Controlling bacterial infections by inhibiting proton-dependent processes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1858, Issue 5, 2016, Pages 995-1003

  Kaneti, Galoz ^a   Meir, Ohad ^a   Mor, Amram ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Drug resistance; Host defense peptides; Membrane potential; Membrane active compounds; Oligomers of acylated cations; Signal transduction; Virulence

Indexed keywords

BETA LACTAM ANTIBIOTIC; CARBENICILLIN; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CERULENIN; CHLORAMPHENICOL; DAPTOMYCIN; DERMASEPTIN; GENTAMICIN; HEMOLYSIN; LINEZOLID; MACROLIDE; NOVOBIOCIN; OLIGOMER; OXACILLIN; PANTON VALENTINE LEUKOCIDIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; THIORIDAZINE; TOXIC SHOCK SYNDROME TOXIN 1; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; PROTON;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL THERAPY; ARTICLE; BACTERIAL INFECTION; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; BIOENERGY; BIOFILM; CELL DIVISION; CYTOPLASM; DISSOCIATION CONSTANT; ENERGY METABOLISM; GENE EXPRESSION; HOST RESISTANCE; HUMAN; INFECTION CONTROL; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTON MOTIVE FORCE; QUORUM SENSING; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; BACTERIAL INFECTIONS; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE;

ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL INFECTIONS; CELL MEMBRANE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HUMANS; MEMBRANE POTENTIALS; MICROBIAL SENSITIVITY TESTS; PROTONS; QUORUM SENSING; SIGNAL TRANSDUCTION;

EID: 84960877623     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2015.10.022     Document Type: Article

References (106)

1. T.F. Schaberle, and I.M. Hack Overcoming the current deadlock in antibiotic research Trends Microbiol. 22 2014 165 167
2. R. Eckert Road to clinical efficacy: challenges and novel strategies for antimicrobial peptide development Future Microbiol 6 2011 635 651
3. E.F. Haney, and R.E. Hancock Peptide design for antimicrobial and immunomodulatory applications Biopolymers 100 2013 572 583
4. M.S. Kinch, A. Haynesworth, S.L. Kinch, and D. Hoyer An overview of FDA-approved new molecular entities: 1827-2013 Drug Discov. Today 19 2014 1033 1039
5. L.L. Silver Challenges of antibacterial discovery Clin. Microbiol. Rev. 24 2011 71 109
6. M.A. Fischbach, and C.T. Walsh Antibiotics for emerging pathogens Science 325 2009 1089 1093
7. J.M.A. Blair, M.A. Webber, A.J. Baylay, D.O. Ogbolu, and L.J.V. Piddock Molecular mechanisms of antibiotic resistance Nat. Rev. Microbiol. 13 2015 42 51
8. N. McCallum, B. Berger-Bächi, and M.M. Senn Regulation of antibiotic resistance in Staphylococcus aureus Int. J. Med. Microbiol. 300 2010 118 129
9. K. Poole Bacterial stress responses as determinants of antimicrobial resistance J. Antimicrob. Chemother. 67 2012 2069 2089
10. J.K. Klitgaard, M.N. Skov, B.H. Kallipolitis, and H.J. Kolmos Reversal of methicillin resistance in Staphylococcus aureus by thioridazine J. Antimicrob. Chemother. 62 2008 1215 1221
11. J.G. Hurdle, A.J. O'Neill, I. Chopra, and R.E. Lee Targeting bacterial membrane function: an underexploited mechanism for treating persistent infections Nat. Rev. Microbiol. 9 2011 62 75
