest that a sequence of progressive misfolding of tau proteins, circuit-based transfer to new cell populations, and deafferentation induced degeneration are part of a process of tau-induced neurodegeneration.

AI snapshot

Written from the paper’s full text.

TL;DR

A transgenic mouse model with human P301L tau restricted mainly to entorhinal cortex layer II shows age-dependent tau misfolding that later appears in neurons without detectable transgene mRNA, including hippocampal and cingulate targets. The findings support circuit-based spread of tau pathology, recruitment of endogenous mouse tau, and subsequent synaptic and neuronal degeneration.

Key findings

  • In rTgTauEC mice, tau pathology progressed with age: Alz50 reactivity first appeared at 3 months in the perforant pathway terminal zone, somatic Alz50 at 6 months, PHF1 at 12 months, Gallyas staining at 18 months, and Thioflavin S at 24 months.
  • Pathology spread to synaptically connected regions: dentate gyrus granule cells showed Alz50/PHF1 somata at 18 months and Gallyas/ThioS somata at 24 months, while CA1 and CA2/3 developed aggregates by 21 months; cingulate cortex also contained affected neurons.
  • Human tau protein appeared in cells lacking detectable human tau mRNA. In entorhinal cortex, only 33.3% of Alz50-positive neurons expressed human tau mRNA at 12 months, and by 24 months 96.4% (SD ±6.45, p<0.001) of Alz50-positive neurons had no detectable transgene expression.
  • Endogenous mouse tau was recruited into aggregates, appearing in the somatodendritic compartment and in sarkosyl-soluble and insoluble fractions. At 24 months, synaptic markers were reduced in the middle molecular layer, and entorhinal cortex layer II showed a 42% decrease in neuron density; transgene-expressing layer II neurons fell from about 12% at 3–18 months to about 4% at 24 months (p<0.005).

Methods

  • The rTgTauEC line was made by crossing tetO-tauP301L mice with a neuropsin-promoter-driven tet transactivator line, restricting human P301L tau expression largely to medial entorhinal cortex superficial layers and pre-/parasubiculum. Only F1 animals were used; the study included 183 mice (97 transgenic, 86 control) across eight age groups from 3 to 24 months.
  • Analyses included immunohistochemistry, in situ hybridization and FISH, laser capture microdissection followed by qPCR, western blotting, sarkosyl insolubility assays, stereological neuron counts, and array tomography for synaptic density.
  • The main comparisons tracked age-dependent tau epitopes, transgene mRNA versus human tau protein/pathology, endogenous mouse tau aggregation, synaptic marker loss, and neuronal loss in transgenic versus control mice.

Limitations

  • The paper states that it cannot distinguish whether misfolded axonal tau causes dying-back terminal degeneration or whether released tau is synaptotoxic, and it notes that how or whether misfolded tau is released and taken up remains unclear. It also lists unresolved questions about why some connected populations are protected, whether tau acts extracellularly or in membrane-bound compartments such as exosomes, and which tau species transmit aggregation.
  • Evident from the text: this is a mouse model using artificial overexpression of a mutant tau linked to frontotemporal dementia, so it may not fully capture sporadic Alzheimer’s disease; several quantitative analyses used small groups (for example, n=3–4 animals per group for neuronal counts and n=3–5 for array tomography), and the spread evidence is largely correlational with respect to timing and circuit connectivity.

Model-written summary. Check it against the paper before relying on it.

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Registry

Crossref · 10.1016/j.neuron.2011.11.033

Cites

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Claims the paper makes

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  • Findingown data

    Human tau protein and PHF tau are detectable in the entorhinal cortex and hippocampus of 17-month-old rTgTauEC mice.

    “Human tau protein as well as PHF tau could be detected in the EC and hippocampus of rTgTauEC (Fig S3A–B), confirming the histological data showing human tau protein present in the hippocampal formation.”
    Quote in the paperSubstantial claim
  • Findingown data

    In rTgTauEC mice, human tau P301L expression is restricted largely to superficial layers of the medial entorhinal cortex and the closely related pre- and parasubiculum.

