Are cationic antimicrobial peptides also 'double-edged swords'?

Expert Review of Anti-Infective Therapy

Volumn 6, Issue 4, 2008, Pages 453-462

  Ginsburg, Isaac ^a   Koren, Erez ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Antibiotic resistance; Autolytic enzymes; Bacteriolysis; Cationic antimicrobial peptides; Lipoteichoic acid; Lysozyme; Membrane permeability; Postinfectious sequelae; Staphylococcus aureus

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; CHLORAMPHENICOL; CLINDAMYCIN; CLOXACILLIN; CURCUMIN; EPIGALLOCATECHIN GALLATE; LYSOZYME; METICILLIN; NAFCILLIN; PENICILLIN G; POLYCATION; POLYPHENOL; QUERCETIN; TANNIN; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIOXIDANT ACTIVITY; ARTICLE; BACTERIAL INFECTION; BACTERIOLYSIS; CELL WALL; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; LEUKOCYTE; NONHUMAN; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; BACTERIUM; DRUG EFFECT; REVIEW;

ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIA; BACTERIAL INFECTIONS; HUMANS;

EID: 54449085000     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/14787210.6.4.453     Document Type: Article

References (101)

1. Brogden KA. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3(3), 238-250 (2005).
2. Hale JD, Hancock RE. Alternative mechanisms of action of cationic antimicrobial peptides on bacteria. Expert Rev. Anti Infect. Ther. 5(6), 951-959 (2007).
3. Fleming A. On the remarkable bacteriolytic element found in tissues and secretion. Proc. R. Soc. B (93), 303-317 (1922).
4. Bichowsky-Slomnicki L, Berger A, Katchalski E, Kurtz J. The anti-bacterial action of some basic amino acid copolymers. Arch. Biochem. Biophys. 65(1), 400-413 (1956).
5. Chertov O, Yang D, Howard OM, Oppenheim JJ. Leukocyte granule proteins mobilize innate host defenses and adaptive immune responses. Immunol. Rev. 177, 68-78 (2000).
6. Elsbach P. The bactericidal/permeability-increasing protein (BPI) in antibacterial host defense. J. Leukoc. Biol. 64(1), 14-18 (1998).
7. 2-independent microbicidal systems of phagocytes. Rev. Infect. Dis. 5(5), 843-853 (1983).
8. Ganz T. Antimicrobial polypeptides in host defense of the respiratory tract. J. Clin. Invest. 109(6), 693-697 (2002).
9. Ganz T, Lehrer RI. Antibiotic peptides from higher eukaryotes: biology and applications. Mol. Med. Today 5(7), 292-297 (1999).
10. Glynn AA. The complement lysozyme sequence in immune bacteriolysis. Immunology 16(4), 463-471 (1969).
11. Hancock RE. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 1(3), 156-164 (2001).
12. Hancock RE, Scott MG. The role of antimicrobial peptides in animal defenses. Proc. Natl Acad. Sci. USA 97(16), 8856-8861 (2000).
13. Hirsch JG. Bactericidal action of histone. J. Exp. Med. 108(6), 925-944 (1958).
14. Lehrer RI, Ganz T. Cathelicidins: a family of endogenous antimicrobial peptides. Curr. Opin. Hematol. 9(1), 18-22 (2002).
15. Levy O. A neutrophil-derived anti-infective molecule: bactericidal/ permeability-increasing protein. Antimicrob. Agents Chemother. 44(11), 2925-2931 (2000).
16. Levy O. Antimicrobial proteins and peptides of blood: templates for novel antimicrobial agents. Blood 96(8), 2664-2672 (2000).
17. Odeberg H, Olsson I. Antibacterial activity of cationic proteins from human granulocytes. J. Clin. Invest. 56(5), 1118-1124 (1975).
18. Otvos L Jr. Antibacterial peptides and proteins with multiple cellular targets. J. Pept. Sci. 11(11), 697-706 (2005).
19. Risso A. Leukocyte antimicrobial peptides: multifunctional effector molecules of innate immunity. J. Leukoc. Biol. 68(6), 785-792 (2000).
20. Skarness RC, Watson DW. Anti-microbial factors of normal tissues and fluids. Bacteriol. Rev. 21, 273-294 (1957).
21. Yeaman MR, Bayer AS. Antimicrobial peptides from platelets. Drug Resist. Updat. 2(2), 116-126 (1999).
22. Yeaman MR, Yount NY. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55(1), 27-55 (2003).
23. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (6870), 389-395 (2002).
