Probing the penetration of antimicrobial polymyxin lipopeptides into gram-negative bacteria

Bioconjugate Chemistry

Volumn 25, Issue 4, 2014, Pages 750-760

  Deris, Zakuan Z ^a   Swarbrick, James D ^b   Roberts, Kade D ^b   Azad, Mohammad A K ^a   Akter, Jesmin ^a   Horne, Andrew S ^b   Nation, Roger L ^a   Rogers, Kelly L ^c   Thompson, Phillip E ^b   Velkov, Tony ^a   Li, Jian ^a  

^a SCHOOL OF MEDICAL SCIENCES   (Malaysia)

^b MONASH UNIVERSITY   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CYTOLOGY; MOLECULAR IMAGING; PROBES;

'DRY' [; ANTI-BACTERIAL ACTIVITY; GRAM-NEGATIVE BACTERIA; IMAGING PROBE; LIFE-THREATENING INFECTIONS; LIPOPEPTIDES; MULTIDRUG RESISTANTS; POLYMYXIN B; REGIOSELECTIVE MODIFICATION; RESISTANCE MECHANISMS;

ANTIBIOTICS;

COLISTIN; POLYMYXIN B; ANTIINFECTIVE AGENT;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DRUG DESIGN; DRUG PENETRATION; DRUG SYNTHESIS; GRAM NEGATIVE BACTERIUM; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR IMAGING; MOLECULAR PROBE; NONHUMAN; OUTER MEMBRANE; ACINETOBACTER BAUMANNII; ANALOGS AND DERIVATIVES; ANTIBIOTIC RESISTANCE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; CYTOLOGY; DRUG EFFECTS; ELECTRON MICROSCOPY; GROWTH, DEVELOPMENT AND AGING; KLEBSIELLA PNEUMONIAE; METABOLISM; MICROBIAL SENSITIVITY TEST; PSEUDOMONAS AERUGINOSA; SYNTHESIS;

ACINETOBACTER BAUMANNII; ANTI-BACTERIAL AGENTS; DRUG DESIGN; DRUG RESISTANCE, BACTERIAL; GRAM-NEGATIVE BACTERIA; KLEBSIELLA PNEUMONIAE; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR IMAGING; POLYMYXIN B; PSEUDOMONAS AERUGINOSA;

EID: 84898970487     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc500094d     Document Type: Article

References (62)

