Binding of Pediocin PA-1 with Anionic Lipid Induces Model Membrane Destabilization

Applied and Environmental Microbiology

Volumn 69, Issue 11, 2003, Pages 6777-6784

  Gaussier, Hélène ^a   Lefèvre, Thierry ^a   Subirade, Muriel ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOLOGICAL MEMBRANES; CONFORMATIONS; DEHYDRATION; FOURIER TRANSFORM INFRARED SPECTROSCOPY; PHASE TRANSITIONS; PHOSPHOLIPIDS;

STRETCHING VIBRATIONS;

LIPIDS;

DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIMYRISTOYLPHOSPHATIDYLGLYCEROL; PEDIOCIN; PEDIOCIN PA 1; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; CONFORMATION; INFRARED SPECTROSCOPY; LIPID BILAYER; MEMBRANE BIOLOGY; MEMBRANE DESTABILIZATION; PHASE TRANSITION; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE;

ANTI-BACTERIAL AGENTS; BACTERIOCINS; CELL MEMBRANE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; LIPID BILAYERS; MEMBRANE LIPIDS; MODELS, BIOLOGICAL; PHOSPHATIDYLGLYCEROLS; PROTEIN CONFORMATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 10744227640     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.69.11.6777-6784.2003     Document Type: Article

References (78)

