Hen egg white lysozyme permeabilizes Escherichia coli outer and inner membranes

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 41, 2013, Pages 9922-9929

  Derde, Melanie ^a,b   Lechevalier, Valérie ^a,b   Guérin Dubiard, Catherine ^a,b   Cochet, Marie Françoise ^a,b   Jan, Sophie ^a,b   Baron, Florence ^a,b   Gautier, Michel ^a,b   Vié, Véronique ^c   Nau, Françoise ^a,b  

^a AGROCAMPUS OUEST   (France)

^b UMR1253   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

antimicrobial activity; Gram negative bacteria; lysozyme; membrane permeability

Indexed keywords

ANTI-MICROBIAL ACTIVITY; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIUM; HEN EGG WHITE LYSOZYME; MEMBRANE PERMEABILITY; NATURAL PRESERVATIVES; SPECTRO-PHOTOMETRIC METHOD; SYNTHETIC MOLECULES;

BACTERIA; ENZYMES; ESCHERICHIA COLI;

MEMBRANES;

ANTIINFECTIVE AGENT; HEN EGG LYSOZYME; LYSOZYME;

ANIMAL; ARTICLE; CELL MEMBRANE PERMEABILITY; CHEMISTRY; CHICKEN; DRUG EFFECT; ESCHERICHIA COLI;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL MEMBRANE PERMEABILITY; CHICKENS; ESCHERICHIA COLI; MURAMIDASE;

EID: 84886909835     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf4029199     Document Type: Article

References (46)

