1887

Abstract

Bacteria offer resistance to a broad range of antibiotics by activating their export channels of ATP-binding cassette transporters. These transporters perform a central role in vital processes of self-immunity, antibiotic transport and resistance. The majority of ATP-binding cassette transporters are capable of detecting the presence of antibiotics in an external vicinity and are tightly regulated by two-component systems. The presence of an extracellular loop and an adjacent location of both the transporter and two-component system offers serious assistance to induce a quick and specific response against antibiotics. Both systems have demonstrated their ability of sensing such agents, however, the exact mechanism is not yet fully established. This review highlighted the three key functions of antibiotic resistance, transport and self-immunity of ATP-binding cassette transporters and an adjacent two-component regulatory system.

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2019-06-17
2020-11-25
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References

  1. Koprivnjak T, Peschel A. Bacterial resistance mechanisms against host defense peptides. Cell Mol Life Sci 2011; 68:2243–2254 [CrossRef]
    [Google Scholar]
  2. Neu HC. The crisis in antibiotic resistance. Science 1992; 257:1064–1073 [CrossRef]
    [Google Scholar]
  3. Chatterjee C, Paul M, Xie L, van der Donk WA. Biosynthesis and mode of action of lantibiotics. Chem Rev 2005; 105:633–684 [CrossRef]
    [Google Scholar]
  4. Andersson DI, Hughes D, Kubicek-Sutherland JZ. Mechanisms and consequences of bacterial resistance to antimicrobial peptides. Drug Resist Updat 2016; 26:43–57 [CrossRef]
    [Google Scholar]
  5. Aoki W, Kuroda K, Ueda M. Next generation of antimicrobial peptides as molecular targeted medicines. J Biosci Bioeng 2012; 114:365–370 [CrossRef]
    [Google Scholar]
  6. Nawrocki KL, Crispell EK, McBride SM. Antimicrobial peptide resistance mechanisms of gram-positive bacteria. Antibiotics 2014; 3:461–492 [CrossRef]
    [Google Scholar]
  7. Drlica K, Zhao X. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 1997; 61:377–392
    [Google Scholar]
  8. Tenover FC. Mechanisms of antimicrobial resistance in bacteria. Am J Med 2006; 119:S3–S10 [CrossRef]
    [Google Scholar]
  9. Berger-Bächi B, Rohrer S. Factors influencing methicillin resistance in staphylococci. Arch Microbiol 2002; 178:165–171 [CrossRef]
    [Google Scholar]
  10. Matsuhashi M, Song MD, Ishino F, Wachi M, Doi M et al. Molecular cloning of the gene of a penicillin-binding protein supposed to cause high resistance to beta-lactam antibiotics in Staphylococcus aureus . J Bacteriol 1986; 167:975–980 [CrossRef]
    [Google Scholar]
  11. Boyle-Vavra S, Yin S, Challapalli M, Daum RS. Transcriptional induction of the penicillin-binding protein 2 gene in Staphylococcus aureus by cell wall-active antibiotics oxacillin and vancomycin. Antimicrob Agents Chemother 2003; 47:1028–1036 [CrossRef]
    [Google Scholar]
  12. Kuroda M, Kuroda H, Oshima T, Takeuchi F, Mori H et al. Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus . Mol Microbiol 2003; 49:807–821 [CrossRef]
    [Google Scholar]
  13. Nizet V. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr Issues Mol Biol 2006; 8:11–26
    [Google Scholar]
  14. Stratton CW. Mechanisms of bacterial resistance to antimicrobial agents. J Med Liban 2000; 48:186–198
    [Google Scholar]
  15. Zhang H, Ma G, Zhu Y, Zeng L, Ahmad A et al. Active-site conformational fluctuations promote the enzymatic activity of NDM-1. Antimicrob Agents Chemother 2018; 62: [CrossRef]
    [Google Scholar]
  16. Ma G, Zhu Y, Yu Z, Ahmad A, Zhang H. High resolution crystal structure of the catalytic domain of MCR-1. Sci Rep 2016; 6:39540 [CrossRef]
    [Google Scholar]
  17. Tomii K, Kanehisa M. A comparative analysis of ABC transporters in complete microbial genomes. Genome Res 1998; 8:1048–1059 [CrossRef]
    [Google Scholar]
  18. Bernard R, Guiseppi A, Chippaux M, Foglino M, Denizot F. Resistance to bacitracin in Bacillus subtilis: unexpected requirement of the BceAB ABC transporter in the control of expression of its own structural genes. J Bacteriol 2007; 189:8636–8642 [CrossRef]
    [Google Scholar]
