Cholinotrophic basal forebrain system alterations in 3xTg-AD transgenic mice

Perez, Sylvia E.; He, Bin; Muhammad, Nadeem; Oh, Kwang-Jin; Fahnestock, Margaret; Ikonomovic, Milos D.; Mufson, Elliott J.

doi:10.1016/j.nbd.2010.10.002

Cited by 80Alzheimer's disease research and treatmentsCholinesterase and Neurodegenerative DiseasesNeuroscience and Neuropharmacology Research

Cholinotrophic basal forebrain system alterations in 3xTg-AD transgenic mice

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Perez, Sylvia E., He, Bin, Muhammad, Nadeem, Oh, Kwang-Jin, Fahnestock, Margaret, Ikonomovic, Milos D., Mufson, Elliott J.·2011·Neurobiology of Disease

DOI 10.1016/j.nbd.2010.10.002PMC PMC3014453

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Abstract

The cholinotrophic system, which is dependent upon nerve growth factor and its receptors for survival, is selectively vulnerable in Alzheimer's disease (AD). But, virtually nothing is known about how this deficit develops in relation to the hallmark lesions of this disease, amyloid plaques and tau containing neurofibrillary tangles. The vast majority of transgenic models of AD used to evaluate the effect of beta amyloid (Aβ) deposition upon the cholinotrophic system over-express the amyloid precursor protein (APP). However, nothing is known about how this system is affected in triple transgenic (3xTg)-AD mice, an AD animal model displaying Aβ plaque- and tangle-like pathology in the cortex and hippocampus, which receive extensive cholinergic innervation. We performed a detailed morphological and biochemical characterization of the cholinotrophic system in young (2-4 months), middle-aged (13-15 months) and old (18-20 months) 3xTg-AD mice. Cholinergic neuritic swellings increased in number and size with age, and were more conspicuous in the hippocampal-subicular complex in aged female than in 3xTg-AD male mice. Stereological analysis revealed a reduction in choline acetyltransferase (ChAT) positive cells in the medial septum/vertical limb of the diagonal band of Broca in aged 3xTg-AD mice. ChAT enzyme activity levels decreased significantly in the hippocampus of middle-aged 3xTg-AD mice compared to age-matched non-transgenic (or wild type) mice. ProNGF protein levels increased in the cortex of aged 3xTg-AD mice, whereas TrkA protein levels were reduced in a gender-dependent manner in aged mutant mice. In contrast, p75(NTR) protein cortical levels were stable but increased in the hippocampus of aged 3xTg-AD mice. These data demonstrate that cholinotrophic alterations in 3xTg-AD mice are age- and gender-dependent and more pronounced in the hippocampus, a structure more severely affected by Aβ plaque pathology.

