Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Fungicidal Effect of Prenylated Flavonol, Papyriflavonol A, Isolated from Broussonetia papyrifera (L.) Vent. Against Candida albicans

  • Sohn, Ho-Yong (Department of Food and Nutrition, Andong National University) ;
  • Kwon, Chong-Suk (Department of Food and Nutrition, Andong National University) ;
  • Son, Kun-Ho (Department of Food and Nutrition, Andong National University)
  • Received : 2010.07.13
  • Accepted : 2010.07.22
  • Published : 2010.10.28
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Abstract

Papyriflavonol A (PapA), a prenylated flavonoid [5,7,3',4'-tetrahydroxy-6,5'-di-(${\gamma},{\gamma}$-dimethylallyl)-flavonol], was isolated from the root barks of Broussonetia papyrifera. Our previous study showed that PapA has a broad-spectrum antimicrobial activity against pathogenic bacteria and fungi. In this study, the mode of action of PapA against Candida albicans was investigated to evaluate PapA as an antifungal agent. The minimal inhibitory concentration (MIC) values were 10~25 ${\mu}g/ml$ for C. albicans and Saccharomyces cerevisiae, Gram-negative bacteria (Escherichia coli and Salmonella typhimurium), and Gram-positive bacteria (Staphylococcus epidermidis and Staphylococcus aureus). The kinetics of cell growth inhibition, scanning electron microscopy, and measurement of plasma membrane florescence anisotrophy revealed that the antifungal activity of PapA against C. albicans and S. cerevisiae is mediated by its ability to disrupt the cell membrane integrity. Compared with amphotericin B, a cell-membrane-disrupting polyene antibiotic, the hemolytic toxicity of PapA was negligible. At 10~25 ${\mu}g/ml$ of MIC levels for the tested strains, the hemolysis ratio of human erythrocytes was less than 5%. Our results suggest that PapA could be a therapeutic fungicidal agent having potential as a broad spectrum antimicrobial agent.