    “We describe a transgenic mouse model in which overexpression of human tau P301L is restricted to EC-II.”
    • Also stated in: § Restricted transgene expression and age-dependent pathology in EC of rTgTauEC mice · plain
      “Human tau expression in bigenic rTgTauEC mice is limited largely to the superficial layers of medial entorhinal cortex and the closely related pre- and para-subicular cortices (Fig 1B–C).”
    Quote in the paperSubstantial claim
  • Findingown data

    In 24-month-old rTgTauEC and rTg4510 brains, sarkosyl extraction yields a 64 kDa insoluble hyperphosphorylated tau species that is absent in age-matched controls.

    “After sarkosyl extraction, a 64 kDa insoluble hyperphosphorylated tau species was detected by immunoblot in both rTg4510 and rTgTauEC brains, but was absent in age-matched control brains when analyzed using a total tau antibody (Fig 2G–H).”
    Quote in the paperSubstantial claim
  • Findingown data

    qPCR of laser-captured neurons confirms that neurons positive for human tau protein but negative for human tau mRNA by FISH do not express detectable levels of the tau transgene.

    “The qPCR data clearly show that the neurons that were human tau protein positive and were RNA negative by FISH indeed did not express detectable levels of the tau transgene (Fig 3G), in contrast to robust detection of tau mRNA in neurons positive for tau mRNA by FISH.”
    Quote in the paperSubstantial claim
  • Findingown data

    In rTgTauEC mice, the proportion of Alz50-positive entorhinal cortex neurons lacking detectable human tau mRNA increases with age, from 66.7% at 12 months to 96.4% at 24 months.

    “In the EC, quantification of human tau mRNA and Alz50 positive cells, reveals that only 33.3% of the Alz50 positive neurons in EC express human tau mRNA at 12 months, indicating spread of misfolded tau to neighboring neurons within the EC without detectable transgene expression (Fig 3F).”
    • Also stated in: § Human tau protein propagates to synaptically connected brain regions · boosted
      “By 24 months of age, astonishingly 97% of Alz50-positive neurons (96.4%; stdv +/−6.45; p<0.001) did not have any detectable human transgene expression, showing that the propagation to neighboring cells increased with age (Fig 3F) and indicating that transgene expressing neurons may be lost as will be discussed later.”
    Quote in the paperSubstantial claim
  • May combine two claims. 25
  • The quote only partly states this claim. 5
  • Classified as probably not a substantial claim. 15
  • May combine two claims. The quote only partly states this claim.

    Findingown data

    In 24-month-old rTgTauEC mice, endogenous mouse tau accumulates in the somatodendritic compartment of medial entorhinal cortex neurons and co-localizes with Alz50.

    “To determine whether mouse tau is recruited by human tau to aggregate, we performed immunohistochemistry using an antibody specific for mouse tau that revealed that mouse tau indeed accumulates in the somatodendritic compartment of MEC neurons of 24 month-old rTgTauEC mice (Fig 4A).”
    • Also stated in: § Human tau seeds mouse tau aggregation · plain
      “Results from double labeling using Alz50 and mouse tau antibodies shows that Alz50 and mouse tau staining co-localize in neuronal cell bodies of MEC which is further evidence for mouse tau recruitment into aggregates in the rTgTauEC mouse model (Fig 4B).”
    Quote in the paperSubstantial claim
  • May combine two claims. The quote only partly states this claim.

    Findingown data

    Human tau expression in the medial entorhinal cortex causes age-dependent accumulation of tau pathology in transgene-expressing neurons, with Alz50 axonal staining at 3 months preceding somatic Alz50 at 6 months, PHF1 at 12 months, Gallyas at 18 months, and Thioflavin S at 24 months.

