Capsaicin, a novel inhibitor of the NorA efflux pump, reduces the intracellular invasion of Staphylococcus aureus

Journal of Antimicrobial Chemotherapy

Volumn 67, Issue 10, 2012, Pages 2401-2408

  Kalia, Nitin Pal ^a   Mahajan, Priya ^a   Mehra, Rukmankesh ^a   Nargotra, Amit ^a   Sharma, Jai Parkash ^a   Koul, Surrinder ^a   Khan, Inshad Ali ^a  

^a CSIR INDIAN INSTITUTE OF INTEGRATIVE MEDICINE   (India)

Author keywords

Ciprofloxacin; Kill kinetics; Macrophages; Major facilitator superfamily; Post antibiotic effect

Indexed keywords

BACTERIAL PROTEIN; CAPSAICIN; CIPROFLOXACIN; ETHIDIUM BROMIDE; NORA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CELL CULTURE; CELL INVASION; CONTROLLED STUDY; MACROPHAGE; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DOCKING; NONHUMAN; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CAPSAICIN; CELL LINE; CIPROFLOXACIN; ENDOCYTOSIS; ENZYME INHIBITORS; GENE KNOCKOUT TECHNIQUES; MACROPHAGES; MICE; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; STAPHYLOCOCCUS AUREUS; VIRULENCE;

EID: 84866615646     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dks232     Document Type: Article

References (58)