  19. Tsuda H, Yamashita Y, Shibata Y, Nakano Y, Koga T. Genes involved in bacitracin resistance in Streptococcus mutans. Antimicrob Agents Chemother 2002; 46:3756–3764 [CrossRef]
    [Google Scholar]
  20. Coumes-Florens S, Brochier-Armanet C, Guiseppi A, Denizot F, Foglino M. A new highly conserved antibiotic sensing/resistance pathway in firmicutes involves an ABC transporter interplaying with a signal transduction system. PLoS One 2011; 6:e15951 [CrossRef]
    [Google Scholar]
  21. Linton KJ, Higgins CF. The Escherichia coli ATP-binding cassette (ABC) proteins. Mol Microbiol 1998; 28:5–13 [CrossRef]
    [Google Scholar]
  22. Young J, Holland IB. ABC transporters: bacterial exporters-revisited five years on. Biochimica et Biophysica Acta (BBA) - Biomembranes 1999; 1461:177–200 [CrossRef]
    [Google Scholar]
  23. Higgins CF. ABC transporters: physiology, structure and mechanism-an overview. Res Microbiol 2001; 152:205–210 [CrossRef]
    [Google Scholar]
  24. Cotter PD, Hill C, Ross RP. Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 2005; 3:777–788 [CrossRef]
    [Google Scholar]
  25. Gebhard S. ABC transporters of antimicrobial peptides in firmicutes bacteria - phylogeny, function and regulation. Mol Microbiol 2012; 86:1295–1317 [CrossRef]
    [Google Scholar]
  26. Saier MH, Reddy VS, Tsu BV, Ahmed MS, Li C et al. The transporter classification database (tcdB): recent advances. Nucleic Acids Res 2016; 44:D372–D379 [CrossRef]
    [Google Scholar]
  27. Stein T, Heinzmann S, Solovieva I, Entian KD. Function of Lactococcus lactis nisin immunity genes nisI and nisFEG after coordinated expression in the surrogate host Bacillus subtilis . J Biol Chem 2003; 278:89–94 [CrossRef]
    [Google Scholar]
  28. Mascher T, Margulis NG, Wang T, Ye RW, Helmann JD. Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol Microbiol 2003; 50:1591–1604 [CrossRef]
    [Google Scholar]
  29. Majchrzykiewicz JA, Kuipers OP, Bijlsma JJE. Generic and specific adaptive responses of Streptococcus pneumoniae to challenge with three distinct antimicrobial peptides, bacitracin, LL-37, and nisin. Antimicrob Agents Chemother 2010; 54:440–451 [CrossRef]
    [Google Scholar]
  30. Martínez B, Zomer AL, Rodríguez A, Kok J, Kuipers OP. Cell envelope stress induced by the bacteriocin Lcn972 is sensed by the lactococcal two-component system CesSR. Mol Microbiol 2007; 64:473–486 [CrossRef]
    [Google Scholar]
  31. Okuda K-ichi, Aso Y, Nakayama J, Sonomoto K. Cooperative transport between NukFEG and NukH in immunity against the lantibiotic nukacin ISK-1 produced by Staphylococcus warneri ISK-1. J Bacteriol 2008; 190:356–362 [CrossRef]
    [Google Scholar]
  32. Altena K, Guder A, Cramer C, Bierbaum G. Biosynthesis of the lantibiotic mersacidin: organization of a type B lantibiotic gene cluster. Appl Environ Microbiol 2000; 66:2565–2571 [CrossRef]
    [Google Scholar]
  33. Draper LA, Ross RP, Hill C, Cotter PD. Lantibiotic immunity. Curr Protein Pept Sci 2008; 9:39–49
    [Google Scholar]
  34. Okuda K-ichi, Yanagihara S, Sugayama T, Zendo T, Nakayama J, Okuda K et al. Functional significance of the E loop, a novel motif conserved in the lantibiotic immunity ATP-binding cassette transport systems. J Bacteriol 2010; 192:2801–2808 [CrossRef]
    [Google Scholar]
  35. Guder A, Schmitter T, Wiedemann I, Sahl HG, Bierbaum G. Role of the single regulator MrsR1 and the two-component system MrsR2/K2 in the regulation of mersacidin production and immunity. Appl Environ Microbiol 2002; 68:106–113 [CrossRef]
    [Google Scholar]
  36. Rincé A, Dufour A, Uguen P, Le Pennec JP, Haras D. Characterization of the lacticin 481 operon: the Lactococcus lactis genes lctF, lctE, and lctG encode a putative ABC transporter involved in bacteriocin immunity. Appl Environ Microbiol 1997; 63:4252–4260
    [Google Scholar]
  37. Otto M, Peschel A, Götz F. Producer self-protection against the lantibiotic epidermin by the ABC transporter EpiFEG of Staphylococcus epidermidis Tü3298. FEMS Microbiol Lett 1998; 166:203–211 [CrossRef]
    [Google Scholar]
  38. Hilmi HTA, Kylä-Nikkilä K, Ra R, Saris PEJ. Nisin induction without nisin secretion. Microbiology 2006; 152:1489–1496 [CrossRef]
    [Google Scholar]
  39. Greene NP, Kaplan E, Crow A, Koronakis V. Antibiotic resistance mediated by the MacB ABC transporter family: a structural and functional perspective. Front Microbiol 2018; 9:950 [CrossRef]