    “Human tau expression in the MEC results in an age-dependent accumulation of tau pathology in transgene expressing neurons.”
    • Also stated in: § Restricted transgene expression and age-dependent pathology in EC of rTgTauEC mice · plain
      “The first sign of tau pathology was detected at 3 months of age with Alz50 staining, an early indicator of tau misfolding, in the projection input zone of MEC, corresponding to the middle third of the molecular layer of the dentate gyrus (Fig 1E, left most panel), while the inner and outer layers were non-reactive (for higher magnification see S2).”
    • Also stated in: § Restricted transgene expression and age-dependent pathology in EC of rTgTauEC mice · plain
      “From 6 months, a slow progression of tau epitopes in the soma of MEC neurons towards later stages of pathology was observed, marked by the presence of PHF1 staining, recognizing the late phosphorylation of Ser 396/404 sites, starting at the age of 12 months (Fig 1E, middle panel and S2), Gallyas staining (Paired Helical Filament-specific silver impregnation) at the age of 18 months (Fig 1E, second”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In rTgTauEC mice, axon terminals undergo age-dependent degeneration: Alz50 staining increases through 12 months, decreases at 18 months with more prominent somatic dentate gyrus staining, and becomes irregular patches from 21 months.

    “We observed age-dependent degeneration of axon terminals in rTgTauEC mice (Fig 5A, for higher magnification images see Fig S2 and for pathology progression see ST1).”
    • Also stated in: § Progressive neurodegeneration and gliosis in rTgTauEC neural circuits · hedged
      “Alz50 tau staining of misfolded tau in axon terminals increased with age through 12 months (Fig 5A, second left panel). At 18 months, the reactivity in axon terminals decreased and staining in soma of the molecular layer of the DG became more prominent, indicating the possibility that EC-II axons began to degenerate and DG granular neurons took up the misfolded protein (Fig 5A, middle panel).”
    • Also stated in: § Progressive neurodegeneration and gliosis in rTgTauEC neural circuits · plain
      “From 21 months of age, the pattern of Alz50 reactivity in the middle molecular layer of the DG changed from a clear layer to irregular patches in the axon terminal zone (Fig 5A, right panels), similar to a pattern observed in AD patients (Hyman et al., 1988).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hyman et al., 1988

      Not checked in the free run.

  • May combine two claims. The quote only partly states this claim.

    Findingown data

    Mouse tau increases with age in rTgTauEC mice and is present in both sarkosyl insoluble and soluble fractions.

    “Immunoblotting using the mouse tau specific antibody also revealed that mouse tau increases with age in rTgTauEC mice (Fig 4C), indicating that it may be accumulating in tangles.”
    • Also stated in: § Human tau seeds mouse tau aggregation · plain
      “In confirmation of this idea, sarkosyl insoluble and soluble fractions both contain endogenous mouse tau (Fig 4D).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In rTgTauEC mice, human tau transgene mRNA is intensely expressed in a subset of medial entorhinal cortex and pre/parasubiculum neurons as early as 3 months, predominantly in layer II, with rare expression in other regions.

    “We observed intense expression as early as 3 months of age, in a subset of neurons in the medial entorhinal cortex (MEC) and pre- and para-subiculum (Pre and Para) (Fig 1C).”
    • Also stated in: § Restricted transgene expression and age-dependent pathology in EC of rTgTauEC mice · plain
      “The positive neurons in the MEC were detected prominently in layer II, although rare positive neurons were observed in layer III, especially in the area adjacent to para-subiculum. A few rare neurons in the granular layer and the hilum of the dentate gyrus (DG) showed some transgene expression in accord with observations in the parental line (Yasuda and Mayford, 2006), as well as very rare neurons”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Yasuda and Mayford, 2006

      Not checked in the free run.

  • May combine two claims. The quote only partly states this claim.

