Bacteriocins-a viable alternative to antibiotics?

Nature Reviews Microbiology

Volumn 11, Issue 2, 2013, Pages 95-105

  Cotter, Paul D ^a,b   Ross, R Paul ^a,b   Hill, Colin ^b,c  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANACYCLAMIDE LIKE CYANOBACTIN; BACTERIOCIN; BOTTROMYCIN; CYANOBACTIN; GLYCOCIN; LANTIBIOTIC; LFF 571; LINARIDIN; METRONIDAZOLE; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; NISIN; PATELLAMIDE LIKE CYANOBACTIN; PRAMICONAZOLE; PROBIOTIC AGENT; PROTEUSIN; PYRROLE; SACTIBIOTIC; THIOPEPTIDE; THURICIN; UNCLASSIFIED DRUG; VANCOMYCIN;

BIOENGINEERING; CLOSTRIDIUM DIFFICILE INFECTION; DRUG ACTIVITY; DRUG CLASSIFICATION; DRUG MECHANISM; DRUG POTENCY; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LACTIC ACID BACTERIUM; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIOCINS; DRUG RESISTANCE, BACTERIAL;

EID: 84872488958     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro2937     Document Type: Review

References (161)

1. White, A. R. Effective antibacterials: at what cost? The economics of antibacterial resistance and its control. J. Antimicrob. Chemother. 66, 1948-1953 (2011).
2. Cooper, M. A. & Shlaes, D. Fix the antibiotics pipeline. Nature 472, 32 (2011).
3. Blaser, M. Antibiotic overuse: stop the killing of beneficial bacteria. Nature 476, 393-394 (2011).
4. Willing, B. P., Russell, S. L & Finlay, B. B. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nature Rev. Microbiol. 9, 233-243 (2011).
5. Cotter, P. D., Stanton, C., Ross, R. P. & Hill, C The impact of antibiotics on the gut microbiota as revealed by high throughput DNA sequencing. Discov. Med. 13, 193-199 (2012).
6. Savoia, D. Plant-derived antimicrobial compounds: alternatives to antibiotics. Future Microbiol. 7, 979-990 (2012).
7. Burrowes, B., Harper, D. R., Anderson, J., McConville, M. & Enright, M. C Bacteriophage therapy: potential uses in the control of antibiotic-resistant pathogens. Expert Rev. Anti Infect. Ther. 9, 775-785 (2011).
8. Kole, R., Krainer, A. R. & Altman, S. RNA therapeutics: beyond RNA interference and antisense oligonucleotides. Nature Rev. Drug Discov. 11, 125-140 (2012).
9. Shanahan, F Probiotics in perspective. Gastroenterology 139, 1808-1812 (2010).
10. Li, Y., Xiang, Q., Zhang, Q., Huang, Y & Su, Z. Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides 37, 207-215 (2012).
11. Cotter, P. D., Hill, C & Ross, R. P. Bacteriocins: developing innate immunity for food. Nature Rev. Microbiol. 3, 777-788 (2005).
12. Rea, M. C et al. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc Natl Acad. Sci. USA 107, 9352-9357 (2010).
13. Boakes, S. et al. Generation of an actagardine A variant library through saturation mutagenesis. Appl. Microbiol. Biotechnol. 95, 1509-1517 (2012).
14. Svetoch, E. A. & Stern, N. J. Bacteriocins to control Campylobacter spp. in poultry\-a review. Poult Sci. 89, 1763-1768 (2010).
15. Desriac, F et al. Bacteriocin as weapons in the marine animal-associated bacteria warfare: inventory and potential applications as an aquaculture probiotic Mar. Drugs 8, 1153-1177 (2010).
16. Piper, C., Cotter, P. D., Ross, R. P. & Hill, C Discovery of medically significant lantibiotics. Curr. Drug Discov. Technol. 6, 1-18 (2009).
17. Zhang, C et al. Thiazomycins, thiazolyl peptide antibiotics from Amycolatopsis fastidiosa. J. Nat. Prod. 72, 841-847 (2009).
18. Zhang, C et al. Isolation, structure, and antibacterial activity of philipimycin, a thiazolyl peptide discovered from Actinoplanes philippinensis MA7347. J. Am. Chem. Soc 130, 12102-121 10 (2008).
19. Singh, S. B. et al. Antibacterial evaluations of thiazomycin \- a potent thiazolyl peptide antibiotic from Amycolatopsis fastidiosa. J. Antibiot 60, 565-571 (2007).
