Nicotine normalizes intracellular subunit stoichiometry of nicotinic receptors carrying mutations linked to autosomal dominant nocturnal frontal lobe epilepsy
Open accessAbstract
Autosomal dominant nocturnal frontal lobe epilepsy (ADNFLE) is linked with high penetrance to several distinct nicotinic receptor (nAChR) mutations. We studied (alpha4)(3)(beta2)(2) versus (alpha4)(2)(beta2)(3) subunit stoichiometry for five channel-lining M2 domain mutations: S247F, S252L, 776ins3 in alpha4, V287L, and V287M in beta2. alpha4 and beta2 subunits were constructed with all possible combinations of mutant and wild-type (WT) M2 regions, of cyan and yellow fluorescent protein, and of fluorescent and nonfluorescent M3-M4 loops. Sixteen fluorescent subunit combinations were expressed in N2a cells. Förster resonance energy transfer (FRET) was analyzed by donor recovery after acceptor photobleaching and by pixel-by-pixel sensitized emission, with confirmation by fluorescence intensity ratios. Because FRET efficiency is much greater for adjacent than for nonadjacent subunits and the alpha4 and beta2 subunits occupy specific positions in nAChR pentamers, observed FRET efficiencies from (alpha4)(3)(beta2)(2) carrying fluorescent alpha4 subunits were significantly higher than for (alpha4)(2)(beta2)(3); the converse was found for fluorescent beta2 subunits. All tested ADNFLE mutants produced 10 to 20% increments in the percentage of intracellular (alpha4)(3)(beta2)(2) receptors compared with WT subunits. In contrast, 24- to 48-h nicotine (1 muM) exposure increased the proportion of (alpha4)(2)(beta2)(3) in WT receptors and also returned subunit stoichiometry to WT levels for alpha4S248F and beta2V287L nAChRs. These observations may be relevant to the decreased seizure frequency in patients with ADNFLE who use tobacco products or nicotine patches. Fluorescence-based investigations of nAChR subunit stoichiometry may provide efficient drug discovery methods for nicotine addiction or for other disorders that result from dysregulated nAChRs.
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In cells expressing equal numbers of α4 subunits tagged with donor or acceptor FPs plus untagged β2 subunits, 50% of nAChRs with the (α4)3(β2)2 stoichiometry possess adjacent donor and acceptor α4-FP subunits, and these nAChRs show greater NFRET values than the (α4)2(β2)3 stoichiometry.
“Our previous work exploited the idea that in cells expressing equal numbers of α4 subunits tagged with donor or acceptor FPs (α4-FP subunits plus untagged β2 subunits), 50% of nAChRs with the (α4)3(β2)2 stoichiometry possess adjacent donor and acceptor α4-FP subunits. These nAChRs show greater NFRET values than the (α4)2(β2)3 nAChR stoichiometry, which has nonadjacent donors and acceptors (Son et”
From Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning (2011) · cites this paper as Son et al., 2009
Nicotine is thought to increase the assembly of receptors with a (α4)2(β2)3 stoichiometry.
“Because nicotine is thought to increase the assembly of receptors with a (α4)2(β2)3 stoichiometry (Nelson et al., 2003; Son et al., 2009)”
From Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning (2011) · cites this paper as Son et al., 2009
Pixel-based NFRET is an appropriate method to determine the stoichiometry of protein complexes in Neuro-2a cells.
“Pixel-based NFRET is an appropriate method to determine the stoichiometry of protein complexes in Neuro-2a cells (Moss et al., 2009; Son et al., 2009).”
From Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning (2011) · cites this paper as Son et al., 2009
Previous measurements have detected no differences between FP-labeled and unlabeled wt α4 subunits.
“We cannot state that the FP-labeled subunits perfectly emulate the unlabeled subunit, but our previous measurements have detected no differences between the FP-labeled and unlabeled wt α4 subunits.”
From Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning (2011) · cites this paper as Son et al., 2009
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Allosteric Control of Super-Agonism in a Ligand-Gated Ion ChannelPreprint
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- Authors
- Son, C. D., Moss, F. J., Cohen, B. N., & Lester, H. A.
- Affiliations
- California Institute of Technology (US)
- Venue
- Molecular Pharmacology
- Publisher
- Elsevier BV
- Published
- 2009-05
- Volume
- 75
- Issue
- 5
- Pages
- 1137-1148
- ISSN
- 0026-895X (ISSN-L)
- PMC
- PMC2672806
- OpenAlex
- W2075337277
- Cited by
- 58
- References
- 52
- Citations by year
- 2025: 3 · 2024: 1 · 2023: 4 · 2022: 2 · 2021: 3 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 2 · 2016: 5 · 2015: 6 · 2014: 1 · 2013: 3 · 2012: 6
- FWCI
- 2.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Pharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- OpenMETU (Middle East Technical University) (submittedVersion, cc-by-nc-nd)
- Funders
- American Heart Association
- National Institutes of Health
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- autosomal dominant nocturnal frontal lobe epilepsy, nicotinic acetylcholine receptors, subunit stoichiometry, alpha4 subunit, beta2 subunit, nicotine, fluorescence resonance energy transfer, nicotine patch, tobacco use, seizure frequency, nicotine dependence
- MeSH terms
- Cells, Cultured, Humans, Mutation, Nicotine, Receptors, Nicotinic, Epilepsy, Frontal Lobe, Protein Subunits, Fluorescence Resonance Energy Transfer, Photobleaching
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