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Cited by 468Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

Synthetic amyloid-β oligomers impair long-term memory independently of cellular prion protein

Open access
Balducci, Claudia, Beeg, Marten, Stravalaci, Matteo, Bastone, Antonio, Sclip, Alessandra, Biasini, Emiliano, Tapella, Laura, Colombo, Laura +6 more·2010·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.0911829107PMC PMC2836680
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Abstract

Inability to form new memories is an early clinical sign of Alzheimer’s disease (AD). There is ample evidence that the amyloid-β (Aβ) peptide plays a key role in the pathogenesis of this disorder. Soluble, bio-derived oligomers of Aβ are proposed as the key mediators of synaptic and cognitive dysfunction, but more tractable models of Aβ−mediated cognitive impairment are needed. Here we report that, in mice, acute intracerebroventricular injections of synthetic Aβ 1–42 oligomers impaired consolidation of the long-term recognition memory, whereas mature Aβ 1–42 fibrils and freshly dissolved peptide did not. The deficit induced by oligomers was reversible and was prevented by an anti-Aβ antibody. It has been suggested that the cellular prion protein (PrP C ) mediates the impairment of synaptic plasticity induced by Aβ. We confirmed that Aβ 1–42 oligomers interact with PrP C , with nanomolar affinity. However, PrP-expressing and PrP knock-out mice were equally susceptible to this impairment. These data suggest that Aβ 1–42 oligomers are responsible for cognitive impairment in AD and that PrP C is not required.

AI snapshot

Written from the paper’s full text.

TL;DR

Acute intracerebroventricular injection of synthetic Aβ1–42 oligomers impaired consolidation of long-term object-recognition memory in mice, whereas fibrils and freshly dissolved peptide did not. Although Aβ oligomers bound cellular prion protein (PrPC) with high affinity, PrP-expressing and PrP knockout mice were equally susceptible, indicating PrPC is not required for this memory impairment.

Key findings

  • Synthetic Aβ1–42 oligomers (estimated 10–50 nM) impaired long-term recognition memory; mature fibrils and freshly dissolved Aβ did not.
  • The oligomer-induced deficit was reversible: memory had fully recovered 10 days after injection without further Aβ, and was completely prevented by i.c.v. pretreatment with 0.25 μg/2 μL of the anti-Aβ antibody 4G8.
  • Aβ oligomers bound PrPC with high affinity (Kd ≤20 nM monomer equivalent), but Prnp 0/0 mice were as susceptible as Prnp +/+ mice to oligomer-induced memory impairment; oligomers were also toxic to both Prnp +/+ and Prnp 0/0 hippocampal neurons in vitro.
  • Oligomers disrupted memory encoding/consolidation but not retrieval: injection before familiarization prevented memory, whereas injection before the test phase did not.

Methods

  • Male C57BL/6 mice, 7–8 weeks old, received acute i.c.v. injections of synthetic Aβ1–42 preparations and were tested in the novel-object recognition task; Prnp 0/0 and Prnp +/+ mice were compared.
  • Aβ1–42 oligomers, fibrils, and initial-state peptide were characterized by atomic force microscopy and size exclusion chromatography before behavioral testing.
  • Binding to PrPC was measured by surface plasmon resonance using brain homogenates and anti-PrP antibodies; primary hippocampal neuron cultures were treated with 1–3 μM oligomers for 72 h and survival measured by MTT assay. Statistical analysis used ANOVA with post hoc tests.

Limitations

  • The paper states that one limitation is the use of oligomeric Aβ preparations not proven identical to those found in AD patient brains.
  • Evident from the text: object recognition memory is associated more with perirhinal cortex than hippocampus, so the behavioral model may not fully align with hippocampal LTP studies.
  • Evident from the text: the study used only male C57BL/6 mice and a single behavioral task, and it does not establish the mechanism linking Aβ oligomer binding to PrPC with memory impairment.

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

Integrity signals

Registry

Crossref · 10.1073/pnas.0911829107

Cites

57 of 57 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 32 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § Abstract

    The memory deficit induced by Aβ1-42 oligomers in mice was reversible.

