Cell autonomy, receptor autonomy, and thermodynamics in nicotine receptor up-regulation
Open accessAbstract
Chronic nicotine exposure, in smokers or in experimental rodents administered nicotine, produces elevated levels of nicotinic acetylcholine receptors in several brain regions. However, there are few data on up-regulation of receptors in specific neuronal subtypes. We tested whether functional up-regulation of nicotinic responses occurs in cultured GABAergic neurons of the ventral midbrain. Fura-2 measurements of nicotinic responses were made on ventral midbrain neurons from knock-in mice heterozygous for the alpha4-M2 domain Leu9'Ala mutation, which confers nicotine hypersensitivity. Chronic nicotine exposure at a concentration (10 nM for 3 days) that activates only the hypersensitive alpha4* (Leu9'Ala) receptors, but not wild-type receptors, resulted in significant potentiation of ACh (100 microM)-elicited responses. Experiments were also performed on midbrain neuronal cultures heterozygous for the alpha4* (Leu9'Ala) mutation as well as for a GFP protein fused to a GABA transporter that reliably reveals GABAergic neurons. In cultures chronically treated with 10nM nicotine, there was significantly increased alpha4* nicotinic-induced Ca(2+) influx elicited by low concentration of ACh (3 microM). Furthermore, chronic exposure to the competitive antagonist dihydro-beta-erythroidine, but not to the noncompetitive antagonist mecamylamine, induced up-regulation of ACh elicited nicotinic responses. These results suggest that occupation of alpha4* nicotinic receptor binding site(s), at the interface between two subunits, is sufficient to promote assembly and/or up-regulation of functional receptors in GABAergic neurons. Up-regulation in neurons is both "cell-autonomous", occurring at the cell itself, and "receptor autonomous", occurring at the receptor itself, and may be a thermodynamic necessity of ligand-protein interactions.
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Activation of no other nicotinic receptors appears necessary for upregulation (receptor autonomy).
“We summarized these findings with the term “receptor autonomy” because activation of no other nicotinic receptors appears necessary (48).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
Selective nicotine binding to α4* nAChRs is sufficient for α4* receptor upregulation when α4* receptors are heterologously expressed in mammalian cell lines, as well as in almost pure cultures of GABAergic ventral midbrain neurons.
“Selective nicotine binding to α4* nAChRs is sufficient for α4* receptor upregulation when α4* receptors are heterologously expressed in mammalian cell lines, as well as in almost pure cultures of GABAergic ventral midbrain neurons (48).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
Upregulation does not require synaptic transmission or other diffusible extracellular signals.
“Upregulation does not require synaptic transmission or other diffusible extracellular signals.”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
Experiments with cultures from α4-hypersensitive mice show that upregulation occurs at chronic nicotine concentrations that activate only α4* receptors, in homotypic GABAergic cultures lacking their typical presynaptic partners, and when tested with ACh concentrations that activate only the α4* receptors.
“Experiments with cultures from α4-hypersensitive mice also show that upregulation occurs (a) at chronic nicotine concentrations that activate only α4* receptors, (b) in homotypic GABAergic cultures lacking their typical presynaptic partners, and (c) when tested with ACh concentrations that activate only the α4* receptors (48,49).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
Upregulation displays cell autonomy: upregulation occurs in the very cell where nicotine acts on the appropriate receptors.
“We extended classical genetic concepts to state that upregulation displays “cell autonomy”. This means that upregulation occurs in the very cell where nicotine acts on the appropriate receptors (48).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
Desensitization is one set of conformational states that increase the thermodynamic driving force for SePhaChARNS.
“In summary, desensitization is one set of conformational states that increase the thermodynamic driving force for SePhaChARNS (48).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
Stabilization of high-affinity nicotinic receptors by chronic nicotine is a thermodynamic necessity.
“Thus, in one view, stabilization of high-affinity nicotinic receptors by chronic nicotine is a thermodynamic necessity (48).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
The competitive antagonist DHβE induces functional upregulation at higher concentrations consistent with the limited number of states available to an antagonist.
“The competitive antagonist DHβE also induces functional upregulation, but at higher concentrations consistent with the limited number of states available to an antagonist (48).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
Covalent modifications during ERAD and ER exit likely amplify the kinetically based effects of SePhaChARNS.
“However, it is quite likely that the covalent modifications during endoplasmic reticulum-associated degradation (ERAD) and ER exit do amplify the kinetically based effects of SePhaChARNS (48).”
From Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery (2009) · cites this paper as [48]
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- Authors
- Nashmi, R., & Lester, H.
- Affiliations
- California Institute of Technology (US)
- Corresponding author
- Lester, Henry
- Venue
- Biochemical Pharmacology
- Publisher
- Elsevier BV
- Published
- 2007-10
- Volume
- 74
- Issue
- 8
- Pages
- 1145-1154
- ISSN
- 0006-2952 (ISSN-L)
- PMC
- PMC2128788
- OpenAlex
- W2086750594
- Cited by
- 43
- References
- 60
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2021: 1 · 2019: 2 · 2018: 2 · 2017: 1 · 2016: 2 · 2015: 2 · 2014: 3 · 2013: 1 · 2012: 1
- FWCI
- 2.91
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biochemical Pharmacology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Drug Abuse (DA17279, R01DA017279)
- National Institute of Neurological Disorders and Stroke (NS 11756, R01NS011756)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
- Keywords
- nicotinic acetylcholine receptors, receptor up-regulation, chronic nicotine exposure, GABAergic neurons, ventral midbrain, calcium influx, dihydro-beta-erythroidine, mecamylamine, protein-ligand interactions, receptor assembly, cell autonomy
- MeSH terms
- Animals, Cells, Cultured, Dihydro-beta-Erythroidine, Mecamylamine, Mesencephalon, Nicotine, Receptors, Nicotinic, Thermodynamics, Up-Regulation, Mice
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