Nicotine acts as a pharmacological chaperone to up-regulate human α4β2 acetylcholine receptors
Abstract
Human neuronal nicotinic acetylcholine receptor (AChR) alpha4 subunits and an alpha4 mutant (S247Falpha4) found in autosomal-dominant nocturnal frontal lobe epilepsy (ADNFLE) were expressed along with beta2 in permanently transfected tsA201 human embryonic kidney cell lines. Their sensitivity to activation, desensitization, and up-regulation by cholinergic ligands was investigated. Up-regulation after 3 to 24 h resulted primarily from an increase in assembly of AChRs from large pools of unassembled subunits, but up-regulation also resulted from a 5-fold increase in the lifetime of AChRs in the surface membrane. Up-regulation does not require current flow through surface membrane AChRs, because up-regulation occurs in the presence of the channel blocker mecamylamine and with the alpha4 mutant, which prevents nearly all AChR function. Both membrane-permeable ligands like nicotine and much less permeable quaternary amine cholinergic ligands can act as pharmacological chaperones within the endoplasmatic reticulum to promote the assembly of AChRs. Agonists are more potent pharmacological chaperones than antagonists, presumably because activated or desensitized conformations assemble more efficiently. Assembly intermediates are disrupted by solubilization in Triton X-100, but chemical cross-linking stabilizes a putative assembly intermediate approximately the size of an alpha4beta2alpha4beta2 tetramer.
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Current evidence indicates that nicotine, and presumably varenicline, raise nicotinic receptor density by promoting subunit assembly into mature receptors in the endoplasmic reticulum.
“where current evidence indicates that nicotine and presumably varenicline act to increase nAChR density by stimulating assembly of subunits into mature receptors (Sallette et al., 2004(Sallette et al., , 2005;;Kuryatov et al., 2005;Lomazzo et al., 2011;Srinivasan et al., 2011).”
From Chronic Sazetidine-A at Behaviorally Active Doses Does Not Increase Nicotinic Cholinergic Receptors in Rodent Brain (2012) · cites this paper as Kuryatov et al., 2005
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 Kuryatov et al., 2005
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 Kuryatov et al., 2005
Previous results based on glycosylation and molecular weight measures show that up-regulation is initiated in the ER.
“These data correspond with previous results based on glycosylation and molecular weight measures, showing that up-regulation is initiated in the ER (Nelson et al., 2003; Kuryatov et al., 2005; Sallette et al., 2005).”
From Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning (2011) · cites this paper as Kuryatov et al., 2005
Chronic administration of either nicotine or nAChR antagonists results in nAChR up-regulation.
“Moreover, it is well established that chronic administration of either nicotine or nAChR antagonists both result in nAChR up-regulation (Hulihan-Giblin et al., 1990a,b;Kuryatov et al., 2005;Picciotto et al., 2008;Buccafusco et al., 2009).”
From Nicotinic receptor-mediated reduction in l-DOPA-induced dyskinesias may occur via desensitization (2010) · cites this paper as Kuryatov et al., 2005
ACh and other quaternary amine agonists do penetrate into intracellular organelles within ~3 h, albeit much more slowly than nicotine.
“However, in experiments with clonal cell lines, ACh, and other quaternary amine agonists do penetrate into intracellular organelles within ~3 h, albeit much more slowly than nicotine (39).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [39]
Descriptions that may be essentially equivalent to SePhaChARNS are the statements that nicotine acts as a maturational enhancer or a novel slow stabilizer for α4β2* receptors.
“Descriptions that may be essentially equivalent to SePhaChARNS are the statements that nicotine acts as a “maturational enhancer” or a “novel slow stabilizer” for α4β2* receptors (39,50–52).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [39]
Evidence is accumulating to support Lindstrom's proposal that nicotine acts as pharmacological chaperone for nascent nAChRs.
“Evidence is accumulating to support Lindstrom’s proposal that nicotine acts as pharmacological chaperone for nascent nAChRs (39).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [39]
Human α4 harboring a Ser247Phe mutation renders the channel nonfunctional in HEK tsA201 cells, yet chronic nicotine induces robust upregulation of the receptor in this clonal cell line.
“Human α4 harboring a Ser247Phe mutation (at the M2 6′ position) renders the channel nonfunctional in HEK tsA201 cells, and yet chronic nicotine induces robust upregulation of the receptor in this clonal cell line (39).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [39]
During prolonged exposure to nicotine, there is decreased receptor degradation, presumably via endocytosis.
“During prolonged exposure to nicotine, there is deceased receptor degradation (presumably via endocytosis), and this mechanism for upregulation must be considered as an adjunct to SePhaChARNS (8,39,66,87).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [39]
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- Authors
- Kuryatov, A., Luo, J., Cooper, J., & Lindstrom, J.
- Affiliations
- University of Pennsylvania (US)
- ORCID
- Luo, J.
- Venue
- Molecular Pharmacology
- Publisher
- Elsevier BV
- Published
- 2005-12
- Volume
- 68
- Issue
- 6
- Pages
- 1839-1851
- ISSN
- 0026-895X (ISSN-L)
- OpenAlex
- W2285361820
- Cited by
- 275
- References
- 46
- Citations by year
- 2025: 5 · 2024: 4 · 2023: 6 · 2022: 7 · 2021: 3 · 2020: 10 · 2019: 9 · 2018: 8 · 2017: 12 · 2016: 19 · 2015: 24 · 2014: 17 · 2013: 17 · 2012: 22
- FWCI
- 6.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Pharmacology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (NS11323, R01NS011323)
- 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
- nicotine, pharmacological chaperones, nicotinic acetylcholine receptors, alpha4beta2 receptor, receptor up-regulation, receptor assembly, autosomal dominant nocturnal frontal lobe epilepsy, receptor desensitization, mecamylamine, cholinergic ligands, endoplasmic reticulum, Triton X-100 solubilization, crosslinking
- MeSH terms
- Cell Line, Cross-Linking Reagents, Humans, Mutation, Nicotine, Receptors, Nicotinic, Transfection, Up-Regulation, Epilepsy, Frontal Lobe, Octoxynol, Molecular Chaperones, Dimerization, Protein Subunits
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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