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Model lipid systems and their use to evaluate the phase state of biomembranes, their mechanical properties and the effect of non-conventional antibiotics: the case of daptomycin

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Abstract

The lipid bilayer is the basis of the structure and function of the cell membrane. The study of the molecular phenomena that affect biological membranes has a great impact on the understanding of cellular physiology. To understand these phenomena, it has become increasingly necessary to develop simple synthetic models that allow the most basic details of such processes to be reproduced. In this short communication, we took advantage of the properties of two well-established lipid model systems, GUVs and SLBs, with compositions mimicking the cell membrane present in mammals and bacteria, to study the thermotropic phase behavior of lipids as well as the effect of daptomycin, a cyclic lipopeptide used as an antibiotic. The study of mechanical and thermodynamical properties of these model systems could contribute to establish a theoretical framework to develop more efficient strategies for biological control.

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References

  • Andersen OS, Koeppe RE 2nd (2007) Bilayer thickness and membrane protein function: an energetic perspective. Annu Rev Biophys Biomol Struct 36:107–130

    Article  CAS  Google Scholar 

  • Bakht O, Pathak P, London E (2007) Effect of the structure of lipids favoring disordered domain formation on the stability of cholesterol-containing ordered domains (lipid rafts): identification of multiple raft-stabilization mechanisms. Biophys J 93(12):4307–4318

    Article  CAS  Google Scholar 

  • Balleza D, Alessandrini A, Beltrán García MJ (2019a) Role of lipid composition, physicochemical interactions, and membrane mechanics in the molecular actions of microbial cyclic lipopeptides. J Membr Biol 252:131–157

    Article  CAS  Google Scholar 

  • Balleza D, Mescola A, Marín-Medina N, Ragazzini G, Pieruccini M, Facci P, Alessandrini A (2019b) Complex phase behavior of GUVs containing different sphingomyelins. Biophys J 116:503–517

    Article  CAS  Google Scholar 

  • Baltz RH, Miao V, Wrigley SK (2005) Natural products to drugs: daptomycin and related lipopeptide antibiotics. Nat Prod Rep 22(6):717–741

    Article  CAS  Google Scholar 

  • Benvegnu DJ, McConnell HM (1993) Surface dipole densities in lipid monolayers. J Phys Chem 97(25):6686–6691

    Article  CAS  Google Scholar 

  • Chen YF, Sun TL, Sun Y, Huang HW (2014) Interaction of daptomycin with lipid bilayers: a lipid extracting effect. Biochemistry 53:5384–5392

    Article  CAS  Google Scholar 

  • Ciumac D, Gong H, Hu X, Lu JR (2019) Membrane targeting cationic antimicrobial peptides. J Colloid Interface Sci 537:163–185

    Article  CAS  Google Scholar 

  • Clejan S, Krulwich TA, Mondrus KR, Seto-Young D (1986) Membrane lipid composition of obligately and facultatively alkalophilic strains of Bacillus spp. J Bacteriol 168:334–340

    Article  CAS  Google Scholar 

  • Cochrane SA, Vederas JC (2016) Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med Res Rev 36(1):4–31

    Article  CAS  Google Scholar 

  • Hollmann A, Martinez M, Maturana P, Semorile LC, Maffia PC (2018) Antimicrobial peptides: interaction with model and biological membranes and synergism with chemical antibiotics. Front Chem 6:204

    Article  Google Scholar 

  • Hussain A, Singh S, Sharma D, Webster TJ, Shafaat K, Faruk A (2017) Elastic liposomes as novel carriers: recent advances in drug delivery. Int J Nanomed 12:5087–5108

    Article  CAS  Google Scholar 

  • Janmey PA, Kinnunen PK (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16:538–546

    Article  CAS  Google Scholar 

  • Jung D, Powers JP, Straus SK, Hancock RE (2008) Lipid-specific binding of the calcium-dependent antibiotic daptomycin leads to changes in lipid polymorphism of model membranes. Chem Phys Lipids 154(2):120–128

    Article  CAS  Google Scholar 

  • Kanafani ZA, Corey GR (2007) Daptomycin: a rapidly bactericidal lipopeptide for the treatment of Gram-positive infections. Expert Rev Anti Infect Ther 5(2):177–184

    Article  CAS  Google Scholar 

  • Kay JG, Fairn GD (2019) Distribution, dynamics and functional roles of phosphatidylserine within the cell. Cell Commun Signal 17(1):126

    Article  Google Scholar 

  • Kreutzberger MA, Pokorny A, Almeida PF (2017) Daptomycin-phosphatidylglycerol domains in lipid membranes. Langmuir 33(47):13669–13679

    Article  CAS  Google Scholar 

  • Kurihara K, Okura Y, Matsuo M, Toyota T, Suzuki K, Sugawara T (2015) A recursive vesicle-based model protocell with a primitive model cell cycle. Nat Commun 29(6):8352

