A secondary mode of action of polymyxins against Gram-negative bacteria involves the inhibition of NADH-quinone oxidoreductase activity

Journal of Antibiotics

Volumn 67, Issue 2, 2014, Pages 147-151

  Deris, Zakuan Z ^a,b   Akter, Jesmin ^a   Sivanesan, Sivashangarie ^a   Roberts, Kade D ^a   Thompson, Philip E ^a   Nation, Roger L ^a   Li, Jian ^a   Velkov, Tony ^a  

^a MONASH UNIVERSITY   (Australia)

^b SCHOOL OF MEDICAL SCIENCES   (Malaysia)

Author keywords

Acinetobacter baumannii; colistin; Escherichia coli; Klebsiella pneumonia; polymyxin B; type II NADH quinone oxidoreductase

Indexed keywords

COLISTIN; POLYMYXIN B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIDECARENONE;

ACINETOBACTER BAUMANNII; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; COMPETITIVE INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; INHIBITION KINETICS; KLEBSIELLA PNEUMONIAE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY CHAIN;

ACINETOBACTER BAUMANNII; ANTI-BACTERIAL AGENTS; CELL MEMBRANE; COLISTIN; ESCHERICHIA COLI; GRAM-NEGATIVE BACTERIA; KLEBSIELLA PNEUMONIAE; NAD; POLYMYXIN B; QUINONE REDUCTASES; UBIQUINONE;

EID: 84896804072     PISSN: 00218820     EISSN: 18811469     Source Type: Journal    
DOI: 10.1038/ja.2013.111     Document Type: Article

References (47)