1. TNS Opinion and Social. Special Eurobarometer 354: Food-related risks, 2010.
2. Bruhn, C. M. Consumer attitudes toward food additives. In Food Additives, 2; Branen, A. L., Davidson, P. M., Salminen, S., Thorngate, J. H., Eds.; Dekker: New York, 2002; pp 111-119.
3. Masschalck, B.; Michiels, C. W. Antimicrobial properties of lysozyme in relation to foodborne vegetative bacteria Crit. Rev. Microbiol. 2003, 29, 191-214
4. Sonni, F.; Chinnici, F.; Natali, N.; Riponi, C. Pre-fermentative replacement of sulphur dioxide by lysozyme and oenological tannins: effect on the formation and evolution of volatile compounds during the bottle storage of white wines Food Chem. 2011, 129, 1193-1200
5. Carini, S.; Mucchetti, G.; Neviani, E. Lysozyme: activity against Clostridia and use in cheese production-a review Microbiol., Aliments, Nutr. 1985, 3, 299-320
6. Pellegrini, A.; Thomas, U.; Vonfellenberg, R.; Wild, P. Bactericidal activities of lysozyme and aprotinin against Gram-negative and Gram-positive bacteria related to their basic character J. Appl. Bacteriol. 1992, 72, 180-187
7. Pellegrini, A.; Thomas, U.; Wild, P.; Schraner, E.; von Fellenberg, R. Effect of lysozyme or modified lysozyme fragments on DNA and RNA synthesis and membrane permeability of Escherichia coli Microbiol. Res. 2000, 155, 69-77
8. Laible, N. J.; Germaine, G. R. Bactericidal activity of human lysozyme, muramidase-inactive lysozyme, and cationic polypeptides against Streptococcus-sanguis and Streptococcus-faecalis inhibition by chitin oligosaccharides Infect. Immun. 1985, 48, 720-728
9. Mine, Y.; Ma, F.; Lauriau, S. Antimicrobial peptides released by enzymatic hydrolysis of hen egg white lysozyme J. Agric. Food Chem. 2004, 52, 1088-1094
10. Ibrahim, H. R.; Thomas, U.; Pelligrini, A. A helix-loop-helix peptide at the upper lip of the active site cleft of lysozyme confers potent antimicrobial activity with membrane permeabilization action J. Biol. Chem. 2001, 47, 43767-43774
11. Ibrahim, H. R.; Imazato, K.; Ono, H. Human lysozyme possesses novel antimicrobial peptides within its N-terminal domain that target bacterial respiration J. Agri. Food Chem. 2011, 59, 10336-10345
12. Ibrahim, H. R.; Kato, A.; Kobayashi, K. Antimicrobial effects of lysozyme against Gram-negative bacteria due to covalent binding of palmitic acid J. Agri. Food Chem. 1991, 39, 2077-2082
13. Ibrahim, H. R.; Hatta, H.; Fujiki, M.; Kim, M.; Yamamoto, T. Enhanced antimcirobial action of lysozyme against Gram-negative and Gram-positive bacteria due to modification with perillaldehyde J. Agric. Food Chem. 1994, 42, 1813-1817
14. Ibrahim, H. R.; Kobayashi, K.; Kato, A. Length of hydrocarbon chain and antimicrobial action to Gram-negative bacteria of fatty acylated lysozyme J. Agric. Food Chem. 1993, 41, 1164-1168
15. Nakamura, S.; Kato, A.; Kobayashi, K. Bifunctional lysozyme galactomannan conjugate having excellent emulsifying properties and bactericidal effect J. Agric. Food Chem. 1992, 40, 735-739
16. Nakamura, S.; Kato, A.; Kobayashi, K. New antimicrobial characteristics of lysozyme dextran conjugate J. Agric. Food Chem. 1991, 39, 647-650
17. Ibrahim, H. R. On the novel catalytically-independent antimicrobial function of hen egg-white lysozyme: a conformation-dependent activity Nahrung 1998, 42, 187-193
18. Ibrahim, H. R.; Higashiguchi, S.; Koketsu, M.; Juneja, L. R.; Kim, M.; Yamamoto, T.; Sugimoto, Y.; Aoki, T. Partially unfolded lysozyme at neutral pH agglutinates and kills Gram-negative and Gram-positive bacteria through membrane damage mechanism J. Agric. Food Chem. 1996, 44, 3799-3806
19. Ibrahim, H. R.; Higashiguchi, S.; Juneja, L. R.; Kim, M.; Yamamoto, T. A structural phase of heat-denatured lysozyme with novel antimicrobial action J. Agric. Food Chem. 1996, 44, 1416-1423
20. Ibrahim, H. R.; Higashiguchi, S.; Sugimoto, Y.; Aoki, T. Role of divalent cations in the novel bactericidal activity of the partially unfolded lysozyme J. Agric. Food Chem. 1997, 45, 89-94
21. Nguyen, L. T.; Haney, E. F.; Vogel, H. J. The expanding scope of antimicrobial peptide structures and their modes of action Trends Biotechnol. 2011, 29, 464-472
22. Jenssen, H.; Hamill, P.; Hancock, R. E. Peptide antimicrobial agents Clin. Microbiol. Rev. 2006, 19, 491-511
