Effects of surfactin on membrane models displaying lipid phase separation

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 2, 2013, Pages 801-815

  Deleu, Magali ^a   Lorent, Joseph ^b   Lins, Laurence ^a   Brasseur, Robert ^a   Braun, Nathalie ^b   El Kirat, Karim ^b   Nylander, Tommy ^c   Dufrêne, Yves F ^b   Mingeot Leclercq, Marie Paule ^b  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c LUND UNIVERSITY   (Sweden)

Author keywords

AFM; Ellipsometry; Laurdan and DPH fluorescence; Membrane interaction; Phase coexistence; Surfactin

Indexed keywords

DIOLEOYLPHOSPHATIDYLCHOLINE; DIPALMITOYLPHOSPHATIDYLCHOLINE; LIPOSOME; SURFACTIN;

ARTICLE; CHEMICAL COMPOSITION; CHEMICAL INTERACTION; CONTROLLED STUDY; HYDROPHOBICITY; LIPID BILAYER; LIPID MEMBRANE; PARTICLE SIZE; PH; PHASE SEPARATION; PRIORITY JOURNAL; SURFACE PROPERTY; TEMPERATURE;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; 2-NAPHTHYLAMINE; BACTERIAL PHYSIOLOGICAL PHENOMENA; CALORIMETRY; CELL MEMBRANE; DIPHENYLHEXATRIENE; FLUORESCEINS; LAURATES; LIGHT; LIPID BILAYERS; LIPIDS; LIPOPEPTIDES; LIPOSOMES; MICELLES; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; PEPTIDES, CYCLIC; PHOSPHATIDYLCHOLINES; PHOSPHOLIPIDS; RHODAMINES; SCATTERING, RADIATION; SPECTROMETRY, FLUORESCENCE;

BACTERIA (MICROORGANISMS);

EID: 84870666552     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.11.007     Document Type: Article

References (98)

