Cited by 213Alzheimer's disease research and treatmentsNeuroinflammation and Neurodegeneration MechanismsNicotinic Acetylcholine Receptors Study

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Accelerated Plaque Accumulation, Associative Learning Deficits, and Up-regulation of α7 Nicotinic Receptor Protein in Transgenic Mice Co-expressing Mutant Human Presenilin 1 and Amyloid Precursor Proteins

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Dineley, Kelly T., Xia, Xuefeng, Bui, Duy, Sweatt, J. David, Zheng, Hui·2002·Journal of Biological Chemistry

DOI 10.1074/jbc.m200164200

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Abstract

Familial Alzheimer's disease-associated mutations in presenilin 1 or 2 or amyloid precursor protein result in elevated beta-amyloid, beta-amyloid accumulation, and plaque formation in the brains of affected individuals. By crossing presenilin 1 transgenic mice carrying the A246E mutation with plaque-producing amyloid precursor protein K670N/M671L transgenic mice (Tg2576), we show that co-expression of both mutant transgenes results in acceleration of amyloid accumulation and associative learning deficits. At 5 months of age with no detectable plaque pathology, amyloid precursor protein transgenic animals are impaired in contextual fear learning following two pairings of conditioned and unconditioned stimuli but appear normal following a more robust five-pairing training. At 9 months of age when beta-amyloid deposition is evident, these mice are impaired following both two-pairing and five-pairing protocols. Mice carrying both transgenes are impaired in contextual fear conditioning at either age. All transgenic animal groups performed as well as controls in cued fear conditioning, indicating that the contextual fear learning deficits are hippocampus-specific. The associative learning impairments are coincident with elevated alpha 7 nicotinic acetylcholine receptor protein in the dentate gyrus. These findings provide two robust and rapid assays for beta-amyloid-associated effects that can be performed on young animals: impaired contextual fear learning and up-regulation of alpha 7 nicotinic receptors.

