Membrane-permeabilizing activity of reverse-amide 2-aminoimidazole antibiofilm agents against Acinetobacter baumannii

Current Drug Delivery

Volumn 12, Issue 2, 2015, Pages 223-230

  Stowe, Sean D ^a   Thompson, Richele J ^a   Peng, Lingling ^a,b   Su, Zhaoming ^a,c   Blackledge, Meghan S ^a   Logan Draughn, G ^a   Coe, William H ^a   Johannes, Eva ^a   Lapham, Valerie K ^a   Mackenzie, John ^a   Melander, Christian ^a   Cavanagh, John ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

2 aminoimidazole; Acinetobacter baumannii; Biofilm; Membrane permeabilization; Reverse amide; SEM

Indexed keywords

2 AMINOIMIDAZOLE DERIVATIVE; AMIDE; ANTIINFECTIVE AGENT; IMIDAZOLE DERIVATIVE; UNCLASSIFIED DRUG; 2-AMINOIMIDAZOLE;

ACINETOBACTER BAUMANNII; ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BIOFILM; CELL MEMBRANE PERMEABILITY; CELL PERMEABILIZATION; COLORIMETRY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG ACTIVITY; DRUG DISTRIBUTION; DRUG EFFECT; DRUG STRUCTURE; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; STRUCTURE ACTIVITY RELATION; CELL CULTURE; CHEMISTRY; CROSS INFECTION; DRUG EFFECTS; MICROBIAL SENSITIVITY TEST;

ACINETOBACTER BAUMANNII; AMIDES; ANTI-BACTERIAL AGENTS; BIOFILMS; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CROSS INFECTION; IMIDAZOLES; MICROBIAL SENSITIVITY TESTS;

EID: 84930894419     PISSN: 15672018     EISSN: 18755704     Source Type: Journal    
DOI: 10.2174/1567201811666140924125740     Document Type: Article

References (42)