12. R.C. Allen, R. Popat, S.P. Diggle, and S.P. Brown Targeting virulence: can we make evolution-proof drugs? Nat. Rev. Microbiol. 12 2014 300 308
13. R.M. Epand, and H.J. Vogel Diversity of antimicrobial peptides and their mechanisms of action Biochim. Biophys. Acta 1462 1999 11 28
14. R.F. Epand, W.L. Maloy, A. Ramamoorthy, and R.M. Epand Probing the "charge cluster mechanism" in amphipathic helical cationic antimicrobial peptides Biochemistry 49 2010 4076 4084
15. R.E.W. Hancock, and D.S. Chapple Peptide antibiotics Antimicrob. Agents Chemother. 43 1999 1317 1323
16. S. Rotem, and A. Mor Antimicrobial peptide mimics for improved therapeutic properties Biochim. Biophys. Acta 1788 2009 1582 1592
17. H. Sarig, L. Livne, V. Held-Kuznetsov, F. Zaknoon, A. Ivankin, D. Gidalevitz, and A. Mor A miniature mimic of host defense peptides with systemic antibacterial efficacy FASEB J. 24 2010 1904 1913
18. D.B. Hicks, D.M. Cohen, and T.A. Krulwich Reconstitution of energy-linked activities of the solubilized F1F0 ATP synthase from Bacillus subtilis J. Bacteriol. 176 1994 4192 4195
19. E. Padan, E. Bibi, M. Ito, and T.A. Krulwich Alkaline pH homeostasis in bacteria: new insights Biochim. Biophys. Acta 1717 2005 67 88
20. A.K. Marr, W.J. Gooderham, and R.E.W. Hancock Antibacterial peptides for therapeutic use: obstacles and realistic outlook Curr. Opin. Pharmacol. 6 2006 468 472
21. T. Schuerholz, K. Brandenburg, and G. Marx Antimicrobial peptides and their potential application in inflammation and sepsis Crit. Care 16 2012 207
22. A. Patrzykat, C.L. Friedrich, L. Zhang, V. Mendoza, and R.E. Hancock Sublethal concentrations of pleurocidin-derived antimicrobial peptides inhibit macromolecular synthesis in Escherichia coli Antimicrob. Agents Chemother. 46 2002 605 614
23. S. Rotem, I.S. Radzishevsky, D. Bourdetsky, S. Navon-Venezia, Y. Carmeli, and A. Mor Analogous oligo-acyl-lysines with distinct antibacterial mechanisms FASEB J. 22 2008 2652 2661
24. M. Vaara, J. Fox, G. Loidl, O. Siikanen, J. Apajalahti, F. Hansen, N. Frimodt-Møller, J. Nagai, M. Takano, and T. Vaara Novel polymyxin derivatives carrying only three positive charges are effective antibacterial agents Antimicrob. Agents Chemother. 52 2008 3229 3236
25. L. Zhang, P. Dhillon, H. Yan, S. Farmer, and R.E.W. Hancock Interactions of bacterial cationic peptide antibiotics with outer and cytoplasmic membranes of Pseudomonas aeruginosa Antimicrob. Agents Chemother. 44 2000 3317 3321
26. J.G. Sawyer, N.L. Martin, and R.E.W. Hancock Interaction of macrophage cationic proteins with the outer membrane of Pseudomonas aeruginosa Infect. Immun. 56 1988 693 698
27. E. Ruhr, and H.G. Sahl Mode of action of the peptide antibiotic nisin and influence on the membrane potential of whole cells and on cytoplasmic and artificial membrane vesicles Antimicrob. Agents Chemother. 27 1985 841 845
28. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395
29. R.E.W. Hancock Mechanisms of action of newer antibiotics for Gram-positive pathogens Lancet Infect. Dis. 5 2005 209 218
30. P. Reisinger, H. Seidel, H. Tschesche, and W.P. Hammes The effect of nisin on murein synthesis Arch. Microbiol. 127 1980 187 193