24. Zeya HI, Spitznagel JK. Antibacterial and enzymic basic proteins from leukocyte lysosomes: separation and identification. Science 142, 1085-1087 (1963).
25. Stolp H, Starr MP. Bacteriolysis. Annu. Rev. Microbiol. 19, 79-104 (1965).
26. Ferne M, Duchan Z, Rabinowitz-Begner S, Sela MN, Ginsburg I. The effect of leukocyte hydrolases on bacteria. XII. The release of lipopolysaccharide (LPS) from Salmonella typhi by leukocyte extracts, lysozyme, inflammatory exudates and by serum and synovial fluid and the modulation by anionic and cationic polyelectrolytes of LPS release and the sensitization of erythrocytes. Inflammation 3(1), 59-80 (1978).
27. Ginsburg I. Cationic polyelectrolytes: a new look at their possible roles as opsonins, as stimulators of respiratory burst in leukocytes, in bacteriolysis, and as modulators of immune-complex diseases (a review hypothesis). Inflammation 11 (4), 489-515 (1987).
28. Ginsburg I. The biochemistry of bacteriolysis: paradoxes, facts and myths. Microbiol. Sci. 5(5), 137-142 (1988).
29. Ginsburg I. Cationic polyelectrolytes: potent opsonic agents which activate the respiratory burst in leukocytes. Free Radic. Res. Commun. 8(1), 11-26 (1989).
30. Ginsburg I. Hypothesis: is a failure to prevent bacteriolysis and the synergy among microbial and host-derived proinflammatory agonists the main contributory factors to the pathogenesis of post-infectious sequelae? Inflammation 25(1), 1-6 (2001).
31. Ginsburg I. Cationic peptides from leukocytes might kill bacteria by activating their autolytic enzymes causing bacteriolysis: why are publications proposing this concept never acknowledged? Blood 97(8), 2530-2531 (2001).
32. Ginsburg I. Role of lipoteichoic acid in infection and inflammation. Lancet Infect. Dis. 2(3), 171-179 (2002).
33. Ginsburg I. Ihe role of bacteriolysis in the pathophysiology of inflammation, infection and post-infectious sequelae. APMIS 110(11), 753-770 (2002).
34. Ginsburg I. Bactericidal cationic peptides can also function as bacteriolysis-inducing agents mimicking β-lactam antibiotics?; it is enigmatic why this concept is consistently disregarded. Med. Hypotheses 62(3), 367-374 (2004).
35. Ginsburg I, Lahav M. Lysis and biodegradation of microorganisms in infectious sites may involve cooperation between leukocyte, serum factors and bacterial wall autolysins: a working hypothesis. Eur. J. Clin. Microbiol. 2(3), 186-191 (1983).
36. Ginsburg I, Lahav M, Giesbrecht P. Effect of leukocyte hydrolases on bacteria. XVI. Activation by leukocyte factors and cationic substances of autolytic enzymes in Staphylococcus aureus: modulation by anionic polyelectrolytes in relation to survival of bacteria in inflammatory exudates. Inflammation 6(3), 269-284 (1982).
37. Ginsburg I, Lahav M, Ne'eman N, Duchan Z, Chanes S, Sela MN. The interaction of leukocytes and their hydrolases with bacteria in vitro and in vivo: the modification of the bactericidal and bacteriolytic reactions by cationic and anionic macromolecular substances and by anti-inflammatory agents. Agents Actions 6(1-3), 292-305 (1976).
38. Lahav M, Ginsburg I. Effect of leukocyte hydrolases on bacteria. X. The role played by leukocyte factors, cationic polyelectrolytes, and by membrane-damaging agents in the lysis of Staphylacoccus aureus: relation to chronic inflammatory processes. Inflammation 2(2), 165-177 (1977).
39. Lahav M, Ne'eman N, Adler E, Ginsburg I. Effect of leukocyte hydrolases on bacteria. I. Degradation of 14C-labeled Streptococcus and Staphylococcus by leukocyte lysates in vitro. J. Infict. Dis. 129(5), 528-537 (1974).
40. Neeman N, Lahav M, Ginsburg I. The effect of leukocyte hydrolases on bacteria. II. The synergistic action of lysozyme and extracts of PMN, macrophages, lymphocytes, and platelets in bacteriolysis. Proc. Soc. Exp. Biol. Med. 146(4), 1137-1145 (1974).