20. Morris, R. P. et al. Ribosomally synthesized thiopeptide antibiotics targeting elongation factor Tu. J. Am. Chem. Soc 131, 5946-5955 (2009).
21. Leeds, J. A., Sachdeva, M., Mullin, S., Dzink-Fox, J. & Lamarche, M. J. Mechanism of action of, and mechanism of reduced susceptibility to the novel anti-Clostridium difficile compound LFF571. Antimicrob. Agents Chemother. 56, 4463-4465 (2012).
22. Shelburne, C E. et al. The spectrum of antimicrobial activity of the bacteriocin subtilosin A. J. Antimicrob. Chemother. 59, 297-300 (2007).
23. Noll, K. S., Sinko, P. J. & Chikindas, M. L. Elucidation of the molecular mechanisms of action of the natural antimicrobial peptide subtilosin against the bacterial vaginosis-associated pathogen Gardnerella vaginalis. Probiotics Antimicrob. Proteins 3, 41-47 (2011).
24. Paik, S. H., Chakicherla, A. & Hansen, J. N. Identification and characterization of the structural and transporter genes for, and the chemical and biological properties of, sublancin 168, a novel lantibiotic produced by Bacillus subtilis 168. J. Biol. Chem. 273, 23134-23142 (1998).
25. Freeman, M. F et al. Metagenome mining reveals polytheonamides as posttranslationally modified ribosomal peptides. Science 338, 387-390 (2012).
26. Kobayashi, Y. et al. Bottromycin derivatives: efficient chemical modifications of the ester moiety and evaluation of anti-MRSA and anti-VRE activities. Bioorg. Med. Chem. Lett. 20, 6116-6120 (2010).
27. Eijsink, V. G., Skeie, M., Middelhoven, P. H., Brurberg, M. B. & Nes, I. F Comparative studies of class IIa bacteriocins of lactic acid bacteria. Appl. Environ. Microbiol. 64, 3275-3281 (1998).
28. Drider, D., Fimland, G., Hechard, Y, McMullen, L M. & Prevost, H. The continuing story of class IIa bacteriocins. Microbiol. Mol. Biol. Revs 70, 564-582 (2006).
29. Sanchez-Hidalgo, M. et al. AS-48 bacteriocin: close to perfection. Cell. Mol. Life Sci. 68, 2845-2857 (2011).
30. Sandiford, S. & Upton, M. Identification, characterization, and recombinant expression of epidermicin NI01, a novel unmodified bacteriocin produced by Staphylococcus epidermidis that displays potent activity against staphylococci. Antimicrob. Agents Chemother. 56, 1539-1547 (2012).
31. Garcia-Bustos, J. F, Pezzi, N. & Mendez, E. Structure and mode of action of microcin 7, an antibacterial peptide produced by Escherichia coli. Antimicrob. Agents Chemother. 27, 791-797 (1985).
32. 16 ß-hairpin region in the recognition mechanism. Biochem. J. 389, 869-876 (2005).
33. Soudy, R., Wang, L & Kaur, K. Synthetic peptides derived from the sequence of a lasso peptide microcin J25 show antibacterial activity. Bioorg. Med. Chem. 20, 1794-1800 (2012).
34. Asensio, C & Perez-Diaz, J. C A new family of low molecular weight antibiotics from enterobacteria. Biochem. Biophys. Res. Commun. 69, 7-14 (1976).
35. Baquero, F. & Moreno, F. The microcins. FEMS Microbiol. Lett. 23, 117-124 (1984).
36. Havarstein, L S., Holo, H. & Nes, I. F. The leader peptide of colicin V shares consensus sequences with leader peptides that are common among peptide bacteriocins produced by Gram-positive bacteria. Microbiology 140, 2383-2389 (1994).
37. Pons, A. M. et al. Genetic analysis and complete primary structure of microcin L Antimicrob. Agents Chemother. 48, 505-513 (2004).
38. Thomas, X. et al. Siderophore peptide, a new type of post-translationally modified antibacterial peptide with potent activity. J. Biol. Chem. 279, 28233-28242 (2004).
39. Vassiliadis, G., Destoumieux-Garzon, D., Lombard, C., Rebuffat, S. & Peduzzi, J. Isolation and characterization of two members of the siderophore-microcin family, microcins M and H47. Antimicrob. Agents Chemother. 54, 288-297 (2010).
