Effect of methylglyoxal on multidrug-resistant Pseudomonas aeruginosa

Frontiers in Microbiology

Volumn 5, Issue APR, 2014, Pages

  Hayashi, Katsuhiko ^a   Fukushima, Aiko ^a   Hayashi Nishino, Mitsuko ^a   Nishino, Kunihiko ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Drug efflux system; Manuka honey; Methylglyoxal; Multidrug resistance; Pseudomonas aeruginosa

Indexed keywords

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATION; DRUG SENSITIVITY; ESCHERICHIA COLI; GENE AMPLIFICATION; GENE DELETION; GENE MUTATION; HONEY; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS;

EID: 84899686836     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00180     Document Type: Article

References (42)

1. Adams, C. J., Boult, C. H., Deadman, B. J., Farr, J. M., Grainger, M. N. C., Manley-Harris, M., et al. (2009a). Isolation by HPLC and characterization of the bioactive fraction of New Zealand manuka (Leptospermum scoparium) honey. Carbohydr. Res. 344, 2609-2609. doi: 10.1016/j.carres.2009.08.008
2. Adams, C. J., Manley-Harris, M., and Molan, P. C. (2009b). The origin of methylglyoxal in New Zealand manuka (Leptospermum scoparium) honey. Carbohydr. Res. 344, 1050-1053. doi: 10.1016/j.carres.2009.03.020
3. Allen, K. L., Molan, P. C., and Reid, G. M. (1991). A survey of the antibacterial activity of some New Zealand honeys. J. Pharm. Pharmacol. 43, 817-822. doi: 10.1111/j.2042-7158.1991.tb03186.x
4. Blair, S. E., Cokcetin, N. N., Harry, E. J., and Carter, D. A. (2009). The unusual antibacterial activity of medical-grade Leptospermum honey: antibacterial spectrum, resistance and transcriptome analysis. Eur. J. Clin. Microbiol. Infect. Dis. 28, 1199-1208. doi: 10.1007/s10096-009-0763-z
5. Blaser, G., Santos, K., Bode, U., Vetter, H., and Simon, A. (2007). Effect of medical honey on wounds colonised or infected with MRSA. J. Wound Care 16, 325-328.
6. Blattner, F. R., Plunkett, G. 3rd., Bloch, C. A., Perna, N. T., Burland, V., Riley, M., et al. (1997). The complete genome sequence of Escherichia coli K-12. Science 277, 1453-1462. doi: 10.1126/science.277.5331.1453
7. Cooper, R. A., and Anderson, A. (1970). The formation and catabolism of methylglyoxal during glycolysis in Escherichia coli. FEBS Lett. 11, 273-276. doi: 10.1016/0014-5793(70)80546-4
8. Cooper, R. A., Halas, E., and Molan, P. C. (2002a). The efficacy of honey in inhibiting strains of Pseudomonas aeruginosa from infected burns. J. Burn Care Rehabil. 23, 366-370. doi: 10.1097/00004630-200211000-00002
9. Cooper, R. A., Jenkins, L., Henriques, A. F., Duggan, R. S., and Burton, N. F. (2010). Absence of bacterial resistance to medical-grade manuka honey. Eur. J. Clin. Microbiol. Infect. Dis. 29, 1237-1241. doi: 10.1007/s10096-010-0992-1
10. Cooper, R. A., Molan, P. C., and Harding, K. G. (1999). Antibacterial activity of honey against strains of Staphylococcus aureus from infected wounds. J. R. Soc. Med. 92, 283-285.
11. Cooper, R. A., Molan, P. C., and Harding, K. G. (2002b). The sensitivity to honey of Gram-positive cocci of clinical significance isolated from wounds. J. Appl. Microbiol. 93, 857-863. doi: 10.1046/j.1365-2672.2002.01761.x
12. Datsenko, K. A., and Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645. doi: 10.1073/pnas.120163297
13. Davis, R. W., Bolstein, D., and Roth, J. R. (1980). Advanced Bacterial Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
14. Fields, P. I., Swanson, R. V., Haidaris, C. G., and Heffron, F. (1986). Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. U.S.A. 83, 5189-5193. doi: 10.1073/pnas.83.14.5189
15. Gethin, G., and Cowman, S. (2008). Bacteriological changes in sloughy venous leg ulcers treated with manuka honey or hydrogel: an RCT. J. Wound Care 17, 241-244, 246-247.
16. Henriques, A. F., Jenkins, R. E., Burton, N. F., and Cooper, R. A. (2010). The intracellular effects of manuka honey on Staphylococcus aureus. Eur. J. Clin. Microbiol. Infect. Dis. 29, 45-50. doi: 10.1007/s10096-009-0817-2
17. Horiyama, T., Nikaido, E., Yamaguchi, A., and Nishino, K. (2011). Roles of Salmonella multidrug efflux pumps in tigecycline resistance. J. Antimicrob. Chemother. 66, 105-110. doi: 10.1093/jac/dkq421
18. Horiyama, T., Yamaguchi, A., and Nishino, K. (2010). TolC dependency of multidrug efflux systems in Salmonella enterica serovar Typhimurium. J. Antimicrob. Chemother. 65, 1372-1376. doi: 10.1093/jac/dkq160
19. Jenkins, R., and Cooper, R. (2012). Improving antibiotic activity against wound pathogens with manuka honey in vitro. PLoS ONE 7:e45600. doi: 10.1371/journal.pone.0045600
