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The Cyclic Lipopeptide Antibiotics

Chapter
Part of the Topics in Medicinal Chemistry book series (TMC, volume 26)

Abstract

The cyclic lipopeptides comprise a number of clinically relevant classes of antibiotics that date back from the discovery of the polymyxins in 1947 to the recent introduction of the semi-synthetic lipoglycopeptides. These natural products and natural product derivatives most often originate from soil-inhabiting and/or plant-derived producing organisms. The cyclic lipopeptides consist of peptide macrocycles that are acylated with a fatty acid lipid, and show great structural diversity owing to their nearly exclusive non-ribosomal synthesis production and/or post-translational modification. This review presents a summary of the main classes of cyclic lipopeptide antibiotics with regard to their characteristic structural features, modes of action, clinical relevance, and the onset of bacterial resistance.

Keywords

Bacitracin Colistin Daptomycin Lantibiotics Lipopeptides Mode of action Polymyxin Ramoplanin Resistance Teicoplanin Teixobactin 

Notes

Statement of Clarity

L. H. J. Kleijn and N. I. Martin declare competing financial interests as both authors are co-founders of Karveel Pharmaceuticals.

References

  1. 1.
    Dexter AF, Middelberg APJ (2008) Peptides as functional surfactants. Ind Eng Chem Res 47:6391–6398. doi: 10.1021/ie800127fCrossRefGoogle Scholar
  2. 2.
    Rosenberg E, Ron EZ (1999) High- and low-molecular-mass microbial surfactants. Appl Microbiol Biotechnol 52:154–162. doi: 10.1007/s002530051502CrossRefPubMedGoogle Scholar
  3. 3.
    Schneider T, Müller A, Miess H, Gross H (2014) Cyclic lipopeptides as antibacterial agents – potent antibiotic activity mediated by intriguing mode of actions. Int J Med Microbiol 304:37–43. doi: 10.1016/j.ijmm.2013.08.009CrossRefPubMedGoogle Scholar
  4. 4.
    Cochrane SA, Vederas JC (2016) Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med Res Rev 36:4–31. doi: 10.1002/med.21321CrossRefPubMedGoogle Scholar
  5. 5.
    Cotter PD, Ross RP, Hill C (2013) Bacteriocins – a viable alternative to antibiotics? Nat Rev Microbiol 11:95–105. doi: 10.1038/nrmicro2937CrossRefPubMedGoogle Scholar
  6. 6.
    Fox JL (2013) Antimicrobial peptides stage a comeback. Nat Biotechnol 31:379–382. doi: 10.1038/nbt.2572CrossRefPubMedGoogle Scholar
  7. 7.
    Liu G, Chater KF, Chandra G, Niu G, Tan H (2013) Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev 77:112–143. doi: 10.1128/MMBR.00054-12CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Bachmann BO, Van Lanen SG, Baltz RH (2014) Microbial genome mining for accelerated natural products discovery: is a renaissance in the making? J Ind Microbiol Biotechnol 41:175–184. doi: 10.1007/s10295-013-1389-9CrossRefPubMedGoogle Scholar
  9. 9.
    Zhao X, Kuipers OP (2016) Identification and classification of known and putative antimicrobial compounds produced by a wide variety of Bacillales species. BMC Genomics 17(1):882. doi: 10.1186/s12864-016-3224-yCrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Raaijmakers JM, de Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. doi: 10.1111/j.1574-6976.2010.00221.xCrossRefPubMedGoogle Scholar
  11. 11.
    Stansly PG, Shepherd RG, White HJ (1947) Polymyxin: a new chemotherapeutic agent. Johns Hopkins Med J 81:43–54Google Scholar
  12. 12.
    Trimble MJ, Mlynárčik P, Kolář M, Hancock REW (2016) Polymyxin: alternative mechanisms of action and resistance. Cold Spring Harb Perspect Med 6:a025288. doi: 10.1101/cshperspect.a025288CrossRefPubMedGoogle Scholar
  13. 13.
    Newton BA (1956) The properties and mode of action of the polymyxins. Bacteriol Rev 20:14–27PubMedPubMedCentralGoogle Scholar
  14. 14.
    Velkov T, Thompson PE, Nation RL, Li J (2009) Structure-activity relationships of polymyxin antibiotics. J Med Chem 53:1898–1916. doi: 10.1021/jm900999hCrossRefGoogle Scholar
  15. 15.
