Molecular mechanisms of bacterial resistance to antimicrobial peptides

Current Topics in Microbiology and Immunology

Volumn 306, Issue , 2006, Pages 231-250

  Kraus, D ^a   Peschel, A ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSE; AUREOLYSIN; BACTERIAL PROTEIN; BACTERIOCIN; CATHELICIDIN; DAPTOMYCIN; DEFENSIN; FATTY ACID; KINOCIDIN; LIPID A; MYCOLIC ACID; NISIN; PHOSPHOLIPID; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN EPIFEG; PROTEIN M1; PROTEIN MTRCDE; PROTEIN OMPT; PROTEIN PGTE; PROTEIN ROSA; PROTEIN ROSB; PROTEIN SIC; SERINE PROTEASE V8; STAPHYLOKINASE; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; CARRIER PROTEIN;

ANTIBIOTIC RESISTANCE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; CELL SURFACE; DRUG EFFICACY; ECOLOGY; EFFUSION; ELECTRICITY; ENERGY; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; GENE CONTROL; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; KLEBSIELLA PNEUMONIAE; MOLECULAR DYNAMICS; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA GONORRHOEAE; NONHUMAN; PORPHYROMONAS GINGIVALIS; PREVOTELLA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEUS MIRABILIS; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; REVIEW; SALMONELLA; SALMONELLA ENTERICA; SHIGELLA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS PYOGENES; YERSINIA; ANIMAL; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

BACTERIA (MICROORGANISMS);

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL INFECTIONS; CARRIER PROTEINS; DRUG RESISTANCE, BACTERIAL; ELECTROSTATICS; HUMANS;

EID: 33745194211     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/3-540-29916-5_9     Document Type: Review

References (97)