31. V. Sass, T. Schneider, M. Wilmes, C. Körner, A. Tossi, N. Novikova, O. Shamova, and H.G. Sahl Human beta-defensin 3 inhibits cell wall biosynthesis in Staphylococci Infect. Immun. 78 2010 2793 2800
32. R.M. Epand, and R.F. Epand Lipid domains in bacterial membranes and the action of antimicrobial agents Biochim. Biophys. Acta 1788 2009 289 294
33. F. Jean-François, S. Castano, B. Desbat, B. Odaert, M. Roux, M.H. Metz-Boutigue, and E.J. Dufourc Aggregation of cateslytin beta-sheets on negatively charged lipids promotes rigid membrane domains. A new mode of action for antimicrobial peptides? Biochemistry 47 2008 6394 6402
34. R.M. Epand, S. Rotem, A. Mor, B. Berno, and R.F. Epand Bacterial membranes as predictors of antimicrobial potency J. Am. Chem. Soc. 130 2008 14346 14352
35. R.D. Jahnsen, E.F. Haney, H. Franzyk, and R.E.W. Hancock Characterization of a proteolytically stable multifunctional host defense peptidomimetic Chem. Biol. 20 2013 1286 1295
36. B. Mensa, Y.H. Kim, S. Choi, R. Scott, G.A. Caputo, and W.F. DeGrado Antibacterial mechanism of action of arylamide foldamers Antimicrob. Agents Chemother. 55 2011 5043 5053
37. J. Jammal, F. Zaknoon, G. Kaneti, K. Goldberg, and A. Mor Sensitization of Gram-negative bacteria to rifampin and OAK combinations Sci. Rep. 5 2015 1 6
38. K. Goldberg, H. Sarig, F. Zaknoon, R.F. Epand, R.M. Epand, and A. Mor Sensitization of Gram-negative bacteria by targeting the membrane potential FASEB J. 27 2013 3818 3826
39. L. Livne, R.F. Epand, B. Papahadjopoulos-Sternberg, R.M. Epand, and A. Mor OAK-based cochleates as a novel approach to overcome multidrug resistance in bacteria FASEB J. 24 2010 5092 5101
40. A. Dhand, A.S. Bayer, J. Pogliano, S.J. Yang, M. Bolaris, V. Nizet, G. Wang, and G. Sakoulas Use of antistaphylococcal beta-lactams to increase daptomycin activity in eradicating persistent bacteremia due to methicillin-resistant Staphylococcus aureus: role of enhanced daptomycin binding Clin. Infect. Dis. 53 2011 158 163
41. G. Sakoulas, C.Y. Okumura, W. Thienphrapa, J. Olson, P. Nonejuie, Q. Dam, A. Dhand, J. Pogliano, M.R. Yeaman, M.E. Hensler, A.S. Bayer, and V. Nizet Nafcillin enhances innate immune-mediated killing of methicillin-resistant Staphylococcus aureus J. Mol. Med. 92 2014 139 149
42. M. Paul, Y. Carmeli, E. Durante-Mangoni, J.W. Mouton, E. Tacconelli, U. Theuretzbacher, C. Mussini, and L. Leibovici Combination therapy for carbapenem-resistant Gram-negative bacteria J. Antimicrob. Chemother. 69 2014 2305 2309
43. S.A. Li, J. Liu, Y. Xiang, Y.J. Wang, W.H. Lee, and Y. Zhang Therapeutic potential of the antimicrobial peptide OH-CATH30 for antibiotic-resistant Pseudomonas aeruginosa keratitis Antimicrob. Agents Chemother. 58 2014 3144 3150
44. G. Kaneti, H. Sarig, I. Marjieh, F. Zaknoon, and A. Mor Simultaneous breakdown of multiple antibiotic resistance mechanisms in S. aureus FASEB J. 27 2013 4834 4843
45. D. Liu, S. Choi, B. Chen, R.J. Doerksen, D.J. Clements, J.D. Winkler, M.L. Klein, and W.F. DeGrado Nontoxic membrane-active antimicrobial arylamide oligomers Angew. Chem. Int. Ed. Engl. 43 2004 1158 1162
46. N.P. Chongsiriwatana, J.A. Patch, A.M. Czyzewski, M.T. Dohm, A. Ivankin, D. Gidalevitz, R.N. Zuckermann, and A.E. Barron Peptoids that mimic the structure, function, and mechanism of helical antimicrobial peptides Proc. Natl. Acad. Sci. U. S. A. 105 2008 2794 2799