    Article  Google Scholar 

  • Lee MT, Yang PY, Charron NE, Hsieh MH, Chang YY, Huang HW (2018) Comparison of the effects of daptomycin on bacterial and model membranes. Biochemistry 57(38):5629–5639

    Article  CAS  Google Scholar 

  • Lee TH, Hofferek V, Separovic F, Reid GE, Aguilar MI (2019) The role of bacterial lipid diversity and membrane properties in modulating antimicrobial peptide activity and drug resistance. Curr Opin Chem Biol 52:85–92

    Article  CAS  Google Scholar 

  • Lira RB, Robinson T, Dimova R, Riske KA (2019) Highly efficient protein-free membrane fusion: a giant vesicle study. Biophys J 116(1):79–91

    Article  CAS  Google Scholar 

  • Marín-Medina N, Mescola A, Alessandrini A (2018) Effects of the peptide magainin H2 on supported lipid bilayers studied by different biophysical techniques. Biochim Biophys Acta 1860(12):2635–2643

    Article  Google Scholar 

  • Marquette A, Bechinger B (2018) Biophysical investigations elucidating the mechanisms of action of antimicrobial peptides and their synergism. Biomolecules 8(2):18

    Article  Google Scholar 

  • Mescola A, Marín-Medina N, Ragazzini G, Accolla M, Alessandrini A (2019) Magainin-H2 effects on the permeabilization and mechanical properties of giant unilamellar vesicles. J Colloid Interface Sci 553:247–258

    Article  CAS  Google Scholar 

  • Munusamy S, Conde R, Bertrand B, Munoz-Garay C (2020) Biophysical approaches for exploring lipopeptide-lipid interactions. Biochimie 170:173–202

    Article  CAS  Google Scholar 

  • Muraih JK, Pearson A, Silverman J, Palmer M (2011) Oligomerization of daptomycin on membranes. Biochim Biophys Acta 1808(4):1154–1160

    Article  CAS  Google Scholar 

  • Pokorny A, Khatib TO, Stevenson H (2018) A quantitative model of Daptomycin binding to lipid bilayers. J Phys Chem B 122(39):9137–9146

    Article  CAS  Google Scholar 

  • Prévost C, Tsai FC, Bassereau P, Simunovic M (2017) Pulling membrane nanotubes from giant unilamellar vesicles. J Vis Exp (130):56086

  • Rappolt M, Pabst G (2008) Flexibility and structure of fluid bilayer interfaces. In: Nag K (ed) Structure and dynamics of membranous interfaces. Wiley, Hoboken

    Google Scholar 

  • Rolain JM, Abat C, Jimeno MT, Fournier PE, Raoult D (2016) Do we need new antibiotics? Clin Microbiol Infect 22(5):408–415

    Article  Google Scholar 

  • Seydlová G, Sokol A, Lišková P, Konopásek I, Fišer R (2018) Daptomycin pore formation and stoichiometry depend on membrane potential of target membrane. Antimicrob Agents Chemother 63(1):e01589-18

    Article  Google Scholar 

  • Sheard DE, O’Brien-Simpson NM, Wade JD, Separovic F (2019) Combating bacterial resistance by combination of antibiotics with antimicrobial peptides. Pure Appl Chem 99:199–209

    Article  Google Scholar 

  • Shinoda W, Mikami M, Baba T, Hato M (2004) Molecular dynamics study on the effects of chain branching on the physical properties of lipid bilayers: 2. Permeability. J Phys Chem B 108(26):9346–9356

    Article  CAS  Google Scholar 

  • Yılmaz Ç, Özcengiz G (2017) Antibiotics: pharmacokinetics, toxicity, resistance and multidrug efflux pumps. Biochem Pharmacol 133:43–62

    Article  Google Scholar 

  • Zhang T, Muraih JK, Tishbi N, Herskowitz J, Victor RL, Silverman J, Uwumarenogie S, Taylor SD, Palmer M, Mintzer E (2014) Cardiolipin prevents membrane translocation and permeabilization by daptomycin. J Biol Chem 289(17):11584–11591

    Article  CAS  Google Scholar 

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DB, AM, and AA designed research’s strategy and performed experiments. All authors analyzed the data and contributed to the manuscript writing. No potential competing interest was reported by the authors.

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Correspondence to Daniel Balleza.

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No potential competing interest was reported by the authors.

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Balleza, D., Mescola, A. & Alessandrini, A. Model lipid systems and their use to evaluate the phase state of biomembranes, their mechanical properties and the effect of non-conventional antibiotics: the case of daptomycin. Eur Biophys J 49, 401–408 (2020). https://doi.org/10.1007/s00249-020-01445-w

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  • DOI: https://doi.org/10.1007/s00249-020-01445-w

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