    Beveridge EG, Martin AJ (1967) Sodium sulphomethyl derivatives of polymyxins. Br J Pharmacol 29:125–135. doi: 10.1111/j.1476-5381.1967.tb01946.xCrossRefGoogle Scholar
  16. 16.
    Li J, Milne RW, Nation RL, Turnidge JD, Smeaton TC, Coulthard K (2004) Pharmacokinetics of colistin methanesulphonate and colistin in rats following an intravenous dose of colistin methanesulphonate. J Antimicrob Chemother 53:837–840. doi: 10.1093/jac/dkh167CrossRefPubMedGoogle Scholar
  17. 17.
    Conway SP, Pond MN, Watson A, Etherington C, Robey HL, Goldman MH (1997) Intravenous colistin sulphomethate in acute respiratory exacerbations in adult patients with cystic fibrosis. Thorax 52:987–993. doi: 10.1136/thx.52.11.987CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Falagas ME, Rizos M, Bliziotis LA, Rellos K, Kasiakou SK, Michalopoulos A (2005) Toxicity after prolonged (more than four weeks) administration of intravenous colistin. BMC Infect Dis 5:1. doi: 10.1186/1471-2334-5-1CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Falagas ME, Kasiakou SK (2005) Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin Infect Dis 40:1333–1341. doi: 10.1086/429323CrossRefPubMedGoogle Scholar
  20. 20.
    Monaco M, Giani T, Raffone M, Arena F, Garcia-Fernandez A, Pollini S, Network EuSCAPE-Italy C, Grundmann H, Pantosti A, Rossolini G (2014) Colistin resistance superimposed to endemic carbapenem-resistant Klebsiella pneumoniae: a rapidly evolving problem in Italy, Nov 2013–Apr 2014. Eurosurveillance 19:20939–20918. doi: 10.2807/1560-7917.ES2014.19.42.20939CrossRefPubMedGoogle Scholar
  21. 21.
    Cai Y, Chai D, Wang R, Liang B, Bai N (2012) Colistin resistance of Acinetobacter baumannii: clinical reports, mechanisms and antimicrobial strategies. J Antimicrob Chemother 67:1607–1615. doi: 10.1093/jac/dks084CrossRefPubMedGoogle Scholar
  22. 22.
    Groisman EA, Kayser J, Soncini FC (1997) Regulation of polymyxin resistance and adaptation to low-Mg2+ environments. J Bacteriol 179:7040–7045. doi: 10.1128/jb.179.22.7040-7045.1997CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Gunn JS, Lim KB, Krueger J, Kim K, Guo L, Hackett M, Miller SI (1998) PmrA–PmrB-regulated genes necessary for 4-aminoarabinose lipid a modification and polymyxin resistance. Mol Microbiol 27:1171–1182. doi: 10.1046/j.1365-2958.1998.00757.xCrossRefPubMedGoogle Scholar
  24. 24.
    Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu L-F, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu J-H, Shen J (2016) Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16:161–168. doi: 10.1016/S1473-3099(15)00424-7CrossRefPubMedGoogle Scholar
  25. 25.
    Heinemann B, Kaplan M, Muir R, Hooper I (1953) Amphomycin, a new antibiotic. Antibiot Chemother (Northfield) 3:1239–1242Google Scholar
  26. 26.
    Debono M, Barnhart M, Carrell CB, Hoffmann JA, Occolowitz JL, Abbott BJ, Fukuda DS, Hamill RL, Biemann K, Herlihy WC (1987) A21978C, a complex of new acidic peptide antibiotics: isolation, chemistry, and mass spectral structure elucidation. J Antibiot 40:761–777. doi: 10.7164/antibiotics.40.761CrossRefPubMedGoogle Scholar
  27. 27.
    Robbel L, Marahiel MA (2010) Daptomycin, a bacterial lipopeptide synthesized by a nonribosomal machinery. J Biol Chem 285:27501–27508. doi: 10.1074/jbc.R110.128181CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Pogliano J, Pogliano N, Silverman JA (2012) Daptomycin-mediated reorganization of membrane architecture causes mislocalization of essential cell division proteins. J Bacteriol 194:4494–4504. doi: 10.1128/JB.00011-12CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Müller A, Wenzel M, Strahl H, Grein F, Saaki TNV, Kohl B, Siersma T, Bandow JE, Sahl H-G, Schneider T, Hamoen LW (2016) Daptomycin inhibits cell envelope synthesis by interfering with fluid membrane microdomains. Proc Natl Acad Sci U S A 113:7077–7086. doi: 10.1073/pnas.1611173113CrossRefGoogle Scholar
  30. 30.
