D-Alanylation of Lipoteichoic Acids Confers Resistance to Cationic Peptides in Group B Streptococcus by Increasing the Cell Wall Density

PLoS Pathogens

Volumn 8, Issue 9, 2012, Pages

  Saar Dover, Ron ^a   Bitler, Arkadi ^a   Nezer, Ravit ^a   Shmuel Galia, Liraz ^a   Firon, Arnaud ^b   Shimoni, Eyal ^a   Trieu Cuot, Patrick ^b   Shai, Yechiel ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; DEXTRO ALANINE; LIPOTEICHOIC ACID;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL DENSITY; CELL MEMBRANE PERMEABILITY; CELL SURFACE; CHEMICAL MODIFICATION; CONFORMATION; HOST PATHOGEN INTERACTION; NONHUMAN; PROTEIN BINDING; PROTEIN INTERACTION; STATIC ELECTRICITY; STREPTOCOCCUS AGALACTIAE; TRANSMISSION ELECTRON MICROSCOPY; WILD TYPE;

ALANINE; AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL WALL; DRUG RESISTANCE, MICROBIAL; HUMANS; LIPOPOLYSACCHARIDES; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; OSMOLAR CONCENTRATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS; SURFACE PROPERTIES; TEICHOIC ACIDS;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOCOCCUS SP. 'GROUP B';

EID: 84866951984     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002891     Document Type: Article

References (50)