40. Kuwano, K. et al. Dual antibacterial mechanisms of nisin Z against Gram-positive and Gram-negative bacteria. Int. J. Antimicrob. Agents 26, 396-402 (2005).
41. Morency, H., Mota-Meira, M., LaPointe, G., Lacroix, C & Lavoie, M. C Comparison of the activity spectra against pathogens of bacterial strains producing a mutacin or a lantibiotic Can. J. Microbiol. 47, 322-331 (2001).
42. Svetoch, E. A. et al. Inactivating methicillin-resistant Staphylococcus aureus and other pathogens by use of bacteriocins OR-7 and E 50-52. J. Clin. Microbiol. 46, 3863-3865 (2008).
43. Giacometti, A., Cirioni, O., Barchiesi, F. & Scalise, G. In?vitro activity and killing effect of polycationic peptides on methicillin-resistant Staphylococcus aureus and interactions with clinically used antibiotics. Diagn. Microbiol. Infect. Dis. 38, 115-118 (2000).
44. Brumfitt, W., Salton, M. R. & Hamilton-Miller, J. M. Nisin, alone and combined with peptidoglycan-modulating antibiotics: activity against methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci. J. Antimicrob. Chemother 50, 731-734 (2002).
45. Pomares, M. F., Delgado, M. A., Corbalan, N. S., Farias, R. N. & Vincent, P. A. Sensitization of microcin J25-resistant strains by a membrane-permeabilizing peptide. Appl. Environ. Microbiol. 76, 6837-6842 (2010).
46. Salvucci, E., Hebert, E. M., Sesma, F. & Saavedra, L Combined effect of synthetic enterocin CRL35 with cell wall, membrane-acting antibiotics and muranolytic enzymes against Listeria cells. Lett. Appl. Microbiol. 51, 191-195 (2010).
47. Noll, K. S., Prichard, M. N., Khaykin, A., Sinko, P. J. & Chikindas, M. L. The natural antimicrobial peptide subtilosin acts synergistically with glycerol monolaurate, lauric arginate, and ε-poly-L-lysine against bacterial vaginosis-associated pathogens but not human lactobacilli. Antimicrob. Agents Chemother 56, 1756-1761 (2012).
48. Fontana, M. B., de Bastos Mdo, C & Brandelli, A. Bacteriocins Pep5 and epidermin inhibit Staphylococcus epidermidis adhesion to catheters. Curr Microbiol. 52, 350-353 (2006).
49. Goldstein, B. P, Wei, J., Greenberg, K. & Novick, R. Activity of nisin against Streptococcus pneumoniae, in vitro, and in a mouse infection model. J. Antimicrob. Chemother 42, 277-278 (1998).
50. van Staden, A. D., Brand, A. M. & Dicks, L M. Nisin F-loaded brushite bone cement prevented the growth of Staphylococcus aureus in vivo. J. Appl. Microbiol. 11 2, 831-840 (2012).
51. De Kwaadsteniet, M., Doeschate, K. T & Dicks, L M. Nisin F in the treatment of respiratory tract infections caused by Staphylococcus aureus. Lett. Appl. Microbiol. 48, 65-70 (2009).
52. Brand, A. M., de Kwaadsteniet, M. & Dicks, L M. The ability of nisin F to control Staphylococcus aureus infection in the peritoneal cavity, as studied in mice. Lett. Appl. Microbiol. 51, 645-649 (2010).
53. Mota-Meira, M., Morency, H. & Lavoie, M. C In vivo activity of mutacin B-Ny266. J. Antimicrob. Chemother. 56, 869-871 (2005).
54. Chatterjee, S. et al. Mersacidin, a new antibiotic from Bacillus. In vitro and in vivo antibacterial activity. J. Antibiot (Tokyo) 45, 839-845 (1992).
55. Kruszewska, D. et al. Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model. J. Antimicrob. Chemother 54, 648-653 (2004).
56. Niu, W. W. & Neu, H. C Activity of mersacidin, a novel peptide, compared with that of vancomycin, teicoplanin, and daptomycin. Antimicrob. Agents Chemother 35, 998-1000 (1991).
57. Castiglione, F. et al. A novel lantibiotic acting on bacterial cell wall synthesis produced by the uncommon actinomycete Planomonospora sp. Biochemistry 46, 5884-5895 (2007).
58. Haste, N. M. et al. Activity of the thiopeptide antibiotic nosiheptide against contemporary strains of methicillin-resistant Staphylococcus aureus. J. Antibiot. (Tokyo) 10 Oct 2012 (doi:10.1038/ ja.2012.77).
