[en] Mixed monolayers of the surface-active lipopeptide surfactin-C-15 and various lipids differing by their chain length (DMPC, DPPC, DSPC) and polar headgroup (DPPC, DPPE, DPPS) were investigated by atomic force microscopy (AFM) in combination with molecular modeling (Hypermatrix procedure) and surface pressure-area isotherms. In the presence of surfactin, AFM topographic images showed phase separation for each surfactin-phospholipid system except for surfactin-DMPC, which was in good agreement with compression isotherms. On the basis of domain shape and line tension theory, we conclude that the miscibility between surfactin and phospholipids is higher for shorter chain lengths (DMPC > DPPC > DSPC) and that the polar headgroup of phospholipids influences the miscibility of surfactin in the order DPPC > DPPE > DPPS. Molecular modeling data show that mixing surfactin and DPPC has a destabilizing effect on DPPC monolayer while it has a stabilizing effect towards DPPE and DPPS molecular interactions. Our results provide valuable information on the activity mechanism of surfactin and may be useful for the design of surfactin delivery systems. (c) 2007 Elsevier B.V. All rights reserved.
Disciplines :
Agriculture & agronomy
Author, co-author :
Bouffioux, O.
Berquand, A.
Eeman, M.
Paquot, Michel ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Gembloux Agro-Bio Tech
Dufrene, Y. F.
Brasseur, Robert ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Gembloux Agro-Bio Tech
Arima K., Kakinuma A., and Tamura G. Surfactin, a crystalline peptide-lipid surfactant produced by B. subtilis: isolation, characterization and its inhibition of fibrin clot formation. Biochem. Biophys. Res. Commun. 31 (1968) 488-494
Kakinuma A., Ouchida A., Shima T., Sugino H., Isono M., Tamura G., and Arima K. Confirmation of the structure of surfactin by mass spectrometry. Agric. Biol. Chem. 33 (1969) 1669-1671
Kameda Y., Oira S., Matsui K., Kanatomo S., and Hase T. Antitumor activity of Bacillus natto. V. Isolation and characterization of surfactin in the culture medium of Bacillus natto KMD 2311. Chem. Pharm. Bull. 22 (1974) 938-944
Bernheimer A.W., and Avigad L.S. Nature and properties of a cytolytic agent produced by Bacillus subtilis. J. Gen. Microbiol. 61 (1970) 361-369
Hosono K., and Suzuki H. Acylpeptides, the inhibitors of cyclic adenosine 3′, 5′-monophosphate phosphodiesterase. I. Purification, physicochemical properties and structures of fatty acid residues. J. Antibiot. 36 (1983) 667-673
Vollenbroich D., Özel M., Vater J., Kamp R.M., and Pauli G. Mechanism of inactivation of enveloped viruses by the biosurfactant surfactin from Bacillus subtilis. Biologicals 25 (1997) 289-297
Vollenbroich D., Pauli G., Özel M., and Vater J. Antimycoplasma properties and application in cell culture of surfactin, a lipopeptide antibiotic from Bacillus subtilis. Appl. Environ. Microbiol. 63 (1997) 44-49
Sheppard J.D., Jumarie C., Cooper D.G., and Laprade R. Ionic channels induced by surfactin in planar lipid bilayer membranes. Biochim. Biophys. Acta 1064 (1991) 13-23
Maget-Dana R., and Ptak M. Interactions of surfactin with membrane models. Biophys. J. 68 (1995) 1937-1943
Deleu M., Paquot M., Jacques P., Thonart P., Adriaensen Y., and Dufrêne Y.F. Nanometer scale organization of mixed surfactin/phosphatidylcholine monolayers. Biophys. J. 77 (1999) 2304-2310
Deleu M., Nott K., Brasseur R., Jacques P., Thonart P., and Dufrêne Y.F. Imaging mixed lipid monolayers by dynamic atomic force microscopy. Biochim. Biophys. Acta 1513 (2001) 55-62
Grau A., Gómez Fernández J.C., Peypoux F., and Ortiz A. A study on the interactions of surfactin with phospholipid vesicles. Biochim. Biophys. Acta 1418 (1999) 307-319
Eeman M., Berquand A., Dufrêne Y.F., Paquot M., Dufour S., and Deleu M. Penetration of surfactin into phospholipid monolayers: nanoscale interfacial organization. Langmuir 22 (2006) 11337-11345
Dufrêne Y.F., Barger W.R., Green J.-B.D., and Lee G.U. Nanometer-scale surface properties of mixed phospholipid monolayers and bilayers. Langmuir 13 (1997) 4779-4784
Connell S.D., and Smith D.A. The atomic force microscopy as a tool for studying phase separation in lipid membranes. Mol. Membr. Biol. 23 (2006) 17-28
Maget-Dana R. The monolayer technique: a potent tool for studying the interfacial properties of antimicrobial and membrane-lytic peptides and their interactions with lipid membranes. Biochim. Biophys. Acta 1462 (1999) 109-140