    Renzoni A, Kelley WL, Rosato RR, Martinez MP, Roch M, Fatouraei M, Haeusser DP, Margolin W, Fenn S, Turner RD, Foster SJ, Rosato AE (2017) Molecular bases determining daptomycin resistance-mediated resensitization to β-lactams (seesaw effect) in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 61:e01634–e01616. doi: 10.1128/AAC.01634-16CrossRefPubMedGoogle Scholar
  31. 31.
    Henson KER, Yim J, Smith JR, Sakoulas G, Rybak MJ (2017) β-lactamase inhibitors enhance the synergy between β-lactam antibiotics and daptomycin against methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 61:e01564–e01516. doi: 10.1128/AAC.01564-16CrossRefPubMedGoogle Scholar
  32. 32.
    Taylor SD, Palmer M (2016) The action mechanism of daptomycin. Bioorg Med Chem 24:6253–6268. doi: 10.1016/j.bmc.2016.05.052CrossRefPubMedGoogle Scholar
  33. 33.
    May M (2014) Drug development: time for teamwork. Nature 509:S4–S5. doi: 10.1038/509S4aCrossRefPubMedGoogle Scholar
  34. 34.
    Munita JM, Murray BE, Arias CA (2014) Daptomycin for the treatment of bacteraemia due to vancomycin-resistant Enterococci. Int J Antimicrob Agents 44:387–395. doi: 10.1016/j.ijantimicag.2014.08.002CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kosmidis C, Levine DP (2010) Daptomycin: pharmacology and clinical use. Expert Opin Pharmacother 11:615–625. doi: 10.1517/14656561003598893CrossRefPubMedGoogle Scholar
  36. 36.
    Stefani S, Campanile F, Santagati M, Mezzatesta ML, Cafiso V, Pacini G (2015) Insights and clinical perspectives of daptomycin resistance in Staphylococcus aureus: a review of the available evidence. Int J Antimicrob Agents 46:278–289. doi: 10.1016/j.ijantimicag.2015.05.008CrossRefPubMedGoogle Scholar
  37. 37.
    Bayer AS, Schneider T, Sahl H-G (2013) Mechanisms of daptomycin resistance in Staphylococcus aureus: role of the cell membrane and cell wall. Ann N Y Acad Sci 1277:139–158. doi: 10.1111/j.1749-6632.2012.06819.xCrossRefPubMedGoogle Scholar
  38. 38.
    Miller WR, Bayer AS, Arias CA (2016) Mechanism of action and resistance to daptomycin in Staphylococcus aureus and Enterococci. Cold Spring Harb Perspect Med 6:a026997. doi: 10.1101/cshperspect.a026997CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Pader V, Hakim S, Painter KL, Wigneshweraraj S, Clarke TB, Edwards AM (2016) Staphylococcus aureus inactivates daptomycin by releasing membrane phospholipids. Nat Microbiol. doi:  10.1038/nmicrobiol.2016.194
  40. 40.
    Borders DB, Leese RA, Jarolmen H, Francis ND, Fantini AA, Falla T, Fiddes JC, Aumelas A (2007) Laspartomycin, an acidic lipopeptide antibiotic with a unique peptide core. J Nat Prod 70:443–446. doi: 10.1021/np068056fCrossRefPubMedGoogle Scholar
  41. 41.
    Müller C, Nolden S, Gebhardt P, Heinzelmann E, Lange C, Puk O, Welzel K, Wohlleben W, Schwartz D (2007) Sequencing and analysis of the biosynthetic gene cluster of the lipopeptide antibiotic friulimicin in Actinoplanes friuliensis. Antimicrob Agents Chemother 51:1028–1037. doi: 10.1128/AAC.00942-06CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Schneider T, Gries K, Josten M, Wiedemann I, Pelzer S, Labischinski H, Sahl HG (2009) The lipopeptide antibiotic friulimicin B inhibits cell wall biosynthesis through complex formation with bactoprenol phosphate. Antimicrob Agents Chemother 53:1610–1618. doi: 10.1128/AAC.01040-08CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Kleijn LHJ, Oppedijk SF, t Hart P, van Harten RM, Martin-Visscher LA, Kemmink J, Breukink E, Martin NI (2016) Total synthesis of laspartomycin C and characterization of its antibacterial mechanism of action. J Med Chem 59:3569–3574. doi: 10.1021/acs.jmedchem.6b00219CrossRefPubMedGoogle Scholar
  44. 44.
