Biscatecholate-monohydroxamate mixed ligand siderophore-carbacephalosporin conjugates are selective sideromycin antibiotics that target Acinetobacter baumannii

Journal of Medicinal Chemistry

Volumn 56, Issue 10, 2013, Pages 4044-4052

  Wencewicz, Timothy A ^a   Miller, Marvin J ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAM ANTIBIOTIC; CIPROFLOXACIN; IRON; LORACARBEF; SIDEROMYCIN; SIDEROPHORE; UNCLASSIFIED DRUG;

ACINETOBACTER BAUMANNII; ACTIVE TRANSPORT; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL OUTER MEMBRANE; CONJUGATE; DRUG SCREENING; DRUG SYNTHESIS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; AGAR; ANTI-BACTERIAL AGENTS; CEPHALOSPORINS; CULTURE MEDIA; DNA GYRASE; FERROUS COMPOUNDS; INDICATORS AND REAGENTS; IRON; MICROBIAL SENSITIVITY TESTS; PEPTIDES;

EID: 84878035473     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm400265k     Document Type: Article

References (54)

1. Fischback, M. A.; Walsh, C. T. Antibiotics for emerging pathogens Science 2009, 325, 1089-1093
2. Boucher, H. W.; Talbot, G. H.; Bradley, J. S.; Edwards, J. E., Jr.; 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
3. Visca, P.; Seifert, H.; Towner, K. J. Acinetobacter infection-an emerging threat to human health IUBMB Life 2011, 63, 1048-1054
4. Peleg, A. Y.; Seifert, H.; Paterson, D. L. Acinetobacter baumannii: emergence of a successful pathogen Clin. Microbiol. Rev. 2008, 21, 538-582
5. Vila, J.; Pachón, J. Acinetobacter baumannii resistant to everything: What should we do? Clin. Microbiol. Infect. 2011, 17, 955-956
6. Bassetti, M.; Repetto, E.; Righi, E.; Boni, S.; Diverio, M.; Molinari, M. P.; Mussap, M.; Artioli, S.; Ansaldi, F.; Durando, P.; Orengo, G.; Bobbio Pallavicini, F.; Viscoli, C. Colistin and rifampicin in the treatment of multidrug-resistant Acinetobacter baumannii infections J. Antimicrob. Chemother. 2008, 61, 417-420
7. Lee, N. Y.; Wang, C. L.; Chuang, Y. C.; Yu, W. L.; Lee, H. C.; Chang, C. M.; Wang, L. R.; Ko, W. C. Combination carbapenem-sulbactam therapy for critically ill patients with multidrug-resistant Acinetobacter baumannii bacteremia: four case reports and an in vitro combination synergy study Pharmacotherapy 2007, 27, 1506-1511
8. Radu Mihu, M.; Martinez, L. R. Novel therapies for treatment of multidrug-resistant Acinetobacter baumannii skin infections Virulence 2011, 2, 97-102
9. Shankar, R.; He, L. K.; Szilagy, A.; Muthu, K.; Gamelli, R. L.; Filutowicz, M.; Wendt, J. L.; Suzuki, H.; Dominguez, M. A novel antibacterial gene transfer treatment for multidrug-resistant Acinetobacter baumannii -induced burn sepsis J. Burn Care Res. 2007, 28, 6-12
10. Thomas-Virnig, C. L.; Centanni, J. M.; Johnston, C. E.; He, L. K.; Schlosser, S. J.; Van Winkle, K. F.; Chen, R.; Gibson, A. L.; Szilagy, A.; Li, L.; Shankar, R.; Allen-Hoffmann, B. L. Inhibition of multidrug-resistant Acinetobacter baumannii by nonviral expression of hCAP-18 in a bioengineered human skin tissue Mol. Ther. 2009, 17, 562-569
11. Friedman, A. J.; Han, G.; Navati, M. S.; Chacko, M.; Gunther, L.; Alfieri, A.; Friedman, J. M. Sustained release nitric oxide releasing nanoparticles: characterization of a novel delivery platform based on nitrite containing hydrogel/glass composites Nitric Oxide 2008, 19, 12-20
