Mechanisms of lipid-mediated regulation of the pore-forming activity of antimicrobial agents: studies on planar lipid bilayers

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Abstract

Planar lipid bilayers are unique tools designed for modeling cell membranes and electrophysiological studies of incorporated ion channels. Such model systems are designed to limit the number of components taking part in the functioning of biological membranes in order to characterize in detail the occurring processes under well-controlled experimental conditions. Planar lipid bilayers make it possible to record single events with a measured current of more than a tenth of a picoampere. The relative simplicity of the method, the ability to observe single molecular events, and the high reproducibility of the results obtained determines the unprecedented effectiveness of using planar lipid bilayers to identify key physical and chemical factors responsible for regulating the functioning of ion channels. This review represents an analysis of literature data concerning the mechanisms of lipid-associated regulation of ion channels formed by various antimicrobial agents. The examination allows us to consider the lipids as molecular chaperones that ensure the formation of pores in target membranes by antimicrobials.

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About the authors

S. S. Efimova

Institute of Cytology, Russian Academy of Sciences

Author for correspondence.
Email: efimova@incras.ru
Russian Federation, St. Petersburg, 194064

O. S. Ostroumova

Institute of Cytology, Russian Academy of Sciences

Email: efimova@incras.ru
Russian Federation, St. Petersburg, 194064

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2. Fig. 1. Schematic representation of the formation of flat lipid membranes using the Müller–Rudin (a) and Montal–Müller (b) methods [5].

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3. Fig. 2. Chemical structures of pore-forming antimicrobial peptides: gramicidin A, alamethicin, ceratoxin, cecropin A, melittin, magainin II, α-defensin NP-1, protegrin-1, nisin, and cinnamycin. Only D-enantiomers of amino acids are indicated. α-Me-Ala – α-methylalanyl; Phe-ol – phenylalaninol; Dha – dehydroalanine; Dhb – dehydrobutyrin; Abu – α-aminobutyric acid.

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4. Fig. 3. Various models of ion channel formation by antimicrobial peptides: by dimerization of gramicidin A helices (a); association of alamethicin α-helices into a peptide “barrel” (b); formation of a peptide-lipid toroidal pore by melittin (c) and formation of an asymmetric lipopeptide-lipid pore by syringomycin E (d).

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5. Fig. 4. Chemical structures of pore-forming antimicrobial cyclic lipopeptides: iturin A, surfactin, fengycin A, tolaazin, syringomycin E, syringostatin A, syringotoxin B, syringopeptin 22A, peptidolipin NA, polymyxin B, daptomycin, and gausemycin A. Only D-enantiomers of amino acids are shown. Orn – ornithine; Dab – 2,4-diaminobutyric acid; Dhb – 2,3-dehydroaminobutyric acid; Thr(4-Cl) – 4-chlorothreonine; MeOGlu – 3-methylglutamic acid; Kyn – kynurenine; Ahpb – 2-amino-4-hydroxy-4-phenylbutyric acid.

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6. Fig. 5. Chemical structure of pore-forming antimicrobial agents of non-peptide nature: amphotericin B, nystatin, mycoheptin, levorin A2, trichomycin, candicidin, filipin, aureofuscin, elaiophilin and beticolin 3.

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