1. Hooper DC. Efflux pumps and nosocomial antibiotic resistance: a primer for hospital epidemiologists. Clin Infect Dis 2005; 40: 1811-7.
2. Webber MA, Piddock LJV. The importance of efflux pumps in bacterial antibiotic resistance. J Antimicrob Chemother 2003; 51: 9-11.
3. Piddock LJ. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev 2006; 19: 382-402.
4. Garzoni C, Kelley WL. Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol 2009; 17: 59-65.
5. Van Bambeke F, Balzi E, Tulkens PM. Antibiotic efflux pumps. Biochem Pharmacol 2000; 60: 457-70.
6. Hsieh PC, Siegel SA, Rogers B et al. Bacteria lacking a multidrug pump: a sensitive tool for drug discovery. Proc Natl Acad Sci USA 1998; 95: 6602-6.
7. Lomovskaya O, Lee A, Hoshino K et al. Use of genetic approach to evaluate the consequences of inhibition of efflux pumps in Pseudomonas aeruginosa. Antimicrob Agents Chemother 1999; 43: 1340-6.
8. Kumar A, Schweizer HP. Bacterial resistance to antibiotics: active efflux and reduced uptake. Adv Drug Deliv Rev 2005; 57: 1486-513.
9. Lawrence LE, Barrett JF. Inhibition of bacterial efflux: needs, opportunities, and strategies. Curr Opin Antiinfect Investig Drugs 2000; 2: 145-53.
10. Poole K. Efflux pumps as antimicrobial resistance mechanisms. Ann Med 2007; 39: 162-76.
11. Yoshida H, Bogaki M, Nakamura S et al. Nucleotide sequence and characterization of the Staphylococcus aureus norA gene, which confers resistance to quinolones. J Bacteriol 1990; 172: 6942-9.
12. Truong-Bolduc QC, Dunman PM, Strahilevitz J et al. MgrA is a multiple regulator of two new efflux pumps in Staphylococcus aureus. J Bacteriol 2005; 187: 2395-405.
13. Truong-Bolduc QC, Strahilevitz J, Hooper DC. NorC a new efflux pump regulated by MgrA of Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50: 1104-7.
14. Huang J, O'Toole P, Shen W et al. Novel chromosomally encoded multidrug efflux transporter MdeA in Staphylococcus aureus. Antimicrob Agents Chemother 2004; 48: 909-17.
15. Yamada Y, Hideka K, Shiota S et al. Gene cloning and characterization of SdrM, a chromosomally-encoded multidrug efflux pump, from Staphylococcus aureus. Biol Pharm Bull 2006; 29: 554-6.
16. Tennent JM, Lyon BR, Gillespie MT et al. Cloning and expression of Staphylococcus aureus plasmid-mediated quaternary ammonium resistance in Escherichia coli. Antimicrob Agents Chemother 1985; 27: 79-83.
17. Kaatz GW, Seo SM, Ruble CA. Efflux mediated fluoroquinolone resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1993; 37: 1086-94.
18. Gibbons S, Moser E, Kaatz GW. Catechin gallates inhibit multidrug resistance (MDR) in Staphylococcus aureus. Planta Med 2004; 70: 1240-2.
19. Kaatz GW, Moudgal VV, Seo SM et al. Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus. Antimicrob Agents Chemother 2003; 47: 719-26.
20. Kaatz GW, Moudgal VV, Seo SM et al. Phenylpiperidine selective serotonin reuptake inhibitors interfere with multidrug efflux pump activity in Staphylococcus aureus. Int J Antimicrob Agents 2003; 22: 254-61.
21. Khan IA, Mirza ZM, Kumar A et al. Piperine, a phytochemical potentiator of ciprofloxacin against Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50: 810-2.
22. Mullin S, Mani N, Grossman TH. Inhibition of antibiotic efflux in bacteria by the novel multidrug resistance inhibitor biricodar (VX-710) and timcodar (VX-853). Antimicrob Agents Chemother 2004; 48: 4171-6.
23. Schmitz F, Fluit A, Luckefahr M et al. The effect of reserpine, an inhibitor of multidrug efflux pumps, on the in vitro activities of ciprofloxacin, sparfloxacin and moxifloxacin against clinical isolates of Staphylococcus aureus. J Antimicrob Chemother 1998; 42: 807-10.
24. Stermitz FR, Lorenz P, Tawara JN et al. Synergy in a medicinal plant: antimicrobial action of berberine potentiated by 5-methoxyhydnocarpin, a multidrug pump inhibitor. Proc Natl Acad Sci USA 2000; 97: 1433-7.
25. Vidaillac C, Guillon J, Arpin C et al. Synthesis of omeprazole analogues and evaluation of these as potential inhibitors of the multidrug efflux pump NorA of Staphylococcus aureus. Antimicrob Agents Chemother 2007; 51: 831-8.
26. Kang JY, Teng CH, Chen C et al. Effect of capsaicin and chilli on ethanol induced gastric mucosal injury in the rat. Gut 1995; 6: 664-9.
27. Park JS, Choi MA, Kim BS et al. Capsaicin protects against ethanol-induced oxidative injury in the gastric mucosa of rats. Life Sci 2000; 67: 3087-93.
28. Han Y, Tan TMC, Lim LY. Effects of capsaicin on P-gp function and expression in Caco-2 cells. Biochem Pharmacol 2006; 71: 1727-34.
29. Virus RM, Gebhart GF. Pharmacologic actions of capsaicin: apparent involvement of substance P and serotonin. Life Sci 1979; 25: 1273-84.
30. Jones NL, Shabib S, Sherman PM. Capsaicin as an inhibitor of the growth of the gastric pathogen Helicobacter pylori. FEMS Microbiol Lett 1997; 146: 223-7.