1. Abachin E, Poyart C, Pellegrini E, Milohanic E, Fiedler F, Berche P, Trieu-Cuot P (2002) Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol Microbiol 43:1-14
2. Andres E, Dimarcq JL (2004) Cationic antimicrobial peptides: update of clinical development. J Intern Med 255:519-520
3. Bader MW, Navarre WW, Shiau W, Nikaido H, Frye JG, McClelland M, Fang FC, Miller SI (2003) Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol Microbiol 50:219-230
4. Bader MW, Sanowar S, Daley ME, Schneider AR, Cho U, Xu W, Klevit RE, LeMoual H, Miller SI (2005) Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461-472
5. Bayer AS, Prasad R, Chandra J, Koul A, Smriti M, Varma A, Skurray RA, Firth N, Brown MH, Koo S-P, Yeaman MR (2000) In vitro resistance of Staphylococcus aureus to thrombin-induced platelet microbicidal proteins is associated with alterations in cytoplasmic membrane fluidity. Infect Immun 68:3548-3553
6. Bengoechea JA, Skurnik M (2000) Temperature-regulated efflux pump/potassium antiporter system mediates resistance to cationic antimicrobial peptides in Yersinia. Mol Microbiol 37:67-80
7. Bisno AL, Brito MO, Collins CM (2003) Molecular basis of group A streptococcal virulence. Lancet Infect Dis 3:191-200
8. Brissette CA, Simonson LG, Lukehart SA (2004) Resistance to human beta-defensins is common among oral treponemes. Oral Microbiol Immunol 19:403-407
9. Campos MA, Vargas MA, Regueiro V, Llompart CM, Alberti S, Bengoechea JA (2004) Capsule polysaccharide mediates bacterial resistance to antimicrobial peptides. Infect Immun 72:7107-7114
10. Cao M, Helmann JD (2004) The Bacillus subtilis extracytoplasmic-function sigmaX factor regulates modification of the cell envelope and resistance to cationic antimicrobial peptides. J Bacteriol 186:1136-1146
11. Collins LV, Kristian SA, Weidenmaier C, Faigle M, Van Kessel KP, Van Strijp JA, Gotz F, Neumeister B, Peschel A (2002) 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
12. Cotter PD, Guinane CM, Hill C (2002) The LisRK signal transduction system determines the sensitivity of Listeria monocytogenes to nisin and cephalosporins. Antimicrob Agents Chemother 46:2784-2790
13. Devaux PF, Morris R (2004) Transmembrane asymmetry and lateral domains in biological membranes. Traffic 5:241-246
14. Dorschner RA, Lopez-Garcia B, Peschel A, Kraus D, Morikawa K, Nizet V, Gallo RL (2006) The mammalian ionic environment dictates microbial susceptibility to antimicrobial defense peptides. FASEB J 20:35-42
15. Dunman PM, Murphy E, Haney S, Palacios D, Tucker-Kellogg G, Wu S, Brown EL, Zagursky RJ, Shlaes D, Projan SJ (2001) Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 183:7341-7353
16. Dürr M, Peschel A (2002) Chemokines meet defensins - the merging concepts of chemoattractants and antimicrobial peptides in host defense. Infect Immun 70:6515-6517
17. Edelstein PH, Hu B, Higa F, Edelstein MA (2003) lvgA, a novel Legionella pneumophila virulence factor. Infect Immun 71:2394-2403
18. Ernst RK, Yi EC, Guo L, Lim KB, Burns JL, Hackett M, Miller SI (1999) Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286:1561-1565
19. Ernst RK, Guina T, Miller SI (2001) Salmonella typhimurium outer membrane remodeling: role in resistance to host innate immunity. Microbes Infect 3:1327-1334
20. Frick IM, Akesson P, Rasmussen M, Schmidtchen A, Bjorck L (2003) SIC, a secreted protein of Streptococcus pyogenes that inactivates antibacterial peptides. J Biol Chem 278:16561-16566
21. Ganz T (2003) Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3:710-720
22. Gao LY, Laval F, Lawson EH, Groger RK, Woodruff A, Morisaki JH, Cox JS, Daffe M, Brown EJ (2003) Requirement for kasB in Mycobacterium mycolic acid biosynthesis, cell wall impermeability and intracellular survival: implications for therapy. Mol Microbiol 49:1547-1563
23. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84:165-174
24. Groisman EA (1994) How bacteria resist killing by host defense peptides. Trends Microbiol Sci 2:444-448
25. Groisman EA (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183:1835-1842
