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Fluorescence Studies of Nicotinic Acetylcholine Receptor and Its Associated Lipid Milieu: The Influence of Erwin London’s Methodological Approaches

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Abstract

Erwin London dedicated considerable effort to understanding lipid interactions with membrane-resident proteins and how these interactions shaped the formation and maintenance of lipid phases and domains. In this endeavor, he developed ad hoc techniques that greatly contributed to advancements in the field. We have employed and/or modified/extended some of his methodological approaches and applied them to investigate lipid interaction with the nicotinic acetylcholine receptor (nAChR) protein, the paradigm member of the superfamily of rapid pentameric ligand-gated ion channels (pLGIC). Our experimental systems ranged from purified receptor protein reconstituted into synthetic lipid membranes having known effects on receptor function, to cellular systems subjected to modification of their lipid content, e.g., varying cholesterol levels. We have often employed fluorescence techniques, including fluorescence quenching of diphenylhexatriene (DPH) extrinsic fluorescence and of nAChR intrinsic fluorescence by nitroxide spin-labeled phospholipids, DPH anisotropy, excimer formation of pyrene-phosphatidylcholine, and Förster resonance energy transfer (FRET) from the protein moiety to the extrinsic probes Laurdan, DPH, or pyrene-phospholipid to characterize various biophysical properties of lipid–receptor interactions. Some of these strategies are revisited in this review. Special attention is devoted to the anionic phospholipid phosphatidic acid (PA), which stabilizes the functional resting form of the nAChR. The receptor protein was shown to organize its PA-containing immediate microenvironment into microdomains with high lateral packing density and rigidity. PA and cholesterol appear to compete for the same binding sites on the nAChR protein.

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Abbreviations

nAChR:

Nicotinic acetylcholine receptor

DPH:

Diphenylhexatriene

DOPC:

Dioleoyl phosphatidylcholine

DPPC:

Dipalmitoyl phosphatidylcholine

POPC:

1-Palmitoyl-2-oleoyl phosphatidylcholine

POPA:

1-Palmitoyl-2-oleoyl phosphatidic acid

MLV:

Multilamellar vesicles

SLPC:

Nitroxide-spin-labeled 1-palmitoyl-2-stearoyl-(doxyl)-sn-glycero-3-phosphocholine

PA:

Phosphatidic acid

PyPC:

1-Hexadecanoyl-2-(1-pyrenedecanoyl)-sn-glycero-3-phosphocholine

T m :

Transition temperature

F:

Fluorescence intensity

FRET:

Förster energy transfer

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Acknowledgements

Thanks are due to Dr. Ana Sofía Vallés for her help with the Graphical Abstract, drawn using Servier Medical Art Commons Attribution 3.0 Unported License (http://smart.servier.com). Servier Medical Art by Servier is licensed under a Creative Commons Attribution 3.0 Unported License.

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  1. Laboratory of Molecular Neurobiology, Institute of Biomedical Research (BIOMED), UCA-CONICET, Av. Alicia Moreau de Justo 1600, C1107AFF, Buenos Aires, Argentina

    Francisco J. Barrantes

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This article is part of Topical Collection “Thematic Collection on Membrane Biophysics in Honor of Prof. Erwin London”.

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Barrantes, F.J. Fluorescence Studies of Nicotinic Acetylcholine Receptor and Its Associated Lipid Milieu: The Influence of Erwin London’s Methodological Approaches. J Membrane Biol 255, 563–574 (2022). https://doi.org/10.1007/s00232-022-00239-9

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