1. K. Arima, A. Kakinuma, and G. Tamura Surfactin, a crystalline peptidelipid surfactant produced by Bacillus subtilis: isolation, characterization and its inhibition of fibrin clot formation Biochem. Biophys. Res. Commun. 31 1968 488 494
2. A. Kakinuma, G. Tamura, and K. Arima Wetting of fibrin plate and apparent promotion of fibrinolysis by surfactin, a new bacterial peptidelipid surfactant Experientia 24 1968 1120 1121
3. 1H-NMR, distance geometry, and molecular dynamics Biopolymers 34 1994 975 986
4. P. Tsan, L. Volpon, F. Besson, and J.M. Lancelin Structure and dynamics of surfactin studied by NMR in micellar media J. Am. Chem. Soc. 129 2007 1968 1977
5. M. Kracht, H. Rokos, M. Ozel, M. Kowall, G. Pauli, and J. Vater Antiviral and hemolytic activities of surfactin isoforms and their methyl ester derivatives J. Antibiot. Tokyo 52 1999 613 619
6. D. Vollenbroich, M. Ozel, J. Vater, R.M. Kamp, and G. Pauli Mechanism of inactivation of enveloped viruses by the biosurfactant surfactin from Bacillus subtilis Biologicals 25 1997 289 297
7. D. Vollenbroich, G. Pauli, M. Ozel, and J. Vater Antimycoplasma properties and application in cell culture of surfactin, a lipopeptide antibiotic from Bacillus subtilis Appl. Environ. Microbiol. 63 1997 44 49
8. A.W. Bernheimer, and L.S. Avigad Nature and properties of a cytolytic agent produced by Bacillus subtilis J. Gen. Microbiol. 61 1970 361 369
9. X. Huang, Z. Wei, G. Zhao, X. Gao, S. Yang, and Y. Cui Optimization of sterilization of Escherichia coli in milk by surfactin and fengycin using a response surface method Curr. Microbiol. 56 2008 376 381
10. N. Tsukagoshi, G. Tamura, and K. Arima A novel protoplast-bursting factor (surfactin) obtained from Bacillus subtilis IAM 1213. II. The interaction of surfactin with bacterial membranes and lipids Biochim. Biophys. Acta 196 1970 211 214
11. A.E. Zeraik, and M. Nitschke Biosurfactants as agents to reduce adhesion of pathogenic bacteria to polystyrene surfaces: effect of temperature and hydrophobicity Curr. Microbiol. 61 2010 554 559
12. L.K. Assie, M. Deleu, L. Arnaud, M. Paquot, P. Thonart, C. Gaspar, and E. Haubruge Insecticide activity of surfactins and iturins from a biopesticide Bacillus subtilis Cohn (S499 strain) Meded. Rijksuniv. Gent Fak. Landbouwkd. Toegep. Biol. Wet. 67 2002 647 655
13. Y. Imai, T. Sugino, A. Fujita, and A. Kakinuma Hypocholesterolimic effect of surfactin, a novel bacterial peptide lipid J. Takeda Res. Lab. 30 1971 728 734
14. D.H. Kim, K.W. Yu, E.A. Bae, H.J. Park, and J.W. Choi Metabolism of kalopanaxsaponin B and H by human intestinal bacteria and antidiabetic activity of their metabolites Biol. Pharm. Bull. 21 1998 360 365
15. M. Ongena, G. Henry, A. Adam, E. Jourdan, and P. Thonart Insights into the plant defense mechanisms induced by Bacillus lipopeptides Biol. Plant-Microb. Interactions 7 2010 1 5
16. S. Dufour, M. Deleu, K. Nott, B. Wathelet, P. Thonart, and M. Paquot Hemolytic activity of new linear surfactin analogs in relation to their physico-chemical properties Biochim. Biophys. Acta 1726 2005 87 95
17. 2 + is associated with mitochondria permeability transition pore involved in surfactin-induced MCF-7 cells apoptosis Chem. Biol. Interact. 190 2011 16 27
18. M. Deleu, H. Bouffioux, H. Razafindralambo, M. Paquot, C. Hbid, Ph. Thonart, Ph. Jacques, and R. Brasseur Interaction of surfactin with membranes: a computational approach Langmuir 19 2003 3377 3385
19. H. Heerklotz, and J. Seelig Detergent-like action of the antibiotic peptide surfactin on lipid membranes Biophys. J. 81 2001 1547 1554
20. H. Heerklotz, and J. Seelig Leakage and lysis of lipid membranes induced by the lipopeptide surfactin Eur. Biophys. J. 36 2007 305 314
