Nicotine enhances intracellular nicotinic receptor maturation: a novel mechanism of neural plasticity?

Corringer, Pierre-Jean; Sallette, Jérôme; Changeux, Jean-Pierre

doi:10.1016/j.jphysparis.2005.12.012

Cited by 86Nicotinic Acetylcholine Receptors StudySmoking Behavior and CessationNeuroscience and Neuropharmacology Research

Nicotine enhances intracellular nicotinic receptor maturation: a novel mechanism of neural plasticity?

Corringer, Pierre-Jean, Sallette, Jérôme, Changeux, Jean-Pierre·2006·Journal of Physiology-Paris

DOI 10.1016/j.jphysparis.2005.12.012

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Abstract

Nicotine addiction, the primary cause of tobacco consumption, is mediated through nicotine binding to brain nicotinic acetylcholine receptor (nAChRs). Upon chronic exposure, nicotine elicits a cascade of events, starting with nAChR activation and desensitization, followed by a long term up-regulation that corresponds to an increase in the number of the high affinity nAChRs, a paradoxical process that occurs in the brain of smokers. Recent investigation of the maturation and trafficking of the major brain alpha4beta2 nAChR demonstrates that up-regulation is initiated in the endoplasmic reticulum soon after protein translation. The data thus far accumulated provide evidence that nicotine elicits up-regulation by promoting maturation of nAChR precursors that would otherwise be degraded. This "maturational enhancer" action of nicotine probably contributes to the long term effect of chronic nicotine, and suggests a novel mechanism of neuronal plasticity through an yet unknown endogenous substance which would modulate the receptor expression under physiological conditions.

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Nicotine initially activates and then subsequently desensitizes or inactivates nAChRs, with a consequent receptor block.
“The molecular basis for these seemingly discrepant observations may relate to findings that nicotine initially activates and then subsequently desensitizes or inactivates nAChRs, with a consequent receptor block (Corringer et al., 2006;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 Corringer et al., 2006
Desensitization most likely involves post-translational receptor changes including receptor phosphorylation.
“Desensitization most likely involves post-translational receptor changes including receptor phosphorylation (Corringer et al., 2006;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 Corringer et al., 2006

