The co-evolution of host cationic antimicrobial peptides and microbial resistance

Nature Reviews Microbiology

Volumn 4, Issue 7, 2006, Pages 529-536

  Peschel, Andreas ^a   Sahl, Hans Georg ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DEFENSIN; ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; BACTERIAL PROTEIN; BETA DEFENSIN; BETA DEFENSIN 1; BETA DEFENSIN 2; BETA DEFENSIN 3; BETA LACTAM ANTIBIOTIC; CECROPIN; CRYPTDIN RELATED SEQUENCE PEPTIDE; ELAFIN; HEPCIDIN; KINOCIDIN DERIVATIVE; LANTIBIOTIC; LECTIN; LIPID A; MAGAININ DERIVATIVE; NISIN; ORITAVANCIN; OXACILLIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEGRIN; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; STAPHYLOKINASE; TACHYPLESIN; TEICHOIC ACID; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANCOMYCIN;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIVIRAL ACTIVITY; BACTERIAL GENOME; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BINDING AFFINITY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; ENDOCARDITIS; FIBRINOLYSIS; GENETIC CODE; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; MICROBIAL DIVERSITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN VARIANT; REVIEW; STRUCTURE ANALYSIS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; DRUG RESISTANCE, BACTERIAL; EVOLUTION; HUMANS;

EID: 33745217570     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1441     Document Type: Review

References (96)

1. Woolhouse, M. E., Webster, J. P., Domingo, E., Charlesworth, B. & Levin, B. R. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genet. 32, 569-577 (2002).
2. Grenfell, B. T. et al. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303, 327-332 (2004).
3. Brubaker, R. R. The recent emergence of plague: A process of felonious evolution. Microb. Ecol. 47, 293-299 (2004).
4. Waldvogel, F. A Infectious diseases in the 21st century: Old challenges and new opportunities. Int. J. Infect. Dis. 8, 5-12 (2004).
5. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 415, 389-395 (2002).
6. Hancock, R. E. W. & Diamond, G. The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol. 8, 402-410 (2000).
7. Ganz, T. Defensins: Antimicrobial peptides of innate immunity. Nature Rev. Immunol. 3, 710-720 (2003).
8. Lehrer, R. I. Primate defensins. Nature Rev. Microbiol. 2, 727-738 (2004).
9. Brogden, K. A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nature Rev. Microbiol. 3, 238-250 (2005).
10. Selsted, M. E. & Ouellette, A. J. Mammalian defensins in the antimicrobial immune response. Nature Immunol. 6, 551-557 (2005).
11. Dorschner, R. A. et al. The mammalian ionic environment dictates microbial susceptibility to antimicrobial defense peptides: FASEB J. 20, 35-42 (2006).
12. Sahl, H. G. et al. Mammalian defensins: Structures and mechanism of antibiotic activity. J. Leukoc. Biol. 77, 466-475 (2005).
13. Yang, D., Biragyn, A., Kwak, L. W. & Oppenheim, J. J. Mammalian defensins in immunity: More than just microbicidal. Trends Immunal. 23, 291-296 (2002).
14. Bals, R. & Wilson, J. M. Cathelicidins - a family of multifunctional antimicrobial peptides Cell. Mol. Life Sci. 60, 711-720 (2003).
15. Bowdish, D. M. et al. Impact of LL-37 on anti-infective immunity. J. Leukoc. Biol. 77, 451-459 (2005).
16. Dürr, M. & Peschel, A Chemokines meet defensins - the merging concepts of chemoattractants and antimicrobial peptides in host defense. Infect. Immun. 70, 6515-6517 (2002).
17. Rosenfeld, Y., Papo, N. & Shai, Y. Endotoxin (LPS) neutralization by innate immunity host-defense peptides: Peptides' properties and plausible modes of action. J. Biol. Chem. 281, 1636-1643 (2006).
18. Vallender, E. J. & Lahn, B. T. Positive selection on the human genome. Hum. Mol. Genet. 13, R245-R254 (2004).
19. Patil, A, Hughes, A. L. & Zhang, G. Rapid evolution and diversification of mammalian α-defensins as revealed by comparative analysis of rodent and primate genes. Physiol. Genomics 20, 1-11 (2004).
20. Nusbaum, C. et al. DNA sequence and analysis of human chromosome 8. Nature 439, 331-335 (2006).
21. Crovella, S. et al. Primate β-defensins - structure, function and evolution. Curr. Protein Pept. Sci. 6, 7-21 (2005).