    Bunkoczi G, Vertesy L, Sheldrick GM (2005) Structure of the lipopeptide antibiotic tsushimycin. Acta Cryst D 61:1160–1164. doi: 10.2210/pdb1w3m/pdbCrossRefGoogle Scholar
  45. 45.
    Rubinchik E, Schneider T, Elliott M, Scott WRP, Pan J, Anklin C, Yang H, Dugourd D, Müller A, Gries K, Straus SK, Sahl HG, Hancock REW (2011) Mechanism of action and limited cross-resistance of new lipopeptide MX-2401. Antimicrob Agents Chemother 55:2743–2754. doi: 10.1128/AAC.00170-11CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Ryder NS (2009) Discontinued drugs in 2008: anti-infectives. Expert Opin Investig Drugs 19:1–21. doi: 10.1517/13543780903473150CrossRefGoogle Scholar
  47. 47.
    Kahne D, Leimkuhler C, Lu W, Walsh C (2005) Glycopeptide and lipoglycopeptide antibiotics. Chem Rev 105:425–448. doi: 10.1021/cr030103aCrossRefPubMedGoogle Scholar
  48. 48.
    Leclercq R, Derlot E, Duval J, Courvalin P (2010) Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. N Engl J Med 319:157–161. doi: 10.1056/NEJM198807213190307CrossRefGoogle Scholar
  49. 49.
    Van Bambeke F (2015) Lipoglycopeptide antibacterial agents in gram-positive infections: a comparative review. Drugs 75:2073–2095. doi: 10.1007/s40265-015-0505-8CrossRefPubMedGoogle Scholar
  50. 50.
    Leadbetter MR, Adams SM, Bazzini B, Fatheree PR, Karr DE, Krause KM, Lam BMT, Linsell MS, Nodwell MB, Pace JL, Quast K, Shaw J-P, Soriano E, Trapp SG, Villena JD, Wu TX, Christensen BG, Judice JK (2004) Hydrophobic vancomycin derivatives with improved ADME properties. J Antibiot 57:326–336. doi: 10.7164/antibiotics.57.326CrossRefPubMedGoogle Scholar
  51. 51.
    Cooper RDG, Snyder NJ, Zweifel MJ, Staszak MA, Wilkie SC, Nicas TI, Muller DL, Butler TF, Rodriguez MJ, Huff BE, Thompson RC (1996) Reductive alkylation of glycopeptide antibiotics: synthesis and antibacterial activity. J Antibiot 49:575–581. doi: 10.7164/antibiotics.49.575CrossRefPubMedGoogle Scholar
  52. 52.
    Malabarba A, Ciabatti R, Scotti R, Goldstein BP, Ferrari P, Kurz M, Andreini BP, Denaro M (1995) New semisynthetic glycopeptides MDL 63246 and MDL 63042, and other amide derivatives of antibiotic A-40926 active against highly glycopeptide-resistant VanA Enterococci. J Antibiot 48:869–883. doi: 10.7164/antibiotics.48.869CrossRefPubMedGoogle Scholar
  53. 53.
    Zeng D, Debabov D, Hartsell TL, Cano RJ, Adams S, Schuyler JA, McMillan R, Pace JL (2016) Approved glycopeptide antibacterial drugs: mechanism of action and resistance. Cold Spring Harb Perspect Med 6:a026989. doi: 10.1101/cshperspect.a026989CrossRefPubMedGoogle Scholar
  54. 54.
    Barna JCJ, Williams DH (1984) The structure and mode of action of glycopeptide antibiotics of the vancomycin group. Annu Rev Microbiol 38:339–357CrossRefGoogle Scholar
  55. 55.