47. M.W. Lee, S. Chakraborty, N.W. Schmidt, R. Murgai, S.H. Gellman, and G.C. Wong Two interdependent mechanisms of antimicrobial activity allow for efficient killing in nylon-3-based polymeric mimics of innate immunity peptides Biochim. Biophys. Acta 1838 2014 2269 2279
48. I.S. Radzishevsky, S. Rotem, D. Bourdetsky, S. Navon-Venezia, Y. Carmeli, and A. Mor Improved antimicrobial peptides based on acyl-lysine oligomers Nat. Biotechnol. 25 2007 657 659
49. S. Choi, A. Isaacs, D. Clements, D. Liu, H. Kim, R.W. Scott, J.D. Winkler, and W.F. DeGrado De novo design and in vivo activity of conformationally restrained antimicrobial arylamide foldamers Proc. Natl. Acad. Sci. U. S. A. 106 2009 6968 6973
50. M.T. Guskey, and B.T. Tsuji A comparative review of the lipoglycopeptides: oritavancin, dalbavancin, and telavancin Pharmacotherapy 30 2010 80 94
51. M.S. Wilke, A.L. Lovering, and N.C. Strynadka Beta-lactam antibiotic resistance: a current structural perspective Curr. Opin. Microbiol. 8 2005 525 533
52. T. Krell, J. Lacal, A. Busch, H. Silva-Jiménez, M.E.E. Guazzaroni, and J.L. Ramos Bacterial sensor kinases: diversity in the recognition of environmental signals Annu. Rev. Microbiol. 64 2010 539 559
53. S.D. Goldberg, G.D. Clinthorne, M. Goulian, and W.F. DeGrado Transmembrane polar interactions are required for signaling in the Escherichia coli sensor kinase PhoQ Proc. Natl. Acad. Sci. U. S. A. 107 2010 8141 8146
54. K. Lohner, and F. Prossnigg Biological activity and structural aspects of PGLa interaction with membrane mimetic systems Biochim. Biophys. Acta 1788 2009 1656 1666
55. P. Dimroth, G. Kaim, and U. Matthey Crucial role of the membrane potential for ATP synthesis by F(1)F(o) ATP synthases J. Exp. Biol. 203 2000 51 59
56. H. Strahl, and L.W. Hamoen Membrane potential is important for bacterial cell division Proc. Natl. Acad. Sci. U. S. A. 107 2010 12281 12286
57. I.T. Paulsen, M.H. Brown, and R.A. Skurray Proton-dependent multidrug efflux systems Microbiol. Rev. 60 1996 575 608
58. K. Poole Efflux-mediated antimicrobial resistance J. Antimicrob. Chemother. 56 2005 20 51
59. S.M. Daly, B.O. Elmore, J.S. Kavanaugh, K.D. Triplett, M. Figueroa, H.A. Raja, T. El-Elimat, H.A. Crosby, J.K. Femling, N.B. Cech, A.R. Horswill, N.H. Oberlies, and P.R. Hall ω-hydroxyemodin limits Staphylococcus aureus quorum sensing-mediated pathogenesis and inflammation Antimicrob. Agents Chemother. 59 2015 2223 2235
60. W.J. Gooderham, and R.E.W. Hancock Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa FEMS Microbiol. Rev. 33 2009 279 294
61. T.J. Foster Immune evasion by staphylococci Nat. Rev. Microbiol. 3 2005 948 958
62. V. Nizet Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets J. Allergy Clin. Immunol. 120 2007 13 22
63. E.C. Carnes, D.M. Lopez, N.P. Donegan, A. Cheung, H. Gresham, G.S. Timmins, and J.C. Brinker Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria Nat. Chem. Biol. 6 2010 41 45
64. E.K. Sully, N. Malachowa, B.O. Elmore, S.M. Alexander, J.K. Femling, B.M. Gray, F.R. DeLeo, M. Otto, A.L. Cheung, B.S. Edwards, L.A. Sklar, A.R. Horswill, P.R. Hall, and H.D. Gresham Selective chemical inhibition of agr quorum sensing in Staphylococcus aureus promotes host defense with minimal impact on resistance PLoS Pathogens 10 2014