21. H. Heerklotz, A. Tsamaloukas, K. Kita-Tokarczyk, P. Strunz, and T. Gutberlet Structural, volumetric, and thermodynamic characterization of a micellar sphere-to-rod transition J. Am. Chem. Soc. 126 2004 16544 16552
22. G. Henry, M. Deleu, E. Jourdan, P. Thonart, and M. Ongena The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses Cell. Microbiol. 13 2011 1824 1837
23. H. Kell, J.F. Holzwarth, C. Boettcher, R.K. Heenan, and J. Vater Physicochemical studies of the interaction of the lipoheptapeptide surfactin with lipid bilayers of L-alpha-dimyristoyl phosphatidylcholine Biophys. Chem. 128 2007 114 124
24. G. Francius, S. Dufour, M. Deleu, M. Paquot, M.P. Mingeot-Leclercq, and Y.F. Dufrene Nanoscale membrane activity of surfactins: influence of geometry, charge and hydrophobicity Biochim. Biophys. Acta 1778 2008 2058 2068
25. J. Liu, A. Zou, and B. Mu Toluidine blue: aggregation properties and distribution behavior in surfactin micelle solution Colloids Surf. B Biointerfaces 75 2010 496 500
26. H.H. Shen, R.K. Thomas, J. Penfold, and G. Fragneto Destruction and solubilization of supported phospholipid bilayers on silica by the biosurfactant surfactin Langmuir 26 2010 7334 7342
27. O. Bouffioux, A. Berquand, M. Eeman, M. Paquot, Y.F. Dufrene, R. Brasseur, and M. Deleu Molecular organization of surfactin-phospholipid monolayers: effect of phospholipid chain length and polar head Biochim. Biophys. Acta 1768 2007 1758 1768
28. C. Carrillo, J.A. Teruel, F.J. Aranda, and A. Ortiz Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin Biochim. Biophys. Acta 1611 2003 91 97
29. M. Eeman, A. Berquand, Y.F. Dufrene, M. Paquot, S. Dufour, and M. Deleu Penetration of surfactin into phospholipid monolayers: nanoscale interfacial organization Langmuir 22 2006 11337 11345
30. A. Grau, J.C. Gomez Fernandez, F. Peypoux, and A. Ortiz A study on the interactions of surfactin with phospholipid vesicles Biochim. Biophys. Acta 1418 1999 307 319
31. R. Maget-Dana, and M. Ptak Interactions of surfactin with membrane models Biophys. J. 68 1995 1937 1943
32. K. Simons, and W.L. Vaz Model systems, lipid rafts, and cell membranes Annu. Rev. Biophys. Biomol. Struct. 33 2004 269 295
33. L.A. Bagatolli, J.H. Ipsen, A.C. Simonsen, and O.G. Mouritsen An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes Prog. Lipid Res. 49 2010 378 389
34. J. Juhasz, J.H. Davis, and F.J. Sharom Fluorescent probe partitioning in giant unilamellar vesicles of 'lipid raft' mixtures Biochem. J. 430 2010 415 423
35. M.L. Schmidt, L. Ziani, M. Boudreau, and J.H. Davis Phase equilibria in DOPC/DPPC: conversion from gel to subgel in two component mixtures J. Chem. Phys. 131 Nov 2009 175103
36. S. Buchoux, J. Lai-Kee-Him, M. Garnier, P. Tsan, F. Besson, A. Brisson, and E.J. Dufourc Surfactin-triggered small vesicle formation of negatively charged membranes: a novel membrane-lysis mechanism Biophys. J. 95 2008 3840 3849
37. F. Van Bambeke, M.P. Mingeot-Leclercq, A. Schanck, R. Brasseur, and P.M. Tulkens Alterations in membrane permeability induced by aminoglycoside antibiotics: studies on liposomes and cultured cells Eur. J. Pharmacol. 247 1993 155 168
38. H. Razafindralambo, M. Paquot, C. Hbid, P. Jacques, J. Destain, and P. Thonart Purification of antifungal lipopeptides by reversed-phase high-performance liquid chromatography J. Chromatogr. 639 1993 81 85
39. J.P. Montenez, F. Van Bambeke, J. Piret, R. Brasseur, P.M. Tulkens, and M.P. Mingeot-Leclercq Interactions of macrolide antibiotics (Erythromycin A, roxithromycin, erythromycylamine [Dirithromycin], and azithromycin) with phospholipids: computer-aided conformational analysis and studies on acellular and cell culture models Toxicol. Appl. Pharmacol. 156 1999 129 140
40. G.R. Bartlett Colorimetric assay methods for free and phosphorylated glyceric acids J. Biol. Chem. 234 1959 469 471