    Findingown data

    In rTgTauEC mice, total tau and human tau increase with age, and phospho-tau epitopes AT180, PHF1, and CP13 increase with age when normalized to total tau.

    “Western blot analysis of whole brain extracts obtained from 12, 18 and 24 month-old rTgTauEC and control mice confirm human tau protein is expressed in the brain and shows an age-dependent increase in total tau and human tau (Fig 2A–C).”
    • Also stated in: § Restricted transgene expression and age-dependent pathology in EC of rTgTauEC mice · plain
      “rTgTauEC mice present an age-dependent increase in all phospho epitopes (Fig 2D–F).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Cortical areas with limited transgene expression outside the entorhinal cortex but without direct entorhinal input do not show tau aggregation, and the cerebellum, which expresses human P301L tau mRNA, does not develop fibrillar human tau accumulation in the soma.

    “Importantly, unlike the anterior cingulate cortex, cortical areas that showed limited transgene expression outside of the EC, but do not receive direct input from the entorhinal cortex, did not show any tau aggregation. Moreover, the cerebellum, which expresses human P301L tau mRNA, did not develop any fibrillar accumulation of htau in the soma.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Endogenous mouse tau accumulates in the somatodendritic compartment of entorhinal cortex neurons, where it co-aggregates with human tau.

    “endogenous mouse tau accumulates in the somatodendritic compartment of EC neurons where it co-aggregates with human tau”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In rTgTauEC mice, significant neuronal loss occurs at 24 months in EC-II and parasubiculum, with a 42% decrease in neuron density in entorhinal cortex layer II, but no significant loss up to 21 months.

    “In rTgTauEC mice, significant neuronal loss was detected at 24 months of age, in the area of transgene expression, EC-II and parasubiculum, compared to the average neuron number in age-matched control brains (Fig 6C).”
    • Also stated in: § Progressive neurodegeneration and gliosis in rTgTauEC neural circuits · plain
      “We observed a 42% decrease in neuron density in layer II of entorhinal cortex. We did not observe significant neuronal loss up to 21 months of age.”
    Quote in the paperSubstantial claim
  • May combine two claims. The quote only partly states this claim.

    Findingown data

    Axonal degeneration in rTgTauEC mice is accompanied by microglial activation and astrogliosis, with Alz50-positive terminal patches surrounded by activated microglia at 24 months.

    “Axonal degeneration was accompanied by gliosis in rTgTauEC brain. rTgTauEC mice showed evidence of microglial activation (Fig 5B–C) and astrogliosis (Fig 5D–E).”
    • Also stated in: § Progressive neurodegeneration and gliosis in rTgTauEC neural circuits · hedged
      “At 24 months of age, Alz50-positive patches of axon terminals in the middle molecular layer were surrounded by activated microglia (Fig 5C) suggesting that axon terminals and their synapses were degenerating in this area.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In rTgTauEC mice, approximately 12% of EC-II neurons express the human tau transgene at 3 months, unchanged at 12 and 18 months, and only about 4% at 24 months.

    “Stereological counts of human tau expressing neurons labeled with in situ hybridization show that approximately 12% of neurons (12.4%; sem +/− 1.69) in layer-II of entorhinal cortex expressed the transgene at 3 months of age (Fig 6E–F).”
    • Also stated in: § Progressive neurodegeneration and gliosis in rTgTauEC neural circuits · plain
      “This number was unchanged at 12 months (13.21%; sem +/− 0.86; p=0.366) and 18 months of age (12.18%; sem +/− 1.96; p=0.481), showing that only a portion of neurons in the EC-II expressed the human tau transgene. At 24 months of age, only ~4% (3.71%; sem +/− 0.84) of the neurons expressed the transgene (Fig 1C and 1D) (p<0.005).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In rTgTauEC mice, 47% of EC-II neurons are Alz50 positive at 12 months, dropping to approximately 10% at 24 months.

