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Microbiology and Biotechnology Letters

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Molecular and Cellular Microbiology / Biomedical Sciences  |  Clinical Microbiology and Biomedical Sciences

Microbiol. Biotechnol. Lett. 2019; 47(3): 465-472

https://doi.org/10.4014/mbl.1901.01007

Received: January 18, 2019; Accepted: February 25, 2019

단삼에 의한 Candida albicans 바이오필름 발달의 억제

Growth of Candida albicans Biofilm is Inhibited by Salvia miltiorrhiza

Heung-Shick Lee 1 and Younhee Kim 2*

1Department of Biotechnology and Bioinformatics, Korea University, Sejongsi 30019, Republic of Korea, 22Department of Korean Medicine, Semyung University, Republic of Korea

Abstract

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Candida albicans is an opportunistic human pathogen that causes infections. Candidiasis is often related to antifungal resistance because the pathogen has the ability to form biofilms. In a previous study, we found that the Salvia miltiorriza ethanol extract demonstrated anticandidal activity by altering membrane permeability and inhibiting the cell wall synthesis in C. albicans. Our results here demonstrate that 78 μg/ ml of the S. miltiorriza extract significantly diminished the early stage biofilms formed by 10 clinical C. albicans isolates by 51.3%; this was analyzed by 2,3-Bis-(2-methoxy-4-nitro-5-sulfophenyl)-2H-tetrazolium-5- carboxanilide salt (XTT) reduction assay. The effect of the S. miltiorrhiza extract on the adhesion of C. albicans cells to polystyrene plates and germ tube formation was examined via microscopic investigation. Although the density of the adhered cells was remarkably reduced up on incubation with 39 μg/ml S. miltiorrhiza extract, germ tube formation by C. albicans was rarely affected. Quantitative real-time PCR analysis showed that the S. miltiorrhiza extract downregulated the expression of C. albicans hypha-specific genes, EAP1 by 34.7% (p < 0.001), ALS1 by 45.0% (p < 0.001), ALS3 by 48.1% (p < 0.001), and ECE1 by 21.3% (p = 0.006), respectively. Our data suggest that the S. miltiorrhiza ethanol extract significantly inhibited the early stage of biofilm formation by C. albicans by interfering with cell adhesion, by downregulating EAP1, ALS1 and ALS3, and presumably by modifying the cell wall and membrane structure.

Keywords: Antifungal, biofilm, Candida albicans, hypha-specific gene, Salvia miltiorrhiza