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“Other mechanisms that likely contribute to upregulation are decreased surface receptor turnover (Peng et al. 1997) and increased receptor assembly at the endoplasmic reticulum (Corringer et al. 2006; Darsow et al. 2005; Rezvani et al. 2007, 2010; Sallette et al. 2005).”
Background
α4β2 Nicotinic Receptors with High and Low Acetylcholine Sensitivity: Pharmacology, Stoichiometry, and Sensitivity to Long-Term Exposure to Nicotine
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Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity
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Nicotinic receptors, allosteric proteins and medicine
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Long-term consequences of maternal smoking and developmental chronic nicotine exposure
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IgE-induced degranulation of mucosal mast cells is negatively regulated via nicotinic acetylcholine receptors
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Nicotinic receptor-mediated reduction in l-DOPA-induced dyskinesias may occur via desensitization
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β3 Subunits Promote Expression and Nicotine-Induced Up-Regulation of Human Nicotinic α6* Nicotinic Acetylcholine Receptors Expressed in Transfected Cell Lines
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Pharmacological Chaperoning of Nicotinic Acetylcholine Receptors Reduces the Endoplasmic Reticulum Stress Response
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Evidence for a role of nicotinic acetylcholine receptors in schizophrenia
Catherine, E. A. (2007) · Frontiers in bioscience · doi:10.2741/2424 · Cited by 63 · see citing works
Lending a helping hand, screening chemical libraries for compounds that enhance β‐hexosaminidase A activity in GM2 gangliosidosis cells
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Nicotine-Modulated Subunit Stoichiometry Affects Stability and Trafficking of 3 4 Nicotinic Receptor
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Neurophysiology of Nicotine Addiction
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GABA acts as a ligand chaperone in the early secretory pathway to promote cell surface expression of GABAA receptors
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Nicotine and Behavioral Sensitization
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Cellular trafficking of nicotinic acetylcholine receptors
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Intracellular localization of nicotinic acetylcholine receptors in human cell lines
Kalashnyk, O., Gergalova, G., Комісаренко, С. В., & Skok, M. V. (2012) · Life Sciences · doi:10.1016/j.lfs.2012.02.005 · Cited by 45 · see citing works
Tolerance to the sedative and anxiolytic effects of diazepam is associated with different alterations of GABAA receptors in rat cerebral cortex
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α7‐type acetylcholine receptor localization and its modulation by nicotine and cholesterol in vascular endothelial cells
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Nicotine primes the effect of cocaine on the induction of LTP in the amygdala
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High-affinity nicotinic acetylcholine receptor expression and trafficking abnormalities in psychiatric illness
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Effects of chronic nicotine on heteromeric neuronal nicotinic receptors in rat primary cultured neurons
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Structural answers and persistent questions about how nicotinic receptors work
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Nicotinic acetylcholine receptors in cancer: Limitations and prospects
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The retrotrapezoid nucleus and the neuromodulation of breathing
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Smoking Cessation Pharmacotherapy—Nicotine and Non‐Nicotine Preparations
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SARS-CoV-2 spike ectodomain targets α7 nicotinic acetylcholine receptors
O’Brien, B. C. V., Weber, L., Hueffer, K., & Weltzin, M. M. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104707 · Cited by 32 · see citing works
Synaptogenèses et épigenèses cérébrales
Bourgeois, J. (2005) · médecine/sciences · doi:10.1051/medsci/2005214428 · Cited by 29 · see citing works
bPiDI: a novel selective α6β2* nicotinic receptor antagonist and preclinical candidate treatment for nicotine abuse
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Chronic nicotine treatment decreases LPS signaling through NF-κB and TLR-4 modulation in the hippocampus
Café-Mendes, C. C., Garay-Malpartida, M., Malta, M. B., Lima, L. D. S., Scavone, C., Ferreira, Z. S., Markus, R. P., & Marcourakis, T. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.10.056 · Cited by 29 · see citing works
Nicotine-induced changes of glutamate and arginine in naive and chronically alcoholized rats: An in vivo microdialysis study
Lallemand, F., Ward, R. J., Драволина, О. А., & Witte, P. D. (2006) · Brain Research · doi:10.1016/j.brainres.2006.06.083 · Cited by 27 · see citing works
Smoking cessation pharmacotherapy
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Alpha7 Nicotinic Acetylcholine Receptor Expression and Activity During Neuronal Differentiation of PC12 Pheochromocytoma Cells
Nery, A. A., Resende, R. R., Martins, A. H. B., Trujillo, C. A., Eterović, V. A., & Ulrich, H. (2010) · Journal of Molecular Neuroscience · doi:10.1007/s12031-010-9369-2 · Cited by 22 · see citing works
Expression of cloned α6* nicotinic acetylcholine receptors
Wang, J., Kuryatov, A., & Lindstrom, J. M. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.10.009 · Cited by 20 · see citing works
Pharmacological Chaperones: Beyond Conformational Disorders
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r-bPiDI, an α6β2* Nicotinic Receptor Antagonist, Decreases Nicotine-Evoked Dopamine Release and Nicotine Reinforcement
Beckmann, J. S., Meyer, A. C., Pivavarchyk, M., Horton, D. B., Zheng, G., Smith, A. M., Wooters, T. E., McIntosh, J. M., Crooks, P. A., Bardo, M. T., et al. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1680-4 · Cited by 17 · see citing works
Decreased α4β2 nicotinic receptor number in the absence of mRNA changes suggests post‐transcriptional regulation in the spontaneously hypertensive rat model of ADHD
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Repeated nicotine administration robustly increases bPiDDB inhibitory potency at α6β2-containing nicotinic receptors mediating nicotine-evoked dopamine release
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Choline Promotes Nicotinic Receptor α4 + β2 Up-regulation
Gahring, L. C., Vasquez-Opazo, G. A., & Rogers, S. W. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.108803 · Cited by 15 · see citing works
Does smoking reduce the risk of Parkinson’s disease through stimulation of the ubiquitin–proteasome system?
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Targeting Reward-Relevant Nicotinic Receptors in the Discovery of Novel Pharmacotherapeutic Agents to Treat Tobacco Dependence
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Elevated Hippocampal Cholinergic Neurostimulating Peptide precursor protein (HCNP-pp) mRNA in the amygdala in major depression
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Differences in Nicotine Encoding Dopamine Release between the Striatum and Shell Portion of the Nucleus Accumbens
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Discovery of a novel nicotinic receptor antagonist for the treatment of nicotine addiction: 1-(3-Picolinium)-12-triethylammonium-dodecane dibromide (TMPD)
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Probing the Allosteric Role of the α5 Subunit of α3β4α5 Nicotinic Acetylcholine Receptors by Functionally Selective Modulators and Ligands
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Abundant extrasynaptic expression of α3β4-containing nicotinic acetylcholine receptors in the medial habenula–interpeduncular nucleus pathway in mice
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Tobacco Nitrosamine N-nitrosonornicotine as Inhibitor of Neuronal Nicotinic Acetylcholine Receptors
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Evaluation of Chronic Oral Nicotine Treatment in Food Consumption, Body Weight and [125I] Epibatidine Binding in Adult Mice
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Unraveling the Role of CHRNA6, the Neuronal α6 Nicotinic Acetylcholine Receptor Subunit
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There is no healthy level of smoking.
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Molecular Dynamics Simulation of Kynurenine Aminotransferase Type II with Nicotine as a Ligand: A Possible Biochemical Role of Nicotine in Schizophrenia
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Administration of Nicotine Can Inhibit Myopic Growth in Animal Models
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CHRFAM7A overexpression in human iPSC-derived Interneurons dysregulates α7- nAChR surface expression and alters response to oligomeric β-amyloid peptidePreprint
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Haubner, A. J. (2008) · UKnowledge (University of Kentucky)
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Involvement of the Cholinergic System in Levodopa-Induced Dyskinesia
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Evidence for the involvement of adenomatous polyposis coli (APC) protein in maintaining cellular distributions of α3β4 nicotinic receptors
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The Effects of Nicotine on the Regulation of Neuronal Alpha7 Nicotinic Acetylcholine Receptors and Intracellular Signalling Pathways
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Dynamics and function of nicotinic acetylcholine receptors in the nervous system
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Smoking-Related Genes and Functional Consequences
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TOWARDS AN UNDERSTANDING OF PHARMACOLOGICALLY INDUCED INTRACELLULAR CHANGES IN NICOTINIC ACETYLCHOLINE RECEPTORS
Fox-Loe, A. M. (2016) · UKnowledge (University of Kentucky) · doi:10.13023/etd.2016.461
Does Pre-cessation Physical Activity Impact Smoking Treatment Outcomes? A Longitudinal Study of Treatment-seeking Smokers in the General Population
Hoang, M. (2020) · TSpace (University of Toronto)
Central Cholinergic Nervous System and Its Correlates
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Genetic regulation of endoplasmic reticulum chaperones and pro-inflammatory cytokines by neuronal α4β2 nicotinic receptors
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Rôle des récepteurs nicotiniques des circuits de l'addiction à la nicotine : une manipulation originale des récepteurs grâce à la lumière
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Diversité des effets de la nicotine sur les neurones dopaminergiques de l’aire tegmentale ventrale
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Exploring the role of CHRFAM7A in the early stages of Alzheimer's disease : in vitro studies and development of a novel humanized mouse model
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Intracellular Signaling Contributions to Behaviors Relevant to Nicotine Addiction
Thompson, L. E. (2011) · VCU Scholars Compass (Virginia Commonwealth University) · doi:10.25772/c371-2y50