    Kim SJ, Cegelski L, Stueber D, Singh M, Dietrich E, Tanaka KSE, Parr Jr TR, Far AR, Schaefer J (2008) Oritavancin exhibits dual mode of action to inhibit cell-wall biosynthesis in Staphylococcus aureus. J Mol Biol 377:281–293. doi: 10.1016/j.jmb.2008.01.031CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Higgins DL, Chang R, Debabov DV, Leung J, Wu T, Krause KM, Sandvik E, Hubbard JM, Kaniga K, Schmidt Jr DE, Gao Q, Cass RT, Karr DE, Benton BM, Humphrey PP (2005) Telavancin, a multifunctional lipoglycopeptide, disrupts both cell wall synthesis and cell membrane integrity in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 49:1127–1134. doi: 10.1128/AAC.49.3.1127-1134.2005CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Svetitsky S, Leibovici L, Paul M (2009) Comparative efficacy and safety of vancomycin versus teicoplanin: systematic review and meta-analysis. Antimicrob Agents Chemother 53:4069–4079. doi: 10.1128/AAC.00341-09CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Wenzler E, Liao S, Rodvold KA (2016) In: Rotschafer JC, Andes DR, Rodvold KA (eds) Antibiotic pharmacodynamics. Springer, New York, NY, pp 285–315Google Scholar
  59. 59.
    Masterton R, Cornaglia G, Courvalin P, Lode HM, Rello J, Torres A (2015) The clinical positioning of telavancin in Europe. Int J Antimicrob Agents 45:213–220. doi: 10.1016/j.ijantimicag.2014.12.006CrossRefPubMedGoogle Scholar
  60. 60.
    Sweeney D, Stoneburner A, Shinabarger DL, Arhin FF, Belley A, Moeck G, Pillar CM (2016) Comparative in vitro activity of oritavancin and other agents against vancomycin-susceptible and -resistant Enterococci. J Antimicrob Chemother. doi:  10.1093/jac/dkw451CrossRefPubMedGoogle Scholar
  61. 61.
    Karlowsky JA, Nichol K, Zhanel GG (2015) Telavancin: mechanisms of action, in vitro activity, and mechanisms of resistance. Clin Infect Dis 61:S58–S68. doi: 10.1093/cid/civ534CrossRefPubMedGoogle Scholar
  62. 62.
    Goto S, Kuwahara S, Zenyoji H, Okubo N (1968) In vitro and in vitro evaluation of enduracidin, a new peptide antibiotic substance. J Antibiot 21:119–125. doi: 10.7164/antibiotics.21.119CrossRefPubMedGoogle Scholar
  63. 63.
    Cavalleri B, Pagani H, Volpe G, Selva E, Parenti F (1984) A-16686, a new antibiotic from Actinoplanes. J Antibiot 37:309–317. doi: 10.7164/antibiotics.37.309CrossRefPubMedGoogle Scholar
  64. 64.
    Shin D, Rew Y, Boger DL (2004) Total synthesis and structure of the ramoplanin A1 and A3 aglycons: two minor components of the ramoplanin complex. Proc Natl Acad Sci U S A 101:11977–11979. doi: 10.1073/pnas.0401419101CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Castiglione F, Marazzi A, Meli M, Colombo G (2005) Structure elucidation and 3D solution conformation of the antibiotic enduracidin determined by NMR spectroscopy and molecular dynamics. Magn Reson Chem 43:603–610. doi: 10.1002/mrc.1606CrossRefPubMedGoogle Scholar
  66. 66.
    Fang X, Tiyanont K, Zhang Y, Wanner J, Boger D, Walker S (2006) The mechanism of action of ramoplanin and enduracidin. Mol Biosyst 2:69–76. doi: 10.1039/B515328JCrossRefPubMedGoogle Scholar
  67. 67.
    Cheng M, Huang JX, Ramu S, Butler MS, Cooper MA (2014) Ramoplanin at bactericidal concentrations induces bacterial membrane depolarization in Staphylococcus aureus. Antimicrob Agents Chemother 58:6819–6827. doi: 10.1128/AAC.00061-14CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Farver DK, Hedge DD, Lee SC (2005) Ramoplanin: a lipoglycodepsipeptide antibiotic. Ann Pharmacother 39:863–868. doi: 10.1345/aph.1E397CrossRefPubMedGoogle Scholar
  69. 69.