65. B.K. Sharma-Kuinkel, E.E. Mann, J.S.S. Ahn, L.J. Kuechenmeister, P.M. Dunman, and K.W. Bayles The Staphylococcus aureus LytSR two-component regulatory system affects biofilm formation J. Bacteriol. 191 2009 4767 4775
66. T. Koprivnjak, and A. Peschel Bacterial resistance mechanisms against host defense peptides Cell. Mol. Life Sci. 68 2011 2243 2254
67. A. Nielsen, M. Månsson, M.S. Bojer, L. Gram, T.O. Larsen, R.P. Novick, D. Frees, H. Frøkiær, and H. Ingmer Solonamide B inhibits quorum sensing and reduces Staphylococcus aureus mediated killing of human neutrophils PLoS One 9 2014
68. T. Shprung, A. Peleg, Y. Rosenfeld, P. Trieu-Cuot, and Y. Shai Effect of PhoP-PhoQ activation by broad repertoire of antimicrobial peptides on bacterial resistance J. Biol. Chem. 287 2012 4544 4551
69. L.R. Marks, E.A. Clementi, and A.P. Hakansson The human milk protein-lipid complex HAMLET sensitizes bacterial pathogens to traditional antimicrobial agents PLoS One 7 2012 e43514
70. J. Overhage, A. Campisano, M. Bains, E.C. Torfs, B.H. Rehm, and R.E.W. Hancock Human host defense peptide LL-37 prevents bacterial biofilm formation Infect. Immun. 76 2008 4176 4182
71. C. de la Fuente-Núñez, V. Korolik, M. Bains, U. Nguyen, E.B. Breidenstein, S. Horsman, S. Lewenza, L. Burrows, and R.E.W. Hancock Inhibition of bacterial biofilm formation and swarming motility by a small synthetic cationic peptide Antimicrob. Agents Chemother. 56 2012 2696 2704
72. X.Z. Li, H. Nikaido, and K. Poole Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa Antimicrob. Agents Chemother. 39 1995 1948 1953
73. D. Ma, D.N. Cook, M. Alberti, N.G. Pon, H. Nikaido, and J.E. Hearst Molecular cloning and characterization of acrA and acrE genes of Escherichia coli J. Bacteriol. 175 1993 6299 6313
74. H. Yoshida, M. Bogaki, S. Nakamura, K. Ubukata, and M. Konno Nucleotide sequence and characterization of the Staphylococcus aureus norA gene, which confers resistance to quinolones J. Bacteriol. 172 1990 6942 6949
75. M. Wenzel, A.I. Chiriac, A. Otto, D. Zweytick, C. May, C. Schumacher, R. Gust, H.B. Albada, M. Penkova, and U. Krämer Small cationic antimicrobial peptides delocalize peripheral membrane proteins Proc. Natl. Acad. Sci. 111 2014 E1409 E1418
76. K.A. Brogden Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 2005 238 250
77. A. Muthaiyan, J.A. Silverman, R.K. Jayaswal, and B.J. Wilkinson Transcriptional profiling reveals that daptomycin induces the Staphylococcus aureus cell wall stress stimulon and genes responsive to membrane depolarization Antimicrob. Agents Chemother. 52 2008 980 990
78. J.M. Saugar, T. Alarcón, S. López-Hernández, M. López-Brea, D. Andreu, and L. Rivas Activities of polymyxin B and cecropin A-,melittin peptide CA(1-8)M(1-18) against a multiresistant strain of Acinetobacter baumannii Antimicrob. Agents Chemother. 46 2002 875 878
79. K. Marynka, S. Rotem, I. Portnaya, U. Cogan, and A. Mor In vitro discriminative antipseudomonal properties resulting from acyl substitution of N-terminal sequence of dermaseptin S4 derivatives Chem. Biol. 14 2007 75 85