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Background
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Background
Research tool: validation of floxed α7 nicotinic acetylcholine receptor conditional knockout mice using in vitro and in vivo approaches
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MethodSelf-citation
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Background
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Background
Somato‐dendritic nicotinic receptor responses recorded in vitro from the medial septal diagonal band complex of the rodent
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BackgroundSelf-citation
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“In addition, the upregulation of a7 nAChRs elicited by Ab appears to play a role in the coupling of Ab to the mitogen-activated protein kinase cascade and the decreased phosphorylation of cAMP-regulatory element binding protein (Dineley et al., 2001, 2002a).”
Background
Building a More Perfect Beast
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Background
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Background
The occurrence of a deficit in contextual fear extinction in adult amyloid-over-expressing TASTPM mice is independent of the strength of conditioning but can be prevented by mild novel cage stress
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“In our study, the Cisplatin treated group G2 showed higher immunostaining expression of α7 nAChRs than G3, G4, and G5 [26, 27, 29].”
Background
Neuronal and Glial α7 Nicotinic Acetylcholine Receptors: Role in Alzheimer’s Disease Pathophysiology
Rennie, K. (2025) · Life · doi:10.3390/life15071032 · Cited by 11
“In mice co-expressing human mutant APP with a mutant presenilin 1 (PS1; A246E), upregulation of α 7nAChR was even more pronounced than in mice expressing mutant APP alone [79].”
Beta-amyloid peptide-induced modifications in α7 nicotinic acetylcholine receptor immunoreactivity in the hippocampus of the rat: Relationship with GABAergic and calcium-binding proteins perikarya
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Acute inhalation of combustion smoke triggers neuroinflammation and persistent anxiety-like behavior in the mouse
Gorgun, M. F., Zhuo, M., Cortez, I., Dineley, K. T., & Englander, E. W. (2017) · Inhalation Toxicology · doi:10.1080/08958378.2018.1432728 · Cited by 10
“The training was using standard fear conditioning equipment (Med Associates) for a total of 7min following our standard fearconditioning protocol (Dineley et al., 2002; Rodriguez-Rivera et al., 2011).”
BackgroundMethodInfluentialSelf-citation
α7-Nicotinic Acetylcholine Receptors: New Therapeutic Avenues in Alzheimer’s Disease
Öz, M., Petroianu, G. A., & Lorke, D. E. (2016) · Neuromethods · doi:10.1007/978-1-4939-3768-4_9 · Cited by 10
PS1 knockin mice with the Japanese I213T mutation: Effects on exploratory activity, motor coordination, and spatial learning
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Diffusible amyloid oligomers trigger systemic amyloidosis in mice
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Outcome-specific satiety reveals a deficit in context-outcome, but not stimulus- or action-outcome, associations in aged Tg2576 mice.
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Arbovirus infection increases the risk for the development of neurodegenerative disease pathology in the murine model
Fongsaran, C., Jirakanwisal, K., Peng, B.-H., Fracassi, A., Taglialatela, G., Dineley, K. T., Paessler, S., & Cisneros, I. E. (2024) · Brain, Behavior, & Immunity - Health · doi:10.1016/j.bbih.2024.100780 · Cited by 9
“Fear in Tg2576 mice is a common observation made in this genotype (Dineley et al., 2002).”
BackgroundSelf-citation
Harnessing neurogenesis in the adult brain—A role in type 2 diabetes mellitus and Alzheimer's disease
Lazarov, O., Minshall, R. D., & Bonini, M. G. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2020.03.020 · Cited by 9
“…2001), including acquisition of long-term spatial memory (Arendash et al., 2001; Chapman et al., 1999; Chishti et al., 2001; Dewachter et al., 2002; Dineley et al., 2002; Janus et al., 2000; Morgan et al., 2000; Trinchese et al., 2004), spatial reversal learning, utilization of spatial working…”
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β‐Amyloid pathology alters neural network activation during retrieval of contextual fear memories in a mouse model of Alzheimer's disease
Lelos, M. J., & Good, M. A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12527 · Cited by 9
“Indeed, several authors have shown that Tg2576 mice are impaired in freezing to a context paired with footshock (Dineley et al., 2002; Comery et al., 2005; Dong et al., 2005; Ohno et al., 2006; Quinn et al., 2007), as well as demonstrating reduced freezing to a punctuate auditory cue (Corcoran et…”
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The involvement of the cholinergic system in Alzheimer disease
Cuello, A. C. (2025) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19088-9.00005-6 · Cited by 8
Signs of Alzheimer’s Disease: Tied to Aging
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“…[145] TgCRND8 type (K670N/M671L and V717I double mutation in APP gene) [146,147] A β transgenic AD model Mice BRI-A β 42 Type A (BRI protein was used as a carrier to fuse A β 42 to its C-terminus) [148] APP/precocene double-turn AD model Mice PSAPP type (Tg2576 × PSI) [165] APPswe/PS1 ∆ E9 type.”
The Role of Aβ and Tau Oligomers in the Pathogenesis of Alzheimer’s Disease
Bhaskar, K., & Lamb, B. T. (2011) · Springer eBooks · doi:10.1007/978-94-007-2774-8_5 · Cited by 8
Computational investigation of mechanistic insights of Aβ42 interactions against extracellular domain of nAChRα7 in Alzheimer’s disease
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“Another study also showed that the accumulation of Ab results in an upregulation of hippocampal nAChRa7 in aged Tg2576 mice [13,14].”
Background
Molecular Hybridization
Zhang, S., Saathoff, J. M., & Liu, H. (2017) · Elsevier eBooks · doi:10.1016/b978-0-08-101011-2.00008-8 · Cited by 8
Immunization therapy in Alzheimer's disease