References

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  1. Pfaller MA, Diekema DJ. 2007. Epidemiology of invasive candidiasis:a persistent public health problem. Clin. Microbiol. Rev. 20: 133-163.
    Pubmed KoreaMed CrossRef
  2. Pfaller M, Neofytos D, Diekema D, Azie N, Meier-Kriesche HU, Quan SP, et al. 2012. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance?) registry, 2004–2008. Diagn. Microbiol. Infect. Dis. 74: 323-331.
    Pubmed CrossRef
  3. Mukaremera L, Lee KK, Mora-Montes HM, Gow NAR. 2017. Candida albicans yeast, pseudohyphal, and hyphal morphogenesis differentially affects immune recognition. Front. Immunol. 8: 629.
    Pubmed KoreaMed CrossRef
  4. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, et al. 1987. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41: 435-464.
    Pubmed CrossRef
  5. Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8: 881-890.
    Pubmed KoreaMed CrossRef
  6. Ramage G, Martínez JP, López‐Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6: 979-986.
    Pubmed CrossRef
  7. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183: 5385-5394.
    Pubmed KoreaMed CrossRef
  8. Douglas LJ. 2003. Candida biofilms and their role in infection. Trends Microbiol. 11: 30-36.
    CrossRef
  9. Ramage G, Saville SP, Thomas DP, Lopez-Ribot JL. 2005. Candida biofilms: an update. Eukaryot. Cell 4: 633-638.
    Pubmed KoreaMed CrossRef
  10. Lee HS, Kim Y. 2014. Antifungal activity of Rheum undulatum on Candida albicans by the changes in membrane permeability. Korean J. Microbiol. 50: 360-367.
    CrossRef
  11. Guarrera PM. 2005. Traditional phytotherapy in central Italy (Marche, Abruzzo, and Latium). Fitoterapia 76: 1-25.
    Pubmed CrossRef
  12. Lee HS, Kim Y. 2016. Antifungal activity of Salvia miltiorrhiza against Candida albicans is associated with the alteration of membrane permeability and (1, 3)-β-D-glucan synthase activity. J. Microbiol. Biotechnol. 26: 610-617.
    Pubmed CrossRef
  13. Park SJ, Choi SJ, Shin WS, Lee HM, Lee KS, Lee KH. 2009. Relationship between biofilm formation ability and virulence of Candida albicans. J. Bacteriol. Virol. 39: 119-124.
    CrossRef
  14. Clinical Laboratory Standards Institute. 2008. Reference method for broth dilution antifungal susceptibility testing of yeasts:approved standard M27-A3, 3rd ed. Wayne: Clinical and Laboratory Standards Institute.
  15. Liu M, Seidel V, Katerere DR, Gray AI. 2007. Colorimetric broth microdilution method for the antifungal screening of plant extracts against yeast. Methods 42: 325-329.
    Pubmed CrossRef
  16. Ramage G, Vande Walle K, Wickes BL, López-Ribot JL. 2001. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob. Agents Chemother. 45: 2475-2479.
    Pubmed KoreaMed CrossRef
  17. Lee HS, Kim Y. 2018. Development of Candida albicans biofilms is diminished by Paeonia lactiflora via obstruction of cell adhesion and cell lysis. J. Microbiol. Biotechnol. 28: 482-490.
    Pubmed CrossRef
  18. Scudiero DA, Shoemaker RH, Paull KD, Monks A, Tierney S, cNofziger TH, et al. 1988. Evaluation of a soluble tetrazolium/formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines. Cancer Res. 48: 4827-4833.
  19. Kucharíková S, Tournu H, Lagrou K, Van Dijck P, Bujdakova H. 2011. Detailed comparison of Candida albicans and Candida glabrata biofilms under different conditions and their susceptibility to caspofungin and anidulafungin. J. Med. Microbiol. 60: 1261-1269.
    Pubmed CrossRef
  20. Li F, Palecek SP. 2003. EAP1, A Candida albicans gene involved in binding human epithelial cells. Eukaryot. Cell 2: 1266-1273.
    Pubmed KoreaMed CrossRef
  21. Ramsook CB, Tan C, Garcia MC, Fung R, Soybelman G, Henry R, et al. 2010. Yeast cell adhesion molecules have functional amyloidforming sequences. Eukaryot. Cell 9: 393-404.
    Pubmed KoreaMed CrossRef
  22. Hoyer LL, Payne TL, Bell M, Myers AM, Scherer S. 1998. Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr. Genet. 33: 451-459.
    Pubmed CrossRef
  23. Liu Y, Filler SG. 2011. Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryot. Cell 10: 168-173.
    Pubmed KoreaMed CrossRef
  24. Birse CE, Irwin MY, Fonzi WA, Sypherd PS. 1993. Cloning and characterization of ECE1, a gene expressed in association with cell elongation of the dimorphic pathogen Candida albicans. Infect. Immun. 61: 3648-3655.
  25. Moyes DL, Wilson D, Richardson JP, Mogavero S, Tang SX, Wernecke J, et al. 2016. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature 532: 64.
    Pubmed KoreaMed CrossRef
  26. Staab JF, Sundstrom P. 1998. Genetic organization and sequence analysis of the hypha‐specific cell wall protein gene HWP1 of Candida albicans. Yeast 14: 681-686.
    CrossRef
  27. Richardson MD, Smith H. 1981. Production of germ tubes by virulent and attenuated strains of Candida albicans. J. Infect. Dis. 144: 565-569.
    Pubmed CrossRef

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