12. Lin, N. T.; Chiou, P. Y.; Chang, K. C.; Chen, L. K.; Lai, M. J. Isolation and characterization of phi AB2: a novel bacteriophage of Acinetobacter baumannii Res. Microbiol. 2010, 161, 308-314
13. Dai, T.; Tegos, G. P.; Lu, Z.; Huang, L.; Zhiyentayev, T.; Franklin, M. J.; Baer, D. G.; Hamblin, M. R. Photodynamic therapy for Acinetobacter baumannii burn infections in mice Antimcrob. Agents Chemother. 2009, 53, 3929-3934
14. Dadachova, E.; Casadevall, A. Antibodies as delivery vehicles for radioimmunotherapy of infectious diseases Expert Opin. Drug Delivery 2005, 2, 1075-1084
15. Antunes, L. C.; Imperi, F.; Minandri, F.; Visca, P. In vitro and in vivo antimicrobial activity of gallium nitrate against multidrug resistant Acinetobacter baumannii Antimcrob. Agents Chemother. 2012, 56, 5961-5970
16. Vila, J.; Martí, S.; Sánchez-Céspedes, J. Porins, efflux pumps and multidrug resistance in Acinetobacter baumannii J. Antimicrob. Chemother. 2007, 59, 1210-1215
17. Ji, C.; Juárez-Hernández, R. E.; Miller, M. J. Exploiting bacterial iron acquisition: siderophore conjugates Future Med. Chem. 2012, 4, 297-313
18. Möllmann, U.; Heinisch, L.; Bauernfeind, A.; Köhler, T.; Ankel-Fuchs, D. Siderophores as drug delivery agents: application of the "Trojan Horse" strategy Biometals 2009, 22, 615-624
19. Ghosh, A.; Ghosh, M.; Niu, C.; Malouin, F.; Moellmann, U.; Miller, M. J. Iron transport-mediated drug delivery using mixed-ligand siderophore-β- lactam conjugates Chem. Biol. 1996, 3, 1011-1019
20. Braun, V.; Pramanik, A.; Gwinner, T.; Köberle, M.; Bohn, E. Sideromycins: tools and antibiotics Biometals 2009, 22, 3-13
21. Ji, C.; Miller, P. A.; Miller, M. J. Iron transport-mediated drug delivery: practical syntheses and in vitro antibacterial studies of tris-catecholate siderophore-aminopenicillin conjugates reveals selectively potent antipseudomonal activity J. Am. Chem. Soc. 2012, 134, 9898-9901
22. Flanagan, M. E.; Brickner, S. J.; Manjinder, L.; Casavant, J.; Deschenes, L.; Finegan, S. M.; George, D. M.; Granskog, K.; Hardink, J. R.; Huband, M. D.; Hoang, T.; Lamb, L.; Marra, A.; Mitton-Fry, M.; Mueller, J. P.; Mullins, L. M.; Noe, M. C.; O'Donnell, J. P.; Pattavina, D.; Penzien, J. B.; Schuff, B. P.; Sun, J.; Whipple, D. A.; Young, J.; Gootz, T. D. Preparation, Gram-negative antibacterial activity, and hydrolytic stability of novel siderophore-conjugated monocarbam diols ACS Med. Chem. Lett. 2011, 385-390
23. Page, M. G. P.; Dantier, C.; Desarbre, E. In vitro properties of BAL30072, a novel siderophore sulfactam with activity against multiresistant Gram-negative bacilli Antimcrob. Agents Chemother. 2010, 54, 2291-2302
24. Heinisch, L.; Wittmann, S.; Stoiber, T.; Berg, A.; Ankel-Fuchs, D.; Möllmann, U. Highly antibacterial active aminoacyl penicillin conjugates with bis-catecholate siderophores based on secondary diamino acids and related compounds J. Med. Chem. 2002, 45, 3032-3040
25. Walsh, C. Antibiotics: Actions, Origins, and Resistance; ASM Press: Washington, DC, 2003.
26. Ghosh, M.; Miller, M. J. Synthesis and in vitro antibacterial activity of spermidine-based mixed catechol- and hydroxamate-containing siderophore-vancomycin conjugates Bioorg. Med. Chem. 1996, 4, 43-48