    “The deficit induced by oligomers was reversible and was prevented by an anti-Aβ antibody.”
    • Also stated in: § Results · plain
      “After 10 days, with no further Aβ injection, the memory deficit had fully recovered (Fig. 3A).”
    Quote in the paperSubstantial claim
  • Findingown data
    § Abstract

    PrP-expressing and PrP knock-out mice were equally susceptible to Aβ1-42 oligomer-induced memory impairment.

    “However, PrP-expressing and PrP knock-out mice were equally susceptible to this impairment.”
    • Also stated in: § Results · plain
      “We found that Prnp 0/0 mice were as susceptible as Prnp +/+ mice to oligomer-induced memory impairment (Figs. 2B and 4A).”
    Quote in the paperSubstantial claim
  • Findingown data
    § Abstract

    In mice, acute intracerebroventricular injection of synthetic Aβ1-42 oligomers impaired consolidation of long-term recognition memory.

    “Here we report that, in mice, acute intracerebroventricular injections of synthetic Aβ1–42 oligomers impaired consolidation of the long-term recognition memory, whereas mature Aβ1–42 fibrils and freshly dissolved peptide did not.”
    • Also stated in: § Results · plain
      “Aβ oligomer–injected mice were unable to distinguish the new object, with no significant difference in the percentage of time spent investigating the two (Fig. 2A), and a discrimination index significantly lower than vehicle-injected mice (Fig. 2B).”
    Quote in the paperSubstantial claim
  • Findingown data
    § Abstract

    Aβ1-42 oligomers interact with PrPC with nanomolar affinity.

    “We confirmed that Aβ1–42 oligomers interact with PrPC, with nanomolar affinity.”
    • Also stated in: § Results · plain
      “The binding was dose dependent, with a dissociation constant (K d) of ≤20 nM monomer equivalent (Fig. 7 B and D).”
    Quote in the paperSubstantial claim
  • Findingown data
    § Abstract

    The memory impairment induced by Aβ1-42 oligomers in mice was prevented by pretreatment with anti-Aβ antibody 4G8.

    “The deficit induced by oligomers was reversible and was prevented by an anti-Aβ antibody.”
    • Also stated in: § Results · plain
      “An i.c.v. injection of 0.25 μg/2 μL of 4G8, 5 min before the Aβ oligomers, completely prevented the memory impairment (Fig. 3B).”
    Quote in the paperNot a substantial claim
  • May combine two claims. 14
  • Classified as probably not a substantial claim. 15

  • May combine two claims.

    Findingown data
    § Abstract

    Mature Aβ1-42 fibrils and freshly dissolved Aβ1-42 did not impair long-term recognition memory in mice.

    “whereas mature Aβ1–42 fibrils and freshly dissolved peptide did not.”
    • Also stated in: § Results · plain
      “Neither Aβ in the initial state nor the fibrils affected memory (Fig. 2 A and B).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    Only Aβ1-42 oligomers bound PrPC specifically; Aβ initial state and fibrils did not.

    “When Aβ initial state, oligomers or fibrils were assayed for their binding to PrPC, only Aβ oligomers bound PrPC specifically, and Aβ initial state and fibrils did not (Fig. 7 A and C).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data
    § Results

    Mice injected with Aβ1-42 oligomers 2 h before familiarization were unable to remember the object previously investigated, whereas mice injected 2 h before the test phase recalled the familiar object investigated the day before.

    “Mice injected 2 h before familiarization were unable to remember the object previously investigated, whereas mice injected 2 h before the test phase recalled the familiar object investigated the day before (Fig. 8).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    The protein captured on the surface plasmon resonance chips was actually PrPC, as no capture was detected when flowing brain homogenate from Prnp 0/0 mice.

    “Preliminary data confirmed that the captured protein is actually PrPC, as no capture was detected when flowing brain homogenate from Prnp 0/0 mice (Fig. 6).”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § Abstract

    PrPC binds synthetic Aβ oligomers with high affinity and plays a role in oligomer-mediated inhibition of long-term potentiation.

    “PrPC binds synthetic Aβ oligomers with high affinity and plays a role in the oligomer-mediated inhibition of LTP (17).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [17] Laurén J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature. 2009;457:1128–1132. doi: 10.1038/nature07761. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

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

    Premisecitation
    § Discussion

    All of these processes are affected by Aβ oligomers in vitro, using primary neuronal cultures.