1. Asher, I. M., and I. W. Levin. 1977. Effects of temperature and molecular interactions on the vibrational infrared spectra of phospholipid vesicles. Biochim. Biophys. Acta 468:63-72.
2. Barone, G., F. Catanzano, P. Del Vecchio, D. Fessas, C. Giancola, and G. Graziano. 1994. The effect of pH on thermal stability of globular proteins: a critical insight. J. Therm. Anal. 42:383-395.
3. Benachir, T., and M. Lafleur. 1995. Study of vesicle leakage induced by melittin. Biochim. Biophys. Acta 1235:452-460.
4. Bennick, M. H. J., B. Vanloo, R. Brasseur, L. G. M. Gorris, and E. J. Smid. 1998. A novel bacteriocin with a YGNGV motif from vegetable-associated Enterococcus mundtii: full characterization and interaction with target organisms. Biochim. Biophys. Acta 1373:47-58.
5. Bhunia, A. K., M. C. Johnson, and B. Ray. 1988. Purification, characterization and antimicrobial spectrum of a bacteriocin produced by Pediococcus acidilactici. J. Appl. Bacteriol. 65:261-268.
6. Blume, A., W. Hubner, and G. Messner. 1988. Fourier transform infrared spectroscopy of 13C=O-labeled phospholipids hydrogen bonding to carbonyl groups. Biochemistry 27:8239-8249.
7. 2H NMR study. Biochemistry 39:11425-11433.
8. Bouchard, M., and M. Auger. 1993. Solvent history dependence of gramicidin-lipid interactions: a Raman and infrared spectroscopic study. Biophys. J. 65:2484-2492.
9. Breukink, E., P. Ganz, B. de Kruijff, and J. Seelig. 2000. Binding of nisin Z to bilayer vesicles as determined with isothermal titration calorimetry. Biochemistry 39:10247-19254.
10. a. Byler, D. M., and H. Susi. 1986. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25:469-487.
11. Cameron, D. G., H. L. Casal, and H. H. Mantsch. 1980. Characterization of the pretransition in 1, 2-dipalmitoyl-sn-glycero-3-phosphocholine by Fourier transform infrared spectroscopy. Biochemistry 19:3665-3672.
12. Carrier, D., H. H. Mantsch, and P. T. T. Wong. 1990. Pressure-induced reversible changes in secondary structure of poly(L-Lysine): an IR spectroscopic study. Biopolymers 29:837-844.
13. Casal, H. L., and H. H. Mantsch. 1984. Polymorphic phase behavior of phospholipid membranes studied by infrared spectroscopy. Biochim. Biophys. Acta 779:381-401.
14. Casal, H. L., H. H. Mantsch, and H. Hauser. 1987. Infrared studies of fully hydrated saturated phosphatidylserine bilayers. Effect of Li+ and Ca2+. Biochemistry 26:4408-4416.
15. Chen, Y., R. Shapira, M. Eisenstein, and T. J. Montville. 1997. Functional characterization of pediocin PA-1 binding to liposomes in the absence of a protein receptor and its relationship to a predicted tertiary structure. Appl. Environ. Microbiol. 63:524-531.
16. Chen, Y., R. D. Ludescher, and T. J. Montville. 1997. Electrostatic interactions, but not the YGNGV consensus motif, govern the binding of pediocin PA-1 and its fragments to phospholipid vesicles. Appl. Environ. Microbiol. 63:4770-4777.
17. Chen, Y., R. D. Ludescher, and T. J. Montville. 1998. Influence of lipid composition on pediocin PA-1 binding to phospholipid vesicles. Appl. Environ. Microbiol. 64:3530-3532.
18. Chinkindas, M. L., M. J. Garcia-Garcera, A. J. M. Dreissen, A. M. Ledeboer, J. Nissen-Meyer, I. F. Nes, T. Abee, W. N. Konings, and G. Venema. 1993. Pediocin PA-1, a bacteriocin from Pediococcus acidilactici PAC 1.0, forms hydrophilic pores in the cytoplasmic membrane of target cells. Appl. Environ. Microbiol. 59:3577-3584.
19. Chirgadze, Y. N., O. V. Fedorov, and N. P. Trushina. 1975. Estimation of amino acid residue side-chain absorption in the infrared spectra of protein solutions in heavy water. Biopolymers 14:679-694.
20. Clark, A. H., D. H. Saunderson, and A. Suggett. 1981. Infrared and laser-Raman spectroscopic studies of thermally-induced globular protein gels. Int. J. Pept. Protein Res. 17:353-364.
21. Dave, N., A. Troullier, I. Mus-Veteau, M. Dunach, G. Leblanc, and E. Padros. 2000. Secondary structure components and properties of the melibiose permease from Escherichia coli: a Fourier transform infrared spectroscopy analysis. Biophys. J. 79:747-755.
22. Dluhy, R., D. G. Cameron, H. H. Mantsch, and R. Mendelsohn. 1983. Fourier transform infrared spectroscopic studies of the effect of calcium ions on phosphatidylserine. Biochemistry 22:6318-6325.
23. Eijsink, V. G., M. Skeie, P. H. Middelhoven, M. B. Brurberg, and I. F. Nes. 1998. Comparative studies of class IIa bacteriocins of lactic acid bacteria. Appl. Environ. Microbiol. 64:3275-3281.
24. El Jastimi, R., and M. Lafleur. 1997. Structural characterization of free and membrane-bound nisin by infrared spectroscopy. Biochim. Biophys. Acta 1324:151-158.
25. El Jastimi, R., and M. Lafleur. 1999. Characterization of permeability and morphological perturbations induced by nisin on phosphatidylcholine membranes. Biophys. J. 77:842-852.
26. Ennahar, S., T. Sashihara, K. Sonomoto, and A. Ishizaki. 2000. Class IIa bacteriocin: biosynthesis, structure and activity. FEMS Microbiol. 24:85-106.