20. Jervis-Bardy, J., Foreman, A., Bray, S., Tan, L., and Wormald, P. J. (2011). Methylglyoxal-infused honey mimics the anti-Staphylococcus aureus biofilm activity of manuka honey: potential implication in chronic rhinosinusitis. Laryngoscope 121, 1104-1107. doi: 10.1002/lary.21717
21. Krymkiewicz, N., Dieguez, E., Rekarte, U. D., and Zwaig, N. (1971). Properties and mode of action of a bactericidal compound (=methylglyoxal) produced by a mutant of Escherichia coli. J. Bacteriol. 108, 1338-1347.
22. Kwakman, P. H., de Boer, L., Ruyter-Spira, C. P., Creemers-Molenaar, T., Helsper, J. P., Vandenbroucke-Grauls, C. M., et al. (2011). Medical-grade honey enriched with antimicrobial peptides has enhanced activity against antibiotic-resistant pathogens. Eur. J. Clin. Microbiol. Infect. Dis. 30, 251-257. doi: 10.1007/s10096-010-1077-x
23. Kwakman, P. H., te Velde, A. A., de Boer, L., Speijer, D., Vandenbroucke-Grauls, C. M., and Zaat, S. A. (2010). How honey kills bacteria. FASEB J. 24, 2576-2582. doi: 10.1096/fj.09-150789
24. Lister, P. D., Wolter, D. J., and Hanson, N. D. (2009). Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin. Microbiol. Rev. 22, 582-610. doi: 10.1128/CMR.00040-09
25. Mavric, E., Wittmann, S., Barth, G., and Henle, T. (2008). Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand. Mol. Nutr. Food Res. 52, 483-489. doi: 10.1002/mnfr.200700282
26. Nakashima, R., Sakurai, K., Yamasaki, S., Nishino, K., and Yamaguchi, A. (2011). Structures of the multidrug exporter AcrB reveal a proximal multisite drug-binding pocket. Nature 480, 565-569. doi: 10.1038/nature10641
27. Natarajan, S., Williamson, D., Grey, J., Harding, K. G., and Cooper, R. A. (2001). Healing of an MRSA-colonized, hydroxyurea-induced leg ulcer with honey. J. Dermatol. Treat. 12, 33-36. doi: 10.1080/095466301750163563
28. Nikaido, H. (1996). Multidrug efflux pumps of gram-negative bacteria. J. Bacteriol. 178, 5853-5859.
29. Nikaido, H. (2011). Structure and mechanism of RND-type multidrug efflux pumps. Adv. Enzymol. Relat. Areas Mol. Biol. 77, 1-60. doi: 10.1002/9780470920541.ch1
30. Nikaido, H., and Pages, J. M. (2012). Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria. FEMS Microbiol. Rev. 36, 340-363. doi: 10.1111/j.1574-6976.2011.00290.x
31. Nishino, K., Latifi, T., and Groisman, E. A. (2006). Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 59, 126-141. doi: 10.1111/j.1365-2958.2005.04940.x
32. Nishino, K., Yamada, J., Hirakawa, H., Hirata, T., and Yamaguchi, A. (2003). Roles of TolC-dependent multidrug transporters of Escherichia coli in resistance to beta-lactams. Antimicrob. Agents Chemother. 47, 3030-3033. doi: 10.1128/AAC.47.9.3030-3033.2003
33. Ortega, B., Groeneveld, A. B., and Schultsz, C. (2004). Endemic multidrug-resistant Pseudomonas aeruginosa in critically ill patients. Infect. Control Hosp. Epidemiol. 25, 825-831. doi: 10.1086/502303
34. Piddock, L. J. (2006). Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin. Microbiol. Rev. 19, 382-402. doi: 10.1128/CMR.19.2.382-402.2006
35. Poole, K. (2004). Efflux-mediated multiresistance in Gram-negative bacteria. Clin. Microbiol. Infect. 10, 12-26. doi: 10.1111/j.1469-0691.2004.00763.x
36. Roberts, A. E. L., Maddocks, S. E., and Cooper, R. A. (2012). Manuka honey is bactericidal against Pseudomonas aeruginosa and results in differential expression of oprF and algD. Microbiol. 158, 3005-3013. doi: 10.1099/mic.0.062794-0
37. Sekiguchi, J. I., Asagi, T., Miyoshi-Akiyama, T., Kasai, A., Mizuguchi, Y., Araake, M., et al. (2007). Outbreaks of multidrug-resistant Pseudomonas aeruginosa in community hospitals in Japan. J. Clin. Microbiol. 45, 979-989. doi: 10.1128/JCM.01772-06
38. Sekiya, H., Mima, T., Morita, Y., Kuroda, T., Mizushima, T., and Tsuchiya, T. (2003). Functional cloning and characterization of a multidrug efflux pump, mexHI-opmD, from a Pseudomonas aeruginosa mutant. Antimicrob. Agents Chemother. 47, 2990-2992. doi: 10.1128/AAC.47.9.2990-2992.2003
39. Stover, C. K., Pham, X. Q., Erwin, A. L., Mizoguchi, S. D., Warrener, P., Hickey, M. J., et al. (2000). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959-964. doi: 10.1038/35023079
40. Visavadia, B. G., Honeysett, J., and Danford, M. (2008). Manuka honey dressing: an effective treatment for chronic wound infections. Br. J. Oral Maxillofac. Surg. 46, 696-697. doi: 10.1016/j.bjoms.2007.12.014
41. Weston, R. J., Mitchell, K. R., and Allen, K. L. (1999). Antibacterial phenolic components of New Zealand manuka honey. Food Chem. 64, 295-301. doi: 10.1016/S0308-8146(98)00100-9
42. Yamasaki, S., Nagasawa, S., Hayashi-Nishino, M., Yamaguchi, A., and Nishino, K. (2011). AcrA dependency of the AcrD efflux pump in Salmonella enterica serovar Typhimurium. J. Antibiot. 64, 433-437. doi: 10.1038/ja.2011.28