Nicotinic acetylcholine receptor activation induces BACE1 transcription via the phosphorylation and stabilization of nuclear SP1

Epidemiological studies have shown that cigarette smoking increases the risk of Alzheimer disease. However, inconsistent results have been reported regarding the effects of smoking or nicotine on brain amyloid β (Aβ) deposition. In this study, we found that stimulation of the nicotinic acetylcholine...

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Main Authors: Masaki Nakano, Tomohiro Tsuchida, Yachiyo Mitsuishi, Masaki Nishimura
Format: Article
Language:English
Published: Elsevier 2024-06-01
Series:Neuroscience Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S0168010223002195
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author Masaki Nakano
Tomohiro Tsuchida
Yachiyo Mitsuishi
Masaki Nishimura
author_facet Masaki Nakano
Tomohiro Tsuchida
Yachiyo Mitsuishi
Masaki Nishimura
author_sort Masaki Nakano
collection DOAJ
description Epidemiological studies have shown that cigarette smoking increases the risk of Alzheimer disease. However, inconsistent results have been reported regarding the effects of smoking or nicotine on brain amyloid β (Aβ) deposition. In this study, we found that stimulation of the nicotinic acetylcholine receptor (nAChR) increased Aβ production in mouse brains and cultured neuronal cells. nAChR activation triggered the MEK/ERK pathway, which then phosphorylated and stabilized nuclear SP1. Upregulated SP1 acted on two recognition motifs in the BACE1 gene to induce its transcription, resulting in enhanced Aβ production. Mouse brain microdialysis revealed that nAChR agonists increased Aβ levels in the interstitial fluid of the cerebral cortex but caused no delay of Aβ clearance. In vitro assays indicated that nicotine inhibited Aβ aggregation. We also found that nicotine modified the immunoreactivity of anti-Aβ antibodies, possibly through competitive inhibition and Aβ conformation changes. Using anti-Aβ antibody that was carefully selected to avoid these effects, we found that chronic nicotine treatment in Aβ precursor protein knockin mice increased the Aβ content but did not visibly change the aggregated Aβ deposition in the brain. Thus, nicotine influences brain Aβ deposition in the opposite direction, thereby increasing Aβ production and inhibiting Aβ aggregation.
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spelling doaj-art-88fe2a83e4b247a2a779fcf5f11d56fb2024-11-21T06:02:26ZengElsevierNeuroscience Research0168-01022024-06-012032841Nicotinic acetylcholine receptor activation induces BACE1 transcription via the phosphorylation and stabilization of nuclear SP1Masaki Nakano0Tomohiro Tsuchida1Yachiyo Mitsuishi2Masaki Nishimura3Molecular Neuroscience Research Center, Shiga University of Medical Science, Shiga 520-2192, Japan; Corresponding author.Molecular Neuroscience Research Center, Shiga University of Medical Science, Shiga 520-2192, JapanMolecular Neuroscience Research Center, Shiga University of Medical Science, Shiga 520-2192, JapanMolecular Neuroscience Research Center, Shiga University of Medical Science, Shiga 520-2192, Japan; Department of Neurology, Yoka Municipal Hospital, Hyogo 667-8555, Japan; Corresponding author at: Molecular Neuroscience Research Center, Shiga University of Medical Science, Shiga 520-2192, Japan.Epidemiological studies have shown that cigarette smoking increases the risk of Alzheimer disease. However, inconsistent results have been reported regarding the effects of smoking or nicotine on brain amyloid β (Aβ) deposition. In this study, we found that stimulation of the nicotinic acetylcholine receptor (nAChR) increased Aβ production in mouse brains and cultured neuronal cells. nAChR activation triggered the MEK/ERK pathway, which then phosphorylated and stabilized nuclear SP1. Upregulated SP1 acted on two recognition motifs in the BACE1 gene to induce its transcription, resulting in enhanced Aβ production. Mouse brain microdialysis revealed that nAChR agonists increased Aβ levels in the interstitial fluid of the cerebral cortex but caused no delay of Aβ clearance. In vitro assays indicated that nicotine inhibited Aβ aggregation. We also found that nicotine modified the immunoreactivity of anti-Aβ antibodies, possibly through competitive inhibition and Aβ conformation changes. Using anti-Aβ antibody that was carefully selected to avoid these effects, we found that chronic nicotine treatment in Aβ precursor protein knockin mice increased the Aβ content but did not visibly change the aggregated Aβ deposition in the brain. Thus, nicotine influences brain Aβ deposition in the opposite direction, thereby increasing Aβ production and inhibiting Aβ aggregation.http://www.sciencedirect.com/science/article/pii/S0168010223002195Alzheimer's diseaseNicotinic acetylcholine receptorAβBACE1SP1Nicotine
spellingShingle Masaki Nakano
Tomohiro Tsuchida
Yachiyo Mitsuishi
Masaki Nishimura
Nicotinic acetylcholine receptor activation induces BACE1 transcription via the phosphorylation and stabilization of nuclear SP1
Neuroscience Research
Alzheimer's disease
Nicotinic acetylcholine receptor

BACE1
SP1
Nicotine
title Nicotinic acetylcholine receptor activation induces BACE1 transcription via the phosphorylation and stabilization of nuclear SP1
title_full Nicotinic acetylcholine receptor activation induces BACE1 transcription via the phosphorylation and stabilization of nuclear SP1
title_fullStr Nicotinic acetylcholine receptor activation induces BACE1 transcription via the phosphorylation and stabilization of nuclear SP1
title_full_unstemmed Nicotinic acetylcholine receptor activation induces BACE1 transcription via the phosphorylation and stabilization of nuclear SP1
title_short Nicotinic acetylcholine receptor activation induces BACE1 transcription via the phosphorylation and stabilization of nuclear SP1
title_sort nicotinic acetylcholine receptor activation induces bace1 transcription via the phosphorylation and stabilization of nuclear sp1
topic Alzheimer's disease
Nicotinic acetylcholine receptor

BACE1
SP1
Nicotine
url http://www.sciencedirect.com/science/article/pii/S0168010223002195
work_keys_str_mv AT masakinakano nicotinicacetylcholinereceptoractivationinducesbace1transcriptionviathephosphorylationandstabilizationofnuclearsp1
AT tomohirotsuchida nicotinicacetylcholinereceptoractivationinducesbace1transcriptionviathephosphorylationandstabilizationofnuclearsp1
AT yachiyomitsuishi nicotinicacetylcholinereceptoractivationinducesbace1transcriptionviathephosphorylationandstabilizationofnuclearsp1
AT masakinishimura nicotinicacetylcholinereceptoractivationinducesbace1transcriptionviathephosphorylationandstabilizationofnuclearsp1