1. Dijkshoorn, L.; Nemec, A.; Seifert, H. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat. Rev. Micro., 2007, 5(12), 939-951.
2. Peleg, A. Y.; Seifert, H.; Paterson, D. L. Acinetobacter baumannii: Emergence of a Successful Pathogen. Clin. Microbiol. Rev., 2008, 21(3), 538-582.
3. McConnell, M. J.; Actis, L.; Pachon, J. Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models. FEMS Microbiol. Rev., 2013, 37(2), 130-155.
4. Jawad, A.; Seifert, H.; Snelling, A. M.; Heritage, J.; Hawkey, P. M. Survival of Acinetobacter baumannii on Dry Surfaces: Comparison of Outbreak and Sporadic Isolates. J. Clin. Microbiol., 1998, 36(7), 1938-1941.
5. Žula, A.; Kikelj, D.; Ilaš, J. 2-Aminoimidazoles in medicinal chemistry. Mini Rev. Med. Chem., 2013, 13, 1921-43.
6. Gaddy, J. A.; Actis, L. A. Regulation of Acinetobacter baumannii biofilm formation. Future Microbiol., 2009, 4(3), 273-278.
7. Lee, H. W.; Koh, Y. M.; Kim, J.; Lee, J. C.; Lee, Y. C.; Seol, S. Y.; Cho, D. T. Capacity of multidrug-resistant clinical isolates of Acinetobacter baumannii to form biofilm and adhere to epithelial cell surfaces. Clin. Microbiol. Infect., 2008, 14(1), 49-54.
8. Tomaras, A. P.; Dorsey, C. W.; Edelmann, R. E.; Actis, L. A. Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperone-usher pili assembly system. Microbiology, 2003, 149(12), 3473-3484.
9. Longo, F.; Vuotto, C.; Donelli, G., Biofilm formation in Acinetobacter baumannii. New Microbiol., 2014, 37, 119-27.
10. Tomaras, A. P.; Flagler, M. J.; Dorsey, C. W.; Gaddy, J. A.; Actis, L. A. Characterization of a two-component regulatory system from Acinetobacter baumannii that controls biofilm formation and cellular morphology. Microbiology, 2008, 154(11), 3398-3409.
11. Barrett, J. F.; Hoch, J. A. Two-Component Signal Transduction as a Target for Microbial Anti-Infective Therapy. Antimicrob. Agents Chemother., 1998, 42(7), 1529-1536.
12. Chow, J. Y.; Yang, Y.; Tay, S. B.; Chua, K. L.; Yew, W. S. Disruption of Biofilm Formation by the Human Pathogen Acinetobacter baumannii Using Engineered Quorum-Quenching Lactonases. Antimicrob. Agents Chemother., 2014, 58(3), 1802-1805.
13. Sambanthamoorthy, K.; Feng, X.; Patel, R.; Patel, S.; Paranavitana, C. Antimicrobial and antibiofilm potential of biosurfactants isolated from lactobacilli against multi-drug-resistant pathogens. BMC Microbiol., 2014, 14(197), doi: 10. 1186/1471-2180-14-197.
14. Reffuveille, F.; de la Fuente-Nunez, C.; Mansour, S.; Hancock, R. E. W. A Broad-Spectrum Antibiofilm Peptide Enhances Antibiotic Action against Bacterial Biofilms. Antimicrob. Agents Chemother., 2014, 58(9), 5363-5371.
15. Nait Chabane, Y.; Mlouka, M.; Alexandre, S.; Nicol, M.; Marti, S.; Pestel-Caron, M.; Vila, J.; Jouenne, T.; De, E. Virstatin inhibits biofilm formation and motility of Acinetobacter baumannii. BMC Microbiol., 2014, 14(62).
16. Hodnik, Z.; Los, J. M.; Zula, A.; Zidar, N.; Jakopin, Z.; Los, M.; Sollner Dolenc, M.; Ilas, J.; Wegrzyn, G.; Peterlin Masic, L.; Kikelj, D. Inhibition of biofilm formation by conformationally constrained indole-based analogues of the marine alkaloid oroidin. Bioorg. Med. Chem. Lett., 2014, 24(11), 2530-2534.
17. Chusri, S.; Na-Phatthalung, P.; Siriyong, T.; Paosen, S.; Voravuthikunchai, S. P. Holarrhena antidysenterica as a resistance modifying agent against Acinetobacter baumannii: Its effects on bacterial outer membrane permeability and efflux pumps. Microbiol. Res., 2014, 169(5-6), 417-424.
18. Zidar, N.; Montalvao, S.; Hodnik, Z.; Nawrot, D.; Zula, A.; Ilas, J.; Kikelj, D.; Tammela, P.; Masic, L. Antimicrobial Activity of the Marine Alkaloids, Clathrodin and Oroidin, and Their Synthetic Analogues. Mar. Drugs, 2014, 12(2), 940-963.
19. Worthington, R. J.; Blackledge, M. S.; Melander, C. Smallmolecule inhibition of bacterial two-component systems to combat antibiotic resistance and virulence. Future Med. Chem., 2013, 5(11), 1265-1284.
20. Wright, C. J.; Wu, H.; Melander, R. J.; Melander, C.; Lamont, R. J. Disruption of heterotypic community development by Porphyromonas gingivalis with small molecule inhibitors. Mol. Oral Microbiol., 2014, 29(5), 185-93.
21. Ballard, T. E.; Richards, J. J.; Wolfe, A. L.; Melander, C., Synthesis and antibiofilm activity of a second-generation reverse-amide oroidin library: a structure-activity relationship study. Chemistry, 2008, 14(34), 10745-61.
