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Upregulation of Surface α4β2 Nicotinic Receptors Is Initiated by Receptor Desensitization after Chronic Exposure to Nicotine
Open accessAbstract
It is hypothesized that desensitization of neuronal nicotinic acetylcholine receptors (nAChRs) induced by chronic exposure to nicotine initiates upregulation of nAChR number. To test this hypothesis directly, oocytes expressing α4β2 receptors were chronically incubated (24–48 hr) in nicotine, and the resulting changes in specific [3 H]nicotine binding to surface receptors on intact oocytes were compared with functional receptor desensitization. Four lines of evidence strongly support the hypothesis. (1) The half-maximal nicotine concentration necessary to produce desensitization (9.7 n m) was the same as that needed to induce upregulation (9.9 n m). (2) The concentration of [3 H]nicotine for half-maximal binding to surface nAChRs on intact oocytes was also similar (11.1 n m), as predicted from cyclical desensitization models. (3) Functional desensitization of α3β4 receptors required 10-fold higher nicotine concentrations, and this was mirrored by a 10-fold shift in concentrations necessary for upregulation. (4) Mutant α4β2 receptors that do not recover fully from desensitization, but not wild-type channels, were upregulated after acute (1 hr) applications of nicotine. Interestingly, the nicotine concentration required for half-maximal binding of α4β2 receptors in total cell membrane homogenates was 20-fold lower than that measured for surface nAChRs in intact oocytes. These data suggest that cell homogenate binding assays may not accurately reflect the in vivo desensitization affinity of surface nAChRs and may account for some of the previously reported differences in the efficacy of nicotine for inducing nAChR desensitization and upregulation.
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“While some combinations of nAChR subunits render receptor complexes more prone to upregulation than others, desensitization is a prominent mechanism that contributes to this upregulation (Fenster et al. 1999).”
From Nicotine Withdrawal (2015) · cites this paper as Fenster et al. 1999
In the citing paper
“Nicotine desensitizes nAChRs and renders them unresponsive and this phenomenon drives an increase in receptor levels as part of an attempt to maintain circuit-level homeostasis [87–89].”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [87]
In the citing paper
“These data suggest there is decreased ACh signaling through some nAChR subtypes during ongoing smoking, but likely to be restored and potentially increased over time (because high affinity nAChRs are upregulated by chronic nicotine use as experienced by smokers (Fenster et al., 1999) as nicotine is cleared during withdrawal.”
From Mood and anxiety regulation by nicotinic acetylcholine receptors: A potential pathway to modulate aggression and related behavioral states (2015) · cites this paper as Fenster et al., 1999
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Bohler, S., Gay, S., Bertrand, S., Corringer, P. J., Edelstein, S. J., Changeux, J., & Bertrand, D. (2001) · Biochemistry · doi:10.1021/bi0020022 · Cited by 41
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Metadata
- Authors
- Fenster, C. P., Whitworth, T. L., Sheffield, E. B., Quick, M. W., & Lester, R. A. J.
- Affiliations
- University of Alabama at Birmingham (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1999-06-15
- Volume
- 19
- Issue
- 12
- Pages
- 4804-4814
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6782670
- OpenAlex
- W4322703267
- Cited by
- 204
- References
- 39
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 4 · 2022: 1 · 2021: 6 · 2020: 9 · 2019: 2 · 2018: 5 · 2017: 6 · 2016: 7 · 2015: 9 · 2014: 9 · 2013: 6 · 2012: 7
- FWCI
- 4.49
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Funders
- W. M. Keck Foundation
- U.S. Public Health Service
- National Institute on Drug Abuse (DA-11940, R01DA011940)
- National Institute of Neurological Disorders and Stroke (NS31699, R29NS031669, R01NS031669)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- nicotinic acetylcholine receptors, alpha4beta2 receptor, receptor desensitization, receptor up-regulation, chronic nicotine exposure, oocyte expression
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