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Complex electrostatic effects on the selectivity of membrane-permeabilizing cyclic lipopeptides.

Jessica Steigenberger1, Yentl Verleysen2, Niels Geudens3

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Anionic cyclic lipopeptides (CLiPs) like viscosin can be more active against anionic membranes than cationic analogs. Membrane charge and lipid concentration determine CLiP selectivity and activity, impacting biological and medical applications.

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Area of Science:

  • Biochemistry
  • Membrane Biophysics
  • Microbiology

Background:

  • Cyclic lipopeptides (CLiPs) are amphipathic molecules with diverse biological functions, including membrane permeabilization.
  • Understanding CLiP-membrane interactions is crucial for their technical and medical applications, particularly their selectivity towards different membrane compositions.
  • Electrostatic interactions between charged CLiPs and lipid bilayers significantly influence their behavior and efficacy.

Purpose of the Study:

  • To investigate the role of electrostatic effects in the target selectivity of CLiPs.
  • To compare the membrane activity and selectivity of an anionic CLiP (viscosin), a neutral analog (pseudodesmin A), and a cationic analog (viscosin-E2K).
  • To elucidate how lipid concentration and charge density affect CLiP-induced membrane leakage.

Main Methods:

  • Utilized time-resolved fluorescence to measure calcein leakage from liposomes composed of anionic (phosphatidylglycerol, phosphatidylethanolamine) and neutral (phosphatidylcholine) lipids.
  • Employed equi-activity analysis to determine reciprocal partition coefficients (1/K) and CLiP-to-lipid mole ratios (Re50) at 50% leakage.
  • Investigated CLiP activity across a range of lipid concentrations to assess the influence of the lipid regime.

Main Results:

  • Contrary to typical cationic peptide behavior, the anionic viscosin showed higher activity against anionic phosphatidylglycerol/phosphatidylethanolamine membranes than the cationic viscosin-E2K at higher lipid concentrations.
  • Selectivity was reversed at very low lipid concentrations, with the cationic viscosin-E2K exhibiting higher affinity (lower 1/K) for anionic membranes.
  • Viscosin induced stronger local membrane damage and leakage (Re50 = 0.08) due to membrane expansion and asymmetry, while viscosin-E2K required charge compensation for leakage (Re50 = 0.32).

Conclusions:

  • CLiP activity and selectivity are highly dependent on the lipid concentration (lipid regime) and the interplay between electrostatic attraction/repulsion and membrane perturbation.
  • The 'cation attacks anionic membrane' paradigm is only restored in the low-lipid regime where partition coefficients dominate.
  • Accurate prediction of CLiP behavior requires knowledge of both partition coefficients (1/K) and membrane damage potential (Re50) across different lipid concentrations.