The plant alkaloid piperine as a potential inhibitor of ethidium bromide efflux in Mycobacterium smegmatis

References

1. Atal C. K., Zutshi U., Rao P. G. 1981; Scientific evidence on the role of ayurvedic herbals on bioavailability of drugs. J Ethnopharmacol 4:229–232 [CrossRef]
   [Google Scholar]
2. Atal C. K., Dubey R. K., Singh J. 1985; Biochemical basis of enhanced drug bioavailability by piperine: evidence that piperine is a potent inhibitor of drug metabolism. J Pharmacol Exp Ther 232:258–262
   [Google Scholar]
3. Badmaev V., Majeed M., Norkus E. P. 1999; Piperine, an alkaloid derived from black pepper, increases serum response of β -carotene during 14 days of oral β -carotene supplementation. Nutr Res 19:381–388 [CrossRef]
   [Google Scholar]
4. Bhardwaj R. K., Glaeser H., Becquemont L., Klotz U., Gupta S. K., Fromm M. F. 2002; Piperine, a major constituent of black pepper, inhibits human P-glycoprotein and CYP3A4. J Pharmacol Exp Ther 302:645–650 [CrossRef]
   [Google Scholar]
5. Bigi F., Alito A., Romano M. I., Zumarraga M., Caimi K., Cataldi A. 2000; The gene encoding P27 lipoprotein and a putative antibiotic-resistance gene form an operon in Mycobacterium tuberculosis and Mycobacterium bovis . Microbiology 146:1011–1018
   [Google Scholar]
6. Bloom B. R., Murray C. J. 1992; Tuberculosis: commentary on a reemergent killer. Science 257:1055–1064 [CrossRef]
   [Google Scholar]
7. Chacon O., Feng Z., Harris N. B., Cáceres N. E., Adams L. G., Barletta R. G. 2002; Mycobacterium smegmatis d-alanine racemase mutants are not dependent on d-alanine for growth. Antimicrob Agents Chemother 46:47–54 [CrossRef]
   [Google Scholar]
8. NCCLS 2003 Susceptibility Testing of Mycobacteria, Nocardiae, and Other Aerobic Actinomycetes , approved standard M24-A Wayne, PA: National Committee for Clinical Laboratory Standards;
   [Google Scholar]
9. Coldham N. G., Webber M., Woodward M. J., Piddock L. J. 2010; A 96-well plate fluorescence assay for assessment of cellular permeability and active efflux in Salmonella enterica serovar Typhimurium and Escherichia coli . J Antimicrob Chemother 65:1655–1663 [CrossRef]
   [Google Scholar]
10. Couto I., Costa S. S., Viveiros M., Martins M., Amaral L. 2008; Efflux-mediated response of Staphylococcus aureus exposed to ethidium bromide. J Antimicrob Chemother 62:504–513 [CrossRef]
    [Google Scholar]
11. De Rossi E., Ainsa J. A., Riccardi G. 2006; Role of mycobacterial efflux transporters in drug resistance: an unresolved question. FEMS Microbiol Rev 30:36–52 [CrossRef]
    [Google Scholar]
12. Eilam Y. 1983; Membrane effects of phenothiazines in yeasts. I. Stimulation of calcium and potassium fluxes. Biochim Biophys Acta 733:242–248 [CrossRef]
    [Google Scholar]
13. EUCAST–ESCMID 2000; EUCAST Definitive Document E.Def 1.2; May 2000; Terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. Clin Microbiol Infect 6:503–508 [CrossRef]
    [Google Scholar]
14. Farrow M. F., Rubin E. J. 2008; Function of a mycobacterial major facilitator superfamily pump requires a membrane-associated lipoprotein. J Bacteriol 190:1783–1791 [CrossRef]
    [Google Scholar]
15. Flores A. R., Parsons L. M., Pavelka M. S. Jr 2005; Genetic analysis of the β -lactamases of Mycobacterium tuberculosis and Mycobacterium smegmatis and susceptibility to β -lactam antibiotics. Microbiology 151:521–532 [CrossRef]
    [Google Scholar]
16. Gibbons S., Oluwatuyi M., Kaatz G. W. 2003; A novel inhibitor of multidrug efflux pumps in Staphylococcus aureus . J Antimicrob Chemother 51:13–17
    [Google Scholar]
17. Gupta A. K., Chauhan D. S., Srivastava K., Das R., Batra S., Mittal M., Goswami P., Singhal N., Sharma V. D. other authors 2006; Estimation of efflux mediated multi-drug resistance and its correlation with expression levels of two major efflux pumps in mycobacteria. J Commun Dis 38:246–254
    [Google Scholar]
18. Jennings B. R., Ridler P. J. 1983; Interaction of chromosomal stains with DNA. An electrofluorescence study. Biophys Struct Mech 10:71–79 [CrossRef]
    [Google Scholar]
19. Kaatz G. W., Moudgal V. V., Seo S. M., Kristiansen J. E. 2003; Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus . Antimicrob Agents Chemother 47:719–726 [CrossRef]
    [Google Scholar]
20. Khan I. A., Mirza Z. M., Kumar A., Verma V., Qazi G. N. 2006; Piperine, a phytochemical potentiator of ciprofloxacin against Staphylococcus aureus . Antimicrob Agents Chemother 50:810–812 [CrossRef]
    [Google Scholar]