27. Jung, M. E.; Yang, E. C.; Vu, B. T.; Kiankarimi, M.; Spyrou, E.; Kaunitz, J. Glycosylation of fluoroquinolones through direct oxygenated polymethylene linkages as a sugar-mediated active transport system for antimicrobials J. Med. Chem. 1999, 42, 3899-3909
28. Brochu, A.; Brochu, N.; Nicas, T. I.; Parr, T. R., Jr.; Minnick, A. A., Jr.; Dolence, E. K.; McKee, J. A.; Miller, M. J.; Lavoie, M. C.; Malouin, F. Modes of action and inhibitory activities of new siderophore-β-lactam conjugates that use specific iron uptake pathways for entry into bacteria Antimcrob. Agents Chemother. 1992, 36, 2166-2175
29. Hennard, C.; Truong, Q. C.; Desnottes, J.-F.; Paris, J.-M.; Moreau, N. J.; Abdallah, M. A. Synthesis and activities of pyoverdin-quinolone adducts: a prospective approach to a specific therapy against Pseudomonas aeruginosa J. Med. Chem. 2001, 44, 2139-2151
30. Methods for Dilution: Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically, 8th ed.; CLSI: Villanova, PA, 2009.
31. Pramanik, A.; Braun, V. Albomycin uptake via a ferric hydroxamate transport system of Streptococcus pneumoniae R6 J. Bacteriol. 2006, 188, 3878-3886
32. de Lorenzo, V.; Perez-Martín, J.; Escolar, L.; Pesole, G.; Bertoni, G., Mode of binding of the Fur protein to target DNA: negative regulation of iron-controlled gene expression. In Iron Transport in Bacteria; Crosa, J. H.; Mey, A. R.; Payne, S. M., Eds.; ASM Press: Washington, D.C., 2004; pp 185-196.
33. Bauer, A. W.; Kirby, W. M. M.; Sherris, J. C.; Turck, M. Antibiotic susceptibility testing by a standardized single disk method Am. J. Clin. Pathol. 1966, 45, 493-496
34. Wencewicz, T. A.; Yang, B.; Rudloff, J. R.; Oliver, A. G.; Miller, M. J. N-O Chemistry for antibiotics: discovery of N -alkyl- N -(pyridin-2-yl) hydroxylamine scaffolds as selective antibacterial agents using nitroso Diels-Alder and ene chemistry J. Med. Chem. 2011, 54, 6843-6858
35. Adams, M. D.; Goglin, K.; Molyneaux, N.; Hujer, K. M.; Lavender, H.; Jamison, J. J.; MacDonald, I. J.; Martin, K. M.; Russo, T.; Campagnari, A. A.; Hujer, A. M.; Bonomo, R. A.; Gill, S. R. Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii J. Bacteriol. 2008, 190, 8053-8064
36. Iacono, M.; Villa, L.; Fortini, D.; Bordoni, R.; Imperi, F.; Bonnal, R. J.; Sicheritz-Ponten, T.; De Bellis, G.; Visca, P.; Cassone, A.; Carattoli, A. Whole-genome pyrosequencing of an epidemic multidrug-resistant Acinetobacter baumannii strain belonging to the European clone II group Antimcrob. Agents Chemother. 2008, 52, 2616-2625
37. Smith, M. G.; Gianoulis, T. A.; Pukatzki, S.; Mekalanos, J. J.; Ornston, L. N.; Gerstein, M.; Snyder, M. New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis Genes Dev. 2007, 21, 601-614
38. Vallenet, D.; Nordmann, P.; Barbe, V.; Poirel, L.; Mangenot, S.; Bataille, E.; Dossat, C.; Gas, S.; Kreimeyer, A.; Lenoble, P.; Oztas, S.; Poulain, J.; Segurens, B.; Robert, C.; Abergel, C.; Claverie, J. M.; Raoult, D.; Médique, C.; Weissenbach, J.; Cruveiller, S. Comparative analysis of Acinetobacters: three genomes for three lifestyles PLoS One 2008, 3, e1805
39. Antunes, L. C. S.; Imperi, F.; Towner, K. J.; Visca, P. Genome-assisted identification of putative iron-utilization genes in Acinetobacter baumannii and their distribution among a genotypically diverse collection of clinical isolates Res. Microbiol. 2011, 162, 279-284
