Antibacterial activities of aminoglycoside antibiotics-derived cationic amphiphiles. Polyol-modified neomycin B-, Kanamycin A-, Amikacin-, and Neamine-based amphiphiles with potent broad spectrum antibacterial activity

Journal of Medicinal Chemistry

Volumn 53, Issue 9, 2010, Pages 3626-3631

  Bera, Smritilekha ^a   Zhanel, George G ^a   Schweizer, Frank ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AMPHOPHILE; CARBAMIC ACID DERIVATIVE; FRAMYCETIN; KANAMYCIN A; NEAMINE; POLYETHER; POLYOL;

ACINETOBACTER BAUMANNII; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; DRUG POTENCY; DRUG STRUCTURE; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ESCHERICHIA COLI; HYDROPHOBICITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS EPIDERMIDIS; STENOTROPHOMONAS MALTOPHILIA; STREPTOCOCCUS PNEUMONIAE;

EID: 77952069162     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm1000437     Document Type: Article

References (60)

1. Boucher, H. W.; Talbot, G. H.; Bradley, J. S.; Edwards, J. E.; Gilbert, D.; Rice, L. B.; Scheld, M.; Spellberg, B.; Bartlett, J. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America Clin. Infect. Dis 2009, 48, 1-12
2. Neu, H. C. The crisis in antibiotic resistance Science 1992, 257, 1064-1073
3. Peterson, A. A.; Hancock, R. E. W.; McGroarty, E. J. Binding of polycationic antibiotics and polyamines to lipopolysaccharides of Pseudomonas aeruginosa J. Bacteriol. 1985, 164, 1256-1261
4. Moore, R. A.; Bates, N. C.; Hancock, R. E. W. Interaction of polycationic antibiotics with Pseudomonas aeruginosa lipopolysaccharide and lipid A studied by using dansyl-polymyxin Antimicrob. Agents Chemother. 1986, 29, 496-500
5. Davis, B. D. Mechanism of bactericidal action of aminoglycosides Microbiol. Rev. 1987, 51, 341-350
6. Arya, D. P., Ed. Aminoglycoside Antibiotics: From Chemical Biology to Drug Discovery; John Wiley & Sons: Chichester, U.K., 2007; pp 1-319.
7. Hancock, R. E. W.; Sahl, H. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies Nat. Biotechnol. 2006, 24, 1551-1557
8. Zasloff, M. Antimicrobial peptides of multicellular organisms Nature 2002, 415, 389-395
9. Hamuro, Y.; Schneider, J. P.; DeGrado, W. F. De novo design of antibacterial beta-peptides J. Am. Chem. Soc. 1999, 121, 12200-12201
10. Porter, E. A.; Wang, X. F.; Lee, H. S.; Weisblum, B.; Gellman, S. H. Non haemolytic beta-amino acid oligomers Nature 2000, 404, 565
11. Schmitt, M. A.; Weisblum, B.; Gellman, S. H. Interplay among folding sequence and lipophilicity in the antibacterial and hemolytic activities of alpha/beta-peptides J. Am. Chem. Soc. 2007, 129, 417-428
12. Patch, J. A.; Barron, A. E. Helical peptoid mimics of magainin-2 amide J. Am. Chem. Soc. 2004, 48, 3127-3129
13. Radzishevsky, I. S.; Rotem, S.; Bourdetsky, D.; Navon-Venezia, S.; Carmeli, Y.; Mor, A. Improved antimicrobial peptides based on acyl-lysine oligomers Nat. Biotechnol. 2007, 25, 657-659
14. Zorko, M.; Majerle, A.; Sarlah, D.; Keber, M. M.; Mohar, B.; Jerala, R. Combination of antimicrobial and endotoxin-neutralizing activities of novel oleoylamines Antimicrob. Agents Chemother. 2005, 49, 2307-2313
15. Liu, D.; Choi, S.; Chen, B.; Doerksen, R. J.; Clements, D. J.; Winkler, J. D.; KleM. L.; DeGrado, W. F. Nontoxic membrane-active antimicrobial arylamide oligomers Angew. Chem., Int. Ed. 2004, 43, 1158-1162
16. Tew, G. N.; Liu, D.; Chen, B.; Doerksen, R. J.; Kaplan, J.; Carroll, P. J.; KleM. L.; DeGrado, W. F. De novo design of biomimetic antimicrobial polymers Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 5110-5114
17. Chongsiriwatana, N. P.; Patch, J. A.; Csyzewski, A. M.; Dohm, M. T.; IvankA.; Gidaevits, D.; Zuckermann, R. N.; Barron, A. E. Peptoids that mimic the structure, function and mechanism of helical antimicrobial peptides Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 2794-2799
18. Som, A.; Tew, G. N. Influence of lipid composition on membrane activity of antimicrobial phenylene ethynylene oligomers J. Phys. Chem. B 2008, 112, 3495-3502