22. Nizet, V. in Antimicrobial Peptides in Human Health and Disease (ed. Gallo, R. L.) 277-304 (Horizon Bioscience, Norfolk, 2005).
23. Peschel, A. How do bacteria resist human antimicrobial peptides? Trends Microbiol. 10, 179-186 (2002).
24. Kraus, D. & Peschel, A. Molecular mechanisms of bacterial resistance to antimicrobial peptides. Curr. Top. Microbiol. Immunol. 306, 231-250 (2006).
25. Kristian, S. A. et al. Alanylation of teichoic acids protects Staphylococcus aureus against Toll-like receptor 2-dependent host defense in a mouse tissue cage infection model. J. Infect. Dis. 188, 414-423 (2003).
26. Nizet, V. et al. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414, 454-457 (2001).
27. Gunn, J. S., Ryan, S. S., Van Velkinburgh, J. C., Ernst, R. K. & Miller, S. I. Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 68, 6139-6146 (2000).
28. Weidenmaier, C. et al. DItABCD- and MprF-mediated cell envelope modifications of Staphylococcus aureus confer resistance to platelet microbicidal proteins and contribute to virulence in a rabbit endocarditis model. Infect. Immun. 73, 8033-8038 (2005).
29. Kramer, N. E., yan Hijum, S. A. F. T., Knol, J., Kok, J. & Kuipers, O. Transcriptome analysis reveals mechanisms by which Lactococcus lactis acquires nisin resistance. Antimicrob. Agents Chemother. 50, 1753-1761 (2006).
30. Perron, G. G., Zasloff, M. & Bell, G. Experimental evolution of resistance to an antimicrobial peptide. Proc. Biol. Sci. 273, 251-256 (2006).
31. Levy, S. B. & Marshall, B. Antibacterial resistance worldwide: Causes; challenges and responses. Nature Med. 10, S122-S129 (2004).
32. Chambers, H. F. Community-associated MRSA-resistance and virulence converge. N. Engl. J. Med. 352, 1485-1487 (2005).
33. Foster, T. J. The Staphylococcus aureus 'superbug'. J. Clin. Invest. 114, 1693-1696 (2004).
34. Andres, E. & Dimarcq, J. L. Cationic antimicrobial peptides: Update of clinical development. J. Intern. Med. 255, 519-520 (2004).
35. Mygind, P. H. et al. Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 437, 975-980 (2005).
36. Sieprawska-Lupa, M. et al. Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob. Agents Chemother. 48, 4673-4679 (2004).
37. Guina, T., Yi, E. C., Wang, H., Hackett, M. & Miller, S. I. A PhoP-regulated outer membrane protease of Salmonella enterica serovar Typhimurium promotes resistance to α-helical antimicrobial peptides. J. Bacteriol. 182, 4077-4086 (2000).
38. Nyberg, P., Rasmussen, M. & Bjorck, L. α2-Macroglobulin-proteinase complexes protect Streptococcus pyogenes from killing by the antimicrobial peptide LL-37. J. Biol. Chem. 279, 52820-52823 (2004).
39. Schmidtchen, A., Frick, I. M., Andersson, E., Tapper, H. & Bjorck, L. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol. 46, 157-168 (2002).
40. Wu, Z. et al. Engineering disulfide bridges to dissect antimicrobial and chemotactic activities of human β-defensin 3. Proc. Natl Acad. Sci. USA 100, 8880-8885 (2003).
41. Maemoto, A. et al. Functional analysis of the α-defensin disulfide array in mouse cryptdin-4. J. Biol. Chem. 279, 44188-44196 (2004).
42. Campopiano, D. J. et al. Structure-activity relationships in defensin dinners: A novel link between β-defensin tertiary structure and antimicrobial activity. J. Biol. Chem. 279, 48671-48679 (2004).
43. Rozek, A., Powers, J. P., Friedrich, C. L. & Hancock, R. E. Structure-based design of an indolicidin peptide analogue with increased protease stability. Biochemistry 42, 14130-14138 (2003).
44. Harwig, S. S. et al. Intramolecular disulfide bonds enhance the antimicrobial and Wic activities of protegrins at physiological sodium chloride concentrations. Eur. J. Biochem. 240, 352-357 (1996).
45. Hornef, M. W., Putsep, K., Karlsson, J., Refai, E. & Andersson, M. Increased diversity of intestinal antimicrobial peptides by covalent dinner formation. Nature Immunol. 5, 836-843 (2004).