    “All of these processes are affected by Aβ oligomers in vitro, using primary neuronal cultures (12, 15, 36, 37).”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [12] Shankar GM, et al. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci. 2007;27:2866–2875. doi: 10.1523/JNEUROSCI.4970-06.2007. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [15] Lacor PN, et al. Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer’s disease. J Neurosci. 2007;27:796–807. doi: 10.1523/JNEUROSCI.3501-06.2007. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [36] Hsieh H, et al. AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron. 2006;52:831–843. doi: 10.1016/j.neuron.2006.10.035. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [37] Lacor PN, et al. Synaptic targeting by Alzheimer’s-related amyloid beta oligomers. J Neurosci. 2004;24:10191–10200. doi: 10.1523/JNEUROSCI.3432-04.2004. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

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

    Premisecitation
    § Discussion

    Several neuronal receptors have been proposed as mediating the effect of Aβ on synaptic plasticity and memory, including α-7-nicotinic, glutamatergic, and insulin receptors.

    “Several neuronal receptors have been proposed as mediating the effect of Aβ on synaptic plasticity and memory, including the α-7-nicotinic (16), glutamatergic (39–40), and insulin (14) receptors.”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [16] Snyder EM, et al. Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci. 2005;8:1051–1058. doi: 10.1038/nn1503. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [39] De Felice FG, et al. Alzheimer’s disease-type neuronal tau hyperphosphorylation induced by A beta oligomers. Neurobiol Aging. 2008;29:1334–1347. doi: 10.1016/j.neurobiolaging.2007.02.029. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [40] Irvine GB, El-Agnaf OM, Shankar GM, Walsh DM. Protein aggregation in the brain: The molecular basis for Alzheimer’s and Parkinson’s diseases. Mol Med. 2008;14:451–464. doi: 10.2119/2007-00100.Irvine. [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [14] De Felice FG, et al. Protection of synapses against Alzheimer’s-linked toxins: Insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc Natl Acad Sci USA. 2009;106:1971–1976. doi: 10.1073/pnas.0809158106. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data
    § Results

    Aβ1-42 oligomers acutely disrupt anterograde memory storage but do not interfere with retrieval when information has been properly stored.

    “These data indicate that Aβ oligomers acutely disrupt anterograde memory storage but do not interfere with its retrieval when the information has been properly stored.”
    • Also stated in: § Discussion · plain
      “Aβ oligomers inhibited the encoding/consolidation of information, without affecting its retrieval if properly stored.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).

    Premisecitation
    § Discussion

    Lauren et al. reported that PrPC mediates Aβ oligomer-induced hippocampal synaptic plasticity impairment.

    “In an elegant study Lauren et al. (17) reported that PrPC mediates the Aβ oligomer-induced hippocampal synaptic plasticity impairment.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [17] Laurén J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature. 2009;457:1128–1132. doi: 10.1038/nature07761. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation
    § Results

    Recognition memory is dependent on the medial temporal lobe including the hippocampus.

    “Because recognition memory is dependent on the medial temporal lobe including the hippocampus (25), we examined whether oligomer-mediated memory impairment was also related to PrPC expression.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [25] Squire LR, Wixted JT, Clark RE. Recognition memory and the medial temporal lobe: A new perspective. Nat Rev Neurosci. 2007;8:872–883. doi: 10.1038/nrn2154. [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

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

    Premisenone given
    § Discussion

    Synthetic Aβ oligomers are chemically defined and can be easily produced and biophysically characterized.

    “Unlike Aβ aggregates purified from biological sources, synthetic Aβ oligomers are chemically defined, and can be easily produced and biophysically characterized.”
    Quote in the paperNot a substantial claim

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

    Premisecitation
    § Discussion

    Human and primate studies have shown that hippocampal lesions result in impaired object recognition.

    “However, some human and primate studies have shown that hippocampal lesions result in impaired object recognition (41, 42)”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [41] Reed JM, Squire LR. Impaired recognition memory in patients with lesions limited to the hippocampal formation. Behav Neurosci. 1997;111:667–675. doi: 10.1037//0735-7044.111.4.667. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [42] Zola SM, et al. Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci. 2000;20:451–463. doi: 10.1523/JNEUROSCI.20-01-00451.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data
    § Results

    The Aβ1-42 preparations and freshly dissolved Aβ1-42 were characterized by atomic force microscopy and size exclusion chromatography before behavioral investigation.