41. M.P. Mingeot-Leclercq, M. Deleu, R. Brasseur, and Y.F. Dufrêne Atomic force microscopy of supported lipid bilayers Nat. Protoc. 3 2008 1654 1659
42. H.P. Vacklin, F. Tiberg, and R.K. Thomas Formation of supported phospholipid bilayers via co-adsorption with beta-D-dodecyl maltoside Biochim. Biophys. Acta 1668 2005 17 24
43. F. Tiberg, and M. Landgren Characterization of thin nonionic surfactant films at the silica/water interface by means of ellipsometry Langmuir 9 1993 927 932
44. M. Landgren, and B. Jönsson Determination of the optical properties of Si/SiO* surfaces by means of ellipsometry, using different ambient media J. Phys. Chem. 97 1993 1656 1660
45. F.L. McCrackin, E. Passaglia, R.R. Stromberg, and H.L. Steinberg Measurement of the thickness and refractive index of very thin films and the optical properties of surfaces by ellipsometry J. Res. Natl. Bur. Stand. Sect. A 67A 1963 363 377
46. H.P. Vacklin, F. Tiberg, G. Fragneto, and R.K. Thomas Phospholipase A2 hydrolysis of supported phospholipid bilayers: a neutron reflectivity and ellipsometry study Biochemistry 44 2005 2811 2821
47. P.A. Cuypers, J.W. Corsel, M.P. Janssen, J.M. Kop, W.T. Hermens, and H.C. Hemker The adsorption of prothrombin to phosphatidylserine multilayers quantitated by ellipsometry J. Biol. Chem. 258 1983 2426 2431
48. T. Parasassi, G. De Stasio, G. Ravagnan, R.M. Rusch, and E. Gratton Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence Biophys. J. 60 1991 179 189
49. T. Parasassi, and E. Gratton Membrane lipid domains and dynamics as detected by Laurdan fluorescence J. Fluoresc. 5 1995 59 69
50. L.A. Bagatolli, and E. Gratton Direct observation of lipid domains in free-standing bilayers using two-photon excitation fluorescence microscopy J. Fluoresc. 11 2001 141 161
51. W. Yu, P.T. So, T. French, and E. Gratton Fluorescence generalized polarization of cell membranes: a two-photon scanning microscopy approach Biophys. J. 70 1996 626 636
52. J. Giraldo, N.M. Vivas, E. Vila, and A. Badia Assessing the (a)symmetry of concentration-effect curves: empirical versus mechanistic models Pharmacol. Ther. 95 2002 21 45
53. R. Brasseur, J.A. Killian, B. De Kruijff, and J.M. Ruysschaert Conformational analysis of gramicidin-gramicidin interactions at the air/water interface suggests that gramicidin aggregates into tube-like structures similar as found in the gramicidin-induced hexagonal HII phase Biochim. Biophys. Acta 903 1987 11 17
54. L. Lins, A. Thomas-Soumarmon, T. Pillot, J. Vandekerchkhove, M. Rosseneu, and R. Brasseur Molecular determinants of the interaction between the C-terminal domain of Alzheimer's beta-amyloid peptide and apolipoprotein E alpha-helices J. Neurochem. 73 1999 758 769
55. R. Brasseur TAMMO: theoretical analysis of membrane molecular organisation Molecular Description of Biological Membrane Components by Computer-aided Conformational Analysis Brasser Edt I and II 1990 CRC Press Boca Raton, Fla 203 219
56. R.D. Kaiser, and E. London Location of diphenylhexatriene (DPH) and its derivatives within membranes: comparison of different fluorescence quenching analyses of membrane depth Biochemistry 37 1998 8180 8190
57. B.R. Lentz Use of fluorescent probes to monitor molecular order and motions within liposome bilayers Chem. Phys. Lipids 64 1993 99 116
58. M. Shinitzky, and Y. Barenholz Fluidity parameters of lipid regions determined by fluorescence polarization Biochim. Biophys. Acta 515 1978 367 394
59. J.N. Weinstein, S. Yoshikami, P. Henkart, R. Blumenthal, and W.A. Hagins Liposome-cell interaction: transfer and intracellular release of a trapped fluorescent marker Science 195 1977 489 492
60. P.I. Lelkes Methodogical aspects dealing with stability measurements of liposomes in vitro using the carboxyfluorescein assay Liposome Technology Gregoriadis Edts 3 1984 CRC Press 225 246