Deleu M., Paquot M., and Nylander T. Fengycin interaction with lipid monolayers at the air-aqueous interface- implications for the effect of fengycin on biological membranes. J. Colloid Interface Sci. 283 (2005) 358-365
Eeman M., Deleu M., Paquot M., Thonart P., and Dufrene Y. Nanoscale properties of mixed fengycin/ceramide monolayers explored using atomic force microscopy. Langmuir 21 (2005) 2505-2511
Lins L., Ducarme P., Breukink E., and Brasseur R. Computational study of nisin interaction with model membrane. Biochim. Biophys. Acta 1420 (1999) 111-120
Deleu M., Bouffioux O., Razafindralambo H., Paquot M., Hbid C., Thonart P., Jacques P., and Brasseur R. Interaction of surfactin with membranes: a computational approach. Langmuir 19 (2003) 3377-3385
Gallet X., Deleu M., Razafindralambo H., Jacques P., Thonart P., Paquot M., and Brasseur R. Computer simulation of surfactin conformation at a hydrophobic/hydrophilic interface. Langmuir 15 (1999) 2409-2413
Bonmatin J.-M., Genest M., Labbé H., and Ptak M. Solution three-dimensional structure of surfactin: a cyclic lipopeptide studied by 1H-NMR, distance geometry, and molecular dynamics. Biopolymers 34 (1994) 975-986
Brasseur R., Goormaghtigh E., and Ruysschaert J.-M. Theoretical conformational analysis of phospholipids bilayers. Biochem. Biophys. Res. Commun. 103 (1981) 301-310
Bult G., Gally H.U., Seelig A., and Zaccai G. Neutron diffraction studies on selectively deuterated phospholipids bilayers. Nature 271 (1978) 182-184
Dyck M., Krüger P., and Lösche M. Headgroup organization and hydration of methylated phosphatidylethanolamines in Langmuir monolayers. Phys. Chem. Chem. Phys. 7 (2005) 150-156
Brasseur R. TAMMO : Theoretical Analysis of Membrane Molecular Organization. In: Brasseur R. (Ed). Molecular Description of Biological Membranes by Computer Aided Conformational Analysis (1990), CRC Press, Boca Raton, FL 203-219
Brasseur R., Deleers M., and Ruysschaert J.-M. Mode of organization of amphiphilic molecules at a lipid-water interface: a conformational analysis. J. Colloid Interface Sci. 114 (1986) 277-281
Brasseur R., Deleers M., and Ruysschaert J.-M. Sequence of ionophore conformational changes induced by a simulated membrane/water interface. Biosci. Rep. 4 (1984) 651-658
Razafindralambo H., Paquot M., Hbid C., Jacques P., and Thonart P. Purification of antifungal lipopeptides by reversed-phase high-performance liquid chromatography. J. Chromatogr. 639 (1993) 81-85
Philipps M.C., and Chapman D. Monolayer characteristics of saturated 1,2-diacylphosphatidylcholines (lecithins) and phosphatidylethanolamines at the air-water interface. Biochim. Biophys. Acta 163 (1968) 301-313
Shapovalov V.L., Kotova E.A., Rokitskaya T.I., and Antonenko Y.N. Effect of gramicidin A on the dipole potential of phospholipid membranes. Biophys. J. 77 (1999) 299-305
Bordi F., Cametti C., De Luca F., Gili T., Gaudino D., and Sennato S. Charged lipid monolayers at the air-solution interface: coupling to polyelectrolytes. Colloids Surf., B Biointerfaces 29 (2003) 149-157
Zhao L., and Feng S. Effects of lipid chain length on molecular interactions between paclitaxel and phospholipid within model biomembranes. J. Colloid Interface Sci. 74 (2004) 55-68
Giocondi M., Vie V., Lesniewska E., Milhiet P., Zinke-Allmang M., and Le Grimellec C. Phase topology and growth of single domains in lipid bilayers. Langmuir 17 (2001) 1653-1659
Heerklotz H., and Seelig J. Detergent-like action of the antibiotic peptide surfactin on lipid membranes. Biophys. J. 81 (2001) 1547-1554
Fattal D., and Benshaul A. A molecular-model for lipid-protein interaction in membranes - the role of hydrogen mismatch. Biophys. J. 65 (1993) 1795-1809
Killian J.A. Hydrophobic mismatch between proteins and lipids in membranes. Biochim. Biophys. Acta 1376 (1998) 401-416
Wallace E., Hooper N., and Olmstedz P. Effect of hydrophobic mismatch on phase behavior of lipid membranes. Biophys. J. 90 (2006) 4104-4118
De Koker R.D., and McConnell H.M. Circle to dogbone: shapes and shape transitions of lipid monolayer domains. J. Phys. Chem. 97 (1993) 13419
Seul M., and Andelman D. Domain shapes and patterns - the phenomenology of modulated phases. Science 267 (1995) 476-483
Perkovic S., and McConnell H. Cloverleaf monolayer domains. J. Phys. Chem., B 101 (1997) 381-388
Smorodin V., and Melo E. Shape and dimensions of gel-domains in phospholipid bilayers: a theoretical study. J. Phys. Chem., B 105 (2001) 6010-6016
M. Deleu, Propriétés de la surfactine et de la fengycine A aux interfaces liquide/liquide et dans des emulsions modèles, PhD thesis, Gembloux Agricultural University, 2000, 236p.