    [Google Scholar]
  40. Draper LA, Cotter PD, Hill C, Ross RP, resistance L. Lantibiotic resistance. Microbiol Mol Biol Rev 2015; 79:171–191 [CrossRef]
    [Google Scholar]
  41. Ohki R, Tateno K, Masuyama W, Moriya S et al. The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis . Mol Microbiol 2003; 49:1135–1144 [CrossRef]
    [Google Scholar]
  42. Jung K, Fried L, Behr S, Heermann R. Histidine kinases and response regulators in networks. Curr Opin Microbiol 2012; 15:118–124 [CrossRef]
    [Google Scholar]
  43. Parkinson JS, Kofoid EC. Communication modules in bacterial signaling proteins. Annu Rev Genet 1992; 26:71–112 [CrossRef]
    [Google Scholar]
  44. Swanson RV, Alex LA, Simon MI. Histidine and aspartate phosphorylation: two-component systems and the limits of homology. Trends Biochem Sci 1994; 19:485–490 [CrossRef]
    [Google Scholar]
  45. Mascher T. Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in firmicutes bacteria. FEMS Microbiol Lett 2006; 264:133–144 [CrossRef]
    [Google Scholar]
  46. Dintner S, Staron A, Berchtold E, Petri T, Mascher T et al. Coevolution of ABC transporters and two-component regulatory systems as resistance modules against antimicrobial peptides in firmicutes bacteria. J Bacteriol 2011; 193:3851–3862 [CrossRef]
    [Google Scholar]
  47. Joseph P, Guiseppi A, Sorokin A, Denizot F. Characterization of the Bacillus subtilis YxdJ response regulator as the inducer of expression for the cognate ABC transporter YxdLM. Microbiology 2004; 150:2609–2617 [CrossRef]
    [Google Scholar]
  48. Collins B, Curtis N, Cotter PD, Hill C, Ross RP. The ABC transporter AnrAB contributes to the innate resistance of Listeria monocytogenes to nisin, bacitracin, and various beta-lactam antibiotics. Antimicrob Agents Chemother 2010; 54:4416–4423 [CrossRef]
    [Google Scholar]
  49. Li M, Cha DJ, Lai Y, Villaruz AE, Sturdevant DE et al. The antimicrobial peptide-sensing system APS of Staphylococcus aureus . Mol Microbiol 2007; 66:1136–1147 [CrossRef]
    [Google Scholar]
  50. Meehl M, Herbert S, Götz F, Cheung A. Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus . Antimicrob Agents Chemother 2007; 51:2679–2689 [CrossRef]
    [Google Scholar]
  51. Ouyang J, Tian X-L, Versey J, Wishart A, Li Y-H. The BceABRS four-component system regulates the bacitracin-induced cell envelope stress response in Streptococcus mutans . Antimicrob Agents Chemother 2010; 54:3895–3906 [CrossRef]
    [Google Scholar]
  52. Rietkötter E, Hoyer D, Mascher T. Bacitracin sensing in Bacillus subtilis . Mol Microbiol 2008; 68:768–785 [CrossRef]
    [Google Scholar]
  53. Dufour A, Hindré T, Haras D, Le Pennec JP. The biology of lantibiotics from the lacticin 481 group is coming of age. FEMS Microbiol Rev 2007; 31:134–167 [CrossRef]
    [Google Scholar]
  54. Draper LA, Deegan LH, Hill C, Cotter PD, Ross RP. Insights into lantibiotic immunity provided by bioengineering of LtnI. Antimicrob Agents Chemother 2012; 56:5122–5133 [CrossRef]
    [Google Scholar]
  55. Becker P, Hakenbeck R, Henrich B. An ABC transporter of Streptococcus pneumoniae involved in susceptibility to vancoresmycin and bacitracin. Antimicrob Agents Chemother 2009; 53:2034–2041 [CrossRef]
    [Google Scholar]
  56. Friedman L, Alder JD, Silverman JA. Genetic changes that correlate with reduced susceptibility to daptomycin in Staphylococcus aureus . Antimicrob Agents Chemother 2006; 50:2137–2145 [CrossRef]
    [Google Scholar]
  57. Mukherjee A, DiMario PJ, Grove A. Mycobacterium smegmatis histone-like protein Hlp is nucleoid associated. FEMS Microbiol Lett 2009; 291:232–240 [CrossRef]
    [Google Scholar]
  58. Joseph P, Fichant G, Quentin Y, Denizot F. Regulatory relationship of two-component and ABC transport systems and clustering of their genes in the Bacillus/Clostridium group, suggest a functional link between them. J Mol Microbiol Biotechnol 2002; 4:503–513
    [Google Scholar]
  59. Hoch JA. Two-component and phosphorelay signal transduction. Curr Opin Microbiol 2000; 3:165–170 [CrossRef]
    [Google Scholar]
  60. de Been M, Bart MJ, Abee T, Siezen RJ, Francke C. The identification of response regulator-specific binding sites reveals new roles of two-component systems in Bacillus cereus and closely related low-GC Gram-positives. Environ Microbiol 2008; 10:2796–2809 [CrossRef]