61. D. Hoekstra, T. de Boer, K. Klappe, and J. Wilschut Fluorescence method for measuring the kinetics of fusion between biological membranes Biochemistry 23 1984 5675 5681
62. M.L. Jackson, and B.J. Litman Rhodopsin-phospholipid reconstitution by dialysis removal of octyl glucoside Biochemistry 21 1982 5601 5608
63. M.L. Jackson, C.F. Schmidt, D. Lichtenberg, B.J. Litman, and A.D. Albert Solubilization of phosphatidylcholine bilayers by octyl glucoside Biochemistry 21 1982 4576 4582
64. S. Keller, A. Tsamaloukas, and H. Heerklotz A quantitative model describing the selective solubilization of membrane domains J. Am. Chem. Soc. 127 2005 11469 11476
65. S. Morandat, and K. El Kirat Membrane resistance to Triton X-100 explored by real-time atomic force microscopy Langmuir 22 2006 5786 5791
66. E. Schnitzer, D. Lichtenberg, and M.M. Kozlov Temperature-dependence of the solubilization of dipalmitoylphosphatidylcholine (DPPC) by the non-ionic surfactant Triton X-100, kinetic and structural aspects Chem. Phys. Lipids 126 2003 55 76
67. N. Hauet, F. Artzner, F. Boucher, C. Grabielle-Madelmont, I. Cloutier, G. Keller, P. Lesieur, D. Durand, and M. Paternostre Interaction between artificial membranes and enflurane, a general volatile anesthetic: DPPC-enflurane interaction Biophys. J. 84 2003 3123 3137
68. M. Deleu, M. Paquot, and T. Nylander Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes Biophys. J. 94 2008 2667 2679
69. T. Parasassi, G. Ravagnan, R.M. Rusch, and E. Gratton Modulation and dynamics of phase properties in phospholipid mixtures detected by Laurdan fluorescence Photochem. Photobiol. 57 1993 403 410
70. G. Balogh, G. Maulucci, I. Gombos, I. Horvath, Z. Torok, M. Peter, E. Fodor, T. Pali, S. Benko, T. Parasassi, M. De Spirito, J.L. Harwood, and L. Vigh Heat stress causes spatially-distinct membrane re-modelling in K562 leukemia cells PLoS One 6 2011 e21182
71. K. Gaus, E. Gratton, E.P. Kable, A.S. Jones, I. Gelissen, L. Kritharides, and W. Jessup Visualizing lipid structure and raft domains in living cells with two-photon microscopy Proc. Natl. Acad. Sci. U. S. A. 100 2003 15554 15559
72. L.A. Bagatolli, S.A. Sanchez, T. Hazlett, and E. Gratton Giant vesicles, Laurdan, and two-photon fluorescence microscopy: evidence of lipid lateral separation in bilayers Methods Enzymol. 360 2003 481 500
73. C. Dietrich, L.A. Bagatolli, Z.N. Volovyk, N.L. Thompson, M. Levi, K. Jacobson, and E. Gratton Lipid rafts reconstituted in model membranes Biophys. J. 80 2001 1417 1428
74. K.K. Halling, B. Ramstedt, J.H. Nystrom, J.P. Slotte, and T.K. Nyholm Cholesterol interactions with fluid-phase phospholipids: effect on the lateral organization of the bilayer Biophys. J. 95 2008 3861 3871
75. M. Engelk, P. Bojarski, R. Bloss, and H. Diehl Tamoxifen perturbs lipid bilayer order and permeability: comparison of DSC, fluorescence anisotropy, Laurdan generalized polarization and carboxyfluorescein leakage studies Biophys. Chem. 90 2001 157 173
76. S.V. Balasubramanian, R.B. Campbell, and R.M. Straubinger Propofol, a general anesthetic, promotes the formation of fluid phase domains in model membranes Chem. Phys. Lipids 114 2002 35 44
77. M.R. Gonzalez-Baro, H. Garda, and R. Pollero Effect of fenitrothion on dipalmitoyl and 1-palmitoyl-2-oleoylphosphatidylcholine bilayers Biochim. Biophys. Acta 1468 2000 304 310
78. A.B. Hendrich, K. Michalak, and O. Wesolowska Phase separation is induced by phenothiazine derivatives in phospholipid/sphingomyelin/cholesterol mixtures containing low levels of cholesterol and sphingomyelin Biophys. Chem. 130 2007 32 40
79. A. Berquand, M.P. Mingeot-Leclercq, and Y.F. Dufrene Real-time imaging of drug-membrane interactions by atomic force microscopy Biochim. Biophys. Acta 1664 2004 198 205