1. Boucher, H. W., Talbot, G. H., Benjamin, D. K., Jr., Bradley, J., Guidos, R. J., Jones, R. N., Murray, B. E., Bonomo, R. A., and Gilbert, D. (2013) 10 x 20 Progress - development of new drugs active against gram-negative bacilli: an update from the Infectious Diseases Society of America Clin. Infect. Dis. 56, 1685-94
2. Talbot, G. H., Bradley, J., Edwards, J. E., Jr., Gilbert, D., Scheld, M., and Bartlett, J. G. (2006) Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America Clin. Infect. Dis. 42, 657-68
3. Velkov, T., Roberts, K. D., Nation, R. L., Thompson, P. E., and Li, J. (2013) Pharmacology of polymyxins: new insights into an old class of antibiotics Future Microbiol. 8, 711-24
4. Velkov, T., Thompson, P. E., Nation, R. L., and Li, J. (2010) Structure-activity relationships of polymyxin antibiotics J. Med. Chem. 53, 1898-916
5. Pristovsek, P. and Kidric, J. (2004) The search for molecular determinants of LPS inhibition by proteins and peptides Curr. Top. Med. Chem. 4, 1185-201
6. Ofek, I., Cohen, S., Rahmani, R., Kabha, K., Tamarkin, D., Herzig, Y., and Rubinstein, E. (1994) Antibacterial synergism of polymyxin B nonapeptide and hydrophobic antibiotics in experimental gram-negative infections in mice Antimicrob. Agents Chemother. 38, 374-7
7. Soon, R. L., Velkov, T., Chiu, F., Thompson, P. E., Kancharla, R., Roberts, K., Larson, I., Nation, R. L., and Li, J. (2011) Design, synthesis, and evaluation of a new fluorescent probe for measuring polymyxin- lipopolysaccharide binding interactions Anal. Biochem. 409, 273-83
8. Deris, Z. Z., Yu, H. H., Davis, K., Soon, R. L., Jacob, J., Ku, C. K., Poudyal, A., Bergen, P. J., Tsuji, B. T., Bulitta, J. B., Forrest, A., Paterson, D. L., Velkov, T., Li, J., and Nation, R. L. (2012) The combination of colistin and doripenem is synergistic against Klebsiella pneumoniae at multiple inocula and suppresses colistin resistance in an in vitro pharmacokinetic/ pharmacodynamic model J. Antimicro. Agents. Chemother. 56, 5103-5112
9. Koike, M., Iida, K., and Matsuo, T. (1969) Electron microscopic studies on mode of action of polymyxin J. Bacteriol. 97, 448-52
10. Wang, W., Sass, H. J., Zahringer, U., and Grzesiek, S. (2008) Structure and dynamics of 13C,15N-labeled lipopolysaccharides in a membrane mimetic Angew. Chem., Int. Ed. 47, 9870-4
11. Mares, J., Kumaran, S., Gobbo, M., and Zerbe, O. (2009) Interactions of lipopolysaccharide and polymyxin studied by NMR spectroscopy J. Biol. Chem. 284, 11498-506
12. Zapor, M. J., Erwin, D., Erowele, G., and Wortmann, G. (2008) Emergence of multidrug resistance in bacteria and impact on antibiotic expenditure at a major army medical center caring for soldiers wounded in Iraq and Afghanistan Infect. Control Hosp. Epidemiol. 29, 661-3
13. van Veen, H. W., Margolles, A., Putman, M., Sakamoto, K., and Konings, W. N. (1999) Multidrug resistance in lactic acid bacteria: molecular mechanisms and clinical relevance Antonie Van Leeuwenhoek 76, 347-52
14. Poole, K. (2001) Multidrug resistance in Gram-negative bacteria Curr. Opin. Microbiol. 4, 500-8
15. Nikaido, H. (2009) Multidrug resistance in bacteria Annu. Rev. Biochem. 78, 119-46
16. Crunkhorn, S. (2013) Antibacterial drugs: New antibiotics on the horizon? Nat. Rev. Drug Discovery 12, 99
17. Arrowsmith, J. (2012) A decade of change Nat. Rev. Drug Discovery 11, 17-8
18. Gould, I. M. (2009) Antibiotic resistance: the perfect storm Int. J. Antimicrob. Agents 34 (Suppl 3) S2-5
19. Falagas, M. E., Rafailidis, P. I., Matthaiou, D. K., Virtzili, S., Nikita, D., and Michalopoulos, A. (2008) Pandrug-resistant Klebsiella pneumoniae, Pseudomonas aeruginosa and Acinetobacter baumannii infections: characteristics and outcome in a series of 28 patients Int. J. Antimicrob. Agents 32, 450-4
20. Antoniadou, A., Kontopidou, F., Poulakou, G., Koratzanis, E., Galani, I., Papadomichelakis, E., Kopterides, P., Souli, M., Armaganidis, A., and Giamarellou, H. (2007) Colistin-resistant isolates of Klebsiella pneumoniae emerging in intensive care unit patients: first report of a multiclonal cluster J. Antimicrob. Chemother. 59, 786-90