31. Kaatz GW, Seo SM, Foster TJ. Introduction of a norA promoter region mutation into the chromosome of a fluoroquinolone-susceptible strain of Staphylococcus aureus using plasmid integration. Antimicrob Agents Chemother 1999; 43: 2222-4.
32. Kaatz GW, Seo SM. Inducible NorA-mediated multidrug resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1995; 39: 2650-5.
33. Price CTD, Kaatz GW, Gustafson JE. The multidrug efflux pump NorA is not required for salicylate-induced reduction in drug accumulation by Staphylococcus aureus. Int J Antimicrob Agents 2002; 20: 206-13.
34. Eliopoulos GM, Wennersten CB. Antimicrobial activity of quinupristin- dalfopristin combined with other antibiotics against vancomycin resistant enterococci. Antimicrob Agents Chemother 2002; 46: 1319-24.
35. Eliopoulus GM, Moellering RCJ. Antimicrobial combinations. In: Lorian V, ed. Antibiotics in Laboratory Medicine, 4th edn. Baltimore: Williams & Wilkins, 1996; 330-6.
36. Craig WA, Gudmundsson S. The postantibiotic effect. In: Lorian V, ed. Antibiotics in Laboratory Medicine, 3rd edn. Baltimore: Williams & Wilkins, 1991; 403-31.
37. Drugeon HB, Juvin ME, Bryskier A. Relative potential for selection of fluoroquinolone-resistant Streptococcus pneumoniae strains by levofloxacin: comparison with ciprofloxacin, sparfloxacin and ofloxacin. J Antimicrob Chemother 1999; 43 Suppl C: 55-9.
38. Brenwald NP, Gill MJ, Wise R. Prevalence of putative efflux mechanism among fluoroquinolone-resistant clinical isolates of Streptococcus pneumoniae. Antimicrob Agents Chemother 1998; 42: 2032-5.
39. Cheung AL, Bayles KW. Tissue culture assays used to analyze invasion by Staphylococcus aureus. Curr Protoc Microbiol 2007; Chapter 9: Unit 9C.4 (pp. 4.1-4.7).
40. Maestro, Version 9.2. New York: Schrödinger, 2011. http://www.schrodinger.com/products/14/12/. (27 April 2012, date last accessed).
41. Conf Gen, Version 2.3. New York: Schrödinger, 2011. http://www.schrodinger.com/products/14/26/. (27 April 2012, date last accessed).
42. Lig Prep, Version 2.5. New York: Schrödinger, 2011. http://www.schrodinger.com/products/14/10/. (27 April 2012, date last accessed).
43. Watts KS, Dalal P, Murphy RB et al. ConfGen: a conformational search method for efficient generation of bioactive conformers. J Chem Inf Model 2010; 50: 534-46.
44. Chen I, Foloppe N. Drug-like bioactive structures and conformational coverage with the LigPrep/ConfGen Suite: comparison to programs MOE and Catalyst. J Chem Inf Model 2010; 50: 822-39.
45. Nargotra A, Sharma S, Datt M et al. Structure characterization of NorA, a multidrug resistant efflux pump of Staphylococcus aureus using in silico approaches. In: Abstracts of the Sixth International Conference on Bioinformatics, Hong Kong, 2007. Abstract 33, p. 71.
46. Halgren T. New method for fast and accurate binding-site identification and analysis. Chem Biol Drug Des 2007; 69: 146-8.
47. Glide, Version 5.6. New York: Schrödinger, 2010. http://www.schrodinger.com/products/14/5/. (27 April 2012, date last accessed).
48. Friesner RA, Banks JL, Murphy RB et al. Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J Med Chem 2004; 47: 1739-49.
49. Halgren TA, Murphy RB, Friesner RA et al. Glide: a new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J Med Chem 2004; 47: 1750-9.
50. Marchler-Bauer A, Lu S, Anderson JB et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 2011; 39 (Database issue): D225-9.
51. Li XZ, Nikaido H. Efflux-mediated drug resistance in bacteria: an update. Drugs 2009; 69: 1555-623.
52. Neyfakh A, Bidnenko VF, Chen LB. Efflux-mediated multidrug resistance in Bacillus subtilis: similarities and dissimilarities with the mammalian system. Proc Natl Acad Sci USA 1991; 88: 4781-5.
53. Aeschlimann JR, Dresser LD, Kaatz GW et al. Effects of NorA inhibitors on in vitro antibacterial activities and post antibiotic effects of levofloxacin, ciprofloxacin, and norfloxacin in genetically related strains of Staphylococcus aureus. Antimicrob Agents Chemother 1999; 43: 335-40.
54. Gibbons S, Oluwatuyi M, Kaatz GW. A novel inhibitor of multidrug efflux pumps in Staphylococcus aureus. J Antimicrob Chemother 2003; 53: 13-7.
55. Ba BB, Arpin C, Vidaillac C et al. Activity of gatifloxacin in an in vitro pharmacokinetic-pharmacodynamic model against Staphylococcus aureus strains susceptible to ciprofloxacin or exhibiting various levels and mechanisms of ciprofloxacin resistance. Antimicrob Agents Chemother 2006; 50: 1931-6.
56. Piddock LJ, Johnson MM, Simjee S et al. Expression of efflux pump gene pmrA in fluoroquinolone-resistant and -susceptible clinical isolates of Streptococcus pneumoniae. Antimicrob Agents Chemother 2002; 46: 808-12.
57. Kaatz GW. Bacterial efflux pump inhibition. Curr Opin Investig Drugs 2005; 6: 191-8.
58. Hirakata Y, Kondo A, Hoshino K et al. Efflux pump inhibitors reduce the invasiveness of Pseudomonas aeruginosa. Int J Antimicrob Agents 2009; 34: 343-6.