41. Sela MN, Lahav M, Ginsburg I. Effect of leukocyte hydrolases on bacteria. IX. The release of lipoteichoic acid from group A streptococci and from Strep. mutants by leukocyte extracts and by lysozyme: relation to tissue damage in inflammatory sites. Inflammation 2(2), 151-164 (1977).
42. Wecke J, Lahav M, Ginsburg I, Giesbrecht P. Cell wall degradation of Staphylococcus aureus by lysozyme. Arch. Microbiol. 131(2), 116-123 (1982).
43. Holtje JV. From growth to autolysis: the murein hydrolases in Escherichia coli. Arch. Microbiol. 164(4), 243-254 (1995).
44. Vollmer W, Joris B, Charlier P, Foster S. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32(2), 259-286 (2008).
45. Ginsburg I, Lahav M. How are bacterial cells degraded by leukocytes in vivo? An enigma. Clin. Immunol, Newsl. 4(11), 147-153 (1983).
46. Thorne KJ, Oliver RC, Barrett AJ. Lysis and killing of bacteria by lysosomal proteinases. Infect. Immun. 14(2), 555-563 (1976).
47. Cottagnoud P, Tomasz A. Triggering of pneumococcal autolysis by lysozyme. J. Infect. Dis. 167(3), 684-690 (1993).
48. Coonrod JD, varble R, Yoneda K. Mechanism of killing of pneumococci by lysozyme. J. Infect. Dis. 164(3), 527-532 (1991).
49. Laible NJ, Germaine GR. Bactericidal activity of human lysozyme, muramidase-inactive lysozyme, and cationic polypeptides against Streptococcus sanguis and Streptococcus faecalis: inhibition by chitin oligosaccharides. Infect. Immun. 48(3), 720-728 (1985).
50. Bierbaum G, Sahl HG. Influence of cationic peptides on the activity of the autolytic endo-β-N-acetylglucosominidase of Staphylococcus simulans 22. FEMS Microbiol. Lett. 49(2-3), 223-227 (1989).
51. Galvez A. Valdivia F, Martinez-Bueno M, Maqueda M. Induction of autolysis in Enterococcus faecalis S-47 by peptide AS-48. J. Appl. Bacteriol. 69(3), 406-413 (1990).
52. Sakagami Y, Mimura M, Kajimura K, Yokoyama H, Nishimura H. Electronmicroscopic study ofthe bactericidal effect of OPB-2045, a new mono-biguanide disinfectant produced from biguanide group compounds, against Pseudomonas aeruginosa. J. Pharm. Pharmacol. 51(2), 201-206 (1999).
53. Johansen L, Labischinski H, Burghaus P, Giesbrecht P. Acetylation in different phases of growth of staphylococci and their relation to cell wall degradability by lysozyme. In: The Target of Penicillin. Hakenbeck R, Holtje JV, Labischinski H (Eds). Walter de Gruyter, Berlin, Germany 261-266 (1983).
54. Bera A, Biswas R, Herbert S et al. Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J. Bacteriol. 189(1), 280-283 (2007).
55. Herbert S, Bera A, Nerz C et al. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3(7), e102 (2007).
56. Wecke J, Johannsen L, Giesbrecht P. Reduction of wall degradability of clindamycin-treated staphylococci within macrophages. Infect. Immun. 58(1), 197-204 (1990).
57. Reinicke B, Blumel P, Giesbrecht P. Reduced degradability by lysozyme of staphylococcal cell walls after chloramphenicol treatment. Arch. Microbiol. 135(2), 120-124 (1983).
58. Ganz T. Fatal attraction evaded. How pathogenic bacteria resist cationic polypeptides. J. Exp. Med. 193(9), F31-F34 (2001).
59. Xiong YQ, Yeaman MR, Bayer AS. In vitro antibacterial activities of platelet microbicidal protein and neutrophil defensin against Staphylococcus aureus are influenced by antibiotics differing in mechanism of action. Antimicrob. Agents Chemother. 43(5), 1111-1117 (1999).
60. Yeaman MR, Norman DC, Bayer AS. Platelet microbicidal protein enhances antibiotic-induced killing of and postantibiotic effect in Staphylococcus aureus. Antimicrob. Agents Chemother. 36(8), 1665-1670 (1992).