    “Quantification by stereological counts showed that 47% of all neurons in the EC-II were Alz50 positive at 12 months of age which dropped to approximately 10% at 24 months of age (Fig 6D) as some neurons died.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingcitation

    Parental P301L mice without the transactivator have human tau protein or mRNA below detection thresholds, consistent with a prior observation that the tau-alone parental line expresses less than 2% of rTg4510 levels and does not develop tau pathology with age.

    “Moreover, the parental P301L mice without the transactivator transgene show levels of human tau protein or mRNA (supplemental figure S1) below detection thresholds, in accord with a recent observation that the “tau alone” parental line express <2% of the levels of rTg4510 mice and do not develop any tau pathological alterations with age (Barten et al. 2011).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barten et al. 2011

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    In rTgTauEC mice, human tau immunofluorescence in the entorhinal cortex is significantly reduced at 24 months and dentate gyrus neuron cell bodies become immunoreactive for human tau.

    “There is a significant reduction in the human tau immunofluorescence staining of the EC at 24 months and the cell bodies of the DG neurons become immunoreactive for htau, suggesting the protein is being transmitted (Fig S4).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    In Alzheimer disease, neurofibrillary tangles accumulate first in layer II of the entorhinal cortex and then spread in a hierarchical pattern to limbic and association cortices.

    “Neurofibrillary tangles advance from layer II of the entorhinal cortex (EC-II) toward limbic and association cortices as Alzheimer disease (AD) evolves.”
    • Also stated in: § INTRODUCTION · boosted
      “It has been known for more than 25 years that neurofibrillary tangles have a hierarchical pattern of accumulation reflecting selective vulnerability of neuronal populations in the Alzheimer brain, initially affecting the large projection neurons that connect memory related neural systems (Braak and Braak, 1991; Hyman et al., 1984).”
    • Also stated in: § INTRODUCTION · hedged
      “Over years, a “march” of lesions appears to propagate across limbic and association cortices, creating a pattern so consistent as to be incorporated into criteria for the neuropathological diagnosis of the illness (Hyman and Trojanowski, 1997).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Braak and Braak, 1991 source

      Not checked in the free run.

    • cites Hyman et al., 1984 source

      Not checked in the free run.

    • cites Hyman and Trojanowski, 1997 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Human tau enters neighboring cells without detectable transgene and transmits a misfolded state that recruits endogenous mouse tau into the somatodendritic compartment, contributing to tau aggregation.

    “These data suggest that human tau enters neighboring cells that do not have detectable levels of human tau transgene and transmits a misfolded state which recruits endogenous mouse tau into the somatodendritic compartment, where it becomes misfolded and contributes to tau aggregation.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Prior cell culture studies showed that extracellular tau aggregates can be internalized, transmit tau misfolding, seed fibril formation, and transfer between co-cultured cells.

    “It has been shown previously, in cell culture experiments, that extracellular tau aggregates could be internalized transmitting tau misfolding from outside to inside of the cell where these aggregates could seed fibril formation of recombinant tau monomer. Moreover, the same study showed that tau aggregates were transferred between co-cultured cells. (Frost et al., 2009).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Frost et al., 2009

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data

    The mouse tau antibody is specific: it shows reactivity in rTgTauEC and control mouse brain but not in tau knockout or human Alzheimer disease brain.

    “The specificity of the mouse tau antibody was confirmed by Western blot (Fig 4E) which shows mTau reactivity in rTgTauEC and control mouse brain but not in tau knockout or human AD brain.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    In mice, superficial entorhinal cortex layers project to the dentate gyrus via the perforant pathway, with layer II projecting to the outer two-thirds of the dentate molecular layer.

    “The superficial layers provide neuronal projections to the dentate gyrus in a powerful projection referred to as the perforant pathway (Witter, 2007).”
    • Also stated in: § INTRODUCTION · plain
      “In the mouse, layer II of the EC projects directly to the outer two thirds of the molecular layer of the dentate gyrus, where it connects to dendrites from the granule cells of the dentate gyrus (Hjorth-Simonsen and Jeune, 1972; Steward, 1976).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Witter, 2007

      Not checked in the free run.