27. Fabian, H., C. Schultz, J. Backmann, U. Hahn, W. Saengen, H. H. Mantsh, and D. Nauman. 1994. Secondary structure and oligomerization behavior of equilibrium unfolding intermediates of the λ Cro repressor. Biochemistry 33:10725-10730.
28. Fimland, G., O. R. Blingsmo, K. Sletten, G. Jung, I. F. Nes, and J. Nissen-Meyer. 1996. New biologically active hybrid bacteriocins constructed by combining regions from various pediocin-like bacteriocins: the C-terminal region is important for determining specificity. Appl. Environ. Microbiol. 62:3313-3318.
29. Garidel, P., A. Blume, and W. A. Hubner. 2000. Fourier transform infrared spectroscopic study of the interaction of alkaline earth cations with the negatively charged phospholipid 1, 2-dimyristoyl-sn-glycero-3-phosphoglycerol. Biochim. Biophys. Acta 1466:245-259.
30. Gaussier, H., H. Morency, M. C. Lavoie, M. Subirade. 2002. Replacement of trifluoroacetic acid with HCl in the hydrophobic purification steps of pediocin PA-1: a structural effect. Appl. Environ. Microbiol. 68:4803-4808.
31. Gaussier, H., M. C. Lavoie, and M. Subirade. 2003. Conformational changes of pediocin in an aqueous medium monitored by Fourier transform infrared spectroscopy: a biological implication. Int. J. Biol. Macromol. 32:1-9.
32. Gazit, E., A. Boman, H. G. Boman, and Y. Shai. 1995. Interaction of the mammalian antibacterial peptide cecropin P1 with phospholipid vesicles. Biochemistry 34:11479-11488.
33. Gericke, A., and H. Hühnerfuss. 1995. The conformational order and head-group structure of long-chain alkanoic acid ester monolayers at the air/water interface. Ber. Bunsenges Phys. Chem. 99:641-650.
34. Glaose, P. K., and F. A. Long. 1960. Use of glass electrode to measure acidities in deuterium oxide. J. Phys. Chem. 64:188-190.
35. Goormaghtigh, E., V. Cabiaux, and J. M. Ruysschaert. 1994. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy, p. 329-362. In H. J. Hilderson and G. B. Ralston (ed.), Subcellular biochemistry: physicochemical methods in the study of biomembranes. Plenum Press, New York, N.Y.
36. Henderson, J. T., A. L. Chopko, and P. Dick Van Wassenaar. 1992. Purification and primary structure of pediocin PA-1 produced by Pediococcus acidilactici PAC-1.0. Arch. Biochem. Biophys. 295:5-12.
37. Jackson, M., H. H. Mantsch, and H. Spencer. 1992. Conformation of magainin 2 and related peptides in aqueous solution and membrane environment probed by Fourier transform in infrared spectroscopy. Biochemistry 31:7289-7293.
38. Jager, K., and S. Harlander. 1992. Characterization of a bacteriocin from Pediococcus acidilactici PC and comparison of bacteriocin-producing strains using molecular typing procedures. Appl. Microbiol. Biotechnol. 37:631-637.
39. Klaenhammer, T. R. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12:39-86.
40. Kodati, V. R., and M. Lafleur. 1993. Comparison between orientational and conformational orders in fluid lipid bilayers. Biophys. J. 64:163-170.
41. Krimm, S., and J. Bandekar. 1986. Vibrational spectroscopy and conformation of peptides, polypeptides and proteins. Adv. Protein Chem. 38:181-364.
42. Ladokhin, A. S., and S. H. White. 2001. 'Detergent-like' permeabilization of anionic lipid vesicles by melittin. Biochim. Biophys. Acta 1514:253-260.
43. Ladokhin, A. S., M. E. Selsted, and S. H. White. 1997. Sizing membrane pores in lipid vesicles by leakage of co-encapsulated markers: pore formation by melittin. Biophys. J. 72:1762-1766.
44. Lafrance, C. P., J. E. Blochet, and M. Pezolet. 1997. N-acylphosphatidylethanolamines: effect of the N-acyl chain length on its orientation. Biophys. J. 72:2559-2568.
45. Lefevre, T., and M. Piquart. 1998. Thermotropic aspects of multilamellar organization of mono-unsaturated phospholipid OPPC. Chem. Phys. Lipids 92:79-89.
46. Lefevre, T., and M. Subirade. 2000. Molecular differences in the formation and structure of fine-stranded and particulate beta-lactoglobulin gels. Biopolymers 54:578-586.
47. Lefevre, T., and M. Subirade. 2001. Conformational rearrangement of beta-lactoglobulin upon interaction with an anionic membrane. Biochim. Biophys. Acta 1549:37-50.
48. Lewis, R. N., and R. N. McElhaney. 1992. Structures of the subgel phases of n-saturated diacyl phosphatidylcholine bilayers: FTIR spectroscopic studies of 13 C=O and 2H labeled lipids. Biophys. J. 61:63-77.
49. Lewis, R. N., R. N. McElhaney, W. Pohle, and H. H. Mantsch. 1994. Components of the carbonyl stretching band in the infrared spectra of hydrated 1,2-diacylglycerolipid bilayers: a reevaluation. Biophys. J. 67:2367-2375.
50. Mantsch, H. H., A. Martin, and D. G. Cameron. 1981. Characterization by infrared spectroscopy of the bilayer to nonbilayer phase transition of phosphatidylethanolamines. Biochemistry 20:3138-3145.
51. Matsuzaki, K., M. Harada, S. Funakoshi, N. Fujii, and K. Miyajima. 1991. Physicochemical determinant for the interactions of magainins 1 and 2 with acidic lipid bilayers. Biochim. Biophys. Acta 1063:162-170.
52. Matsuzaki, K., O. Murase, H. Tokuda, S. Funakoshi, N. Fujii, and K. Miyajima. 1994. Orientational and aggregational states of magainin 2 in phospholipid bilayers. Biochemistry 33:3342-3349.