    [Google Scholar]
  61. Turner J, Cho Y, Dinh NN, Waring AJ, Lehrer RI. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob Agents Chemother 1998; 42:2206–2214 [CrossRef]
    [Google Scholar]
  62. Rukmana A, Morimoto T, Takahashi H, Giyanto ON, Ogasawara N. Assessment of transcriptional responses of Bacillus subtilis cells to the antibiotic enduracidin, which interferes with cell wall synthesis, using a high-density tiling CHIP. Genes Genet Syst 2009; 84:253–267 [CrossRef]
    [Google Scholar]
  63. Reiners J, Lagedroste M, Ehlen K, Leusch S, Zaschke-Kriesche J et al. The N-terminal region of nisin is important for the BceAB-type ABC transporter NsrFP from Streptococcus agalactiae COH1. Front Microbiol 2017; 8:1643 [CrossRef]
    [Google Scholar]
  64. Yoshida Y, Matsuo M, Oogai Y, Kato F, Nakamura N et al. Bacitracin sensing and resistance in Staphylococcus aureus . FEMS Microbiol Lett 2011; 320:33–39 [CrossRef]
    [Google Scholar]
  65. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. The Lancet 2006; 368:874–885 [CrossRef]
    [Google Scholar]
  66. Kingston AW, Zhao H, Cook GM, Helmann JD. Accumulation of heptaprenyl diphosphate sensitizes Bacillus subtilis to bacitracin: implications for the mechanism of resistance mediated by the BceAB transporter. Mol Microbiol 2014; 93:37–49 [CrossRef]
    [Google Scholar]
  67. Lowy FD. Antimicrobial resistance: the example of Staphylococcus aureus . J Clin Invest 2003; 111:1265–1273 [CrossRef]
    [Google Scholar]
  68. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus . The Lancet 2001; 357:1225–1240 [CrossRef]
    [Google Scholar]
  69. Pietiäinen M, François P, Hyyryläinen H-L, Tangomo M, Sass V et al. Transcriptome analysis of the responses of Staphylococcus aureus to antimicrobial peptides and characterization of the roles of vraDE and vraSR in antimicrobial resistance. BMC Genomics 2009; 10:429 [CrossRef]
    [Google Scholar]
  70. Falord M, Mäder U, Hiron A, Débarbouillé M, Msadek T. Investigation of the Staphylococcus aureus GraSR regulon reveals novel links to virulence, stress response and cell wall signal transduction pathways. PLoS One 2011; 6:e21323 [CrossRef]
    [Google Scholar]
  71. Cui L, Lian JQ, Neoh HM, Reyes E, Hiramatsu K. DNA microarray-based identification of genes associated with glycopeptide resistance in Staphylococcus aureus . Antimicrob Agents Chemother 2005; 49:3404–3413 [CrossRef]
    [Google Scholar]
  72. Kuroda M, Kuwahara-Arai K, Hiramatsu K. Identification of the up- and down-regulated genes in vancomycin-resistant Staphylococcus aureus strains Mu3 and Mu50 by cDNA differential hybridization method. Biochem Biophys Res Commun 2000; 269:485–490 [CrossRef]
    [Google Scholar]
  73. Herbert S, Bera A, Nerz C, Kraus D, Peschel A et al. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog 2007; 3:e102 [CrossRef]
    [Google Scholar]
  74. Sass P, Bierbaum G. Native graS mutation supports the susceptibility of Staphylococcus aureus strain SG511 to antimicrobial peptides. Int J Med Microbiol 2009; 299:313–322 [CrossRef]
    [Google Scholar]
  75. Weidenmaier C, Peschel A, Kempf VAJ, Lucindo N, Yeaman MR et al. 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 2005; 73:8033–8038 [CrossRef]
    [Google Scholar]
  76. Cafiso V, Bertuccio T, Spina D, Purrello S, Campanile F et al. Modulating activity of vancomycin and daptomycin on the expression of autolysis cell-wall turnover and membrane charge genes in hVISA and visa strains. PLoS One 2012; 7:e29573 [CrossRef]
    [Google Scholar]
  77. Yang SJ, Bayer AS, Mishra NN, Meehl M, Ledala N et al. The Staphylococcus aureus two-component regulatory system, GraRS, senses and confers resistance to selected cationic antimicrobial peptides. Infect Immun 2012; 80:74–81 [CrossRef]
    [Google Scholar]
  78. Li M, Lai Y, Villaruz AE, Cha DJ, Sturdevant DE et al. Gram-positive three-component antimicrobial peptide-sensing system. Proc Natl Acad Sci U S A 2007; 104:9469–9474 [CrossRef]
    [Google Scholar]
  79. Yang SJ, Kreiswirth BN, Sakoulas G, Yeaman MR, Xiong YQ et al. Enhanced expression of dltABCD is associated with the development of daptomycin nonsusceptibility in a clinical endocarditis isolate of Staphylococcus aureus . J Infect Dis 2009; 200:1916–1920 [CrossRef]