    • cites Hjorth-Simonsen and Jeune, 1972

      Not checked in the free run.

    • cites Steward, 1976

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    A prior study reported that brain extracts from NFT-bearing mouse brain injected into wild-type tau expressing mice induce seeding of tau fibrils in neurons.

    “Another recent study reported that brain extracts from NFT-bearing mouse brain injected in wild-type tau expressing mice induces seeding of tau fibrils in neurons (Clavaguera et al., 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Clavaguera et al., 2009 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    An unbiased stereologic counting method was used to determine the number of neurons per brain region.

    “Unbiased stereologic counting method was used to determine the number of neurons per region of the brain (Hyman et al., 1998).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hyman et al., 1998

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Reactive astrocytes in rTgTauEC mice are PHF1-positive at 24 months, and because the tau transgene is not expressed in glia and no PHF1 astrocytes appear earlier, human tau is likely released from terminals and taken up by glia as axons degenerate.

    “Double labeling using PHF1, phospho tau antibody, and GFAP antibody demonstrated reactive astrocytes that were PHF1-positive at 24 months of age (Fig 5E). The tau transgene is not expressed in glia, and there were no PHF1 positive astrocytes at earlier ages, indicating human tau is likely released from terminals and taken up by glia as the axons degenerate.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The data do not rule out the possibility that some tau is released and taken up at earlier ages or under normal physiological conditions.

    “but this does not preclude the possibility that that some tau is released and taken up at earlier ages, or even under normal physiological circumstances.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    cDNA samples were run in triplicate in a 25 μl reaction with 12.5 μl SYBR green Mastermix.

    “Triplicates of cDNA samples were added to a 25 μl reaction containing 12.5 μl SYBR green Mastermix (Applied Biotechnology).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Band density values were normalized to β-actin or total tau when analyzing tau phosphorylation.

    “Band density values were normalized to β-actin or total tau levels when tau phosphorylation levels were analyzed.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    Human tau protein is present in GFAP-positive astrocytes in rTgTauEC mice, suggesting that release of tau from neurons and uptake by glia also takes place in this model.

    “The presence of human tau protein in GFAP positive astrocytes in rTgTauEC mice suggests that release of tau from neurons and uptake by glia also takes place in this model.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation

    Prior data suggest that intracellular tau aggregates can seed aggregation of native tau proteins and propagate their misfolded state in a prion-like manner.

    “Recent data suggest that intracellular protein aggregates of tau have the capacity to seed aggregation of native tau proteins and might propagate their misfolded state in a prion-like manner.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites de Calignon et al., 2010 source

      Not checked in the free run.

    • cites Iliev et al., 2006

      Not checked in the free run.

    • cites Mocanu et al., 2008

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    cDNA clones were verified by sequencing for specificity before being used to generate standard curves.

    “After verifying the respective specificities of the cDNA clones by sequencing, these were used to generate individual standard curves”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    In rTgTauEC mice, tau is transferred to neighboring cells and to synaptically connected neurons, suggesting that tau or a particular tau species may be released at the synapse.

    “Taken together, data presented in this study indicates that, in the rTgTauEC mice, tau was not only transferred to neighboring cells, but also to synaptically-connected neurons, which suggested that tau, or a particular species of tau such as hyperphosphorylated tau, misfolded tau, or a fragment of tau, may have been released at the synapse.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Study design and conductown data

    The mouse tau-specific antibody mTau was characterized by western blot and immunohistochemistry for sensitivity and specificity and did not recognize unspecific proteins in tau knockout mice or human brain.

    “The antibody was characterized by western blot analysis and immunohistochemistry for sensitivity and specificity and did not recognize any unspecific proteins in tau knockout mice or in human brain.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    The levels of tau mRNA were normalized against mouse tau mRNA.