23. Deckers, D.; Masschalck, B.; Aertsen, A.; Callewaert, L.; Van Tiggelen, C. G. M.; Atanassova, M.; Michiels, C. W. Periplasmic lysozyme inhibitor contributes to lysozyme resistance in Escherichia coli Cell Mol. Life Sci. 2004, 61, 1229-1237
24. Callewaert, L.; Aertsen, A.; Deckers, D.; Vanoirbeek, K. G.; Vanderkelen, L.; Van Herreweghe, J. M.; Masschalck, B.; Nakimbugwe, D.; Robben, J.; Michiels, C. W. A new family of lysozyme inhibitors contributing to lysozyme tolerance in Gram-negative bacteria PloS Pathog. 2008, 4, e1000019
25. Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited Microbiol. Mol. Biol. Rev. 2003, 67, 593-656
26. Alakomi, H.; Paananen, A.; Suihko, M.; Helander, I.; Saarela, M. Weakening effect of cell permeabilizers on Gram-negative bacteria causing biodeterioration Appl. Environ. Microbiol. 2006, 72, 4695-4703
27. Vaara, M. Increased outer-membrane resistance to ethylenediaminetetraacetate and cations in novel lipid A mutants J. Bacteriol. 1981, 148, 426-434
28. Orlov, D. S.; Nguyen, T.; Lehrer, R. I. Potassium release, a useful tool for studying antimicrobial peptides J. Microbiol. Methods 2002, 49, 325-328
29. Silvestro, L.; Weiser, J. N.; Axelsen, P. H. Antibacterial and antimembrane activities of cecropin A in Escherichia coli Antimicrob. Agents Chemother. 2000, 44, 602-607
30. Wu, M.; Maier, E.; Benz, R.; Hancock, R. E. Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli Biochemistry 1999, 38, 7235-7242
31. Meincken, A.; Holroyd, D. L.; Rautenbach, M. Atomic force microscopy study of the effect of antimicrobial peptides on the cell envelope of Escherichia coli Antimicrob. Agents Chemother. 2005, 49, 4085-4092
32. Lehrer, R. I.; Barton, A.; Ganz, T. Concurrent assessment of inner and outer-membrane permeabilization and bacteriolysis in Escherichia coli by multiple-wavelength spectrophotometry J. Immunol. Methods 1988, 108, 153-158
33. Epand, R. F.; Pollard, J. E.; Wright, J. O.; Savage, P. B.; Epand, R. M. Depolarization, bacterial membrane composition, and the antimicrobial action of ceragenins Antimicrob. Agents Chemother. 2010, 54, 3708-3713
34. Gonzalez, M.; Gueguen, Y.; Destoumieux-Garzon, D.; Romestand, B.; Fievet, J.; Pugniere, M.; Roquet, F.; Escoubas, J. M.; Vandenbulcke, F.; Levy, O.; Saune, L.; Bulet, P.; Bachere, E. Evidence of a bactericidal permeability increasing protein in an invertebrate, the Crassostrea gigas Cg-BPI Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 17759-17764
35. Turner, J.; Cho, Y.; Dinh, N. N.; Waring, A. J.; Lehrer, R. I. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils Antimicrob. Agents Chemother. 1998, 42, 2206-2214
36. Gorbenko, G. P.; Ioffe, V. M.; Kinnunen, P. K. Binding of lysozyme to phospholipid bilayers: evidence for protein aggregation upon membrane association Biophys. J. 2007, 93, 140-153
37. Canfield, R. E.; Liu, A. K. The disulfide bonds of egg white lysozyme (muramidase) J. Biol. Chem. 1965, 240, 1997-2002
38. Terwilliger, T. C.; Eisenberg, D. The structure of melittin. II. Interpretation of the structure J. Biol. Chem. 1982, 257, 6016-6022
39. Lee, M. T.; Sun, T. L.; Hung, W. C.; Huang, H. W. Process of inducing pores in membranes by melittin Proc. Natl. Acad. Sci. U.S.A. 2013, 10.1073/pnas.1307010110
40. Wild, P.; Gabrieli, A.; Schraner, E. M.; Pellegrini, A.; Thomas, U.; Frederik, P. M.; Stuart, M. C. A.; Vonfellenberg, R. Reevaluation of the effect of lysoyzme on Escherichia coli employing ultrarapid freezing followed by cryoelectronmicroscopy or freeze substitution Microsc. Res. Tech. 1997, 39 (3) 297-304
41. Vollmer, W.; Bertsche, U. Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli Biochim. Biophys. Acta 2008, 1778, 1714-1734
42. Silhavy, T. J; Kahne, D.; Walker, S. The bacterial cell envelope Cold Spring Harbor Perspect. Biol. 2010, 2, a000414
43. Mah, T. F.; O'Toole, G. A. Mechanisms of biofilm resistance to antimicrobial agents Trends Microbiol. 2001, 9, 34-39
44. Waters, C. M.; Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria Annu. Rev. Cell Dev. Biol. 2005, 21, 319-346
45. DeLisa, M. P.; Wu, C. F.; Wang, L.; Valdes, J. J.; Bentley, W. E. DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli J. Bacteriol. 2001, 183, 5239-5247
46. DeLisa, M. P.; Valdes, J. J.; Bentley, W. E. Mapping stress-induced changes in autoinducer AI-2 production in chemostat-cultivated Escherichia coli K-12 J. Bacteriol. 2001, 183, 2918-2928