21. Falagas, M. E. and Bliziotis, I. A. (2007) Pandrug-resistant Gram-negative bacteria: the dawn of the post-antibiotic era? Int. J. Antimicrob. Agents 29, 630-636
22. Valencia, R., Arroyo, L. A., Conde, M., Aldana, J. M., Torres, M. J., Fernandez-Cuenca, F., Garnacho-Montero, J., Cisneros, J. M., Ortiz, C., Pachon, J., and Aznar, J. (2009) Nosocomial outbreak of infection with pan-drug-resistant Acinetobacter baumannii in a tertiary care university hospital Infect. Control Hosp. Epidemiol. 30, 257-63
23. Bergen, P. J., Bulitta, J. B., Forrest, A., Tsuji, B. T., Li, J., and Nation, R. L. (2010) Pharmacokinetic/pharmacodynamic investigation of colistin against Pseudomonas aeruginosa using an in vitro model Antimicrob. Agents Chemother. 54, 3783-9
24. Li, J., Rayner, C. R., Nation, R. L., Owen, R. J., Tan, K. E., and Spelman, D. (2006) Hetero-resistance to colistin in multidrug-resistant Acinetobacter baumannii Antimicrob. Agents Chemother. 50, 2946-50
25. Owen, R. J., Li, J., Nation, R. L., and Spelman, D. (2007) In vitro pharmacodynamics of colistin against Acinetobacter baumannii clinical isolates J. Antimicrob. Chemother. 59, 473-7
26. Tam, V. H., Schilling, A. N., Vo, G., Kabbara, S., Kwa, A. L., Wiederhold, N. P., and Lewis, R. E. (2005) Pharmacodynamics of polymyxin B against Pseudomonas aeruginosa Antimicrob. Agents Chemother. 49, 3624-3630
27. Ko, K. S., Suh, J. Y., Kwon, K. T., Jung, S. I., Park, K. H., Kang, C. I., Chung, D. R., Peck, K. R., and Song, J. H. (2007) High rates of resistance to colistin and polymyxin B in subgroups of Acinetobacter baumannii isolates from Korea J. Antimicrob. Chemother. 60, 1163-7
28. Li, J., Nation, R. L., Turnidge, J. D., Milne, R. W., Coulthard, K., Rayner, C. R., and Paterson, D. L. (2006) Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections Lancet Infect. Dis. 6, 589-601
29. Poirel, L., Labarca, J., Bello, H., Rioseco, M. L., Bernabeu, S., and Nordmann, P. (2014) Emergence of the 16S rRNA methylase RmtG in an extended-spectrum-beta-lactamase-producing and colistin-resistant Klebsiella pneumoniae isolate in Chile Antimicrob. Agents Chemother. 58, 618-9
30. Bahador, A., Taheri, M., Pourakbari, B., Hashemizadeh, Z., Rostami, H., Mansoori, N., and Raoofian, R. (2013) Emergence of rifampicin, tigecycline, and colistin-resistant Acinetobacter baumannii in Iran; spreading of MDR strains of novel International Clone variants Microb. Drug Resist. 19, 397-406
31. Kontopidou, F., Plachouras, D., Papadomichelakis, E., Koukos, G., Galani, I., Poulakou, G., Dimopoulos, G., Antoniadou, A., Armaganidis, A., and Giamarellou, H. (2011) Colonization and infection by colistin-resistant Gram-negative bacteria in a cohort of critically ill patients Clin. Microbiol. Infect. 17, E9-E11
32. Moore, R. A., Bates, N. C., and Hancock, R. E. (1986) Interaction of polycationic antibiotics with Pseudomonas aeruginosa lipopolysaccharide and lipid A studied by using dansyl-polymyxin Antimicrob. Agents Chemother. 29, 496-500
33. Tsubery, H., Ofek, I., Cohen, S., Eisenstein, M., and Fridkin, M. (2002) Modulation of the hydrophobic domain of polymyxin B nonapeptide: effect on outer-membrane permeabilization and lipopolysaccharide neutralization Mol. Pharmacol. 62, 1036-42
34. Tsubery, H., Ofek, I., Cohen, S., and Fridkin, M. (2000) Structure-function studies of polymyxin B nonapeptide: implications to sensitization of gram-negative bacteria J. Med. Chem. 43, 3085-92
35. Tsubery, H., Ofek, I., Cohen, S., and Fridkin, M. (2001) N-terminal modifications of Polymyxin B nonapeptide and their effect on antibacterial activity Peptides 22, 1675-81
36. Benincasa, M., Pacor, S., Gennaro, R., and Scocchi, M. (2009) Rapid and reliable detection of antimicrobial peptide penetration into gram-negative bacteria based on fluorescence quenching Antimicrob. Agents Chemother. 53, 3501-4
37. Gunn, J. S. (2008) The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more Trends Microbiol. 16, 284-90
38. Gunn, J. S., Lim, K. B., Krueger, J., Kim, K., Guo, L., Hackett, M., and Miller, S. I. (1998) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance Mol. Microbiol. 27, 1171-82