26. Gross M, Cramton S, Goetz F, Peschel A (2001) Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect Immun 69:3423-3426
27. Guder A, Wiedemann I, Sahl HG (2000) Posttranslationally modified bacteriocins - the lantibiotics. Biopolymers 55:62-73
28. Guina T, Yi EC, Wang H, Hackett M, Miller SI (2000) A PhoP-regulated outer membrane protease of Salmonella enterica serovar typhimurium promotes resistance to alpha-helical antimicrobial peptides. J Bacteriol 182:4077-4086
29. Gunn JS, Lim KB, Krueger J, Kim K, Guo L, Hackett M, Miller SI (1998) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27:1171-1182
30. Gunn JS, Ryan SS, Van Velkinburgh JC, Ernst RK, Miller SI (2000) 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
31. Guo L, Lim KB, Poduje CM, Daniel M, Gunn JS, Hackett M, Miller SI (1998) Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95:189-198
32. Gustafson J, Strassle A, Hachler H, Kayser FH, Berger-Bachi B (1994) The femC locus of Staphylococcus aureus required for methicillin resistance includes the glutamine synthetase operon. J Bacteriol 176:1460-1467
33. Hancock RE, Chapple DS (1999) Peptide antibiotics. Antimicrob Agents Chemother 43:1317-1323
34. Hornef MW, Putsep K, Karlsson J, Refai E, Andersson M (2004) Increased diversity of intestinal antimicrobial peptides by covalent dimer formation. Nat Immunol 5:836-843
35. Huijbregts RP, de Kroon AI, de Kruijff B (2000) Topology and transport of membrane lipids in bacteria. Biochim Biophys Acta 1469:43-61
36. Islam D, Bandholtz L, Nilsson J, Wigzell H, Christensson B, Agerberth B, Gudmundsson G (2001) Downregulation of bactericidal peptides in enteric infections: a novel immune escape mechanism with bacterial DNA as a potential regulator. Nat Med 7:180-185
37. Jack RW, Bierbaum G, Sahl H-G (1998) Lantibiotics and related peptides. Springer, Berlin Heidelberg New York
38. Jerse AE, Sharma ND, Simms AN, Crow ET, Snyder LA, Shafer WM (2003) A gonococcal efflux pump system enhances bacterial survival ina female mouse model of genital tract infection. Infect Immun 71:5576-5582
39. Jin T, Bokarewa M, Foster T, Mitchell J, Higgins J, Tarkowski A (2004) Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J Immunol 172:1169-1176
40. Joly S, Maze C, McCray PB Jr, Guthmiller JM (2004) Human beta-defensins 2 and 3 demonstrate strain-selective activity against oral microorganisms. J Clin Microbiol 42:1024-1029
41. Katzif S, Danavall D, Bowers S, Balthazar JT, Shafer WM (2003) The major cold shock gene, cspA, is involved in the susceptibility of Staphylococcus aureus to an antimicrobial peptide of human cathepsin G. Infect Immun 71:4304-4312
42. Koprivnjak T, Peschel A, Gelb MH, Liang NS, Weiss JP (2002) 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
43. Kristian SA, Durr M, Van Strijp JA, Neumeister B, Peschel A (2003a) MprF-mediated lysinylation of phospholipids in Staphylococcus aureus leads to protection against oxygen-independent neutrophil killing. Infect Immun 71:546-549
44. Kristian SA, Lauth X, Nizet V, Goetz F, Neumeister B, Peschel A, Landmann R (2003b) 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
45. Kristian S, Datta V, Weidenmaier C, Kansal R, Fedtke I, Peschel A, Gallo R, Nizet V (2005) D-alanylation of teichoic acids promotes group A streptococcus antimirobial peptide resistance, neutrophil survival, and epithelial cell invasion. J Bacteriol 187:6719-6725
46. Kupferwasser LI, Skurray RA, Brown MH, Firth N, Yeaman MR, Bayer AS (1999) Plasmid-mediated resistance to thrombin-induced platelet microbicidal protein in staphylococci: role of the qacA locus. Antimicrob Agents Chemother 43:2395-2399
47. Lay FT, Anderson MA (2005) Defensins - components of the innate immune system in plants. Curr Protein Pept Sci 6:85-101
48. Lehrer RI (2004) Primate defensins. Nat Rev Microbiol 2:727-738
49. Leippe M, Herbst R (2004) Ancient weapons for attack and defense: the pore-forming polypeptides of pathogenic enteric and free-livingamoeboid protozoa. J Eukaryot Microbiol 51:516-521
