Antibacterial Activity of Sophoraflavanone G Isolated from the Roots of Sophora flavescens

  • Cha, Jeong-Dan (Institute of Oral Bioscience and Department of Oral Microbiology, School of Dentistry, Chonbuk National University) ;
  • Jeong, Mi-Ran (Research Center of Bioactive Materials, Chonbuk National University) ;
  • Jeong, Seung-Il (Jeonju Biomaterials Institute) ;
  • Lee, Kyung-Yeol (Institute of Oral Bioscience and Department of Oral Microbiology, School of Dentistry, Chonbuk National University)
  • Published : 2007.05.31

Abstract

This study investigated the antibacterial activities of sophoraflavanone G from Sophora flavescens in combination with two antimicrobial agents against oral bacteria. The combined effect of sophoraflavanone G and the antimicrobial agents was evaluated using the checkerboard method to obtain a fractional inhibitory concentration(FIC) index. The sophoraflavanone G+ampicillin(AM) combination was found to have a synergistic effect against S. mutans, S. sanguinis, S. sobrinus, S. gordonii, A. actinomycetemcomitans, F nucleatum, P. intermedia, and P. gingivalis, whereas the sophoraflavanone G+gentamicin(GM) combination had a synergistic effect against S. sanguinis, S. criceti, S. anginosus, A. actinomycetemcomitans, F nucleatum, P. intermedia, and P. gingivalis. Neither combination exhibited any antagonistic interactions(FIC index>4). In particular, the MICs/MBCs for all the bacteria were reduced to one-half$\sim$one-sixteenth as a result of the drug combinations. A synergistic interaction was also confirmed by time-kill studies for nine bacteria where the checkerboard suggested synergy. Thus, a strong bactericidal effect was exerted through the drug combinations, plus in vitro data suggested that sophoraflavanone G combined with other antibiotics may be microbiologically beneficial rather than antagonistic.