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The increase of FA and KFA in the hippocampus may be related to the progressive loss of cholinergic unmyelinated axons, resulting in a more aligned, anisotropic environment.
“The increase of FA and KFA in the hippocampus may be related to the progressive loss of cholinergic unmyelinated axons [9], resulting in a more aligned, anisotropic environment.”
From Brain microstructure abnormalities in the 3xTg-AD mouse – A diffusion MRI and morphology correlation study (2022) · cites this paper as [9]
The Results section reports a qualitative decrease in cholinergic fiber staining in the subiculum of aged female 3xTg-AD mice, less obvious in the hippocampus proper. The Discussion says the study did not count fibers; it cites other studies for age-dependent fiber loss. Thus, this paper supports cholinergic fiber alteration but does not establish progressive loss of unmyelinated hippocampal axons. The FA/KFA explanation is the citing authors’ proposed interpretation, not a finding attributed to this source. (LLM, conf=0.86)
Experimental — accuracy not yet measured
The 3xTg-AD mouse has synaptic and cholinergic degeneration deficits.
“synaptic and cholinergic degeneration deficits (Perez et al., 2011)”
From Early stage alterations in white matter and decreased functional interhemispheric hippocampal connectivity in the 3xTg mouse model of Alzheimer’s disease. (2019) · cites this paper as Perez et al., 2011
The Discussion section reports age-dependent cholinergic neuritic dystrophy and reduced cholinergic fiber density in 3xTg-AD mice. It does not report synaptic degeneration in these mice; the synaptic findings located in our copy appear only in titles in the References section. No page numbers are available in our copy. (LLM, conf=0.86)
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Olfactory receptor neurons express D2 dopamine receptors
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Neuropathology of Mice Carrying Mutant APPswe and/or PS1M146L Transgenes: Alterations in the p75NTR Cholinergic Basal Forebrain Septohippocampal Pathway
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The impact of Aβ-plaques on cortical cholinergic and non-cholinergic presynaptic boutons in alzheimer's disease-like transgenic mice
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Distribution of nerve growth factor‐like immunoreactive neurons in the adult rat brain following colchicine treatment
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Structural involvement of the glutamatergic presynaptic boutons in a transgenic mouse model expressing early onset amyloid pathology
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TrkA pathway activation induced by amyloid-beta (Abeta)
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Amyloid-Beta: A Crucial Factor in Alzheimer's Disease
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Systematic Phenotyping and Characterization of the 3xTg-AD Mouse Model of Alzheimer’s Disease
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Updates on mouse models of Alzheimer’s disease
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Acetyl-CoA the Key Factor for Survival or Death of Cholinergic Neurons in Course of Neurodegenerative Diseases
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Targeting Synaptic Plasticity in Experimental Models of Alzheimer’s Disease
Mango, D., Saidi, A., Cisale, G. Y., Feligioni, M., Corbo, M., & Nisticò, R. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00778 · Cited by 109 · see citing works
Deciphering Proneurotrophin Actions
Hempstead, B. L. (2014) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-45106-5_2 · Cited by 106 · see citing works
Sexual Dimorphism in the 3xTg-AD Mouse Model and Its Impact on Pre-Clinical Research
Dennison, J. L., Ricciardi, N. R., Lohse, I., Volmar, C., & Wahlestedt, C. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-201014 · Cited by 100 · see citing works
A Small Molecule p75NTR Ligand, LM11A-31, Reverses Cholinergic Neurite Dystrophy in Alzheimer's Disease Mouse Models with Mid- to Late-Stage Disease Progression
Simmons, D. A., Knowles, J. K., Belichenko, N. P., Banerjee, G., Finkle, C., Massa, S. M., & Longo, F. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102136 · Cited by 97 · see citing works
Alzheimer's disease pathology in the neocortex and hippocampus of the western lowland gorilla (Gorilla gorilla gorilla)
Perez, S. E., Raghanti, M. A., Hof, P. R., Kramer, L., Ikonomovic, M. D., Lacor, P. N., Erwin, J. M., Sherwood, C. C., & Mufson, E. J. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23428 · Cited by 95 · see citing works