40. Eijkelkamp, B. A.; Hassan, K. A.; Paulsen, I. T.; Brown, M. H. Investigation of the human pathogen Acinetobacter baumannii under iron limiting conditions BMC Genomics 2011, 12, 126-139
41. Yamamoto, S.; Okujo, N.; Sakakibara, Y. Isolation and structure elucidation of acinetobactin, a novel siderophore from Acinetobacter baumannii Arch. Microbiol. 1994, 162, 249-254
42. Dorsey, C. W.; Tomaras, A. P.; Connerly, P. L.; Tolmasky, M. E.; Crosa, J. H.; Actis, L. A. The siderophore-mediated iron acquisition systems of Acinetobacter baumannii ATCC 19606 and Vibrio anguillarum 775 are structurally and functionally related Microbiology 2004, 150, 3657-3667
43. Mihara, K.; Tanabe, T.; Yamakawa, Y.; Funahashi, T.; Nakao, H.; Narimatsu, S.; Yamamoto, S. Identification and transcriptional organization of a gene cluster involved in biosynthesis and transport of acinetobactin, a siderophore produced by Acinetobacter baumannii ATCC 19606 Microbiology 2004, 150, 2587-2597
44. Sattely, E. S.; Walsh, C. T. A Latent Oxazoline Electrophile for N-O-C Bond Formation in Pseudomonine Biosynthesis J. Am. Chem. Soc. 2008, 130, 12282-12284
45. Wuest, W. M.; Sattely, E. S.; Walsh, C. T. Three Siderophores from One Bacterial Enzymatic Assembly Line J. Am. Chem. Soc. 2009, 131, 5056-5057
46. Takeuchi, Y.; Ozaki, S.; Satoh, M.; Mimura, K.-I.; Hara, S.-I.; Abe, H.; Nishioka, H.; Harayama, T. Synthesis of Acinetobactin Chem. Pharm. Bull. 2010, 58, 1552-1553
47. Proschak, A.; Lubuta, P.; Grün, P.; Löhr, F.; Wilharm, G.; De Berardinis, V.; Bode, H. B. Structure and Biosynthesis of Fimsbactins A-F, Siderophores from Acinetobacter baumannii and Acinetobacter baylyi ChemBioChem 2013, 14, 633-638
48. Crosa, J. H.; Walsh, C. T. Genetics and Assembly Line Enzymology of Siderophore Biosynthesis in Bacteria Microbiol. Mol. Biol. Rev. 2002, 66, 223-249
49. Mitscher, L. A. Bacterial Topoisomerase Inhibitors: Quinolone and Pyridone Antibacterial Agents Chem. Rev. 2005, 105, 559-592
50. Wencewicz, T. A.; Long, T. E.; Möllmann, U.; Miller, M. J. Trihydroxamate Siderophore-Fluoroquinolone Conjugates are Selective Sideromycin Antibiotics that Target Staphylococcus aureus Bioconjugate Chem. 2013, 24, 473-486
51. Ji, C.; Miller, M. J. Chemical syntheses and in vitro antibacterial activity of two desferrioxamine B-ciprofloxacin conjugates with potential esterase and phosphatase triggered drug release linkers Bioorg. Med. Chem. 2012, 20, 3828-3836
52. Wencewicz, T. A.; Möllmann, U.; Long, T. E.; Miller, M. J. Is drug release necessary for antimicrobial activity of siderophore-drug conjugates? Syntheses and biological studies of the naturally occurring salmycin "Trojan Horse" antibiotics and synthetic desferridanoxamine-antibiotic conjugates Biometals 2009, 22, 633-648
53. Zheng, T.; Bullock, J. L.; Nolan, E. M. Siderophore-Mediated Cargo Delivery to the Cytoplasm of Escherichia coli and Pseudomonas aeruginosa: Syntheses of Monofunctionalized Enterobactin Scaffolds and Evaluation of Enterobactin-Cargo Conjugate Uptake J. Am. Chem. Soc. 2012, 134, 18388-18400
54. Murray, P. R.; Baron, E. J.; Pfaller, M. A.; Tenover, F. C.; Yolken, R. H. Manual of Clinical Microbiology. 7th ed.; American Society for Microbiology: Washington, DC, 1999.