Evidence that transmitter‐containing dystrophic neurites precede paired helical filament and Alz‐50 formation within senile plaques in the amygdala of nondemented elderly and patients with Alzheimer's disease

Benzing, William C.; Ikonomovic, Milos D.; Brady, Daniel R.; Mufson, Elliott J.; Armstrong, David M.

doi:10.1002/cne.903340203

Cited by 46Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

Evidence that transmitter‐containing dystrophic neurites precede paired helical filament and Alz‐50 formation within senile plaques in the amygdala of nondemented elderly and patients with Alzheimer's disease

Benzing, William C., Ikonomovic, Milos D., Brady, Daniel R., Mufson, Elliott J., Armstrong, David M.·1993·Journal of Comparative Neurology

DOI 10.1002/cne.903340203

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Abstract

Immunocytochemical techniques were employed to examine the temporal ordering whereby amyloid β‐protein (AβP) and neuronal elements collectively come together to form senile plaques in Alzheimer's disease (AD). Specifically, we addressed three questions: (1) whether AβP deposition precedes or follows neuritic changes; (2) whether paired helical filament (PHF) formation is an early or late event in the genesis of the dystrophic neurites which participate in plaque formation; and (3) whether the density of senile plaques displays any relationship with the prevalence of PHF or Alz‐50 containing neurons. To address these questions we studied the amygdala from a group of patients with AD, a group of nondemented age‐matched individuals exhibiting a sufficient number of senile plaques to be classified by neuropathological criteria as AD, and a group of age‐matched controls without AD pathology. Amyloid‐bearing plaques were demonstrated by AβP immunolabeling and thioflavine‐S staining. Neuritic changes in the form of dystrophic neurites were observed with the aid of antibodies against PHF, Alz‐50, as well as antibodies against several neuropeptides (i.e., substance P, somatostatin, and neurotensin) and the acetylcholine biosynthetic enzyme, choline acetyltransferase. By using a graded range of pathologic changes both within and across the patient population to provide us with a means of evaluating plaque deposition from its earliest to most advanced stages of development, we observed in patients and/or regions of the amygdala displaying a mild degree of pathologic change AβP deposition in the absence of any neuritic changes. With increasing density of AβP, however, we began to observe dystrophic neurites within plaques. In regions of relatively few plaques, the dystrophic neurites were immunolabeled only with antibodies against the various neurotransmitters and they lacked evidence of cytoskeletal pathology (i.e., Alz‐50 or PHF). Only as the density of AβP increased further within a region, were dystrophic neurites observed that exhibited Alz‐50 or PHF. In no instance did we observe a relationship between the density of AβP deposition and the density of Alz‐50 or PHF‐immunoreactive neurons. Collectively, our data suggest that the deposition of AβP is an early pathologic event in senile plaque formation. Thereafter, swollen neurites can be seen in the vicinity of AβP. This early neuritic response, which can first be visualized by immunolabeling for one or another transmitter substance, is followed by alterations in the cytoskeleton as recognized initially by antibodies to Alz‐50 and subsequently by the presence of PHF. © 1993 Wiley‐Liss, Inc.

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NPs represent a nidus in which extracellular plaque substance(s) seem to induce intracellular degenerative changes with tau pathology.
“The particular toxic substance(s) within NPs still have not been completely characterized (90, 103, 278), but NPs represent a nidus in which extracellular plaque substance(s) seem to induce intracellular degenerative changes with tau pathology (18, 50, 279-281).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [279]

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Evidence that transmitter-containing dystrophic neurites precede those containing paired helical filaments within senile plaques in the entorhinal cortex of nondemented elderly and Alzheimer's disease patients
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Authors: Benzing, W. C., Ikonomovic, M. D., Brady, D. R., Mufson, E. J., & Armstrong, D. M.
Affiliations: Rush University Medical Center (US)
National Institutes of Health (US)
Georgetown University (US)
Corresponding author: Armstrong, David M.
ORCID: Mufson, Elliott J.
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 1993-08-08
Volume: 334
Issue: 2
Pages: 176-191
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.903340203
OpenAlex: W2004803322
Cited by: 46
References: 69
Citations by year: 2022: 1 · 2020: 1 · 2017: 1 · 2015: 1 · 2012: 2
FWCI: 3.46
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 4080 d)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01ag008206-15)
National Institute on Aging (AG 08206, AG-05344, AG10688)
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: Alzheimer's disease, amyloid plaques, amyloid-beta, paired helical filaments, dystrophic neurites, amygdala, neuropeptides, substance P, somatostatin, neurotensin, choline acetyltransferase, neuropathology, non-demented elderly, thioflavine S
MeSH terms: Adult, Aged, Aged, 80 and over, Alzheimer Disease, Amygdala, Antigens, Choline O-Acetyltransferase, Female, Humans, Immunohistochemistry, Male, Middle Aged, Neurotensin, Somatostatin, Substance P, Amyloid beta-Peptides, Neurites, Neurofibrillary Tangles

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Evidence that transmitter‐containing dystrophic neurites precede paired helical filament and Alz‐50 formation within senile plaques in the amygdala of nondemented elderly and patients with Alzheimer's disease

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