50. Maxwell AI, Morrison GM, Dorin JR (2003) Rapid sequence divergence in mammalian beta-defensins by adaptive evolution. Mol Immunol 40:413-421
51. McPhee JB, Lewenza S, Hancock RE (2003) Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50:205-217
52. Midorikawa K, Ouhara K, Komatsuzawa H, Kawai T, Yamada S, Fujiwara T, Yamazaki K, Sayama K, Taubman MA, Kurihara H, Hashimoto K, Sugai M (2003) Staphylococcus aureus susceptibility to innate antimicrobial peptides, beta-defensins and CAP18, expressed by human keratinocytes. Infect Immun 71:3730-3739
53. Miller SI, Ernst RK, Bader MW (2005) LPS, TLR4 and infectious disease diversity. Nat Rev Microbiol 3:36-46
54. Neuhaus FC, Baddiley J (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67:686-723
55. Nguyen TX, Cole AM, Lehrer RI (2003) Evolution of primate theta-defensins: a serpentine path to a sweet tooth. Peptides 24:1647-1654
56. Nishimura E, Eto A, Kato M, Hashizume S, Imai S, Nisizawa T, Hanada N (2004) Oral streptococci exhibit diverse susceptibility to human beta-defensin-2: antimicrobial effects of hBD-2 on oral streptococci. Curr Microbiol 48:85-87
57. Nizet V (2005) Antimicrobial peptide resistance in human bacterial pathogens. In: Gallo RL (ed) Antimicrobial peptides in human health and disease. Horizon Bioscience, Norfolk, UK, pp 277-304
58. Nizet V, Gallo RL (2003) Cathelicidins and innate defense against invasive bacterial infection. Scand J Infect Dis 35:670-676
59. Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, Dorschner RA, Pestonjamasp V, Piraino J, Huttner K, Gallo RL (2001) Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414:454-457
60. Nummila K, Kilpeläinen I, Zähringer U, Vaara M, Helander IM (1995) Lipopolysaccharides of polymyxin B-resistant mutants of Escherichia coli are extensively substituted by 2-aminoethyl pyrophosphate and contain aminoarabinose in lipid A. Mol Microbiol 16:271-278
61. Oku Y, Kurokawa K, Ichihashi N, Sekimizu K (2004) Characterization of the Staphylococcus aureus mprF gene, involved in lysinylation of phosphatidylglycerol. Microbiology 150:45-51
62. Otto M (2005) Bacterial evasion of antimicrobial peptides by biofilm formation. In: Shafer WM (ed) Antimicrobial peptides and human disease. Curr Top Microbiol Immunol (in press)
63. Pag U, Sahl HG (2002) Multiple activities in lantibiotics - models for the design of novel antibiotics? Curr Pharm Des 8:815-833
64. Patil A, Hughes AL, Zhang G (2004) Rapid evolution and diversification of mammalian alpha-defensins as revealed by comparative analysis of rodent and primate genes. Physiol Genomics 20:1-11
65. Peacock SJ, de Silva I, Lowy FD (2001) What determines nasal carriage of Staphylococcus aureus? Trends Microbiol 9:605-610
66. Perego M, Glaser P, Minutello A, Strauch MA, Leopold K, Fischer W (1995) Incorporation of D-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. J Biol Chem 270:15598-15606
67. Peschel A (2002) How do bacteria resist human antimicrobial peptides? Trends Microbiol 10:179-186
68. Peschel A, Götz F (1996) Analysis of the Staphylococcus epidermidis genes epiF, E, and G involved in epidermin immunity. J Bacteriol 178:531-536
69. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Götz F (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins and other antimicrobial peptides. J Biol Chem 274:8405-8410
70. Peschel A, Vuong C, Otto M, Götz F (2000) The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolysins. Antimicrob Agents Chemother 44:2845-2847
71. Peschel A, Jack RW, Otto M, Collins LV, Staubitz P, Nicholson G, Kalbacher H, Nieuwenhuizen WF, Jung G, Tarkowski A, van Kessel KPM, van Strijp JAG (2001) 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
72. Poyart C, Pellegrini E, Marceau M, Baptista M, Jaubert F, Lamy MC, Trieu-Cuot P (2003) 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
73. Proctor RA, Kahl B, von Eiff C, Vaudaux PE, Lew DP, Peters G (1998) Staphylococcal small colony variants have novel mechanisms for antibiotic resistance. Clin Infect Dis 27 [Suppl 1]:68-74