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References

  1. Bennis, S., F. Chami, N. Chami, T. Bouchikhi, and A. Remmai. 2004. Surface alteration of Saccharomyces cerevisiae induced by thymol and eugenol. Lett. Appl. Microbiol. 38: 454-458. https://doi.org/10.1111/j.1472-765X.2004.01511.x
  2. Chami, F., N. Chami, S. Bennis, T. Bouchikhi, and A. Remmai. 2005. Oregano and clove essential oils induce surface alteration of Saccharomyces cerevisiae. Phytother. Res. 19: 405-408. https://doi.org/10.1002/ptr.1528
  3. Chen, R. M., L. H. Hu, T. Y. An, J. Li, and Q. Shen. 2002. Natural PTP1B inhibitors from Broussonetia papyrifera. Bioorg. Med. Chem. Lett. 12: 3387-3390. https://doi.org/10.1016/S0960-894X(02)00757-6
  4. Cheng, Z., C. Lin, T. Hwang, and C. Teng. 2001. Broussochalcone A, a potent antioxidant and effective suppressor of inducible nitric oxide synthase in lipopolysaccharide-activated macrophages. Biochem. Pharmacol. 61: 939-946. https://doi.org/10.1016/S0006-2952(01)00543-3
  5. Chi, Y. S., H. G. Jong, K. H. Son, H. W. Chang, S. S. Kang, and H. P. Kim. 2001. Effects of naturally occurring prenylated flavonoids on enzymes metabolizing arachidonic acid: Cyclooxygenases and lipoxygenases. Biochem. Pharmacol. 62: 1185-1191. https://doi.org/10.1016/S0006-2952(01)00773-0
  6. Fernandes, A. R., F. M. Prieto, and I. Sa-Correia. 2000. Modification of plasma membrane lipid order and H+-ATPase activity as part of the response of Saccharomyces cerevisiae to cultivation under mild and high copper stress. Arch. Microbiol. 173: 262-268. https://doi.org/10.1007/s002030000138
  7. Grayer, R. J. and J. B. Harborne. 1994. Survey of antifungal compounds from higher plants. Phytochemistry 37: 19-42. https://doi.org/10.1016/0031-9422(94)85005-4
  8. Hwang, J. H. and B. M. Lee. 2007. Inhibitory effects of plant extracts on tyrosinase, L-DOPA oxidation, and melanin synthesis. J. Toxicol. Environ. Health A 70: 393-407. https://doi.org/10.1080/10937400600882871
  9. Iida, Y., H. Yonemura, K. B. Oh, M. Saito, and H. Matsuoka. 1999. Sensitive screening of antifungal compounds from acetone extracts of medicinal plants with a Bio-Cell Tracer. Yakugaku Zasshi 119: 964-971. https://doi.org/10.1248/yakushi1947.119.12_964
  10. Jones, R. N. and A. L. Barry. 1987. The antimicrobial activity of A-56268 (TE-031) and roxithromycin (RU965) against Legionella using broth microdilution method. J. Antimicrob. Chemother. 19: 841-842. https://doi.org/10.1093/jac/19.6.841
  11. Ko, H. H., S. M. Yu, F. N. Ko, C. M. Teng, and C. N. Lin. 1997. Bioactive constituents of Morus australis and Broussonetia papyrifera. J. Nat. Prod. 60: 1008-1011. https://doi.org/10.1021/np970186o
  12. Ko, H. H., W. L. Chang, and T. M. Lu. 2008. Antityrosinase and antioxidant effects of ent-kaurane diterpenes from leaves of Broussonetia papyrifera. J. Nat. Prod. 71: 1930-1933. https://doi.org/10.1021/np800564z
  13. Kwak, W. J., T. C. Moon, C. X. Lin, H. G. Rhyn, H. Jung, E. Lee, et al. 2003. Papyriflavonol A from Broussonetia papyrifera inhibits the passive cutaneous anaphylaxis reaction and has a secretory phospholipase A2-inhibitory activity. Biol. Pharm. Bull. 26: 299-302. https://doi.org/10.1248/bpb.26.299
  14. Lee, D., K. P. Bhat, H. H. Fong, N. R. Farnsworth, J. M. Pezzuto, and A. D. Kinghorn. 2001. Aromatase inhibitors from Broussonetia papyrifera. J. Nat. Prod. 64: 1286-1293. https://doi.org/10.1021/np010288l
  15. Lee, D. G., Y. Park, I. P. Kim, H. G. Jeong, E. R. Woo, and K. S. Hahm. 2002. Influence on the plasma membrane of Candida albicans by HP (2-9)-magainin 2 (1-12) hybrid peptide. Biochem. Biophys. Res. Comm. 297: 885-889. https://doi.org/10.1016/S0006-291X(02)02230-1
  16. Lee, N. K., K. H. Son, H. W. Chang, S. S. Kang, H. Park, M. Y. Heo, and H. P. Kim. 2004. Prenylated flavonoids as tyrosinase inhibitors. Arch. Pharm. Res. 27: 1132-1135. https://doi.org/10.1007/BF02975118
  17. Lin, L. W., H. Y. Chen, C. R. Wu, P. M. Liao,Y. T. Lin, M. T. Hsieh, and H. Ching. 2008. Comparison with various parts of Broussonetia papyrifera as to the antinociceptive and antiinflammatory activities in rodents. Biosci. Biotechnol. Biochem. 72: 2377-2384. https://doi.org/10.1271/bbb.80276
  18. Mei, R. Q., Y. H. Wang, G. H. Du, G. M. Liu, L. Zhang, and Y. X. Cheng. 2009. Antioxidant lignans from the fruits of Broussonetia papyrifera. J. Nat. Prod. 72: 621-625. https://doi.org/10.1021/np800488p
  19. Pei, R. S., F. Zhou, B. P. Ji, and J. Xu. 2009. Evaluation of combined antibacterial effects of eugenol, cinnamaldehyde, thymol, and carvacrol against E. coli with an improved method. J. Food Sci. 74: M379-M383. https://doi.org/10.1111/j.1750-3841.2009.01287.x
  20. Perry, L. M. and J. Metzger. 1980. Medicinal Plants of East and Southeast Asia: Attributed Properties and Uses MIT Press.
  21. Pinto, E., L. Vale-Silva, C. Cavaleiro, and L. Salgueiro. 2009. Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J. Med. Microbiol. 58: 1454-1462. https://doi.org/10.1099/jmm.0.010538-0
  22. Ryu, H. W., B. W. Lee, M. J. Curtis-Long, S. Jung, Y. B. Ryu, W. S. Lee, and K. H. Park. 2010. Polyphenols from Broussonetia papyrifera displaying potent alpha-glucosidase inhibition. J. Agric. Food Chem. 13: 202-208.
  23. Sohn, H. Y., K. H. Son, C. S. Kwon, G. S. Kwon, and S. S. Kang. 2004. Antimicrobial and cytotoxic activity of 18 prenylated flavonoids isolated from medicinal plants: Morus alba L., Morus mongolica Schneider, Broussoetia papyrifera (L.) Vent, Sophora flavescens Ait and Echinosophora koreensis Nakai. Phytomedicine 11: 666-672. https://doi.org/10.1016/j.phymed.2003.09.005
  24. Son, K. H., S. J. Kwon, H. W. Chang, H. P. Kim, and S. S. Kang. 2001. Papyriflavonol A, a new prenylated flavonol from Broussonetia papyrifera. Fitoterapia 72: 456-458. https://doi.org/10.1016/S0367-326X(00)00329-4
  25. Tsai, F. H., J. C. Lien, L. W. Lin, H. Y. Chen, H. Ching, and C. R. Wu. 2009. Protective effect of Broussonetia papyrifera against hydrogen peroxide-induced oxidative stress in SH-SY5Y cells. Biosci. Biotechnol. Biochem. 73: 1933-1939. https://doi.org/10.1271/bbb.90080
  26. Wong, K. S. and W. K. Tsang. 2009. In vitro antifungal activity of the aqueous extract of Scutellaria baicalensis Georgi root against Candida albicans. Int. J. Antimicrob. Agents 34: 284- 285. https://doi.org/10.1016/j.ijantimicag.2009.03.007
  27. Woo, S. S., Y. K. Park, C. H. Choi, K. S. Hahm, and D. G. Lee. 2007. Mode of antibacterial action of a signal peptide, Pep27 from Streptococcus pneumoniae. Biochem. Biophys. Res. Commun. 363: 806-810. https://doi.org/10.1016/j.bbrc.2007.09.041
  28. Yan, D., C. Jin, X. H. Xiao, and X. P. Dong. 2008. Antimicrobial properties of berberines alkaloids in Coptis chinensis Franch by microcalorimetry. J. Biochem. Biophys. Methods 70: 845-849. https://doi.org/10.1016/j.jbbm.2007.07.009

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