“This dual staining resulted in an easily identifiable two-colored profile: dark blue/black for Alz50 and ChAT profiles and brown or red for APP/Ab-positive plaques/blood vessels (Perez et al., 2011, 2012a).”
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Small Molecule p75NTR Ligands Reduce Pathological Phosphorylation and Misfolding of Tau, Inflammatory Changes, Cholinergic Degeneration, and Cognitive Deficits in AβPPL/S Transgenic Mice
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Sleep and EEG Power Spectral Analysis in Three Transgenic Mouse Models of Alzheimer’s Disease: APP/PS1, 3xTgAD, and Tg2576
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Differential deregulation of NGF and BDNF neurotrophins in a transgenic rat model of Alzheimer's disease
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ProNGF\NGF imbalance triggers learning and memory deficits, neurodegeneration and spontaneous epileptic-like discharges in transgenic mice
Tiveron, C., Fasulo, L., Capsoni, S., Malerba, F., Marinelli, S., Paoletti, F., Piccinin, S., Scardigli, R., Amato, G., Brandi, R., et al. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.22 · Cited by 77 · see citing works
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Dissociable cognitive impairments in two strains of transgenic Alzheimer’s disease mice revealed by a battery of object-based tests
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Chronic 5-HT4 receptor activation decreases Aβ production and deposition in hAPP/PS1 mice.
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Liver X receptor activation attenuates inflammatory response and protects cholinergic neurons in APP/PS1 transgenic mice
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Early stage alterations in white matter and decreased functional interhemispheric hippocampal connectivity in the 3xTg mouse model of Alzheimer’s disease.
Manno, F. A. M., Isla, A. G., Manno, S. H. C., Ahmed, I., Cheng, S. H., Barrios, F. A., & Lau, C. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00039 · Cited by 49 · see citing works
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Rac1b Increases with Progressive Tau Pathology within Cholinergic Nucleus Basalis Neurons in Alzheimer's Disease
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Effects of Maternal Choline Supplementation on the Septohippocampal Cholinergic System in the Ts65Dn Mouse Model of Down Syndrome
Kelley, C. M., Ash, J. A., Powers, B. E., Velázquez, R., Alldred, M. J., Ikonomović, M. D., Ginsberg, S. D., Strupp, B. J., & Mufson, E. J. (2015) · Current Alzheimer Research · doi:10.2174/1567205012666150921100515 · Cited by 43 · see citing works
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Neutralization of Nerve Growth Factor Impairs Proliferation and Differentiation of Adult Neural Progenitors in the Subventricular Zone
Scardigli, R., Capelli, P., Vignone, D., Brandi, R., Ceci, M., Regina, F. L., Piras, E., Cintoli, S., Berardi, N., Capsoni, S., et al. (2014) · Stem Cells · doi:10.1002/stem.1744 · Cited by 37 · see citing works
Sex Steroid Levels and AD ‐Like Pathology in 3x T g AD Mice
Overk, C., Pérez, S. E., Ma, C., Taves, M. D., Soma, K. K., & Mufson, E. J. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02374.x · Cited by 34 · see citing works
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Immunolesion‐induced loss of cholinergic projection neurones promotes β‐amyloidosis and tau hyperphosphorylation in the hippocampus of triple‐transgenic mice
Härtig, W., Saul, A., Kacza, J., Grosche, J., Goldhammer, S., Michalski, D., & Wirths, O. (2014) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12050 · Cited by 34 · see citing works
Sex-Dependent Differences in Spontaneous Autoimmunity in Adult 3xTg-AD Mice
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Small molecule modulation of TrkB and TrkC neurotrophin receptors prevents cholinergic neuron atrophy in an Alzheimer's disease mouse model at an advanced pathological stage
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The Medial Septum Is Insulin Resistant in the AD Presymptomatic Phase: Rescue by Nerve Growth Factor-Driven IRS1 Activation
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Cholinergic neurodegeneration in Alzheimer disease mouse models
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Effects of Reactive Oxygen and Nitrogen Species on TrkA Expression and Signalling: Implications for proNGF in Aging and Alzheimer’s Disease
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Diffusion MRI detects basal forebrain cholinergic abnormalities in the 3xTg‐AD mouse model of Alzheimer's disease
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Involvement of Insulin-Like Growth Factor 1 Receptor Signaling in the Amyloid-β Peptide Oligomers-Induced p75 Neurotrophin Receptor Protein Expression in Mouse Hippocampus