Nicotine-Induced Upregulation of Native Neuronal Nicotinic Receptors Is Caused by Multiple Mechanisms
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Colombo, S. F., Mazzo, F., Pistillo, F., & Gotti, C. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.06.023 · Cited by 118 · see citing works
Nicotine upregulates its own receptors through enhanced intracellular maturation
Sallette, J., Pons, S., Devillers-Thiery, A., Soudant, M., Prado de Carvalho, L., Changeux, J.-P., & Corringer, P. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.03.029 · Cited by 261 · see citing works
Dendritic spine density of prefrontal layer VI neurons is disrupted following chronic in vivo nicotine exposure in development
Kang, L., Bailey, C. D. C., Tian, M. K., & Lambe, E. K. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.08.044
Exocytic trafficking is required for nicotine-induced up-regulation of α4β2 nicotinic acetylcholine receptors
Darsow, T., Booker, T. K., Piña-Crespo, J. C., & Heinemann, S. F. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m501157200 · Cited by 76 · see citing works

Authors: Corringer, P.-J., Sallette, J., & Changeux, J.-P.
Affiliations: Institut Pasteur (FR)
Corresponding author: Corringer, Pierre-Jean
ORCID: Corringer, Pierre-Jean
Changeux, Jean-Pierre
Venue: Journal of Physiology-Paris
Publisher: Elsevier BV
Published: 2006-03
Volume: 99
Issue: 2-3
Pages: 162-171
ISSN: 0928-4257 (ISSN-L)
DOI: 10.1016/j.jphysparis.2005.12.012
OpenAlex: W2003596965
Cited by: 86
References: 88
Citations by year: 2025: 1 · 2024: 3 · 2023: 3 · 2020: 4 · 2019: 2 · 2018: 1 · 2017: 3 · 2016: 3 · 2015: 5 · 2014: 5 · 2013: 3 · 2012: 4
FWCI: 0.90
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Journal of Physiology-Paris (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Funders: Association pour la Recherche sur le Cancer
Fondation pour la Recherche Médicale
Fondation Gilbert Lagrue
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: nicotine, nicotinic acetylcholine receptors, alpha4beta2 nAChR, receptor maturation, receptor trafficking, receptor up-regulation, receptor desensitization, endoplasmic reticulum, neuroplasticity, nicotine dependence, smoking, receptor degradation
MeSH terms: Animals, Brain, Humans, Models, Biological, Neuronal Plasticity, Nicotine, Receptors, Nicotinic, Protein Biosynthesis, Up-Regulation, Protein Subunits, Intracellular Space

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Nicotine enhances intracellular nicotinic receptor maturation: a novel mechanism of neural plasticity?

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