    Van Bambeke F (2006) Glycopeptides and glycodepsipeptides in clinical development: a comparative review of their antibacterial spectrum, pharmacokinetics and clinical efficacy. Curr Opin Investig Drugs 7:740–749PubMedGoogle Scholar
  70. 70.
    Butler MS, Blaskovich MA, Cooper MA (2017) Antibiotics in the clinical pipeline at the end of 2015. J Antibiot. doi:  10.1038/ja.2016.72CrossRefPubMedGoogle Scholar
  71. 71.
    Stiefel U, Pultz NJ, Helfand MS, Donskey CJ (2004) Efficacy of oral ramoplanin for inhibition of intestinal colonization by vancomycin-resistant Enterococci in mice. Antimicrob Agents Chemother 48:2144–2148. doi: 10.1128/AAC.48.6.2144-2148.2004CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Peromet M, Schoutens E, Yourassowsky E (1973) Clinical and microbiological study of enduracidin in infections due to methicillin-resistant strains of Staphylococcus aureus. Chemotherapy 19:53–61. doi: 10.1159/000221439CrossRefPubMedGoogle Scholar
  73. 73.
    McCafferty DG, Cudic P, Frankel BA, Barkallah S, Kruger RG, Li W (2002) Chemistry and biology of the ramoplanin family of peptide antibiotics. Biopolymers 66:261–284. doi: 10.1002/bip.10296CrossRefPubMedGoogle Scholar
  74. 74.
    Walker S, Chen L, Hu Y, Rew Y, Shin D, Boger DL (2005) Chemistry and biology of ramoplanin: a lipoglycodepsipeptide with potent antibiotic activity. Chem Rev 105:449–476. doi: 10.1021/cr030106nCrossRefPubMedGoogle Scholar
  75. 75.
    Michel KH, Kastner RE (1985) A54556 Antibiotics and process for production thereof. US4492650AGoogle Scholar
  76. 76.
    Brötz-Oesterhelt H, Beyer D, Kroll H-P, Endermann R, Ladel C, Schroeder W, Hinzen B, Raddatz S, Paulsen H, Henninger K, Bandow JE, Sahl H-G, Labischinski H (2005) Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat Med 11:1082–1087. doi: 10.1038/nm1306CrossRefPubMedGoogle Scholar
  77. 77.
    Koshino H, Osada H, Yano T, Uzawa J, Isono K (1991) The structure of enopeptins a and B, novel depsipeptide antibiotics. Tetrahedron Lett 32:7707–7710. doi: 10.1016/0040-4039(91)80571-MCrossRefGoogle Scholar
  78. 78.
    Hinzen B, Raddatz S, Paulsen H, Lampe T, Schumacher A, Häbich D, Hellwig V, Benet Buchholz J, Endermann R, Labischinski H, Brötz-Oesterhelt H (2006) Medicinal chemistry optimization of acyldepsipeptides of the enopeptin class antibiotics. ChemMedChem 1:689–693. doi: 10.1002/cmdc.200600055CrossRefPubMedGoogle Scholar
  79. 79.
    Lee B-G, Park EY, Lee K-E, Jeon H, Sung KH, Paulsen H, Rübsamen-Schaeff H, Brötz-Oesterhelt H, Song HK (2010) Structures of ClpP in complex with acyldepsipeptide antibiotics reveal its activation mechanism. Nat Struct Mol Biol 17:471–478. doi: 10.1038/nsmb.1787CrossRefPubMedGoogle Scholar
  80. 80.
    Carney DW, Schmitz KR, Truong JV, Sauer RT, Sello JK (2014) Restriction of the conformational dynamics of the cyclic acyldepsipeptide antibiotics improves their antibacterial activity. J Am Chem Soc 136:1922–1929. doi: 10.1021/ja410385cCrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Arvanitis M, Li G, Li D-D, Cotnoir D, Ganley-Leal L, Carney DW, Sello JK, Mylonakis E (2016) A conformationally constrained cyclic acyldepsipeptide is highly effective in mice infected with methicillin-susceptible and -resistant Staphylococcus aureus. PLoS One 11:e0153912. doi: 10.1371/journal.pone.0153912CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Conlon BP, Nakayasu ES, Fleck LE, LaFleur MD, Isabella VM, Coleman K, Leonard SN, Smith RD, Adkins JN, Lewis K (2013) Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature 503:365–370. doi: 10.1038/nature12790CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Gominet M, Seghezzi N, Mazodier P (2011) Acyl depsipeptide (ADEP) resistance in Streptomyces. Microbiology 157:2226–2234. doi: 10.1099/mic.0.048454-0CrossRefPubMedGoogle Scholar
  84. 84.
