A microfluidic device for simple and rapid evaluation of multidrug efflux pump inhibitors

Frontiers in Microbiology

Volumn 3, Issue FEB, 2012, Pages

  Iino, Ryota ^a,b   Nishino, Kunihiko ^c   Noji, Hiroyuki ^a,b   Yamaguchi, Akihito ^c   Matsumoto, Yoshimi ^c  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Escherichia coli; Fluorescein di D galactopyranoside; Fluorescence microscopy; Microfluidic channel; Phe Arg naphthylamide; Polymyxin B nonapeptide; Pseudomonas aeruginosa; Pyridopyrimidine

Indexed keywords

EID: 84875206310     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00040     Document Type: Article

References (45)

1. Elkins, C. A., and Mullis, L. B. (2007). Substrate competition studies using whole-cell accumulation assays with the major tripartite multidrug efflux pumps of Escherichia coli. Antimicrob. Agents Chemother. 51, 923-929.
2. Fieldler, F., and Hinz, H. (1994). No intermediate channelling in stepwise hydrolysis of fluorescein di-beta-D-galactoside by beta-galactosidase. Eur. J. Biochem. 222, 75-81.
3. Giske, C. G., Buaro, L., Sunds-fjord, A., and Wretlind, B. (2008). Alterations of porin, pumps, and penicillin-binding proteins in car-bapenem resistant clinical isolates of Pseudomonas aeruginosa. Microb. Drug Resist. 14,23-30.
4. Henrichfreise, B., Wiegand, I., Pfister, W., and Wiedemann, B. (2007). Resistance mechanisms of mul-tiresistant Pseudomonas aeruginosa strains from Germany and correlation with hypermutation. Antimicrob. Agents Chemother. 51, 4062-4070.
5. Kaatz, G. W., Moudgal, V. V., Seo, S. M., and Kristiansen, J. E. (2003). Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus. Antimicrob. Agents Chemother. 47,719-726.
6. Kirikae, T., Mizuguchi, Y., and Arakawa, Y. (2008). Investigation of isolation rates of Pseudomonas aeruginosa with and without multidrug resistance in medical facilities and clinical laboratories in Japan. J. Antimicrob. Chemother. 61, 612-615.
7. 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. Micro-biol Rev. 22, 582-610.
8. Livermore, D. M. (2002). Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin. Infect. Dis. 34, 634-640.
9. Llanes, C., Hocquet, D., Vogne, C., Benali-Baitich, D., Neuwirth, C., and Plesiat, P. (2004). Clinical strains of Pseudomonas aeruginosa overproducing MexAB-OprM and MexXY efflux pumps simultaneously. Antimicrob. Agents Chemother. 48,1797-1802.
10. Lomovskaya, O., Warren, M. S., Lee, A., Galazzo, J., Fronko, R., Lee, M., Blais, J., Cho, D., Chamberland, S., Renau, T., Leger, R., Hecker, S., Watkins, W., Hoshino, K., Ishida, H., and Lee, V. J. (2001). Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrob. Agents Chemother. 45, 105-116.
11. Martins, A., Spengler, G., Rodrigues, L., Viveiros, M., Ramos, J., Martins, M., Couto, I., Fanning, S., Pages, J. M., Bolla, J. M., Molnar, J., and Amaral, L. (2009). pH Modulation of efflux pump activity of multi-drug resistant Escherichia coli: protection during its passage and eventual colonization of the colon. PLoS ONE 4, e6656. doi:10.1371/jour-nal.pone.0006656
12. Masuda, N., Sakagawa, E., Ohya, S., Gotoh, N., Tsujimoto, H., and Nishino, T. (2000). Substrate specificities of MexAB-OprM, MexCD-OprJ, and MexXY-oprM efflux pumps in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44, 3322-3327.
13. Matsumoto, Y., Hayama, K., Sakaki-hara, S., Nishino, K., Noji, H., Iino, R., and Yamaguchi, A. (2011). Evaluation of multidrug efflux pump inhibitors by a new method using microfluidic channels. PLoS ONE 6, e18547. doi:10.1371/journal.pone. 0018547