19. Makovitzki, A.; Avrahami, D.; Shai, Y. Ultrashort antibacterial and antifungal lipopeptides Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 15997-16002
20. Andrä, J.; Lohner, K.; Blondelle, S. E.; Jerala, R.; Moriyon, I.; Koch, M. H. J. Enhancement of endotoxin neutralization by coupling of a C12-alkyl chain to a lactoferricin-derived peptide Biochem. J. 2005, 385, 135-143
21. Japelj, B.; Zorko, M.; Majerle, A.; Pristovek, P.; Sanchez-Gomez, S.; Martinez de Tejada, G. The acyl group as the central element of the structural organization of antimicrobial lipopeptide J. Am. Chem. Soc. 2007, 129, 1022-1023
22. Majerle, A.; Kidric, J.; Jerala, R. Enhancement of antibacterial and lipopolysaccharide binding activities of a human lactoferrin peptide fragment by the addition of acyl chain J. Antimicrob. Chemother. 2003, 51, 1159-1165
23. Wakabayashi, H.; Matsumoto, H.; Hashimoto, K.; Teraguchi, S.; Takase, M.; Hayasawa, H. N-Acylated and d -enantiomer derivatives of a nonamer core peptide of lactoferricin B showing improved antimicrobial activity Antimicrob. Agents Chemother. 1999, 43, 1267-1269
24. Malina, A.; Shai, Y. Conjugation of fatty acids with different lengths modulates the antibacterial and antifungal activity of a cationic biologically inactive peptide Biochem. J. 2005, 390, 695-702
25. Shai, Y.; Makovitzky, A.; Avrahami, D. Host defense peptides and lipopeptides: modes of action and potential candidates for the treatment of bacterial and fungal infections Curr. Protein Pept. Sci. 2006, 7, 479-486
26. Vieira, D. B.; Carmona-Ribeiro, A. M. Cationic lipids and surfactants as antifungal agents: mode of action J. Antimicrob. Chemother. 2006, 58, 760-767
27. David, S. A. Towards a rational development of anti-endotoxin agents: novel approaches to sequestration of bacterial endotoxins with small molecules J. Mol. Recognit. 2001, 14, 370-387
28. Savage, P. B.; Chunhong, L.; Taotafa, U.; Ding, B.; Guan, Q. Antibacterial properties of cationic steroid antibiotics FEMS Microbiol. Lett. 2002, 217, 1-7
29. Palermo, E. F.; Kuroda, K. Chemical structure of cationic groups in amphiphilic polymethacrylates modulates the antimicrobial and hemolytic activities Biomacromolecules 2009, 10, 1416-1428
30. Hancock, R. E. W.; Bell, A. Antibiotic uptake into Gram-negative bacteria Eur. J. Clin. Microbiol. Infect. Dis. 1988, 7, 713-720
31. Chopra, I.; Hodgson, J.; Metcalf, B.; Poste, G. The search for antimicrobial agents effective against bacteria resistant to multiple antibiotics Antimicrob. Agents Chemother. 1997, 41, 497-503
32. Gilbert, P.; Moore, L. E. Cationic antiseptics: diversity of action under a common epithet J. Appl. Microbiol. 2005, 99, 703-715
33. Shelburne, S. A; Musher, D. M.; Hulten, K.; Ceasar, H.; Lu, Y. M.; Bhaila, I.; Hamill, J. R. In vitro killing of community-associated methicillin-resistant Staphylococcus aureus with drug combinations Antimicrob. Agents Chemother. 2004, 48, 4016-4019
34. Drew, K. R. P.; Sanders, L. K.; Culumber, Z. W.; Zibri, O.; Wong, G. C. L. Cationic amphiphiles increase activity of aminoglycoside antibiotic tobramycin in the presence of airway polyelectrolytes J. Am. Chem. Soc. 2009, 131, 486-493
35. Moazed, S.; Noller, H. F. Interaction of antibiotics with functional sites in 16S ribosomal RNA Nature 1987, 327, 389-394
36. Purohit, P.; Stern, S. Interactions of a small RNA with antibiotic and RNA ligands of the 30S subunit Nature 1994, 370, 659-662
37. Giuliano, R. A.; Paulus, G. J.; Verpooten, G. A.; PattijV. M.; Pollet, D. E.; Nouwen, E. J.; De Broe, M. E. Early effects of gentamictobramycin and amikacin on the human kidney Kidney Int. 1984, 26, 838-847
38. Tran Ba Huy, P.; Bernard, P.; Schacht, J. Kinetics of gentamicin uptake and release in the rat. Comparison of inner ear tissues and fluids with other organs J. Clin. Invest. 1986, 77, 1492-1500
39. Magnet, S.; Blanchard, J. S. Molecular insights into aminoglycoside action and resistance Chem. Rev. 2005, 105, 477-497