39. Gunn, J. S., Ryan, S. S., Van Velkinburgh, J. C., Ernst, R. K., and Miller, S. I. (2000) Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar typhimurium Infect. Immun. 68, 6139-46
40. Schurek, K. N., Sampaio, J. L., Kiffer, C. R., Sinto, S., Mendes, C. M., and Hancock, R. E. (2009) Involvement of pmrAB and phoPQ in polymyxin B adaptation and inducible resistance in non-cystic fibrosis clinical isolates of Pseudomonas aeruginosa Antimicrob. Agents Chemother. 53, 4345-51
41. Shi, Y., Cromie, M. J., Hsu, F. F., Turk, J., and Groisman, E. A. (2004) PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B Mol. Microbiol. 53, 229-41
42. Trent, M. S., Ribeiro, A. A., Lin, S., Cotter, R. J., and Raetz, C. R. (2001) An inner membrane enzyme in Salmonella and Escherichia coli that transfers 4-amino-4-deoxy-L-arabinose to lipid A: induction on polymyxin-resistant mutants and role of a novel lipid-linked donor J. Biol. Chem. 276, 43122-31
43. Soon, R. L., Nation, R. L., Cockram, S., Moffatt, J. H., Harper, M., Adler, B., Boyce, J. D., Larson, I., and Li, J. (2011) Different surface charge of colistin-susceptible and -resistant Acinetobacter baumannii cells measured with zeta potential as a function of growth phase and colistin treatment J. Antimicrob. Chemother. 66, 126-33
44. Nikaido, H. (2003) Molecular basis of bacterial outer membrane permeability revisited Microbiol. Mol. Biol. Rev. 67, 593-656
45. Hancock, R. E. (1997) Antibacterial peptides and the outer membranes of gram-negative bacilli J. Med. Microbiol. 46, 1-3
46. Hancock, R. E. (1997) Peptide antibiotics Lancet 349, 418-22
47. Hancock, R. E. (1997) The bacterial outer membrane as a drug barrier Trends Microbiol. 5, 37-42
48. Hancock, R. E. and Lehrer, R. (1998) Cationic peptides: a new source of antibiotics Trends Biotechnol. 16, 82-8
49. Li, J., Milne, R. W., Nation, R. L., Turnidge, J. D., and Coulthard, K. (2003) Stability of colistin and colistin methanesulfonate in aqueous media and plasma as determined by high-performance liquid chromatography Antimicrob. Agents Chemother. 47, 1364-1370
50. Wayne, P. A. (2013) Clinical and Laboratory Standards Institute. 23rd Informational Supplement M100-S23.
51. Poudyal, A., Howden, B. P., Bell, J. M., Gao, W., Owen, R. J., Turnidge, J. D., Nation, R. L., and Li, J. (2008) In vitro pharmacodynamics of colistin against multidrug-resistant Klebsiella pneumoniae J. Antimicrob. Chemother. 62, 1311-1318
52. Nyberg, N. T., Duus, J. AÌ., and SaÌrensen, O. W. (2005) Heteronuclear two-bond correlation: suppressing heteronuclear three-bond or higher NMR correlations while enhancing two-bond correlations even for vanishing 2J(CH) J. Am. Chem. Soc. 127, 6154-6155
53. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions J. Biomol. NMR 2, 661-5
54. Bartels, C., Xia, T. H., Billeter, M., Guntert, P., and Wuthrich, K. (1995) The program XEASY for computer-supported NMR spectral analysis of biological macromolecules J. Biomol. NMR 6, 1-10
55. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-93
56. Guntert, P. (2004) Automated NMR structure calculation with CYANA Methods Mol. Biol. 278, 353-78
57. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 (51-5) 29-32
58. Ferguson, A. D., Welte, W., Hofmann, E., Lindner, B., Holst, O., Coulton, J. W., and Diederichs, K. (2000) A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins Structure 8, 585-92
59. Pogliano, J., Pogliano, N., and Silverman, J. A. (2012) Daptomycin-mediated reorganization of membrane architecture causes mislocalization of essential cell division proteins J. Bacteriol. 194, 4494-4504
60. Vaara, M. and Vaara, T. (1981) Outer membrane permeability barrier disruption by polymyxin in polymyxin-susceptible and -resistant Salmonella typhimurium J. Antimicrob. Chemother. 19, 578-583
61. Deris, Z. Z., Akter, J., Sivanesan, S., Roberts, K. D., Thompson, P. E., Nation, R. L., Li, J., and Velkov, T. (2014) A secondary mode of action of polymyxins against Gram-negative bacteria involves the inhibition of NADH-quinone oxidoreductase activity J. Antibiot. 67, 147-151
62. SATO, T. (1968) A modified method for lead staining of thin sections J. Electron Microsc. 17, 158-159