14. Mesaros, N., Glupczynski, Y., Avrain, L., Caceres, N. E., Tulkens, P. M., and Van Bambeke, F. (2007). A combined phenotypic and genotypic method for the detection of Mex efflux pumps in Pseudomonas aeruginosa. J. Antimicrob. Chemother. 59, 378-386.
15. Mokhonov, V. V., Mokhonova, E. I., Akama, H., and Nakae, T. (2004). Role of the membrane fusion protein in the assembly of resistance-nodulation-cell division multidrug efflux pump in Pseudomonas aeruginosa. Biochem. Biophys. Res. Com-mun. 322, 483-489.
16. Morita, Y., Kimura, N., Mima, T., Mizushima, T., and Tsuchiya, T. (2001). Roles of MexXY-and MexAB-multidrug efflux pumps in intrinsic multidrug resistance of Pseudomonas aeruginosa PAO1. J. Gen. Appl. Microbiol. 47, 27-32.
17. Murakami, S., Nakashima, R., Yamashita, E., Matsumoto, T., and Yamaguchi, A. (2006). Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443, 173-179.
18. Murakami, S., Nakashima, R., Yamashita, E., and Yamaguchi, A. (2002). Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419, 587-593.
19. Nagano, K., and Nikaido, H. (2009). Kinetic behavior of the major multidrug efflux pump AcrB of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 106, 5854-5858.
20. 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.
21. Nishino, K., Senda, Y., and Yamaguchi, A. (2008). The AraC-family regulator GadX enhances multidrug resistance in Escherichia coli by activating expression of mdtEF multidrug efflux genes.J. Infect. Chemother. 14, 23-29.
22. Russo-Marie, F., Roederer, M., Sager, B., Herzenberg, L. A., and Kaiser, D. (1993). Beta-galactosidase activity in single differentiating bacterial cells. Proc. Natl. Acad. Sci. U.S.A. 90, 8194-8198.
23. Ryan, B. M., Dougherty, T. J., Beaulieu, D., Chuang, J., Dougherty, B. A., and Barrett, J. F. (2001). Efflux in bacteria: what do we really know about it? Expert Opin. Investig. Drugs 10, 1409-1422.
24. Satoh, R., Tsukada, H., Tanabe, Y., Tamura, Y., Yamamoto, T., Takano, M., Ozaki, K., Tamura, T., and Gejyo, F. (2008). An outbreak and isolation of drug-resistant Pseudomonas aeruginosa at Niigata University Hospital, Japan. J. Infect. Chemother. 14, 325-329.
25. Schumacher, A., Steinke, P., Bohn-ert, J. A., Akova, M., Jonas, D., and Kern, W. V. (2006). Effect of 1-(1-naphthylmethyl)-piperazine, a novel putative efflux pump inhibitor, on antimicrobial drug susceptibility in clinical isolates of Enter-obacteriaceae other than Escherichia coli. J. Antimicrob. Chemother. 57, 344-348.
26. Schweizer, H. P. (2003). Efflux as a mechanism of resistance to antimicrobials in Pseudomonas aeruginosa and related bacteria: unanswered questions. Genet. Mol. Res. 2,48-62.
27. Sekiguchi, J., Asagi, T., Miyoshi-Akiyama, T., Fujino, T., Kobayashi, I., Morita, K., Kikuchi, Y., Kurat-suji, T., and Kirikae, T. (2005). Multidrug-resistant Pseudomonas aeruginosa strain that caused an outbreak in a neurosurgery ward and its aac(6;)-Iae gene cassette encoding a novel aminoglycoside acetyltransferase. Antimicrob. Agents Chemother. 49, 3734-3742.
28. Sekiguchi, J., Asagi, T., Miyoshi-Akiyama, T., Kasai, A., Mizuguchi, Y., Araake, M., Fujino, T., Kikuchi, H., Sasaki, S., Watari, H., Kojima, T., Miki, H., Kanemitsu, K., Kun-ishima, H., Kikuchi, Y., Kaku, M., Yoshikura, H., Kuratsuji, T., and Kirikae, T. (2007a). Outbreaks of multidrug-resistant Pseudomonas aeruginosa in community hospitals in Japan. J. Clin. Microbiol. 45, 979-989.