    [Google Scholar]
  80. Yang SJ, Xiong YQ, Dunman PM, Schrenzel J, François P et al. Regulation of mprF in daptomycin-nonsusceptible Staphylococcus aureus strains. Antimicrob Agents Chemother 2009; 53:2636–2637 [CrossRef]
    [Google Scholar]
  81. Falord M, Karimova G, Hiron A, Msadek T. GraXSR proteins interact with the VraFG ABC transporter to form a five-component system required for cationic antimicrobial peptide sensing and resistance in Staphylococcus aureus . Antimicrobial Agents and Chemotherapy 2012; 56:1047–1058 [CrossRef]
    [Google Scholar]
  82. Hale JDF, Hancock REW. Alternative mechanisms of action of cationic antimicrobial peptides on bacteria. Expert Rev Anti Infect Ther 2007; 5:951–959 [CrossRef]
    [Google Scholar]
  83. Mehta S, Cuirolo AX, Plata KB, Riosa S, Silverman JA et al. VraSR two-component regulatory system contributes to mprF-mediated decreased susceptibility to daptomycin in in vivo-selected clinical strains of methicillin-resistant Staphylococcus aureus . Antimicrob Agents Chemother 2012; 56:92–102 [CrossRef]
    [Google Scholar]
  84. Hiron A, Falord M, Valle J, Débarbouillé M, Msadek T. Bacitracin and nisin resistance in Staphylococcus aureus: a novel pathway involving the BraS/BraR two-component system (SA2417/SA2418) and both the BraD/BraE and VraD/VraE ABC transporters. Mol Microbiol 2011; 81:602–622 [CrossRef]
    [Google Scholar]
  85. Fritz G, Dintner S, Treichel NS, Radeck J, Gerland U et al. A new way of sensing: need-based activation of antibiotic resistance by a flux-sensing mechanism. MBio 2015; 6:e00975 [CrossRef]
    [Google Scholar]
  86. Gold OG, Jordan HV, van Houte J. A selective medium for Streptococcus mutans . Arch Oral Biol 1973; 18:1357–1364 [CrossRef]
    [Google Scholar]
  87. Jalal N, Tian X-L, Dong G, Upham J, Chen C et al. Identification and characterization of SMU.244 encoding a putative undecaprenyl pyrophosphate phosphatase protein required for cell wall biosynthesis and bacitracin resistance in Streptococcus mutans . Microbiology 2015; 161:1857–1870 [CrossRef]
    [Google Scholar]
  88. Mikami Y, Suzuki N, Takahashi T, Otsuka K, Tsuda H. Bacitracin upregulates mbrAB transcription via mbrCD to confer bacitracin resistance in Streptococcus mutans . J Pharmacol Sci 2011; 117:204–207 [CrossRef]
    [Google Scholar]
  89. Kitagawa N, Shiota S, Shibata Y, Takeshita T, Yamashita Y. Characterization of MbrC involved in bacitracin resistance in Streptococcus mutans . FEMS Microbiol Lett 2011; 318:61–67 [CrossRef]
    [Google Scholar]
  90. Basavanna S, Khandavilli S, Yuste J, Cohen JM, Hosie AHF et al. Screening of Streptococcus pneumoniae ABC transporter mutants demonstrates that LivJHMGF, a branched-chain amino acid ABC transporter, is necessary for disease pathogenesis. Infect Immun 2009; 77:3412–3423 [CrossRef]
    [Google Scholar]
  91. Haas W, Kaushal D, Sublett J, Obert C, Tuomanen EI. Vancomycin stress response in a sensitive and a tolerant strain of Streptococcus pneumoniae . J Bacteriol 2005; 187:8205–8210 [CrossRef]
    [Google Scholar]
  92. Bernard R, Joseph P, Guiseppi A, Chippaux M, Denizot F. YtsCD and YwoA, two independent systems that confer bacitracin resistance to Bacillus subtilis . FEMS Microbiol Lett 2003; 228:93–97 [CrossRef]
    [Google Scholar]
  93. Pietiainen M, Gardemeister M, Mecklin M, Leskela S, Sarvas M. Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems. Microbiology 2005; 151:1577–1592 [CrossRef]
    [Google Scholar]
  94. Gardete S, Kim C, Hartmann BM, Mwangi M, Roux CM et al. Genetic pathway in acquisition and loss of vancomycin resistance in a methicillin resistant Staphylococcus aureus (MRSA) strain of clonal type USA300. PLoS Pathog 2012; 8:e1002505 [CrossRef]
    [Google Scholar]
  95. Utaida S et al. Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 2003; 149:2719–2732 [CrossRef]
    [Google Scholar]
  96. Novak R, Henriques B, Charpentier E, Normark S, Tuomanen E. Emergence of vancomycin tolerance in Streptococcus pneumoniae . Nature 1999; 399:590–593 [CrossRef]
    [Google Scholar]
  97. Abachin E, Poyart C, Pellegrini E, Milohanic E, Fiedler F et al. Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes . Mol Microbiol 2002; 43:1–14 [CrossRef]
    [Google Scholar]