    Johnson BA, Anker H, Meleney FL (1945) Bacitracin: a new antibiotic produced by a member of the B. subtilis group. Science 102:376–377. doi: 10.1126/science.102.2650.376CrossRefPubMedGoogle Scholar
  85. 85.
    Ming L-J, Epperson JD (2002) Metal binding and structure-activity relationship of the metalloantibiotic peptide bacitracin. J Inorg Biochem 91:46–58. doi: 10.1016/S0162-0134(02)00464-6CrossRefPubMedGoogle Scholar
  86. 86.
    Storm DR, Strominger JL (1973) Complex formation between bacitracin peptides and isoprenyl pyrophosphates. J Biol Chem 248:3940–3945PubMedGoogle Scholar
  87. 87.
    Economou NJ, Cocklin S, Loll PJ (2013) High-resolution crystal structure reveals molecular details of target recognition by bacitracin. Proc Natl Acad Sci U S A 110:14207–14212. doi: 10.1073/pnas.1308268110CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Lin FL, Woodmansee D, Patterson R (1998) Near-fatal anaphylaxis to topical bacitracin ointment. J Allergy Clin Immunol 101:136–137. doi: 10.1016/S0091-6749(98)70209-XCrossRefPubMedGoogle Scholar
  89. 89.
    Charlebois A, Jalbert L-A, Harel J, Masson L, Archambault M (2012) Characterization of genes encoding for acquired bacitracin resistance in Clostridium perfringens. PLoS One 7:e44449. doi: 10.1371/journal.pone.0044449CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Pawlowski AC, Wang W, Koteva K, Barton HA, McArthur AG, Wright GD (2016) A diverse intrinsic antibiotic resistome from a cave bacterium. Nat Commun 7:13803. doi: 10.1038/ncomms13803CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Azusa Kato, Seigo Nakaya, Yoshitami Ohashi A, Hirata H, and KF, Harada K-I (1997) WAP-8294A2, a novel anti-MRSA antibiotic produced by Lysobacter sp. J Am Chem Soc 119:6680–6681. doi:  10.1021/ja970895oCrossRefGoogle Scholar
  92. 92.
    Kato A, Nakaya S, Kokubo N, Aiba Y, Ohashi Y, Hirata H, Fujii K, Harada K-I (1998) A new anti-MRSA antibiotic complex, WAP-8294A. J Antibiot 51:929–935. doi: 10.7164/antibiotics.51.929CrossRefPubMedGoogle Scholar
  93. 93.
    Konishi M, Sugawara K, Hanada M, Tomita K, Tomatsu K, Miyaki T, Kawaguchi H, Buck RE, More C, Rossomano VZ (1984) Empedopeptin (Bmy-28117), a new depsipeptide antibiotic. J Antibiot 37:949–957. doi: 10.7164/antibiotics.37.949CrossRefPubMedGoogle Scholar
  94. 94.
    Hashizume H, Sawa R, Harada S, Igarashi M, Adachi H, Nishimura Y, Nomoto A (2011) Tripropeptin C blocks the lipid cycle of cell wall biosynthesis by complex formation with undecaprenyl pyrophosphate. Antimicrob Agents Chemother 55:3821–3828. doi: 10.1128/AAC.00443-11CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Shoji J, Hinoo H, Katayama T, Matsumoto K, Tanimoto T, Hattori T, Higashiyama I, Miwa H, Motokawa K, Yoshida T (1992) Isolation and characterization of new peptide antibiotics, plusbacins A1–A4 and B1–B4. J Antibiot 45:817–823. doi: 10.7164/antibiotics.45.817CrossRefPubMedGoogle Scholar
  96. 96.