29. Sekiguchi, J., Teruya, K., Horii, K., Kuroda, E., Konosaki, H., Mizuguchi, Y., Araake, M., Kawana, A., Yoshikura, H., Kuratsuji, T., Miyazaki, H., and Kirikae, T. (2007b). Molecular epidemiology of outbreaks and containment of drug-resistant Pseudomonas aeruginosa in a Tokyo hospital. J. Infect. Chemother. 13, 418-422.
30. Sennhauser, G., Bukowska, M. A., Briand, C., and Grutter, M. G. (2009). Crystal structure of the multidrug exporter MexB from Pseudomonas aeruginosa. J. Mol. Biol. 389, 134-145.
31. Tohidpour, A., Peerayeh, S. N., Mehrabadi, J. F., and Yazdi, H. R. (2009). Determination of the efflux pump-mediated resistance prevalence in Pseudomonas aeruginosa, using an efflux pump inhibitor. Curr. Microbiol. 59, 352-355.
32. Vaara, M. (1992). Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56, 395-411.
33. Vaara, M. (1993). Outer membrane permeability barrier to azithromycin, clarithromycin, and roxithromycin in gram-negative enteric bacteria. Antimicrob. Agents Chemother. 37, 354-356.
34. Vaara, M. (2009). New approaches in peptide antibiotics. Curr. Opin. Pharmacol. 9,571-576.
35. Vaara, M., and Porro, M. (1996). Group of peptides that act synergis-tically with hydrophobic antibiotics against gram-negative enteric bacteria. Antimicrob. Agents Chemother. 40,1801-1805.
36. Vaara, M., Siikanen, O., Apajalahti, J., Fox, J., Frimodt-Moller, N., He, H., Poudyal, A., Li, J., Nation, R. L., and Vaara, T. (2010). A novel polymyxin derivative that lacks the fatty acid tail and carries only three positive charges has strong synergism with agents excluded by the intact outer membrane. Antimicrob. Agents Chemother. 54, 3341-3346.
37. Vaara, M., and Vaara, T. (1983a). Polycations as outer membrane-disorganizing agents. Antimicrob. Agents Chemother. 24, 114-122.
38. Vaara, M., and Vaara, T. (1983b). Polycations sensitize enteric bacteria to antibiotics. Antimicrob. Agents Chemother. 24, 107-113.
39. Vidal-Aroca, F., Meng, A., Minz, T., Page, M. G. P., and Dreier, J. (2009). Use of resazurin to detect meflo-quine as an efflux-pump inhibitor in Pseudomonas aeruginosa and Escherichia coli. J. Microbiol Methods 79, 232-237.
40. Viljanen, P., and Vaara, M. (1984). Susceptibility of gram-negative bacteria to polymyxin B nonapeptide. Antimicrob. Agents Chemother. 25, 701-705.
41. Vingsbo Lundberg, C., Vaara, T., Frimodt-Moller, N., and Vaara, M. (2010). Novel polymyxin derivatives are effective in treating experimental Escherichia coli peritoneal infection in mice. J. Antimicrob. Chemother. 65,981-985.
42. Viveiros, M., Martins, A., Paixao, L., Rodrigues, L., Martins, M., Couto, I., Fahnrich, E., Kern, W. V., and Amaral,L. (2008). Demonstration of intrinsic efflux activity of Escherichia coli K-12 AG100 by an automated ethidium bromide method. Int. J. Antimicrob. Agents 31, 458-462.
43. Whitesides, G. M., Ostuni, E., Takayama, S., Jiang, X. Y., and Ingber, D. E. (2001). Soft lithography in biology and biochemistry. Annu. Rev. Bio-med. Eng. 3, 335-373.
44. Yang, N. C., and Hu, M. L. (2004). A fluorimetric method using fluores-cein di-beta-D-galactopyranoside for quantifying the senescence-associated beta-galactosidase activity in human foreskin fibroblast Hs68 cells. Anal. Biochem. 325, 337-343.
45. Yoshida, K., Nakayama, K., Ohtsuka, M., Kuru, N., Yokomizo, Y., Sakamoto, A., Takemura, M., Hoshino, K., Kanda, H., Nitanai, H., Namba, K., Imamura, Y., Zhang, J. Z., Lee, V. J., and Watkins, W. J. (2007). MexAB-OprM specific efflux pump inhibitors in Pseudomonas aeruginosa. Part 7: highly soluble and in vivo active quaternary ammonium analogue D13-9001, a potential preclinical candidate. Bioorg. Med. Chem. 15, 7087-7097.