46. Tang, Y. Q. et al. A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated α-defensins. Science 286, 498-502 (1999).
47. Jack, R. W., Bierbaum, G. & Sahl, H.-G. Lantibiotics and Related Peptides (Springer, Berlin, 1998).
48. Cotter, P. D., Hill, C. & Ross, R. P. Bacteriocins: Developing innate immunity for food. Nature Rev. Microbiol. 3, 777-788 (2005).
49. Tjabringa, G. S. et al. Host defense effector molecules in mucosal secretions. FEMS Immunol. Med. Microbiol. 45, 151-158 (2005).
50. Jin, T. et al. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J. Immunol. 172, 1169-1176 (2004).
51. Frick, I. M., Akesson, P., Rasmussen, M., Schmidtchen, A. & Bjorck, L. SIC, a secreted protein of Streptococcus pyogenes that inactivates antibacterial peptides. J. Biol. Chem. 278, 16561-16566 (2003).
52. Shafer, W. M., Qu, X.-D., Waring, A. J. & Lehrer, R. I. Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. Proc. Natl Acad. Sci. USA 95, 1829-1833 (1998).
53. Tzeng, Y. L. et al. Cationic antimicrobial peptide resistance in Neisseria meningitidis. J. Bacteriol. 187, 5387-5396 (2005).
54. Fernie-King, B. A., Seilly D. J. & Lachmann, P. J. The interaction of streptococcal inhibitor of complement (SIC) and its proteolytic fragments with the human β-defensins. Immunology 111, 444-452 (2004).
55. Douglas, S. E., Gallant, J. W., Liebscher, R. S., Dacanay, A. & Tsoi, S. C. Identification and expression analysis of hepcidin-like antimicrobial peptides in bony fish. Dev. Comp. Immunol. 27, 589-601 (2003).
56. Park, C. H., Valore, E. V., Waring, A. J. & Ganz, T. Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J. Biol Chem. 276, 7806-7810 (2001).
57. Ouellette, A. J. & Selsted, M. E. Paneth cell defensins: Endogenous peptide components of intestinal host defense. FASEB J. 10, 1280-1289 (1996).
58. Eckmann, L. Defence molecules in intestinal innate immunity against bacterial infections. Curr. Opin. Gastroenterol. 21, 147-151 (2005).
59. Taudien, S. et al. Polymorphic segmental duplications at 8p23.1 challenge the determination of individual defensin gene repertoires and the assembly of a contiguous human reference sequence. BMC Genomics 5, 92 (2004).
60. Ernst, R. K., Guina, T. & Miller, S. I. Salmonella typhimurium outer membrane remodeling: Role in resistance to host innate immunity. Microbes Infect. 3, 1327-1334 (2001).
61. Neuhaus, F. C. & Baddiley, J. A continuum of anionic charge: Structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67, 686-723 (2003).
62. Peschel, A. et al. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins and other antimicrobial peptides. J. Biol. Chem. 274, 8405-8410 (1999).
63. Abachin, E. et al. Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43, 1-14 (2002).
64. Poyart, C. et al. Attenuated virulence of Streptococcus agalactiae deficient in D-alanyl-lipoteichoic acid is due to an increased susceptibility to defensins and phagocytic cells. Mol. Microbiol. 49, 1615-1625 (2003).
65. Kristian, S. A. et al. D-alanylation of teichoic acid promotes group A Streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. J. Bacteriol. 187, 6719-6725 (2005).
66. Peschel, A. et al. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with L-lysine. J. Exp. Med. 193, 1067-1076 (2001).
67. Weidenmaier, C., Kristian, S. A. & Peschel, A. Bacterial resistance to antimicrobial host defenses - an emerging target for novel antiinfective strategies? Curr. Drug Targets 4, 643-649 (2003).
68. Miller, S. I., Ernst, R. K. & Bader, M. W. UPS, TLR4 and infectious disease diversity. Nature Rev. Microbiol. 3, 36-46 (2005).
69. Koprivnjak, T., Peschel, A., Gelb, M. H., Liang, N. S. & Weiss, J. P. Role of charge properties of bacterial envelope in bactericidal action of human Group IIA phospholipase A2 against Staphylococcus aureus. J. Biol. Chem. 277, 47636-47644 (2002).
70. Collins, L. V. et al. Staphylococcus aureus strains lacking D-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice J. Infect. Dis. 186, 214-219 (2002).