    “These preparations, and freshly dissolved Aβ1−42 (hereafter referred to as “initial state”), were characterized by atomic force microscopy (AFM) and size exclusion chromatography (SEC) before behavioral investigation.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data
    § Results

    Although Aβ oligomers interact with PrPC with high affinity, they do not act together to induce memory derangement.

    “Thus, although Aβ oligomers interact with PrPC with high affinity, they do not act together to induce memory derangement.”
    Quote in the paperSubstantial claim

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

    Premisecitation
    § Discussion

    PrPC has been involved in neurotrophic signaling and in the regulation of Aβ production.

    “PrPC has been involved in neurotrophic signaling (44, 45), and in the regulation of Aβ-production (46), suggesting that PrPC and Aβ may be part of a common molecular pathway governing neuronal differentiation.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [44] Kanaani J, Prusiner SB, Diacovo J, Baekkeskov S, Legname G. Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. J Neurochem. 2005;95:1373–1386. doi: 10.1111/j.1471-4159.2005.03469.x. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [45] Santuccione A, Sytnyk V, Leshchyns’ka I, Schachner M. Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J Cell Biol. 2005;169:341–354. doi: 10.1083/jcb.200409127. [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [46] Parkin ET, et al. Cellular prion protein regulates beta-secretase cleavage of the Alzheimer’s amyloid precursor protein. Proc Natl Acad Sci USA. 2007;104:11062–11067. doi: 10.1073/pnas.0609621104. [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

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

    Premisecitation
    § Discussion

    For the 24 h intertrial interval from familiarization to test phase used in this study, hippocampal activity is required.

    “However, some human and primate studies have shown that hippocampal lesions result in impaired object recognition (41, 42) and that, for the 24 h intertrial interval from familiarization to test phase used in our study, hippocampal activity is required (43).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [43] Hammond RS, Tull LE, Stackman RW. On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol Learn Mem. 2004;82:26–34. doi: 10.1016/j.nlm.2004.03.005. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

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

    Premisecitation
    § Discussion

    Memory processing requires NMDA receptor activation and intracellular signaling leading to AMPA receptor trafficking, synthesis of new proteins, and formation of dendritic spines.

    “Memory processing requires NMDA receptor activation and intracellular signaling leading to AMPA receptor trafficking, synthesis of new proteins, and formation of dendritic spines (34, 35).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [34] Collingridge GL, Isaac JT, Wang YT. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci. 2004;5:952–962. doi: 10.1038/nrn1556. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [35] Lüscher C, Nicoll RA, Malenka RC, Muller D. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci. 2000;3:545–550. doi: 10.1038/75714. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

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

    Premisecitation
    § Discussion

    The novel-object recognition task relies on spontaneous animal behavior without the need for stressor elements such as food or water deprivation, electric foot-shock, or aversive environments like water.

    “The novel-object recognition task is simple and reproducible, it measures recognition memory, which is heavily impaired in AD, and relies on spontaneous animal behavior without the need for stressor elements such as food or water deprivation, electric foot-shock, or aversive environments like water (25).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] Squire LR, Wixted JT, Clark RE. Recognition memory and the medial temporal lobe: A new perspective. Nat Rev Neurosci. 2007;8:872–883. doi: 10.1038/nrn2154. [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data
    § Discussion

    Aβ oligomers are the active amyloid-β species responsible for the memory impairment, as shown by the lack of effect of freshly solubilized Aβ and fibrils.

    “Proof that Aβ oligomers are the active amyloid-β species was the lack of effect of either the freshly solubilized Aβ (initial state) or fibrils.”
    Quote in the paperSubstantial claim

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

    Premisecitation
    § Discussion

    The novel-object recognition task measures recognition memory, which is heavily impaired in AD.

    “The novel-object recognition task is simple and reproducible, it measures recognition memory, which is heavily impaired in AD, and relies on spontaneous animal behavior without the need for stressor elements such as food or water deprivation, electric foot-shock, or aversive environments like water (25).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] Squire LR, Wixted JT, Clark RE. Recognition memory and the medial temporal lobe: A new perspective. Nat Rev Neurosci. 2007;8:872–883. doi: 10.1038/nrn2154. [DOI] [PMC free article] [PubMed] [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § Materials and Methods

    The depsi-peptide is highly soluble and has a much lower propensity to aggregate than native Aβ1-42, preventing spontaneous seed formation in solution.