    “Finally, the respective tau mRNA levels were normalized to murine tau mRNA levels.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    Only F1 offspring were used, ensuring a uniform 50:50 mix of FVB and C57BL/6 genetic backgrounds.

    “Only F1 offspring were used as experimental animals ensuring a uniform 50:50 mix of FVB and C57BL/6 genetic background.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Increased tau levels in cerebrospinal fluid after injury are consistent with injury causing tau release.

    “the presence of increased tau CSF levels after injury is consistent with the possibility that injury induces release (Blennow et al., 1995).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Blennow et al., 1995 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Age-matched littermates carrying only the activator and responder transgenes served as controls.

    “Age matched littermates expressing only the activator transgene and the responder transgene were used as controls.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Mean band densities from rTgTauEC samples were normalized to corresponding control samples.

    “Mean band densities for samples from rTgTauEC mice were normalized to corresponding samples from control mice.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Counting frames of 21.8 μm × 21.8 μm and step lengths of 100-200 μm were chosen to count more than 200 neurons per animal.

    “Counting frames of size 21.8 μm x 21.8 μm, and step length from 100 μm to 200 μm were selected to count >200 neurons per animal.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    Cell loss at 24 months exceeds the number of transgene-expressing neurons, suggesting that neurons developing tau pathology without expressing the transgene might also be lost.

    “Further, the cell loss observed at 24 months exceeds the number of neurons that were expressing the transgene, suggesting that neurons that develop tau pathology without expressing the transgene might also be lost.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Study design and conductown data

    Each of the eight age groups studied (3, 6, 9, 12, 15, 18, 21, and 24 months) included both transgenic and control animals.

    “Each of the 8 age groups studied (3, 6, 9, 12, 15, 18, 21, 24 months) contained transgenic and control animals.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    RNA samples were assessed for quality using an Agilent 6000 Bioanalyzer and a Nanodrop spectrophotometer.

    “RNA samples were assayed for quality with an Agilent 6000 Bioanalyzer and a Nanodrop spectrophotometer.”
    Quote in the paperNot a substantial claim
39 of 39
  • The paper relies on this without support.

    The mechanism by which tau pathology progresses hierarchically in Alzheimer disease is not understood.

    “However, the mechanism involved in this hierarchical pattern of disease progression is unknown.”
    “Despite recognition of the patterns of anatomical connectivity that link vulnerable neurons, there is no clear understanding of the mechanism of disease progression.”
  • The paper relies on this without support.

    Alz50 staining indicates early tau misfolding.

    “The first sign of tau pathology was detected at 3 months of age with Alz50 staining, an early indicator of tau misfolding, in the projection input zone of MEC, corresponding to the middle third of the molecular layer of the dentate gyrus (Fig 1E, left most panel), while the inner and outer layers were non-reactive (for higher magnification see S2).”
  • The paper relies on this without support.

    The rTgTauEC mouse model recapitulates the earliest point in the neurodegenerative cascade of Alzheimer disease.

    “To create a model of the earliest point in the neurodegenerative cascade of Alzheimer disease, we generated a new transgenic mouse model in which a mutant form of tau (P301L) linked to tangle formation in frontotemporal dementia is expressed selectively in a fraction of the neurons of layer II of entorhinal cortex.”
3 of 3

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Tau aggregates can transfer and propagate/spread within synaptic circuits.

    “This may be important as we know that tau aggregates can transfer and propagate/spread within synaptic circuits (Clavaguera et al., 2009, de Calignon et al., 2012).”

    From In vivo imaging of tau pathology using multi-parametric quantitative MRI (2015) · cites this paper as de Calignon et al., 2012

    The Discussion reports tau transfer to synaptically connected neurons in rTgTauEC mice, supporting circuit-based spread. But it explicitly asks which species transfers the aggregated state and whether that species is itself aggregated; the paper does not establish that tau aggregates themselves transfer. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • The pattern of time-progressive 'limbic enhancement' resembles the pattern of neurofibrillary tangle advancement in evolving Alzheimer's disease.