53. Matsuzaki, K., S. Yoneyama, N. Fujii, K. Miyajima, Y. Kirino, and K. Ansai. 1997. Membrane permeabilization mechanisms of a cyclic antimicrobial peptide, tachyplesin I, and its linear analog. Biochemistry 32:9799-9806.
54. Mazzotta, A. S., and T. J. Montville. 1999. Nisin induces changes in membrane fatty acid composition of Listeria monocytogenes nisin-resistant strains at 10°C and 30°C. J. Appl. Microbiol. 82:32-38.
55. Miick, S. M., G. V. Martinez, W. R. Fiori, A. P. Todd, and G. L. Millhauser. 1992. Short alanine-based peptides may form 3(10)-helices and not alpha-helices in aqueous solution. Nature 359:653-655.
56. Montville, T. J., and Y. Chen. 1998. Mechanistic action of pediocin and nisin: recent progress and unresolved questions. Appl. Microbiol. Biotechnol. 50:511-519.
57. Muga, A., H. H. Mantsch, and W. K. Surewicz. 1991. Apocytochrome c interaction with phospholipid membranes studied by Fourier-transform infrared spectroscopy. Biochemistry 30:2629-2635.
58. Muga, A., W. K. Surewicz, P. T. Wong, and H. H. Mantsch. 1990. Structural studies with the uveopathogenic peptide M derived from retinal S-antigen. Biochemistry 29:2925-2930.
59. Nabet, A., M. Auger, and M. Pézolet. 2000. Investigation of the temperature behavior of the bands due to the methylene stretching vibrations of phospholipid acyl chains by two-dimensional infrared correlation spectroscopy. Appl. Spectrosc. 54:948-955.
60. Nissen-Meyer, J., H. H. Hauge, G. Fimland, V. G. H. Eijsink, and I. F. Nes. 1997. Ribosomally synthesized antimicrobial peptides produced by lactic acid bacteria: their function, structure, biogenesis, and their mechanism of action. Dev. Microbiol. 1:141-154.
61. Oren, Z., and Y. Shai. 1997. Selective lysis of bacteria but not mammalian cells by diastereomers of melittin: structure-function study. Biochemistry 36:1826-1835.
62. Panick, G., and R. Winter. 2000. Pressure-induced unfolding/refolding of ribonuclease A: static and kinetic Fourier transform infrared spectroscopy study. Biochemistry 39:1862-1869.
63. Parvez, I. Haris. 2000. Fourier transform infrared spectroscopic studies of peptides: potentials and pitfalls. ACS Symp. Ser. 750:54-95.
64. Pohle, W., C. Selle, H. Fritzsche, and H. Binder. 1998. Fourier Transform infrared spectroscopy as a probe for the study of the hydration of lipid self-assemblies. I. Methodology and general phenomena. Biospectroscopy 4:267-280.
65. Pouny, Y., D. Rapaport, A. Mor, P. Nicolas, and Y. Shai. 1992. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 31:12416-12423.
66. 10-helices in globular proteins. Reexamination of Amide I infrared bands of alpha-lactalbumin and their assignment to secondary structures. Int. J. Pept. Protein Res. 37:508-512.
67. Silvestro, L., and P. H. Axelsen. 2000. Membrane-induced folding of cecropin A. Biophys. J. 79:1465-1477.
68. Snyder, R. G. 1961. Vibrational spectra of crystalline n-paraffins. II. Intermolecular effects. J. Mol. Spectrosc. 7:116-144.
69. Snyder, R. G., H. L. Strauss, and C. A. Elliger. 1982. C-H stretching modes and the structure of n-alkyl chains. I. Long, disordered chains. J. Phys. Chem. 86:5145-5150.
70. Strahilevitz, J., A. Mor, P. Nicolas, and Y. Shai. 1994. Spectrum of antimicrobial activity and assembly of dermaseptin-b and its precursor form in phospholipid membranes. Biochemistry 33:10951-10960.
71. Subirade, M., C. Salesse, D. Marion, and M. Pezolet. 1995. Interaction of a nonspecific wheat lipid transfer protein with phospholipid monolayers imaged by fluorescence microscopy and studied by infrared spectroscopy. Biophys. J. 69:974-988.
72. Surewicz, W. K., and H. H. Mantsch. 1988. New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim. Biophys. Acta 952:115-130.
73. Umemura, J., D. G. Cameron, and H. H. Mantsch. 1980. A Fourier transform infrared spectroscopic study of the molecular interaction of cholesterol with 1,2-dipalmitoyl-sn-glycero-3-phosphocholine. Biochim. Biophys. Acta 602:32-44.
74. Venyaminov, S. Y., and N. N. Kalnin. 1990. Quantitative IR spectrophotometry of peptide compounds in water solutions. Spectral parameters of amino acid residue absorption bands. Biopolymers 30:1243-1257.
75. Verheul, A., N. J. Russell, R. Van'T Hof, F. M. Rombouts, and T. Abee. 1997. Modifications of membrane phospholipid composition in nisin-resistant Listeria monocytogenes Scott A. Appl. Environ. Microbiol. 63:3451-3457.
76. Watson, R. M., R. W. Woody, R. V. Lewis, D. S. Bohle, A. H. Andreotti, B. Ray, and K. W. Miller. 2001. Conformational changes in pediocin AcH upon vesicle binding and approximation of the membrane-bound structure in detergent micelles. Biochemistry 40:14037-14046.
77. Watts, A., K. Harlos, W. Maschke, and D. Marsh. 1978. Control of the structure and fluidity of phosphatidylglycerol bilayers by pH titration. Biochim. Biophys. Acta 510:63-74.
78. Ziegler, G. R., and E. A. Foegeding. 1990. The gelation of proteins. Adv. Food Nutr. Res. 34:203-298.