59. Xu, L et al. Nocathiacin analogs: synthesis and antibacterial activity of novel water-soluble amides. Bioorg. Med. Chem. Lett 19, 3531-3535 (2009).
60. Trzasko, A., Leeds, J. A., Praestgaard, J., Lamarche, M. J. & McKenney, D. The efficacy of LFF571 in the hamster model of Clostridium difficile infection. Antimicrob. Agents Chemother 56, 4459-4462 (2012).
61. Rihakova, J. et al. In vivo activities of recombinant divercin V41 and its structural variants against Listeria monocytogenes. Antimicrob. Agents Chemother 54, 563-564 (2010).
62. Salvucci, E., Saavedra, L., Hebert, E. M., Haro, C & Sesma, F. Enterocin CRL35 inhibits Listeria monocytogenes in a murine model. Foodborne Pathog. Dis. 9, 68-74 (2012).
63. Sosunov, V. et al. Antimycobacterial activity of bacteriocins and their complexes with liposomes. J. Antimicrob. Chemother 59, 919-925 (2007).
64. Lopez, F. E., Vincent, P. A., Zenoff, A. M., Salomon, R. A. & Farias, R. N. Efficacy of microcin J25 in biomatrices and in a mouse model of Salmonella infection. J. Antimicrob. Chemother 59, 676-680 (2007).
65. Maher, S. & McClean, S. Investigation of the cytotoxicity of eukaryotic and prokaryotic antimicrobial peptides in intestinal epithelial cells in vitro. Biochem. Pharmacol. 71, 1289-1298 (2006).
66. Cox, C R., Coburn, P. S. & Gilmore, M. S. Enterococcal cytolysin: a novel two component peptide system that serves as a bacterial defense against eukaryotic and prokaryotic cells. Curr Protein Pept. Sci. 6, 77-84 (2005).
67. Sivonen, K., Leikoski, N., Fewer, D. P. & Jokela, J. Cyanobactins\-ribosomal cyclic peptides produced by cyanobacteria. Appl. Microbiol. Biotechnol. 86, 12 13-1225 (2010).
68. Murinda, S. E., Rashid, K. A. & Roberts, R. F. In vitro assessment of the cytotoxicity of nisin, pediocin, and selected colicins on simian virus 40-transfected human colon and Vero monkey kidney cells with trypan blue staining viability assays. J. Food Prot. 66, 847-853 (2003).
69. Jasniewski, J., Cailliez-Grimal, C., Chevalot, I., Milliere, J. B. & Revol-Junelles, A. M. Interactions between two carnobacteriocins Cbn BM1 and Cbn B2 from Carnobacterium maltaromaticum CP5 on target bacteria and Caco-2 cells. Food Chem. Toxicol. 47, 893-897 (2009).
70. Hetz, C., Bono, M. R., Barros, L F. & Lagos, R. Microcin E492, a channel-forming bacteriocin from Klebsiella pneumoniae, induces apoptosis in some human cell lines. Proc. Natl Acad. Sci. USA 99, 2696-2701 (2002).
71. Lagos, R., Tello, M., Mercado, G., Garcia, V. & Monasterio, O. Antibacterial and antitumorigenic properties of microcin E492, a pore-forming bacteriocin. Curr Pharm. Biotechnol. 10, 74-85 (2009).
72. Nelson, R. L et al. Antibiotic treatment for Clostridium difficile-associated diarrhea in adults. Cochrane Database Syst Rev. 7 Sep 2011 (doi:10.1002/14651858. CD004610.pub4).
73. Rea, M. C et al. Effect of broad- and narrow-spectrum antimicrobials on Clostridium difficile and microbial diversity in a model of the distal colon. Proc. Natl Acad. Sci. USA 108 (Suppl. 1), 4639-4644 (2011).
74. Dabour, N., Zihler, A., Kheadr, E., Lacroix, C & Fliss, I. In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes. Int. J. Food Microbiol. 133, 225-233 (2009).
75. Le Blay, G., Lacroix, C., Zihler, A. & Fliss, I. In vitro inhibition activity of nisin A, nisin Z, pediocin PA-1 and antibiotics against common intestinal bacteria. Lett. Appl. Microbiol. 45, 252-257 (2007).
76. Bernbom, N. et al. Pediocin PA-1 and a pediocin producing Lactobacillus plantarum strain do not change the HMA rat microbiota. Int. J. Food Microbiol. 130, 251-257 (2009).
