Influence of Acyl Chain Saturation on the Membrane-Binding Activity of a Short Antimicrobial Peptide

Overview

Journal ACS Omega

Publisher American Chemical Society

Specialty Chemistry

Date 2018 Jul 20

PMID 30023555

Citations 4

Authors

Daniela Ciumac

Richard A Campbell

Luke A Clifton

Hai Xu

Giovanna Fragneto

Jian R Lu

Affiliations

Soon will be listed here.

Abstract

Different bacterial types and their living environments can lead to different saturations in the chains of their membrane lipids. Such structural differences may influence the efficacy of antibiotics that target bacterial membranes. In this work, the effects of acyl chain saturation on the binding of an antimicrobial peptide G have been examined as a function of the packing density of lipid monolayers by combining external reflection Fourier transform infrared (ER-FTIR) spectroscopy and neutron reflection (NR) measurements. Langmuir monolayers were formed from 1,2-dipalmitoyl--glycero-3-phospho-(1'--glycerol) (DPPG) and 1-palmitoyl-2-oleoyl--glycero-3-phospho-(1'--glycerol) (POPG), respectively, with the initial surface pressures controlled at 8 and 28 mN/m. A reduction in the order of the acyl chains associated with the increase in the layer thickness upon G binding was revealed from ER-FTIR spectroscopy, with peptide binding reaching equilibration faster in POPG than in DPPG monolayers. Whereas the dynamic DPPG-binding process displayed a steady increase in the amide I band area, the POPG-binding process showed little change in the amide area after the initial period. The peptide amide I area from ER-FTIR spectroscopy could be linearly correlated with the adsorbed G amount from NR, irrespective of time, initial pressure, or chain saturation, with clearly more peptide incorporated into the DPPG monolayer. Furthermore, NR revealed that although the peptide was associated with both POPG and DPPG lipid monolayers, it was more extensively distributed in the latter, showing that acyl chain saturation clearly promoted peptide binding and structural disruption.

Citing Articles

Research Progress of Phospholipid Vesicles in Biological Field.

Zhang N, Song J, Han Y Biomolecules. 2025; 14(12.

PMID: 39766335 PMC: 11726895. DOI: 10.3390/biom14121628.

Insights into Molecular Interactions between a GAPDH-Related Fish Antimicrobial Peptide, Analogs Thereof, and Bacterial Membranes.

Cashman-Kadri S, Lague P, Subirade M, Fliss I, Beaulieu L Biochemistry. 2024; 63(10):1257-1269.

PMID: 38683758 PMC: 11112741. DOI: 10.1021/acs.biochem.4c00049.

Encoding a Neutral Trehalase of Is Required for Growth and Virulence of the Pathogen.

Chen L, Ma X, Sun T, Zhu Q, Feng H, Li Y Int J Mol Sci. 2024; 25(1).

PMID: 38203466 PMC: 10778863. DOI: 10.3390/ijms25010294.

Phase variation of manganese oxide in the MnO@ZnO nanocomposite with calcination temperature and its effect on structural and biological activities.

Basak S, Haydar M, Sikdar S, Ali S, Mondal M, Shome A Sci Rep. 2023; 13(1):21542.

PMID: 38057479 PMC: 10700637. DOI: 10.1038/s41598-023-48695-0.

In-Membrane Nanostructuring of Cationic Amphiphiles Affects Their Antimicrobial Efficacy and Cytotoxicity: A Comparison Study between a De Novo Antimicrobial Lipopeptide and Traditional Biocides.

Fa K, Liu H, Gong H, Zhang L, Liao M, Hu X Langmuir. 2022; 38(21):6623-6637.

PMID: 35587380 PMC: 9161444. DOI: 10.1021/acs.langmuir.2c00506.

References

Pan J, Heberle F, Tristram-Nagle S, Szymanski M, Koepfinger M, Katsaras J . Molecular structures of fluid phase phosphatidylglycerol bilayers as determined by small angle neutron and X-ray scattering. Biochim Biophys Acta. 2012; 1818(9):2135-48. PMC: 3673316. DOI: 10.1016/j.bbamem.2012.05.007. View

Knyght I, Clifton L, Saaka Y, Jayne Lawrence M, Barlow D . Interaction of the Antimicrobial Peptides Rhesus θ-Defensin and Porcine Protegrin-1 with Anionic Phospholipid Monolayers. Langmuir. 2016; 32(29):7403-10. DOI: 10.1021/acs.langmuir.6b01688. View

Hazel J, Williams E . The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res. 1990; 29(3):167-227. DOI: 10.1016/0163-7827(90)90002-3. View