  98. Mandin P, Fsihi H, Dussurget O, Vergassola M, Milohanic E et al. VirR, a response regulator critical for Listeria monocytogenes virulence. Mol Microbiol 2005; 57:1367–1380 [CrossRef]
    [Google Scholar]
  99. Kramer NE, van Hijum SAFT, Knol J, Kok J, Kuipers OP. Transcriptome analysis reveals mechanisms by which Lactococcus lactis acquires nisin resistance. Antimicrob Agents Chemother 2006; 50:1753–1761 [CrossRef]
    [Google Scholar]
  100. Ulrich LE, Zhulin IB. The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res 2010; 38:D401–D407 [CrossRef]
    [Google Scholar]
  101. UniProt Consortium Reorganizing the protein space at the universal protein resource (UniProt). Nucleic Acids Res 2012; 40:D71–D75 [CrossRef]
    [Google Scholar]
  102. Choudhury HG, Tong Z, Mathavan I, Li Y, Iwata S et al. Structure of an antibacterial peptide ATP-binding cassette transporter in a novel outward occluded state. Proc Natl Acad Sci U S A 2014; 111:9145–9150 [CrossRef]
    [Google Scholar]
  103. Johnson ZL, Chen J. ATP binding enables substrate release from multidrug resistance protein 1. Cell 2018; 172:81–89 [CrossRef]
    [Google Scholar]
  104. Locher KP. Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat Struct Mol Biol 2016; 23:487–493 [CrossRef]
    [Google Scholar]
  105. ter Beek J, Guskov A, Slotboom DJ. Structural diversity of ABC transporters. J Gen Physiol 2014; 143:419–435 [CrossRef]
    [Google Scholar]
  106. Dawson RJP, Locher KP. Structure of a bacterial multidrug ABC transporter. Nature 2006; 443:180–185 [CrossRef]
    [Google Scholar]
  107. Zutz A, Hoffmann J, Hellmich UA, Glaubitz C, Ludwig B et al. Asymmetric ATP hydrolysis cycle of the heterodimeric multidrug ABC transport complex TmrAB from Thermus thermophilus . J Biol Chem 2011; 286:7104–7115 [CrossRef]
    [Google Scholar]
  108. Singh H, Velamakanni S, Deery MJ, Howard J, Wei SL et al. ATP-dependent substrate transport by the ABC transporter MsbA is proton-coupled. Nat Commun 2016; 7:12387 [CrossRef]
    [Google Scholar]
  109. Perez C, Gerber S, Boilevin J, Bucher M, Darbre T et al. Structure and mechanism of an active lipid-linked oligosaccharide flippase. Nature 2015; 524:433–438 [CrossRef]
    [Google Scholar]
  110. Giesemann T, Guttenberg G, Aktories K. Human alpha-defensins inhibit Clostridium difficile toxin B. Gastroenterology 2008; 134:2049–2058 [CrossRef]
    [Google Scholar]
  111. Boman HG. Antibacterial peptides: key components needed in immunity. Cell 1991; 65:205–207 [CrossRef]
    [Google Scholar]
  112. Hancock RE, Diamond G. The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol 2000; 8:402–410 [CrossRef]
    [Google Scholar]
  113. McBride SM, Sonenshein AL. Identification of a genetic locus responsible for antimicrobial peptide resistance in Clostridium difficile . Infect Immun 2011; 79:167–176 [CrossRef]
    [Google Scholar]
  114. Kuipers OP, Beerthuyzen MM, de Ruyter PG, Luesink EJ, de Vos WM. Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J Biol Chem 1995; 270:27299–27304 [CrossRef]
    [Google Scholar]
  115. Plat A, Kluskens LD, Kuipers A, Rink R, Moll GN. Requirements of the engineered leader peptide of nisin for inducing modification, export, and cleavage. Appl Environ Microbiol 2011; 77:604–611 [CrossRef]
    [Google Scholar]
  116. Gauntlett JC, Gebhard S, Keis S, Manson JM, Pos KM et al. Molecular analysis of BcrR, a membrane-bound bacitracin sensor and DNA-binding protein from Enterococcus faecalis . J Biol Chem 2008; 283:8591–8600 [CrossRef]
    [Google Scholar]
  117. Manson JM, Keis S, Smith JMB, Cook GM. Acquired bacitracin resistance in Enterococcus faecalis is mediated by an ABC transporter and a novel regulatory protein, BcrR. Antimicrob Agents Chemother 2004; 48:3743–3748 [CrossRef]
    [Google Scholar]
  118. Ulrich LE, Koonin EV, Zhulin IB. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol 2005; 13:52–56 [CrossRef]
    [Google Scholar]
  119. Kristich CJ, Wells CL, Dunny GM. A eukaryotic-type Ser/Thr kinase in Enterococcus faecalis mediates antimicrobial resistance and intestinal persistence. Proc Natl Acad Sci U S A 2007; 104:3508–3513 [CrossRef]
    [Google Scholar]
  120. Matos R, Pinto VV, Ruivo M, Lopes MdeFS. Study on the dissemination of the bcrABDR cluster in Enterococcus spp. reveals that the BcrAB transporter is sufficient to confer high-level bacitracin resistance. Int J Antimicrob Agents 2009; 34:142–147 [CrossRef]