22. Richards, J. J.; Huigens III, R. W.; Ballard, T. E.; Basso, A.; Cavanagh, J.; Melander, C. Inhibition and dispersion of proteobacterial biofilms. Chem. Commun., 2008, 14, 1698-1700.
23. Stowe, S. D.; Tucker, A. T.; Thompson, R.; Piper, A.; Richards, J. J.; Rogers, S. A.; Mathies, L. D.; Melander, C.; Cavanagh, J. Evaluation of the toxicity of 2-aminoimidazole antibiofilm agents using both cellular and model organism systems. Drug Chem. Toxicol., 2012, 35(3), 310-315.
24. Thompson, R. J.; Bobay, B. G.; Stowe, S. D.; Olson, A. L.; Peng, L.; Su, Z.; Actis, L. A.; Melander, C.; Cavanagh, J. Identification of BfmR, a Response Regulator Involved in Biofilm Development, as a Target for a 2-Aminoimidazole-Based Antibiofilm Agent. Biochemistry(Mosc)., 2012, 51(49), 9776-9778.
25. Silhavy, T. J.; Kahne, D.; Walker, S. The Bacterial Cell Envelope. Cold Spring Harb. Perspect. Biol., 2010, 2(5).
26. Nikaido, H. Molecular Basis of Bacterial Outer Membrane Permeability Revisited. Microbiol. Mol. Biol. Rev., 2003, 67(4), 593-656.
27. Hancock, R. E. W. The bacterial outer membrane as a drug barrier. Trends Microbiol., 1997, 5(1), 37-42.
28. Nikaido, H.; Vaara, M. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev., 1985, 49(1), 1-32.
29. Osborn, M. J.; Rick, P. D.; Lehmann, V.; Rupprecht, E.; Singh, M., Structure and Biogenesis of the Cell Envelope of Gram-Negative Bacteria. Ann. N. Y. Acad. Sci., 1974, 235(1), 52-65.
30. Rietschel, E. T.; Kirikae, T.; Schade, F. U.; Mamat, U.; Schmidt, G.; Loppnow, H.; Ulmer, A. J.; Zahringer, U.; Seydel, U.; Di Padova, F.; Schreier, M.; Brade, H. Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J., 1994, 8(2), 217-25.
31. Snyder, D. S.; McIntosh, T. J. The Lipopolysaccharide Barrier: Correlation of Antibiotic Susceptibility with Antibiotic Permeability and Fluorescent Probe Binding Kinetics. Biochemistry (Mosc)., 2000, 39(38), 11777-11787.
32. Balakrishna, R.; Wood, S. J.; Nguyen, T. B.; Miller, K. A.; Suresh, K. E. V. K.; Datta, A.; David, S. A. Structural Correlates of Antibacterial and Membrane-Permeabilizing Activities in Acylpolyamines. Antimicrob. Agents Chemother., 2006, 50(3), 852-861.
33. Lehrer, R. I.; Barton, A.; Ganz, T. Concurrent assessment of inner and outer membrane permeabilization and bacteriolysis in E. coli by multiple-wavelength spectrophotometry. J. Immunol. Methods, 1988, 108(1-2), 153-158.
34. Richards, J. J.; Ballard, T. E.; Melander, C. Inhibition and dispersion of Pseudomonas aeruginosa biofilms with reverse amide 2-aminoimidazole oroidin analogues. Org. Biomol. Chem., 2008, 6(8), 1356-1363.
35. Huang, E.; Yousef, A. E. The Lipopeptide Antibiotic Paenibacterin Binds to the Bacterial Outer Membrane and Exerts Bactericidal Activity through Cytoplasmic Membrane Damage. Appl. Environ. Microbiol., 2014, 80(9), 2700-2704.
36. Berleman, J.; Auer, M. The role of bacterial outer membrane vesicles for intra-and interspecies delivery. Environ. Microbiol., 2013, 15(2), 347-354.
37. Moon, D.; Choi, C.; Lee, J.; Choi, C.-W.; Kim, H.-Y.; Park, J.; Kim, S.; Lee, J. Acinetobacter baumannii outer membrane protein a modulates the biogenesis of outer membrane vesicles. The J. Microbiol., 2012, 50(1), 155-160.
38. Dhariwal, A.; Tullu, M. Colistin: Re-emergence of the 'forgotten' antimicrobial agent. J. Postgrad. Med., 2013, 59(3), 208-215.
39. Rogers, S. A.; Huigens, R. W., III; Cavanagh, J.; Melander, C. Synergistic Effects between Conventional Antibiotics and 2-Aminoimidazole-Derived Antibiofilm Agents. Antimicrob. Agents Chemother., 2010, 54(5), 2112-2118.
40. Page, M. P. The Role of the Outer Membrane of Gram-negative Bacteria in Antibiotic Resistance: Ajax' Shield or Achilles' Heel? In Antibiotic Resistance, Coates, A. R. M., Ed. Springer Berlin Heidelberg: 2012; Vol. 211, pp 67-86.
41. Guilhelmelli, F.; Vilela, N.; Albuquerque, P.; Derengowski, L.; Silva-Pereira, I.; Kyaw, C. Antimicrobial development challenges: the various mechanisms of action of antimicrobial peptides and of bacterial resistance. Front. Microbiol., 2013, 4(353).
42. Baquero, F.; Coque, T. M.; Canton, R. Counteracting antibiotic resistance: breaking barriers among antibacterial strategies. Expert Opin. Ther. Targets, 2014, 18(8), 851-861.