    “At variance with the native peptide, the depsi-peptide is highly soluble and it has a much lower propensity to aggregate, thus preventing the spontaneous formation of seeds in the solution (49, 50).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [49] Taniguchi A, et al. “Click peptide”: pH-triggered in situ production and aggregation of monomer Abeta1-42. ChemBioChem. 2009;10:710–715. doi: 10.1002/cbic.200800765. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [50] Taniguchi A, et al. ‘O-Acyl isopeptide method’ for peptide synthesis: Solvent effects in the synthesis of Abeta1-42 isopeptide using ‘O-acyl isodipeptide unit’. J Pept Sci. 2007;13:868–874. doi: 10.1002/psc.905. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

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

    Interpretationreasoning
    § Discussion

    The use of oligomeric Aβ preparations that have not been proven identical to those found in the brain of AD patients is a limitation of this study.

    “One limitation of this study worth to be mentioned may be the use of oligomeric Aβ preparations which haven’t been proven to be identical to those found in the brain of AD patients.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.

    Premisenone given
    § Discussion

    The novel-object recognition task is simple and reproducible.

    “The novel-object recognition task is simple and reproducible”
    Quote in the paperNot a substantial claim
23 of 23

  • The paper relies on this without support.

    Synthetic Aβ1–42 oligomers injected intracerebroventricularly in mice reproduce the relevant actions of endogenous Aβ oligomers in Alzheimer’s disease.

    “These data suggest that Aβ1–42 oligomers are responsible for cognitive impairment in AD and that PrPC is not required.”
    “Soluble, bio-derived oligomers of Aβ are proposed as the key mediators of synaptic and cognitive dysfunction, but more tractable models of Aβ−mediated cognitive impairment are needed.”

  • The paper relies on this without support.

    There is no consensus as to which brain-derived oligomeric species mediate cognitive deficits in AD.

    “since there remains no consensus as to which brain-derived oligomeric species mediate cognitive deficits in AD”
2 of 2

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?

  • PrP-expressing and PrP-knockout mice are equally susceptible to long-term memory impairment induced by Aβ oligomers.

    “other studies have shown that PrP-expressing and PrP-knockout mice are equally susceptible to long-term memory impairment induced by Aβ oligomers (Balducci et al., 2010; Calella et al., 2010)”

    From The Aβ oligomer hypothesis for synapse failure and memory loss in Alzheimer’s disease (2011) · cites this paper as Balducci et al., 2010

Cites

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Authors
Balducci, C., Beeg, M., Stravalaci, M., Bastone, A., Sclip, A., Biasini, E., Tapella, L., Colombo, L., Manzoni, C., Borsello, T., Chiesa, R., Gobbi, M., Salmona, M., & Forloni, G.
Affiliations
  • Mario Negri Institute for Pharmacological Research (IT)
  • Dulbecco Telethon Institute (IT)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2010-01-19
Volume
107
Issue
5
Pages
2295-2300
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.0911829107
PMC
PMC2836680
OpenAlex
W2002280328
Semantic Scholar
63625a2fc958c65a2cb276db617f403efa9be515
Cited by
466
References
57
Citations by year
2026: 3 · 2025: 8 · 2024: 14 · 2023: 19 · 2022: 20 · 2021: 24 · 2020: 31 · 2019: 25 · 2018: 32 · 2017: 40 · 2016: 31 · 2015: 35 · 2014: 27 · 2013: 47 · 2012: 36
FWCI
33.78
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Iris (University of Trento) (submittedVersion)
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
amyloid-beta oligomers, amyloid-beta 42, Alzheimer's disease, long-term memory, memory consolidation, recognition memory, cellular prion protein, anti-amyloid antibodies, cognitive impairment, intracerebroventricular administration, amyloid fibrils
MeSH terms
Prion Proteins, Alzheimer Disease, Animals, Cognition Disorders, Humans, Injections, Intraventricular, Male, Memory, Mice, Inbred C57BL, Neuronal Plasticity, Peptide Fragments, Prions, Protein Binding, Amyloid beta-Peptides, Mice, Knockout, PrPC Proteins, Surface Plasmon Resonance, Mice

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