    “We find it compelling how this pattern of time-progressive 'limbic enhancement' resembles the pattern of neurofibrillary tangle advancement in evolving Alzheimer's disease (72), which to date is incompletely understood.”
  • Exogenously supplied tau fibrils seed aggregation of transgenic human and endogenous mouse tau in mouse tauopathy models by enhancing nucleation, and these aggregates spread transsynaptically to remote connected brain regions.

    “Exogenously supplied fibrils will seed aggregation of transgenic human and endogenous mouse tau fibrils in mouse tauopathy models by enhancing nucleation of new fibrils. These aggregates then spread transsynaptically to remote anatomically connected brain regions inducing further seeding and aggregation”

    From Alzheimer Disease: An Update on Pathobiology and Treatment Strategies (2019) · cites this paper as de Calignon et al., 2012

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Degeneration sequence reverses synaptic and axonal loss

    Major

    The discussion places synaptic degeneration before axonal degeneration, but the results summarize axon-terminal degeneration as preceding synapse loss.

  • Laser-capture samples are assigned different ages

    Major

    The results describe the FISH, laser-capture, and qPCR experiment as using 17-month-old animals, while the corresponding procedure says the brain sections came from 24-month-old mice. This leaves the age of the samples supporting that result unclear.

2 of 2

Cites

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Authors
de Calignon, A., Polydoro, M., Suárez-Calvet, M., William, C., Adamowicz, D. H., Kopeikina, K. J., Pitstick, R., Sahara, N., Ashe, K. H., Carlson, G. A., Spires-Jones, T. L., & Hyman, B. T.
Affiliations
  • Harvard University (US)
  • Boston University (US)
  • McLaughlin Research Institute (US)
  • University of Florida (US)
  • University of Minnesota (US)
Corresponding author
Hyman, Bradley T.
Venue
Neuron
Publisher
Elsevier BV
Published
2012-02
Volume
73
Issue
4
Pages
685-697
ISSN
0896-6273 (ISSN-L)
OpenAlex
W2095963715
Cited by
1,427
References
52
Citations by year
2026: 58 · 2025: 74 · 2024: 72 · 2023: 72 · 2022: 94 · 2021: 107 · 2020: 98 · 2019: 106 · 2018: 105 · 2017: 102 · 2016: 115 · 2015: 99 · 2014: 135 · 2013: 118 · 2012: 68
FWCI
90.07
Type
journal article
Language
en
Open access
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
Funders
  • Alzheimer's Association
  • American Health Assistance Foundation
  • National Institutes of Health (K99AG33670, AG08487)
  • National Institute on Aging (AG-08487, R01AG026249, R00AG033670, R01AG008487, AG026249, K99AG33670, R21AG038835, P50AG005134, K99AG033670, P30AG062421)
  • National Institute of Neurological Disorders and Stroke (K08NS069811, R21NS067127)
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords
tau pathology, Alzheimer's disease, neurofibrillary tangles, P301L tau, entorhinal cortex, transgenic mouse model, tau misfolding, synaptic degeneration, deafferentation, neurodegeneration, hippocampus, cingulate cortex, dentate gyrus, disease progression
MeSH terms
Age Factors, Alzheimer Disease, Animals, Epitopes, Disease Models, Animal, Gene Expression Regulation, Glial Fibrillary Acidic Protein, Gliosis, Hippocampus, Humans, Mice, Inbred C57BL, Mice, Transgenic, Mutation, Nerve Degeneration, Neurons, RNA, Messenger, Serine, Neurofibrillary Tangles, tau Proteins, Disease Progression, Entorhinal Cortex, Tauopathies, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-06.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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