Chronic Exposure to Nicotine Upregulates the Human α4β2 Nicotinic Acetylcholine Receptor Function

Buisson, Bruno; Bertrand, Daniel

doi:10.1523/jneurosci.21-06-01819.2001

Cited by 361Nicotinic Acetylcholine Receptors StudySmoking Behavior and CessationNeuroscience and Neuropharmacology Research

Chronic Exposure to Nicotine Upregulates the Human α4β2 Nicotinic Acetylcholine Receptor Function

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Buisson, Bruno, Bertrand, Daniel·2001·The Journal of Neuroscience

DOI 10.1523/jneurosci.21-06-01819.2001PMC PMC6762627

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Abstract

Widely expressed in the brain, the alpha4beta2 nicotinic acetylcholine receptor (nAChR) is proposed to play a major role in the mechanisms that lead to and maintain nicotine addiction. Using the patch-clamp technique and pharmacological protocols, we examined the consequences of long-term exposure to 0.1-10 micrometer nicotine in K-177 cells expressing the major human brain alpha4beta2 receptor. The acetylcholine dose-response curves are biphasic and revealed both a high- and a low-affinity component with apparent EC(50) values of 1.6 and 62 micrometer. Ratios of receptors in the high- and low-affinity components are 25 and 75%, respectively. Chronic exposure to nicotine or nicotinic antagonists [dihydro-beta-erytroidine (DHbetaE) or methyllycaconitine (MLA)] increases the fraction of high-affinity receptors up to 70%. Upregulated acetylcholine-evoked currents increase by twofold or more and are less sensitive to desensitization. Functional upregulation is independent of protein synthesis as shown by the lack of effect of 20 micrometer cycloheximide. Single-channel currents recorded with 100 nm acetylcholine show predominantly high conductances (38.8 and 43.4 pS), whereas additional smaller conductances (16.7 and 23.5 pS) were observed with 30 micrometer acetylcholine. In addition, long-term exposure to dihydro-beta-erytroidine increases up to three times the frequency of channel openings. These data indicate, in contrast to previous studies, that human alpha4beta2 nAChRs are functionally upregulated by chronic nicotine exposure.

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Neuronal nAChR upregulation is an important adaptive change and a major contributor to nicotine's addictive properties.
“Neuronal nAChR upregulation is an important adaptive change and a major contributor to the addictive properties of nicotine [83–86].”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [85]
Nicotine enhances the assembly of functional nAChRs containing the α4 and β2 subunits.
“Data from such favorable systems show that nicotine enhances the assembly of functional nAChRs containing the α4 and β2 subunits and also causes the preferential assembly of receptors with (α4)2(β2)3 stoichiometry (Buisson and Bertrand, 2001; Nelson et al., 2003; Kuryatov et al., 2005; Sallette et al., 2005; Vallejo et al., 2005; Son et al., 2009).”
From Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning (2011) · cites this paper as Buisson and Bertrand, 2001
Nicotine causes the preferential assembly of receptors with (α4)2(β2)3 stoichiometry.
“Data from such favorable systems show that nicotine enhances the assembly of functional nAChRs containing the α4 and β2 subunits and also causes the preferential assembly of receptors with (α4)2(β2)3 stoichiometry (Buisson and Bertrand, 2001; Nelson et al., 2003; Kuryatov et al., 2005; Sallette et al., 2005; Vallejo et al., 2005; Son et al., 2009).”
From Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning (2011) · cites this paper as Buisson and Bertrand, 2001
Chronic nicotine exposure shifts nAChR stoichiometry from approximately equal contributions of the two stoichiometries in nicotine-naive cells to ∼100% (α4)2(β2)3.
“In fact, our experiments and previous data (Buisson and Bertrand, 2001; Nelson et al., 2003; Kuryatov et al., 2005; Sallette et al., 2005; Vallejo et al., 2005; Son et al., 2009) suggest a shift from approximately equal contributions of the two stoichiometries in nicotine-naive cells to ∼100% (α4)2(β2)3 after chronic nicotine exposure.”
From Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning (2011) · cites this paper as Buisson and Bertrand, 2001
α4β2 receptors exist in a mixed population whose nicotine EC50 values differ by 50- to 100-fold (~1 and ~100 μM).
“The α4β2 receptors exist in a mixed population whose nicotine EC50 values differ by 50- to 100-fold (70–73) (~1 and ~100 μM).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [72]

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“One of the most direct and important neuroadaptations induced by chronic nicotine use is the subtype-specific upregulation of nAChRs (Buisson & Bertrand 2001; Changeux et al. 1984; Dani & Heinemann 1996; Flores et al. 1997; Mansvelder et al. 2002; Marks et al. 1983, 1992; Perry et al. 1999; Rezvani…”
Background
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“…nAChR availability is not associated with changes in 2*-nAChR mRNA (Marks et al., 1992; Peng et al., 1994; Zhang et al., 1994) protein synthesis (Buisson and Bertrand, 2001), rate of receptor internalization, postendocytic trafficking, or lysosomal degradation (Darsow et al., 2005), but instead…”
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Authors: Buisson, B., & Bertrand, D.
Affiliations: University of Geneva (CH)
ORCID: Bertrand, Daniel
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2001-03-15
Volume: 21
Issue: 6
Pages: 1819-1829
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.21-06-01819.2001
PMC: PMC6762627
OpenAlex: W2153609942
Cited by: 361
References: 74
Citations by year: 2026: 3 · 2025: 5 · 2024: 9 · 2023: 4 · 2022: 5 · 2021: 3 · 2020: 10 · 2019: 9 · 2018: 7 · 2017: 7 · 2016: 13 · 2015: 7 · 2014: 15 · 2013: 12 · 2012: 16
FWCI: 8.03
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: α4β2 nicotinic acetylcholine receptor, chronic nicotine exposure, receptor up-regulation, nicotine dependence, dihydro-beta-erythroidine, methyllycaconitine, receptor desensitization, single-channel conductance, nicotinic antagonists
MeSH terms: Acetylcholine, Aconitine, Cell Line, Dose-Response Relationship, Drug, Electrophysiology, Humans, Ion Channels, Kidney, Nicotine, Protein Synthesis Inhibitors, Receptors, Nicotinic, Time Factors, Transfection, Up-Regulation, Patch-Clamp Techniques, Nicotinic Antagonists

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Chronic Exposure to Nicotine Upregulates the Human α4β2 Nicotinic Acetylcholine Receptor Function

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