Keywords

References

  1. Al-Lafi, T. and H. Ababneh. 1995. The effect of the extract of the miswak (chewing sticks) used in Jordan and the Middle East on oral bacteria. Int. Dent. J. 45: 218-222
  2. Botelho, M. G. 2005. The antimicrobial activity of a dentin conditioner combined with antibacterial agents. Oper. Dent. 30: 75-82
  3. Cha, J. D., M. R. Jeong, S. C. Jeong, S. E. Moon, J. Y. Kim, B. S. Kil, and Y. H. Song. 2005. Chemical composition and antimicrobial activity of the essential oils of Artemisia scoparia and A. capillaries. Planta Med. 2: 186-190
  4. Chen, L., X. Cheng, W. Shi, Q. Lu, V. L. Go, D. Heber, and L. Ma. 2000. Inhibition of growth of Streptococcus mutans, methicillin-resistant Staphylococcus aureus, and vancomycinresistant enterococci by kurarinone, a bioactive flavonoid isolated from Sophora flavescens. J. Clin. Microbiol. 43: 3574-3575 https://doi.org/10.1128/JCM.43.7.3574-3575.2005
  5. Climo, M. W., R. L. Patron, and G. L. Archer. 1999. Combinations of vancomycin and beta-lactams are synergistic against staphylococci with reduced susceptibilities to vancomycin. Antimicrob. Agents Chemother. 43: 1747- 1753
  6. Dai, S., M. Y. Chan, S. S. Lee, and C. W. Ogle. 1986. The antiarrhythmic effects of Sophora flavescens Ait. in rats and mice. Am. J. Chin. Med. 14: 119-123 https://doi.org/10.1142/S0192415X86000193
  7. DeNaeyer, A., W. Vander Berghe, V. Pocock, S. Milligan, G. Haegeman, and D. De Keukeleire. 2004. Estrogenic and anticarcinogenic properties of kurarinone, a lavandulyl flavanone from the roots of Sophora flavescens. J. Nat. Prod. 67: 1829-1832 https://doi.org/10.1021/np040069a
  8. Ding, P. L., Z. X. Liao, H. Huang, P. Zhou, and D. F. Chen. 2006. (+)-12alpha-Hydroxysophocarpine, a new quinolizidine alkaloid and related anti-HBV alkaloids from Sophora flavescens. Bioorg. Med. Chem. Lett. 16: 1231-1235 https://doi.org/10.1016/j.bmcl.2005.11.073
  9. Hamada, S. and H. D. Slade. 1980. Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol. Rev. 44: 331-384
  10. Hirobumi, Y., Z. Ping, and I. Kenichiro. 2002. Origin of two isoprenoid units in a lavandulyl moiety of sophoraflavanone G from Sophora flavescens cultured cells. Phytochemistry 60: 263-267 https://doi.org/10.1016/S0031-9422(02)00111-5
  11. Hsiang, C. Y., C. L. Hsieh, S. L. Wu, I. L. Lai, and T. Y. Ho. 2001. Inhibitory effect of anti-pyretic and anti-inflammatory herbs on herpes simplex virus replication. Am. J. Chin. Med. 29: 459-467 https://doi.org/10.1142/S0192415X01000472
  12. Iinuma, M., T. Tanaka, M. Mizuno, Y. Shirataki, I. Yokoe, M. Komatsu, and F. A Lang. 1990. Two flavanones in Sophora leachiano and some related structures. Phytochemistry 29: 2667-2669 https://doi.org/10.1016/0031-9422(90)85209-X
  13. Jeon, S. M., H. J. Kim, K. B. Lee, J. W. Kim, and M. N. Kim. 2001. Antibacterial effect of the surface-modified biomedical polyurethane against Staphylococcus aureus and Staphylococcus epidermidis. J. Microbiol. Biotechnol. 11: 259-265
  14. Jung, H. J., K. S. Choi, and D. G. Lee. 2005. Synergistic killing effect of synthetic peptide P20 and cefotaxime on methicillin-resistant nosocomial isolates of Staphylococcus aureus. J. Microbiol. Biotechnol. 15: 1039-1046
  15. Jung, H. J., S. S. Kang, J. J. Woo, and J. S. Choi. 2005. A new lavandulylated flavonoid with free radical and ONOOscavenging activities from Sophora flavescens. Arch Pharm. Res. 28: 1333-1336 https://doi.org/10.1007/BF02977897
  16. Kang, T. H., S. J. Jeong, W. G. Ko, N. Y. Kim, B. H. Lee, M. Inagaki, T. Miyamoto, R. Higuchi, and Y. C. Kim. 2000. Cytotoxic lavandulyl flavanones from Sophora flavescens. J. Nat. Prod. 63: 680-681 https://doi.org/10.1021/np990567x
  17. Kim, Y. C., H. S. Kim, Y. Wataya, D. H. Sohn, T. H. Kang, M. S. Kim, Y. M. Kim, G. M. Lee, J. D. Chang, and H. Park. 2004. Antimalarial activity of lavandulyl flavanones isolated from the roots of Sophora flavescens. Biol. Pharm. Bull. 27: 748-750 https://doi.org/10.1248/bpb.27.748
  18. Kitahara, T., Y. Aoyama, Y. Hirakata, S. Kamihira, S. Kohno, N. Ichikawa, M. Nakashima, H. Sasaki, and S. Higuchi. 2006. In vitro activity of lauric acid or myristylamine in combination with six antimicrobial agents against methicillin-resistant Staphylococcus aureus (MRSA). Int. J. Antimicrob. Agents 27: 51-57 https://doi.org/10.1016/j.ijantimicag.2005.08.020
  19. Kuroyanagi, M., T. Arakawa, Y. Hirayama, and T. Hayashi. 1999. Antibacterial and antiandrogen flavonoids from Sophora flavescens. J. Nat. Prod. 62: 1595-1599 https://doi.org/10.1021/np990051d
  20. Lee, M. J., D. H. Bae, D. H. Lee, K. H. Jang, D. H. Oh, and S. D. Ha. 2006. Reduction of Bacillus cereus in cooked rice treated with sanitizers and disinfectants. J. Microbiol. Biotechnol. 16: 639-642