1. Hancock RE, Scott MG, (2000) The role of antimicrobial peptides in animal defenses. Proc Natl Acad Sci U S A 97: 8856-8861.
2. Zasloff M, (2002) Antimicrobial peptides of multicellular organisms. Nature 415: 389-395.
3. Shai Y, (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66: 236-248.
4. Hancock RE, Sahl HG, (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24: 1551-1557.
5. Cheung J, Hendrickson WA, (2010) Sensor domains of two-component regulatory systems. Curr Opin Microbiol 13: 116-123.
6. Otto M, (2009) Bacterial sensing of antimicrobial peptides. Contrib Microbiol 16: 136-149.
7. Peschel A, (2002) How do bacteria resist human antimicrobial peptides? Trends Microbiol 10: 179-186.
8. Herbert S, Bera A, Nerz C, Kraus D, Peschel A, et al. (2007) Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog 3: e102.
9. 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.
10. Weidenmaier C, Peschel A, (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6: 276-287.
11. Rosenfeld Y, Papo N, Shai Y, (2006) Endotoxin (Lipopolysaccharide) neutralization by innate immunity host-defense peptides: peptide properties and plausible modes of action. J Biol Chem 281: 1636-1643.
12. Brogden KA, (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3: 238-250.
13. Senyurek I, Paulmann M, Sinnberg T, Kalbacher H, Deeg M, et al. (2009) Dermcidin-derived peptides show a different mode of action than the cathelicidin LL-37 against Staphylococcus aureus. Antimicrob Agents Chemother 53: 2499-2509.
14. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, et al. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274: 8405-8410.
15. Kristian SA, Datta V, Weidenmaier C, Kansal R, Fedtke I, et al. (2005) D-alanylation of teichoic acids promotes group a streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. J Bacteriol 187: 6719-6725.
16. Kovacs M, Halfmann A, Fedtke I, Heintz M, Peschel A, et al. (2006) A functional dlt operon, encoding proteins required for incorporation of d-alanine in teichoic acids in gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae. J Bacteriol 188: 5797-5805.
17. Fabretti F, Theilacker C, Baldassarri L, Kaczynski Z, Kropec A, et al. (2006) Alanine esters of enterococcal lipoteichoic acid play a role in biofilm formation and resistance to antimicrobial peptides. Infect Immun 74: 4164-4171.
18. Peschel A, Vuong C, Otto M, Gotz F, (2000) The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 44: 2845-2847.
19. Poyart C, Lamy MC, Boumaila C, Fiedler F, Trieu-Cuot P, (2001) Regulation of D-alanyl-lipoteichoic acid biosynthesis in Streptococcus agalactiae involves a novel two-component regulatory system. J Bacteriol 183: 6324-6334.
20. Maisey HC, Doran KS, Nizet V, (2008) Recent advances in understanding the molecular basis of group B Streptococcus virulence. Expert Rev Mol Med 10: e27.
21. Sutcliffe IC, Black GW, Harrington DJ, (2008) Bioinformatic insights into the biosynthesis of the Group B carbohydrate in Streptococcus agalactiae. Microbiology 154: 1354-1363.
22. Poyart C, Pellegrini E, Marceau M, Baptista M, Jaubert F, et al. (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.
23. Rosenfeld Y, Sahl HG, Shai Y, (2008) Parameters involved in antimicrobial and endotoxin detoxification activities of antimicrobial peptides. Biochemistry 47: 6468-6478.
24. Papo N, Oren Z, Pag U, Sahl HG, Shai Y, (2002) The consequence of sequence alteration of an amphipathic alpha-helical antimicrobial peptide and its diastereomers. J Biol Chem 277: 33913-33921.
25. Rosenfeld Y, Lev N, Shai Y, (2010) Effect of the hydrophobicity to net positive charge ratio on antibacterial and anti-endotoxin activities of structurally similar antimicrobial peptides. Biochemistry 49: 853-861.
26. Bonelli RR, Schneider T, Sahl HG, Wiedemann I, (2006) Insights into in vivo activities of lantibiotics from gallidermin and epidermin mode-of-action studies. Antimicrob Agents Chemother 50: 1449-1457.
27. Bierbaum G, Sahl HG, (2009) Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm Biotechnol 10: 2-18.
28. Koprivnjak T, Peschel A, (2011) Bacterial resistance mechanisms against host defense peptides. Cell Mol Life Sci 68: 2243-2254.
29. Michon F, Brisson JR, Dell A, Kasper DL, Jennings HJ, (1988) Multiantennary group-specific polysaccharide of group B Streptococcus. Biochemistry 27: 5341-5351.
30. Michon F, Katzenellenbogen E, Kasper DL, Jennings HJ, (1987) Structure of the complex group-specific polysaccharide of group B Streptococcus. Biochemistry 26: 476-486.
31. Caliot E, Dramsi S, Chapot-Chartier MP, Courtin P, Kulakauskas S, et al. (2012) Role of the Group B Antigen of Streptococcus agalactiae: A Peptidoglycan-Anchored Polysaccharide Involved in Cell Wall Biogenesis. PLoS Pathog 8: e1002756.
32. Dorschner RA, Lopez-Garcia B, Peschel A, Kraus D, Morikawa K, et al. (2006) The mammalian ionic environment dictates microbial susceptibility to antimicrobial defense peptides. FASEB J 20: 35-42.
33. Swanson J, Gotschlich EC, (1973) Electron microscopic studies on streptococci. II. Group A carbohydrate. J Exp Med 138: 245-258.
34. Sweers KK, van der Werf KO, Bennink ML, Subramaniam V, (2012) Spatially resolved frequency-dependent elasticity measured with pulsed force microscopy and nanoindentation. Nanoscale 4: 2072-2077.
35. Sweers K, van der Werf K, Bennink M, Subramaniam V, (2011) Nanomechanical properties of alpha-synuclein amyloid fibrils: a comparative study by nanoindentation, harmonic force microscopy, and Peakforce QNM. Nanoscale Res Lett 6: 270.
36. Eaton P, Fernandes JC, Pereira E, Pintado ME, Xavier Malcata F, (2008) Atomic force microscopy study of the antibacterial effects of chitosans on Escherichia coli and Staphylococcus aureus. Ultramicroscopy 108: 1128-1134.
37. Tuson HH, Auer GK, Renner LD, Hasebe M, Tropini C, et al. (2012) Measuring the stiffness of bacterial cells from growth rates in hydrogels of tunable elasticity. Mol Microbiol 84: 874-91.
38. Kaconis Y, Kowalski I, Howe J, Brauser A, Richter W, et al. (2011) Biophysical mechanisms of endotoxin neutralization by cationic amphiphilic peptides. Biophys J 100: 2652-2661.
39. Epand RF, Savage PB, Epand RM, (2007) Bacterial lipid composition and the antimicrobial efficacy of cationic steroid compounds (Ceragenins). Biochim Biophys Acta 1768: 2500-2509.
40. Kraus D, Herbert S, Kristian SA, Khosravi A, Nizet V, et al. (2008) The GraRS regulatory system controls Staphylococcus aureus susceptibility to antimicrobial host defenses. BMC Microbiol 8: 85.
41. Peschel A, Jack RW, Otto M, Collins LV, Staubitz P, et al. (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.
42. Kilelee E, Pokorny A, Yeaman MR, Bayer AS, (2010) Lysyl-phosphatidylglycerol attenuates membrane perturbation rather than surface association of the cationic antimicrobial peptide 6W-RP-1 in a model membrane system: implications for daptomycin resistance. Antimicrob Agents Chemother 54: 4476-4479.
43. 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.
44. Nikaido H, (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67: 593-656.
45. Gutberlet T, Frank J, Bradaczek H, Fischer W, (1997) Effect of lipoteichoic acid on thermotropic membrane properties. J Bacteriol 179: 2879-2883.
46. Doyle RJ, Marquis RE, (1994) Elastic, flexible peptidoglycan and bacterial cell wall properties. Trends Microbiol 2: 57-60.
47. Hyyrylainen HL, Pietiainen M, Lunden T, Ekman A, Gardemeister M, et al. (2007) The density of negative charge in the cell wall influences two-component signal transduction in Bacillus subtilis. Microbiology 153: 2126-2136.
48. Mangoni ML, Papo N, Barra D, Simmaco M, Bozzi A, et al. (2004) Effects of the antimicrobial peptide temporin L on cell morphology, membrane permeability and viability of Escherichia coli. Biochem J 380: 859-865.
49. Kliger Y, Aharoni A, Rapaport D, Jones P, Blumenthal R, et al. (1997) Fusion peptides derived from the HIV type 1 glycoprotein 41 associate within phospholipid membranes and inhibit cell-cell fusion. Structure-function study. J Biol Chem 272: 13496-13505.
50. Andre G, Kulakauskas S, Chapot-Chartier MP, Navet B, Deghorain M, et al. (2010) Imaging the nanoscale organization of peptidoglycan in living Lactococcus lactis cells. Nat Commun 1: 27.