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Early Contextual Fear Memory Deficits in a Double-Transgenic Amyloid-βPrecursor Protein/Presenilin 2 Mouse Model of Alzheimer’s Disease
Kishimoto, Y., Fukumoto, K., Nagai, M., Mizuguchi, A., & Kobashi, Y. (2017) · International Journal of Alzheimer s Disease · doi:10.1155/2017/8584205 · Cited by 6
Elevated neuroglobin lessens neuroinflammation and alleviates neurobehavioral deficits induced by acute inhalation of combustion smoke in the mouse
Gorgun, M. F., Zhuo, M., Dineley, K., & Englander, E. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02856-8 · Cited by 6
“OF testing gauges the mouse locomotor performance and exploratory behavior [34, 35, 37], whereas NOR testing serves to assess learning and memory functions [35, 36, 38, 40].”
Self-citation
Links Between Amyloid and Tau Biology in Alzheimer’s Disease and Their Cholinergic Aspects
Siegel, G. J., Chauhan, N. B., & Karczma, A. G. (2007) · Springer eBooks · doi:10.1007/978-0-387-46526-5_10 · Cited by 6
Interaction between ?-amyloid protein and the ?7 nicotinic acetylcholine receptor in cholinergic, gabaergic and calcium-binding proteins-containing neurons in the septum-diagonal band complex of the rat
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Neurobehavioral abnormalities in a brain-specific NADPH-cytochrome P450 reductase knockout mouse model
Fang, C., Bolivar, V. J., Gu, J. H., Yang, W., Zeitlin, S. O., & Ding, X. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.05.027 · Cited by 4
“Fear conditioning with an intensified training paradigm An intensified training paradigm, as previously used to evaluate an Alzheimer’s disease mouse model (Dineley et al., 2002), was adopted in an effort to distinguish contextual memory from conditioning deficit in the fear-conditioning assay.”
Method
Response: Comments on “Memantine Blocks α7* Nicotinic Acetylcholine Receptors More Potently Than N-Methyl-d-aspartate Receptors in Rat Hippocampal Neurons”
Aracava, Y., Pereira, E. F. R., Maelicke, A., & Albuquerque, E. X. (2005) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.104.082222 · Cited by 4
“The work of Dineley et al. (2001, 2002) provided evidence that in the hippocampus of transgenic mice, high levels of A 1-42 lead to increased expression of 7 nAChRs and that A 1-42, acting most likely as an 7 nAChR agonist, causes chronic activation and subsequently down-regulation of the…”
Background
5-HT7 Receptors as Favorable Pharmacological Targets for Drug Discovery
Hedlund, P. B., & Sutcliffe, J. G. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-080-5_18 · Cited by 4
VEEV TC-83 Triggers Dysregulation of the Tryptophan–Kynurenine Pathway in the Central Nervous System That Correlates with Cognitive Impairment in Tg2576 Mice
Fongsaran, C., Dineley, K. T., Paessler, S., & Cisneros, I. E. (2024) · Pathogens · doi:10.3390/pathogens13050397 · Cited by 3
Self-citation
Pleiotropy of Presenilins
Li, A. (2013) · Hereditary Genetics · doi:10.4172/2161-1041.1000e105 · Cited by 3
“Transgenic mice overexpressing the early onset familial AD-associated APP and PSEN1 mutations resulted in accelerated Aβ accumulation and associative learning deficits [28].”
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α7-Nicotinic Acetylcholine Receptors and β-Amyloid Peptides in Alzheimer’s Disease
Lorke, D. E., Petroianu, G. A., & Öz, M. (2016) · Neuromethods · doi:10.1007/978-1-4939-3768-4_10 · Cited by 3
Aging-Related Memory Disorders—Alzheimer’s Disease
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Aging-Related Memory Disorders
Sweatt, J. D. (2003) · Elsevier eBooks · doi:10.1016/b978-012678957-7/50013-x · Cited by 3
Self-citation
Development of a novel alpha7-nicotinic acetylcholine receptor-selective cell-penetrating peptide for intracellular cargo transport
Weber, L., O’Brien, B. C. V., & Weltzin, M. M. (2025) · Drug Delivery · doi:10.1080/10717544.2025.2587378 · Cited by 1
“For example, during early stages of Alzheimer's disease, α7 nAChRs are upregulated in response to chronic exposure to amyloid-β 1-42 (Aβ), which may contribute to hyperexcitability (Liu et al. 2013; Dineley et al. 2002; Rennie 2025).”
Cognition in Rodents
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Authors: Dineley, K. T., Xia, X., Bui, D., Sweatt, J. D., & Zheng, H.
Affiliations: Baylor College of Medicine (US)
Corresponding author: Dineley, Kelly T.
Sweatt, J. David
ORCID: Dineley, Kelly T.
Xia, Xuefeng
Sweatt, J. David
Zheng, Hui
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2002-06
Volume: 277
Issue: 25
Pages: 22768-22780
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m200164200
OpenAlex: W1999234381
Cited by: 212
References: 38
Citations by year: 2026: 1 · 2025: 4 · 2024: 3 · 2023: 2 · 2022: 1 · 2021: 3 · 2020: 6 · 2019: 9 · 2018: 9 · 2017: 10 · 2016: 9 · 2015: 8 · 2014: 10 · 2013: 7 · 2012: 15
FWCI: 7.19
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 6719 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: Alzheimer's Association
National Alliance for Research on Schizophrenia and Depression
National Institutes of Health
National Institute on Aging
National Institute of Mental Health
National Institute of Neurological Disorders and Stroke
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Keywords: familial Alzheimer's disease, presenilin 1, amyloid precursor protein, Tg2576 mice, amyloid-beta deposition, amyloid plaques, contextual fear conditioning, alpha7 nicotinic acetylcholine receptor, dentate gyrus, hippocampus, transgenic mice
MeSH terms: Age Factors, Animals, Behavior, Animal, Fear, Hippocampus, Immunohistochemistry, Learning, Membrane Proteins, Mice, Transgenic, Mutation, Protein Binding, Receptors, Nicotinic, Shock, Time Factors, Immunoblotting, Up-Regulation, Amyloid beta-Protein Precursor, Transgenes, Mice, Presenilin-1, alpha7 Nicotinic Acetylcholine Receptor

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Accelerated Plaque Accumulation, Associative Learning Deficits, and Up-regulation of α7 Nicotinic Receptor Protein in Transgenic Mice Co-expressing Mutant Human Presenilin 1 and Amyloid Precursor Proteins

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