    [Google Scholar]
  121. Watkins KL, Shryock TR, Dearth RN, Saif YM. In-vitro antimicrobial susceptibility of Clostridium perfringens from commercial turkey and broiler chicken origin. Vet Microbiol 1997; 54:195–200 [CrossRef]
    [Google Scholar]
  122. Charlebois A, Jalbert LA, Harel J, Masson L, Archambault M. Characterization of genes encoding for acquired bacitracin resistance in Clostridium perfringens . PLoS One 2012; 7:e44449 [CrossRef]
    [Google Scholar]
  123. Rorres C. Local stability of a population with density-dependent fertility. Theor Popul Biol 1979; 16:283–300 [CrossRef]
    [Google Scholar]
  124. Birri DJ, Brede DA, Nes IF. Salivaricin D, a novel intrinsically trypsin-resistant lantibiotic from Streptococcus salivarius 5M6c isolated from a healthy infant. Appl Environ Microbiol 2012; 78:402–410 [CrossRef]
    [Google Scholar]
  125. Pag U, Heidrich C, Bierbaum G, Sahl HG. Molecular analysis of expression of the lantibiotic PEP5 immunity phenotype. Appl Environ Microbiol 1999; 65:591–598
    [Google Scholar]
  126. Stein T, Heinzmann S, Düsterhus S, Borchert S, Entian KD. Expression and functional analysis of the subtilin immunity genes spaIFEG in the subtilin-sensitive host Bacillus subtilis MO1099. J Bacteriol 2005; 187:822–828 [CrossRef]
    [Google Scholar]
  127. Aso Y, Okuda K, Nagao J, Kanemasa Y, Thi Bich Phuong N et al. A novel type of immunity protein, NukH, for the lantibiotic nukacin ISK-1 produced by Staphylococcus warneri ISK-1. Biosci Biotechnol Biochem 2005; 69:1403–1410 [CrossRef]
    [Google Scholar]
  128. Peschel A, Götz F. Analysis of the Staphylococcus epidermidis genes epiF, -E, and -G involved in epidermin immunity. J Bacteriol 1996; 178:531–536 [CrossRef]
    [Google Scholar]
  129. Hyink O, Wescombe PA, Upton M, Ragland N, Burton JP et al. Salivaricin A2 and the novel lantibiotic salivaricin B are encoded at adjacent loci on a 190-kilobase transmissible megaplasmid in the oral probiotic strain Streptococcus salivarius K12. Appl Environ Microbiol 2007; 73:1107–1113 [CrossRef]
    [Google Scholar]
  130. McAuliffe O, O'Keeffe T, Hill C, Ross RP. Regulation of immunity to the two-component lantibiotic, lacticin 3147, by the transcriptional repressor LtnR. Mol Microbiol 2001; 39:982–993 [CrossRef]
    [Google Scholar]
  131. Qi F, Chen P, Caufield PW. Functional analyses of the promoters in the lantibiotic mutacin II biosynthetic locus in Streptococcus mutans . Appl Environ Microbiol 1999; 65:652–658
    [Google Scholar]
  132. Hille M, Kies S, Götz F, Peschel A. Dual role of GdmH in producer immunity and secretion of the staphylococcal lantibiotics gallidermin and epidermin. Appl Environ Microbiol 2001; 67:1380–1383 [CrossRef]
    [Google Scholar]
  133. Heidrich C, Pag U, Josten M, Metzger J, Jack RW et al. Isolation, characterization, and heterologous expression of the novel lantibiotic epicidin 280 and analysis of its biosynthetic gene cluster. Appl Environ Microbiol 1998; 64:3140–3146
    [Google Scholar]
  134. Kuipers OP, Beerthuyzen MM, Siezen RJ, De Vos WM. Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis. Requirement of expression of the nisA and nisI genes for development of immunity. Eur J Biochem 1993; 216:281–291 [CrossRef]
    [Google Scholar]
  135. Kleerebezem M. Quorum sensing control of lantibiotic production; nisin and subtilin autoregulate their own biosynthesis. Peptides 2004; 25:1405–1414 [CrossRef]
    [Google Scholar]
  136. Gomez A, Ladiré M, Marcille F, Fons M. Trypsin mediates growth phase-dependent transcriptional tegulation of genes involved in biosynthesis of ruminococcin a, a lantibiotic produced by a Ruminococcus gnavus strain from a human intestinal microbiota. J Bacteriol 2002; 184:18–28 [CrossRef]
    [Google Scholar]
  137. Kalmokoff ML, Lu D, Whitford MF, Teather RM. Evidence for production of a new lantibiotic (butyrivibriocin OR79A) by the ruminal anaerobe Butyrivibrio fibrisolvens OR79: characterization of the structural gene encoding butyrivibriocin OR79A. Appl Environ Microbiol 1999; 65:2128–2135
    [Google Scholar]
  138. Rao DK, Kaur P. The Q-loop of DrrA is involved in producing the closed conformation of the nucleotide binding domains and in transduction of conformational changes between DrrA and DrrB. Biochemistry 2008; 47:3038–3050 [CrossRef]