71. Midorikawa, K. et al. Staphylococcus aureus susceptibility to innate antimicrobial peptides, β-defensins and CAP 18, expressed by human keratinocytes Infect. Immun. 71, 3730-3739 (2003).
72. Weidenmaier, C. et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nature Med. 10, 243-245 (2004).
73. Harder, J., Bartels, J., Christophers, E. & Schroder, J. M. Isolation and characterization of human β-defensin-3, a novel human inducible peptide antibiotic. J. Biol. Chem. 276, 5707-5713 (2001).
74. Shafer, W. M., Casey, S. G. & Spitznagel, J. K. Lipid A and resistance of Salmonella typhimurium to antimicrobial granule proteins of human neutrophil granulocytes. Infect. Immun. 43, 834-838 (1984).
75. Guo, L. et al. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95, 189-198 (1998).
76. Vuong, C. et al. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell. Microbiol. 6, 269-275 (2004).
77. Otto, M. Bacterial evasion of antimicrobial peptides by biofilm formation. Curr. Top. Microbiol. Immunol. 306, 251-258 (2006).
78. Ginsburg, I. The role of bacteriolysis in the pathophysiology of inflammation, infection and post-infectious sequelae. APMIS 110, 753-770 (2002).
79. Breukink, E. et al. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286, 2361-2364 (1999).
80. Wiedemann, I. et al. Specific binding of nisin to the peptidoglycan precursor lipid II combines pore formation and inhibition of cell wall biosynthesis for potent antibiotic activity. J. Biol. Chem. 276, 1772-1779 (2001).
81. Bierbaum, G. & Sahl, H. G. Induction of autolysis of staphylococci by the basic peptide antibiotic peps and nisin and their influence on the activity of autolytic enzymes. Arch. Microbiol. 141, 249-254 (1985).
82. Pag, U. & Sahl, H. G. Multiple activities in lantibiotics - models for the design of novel antibiotics? Curr. Pharm. Des. 8, 815-833 (2002).
83. Gravesen, A., Jydegaard Axelsen, A. M., Mendes, d. S., Hansen, T. B. & Knochel, S. Frequency of bacteriocin resistance development and associated fitness costs in Listeria monocytogenes. Appl. Environ. Microbiol. 68, 756-764 (2002).
84. Ganz, T. Hepcidin in iron metabolism. Curr. Opin. Hematol. 11, 251-254 (2004).
85. Nguyen, T. X., Cole, A. M. & Lehrer, R. I. Evolution of primate 0-defensins: A serpentine path to a sweet tooth. Peptides 24, 1647-1654 (2003).
86. Fowler, V. G. Jr et al. Persistent bacteremia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombin-induced platelet microbicidai protein. J. Infect. Dis. 190, 1140-1149 (2004).
87. Fowler, V. G. Jr et al. In vitro resistance to thrombin-induced platelet microbicidal protein in isolates of Staphylococcus aureus from endocarditis patients correlates with an intravascular device source. J. Infect Dis. 182, 1251-1254 (2000).
88. Frantz, S. Drug discovery: Playing dirty. Nature 437, 942-943 (2005).
89. Arthur, M., Reynolds, P. & Courvalin, P. Glycopeptide resistance in enterococci. Trends Microbiol. 4, 401-407 (1996).
90. Allen, N. E. & Nicas, T. I. Mechanism of action of oritavancin and related glycopeptide antibiotics. FEMS Microbiol. Rev. 26, 511-532 (2003).
91. Zhang, H. Z., Hackbarth, C. J., Chansky, K. M. Chambers, H. F. A proteolytic transmembrane signaling pathway and resistance to β-lactams in staphylococci. Science 291, 1962-1965 (2001).
92. Bader, M. W. et al. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122, 461-472 (2005).
93. Jacoby, G. A. & Munoz-Price, L. S. The new β-lactamases N. Engl. J. Med. 352, 380-391 (2005).
94. Hiramatsu, K. Vancomycin-resistant Staphylococcus aureus: A new model of antibiotic resistance. Lancet Infect. Dis. 1, 147-155 (2001).
95. van Veen, H. W. & Konings, W. N. Drug efflux proteins in multidrug resistant bacteria. Biol. Chem. 378, 769-777 (1997).
96. Fux, C. A., Costerton, J. W., Stewart, P. S. & Stoodley, P. Survival strategies of infectious biofilms. Trends Microbiol. 13, 34-40 (2005).