40. Taber, H. W.; Mueller, J. P.; Miller, P. F.; Arrow, A. S. Bacterial uptake of aminoglycoside antibiotics Microbiol. Rev. 1987, 429-457
41. Wright, G. D.; Berghuis, A. M.; Mobashery, S. Adv. Exp. Med. Biol. 1998, 456, 27-69
42. Shakya, T.; Wright, G. D. Mechanisms of Aminoglycoside Antibiotic Resistance in Aminoglycoside Antibiotics; Arya, D. P., Ed.; Wiley: Chichester, U.K., 2007; pp 119-140.
43. Bera, S.; Zhanel, G. G.; Schweizer, F. Design, synthesis and antibacterial activities of neomycin-lipid conjugates: polycationic lipids with potent Gram-positive activity J. Med. Chem. 2008, 51, 6160-6164
44. Zhang, J.; Chiang, F.-I.; Wu, L.; Czyryca, P. G.; Li, D.; Chang, C.-W. T. Surprising alteration of antibacterial activity of 5′′-modified neomycin against resistant bacteria J. Med. Chem. 2008, 51, 7563-7573
45. Zhang, J.; Keller, K.; Takemoto, J. Y.; Bensaci, M.; Litke, A.; Czyryca, P. G.; Chang, C.-W. T. J. Antibiot. 2009, 62, 539-544
46. Documment M100-S16, CLSI/NCCLS M100-S15; Clinical and Laboratory Standards Institute: Wayne, PA, 2006.
47. Zhanel, G. G.; DeCorby, M.; Laing, N.; Weshnoweski, B.; Veshisht, R.; Tailor, F.; Nichol, K. A.; Wierzboski, A.; Baudry, P.; Karlowsky, J. A.; Lagacé-Wiens, P.; Walkty, A.; McCracken, M.; Mulvey, M. R.; Johnson, J.; The Canadian Antimicrobial Resistance Alliance (CARA); Hoban, D. J. Antimicrobial-resistant pathogens in intensive care units in Canada: results of the Canadian National Intensive Care Unit (CAN-ICU) Study, 2005-2006 Antimicrob. Agents Chemother. 2008, 52, 1430-1437
48. Park, C. B.; Kim, H. S.; Kim, S. C. Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions Biochem. Biophys. Res. Commun. 1998, 244, 253-257
49. Serrano, G. N.; Zhanel, G. G.; Schweizer, F. Antibacterial activity of ultrashort cationic lipo-β-peptides Antimicrob. Agents Chemother. 2009, 53, 2215-2217
50. Gales, A. C.; Jones, R. N.; Forward, K. R.; Linares, J.; Sader, H.; Verhoef, J. Emerging importance of multidrug-resistant Acinetobacter species and Stenotrophomonas maltophilia as pathogens in seriously ill patients: geographic patterns, epidemiological features and trends in the SENTRY antimicrobial surveillance program (1997-1999) Clin. Infect. Dis. 2001, 32, S104-S113
51. Ribera, A.; Ruiz, J.; Jimenez de Anta, T.; Vila, J. Effect of an efflux pump inhibitor on the MIC of nalidixic acid for Acinetobacter baumannii and Stenotrophomonas maltophilia clinical isolates [1], Journal of Antimicrobial Chemotherapy. 2002, 49(4), 697-698
52. Chen, L. F.; Kaye, D. Current use for old antibacterial agents: polymyxins, rifamycins and aminoglycosides Infect. Dis. Clin. North Am. 2009, 23, 1053-1075
53. Vaara, M.; Vaara, T. Polycations as outer membrane-disorganizing agents Antimicrob. Agents Chemother. 1983, 24, 114-122
54. Vaara, M. Lipid A: target for antibacterial drugs Science 1996, 274, 939-940
55. Agrawal, K. L.; Khorana, H. G. Studies on polynucleotides. CII. The use of aromatic isocyanates for selective blocking of the terminal 3′-hydroxyl group in protected deoxyribooligonucleotides J. Am. Chem. Soc. 1972, 94, 3578-3585
56. Kuhn, R.; Baer, H. H.; Seeliger, A. Liebigs Ann. Chem. 1958, 611, 236-241
57. Quader, S.; Boyd, S. E.; Jenkins, I. D.; Houston, T. A. Modification of neomycin B: combined Mitsunobu and click chemistry J. Org. Chem. 2007, 72, 1962-1979
58. Disney, M. D.; Barrett, O. J. An aminoglycoside microarray platform for directly monitoring and studying antibiotic resistance Biochemistry 2007, 46, 11223-11230
59. Albert, R.; Dax, K.; Stütz, A. E.; Hildebrandt, J. Chemical modification of amikacin at C-4′′ with inversion of configuration J. Antibiot. 1985, 38, 275-278
60. Kim, C.; Haddad, J.; Vakulenko, S. B.; Meroueh, S. O.; Wu, Y.; Yan, H.; Mobashery, S. Fluorinated aminoglycosides and their mechanistic implication for aminoglycosides 3′-phosphotransferases from Gram-negative bacteria Biochemistry 2004, 43, 2373-2383