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Dimebon alters hippocampal amyloid pathology in 3xTg-AD mice.
Perez, S. E., Nadeem, M., Sadleir, K. R., Matras, J., Kelley, C. M., Counts, S., Vassar, R. J., & Mufson, E. J. (2012) · Europe PMC (PubMed Central) · Cited by 26 · see citing works
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Activity of muscarinic, galanin and cannabinoid receptors in the prodromal and advanced stages in the triple transgenic mice model of Alzheimer’s disease
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Sex-related dimorphism in dentate gyrus atrophy and behavioral phenotypes in an inducible tTa:APPsi transgenic model of Alzheimer's disease
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Function and Redox State of Peritoneal Leukocytes as Preclinical and Prodromic Markers in a Longitudinal Study of Triple-Transgenic Mice for Alzheimer's Disease
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Endocannabinoid and Muscarinic Signaling Crosstalk in the 3xTg-AD Mouse Model of Alzheimer’s Disease
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Noradrenergic Sympathetic Sprouting and Cholinergic Reinnervation Maintains Non-Amyloidogenic Processing of AβPP
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G-Protein-Coupled Inwardly Rectifying Potassium (GIRK) Channel Activation by the p75 Neurotrophin Receptor Is Required for Amyloid β Toxicity
May, L. M., Anggono, V., Gooch, H. M., Jang, S. E., Matusica, D., Kerbler, G. M., Meunier, F. A., Sah, P., & Coulson, E. J. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00455 · Cited by 22 · see citing works
Ovariectomy-induced hormone deprivation aggravates Aβ1-42 deposition in the basolateral amygdala and cholinergic fiber loss in the cortex but not cognitive behavioral symptoms in a triple transgenic mouse model of Alzheimer’s disease
Farkas, S., Szabó, A., Török, B., Sólyomvári, C., Fazekas, C. L., Bánrévi, K., Correia, P., Chaves, T., & Zelena, D. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.985424 · Cited by 24 · see citing works
Inhibition of 5α Reductase Impairs Cognitive Performance, Alters Dendritic Morphology and Increases Tau Phosphorylation in the Hippocampus of Male 3xTg-AD Mice
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Effect of Neocortical and Hippocampal Amyloid Deposition upon Galaninergic and Cholinergic Neurites in AβPPswe/PS1ΔE9 Mice
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Accumulation and age-related elevation of amyloid-β within basal forebrain cholinergic neurons in the rhesus monkey
Norvin, D., Kım, G., Baker‐Nigh, A., & Geula, C. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.011 · Cited by 19 · see citing works
Genotype Load Modulates Amyloid Burden and Anxiety-Like Patterns in Male 3xTg-AD Survivors despite Similar Neuro-Immunoendocrine, Synaptic and Cognitive Impairments
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Authors: Perez, S. E., He, B., Muhammad, N., Oh, K.-J., Fahnestock, M., Ikonomovic, M. D., & Mufson, E. J.
Affiliations: Rush University Medical Center (US)
McMaster University (CA)
Corresponding author: Mufson, Elliott J.
ORCID: Perez, Sylvia E.
Oh, Kwang-Jin
Fahnestock, Margaret
Mufson, Elliott J.
Venue: Neurobiology of Disease
Publisher: Elsevier BV
Published: 2011-02
Volume: 41
Issue: 2
Pages: 338-352
ISSN: 0969-9961 (ISSN-L)
DOI: 10.1016/j.nbd.2010.10.002
PMC: PMC3014453
OpenAlex: W2013770936
Cited by: 80
References: 96
Citations by year: 2026: 2 · 2025: 3 · 2024: 5 · 2023: 5 · 2022: 5 · 2021: 11 · 2020: 1 · 2019: 6 · 2018: 5 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 7 · 2013: 8 · 2012: 6
FWCI: 3.47
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Neurobiology of Disease (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institute on Aging (P01AG014449, AG10688, R01AG043375, R01AG010668)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Pharmacology › Cholinesterase and Neurodegenerative Diseases
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: Alzheimer's disease, 3xTg-AD mice, nerve growth factor, choline acetyltransferase, medial septum, diagonal band of Broca, hippocampus, amyloid plaques, neurofibrillary tangles, amyloid-beta, proNGF, TrkA, p75 neurotrophin receptor, age-related changes, sex differences, cholinergic innervation
MeSH terms: Acetylcholine, Aging, Alzheimer Disease, Animals, Cholinergic Fibers, Disease Models, Animal, Female, Hippocampus, Humans, Male, Mice, Transgenic, Sex Characteristics, Amyloid beta-Peptides, Basal Nucleus of Meynert, Mice, Plaque, Amyloid

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Cholinotrophic basal forebrain system alterations in 3xTg-AD transgenic mice

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