74. Ratledge C, Wilkinson SG (1988) Microbial lipids. Academic Press, London
75. Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56:117-137
76. Sahl HG, Pag U, Bonness S, Wagner S, Antcheva N, Tossi A (2004) Mammalian defensins: structures and mechanism of antibiotic activity. J Leukoc Biol 77:466-475
77. Sahly H, Schubert S, Harder J, Rautenberg P, Ullmann U, Schroder J, Podschun R (2003) Burkholderia is highly resistant to human Beta-defensin 3. Antimicrob Agents Chemother 47:1739-1741
78. Schmidtchen A, Frick IM, Andersson E, Tapper H, Bjorck L (2002) Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol Microbiol 46:157-168
79. Shafer WM, Qu X-D, Waring AJ, Lehrer RI (1998) 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 U S A 95:1829-1833
80. Shelburne CE, Coulter WA, Olguin D, Lantz MS, Lopatin DE (2005) Induction of β-defensin resistance in the oral anaerobe Porphyromonas gingivalis. Antimicrob Agents Chemother 49:183-187
81. Sieprawska-Lupa M, Mydel P, Krawczyk K, Wojcik K, Puklo M, Lupa B, Suder P, Silberring J, Reed M, Pohl J, Shafer W, McAleese F, Foster T, Travis J, Potempa J (2004) Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob Agents Chemother 48:4673-4679
82. Staubitz P, Peschel A (2002) MprF-mediated lysinylation of phospholipids in Bacillus subtilis - protection against bacteriocins in terrestrial environments? Microbiology 148:3331-3332
83. Staubitz P, Neumann H, Schneider T, Wiedemann I, Peschel A (2004) MprF-mediated biosynthesis of lysylphosphatidylglycerol, an important determinant in staphylococcal defensin resistance. FEMS Microbiol Lett 231:67-71
84. Steenbergen JN, Alder J, Thorne GM, Tally FP (2005) Daptomycin: a lipopeptide antibiotic for the treatment of serious Gram-positive infections. J Antimicrob Chemother 53:283-288
85. Stumpe S, Schmid R, Stephens DL, Georgiou G, Bakker EP (1998) Identification of OmpT as the protease that hydrolyzes the antimicrobial peptide protamine before it enters growing cells of Escherichia coli. J Bacteriol 180:4002-4006
86. Van Veen HW, Konings WN (1997) Drug efflux proteins in multidrug resistant bacteria. Biol Chem 378:769-777
87. Von Eiff C, Becker K, Machka K, Stammer H, Peters G (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study group. N Eng J Med 344:11-16
88. Vuong C, Voyich JM, Fischer ER, Braughton KR, Whitney AR, DeLeo FR, Otto M (2004) Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 6:269-275
89. Wecke J, Madela K, Fischer W (1997) The absence of D-alanine from lipoteichoic acid and wall teichoic acid alters surface charge, enhances autolysis and increases susceptibility to methicillin in Bacillus subtilis. Microbiology 143:2953-2960
90. Weidenmaier C, Kristian SA, Peschel A (2003) Bacterial resistance to antimicrobial host defenses - an emerging target for novel antiinfective strategies? Curr Drug Targets 4:643-649
91. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturyia T, Kalbacher H, Gross M, Nicholson G, Neumeister B, Mond JJ, Peschel A (2004) Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10:243-245
92. Weidenmaier C, Peschel A, Kempf VA, Lucindo N, Yeaman MR, Bayer AS (2005) DltABCD- 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
93. Wertheim HF, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JA, van Keulen PH, Vandenbroucke-Grauls CM, Meester MH, Verbrugh HA (2004) Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364:703-705
94. Wosten MM, Kox LF, Chamnongpol S, Soncini FC, Groisman EA (2000) A signal transduction system that responds to extracellular iron. Cell 103:113-125
95. Yang D, Chen Q, Hoover DM, Staley P, Tucker KD, Lubkowski J, Oppenheim JJ (2003) Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J Leukoc Biol 74:448-455
96. Yeaman MR, Bayer AS, Koo S-P, Foss W, Sullam PM (1998) Platelet microbicidal proteins and neutrophil defensin disrupt the Staphylococcus aureus cytoplasmic membrane by distinct mechanisms of action. J Clin Invest 101:178-187
97. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389-395