77. Sutyak, K. E., Wirawan, R. E., Aroutcheva, A. A. & Chikindas, M. L Isolation of the Bacillus subtilis antimicrobial peptide subtilosin from the dairy product-derived Bacillus amyloliquefaciens. J. Appl. Microbiol. 104, 1067-1074 (2008).
78. McCormick, B. A., Franklin, D. P, Laux, D. C & Cohen, P. S. Type 1 pili are not necessary for colonization of the streptomycin-treated mouse large intestine by type 1 -piliated Escherichia coli F-18 and E. coli K-12. Infect Immun. 57, 3022-3029 (1989).
79. Dobson, A., Cotter, P. D., Ross, R. P. & Hill, C Bacteriocin production: a probiotic trait? Appl. Environ. Microbiol. 78, 1-6 (2012).
80. O'Shea, E. F., Cotter, P. D., Stanton, C., Ross, R. P. & Hill, C Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid. Int. J. Food Microbiol. 152, 189-205 (2012).
81. Su, P., Henriksson, A. & Mitchell, H. Prebiotics enhance survival and prolong the retention period of specific probiotic inocula in an in vivo murine model. J. Appl. Microbiol. 103, 2392-2400 (2007).
82. Su, P., Henriksson, A. & Mitchell, H. Survival and retention of the probiotic Lactobacillus casei LAFTI L26 in the gastrointestinal tract of the mouse. Lett. Appl. Microbiol. 44, 120-125 (2007).
83. Gotteland, M. et al. Modulation of Helicobacter pylori colonization with cranberry juice and Lactobacillus johnsonii La1 in children. Nutrition 24, 421-426 (2008).
84. Casey, P. G. et al. A five-strain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs challenged with Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 73, 1858-1863 (2007).
85. Walsh, M. C et al. Predominance of a bacteriocin-producing Lactobacillus salivarius component of a five-strain probiotic in the porcine ileum and effects on host immune phenotype. FEMS Microbiol. Ecol. 64, 317-327 (2008).
86. Corr, S. C et al. Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Natl Acad. Sci. USA 104, 7617-7621 (2007).
87. O'Callaghan, J., Butto, L F., Macsharry, J., Nally, K. & OToole, P. W. Adhesion and bacteriocin production by Lactobacillus salivarius influence the intestinal epithelial cell transcriptional response. Appl. Environ. Microbiol. 78, 5196-5203 (2012).
88. Millette, M. et al. Capacity of human nisin- and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci. Appl. Environ. Microbiol. 74, 1997-2003 (2008).
89. Zschuttig, A. et al. Identification and characterization of microcin S, a new antibacterial peptide produced by probiotic Escherichia coli G3/10. PLoS ONE 7, e33351 (2012).
90. Hillman, J. D., Mo, J., McDonell, E., Cvitkovitch, D. & Hillman, C H. Modification of an effector strain for replacement therapy of dental caries to enable clinical safety trials. J. Appl. Microbiol. 102, 1209-1219 (2007).
91. Hillman, J. D. Genetically modified Streptococcus mutans for the prevention of dental caries. Antonie Van Leeuwenhoek 82, 361-366 (2002).
92. Burton, J. P., Chilcott, C N., Moore, C J., Speiser, G. & Tagg, J. R. A preliminary study of the effect of probiotic Streptococcus salivarius K12 on oral malodour parameters. J. Appl. Microbiol. 100, 754-764 (2006).
93. Tagg, J. R. Prevention of streptococcal pharyngitis by anti- Streptococcus pyogenes bacteriocin-like inhibitory substances (BLIS) produced by Streptococcus salivarius. Indian J. Med. Res. 119 (Suppl.), 13-16 (2004).
94. Dover, S. E., Aroutcheva, A. A., Faro, S. & Chikindas, M. L Natural antimicrobials and their role in vaginal health: a short review Int. J. Probiotics Prebiotics 3, 2 19-230 (2008).
95. Wang, Z. et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57-63 (2011).
96. Sekirov, I., Russell, S. L., Antunes, L. C & Finlay, B. B. Gut microbiota in health and disease. Physiol. Rev. 90, 859-904 (2010).
97. Murphy, E. F. et al. Divergent metabolic outcomes arising from targeted manipulation of the gut microbiota in diet-induced obesity. Gut 16 Feb 2012 (doi:10.1136/gutjnl-2011-300705).