Amrein M., vonNahmen A., and Sieber M. A scanning force and fluorescence light microscopy study of the structure and function of a model pulmonary surfactant. Eur. Biophys. J. 26 (1997) 349-357
Krol S., Ross M., Sieber M., Kunneke S., Galla H., and Janshoff A. Formation of three-dimensional protein-lipid aggregates in monolayer films induced by surfactant protein B. Biophys. J. 79 (2000) 904-918
Rinia H., Boots J., Rijkers D., Kik R., Snel M., Demel R., Killian J., van der Eerden J., and de Kruijff B. Domain formation in phosphatidylcholine bilayers containing transmembrane peptides: specific effects of flanking residues. Biochemistry 41 (2002) 2814-2824
de Planque M., Greathouse D., Koeppe R., Schafer H., Marsh D., and Killian J. Influence of lipid/peptide hydrophobic mismatch on the thickness of diacylphosphatidylcholine bilayers. A H-2 NMR and ESR study using designed transmembrane alpha-helical peptides and gramicidin A. Biochemistry 37 (1998) 9333-9345
Tahara Y., Murata M., Ohnishi S., Fujiyoshi Y., Kikuchi M., and Yamamoto Y. Functional signal peptide reduces bilayer thickness of phosphatidylcholine liposomes. Biochemistry 31 (1992) 8747-8754
Duque D., Li X., Katsov K., and Schick M. Molecular theory of hydrophobic mismatch between lipids and peptides. J. Chem. Phys. 116 (2002) 10478-10484
Miñones J., Patino J.M.R., Conde O., Carrera C., and Seoane R. The effect of polar groups on structural characteristics of phospholipid monolayers spread at the air-water interface. Colloids Surf., A Physicochem. Eng. Asp. 203 (2002) 273-286
Zhao L., and Feng S.-S. Effects of lipid chain unsaturation and headgroup type on molecular interactions between paclitaxel and phospholipids within model biomembrane. J. Colloid Interface Sci. 285 (2005) 326-335
Chernomordik L. Non-bilayer lipids and biological fusion intermediates. Chem. Phys. Lipids 81 (1996) 203-213
Sen A., Yang P., Mantsch H., and Hui S. Extended hydrogen-bonded structures of phosphatidylethanolamine. Chem. Phys. Lipids 47 (1988) 109-116
Seddon J. Structure of the inverted hexagonal (HII) phase, and non-lamellar phase-transitions of lipids. Biochim. Biophys. Acta 1031 (1990) 1-69
Pink D., McNeil S., Quinn B., and Zuckermann M. A model of hydrogen bond formation in phosphatidylethanolamine bilayers. Biochim. Biophys. Acta, Biomembr. 1368 (1998) 289-305
Nicolas J.P. Molecular dynamics simulation of surfactin molecules at the water-hexane interface. Biophys. J. 85 (2003) 1377-1391
Marsh D. Lateral pressure in membranes. Biochim. Biophys. Acta 1286 (1996) 183-223
Kuzmin P., Akimov S., Chizmadzhev Y., Zimmerberg J., and Cohen F. Line tension and interaction energies of membrane rafts calculated from lipid splay and tilt. Biophys. J. 88 (2005) 1120-1133
Kracht M., Rokos H., Ozel M., Kowall M., Pauli G., and Vater J. Antiviral and hemolytic activities of surfactin isoforms and their methyl ester derivatives. J. Antibiot. 52 (1999) 613-619
Cullis P.R., Fenske D.B., and Hope M.J. In: Vance D.E., and Vance J. (Eds). New Comprehensive Biochemistry. Biochemistry of Lipids, Lipoproteins and Membranes vol. 31 (1996), Elsevier, North-Holland, Amsterdam 1-33
Itokawa H., Miyashita T., Morita H., Takeya K., Hirano T., Homma M., and Oka K. Structural and conformational studies of [Ile7] and [Leu7]surfactins from Bacillus subtilis natto. Chem. Pharm. Bull. 42 (1994) 604-607