61. Sahl HG, Pag U, Bonness S, Wagner S, Antcheva N, Tossi A. Mammalian defensins: structures and mechanism of antibiotic activity. J. Leukoc. Biol. 77(4), 466-475 (2005).
62. Mani N, Tobin P, Jayaswal RK. Isolation and characterization of autolysis-defective mutants of Staphylococcus aureus created by Tn917-lacZ mutagenesis. J. Bacteriol. 175(5), 1493-1499 (1993).
63. During K, Porsch P, Mahn A, Brinkmann O, Gieffers W. The non-enzymatic microbicidal activity of lysozymes. FEBS Lett. 449(2-3), 93-100 (1999).
64. Ginsburg I. Role of leukocytes in infectious granulomatosis. In: Lysosomes in Applied Biology and Therapeutics. Dingle J, Jacques P, Shaw I (Eds). North Holland Publishing Company, Amsterdam, The Netherlands (1979).
65. Ginsburg I. Bacteriolysis is inhibited by hydrogen peroxide and by proteases. Agents Actions 28(3-4), 238-242 (1989).
66. Wecke J, Kwa E, Lahav M, Ginsburg I, Giesbrecht P. Suppression of penicillin-induced bacteriolysis of staphylococci by some anticoagulants. J. Antimicrob. Chemother. 20(1), 47-55 (1987).
67. Wecke J, Lahav M, Ginsburg I, Kwa E, Giesbrecht P. Inhibition of wall autolysis of staphylococci by sodium polyanethole sulfonate 'liquoid'. Arch. Microbiol. 144(2), 110-115 (1986).
68. Wecke J, Kersten T, Giesbrecht P. The modulation of the bacteriolytic effect of β-lactam antibiotics by non-antibiotics. APMIS 30(Suppl.), 32-39 (1992).
69. Rakita RM, Michel BR, Rosen H. Inactivation of Escherichia coli penicillin-binding proteins by human neutrophils. Infect. Immun. 62(1), 162-165 (1994).
70. Wilson LA, Spitznagel JK. Molecular and structural damage to Escherichia coli produced by antibody, complement, and lysozyme systems. J. Bacteriol. 96(4), 1339-1348 (1968).
71. Holzheimer RG. The significance of endotoxin release in experimental and clinical sepsis in surgical patients - evidence for antibiotic-induced endotoxin release? Infection 26(2), 77-84 (1998).
72. Periti P, Mazzei T. Antibiotic-induced release of bacterial cell wall components in the pathogenesis of sepsis and septic shock: a review. J. Chemother. 10(6), 427-448 (1998).
73. Shenep JL. Antibiotic-induced bacterial cell lysis: a therapeutic dilemma. Eur. J. Clin. Microbiol. 5(1), 11-12 (1986).
74. Shapiro DN, Varani J, Ginsburg I. Activation of a murine T-cell hybridoma by cationized bacteria. Immunology 67(4), 478-483 (1989).
75. Horn DL, Opal SM, Lomastro E. Andbiotics, cytokines, and endotoxin: a complex and evolving relationship in Gram-negative sepsis. Scand. J. Infect. Dis 101(Suppl.), 9-13 (1996).
76. Ginsburg I. Multi-drug strategies are necessary to inhibit the synergistic mechanism causing tissue damage and organ failure in post infectious sequelae. Inflammopharmacology 7(3), 207-217 (1999).
77. Marikovsky Y, Danon D, Katchalsky A. Agglutination by polylysine of young and old red blood cells. Biochim. Biophys. Acta. 124(1), 154-159 (1966).
78. Ginsburg I, Kohen R. Cell damage in inflammatory and infectious sites might involve a coordinated 'cross-talk' among oxidants, microbial haemolysins and ampiphiles, cationic proteins, phospholipases, fatty acids, proteinases and cytokines (an overview). Free Radic. Res. 22(6), 489-517 (1995).
79. Ginsburg I, Fligiel SE, Kunkel RG, Riser BL, Varani J. Phagocytosis of Candida albicans enhances malignant behavior of murine tumor cells. Science 238(4833), 1573-1575 (1987).
80. Brouwer CP, Wulferink M, Welling MM. The pharmacology of radiolabeled cationic antimicrobial peptides. J. Pharm. Sci. 97(5), 1633-1651 (2007).