    [Google Scholar]
  139. Jones PM, George AM. Mechanism of ABC transporters: a molecular dynamics simulation of a well characterized nucleotide-binding subunit. Proc Natl Acad Sci U S A 2002; 99:12639–12644 [CrossRef]
    [Google Scholar]
  140. Draper LA, Grainger K, Deegan LH, Cotter PD, Hill C et al. Cross-immunity and immune mimicry as mechanisms of resistance to the lantibiotic lacticin 3147. Mol Microbiol 2009; 71:1043–1054 [CrossRef]
    [Google Scholar]
  141. Draper LA, Tagg JR, Hill C, Cotter PD, Ross RP. The spiFEG locus in Streptococcus infantarius subsp. infantarius BAA-102 confers protection against nisin U. Antimicrob Agents Chemother 2012; 56:573–578 [CrossRef]
    [Google Scholar]
  142. Klein C, Entian KD. Genes involved in self-protection against the lantibiotic subtilin produced by Bacillus subtilis ATCC 6633. Appl Environ Microbiol 1994; 60:2793–2801
    [Google Scholar]
  143. Podlesek Z, Comino A, Herzog-Velikonja B, Žgur-Bertok D, Komel R et al. Bacillus licheniformis bacitracin-resistance ABC transporter: relationship to mammalian multidrug resistance. Mol Microbiol 1995; 16:969–976 [CrossRef]
    [Google Scholar]
  144. van der Meer JR, Polman J, Beerthuyzen MM, Siezen RJ, Kuipers OP et al. Characterization of the Lactococcus lactis nisin A operon genes nisP, encoding a subtilisin-like serine protease involved in precursor processing, and nisR, encoding a regulatory protein involved in nisin biosynthesis. J Bacteriol 1993; 175:2578–2588 [CrossRef]
    [Google Scholar]
  145. Koponen O, Tolonen M, Qiao M, Wahlström G, Helin J et al. NisB is required for the dehydration and NisC for the lanthionine formation in the post-translational modification of nisin. Microbiology 2002; 148:3561–3568 [CrossRef]
    [Google Scholar]
  146. Siezen RJ, Kuipers OP, de Vos WM. Comparison of lantibiotic gene clusters and encoded proteins. Antonie Van Leeuwenhoek 1996; 69:171–184 [CrossRef]
    [Google Scholar]
  147. Alkhatib Z, Abts A, Mavaro A, Schmitt L, Smits SHJ. Lantibiotics: how do producers become self-protected?. J Biotechnol 2012; 159:145–154 [CrossRef]
    [Google Scholar]
  148. Qiao M, Ye S, Koponen O, Ra R, Usabiaga M et al. Regulation of the nisin operons in Lactococcus lactis N8. J Appl Bacteriol 1996; 80:626–634 [CrossRef]
    [Google Scholar]
  149. Cheigh CI, Pyun YR. Nisin biosynthesis and its properties. Biotechnol Lett 2005; 27:1641–1648 [CrossRef]
    [Google Scholar]
  150. Nishie M, Sasaki M, Nagao J-ichi, Zendo T, Nakayama J et al. Lantibiotic transporter requires cooperative functioning of the peptidase domain and the ATP binding domain. J Biol Chem 2011; 286:11163–11169 [CrossRef]
    [Google Scholar]
  151. Kiesau P, Eikmanns U, Gutowski-Eckel Z, Weber S, Hammelmann M et al. Evidence for a multimeric subtilin synthetase complex. J Bacteriol 1997; 179:1475–1481 [CrossRef]
    [Google Scholar]
  152. Siegers K, Heinzmann S, Entian KD. Biosynthesis of lantibiotic nisin. Posttranslational modification of its prepeptide occurs at a multimeric membrane-associated lanthionine synthetase complex. J Biol Chem 1996; 271:12294–12301 [CrossRef]
    [Google Scholar]
  153. Kuipers A, de Boef E, Rink R, Fekken S, Kluskens LD et al. NisT, the transporter of the lantibiotic nisin, can transport fully modified, dehydrated, and unmodified prenisin and fusions of the leader peptide with non-lantibiotic peptides. J Biol Chem 2004; 279:22176–22182 [CrossRef]
    [Google Scholar]
  154. Håvarstein LS, Diep DB, Nes IF. A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol Microbiol 1995; 16:229–240 [CrossRef]
    [Google Scholar]
  155. Sun Z, Zhong J, Liang X, Liu J, Chen X et al. Novel mechanism for nisin resistance via proteolytic degradation of nisin by the nisin resistance protein NSR. Antimicrob Agents Chemother 2009; 53:1964–1973 [CrossRef]
    [Google Scholar]
  156. Khosa S, Frieg B, Mulnaes D, Kleinschrodt D, Hoeppner A et al. Structural basis of lantibiotic recognition by the nisin resistance protein from Streptococcus agalactiae . Sci Rep 2016; 6:18679 [CrossRef]
    [Google Scholar]
  157. Laurentaci G. Chloramphenicol and immunological response of lymph nodes to cutaneous burns. Allergol 1967; 14:592–596
    [Google Scholar]
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