98. Riboulet-Bisson, E. et al. Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota. PLoS ONE 7, e31113 (2012).
99. Meijerink, M. et al. Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS ONE 5, e10632 (2010).
100. van Hemert, S. et al. Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiol. 10, 293 (2010).
101. Levengood, M. R., Knerr, P. J., Oman, T. J. & van der Donk, W. A. In vitro mutasynthesis of lantibiotic analogues containing nonproteinogenic amino acids. J. Am. Chem. Soc 131, 12024-12025 (2009).
102. Field, D., Hill, C., Cotter, P. D. & Ross, R. P. The dawning of a 'Golden era' in lantibiotic bioengineering. Mol. Microbiol. 78, 1077-1087 (2010).
103. Ross, A. C., McKinnie, S. M. & Vederas, J. C The synthesis of active and stable diaminopimelate analogues of the lantibiotic peptide lactocin S. J. Am. Chem. Soc 134, 2008-2011 (2012).
104. Arnusch, C J. et al. The vancomycin-nisin(1-12) hybrid restores activity against vancomycin resistant enterococci. Biochemistry 47, 12661-12663 (2008).
105. Citron, D. M., Tyrrell, K. L., Merriam, C V. & Goldstein, E. J. Comparative in vitro activities of LFF571 against Clostridium difficile and 630 other intestinal strains of aerobic and anaerobic bacteria. Antimicrob. Agents Chemother. 56, 2493-2503 (2012).
106. Zamble, D. B. et al. In vitro characterization of DNA gyrase inhibition by microcin B17 analogs with altered bisheterocyclic sites. Proc Natl Acad. Sci. USA 98, 7712-7717 (2001).
107. Van de Vijver, P. et al. Synthetic microcin C analogs targeting different aminoacyl-tRNA synthetases. J. Bacteriol. 191, 6273-6280 (2009).
108. Lohans, C T. & Vederas, J. C Development of Class IIa bacteriocins as therapeutic agents. Int. J. Microbiol. 2012, 386410 (2012).
109. Fimland, G. et al. A C-terminal disulfide bridge in pediocin-like bacteriocins renders bacteriocin activity less temperature dependent and is a major determinant of the antimicrobial spectrum. J. Bacteriol. 182, 2643-2648 (2000).
110. Tominaga, T & Hatakeyama, Y Development of innovative pediocin PA-1 by DNA shuffling among class IIa bacteriocins. Appl. Environ. Microbiol. 73, 5292-5299 (2007).
111. Kazazic, M., Nissen-Meyer, J. & Fimland, G. Mutational analysis of the role of charged residues in target-cell binding, potency and specificity of the pediocin-like bacteriocin sakacin P. Microbiology 148, 2019-2027 (2002).
112. O'Shea, E. F, O'Connor, P. M., Cotter, P. D., Ross, R. P. & Hill, C Synthesis of trypsin-resistant variants of the Listeria-active bacteriocin salivaricin P. Appl. Environ. Microbiol. 76, 5356-5362 (2010).
113. Velasquez, J. E. & van der Donk, W. A. Genome mining for ribosomally synthesized natural products. Curr. Opin. Chem. Biol. 15, 11-21 (2011).
114. Begley, M., Cotter, P. D., Hill, C & Ross, R. P. Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl. Environ. Microbiol. 75, 5451-5460 (2009).
115. Marsh, A. J., O'Sullivan, O., Ross, R. P, Cotter, P. D. & Hill, C In silico analysis highlights the frequency and diversity of type 1 lantibiotic gene clusters in genome sequenced bacteria. BMC Genomics 11, 679 (2010).
116. Wieland Brown, L C. Acker, M. G., Clardy, J., Walsh, C T & Fischbach, M. A. Thirteen posttranslational modifications convert a 14-residue peptide into the antibiotic thiocillin. Proc Natl Acad. Sci. USA 106, 2549-2553 (2009).
117. Li, J. et al. ThioFinder: a web-based tool for the identification of thiopeptide gene clusters in DNA sequences. PLoS ONE 7, e45878 (2012).
118. Claesen, J. & Bibb, M. Genome mining and genetic analysis of cypemycin biosynthesis reveal an unusual class of posttranslationally modified peptides. Proc. Natl Acad. Sci. USA 107, 16297-16302 (2010).
119. Stepper, J. et al. Cysteine S-glycosylation, a new post-translational modification found in glycopeptide bacteriocins. FEBS Lett. 585, 645-650 (2011).