    Müller A, Münch D, Schmidt Y, Reder-Christ K, Schiffer G, Bendas G, Gross H, Sahl H-G, Schneider T, Brötz-Oesterhelt H (2012) Lipodepsipeptide empedopeptin inhibits cell wall biosynthesis through Ca2+-dependent complex formation with peptidoglycan precursors. J Biol Chem 287:20270–20280. doi: 10.1074/jbc.M112.369561CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Cochrane SA, Li X, He S, Yu M, Wu M, Vederas JC (2015) Synthesis of tridecaptin–antibiotic conjugates with in vivo activity against gram-negative bacteria. J Med Chem 58:9779–9785. doi: 10.1021/acs.jmedchem.5b01578CrossRefPubMedGoogle Scholar
  98. 98.
    Cochrane SA, Findlay B, Bakhtiary A, Acedo JZ, Rodriguez-Lopez EM, Mercier P, Vederas JC (2016) Antimicrobial lipopeptide tridecaptin A1 selectively binds to gram-negative lipid II. Proc Natl Acad Sci U S A 113:11561–11566. doi: 10.1073/pnas.1608623113CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Boakes S, Dawson MJ (2014) In: Natural products: discourse, diversity, and design. Wiley, Hoboken, NJ, USA, pp 455–468CrossRefGoogle Scholar
  100. 100.
    Brötz H, Bierbaum G, Leopold K, Reynolds PE, Sahl H-G (1998) The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob Agents Chemother 42:154–160PubMedPubMedCentralGoogle Scholar
  101. 101.
    Oppedijk SF, Martin NI, Breukink E (2016) Hit ‘em where it hurts: the growing and structurally diverse family of peptides that target lipid-II. Biochim Biophys Acta 1858:947–957. doi: 10.1016/j.bbamem.2015.10.024CrossRefPubMedGoogle Scholar
  102. 102.
    Breukink E, Wiedemann I, Van Kraaij C, Kuipers OP, Sahl HG, de Kruijff B (1999) Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286:2361–2364. doi: 10.1126/science.286.5448.2361CrossRefPubMedGoogle Scholar
  103. 103.
    Koopmans T, Wood TM, Hart PT, Kleijn LHJ, Hendrickx APA, Willems RJL, Breukink E, Martin NI (2015) Semisynthetic lipopeptides derived from nisin display antibacterial activity and lipid II binding on par with that of the parent compound. J Am Chem Soc 137:9382–9389. doi: 10.1021/jacs.5b04501CrossRefPubMedGoogle Scholar
  104. 104.
    Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP, Mueller A, Schäberle TF, Hughes DE, Epstein S, Jones M, Lazarides L, Steadman VA, Cohen DR, Felix CR, Fetterman KA, Millett WP, Nitti AG, Zullo AM, Chen C, Lewis K (2015) A new antibiotic kills pathogens without detectable resistance. Nature 517:455–459. doi: 10.1038/nature14098CrossRefPubMedGoogle Scholar
  105. 105.
    Ng V, Chan WC (2016) New found hope for antibiotic discovery: lipid II inhibitors. Chem A Eur J 22:12606–12616. doi: 10.1002/chem.201601315CrossRefGoogle Scholar
  106. 106.
    Yang H, Chen KH, Nowick JS (2016) Elucidation of the teixobactin pharmacophore. ACS Chem Biol 11:1823–1826. doi: 10.1021/acschembio.6b00295CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Dhara S, Gunjal VB, Handore KL, Reddy DS (2016) Solution-phase synthesis of the macrocyclic core of teixobactin. Eur J Org Chem 2016:4289–4293CrossRefGoogle Scholar
  108. 108.
    Jin K, Sam IH, Po KH, Lin D, Ghazvini Zadeh EH, Chen S, Yuan Y, Li X (2016) Total synthesis of teixobactin. Nat Commun 7:12394. doi: 10.1038/ncomms12394CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Giltrap AM, Dowman LJ, Nagalingam G, Ochoa JL, Linington RG, Britton WJ, Payne RJ (2016) Total synthesis of teixobactin. Org Lett 18:2788–2791. doi: 10.1021/acs.orglett.6b01324CrossRefPubMedGoogle Scholar
  110. 110.
    Parmar A, Iyer A, Vincent CS, Van Lysebetten D, Prior SH, Madder A, Taylor EJ, Singh I (2016) Efficient total syntheses and biological activities of two teixobactin analogues. Chem Commun 52:6060–6063. doi: 10.1039/c5cc10249aCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Chemical Biology and Drug Discovery, Utrecht Institute for Pharmaceutical SciencesUtrecht UniversityUtrechtThe Netherlands

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