80. G. Lin, G.A. Pankuch, L.M. Ednie, and P.C. Appelbaum Antistaphylococcal activities of telavancin tested alone and in combination by time-kill assay Antimicrob. Agents Chemother. 54 2010 2201 2205
81. J. Qiu, H. Feng, J. Lu, H. Xiang, D. Wang, J. Dong, J. Wang, X. Wang, J. Liu, and X. Deng Eugenol reduces the expression of virulence-related exoproteins in Staphylococcus aureus Appl. Environ. Microbiol. 76 2010 5846 5851
82. P. Ma, K. Nishiguchi, H.M. Yuille, L.M. Davis, J. Nakayama, and M.K. Phillips-Jones Anti-HIV siamycin I directly inhibits autophosphorylation activity of the bacterial FsrC quorum sensor and other ATP-dependent enzyme activities FEBS Lett. 585 2011 2660 2664
83. J. Nakayama, E. Tanaka, R. Kariyama, K. Nagata, K. Nishiguchi, R. Mitsuhata, Y. Uemura, M. Tanokura, H. Kumon, and K. Sonomoto Siamycin attenuates fsr quorum sensing mediated by a gelatinase biosynthesis-activating pheromone in Enterococcus faecalis J. Bacteriol. 189 2007 1358 1365
84. D.L. Higgins, R. Chang, D.V. Debabov, J. Leung, T. Wu, K.M. Krause, E. Sandvik, J.M. Hubbard, K. Kaniga, D.E.J. Schmidt, Q. Gao, R.T. Cass, D.E. Karr, B.M. Benton, and P.P. Humphrey Telavancin, a multifunctional lipoglycopeptide, disrupts both cell wall synthesis and cell membrane integrity in methicillin-resistant Staphylococcus aureus Antimicrob. Agents Chemother. 49 2005 1127 1134
85. H.C. Chan, Y.T. Huang, S.Y. Lyu, C.J. Huang, Y.S. Li, Y.C. Liu, C.C. Chou, M.D. Tsai, and T.L. Li Regioselective deacetylation based on teicoplanin-complexed Orf2∗crystal structures Mol. BioSyst. 7 2011 1224 1231
86. S. Rotem, I. Radzishevsky, and A. Mor Physicochemical properties that enhance discriminative antibacterial activity of short dermaseptin derivatives Antimicrob. Agents Chemother. 50 2006 2666 2672
87. I.S. Radzishevsky, S. Rotem, F. Zaknoon, L. Gaidukov, A. Dagan, and A. Mor Effects of acyl versus aminoacyl conjugation on the properties of antimicrobial peptides Antimicrob. Agents Chemother. 49 2005 2412 2420
88. S.E. Blondelle, and R.A. Houghten Hemolytic and antimicrobial activities of the twenty-four individual omission analogues of melittin Biochemistry 30 1991 4671 4678
89. R.P. Novick Autoinduction and signal transduction in the regulation of staphylococcal virulence Mol. Microbiol. 48 2003 1429 1449
90. M.S. Wilke, T.L. Hills, H.Z. Zhang, H.F. Chambers, and N.C. Strynadka Crystal structures of the Apo and penicillin-acylated forms of the BlaR1 beta-lactam sensor of Staphylococcus aureus J. Biol. Chem. 279 2004 47278 47287
91. K. Stephenson, Y. Yamaguchi, and J.A. Hoch The mechanism of action of inhibitors of bacterial two-component signal transduction systems J. Biol. Chem. 275 2000 38900 38904
92. O. Dumitrescu, S. Boisset, C. Badiou, M. Bes, Y. Benito, M.E. Reverdy, F. Vandenesch, J. Etienne, and G. Lina Effect of antibiotics on Staphylococcus aureus producing panton-valentine leukocidin Antimicrob. Agents Chemother. 51 2007 1515 1519
93. R.P. Adhikari, and R.P. Novick Subinhibitory cerulenin inhibits staphylococcal exoprotein production by blocking transcription rather than by blocking secretion Microbiology 151 2005 3059 3069
94. K. Bernardo, N. Pakulat, S. Fleer, A. Schnaith, O. Utermöhlen, O. Krut, S. Müller, and M. Krönke Subinhibitory concentrations of linezolid reduce Staphylococcus aureus virulence factor expression Antimicrob. Agents Chemother. 48 2004 546 555