120. Wang, H., Fewer, D. P. & Sivonen, K. Genome mining demonstrates the widespread occurrence of gene clusters encoding bacteriocins in cyanobacteria. PLoS ONE 6, e22384 (2011).
121. Kjos, M. et al. Target recognition, resistance, immunity and genome mining of class II bacteriocins from Gram-positive bacteria. Microbiology 157, 3256-3267 (2011).
122. Garg, N., Tang, W., Goto, Y., Nair, S. K. & van der Donk, W. A. Lantibiotics from Geobacillus thermodenitrificans. Proc Natl Acad. Sci. USA 109, 5241-5246 (2012).
123. Majchrzykiewicz, J. A. et al. Production of a class II two-component lantibiotic of Streptococcus pneumoniae using the class I nisin synthetic machinery and leader sequence. Antimicrob. Agents Chemother. 54, 1498-1505 (2010).
124. Bierbaum, G. & Sahl, H. G. Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm. Biotechnol. 10, 2-18 (2009).
125. Martin, N. I. & Breukink, E. Expanding role of lipid II as a target for lantibiotics. Future Microbiol. 2, 513-525 (2007).
126. Piper, C., Draper, L A., Cotter, P. D., Ross, R. P. & Hill, C A comparison of the activities of lacticin 3147 and nisin against drug-resistant Staphylococcus aureus and Enterococcus species. J. Antimicrob. Chemother. 64, 546-551 (2009).
127. Diep, D. B., Skaugen, M., Salehian, Z., Holo, H. & Nes, I. F Common mechanisms of target cell recognition and immunity for class II bacteriocins. Proc Natl Acad. Sci. USA 104, 2384-2389 (2007).
128. Destoumieux-Garzon, D., Peduzzi, J., Thomas, X., Djediat, C & Rebuffat, S. Parasitism of iron-siderophore receptors of Escherichia coli by the siderophore-peptide microcin E492m and its unmodified counterpart. Biometals 19, 181-191 (2006).
129. Marki, F, Hanni, E., Fredenhagen, A. & van Oostrum, J. Mode of action of the lanthionine-containing peptide antibiotics duramycin, duramycin B and C, and cinnamycin as indirect inhibitors of phospholipase A2. Biochem. Pharmacol. 42, 2027-2035 (1991).
130. Kouwen, T R. et al. The large mechanosensitive channel MscL determines bacterial susceptibility to the bacteriocin sublancin 168. Antimicrob. Agents Chemother. 53, 4702-4711 (2009).
131. Parks, W M., Bottrill, A. R., Pierrat, O. A., Durrant, M. C & Maxwell, A. The action of the bacterial toxin, microcin B17, on DNA gyrase. Biochimie 89, 500-507 (2007).
132. Vincent, P. A. & Morero, R. D. The structure and biological aspects of peptide antibiotic microcin J25. Curr Med. Chem. 16, 538-549 (2009).
133. Novikova, M. et al. The Escherichia coli Yej transporter is required for the uptake of translation inhibitor microcin C. J. Bacteriol. 189, 8361-8365 (2007).
134. Kazakov, T. et al. Escherichia coli peptidase A, B, or N can process translation inhibitor microcin C J. Bacteriol. 190, 2607-2610 (2008).
135. Metlitskaya, A. et al. Aspartyl-tRNA synthetase is the target of peptide nucleotide antibiotic microcin C J. Biol. Chem. 281, 18033-18042 (2006).
136. Bagley, M. C., Dale, J. W., Merritt, E. A. & Xiong, X. Thiopeptide antibiotics. Chem. Rev. 105, 685-714 (2005).
137. Collins, B., Curtis, N., Cotter, P. D., Hill, C & Ross, R. P. The ABC transporter AnrAB contributes to the innate resistance of Listeria monocytogenes to nisin, bacitracin, and various ß-lactam antibiotics. Antimicrob. Agents Chemother. 54, 4416-4423 (2010).
138. Kramer, N. E., van Hijum, S. A., Knol, J., Kok, J. & Kuipers, O. P. Transcriptome analysis reveals mechanisms by which Lactococcus lactis acquires nisin resistance. Antimicrob. Agents Chemother. 50, 1753-1761 (2006).
139. Kjos, M., Nes, I. F & Diep, D. B. Mechanisms ofesistance to bacteriocins targeting the mannose phosphotransferase system. Appl. Environ. Microbiol. 77, 3335-3342 (2011).