21. Kumar A., Khan I. A., Koul S., Koul J. L., Taneja S. C., Ali I., Ali F., Sharma S., Mirza Z. M. other authors 2008; Novel structural analogues of piperine as inhibitors of the NorA efflux pump of Staphylococcus aureus . J Antimicrob Chemother 61:1270–1276 [CrossRef]
    [Google Scholar]
22. Lechner D., Gibbons S., Bucar F. 2008; Plant phenolic compounds as ethidium bromide efflux inhibitors in Mycobacterium smegmatis . J Antimicrob Chemother 62:345–348 [CrossRef]
    [Google Scholar]
23. Lewis K. 1999; Multidrug resistance: versatile drug sensors of bacterial cells. Curr Biol 9:R403–R407 [CrossRef]
    [Google Scholar]
24. Lomovskaya O., Zgurskaya H. I., Totrov M., Watkins W. J. 2007; Waltzing transporters and ‘the dance macabre’ between humans and bacteria. Nat Rev Drug Discov 6:56–65 [CrossRef]
    [Google Scholar]
25. Marquez B. 2005; Bacterial efflux systems and efflux pumps inhibitors. Biochimie 87:1137–1147 [CrossRef]
    [Google Scholar]
26. Martins A., Spengler G., Rodrigues L., Viveiros M., Ramos J., Martins M., Couto I., Fanning S., Pagès J. M. other authors 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 [CrossRef]
    [Google Scholar]
27. Mohtar M., Johari S. A., Li A. R., Isa M. M., Mustafa S., Ali A. M., Basri D. F. 2009; Inhibitory and resistance-modifying potential of plant-based alkaloids against methicillin-resistant Staphylococcus aureus (MRSA). Curr Microbiol 59:181–186 [CrossRef]
    [Google Scholar]
28. Odds F. C. 2003; Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother 52:1 [CrossRef]
    [Google Scholar]
29. Oluwatuyi M., Kaatz G. W., Gibbons S. 2004; Antibacterial and resistance modifying activity of Rosmarinus officinalis . Phytochemistry 65:3249–3254 [CrossRef]
    [Google Scholar]
30. Rodrigues L., Wagner D., Viveiros M., Sampaio D., Couto I., Vavra M., Kern W. V., Amaral L. 2008; Thioridazine and chlorpromazine inhibition of ethidium bromide efflux in Mycobacterium avium and Mycobacterium smegmatis . J Antimicrob Chemother 61:1076–1082 [CrossRef]
    [Google Scholar]
31. Sharma P., Varma M. V., Chawla H. P., Panchagnula R. 2005; In situ and in vivo efficacy of peroral absorption enhancers in rats and correlation to in vitro mechanistic studies. Farmaco 60:874–883 [CrossRef]
    [Google Scholar]
32. Sharma S., Kumar M., Sharma S., Nargotra A., Koul S., Khan I. A. 2010; Piperine as an inhibitor of Rv1258c, a putative multidrug efflux pump of Mycobacterium tuberculosis . J Antimicrob Chemother 65:1694–1701 [CrossRef]
    [Google Scholar]
33. Sharples D., Brown J. R. 1976; Correlation of the base specificity of DNA-intercalating ligands with their physico-chemical properties. FEBS Lett 69:37–40 [CrossRef]
    [Google Scholar]
34. Singh J., Dubey R. K., Atal C. K. 1986; Piperine-mediated inhibition of glucuronidation activity in isolated epithelial cells of the guinea-pig small intestine: evidence that piperine lowers the endogenous UDP-glucuronic acid content. J Pharmacol Exp Ther 236:488–493
    [Google Scholar]
35. Stavri M., Piddock L. J., Gibbons S. 2007; Bacterial efflux pump inhibitors from natural sources. J Antimicrob Chemother 59:1247–1260 [CrossRef]
    [Google Scholar]
36. Tegos G. P., Masago K., Aziz F., Higginbotham A., Stermitz F. R., Hamblin M. R. 2008; Inhibitors of bacterial multidrug efflux pumps potentiate antimicrobial photoinactivation. Antimicrob Agents Chemother 52:3202–3209 [CrossRef]
    [Google Scholar]
37. Thota N., Koul S., Reddy M. V., Sangwan P. L., Khan I. A., Kumar A., Raja A. F., Andotra S. S., Qazi G. N. 2008; Citral derived amides as potent bacterial NorA efflux pump inhibitors. Bioorg Med Chem 16:6535–6543 [CrossRef]
    [Google Scholar]
38. Victor T. C., van Helden P. D., Warren R. 2002; Prediction of drug resistance in M. tuberculosis : molecular mechanisms, tools, and applications. IUBMB Life 53:231–237 [CrossRef]
    [Google Scholar]
39. Viveiros M., Leandro C., Amaral L. 2003; Mycobacterial efflux pumps and chemotherapeutic implications. Int J Antimicrob Agents 22:274–278 [CrossRef]
    [Google Scholar]
40. Werle M. 2008; Polymeric and low molecular mass efflux pump inhibitors for oral drug delivery. J Pharm Sci 97:60–70 [CrossRef]
    [Google Scholar]
41. WHO 2000 Anti-tuberculosis Drug Resistance in the World . Report no. 2: Prevalence and Trends , WHO/CDS/TB/2000.278 Geneva: World Health Organization;
    [Google Scholar]
42. WHO 2009 Global Tuberculosis Control 2009: Epidemiology, Strategy, Financing , WHO/HTM/TB/2009.411 Geneva: World Health Organization;
    [Google Scholar]