Miano F, Zhao X, Lu J, Penfold J . Coadsorption of human milk lactoferrin into the dipalmitoylglycerolphosphatidylcholine phospholipid monolayer spread at the air/water interface. Biophys J. 2006; 92(4):1254-62. PMC: 1783875. DOI: 10.1529/biophysj.105.078592. View

Sitaram N, Nagaraj R . Host-defense antimicrobial peptides: importance of structure for activity. Curr Pharm Des. 2002; 8(9):727-42. DOI: 10.2174/1381612023395358. View

Calvez P, Bussieres S, Demers E, Salesse C . Parameters modulating the maximum insertion pressure of proteins and peptides in lipid monolayers. Biochimie. 2009; 91(6):718-33. DOI: 10.1016/j.biochi.2009.03.018. View

Campbell R, Tummino A, Noskov B, Varga I . Polyelectrolyte/surfactant films spread from neutral aggregates. Soft Matter. 2016; 12(24):5304-12. DOI: 10.1039/c6sm00637j. View

Chen C, Hu J, Zeng P, Pan F, Yaseen M, Xu H . Molecular mechanisms of anticancer action and cell selectivity of short α-helical peptides. Biomaterials. 2013; 35(5):1552-61. DOI: 10.1016/j.biomaterials.2013.10.082. View

Zhao X, Wu H, Lu H, Li G, Huang Q . LAMP: A Database Linking Antimicrobial Peptides. PLoS One. 2013; 8(6):e66557. PMC: 3688957. DOI: 10.1371/journal.pone.0066557. View

10.

Chen C, Chen Y, Yang C, Zeng P, Xu H, Pan F . High Selective Performance of Designed Antibacterial and Anticancer Peptide Amphiphiles. ACS Appl Mater Interfaces. 2015; 7(31):17346-55. DOI: 10.1021/acsami.5b04547. View

11.

Lad M, Birembaut F, Clifton L, Frazier R, Webster J, Green R . Antimicrobial peptide-lipid binding interactions and binding selectivity. Biophys J. 2007; 92(10):3575-86. PMC: 1853145. DOI: 10.1529/biophysj.106.097774. View

12.

Tenover F . Mechanisms of antimicrobial resistance in bacteria. Am J Med. 2006; 119(6 Suppl 1):S3-10. DOI: 10.1016/j.amjmed.2006.03.011. View

13.

Glaser R, Sachse C, Durr U, Wadhwani P, Ulrich A . Orientation of the antimicrobial peptide PGLa in lipid membranes determined from 19F-NMR dipolar couplings of 4-CF3-phenylglycine labels. J Magn Reson. 2004; 168(1):153-63. DOI: 10.1016/j.jmr.2004.02.008. View

14.

Bougis P, Tessier M, Van Rietschoten J, Rochat H, Faucon J, Dufourcq J . Are interactions with phospholipids responsible for pharmacological activities of cardiotoxins?. Mol Cell Biochem. 1983; 55(1):49-64. DOI: 10.1007/BF00229242. View

15.

Kucerka N, Tristram-Nagle S, Nagle J . Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J Membr Biol. 2006; 208(3):193-202. DOI: 10.1007/s00232-005-7006-8. View

16.

Ishitsuka Y, Pham D, Waring A, Lehrer R, Lee K . Insertion selectivity of antimicrobial peptide protegrin-1 into lipid monolayers: effect of head group electrostatics and tail group packing. Biochim Biophys Acta. 2006; 1758(9):1450-60. DOI: 10.1016/j.bbamem.2006.08.001. View

17.

Picas L, Suarez-Germa C, Montero M, Domenech O, Hernandez-Borrell J . Miscibility behavior and nanostructure of monolayers of the main phospholipids of Escherichia coli inner membrane. Langmuir. 2011; 28(1):701-6. DOI: 10.1021/la203795t. View

18.

Denich T, Beaudette L, Lee H, Trevors J . Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Methods. 2002; 52(2):149-82. DOI: 10.1016/s0167-7012(02)00155-0. View

19.

Habermann E, Jentsch J . [Sequence analysis of melittin from tryptic and peptic degradation products]. Hoppe Seylers Z Physiol Chem. 1967; 348(1):37-50. View

20.

Rapaport D, Hague G, Pouny Y, Shai Y . pH- and ionic strength-dependent fusion of phospholipid vesicles induced by pardaxin analogues or by mixtures of charge-reversed peptides. Biochemistry. 1993; 32(13):3291-7. DOI: 10.1021/bi00064a011. View