  21. Lee, S. H. and C. J. Kim. 1999. Antibacterial activity of antimycotic miconazole against methicillin-resistant Staphylococcus aureus. J. Microbiol. Biotechnol. 9: 572- 575
  22. Lee, S. W., H. S. Lee, J. Y. Nam, O. E. Kwon, J. A. Baek, J. S. Chang, M. C. Rho, and Y. K. Kim. 2005. Kurarinone isolated from Sophora flavescens Ait inhibited MCP-1- induced chemotaxis. J. Ethnopharmacol. 97: 515-519 https://doi.org/10.1016/j.jep.2004.12.006
  23. Loesche, W. J. 1986. Role of Streptococcus mutans in human dental decay. Microbiol. Rev. 50: 353-380
  24. Mayrand, D. and S. C. Holt. 1988. Biology of a saccharolytic black-pigmented Bacteroides species. Microbiol. Rev. 52: 134-152
  25. Roldan, S., E. G. Winkel, D. Herrera, M. Sanz and A. J. Van Winkelhoff. 2003. The effects of a new mouthrinse containing chlorhexidine, cetylpyridinium chloride and zinc lactate on the microflora of oral halitosis patients: A dualcentre, double-blind placebo-controlled study. J. Clin. Periodontol. 30: 427-434 https://doi.org/10.1034/j.1600-051X.2003.20004.x
  26. Rosan, B. and R. J. Lamont. 2000. Dental plaque formation. Microbes Infect. 2: 1599-1607 https://doi.org/10.1016/S1286-4579(00)01316-2
  27. Ryu, S. Y., S. K. Kim, Z. No, and J. W. Ahn. 1996. A novel flavonoid from Sophora flavescens. Planta Med. 62: 361- 363 https://doi.org/10.1055/s-2006-957906
  28. Saeki, Y., Y. Ito, M. Shibata, Y. Sato, K. Okuda, and I. Takazoe. 1989. Antimicrobial action of natural substances on oral bacteria. Bull. Tokyo Dent. Coll. 30: 129-135
  29. Shiraishi, T. and Y. Nakagawa. 2002. Evaluation of the bactericidal activity of povidone-iodine and commercially available gargle preparations. Dermatology 204: 37-41
  30. Shirataki, Y., I. Yokoe, M. Noguchi, T. Tomimori, and M. Komatsu. 1988. Studies on the constituents of Sophora species XXII. Constituents of the root of Sophora moorcroftiag Benth. Ex Baker(1). Chem. Pharm. Bull. 36: 2220-2225 https://doi.org/10.1248/cpb.36.2220
  31. Slots, J. and M. A. Listgarten. 1988. Bacteroides gingivalis, Bacteroides intermedius and Actinobacillus actinomycetemcomitans in human periodontal diseases. J. Clin. Periodontol. 15: 85-93 https://doi.org/10.1111/j.1600-051X.1988.tb00999.x
  32. Sote, E. O. and M. Wilson. 1995. In-vitro antibacterial effects of extracts of Nigerian tooth-cleaning sticks on periodontopathic bacteria. Afr. Dent. J. 9: 15-19
  33. Sung, W. S., H. J. Jung, I. S. Lee, H. S. Kim, and D. G. Lee. 2006. Antimicrobial effect of furaneol against human pathogenic bacteria and fungi. J. Microbiol. Biotechnol. 16: 349-354
  34. Tashiro, M., F. Suzuki, Y. Shirataki, Y. Yokote, K. Akahane, N. Motohashi, M. Ishihara, Y. Jiang, and H. Sakagami. 2002. Effects of prenylflavanones from Sophora species on growth and activation of mouse macrophage-like cell line. Anticancer Res. 22: 53-58
  35. Tsai, J. C., S. Tsai, and W. C. Chang. 2004. Effect of ethanol extracts of three Chinese medicinal plants with anti-diarrheal properties on ion transport of the rat intestinal epithelia. J. Pharmacol Sci. 94: 60-66 https://doi.org/10.1254/jphs.94.60
  36. Tsuchiya, H., M. Sato, M. Iinuma, J. Yokoyama, M. Ohyama, T. Tanaka, I. Takase, and I. Namikawa. 1994. Inhibition of the growth of cariogenic bacteria in vitro by plant flavanones. Experientia 50: 846-849 https://doi.org/10.1007/BF01956469
  37. van Winklehoff, A. J., T. J. M. van Steenbergen, and J. DeGraaff. 1988. The role of black-pigmented Bacteroides in human oral infections. J. Clin. Periodontol.15: 145-155 https://doi.org/10.1111/j.1600-051X.1988.tb01561.x
  38. Wolinsky, L. E. and E. O. Sote. 1983. Inhibiting effect of aqueous extracts of eight Nigerian chewing sticks on bacterial properties favouring plaque formation. Caries Res. 17: 253-257 https://doi.org/10.1159/000260674
  39. Xiang, Q., M. Q. Tan, and Y. H. Huang. 2002. Anti-leukemia effect of Sophora flavescens combined with the low molecular weight natural tumor suppressor of the human fetal liver and its mechanism. Hunan Yi Ke Da Xue Xue Bao 27: 108-110
  40. Youn, H. J., J. Lakritz, G. E. Rottinghaus, H. S. Seo, D. Y. Kim, M. H. Cho, and A. E. Marsh. 2004. Anti-protozoal efficacy of high performance liquid chromatography fractions of Torilis japonica and Sophora flavescens extracts on Neospora caninum and Toxoplasma gondii. Vet. Parasitol. 125: 409-414 https://doi.org/10.1016/j.vetpar.2004.08.002
  41. Zhang, Y., H. Zhu, G. Ye, C. Huang, Y. Yang, R. Chen, Y. Yu, and X. Cui. 2006. Antiviral effects of sophoridine against coxsackievirus B3 and its pharmacokinetics in rats. Life Sci. 78: 1998-2005 https://doi.org/10.1016/j.lfs.2005.09.034