81. Parisien A, Allain B, Zhang J, Mandeville R, Lan CQ. Novel alternatives to antibiotics: bacteriophages, bacterial cell wall hydrolases, and antimicrobial peptides. J. Appl. Microbiol. 104(1), 1-13 (2008).
82. Lichtenstein AK, Ganz T, Selsted ME, Lehrer RI. Synergistic cytolysis mediated by hydrogen peroxide combined with peptide defensins. Cell. Immunol. 114(1), 104-116 (1988).
83. Porro GA, Lee JH, de Azavedo J et al. Direct and indirect bacterial killing functions of neutrophil defensins in lung explants. Am. J. Physiol. Lung Cell Mol. Physiol. 281(5), L1240-L1247 (2001).
84. Nagaoka I, Hirota S, Yomogida S, Ohwada A, Hirata M. Synergistic actions of antibacterial neutrophil defensins and cathelicidins. Inflamm. Res. 49(2), 73-79 (2000).
85. Chen X, Niyonsaba F, Ushio H et al. Synergistic effect of antibacterial agents human β-defensins, cathelicidin LL-37 and lysozyme against Staphylacoccus aureus and Escherichia coli. J. Dermatol. Sci. 40(2), 123-132 (2005).
86. Bucki R, Namiot DB, Namiot Z, Savage PB, Janmey PA. Salivary mucins inhibit antibacterial activity of the cathelicidin-derived LL-37 peptide but not the cationic steroid CSA-13. J. Antimicrob. Chemother. DOI: 10.1093/jac/dkn176 (2008) (Epub ahead of print).
87. Dziarski P, Gupta D. Peptidoglycan recognition in innate immunity. J. Endotoxin Res. 11(5), 304-310 (2005).
88. Scott MG, Gold MR, Hancock RE. Interaction of cationic peptides with lipoteichoic acid and Gram-positive bacteria. Infect. Immun. 67(12), 6445-6453 (1999).
89. Dishon T, Finkel R, Marcus Z, Ginsburg I. Cell-sensitizing products of streptococci. Immunology 13(6), 555-564 (1967).
90. Zughaier SM, Shafer WM, Stephens DS. Antimicrobial peptides and endotoxin inhibit cytokine and nitric oxide release but amplify respiratory burst response in human and murine macrophages. Cell. Microbiol. 7(9), 1251-1262 (2005).
91. Barak V, Kalickman I, Halperin T, Birkenfeld S, Ginsburg I. PADMA-28, a Tibetan herbal preparation is an inhibitor of inflammatory cytokine production. Eur. Cytokine Netw. 15(3), 203-209 (2004).
92. Singh PK, Tack BF, McCray PB Jr, Welsh MJ. Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. Am. J. Physiol. Lung Cell. Mol. Physiol. 279(5), L799-L805 (2000).
93. Bucki R, Levental I, Janmey P. Antibacterial peptides - a bright future or a false hope. Anti-Infective Agents Med. Chem. 6(3), 175-184 (2007).
94. Peschel A, Sahl HG. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4(7), 529-536 (2006).
95. Schwab JH, Cromartie WJ, Ohanian SH, Craddock JG. Association of experimental chronic arthritis with the persistence of group A streptococcal cell walls in the articular tissue. J. Bacteriol. 94(5), 1728-1735 (1967).
96. Spanel R, Galle J, Heymer B, Haferkamp O, Schmidt WC. Induction of granulomatous hepatitis in mice infected with group A streptococci and treated with penicillin. Virchows Arch. A Pathol. Anat. Histol. 363(4), 323-332 (1974).
97. Ginsburg I, Gallis HA, Cole RM. Group A streptococci: localization in rabbits and guinea pigs following tissue injury. Science 166(909), 1161-1163 (1969).
98. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 124(4), 783-801 (2006).
99. Stewart-Tull DES. The immunological activities of bacterial peptidoglycans. Ann. Rev. Microbiol. 34, 311-340 (1980).
100. Oshimi K, Kano S, Takaku F, Okumura K. Augmentation of mouse natural killer cell activity by a streptococcal preparation, OK-432. J. Natl Cancer Inst. 65(6), 1265-1269 (1980).
101. Fujimoto T, Duda RB, Szilvasi A. Chen X, Mai M, O'Donnell MA. Streptococcal. preparation OK-432 is a potent inducer of IL-12 and a T helper cell 1 dominant state. J. Immunol. 158(12), 5619-5626 (1997).