95. O. Simonetti, O. Cirioni, R. Ghiselli, G. Goteri, A. Scalise, F. Orlando, C. Silvestri, A. Riva, V. Saba, K.D. Madanahally, A. Offidani, N. Balaban, G. Scalise, and A. Giacometti RNAIII-inhibiting peptide enhances healing of wounds infected with methicillin-resistant Staphylococcus aureus Antimicrob. Agents Chemother. 52 2008 2205 2211
96. N. Balaban, Y. Gov, A. Giacometti, O. Cirioni, R. Ghiselli, F. Mocchegiani, F. Orlando, G. D'Amato, V. Saba, G. Scalise, S. Bernes, and A. Mor A chimeric peptide composed of a dermaseptin derivative and an RNA III-inhibiting peptide prevents graft-associated infections by antibiotic-resistant staphylococci Antimicrob. Agents Chemother. 48 2004 2544 2550
97. D. McDougald, S.A. Rice, and S. Kjelleberg Bacterial quorum sensing and interference by naturally occurring biomimics Anal. Bioanal. Chem. 387 2006 445 453
98. H. Hirakawa, and H. Tomita Interference of bacterial cell-to-cell communication: a new concept of antimicrobial chemotherapy breaks antibiotic resistance Front. Microbiol. 4 2013 1 14
99. C.S. Lunde, S.R. Hartouni, J.W. Janc, M. Mammen, P.P. Humphrey, and B.M. Benton Telavancin disrupts the functional integrity of the bacterial membrane through targeted interaction with the cell wall precursor lipid II Antimicrob. Agents Chemother. 53 2009 3375 3383
100. K.H. Rand, and H.J. Houck Synergy of daptomycin with oxacillin and other beta-lactams against methicillin-resistant Staphylococcus aureus Antimicrob. Agents Chemother. 48 2004 2871 2875
101. S.J. Yang, Y.Q. Xiong, S. Boyle-Vavra, R. Daum, T. Jones, and A.S. Bayer Daptomycin-oxacillin combinations in treatment of experimental endocarditis caused by daptomycin-nonsusceptible strains of methicillin-resistant Staphylococcus aureus with evolving oxacillin susceptibility (the "seesaw effect") Antimicrob. Agents Chemother. 54 2010 3161 3169
102. S.J. Yang, A.S. Bayer, N.N. Mishra, M. Meehl, N. Ledala, M.R. Yeaman, Y.Q. Xiong, and A.L. Cheung The Staphylococcus aureus two-component regulatory system, GraRS, senses and confers resistance to selected cationic antimicrobial peptides Infect. Immun. 80 2012 74 81
103. J. Andrä, T. Goldmann, C.M. Ernst, A. Peschel, and T. Gutsmann Multiple peptide resistance factor (MprF)-mediated resistance of Staphylococcus aureus against antimicrobial peptides coincides with a modulated peptide interaction with artificial membranes comprising lysyl-phosphatidylglycerol J. Biol. Chem. 286 2011 18692 18700
104. I. Fedtke, F. Gotz, and A. Peschel Bacterial evasion of innate host defenses-the Staphylococcus aureus lesson Int. J. Med. Microbiol. 294 2004 189 194
105. L. Fernández, W.J. Gooderham, M. Bains, J.B. McPhee, I. Wiegand, and R.E.W. Hancock Adaptive resistance to the "last hope" antibiotics polymyxin B and colistin in Pseudomonas aeruginosa is mediated by the novel two-component regulatory system ParR-ParS Antimicrob. Agents Chemother. 54 2010 3372 3382
106. M.L. Mangoni, and Y. Shai Short native antimicrobial peptides and engineered ultrashort lipopeptides: similarities and differences in cell specificities and modes of action Cell. Mol. Life Sci. 68 2011 2267 2280