140. Yuzenkova, J. et al. Mutations of bacterial RNA polymerase leading to resistance to microcin J25. J. Biol. Chem. 277, 50867-50875 (2002).
141. Del Castillo, F J., del Castillo, I. & Moreno, F Construction and characterization of mutations at codon 751 of the Escherichia coli gyrB gene that confer resistance to the antimicrobial peptide microcin B17 and alter the activity of DNA gyrase. J. Bacteriol. 183, 2137-2140 (2001).
142. Baumann, S. et al. Molecular determinants of microbial resistance to thiopeptide antibiotics. J. Am. Chem. Soc 132, 6973-6981 (2010).
143. Draper, L. A. et al. Cross-immunity and immune mimicry as mechanisms of resistance to the lantibiotic lacticin 3147. Mol. Microbiol. 71, 1043-1054 (2009).
144. Sun, Z. et al. Novel mechanism for nisin resistance via proteolytic degradation of nisin by the nisin resistance protein NSR. Antimicrob. Agents Chemother. 53, 1964-1973 (2009).
145. Nocek, B. et al. Structural and functional characterization of microcin C resistance peptidase MccF from Bacillus anthracis. J. Mol. Biol. 420, 366-383 (2012).
146. Butcher, B. G. & Helmann, J. D. Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by bacilli. Mol. Microbiol. 60, 765-782 (2006).
147. Rink, R. et al. To protect peptide pharmaceuticals against peptidases. J. Pharmacol. Toxicol. Methods 61, 2 10-2 18 (2010).
148. Febbraro, S., Hancock, A., Boyd, A. & Dawson, M. J. A phase I, double-blind, randomised, placebo-controlled, dose escalating study to assess the safety, tolerability, and pharmacokinetics of single and multiple doses of NVB302 administered orally to healthy volunteers. 52nd Interscience Conference on Antimicrobial Agents and Chemotherapy, 2012. Abstract F-1540c (http://www. icaac.org/images/icaac 2012 finalprogram web4a.pdf).
149. Donadio, S., Maffioli, S., Monciardini, P, Sosio, M. & Jabes, D. Sources of novel antibiotics\-aside the common roads. Appl. Microbiol. Biotechnol. 88, 1261-1267 (2010).
150. Duquesne, S., Destoumieux-Garzon, D., Peduzzi, J. & Rebuffat, S. Microcins, gene-encoded antibacterial peptides from enterobacteria. Nat. Prod. Rep. 24, 708-734 (2007).
151. Arnison, P. G. et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod. Rep. 19 Nov 2012 (doi:10.1039/C2NP20085F).
152. Willey, J. M. & van der Donk, W. A. Lantibiotics: peptides of diverse structure and function. Annu. Rev. Microbiol. 61, 477-501 (2007).
153. Melby, J. O., Nard, N. J. & Mitchell, D. A. Thiazole/ oxazole-modified microcins: complex natural products from ribosomal templates. Curr Opin. Chem. Biol. 15, 369-378 (2011).
154. Li, C & Kelly, W. L Recent advances in thiopeptide antibiotic biosynthesis. Nat Prod. Rep. 27, 153-164 (2010).
155. Knappe, T. A., Linne, U., Xie, X. & Marahiel, M. A. The glucagon receptor antagonist BI-32169 constitutes a new class of lasso peptides. FEBS Lett. 584, 785-789 (2010).
156. Murphy, K. et al. Genome mining for radical SAM protein determinants reveals multiple sactibiotic-like gene clusters. PLoS ONE 6, e20852 (2011).
157. Hou, Y et al. Structure and biosynthesis of the antibiotic bottromycin d. Org. Lett. 14, 5050-5053 (2012).
158. Hsieh, Y S. et al. Synthesis of the bacteriocin glycopeptide sublancin 168 and S-glycosylated variants. Org. Lett. 14, 1910-1913 (2012).
159. Oman, T. J., Boettcher, J. M., Wang, H., Okalibe, X. N. & van der Donk, W. A. Sublancin is not a lantibiotic but an S-linked glycopeptide. Nature Chem. Biol. 7, 78-80 (2011).
160. Severinov, K. & Nair, S. K. Microcin C: biosynthesis and mechanisms of bacterial resistance. Future Microbiol. 7, 281-289 (2012).
161. Leikoski, N. et al. Highly diverse cyanobactins in strains of the genus Anabaena. Appl. Environ. Microbiol. 76, 701-709 (2010).