1. Li, J. & Nation, R. L. Old polymyxins are back: Is resistance close?. Clin. Infect. Dis. 43, 663-664 (2006
2. Li, J. et al. Colistin: The re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet. Infect. Dis. 6, 589-601 (2006
3. Lim,L.M. et al. Resurgence of colistin: A review of resistance, toxicity, pharmacodynamics, and dosing. Pharmacotherapy 30, 1279-1291 (2010
4. Hancock, R. E. W. Peptide antibiotics. Lancet 349, 418-422 (1997
5. Hancock, R. E. W. & Scott, M. G. The role of antimicrobial peptides in animal defenses. Proc. Natl Acad. Sci. USA 97, 8856-8861 (2000
6. Cho, J. & Kim, S. Non-membrane targets of antimicrobial peptides: Novel therapeutic opportunities?. In Advances in Molecular and Cellular Microbiology 18pp. 128-140 (CABI, Wallingford, 2010
7. Otvos, L. Antibacterial peptides and proteins with multiple cellular targets. J. Pep. Sci. 11, 697-706 (2005
8. Velkov, T., Thompson, P. E., Nation, R. L. & Li, J. Structure-activity relationships of polymyxin antibiotics. J. Med. Chem. 53, 1898-1916 (2010
9. Storm, D. R., Rosenthal, K. S. & Swanson, P. E. Polymyxin and related peptide antibiotics. Annu. Rev. Biochem. 46, 723-763 (1977
10. Teuber, M. Action of polymyxin B on bacterial membranes. Arch. Microbiol. 100, 131-144 (1974
11. Kim, M. S. & Kim, Y. J. Enzymatic properties of the membrane bound NADH oxidase system in the aerobic respiratory chain of Bacillus cereus. J. Biochem. Mol. Biol. 37, 753-756 (2004
12. Kerscher, S., Drose, S., Zickermann, V. & Brandt, U. in Bioenergetics. Results and Problems in Cell Differentiation (Eds Scha?fer, G. & Penefsky, H.) pp. 185-222 (Springer, Berlin/Heidelberg, 2008
13. Yagi, T., Yano, T., Di Bernardo, S. & Matsuno-Yagi, A. Procaryotic complex I (NDH-1), an overview. Biochim. Biophys. Acta. 1364, 125-133 (1998
14. Yagi, T. Bacterial NADH-quinone oxidoreductases. J. Bioenerg. Biomembr. 23, 211-225 (1991
15. Yagi, T. & Matsuno-Yagi, A. The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: The secret unlocked. Biochemistry 42, 2266-2274 (2003
16. Mogi, T. & Kita, K. Gramicidin S and polymyxins: The revival of cationic cyclic peptide antibiotics. Cell Mol. Life Sci. 66, 3821-3826 (2009
17. Mogi, T. et al. Identification of new inhibitors for alternative NADH dehydrogenase (NDH-II). FEMS. Microbiol. Lett. 291, 157-161 (2009
18. Mogi, T. et al. Polymyxin B identified as an inhibitor of alternative NADH dehydrogenase and malate: Quinone oxidoreductase from the gram-positive bacterium Mycobacterium smegmatis. J. Biochem. 146, 491-499 (2009
19. Tochikubo, K., Yasuda, Y. & Kozuka, S. Decreased particulate NADH oxidase activity in Bacillus subtilis spores after polymyxin B treatment. J. Gen. Microbiol. 132, 277-287 (1986
20. Sampson, T. R. et al. Rapid killing of Acinetobacter baumannii by polymyxins is mediated by a hydroxyl radical death pathway. Antimicrob. Agents Chemother. 56, 5642-5649 (2012
21. Azad, MA et al. Structure-activity relationships for the binding of polymyxins with human alpha-1-acid glycoprotein. Biochem. Pharmacol. 84, 278-291 (2012
22. Cao, G et al. Development and validation of a reversed-phase high-performance liquid chromatography assay for polymyxin B in human plasma. J. Antimicrob. Chemother. 62, 1009-1014 (2008
23. Li, J, Milne, RW, Nation, RL, Turnidge, JD & Coulthard, K. Stability of colistin and colistin methanesulfonate in aqueous media and plasma as determined by highperformance liquid chromatography. Antimicrob. Agents Chemother. 47, 1364-1370 (2003
24. Bergen, PJ, Li, J, Rayner, CR & Nation, RL. Colistin methanesulfonate is an inactive prodrug of colistin against Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 50, 1953-1958 (2006
25. Velkov, T et al. Surface changes and polymyxin interactions with a resistant strain of Klebsiella pneumoniae. Innate Immun. (e-pub ahead of print 25 July 2013; doi:10.1177/1753425913493337
26. Li, J et al. Heteroresistance to colistin in multidrug-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother. 50, 2946-2950 (2006
27. EUCAST ECoAST. Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin. Microbiol. Infect. 9, ix-xv (2003
28. Dancey, GF, Levine, AE & Shapiro, BM. The NADH dehydrogenase of the respiratory chain of Escherichia coli. I. Properties of the membrane-bound enzyme, its solubilization, and purification to near homogeneity. J. Biol. Chem. 251, 5911-5920 (1976
29. Matsushita, K, Ohnishi, T & Kaback, HR. NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain. Biochemistry 26, 7732-7737 (1987
30. Copelan, RA. Evaluation of Enzyme Inhibition in Drug Discovery: A Guide for Medicinal Chemist and Pharmacologist. 2nd edn (ed A John Wiley & Sons) 57-201 (Inc. Publication, 2013
31. Dimroth, P & Thomer, A. A primary respiratory Na pump of an anaerobic bacterium: The Na-dependent NADH:quinone oxidoreductase of Klebsiella pneumoniae. Arch. Microbiol. 151, 439-444 (1989
32. Melo, AMP, Bandeiras, TM & Teixeira, M. New insights into type II NAD(P)H:quinone oxidoreductases. Microbiol. Mol. Biol. Rev. 68, 603-616 (2004
33. Krebs, W, Steuber, J, Gemperli, AC & Dimroth, P. Na translocation by the NADH:ubiquinone oxidoreductase (complex I) from Klebsiella pneumoniae. Mol. Microbiol. 33, 590-598 (1999
34. Steuber, J, Schmid, C, Rufibach, M & Dimroth, P. Na translocation by complex I (NADH:quinone oxidoreductase) of Escherichia coli. Mol. Microbiol. 35, 428-434 (2000
35. Shiemke, AK, Arp, DJ & Sayavedra-Soto, LA. Inhibition of membrane-bound methane monooxygenase and ammonia monooxygenase by diphenyliodonium: Implications for electron transfer. J. Bacteriol. 186, 928-937 (2004
36. Biagini, GA et al. Generation of quinolone antimalarials targeting the Plasmodium falciparum mitochondrial respiratory chain for the treatment and prophylaxis of malaria. Proc. Natl Acad. Sci. USA 109, 8298-8303 (2012
37. Bjorklof, K, Zickermann, V & Finel, M. Purification of the 45 kDa, membrane bound NADH dehydrogenase of Escherichia coli (NDH-2) and analysis of its interaction with ubiquinone analogs. FEBS Lett. 467, 105-110 (2000
38. Dong, CK et al. Type II NADH dehydrogenase of the respiratory chain of Plasmodium falciparum and its inhibitors. Bioorg. Med. Chem. Lett. 19, 972-975 (2009
39. Weinstein, EA et al. Inhibitors of type II NADH:menaquinone oxidoreductase represent a class of antitubercular drugs. Proc. Natl Acad. Sci. USA 102, 4548-4553 (2005
40. Koul, A, Arnoult, E, Lounis, N, Guillemont, J & Andries, K. The challenge of new drug discovery for tuberculosis. Nature 469, 483-490 (2011
41. Fisher, N, Bray, PG, Ward, SA & Biagini, GA. Malaria-parasite mitochondrial dehydrogenases as drug targets: Too early to write the obituary. Trends Parasitol. 24, 9-10 (2008
42. Fisher, N, Bray, PG, Ward, SA & Biagini, GA. The malaria parasite type II NADH:quinone oxidoreductase: An alternative enzyme for an alternative lifestyle. Trends Parasitol. 23, 305-310 (2007
43. Biagini, GA et al. Generation of quinolone antimalarials targeting the Plasmodium falciparum mitochondrial respiratory chain for the treatment and prophylaxis of malaria. Proc. Natl Acad. Sci. USA 109, 8298-8303 (2012
44. Velazquez, I & Pardo, JP. Kinetic characterization of the rotenone-insensitive internal NADH: Ubiquinone oxidoreductase of mitochondria from Saccharomyces cerevisiae. Arch. Biochem. Biophys. 389, 7-14 (2001
45. Yano, T, Li, LS, Weinstein, E, Teh, JS & Rubin, H. Steady-state kinetics and inhibitory action of antitubercular phenothiazines on mycobacterium tuberculosis type-II NADH-menaquinone oxidoreductase (NDH-2). J. Biol. Chem. 281, 11456-11463 (2006
46. Teh, JS, Yano, T & Rubin, H. Type II NADH: Menaquinone oxidoreductase of Mycobacterium tuberculosis. Infect. Disord. Drug Targets 7, 169-181 (2007
47. Eschemann, A, Galkin, A, Oettmeier, W, Brandt, U & Kerscher, S. HDQ (1-Hydroxy-2-dodecyl-4(1H)quinolone), a high affinity inhibitor for mitochondrial alternative NADH dehydrogenase: Evidence for a ping-pong mechanism. J. Biol. Chem. 280, 3138-3142 (2005