80. M.C. Giocondi, L. Pacheco, P.E. Milhiet, and C. Le Grimellec Temperature dependence of the topology of supported dimirystoyl-distearoyl phosphatidylcholine bilayers Ultramicroscopy 86 2001 151 157
81. Y.F. Dufrene, A. van der Wal, W. Norde, and P.G. Rouxhet X-ray photoelectron spectroscopy analysis of whole cells and isolated cell walls of Gram-positive bacteria: comparison with biochemical analysis J. Bacteriol. 179 1997 1023 1028
82. S. Morandat, and K. El Kirat Solubilization of supported lipid membranes by octyl glucoside observed by time-lapse atomic force microscopy Colloids Surf. B Biointerfaces 55 2007 179 184
83. S. Mukherjee, and A. Chattopadhyay Monitoring the organization and dynamics of bovine hippocampal membranes utilizing Laurdan generalized polarization Biochim. Biophys. Acta 1714 2005 43 55
84. J. Juhasz, J.H. Davis, and F.J. Sharom Fluorescent probe partitioning in GUVs of binary phospholipid mixtures: implications for interpreting phase behavior Biochim. Biophys. Acta 1818 2012 19 26
85. H. Heerklotz Triton promotes domain formation in lipid raft mixtures Biophys. J. 83 2002 2693 2701
86. F.M. Goni, M.A. Urbaneja, J.L. Arrondo, A. Alonso, A.A. Durrani, and D. Chapman The interaction of phosphatidylcholine bilayers with Triton X-100 Eur. J. Biochem. 160 1986 659 665
87. G.M. Alder, W.M. Arnold, C.L. Bashford, A.F. Drake, C.A. Pasternak, and U. Zimmermann Divalent cation-sensitive pores formed by natural and synthetic melittin and by Triton X-100 Biochim. Biophys. Acta 1061 1991 111 120
88. H. Patel, C. Tscheka, K. Edwards, G. Karlsson, and H. Heerklotz All-or-none membrane permeabilization by fengycin-type lipopeptides from Bacillus subtilis QST713 Biochim. Biophys. Acta 1808 2011 2000 2008
89. B. Apellaniz, S. Nir, and J.L. Nieva Distinct mechanisms of lipid bilayer perturbation induced by peptides derived from the membrane-proximal external region of HIV-1 gp41 Biochemistry 48 2009 5320 5331
90. T. Buranda, Y. Wu, D. Perez, A. Chigaev, and L.A. Sklar Real-time partitioning of octadecyl rhodamine B into bead-supported lipid bilayer membranes revealing quantitative differences in saturable binding sites in DOPC and 1:1:1 DOPC/SM/cholesterol membranes J. Phys. Chem. B 114 2010 1336 1349
91. F. Van Bambeke, P.M. Tulkens, R. Brasseur, and M.P. Mingeot-Leclercq Aminoglycoside antibiotics induce aggregation but not fusion of negatively-charged liposomes Eur. J. Pharmacol. 289 1995 321 333
92. A. De la Maza, and J.L. Parra Vesicle-micelle structural transition of phosphatidylcholine bilayers and Triton X-100 Biochem. J. 303 1994 907 914
93. U. Kragh-Hansen, M. le Maire, and J.V. Moller The mechanism of detergent solubilization of liposomes and protein-containing membranes Biophys. J. 75 1998 2932 2946
94. M. Silvander, and K. Edwards A method to detect leakage of DNA intercalators through liposome membranes Anal. Biochem. 242 1996 40 44
95. K. Edwards, J. Gustafsson, M. Almgren, and G. Karlsson Solubilization of lecithin vesicles by a cationic surfactant - intermediate structures in the vesicle micelle transition observed by cryo-transmission electron microscopy J. Colloid Interface Sci. 161 1993 299 309
96. C. Boettcher, H. Kell, J.F. Holzwarth, and J. Vater Flexible loops of thread-like micelles are formed upon interaction of L-alpha-dimyristoyl- phosphatidylcholine with the biosurfactant surfactin as revealed by cryo-electron tomography Biophys. Chem. 149 2010 22 27
97. M.M. Elsayed, and G. Cevc The vesicle-to-micelle transformation of phospholipid-cholate mixed aggregates: a state of the art analysis including membrane curvature effects Biochim. Biophys. Acta 1808 2011 140 153
98. A. Zemel, A. Ben Shaul, and S. May Modulation of the spontaneous curvature and bending rigidity of lipid membranes by interfacially adsorbed amphipathic peptides J. Phys. Chem. B 112 2008 6988 6996