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References

  1. Pfaller MA, Pappas PG, Wingard JR. 2006. Invasive fungal pathogens: current epidemiological trends. Clin. Infect. Dis. 43: S3-S14.
    CrossRef
  2. Martinez LR, Fries BC. 2010. Fungal biofilms: relevance in the setting of human disease. Curr. Fungal Infect. Rep. 4: 266-275.
    Pubmed PMC CrossRef
  3. Ramage G, Martinez JP, Lopez-Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6: 979-986.
    Pubmed CrossRef
  4. Ramage G, Rajendran R, Sherry L, Williams C. 2012. Fungal biofilm resistance. Int. J. Microbiol. 2012: 1-14.
    Pubmed PMC CrossRef
  5. Mathé L, Van Dijck P. 2013. Recent insights into Candida
  6. Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, Köhler JR, et al. 2010. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog. 6: e1000828.
    Pubmed PMC CrossRef
  7. Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA. 2003. Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect. Immun. 71: 4333-4340.
    Pubmed PMC CrossRef
  8. Campbell BC, Chan KL, Kim JH. 2012. Chemosensitization as a means to augment commercial antifungal agents. Front. Microbiol. 3: 79.
    Pubmed PMC CrossRef
  9. Cowen LE. 2008. The evolution of fungal drug resistance:modulating the trajectory from genotype to phenotype. Nat. Rev. Microbiol. 6: 187-198.
    Pubmed CrossRef
  10. Bink A, P ellens K , Cammue B PA, Thevissen K. 2 011. A ntibiofilm strategies: how to eradicate Candida biofilms? Open Mycol. J. 5: 29-38.
  11. Lee HS, Kim Y. 2017. Paeonia lactiflora inhibits cell wall synthesis and triggers membrane depolarization in Candida albicans. J. Microbiol. Biotechnol. 27: 395-404.
    Pubmed CrossRef
  12. 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
  13. 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
  14. 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 PMC CrossRef
  15. Thein ZM, Samaranayake YH, Samaranayake LP. 2007. In vitro biofilm formation of Candida albicans and non-albicans Candida s pecies u nder d ynam ic a nd a naerobic c onditions. Arch. Oral Biol. 52: 761-767.
    Pubmed CrossRef
  16. Skrzypek MS, Binkley J, Binkley G, Miyasato SR, Simison M, Sherlock G. 2017. The Candida Genome Database (CGD):incorporation of Assembly 22, systematic identifiers and visualization of high throughput sequencing data. Nucleic Acids Res. 45: D592-D596.
    Pubmed PMC CrossRef
  17. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. 2012. Primer3 - new capabilities and interfaces. Nucleic Acids Res. 40: e115
    Pubmed PMC CrossRef
  18. 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
  19. Sudbery P, Gow N, Berman J. 2004. The distinct morphogenic states of Candida albicans. Trends Microbiol. 12: 317-324.
    Pubmed CrossRef
  20. Merson-Davies LA, Odds FC. 1989. A morphology index for characterization of cell shape in Candida albicans. J. Gen. Microbiol. 135: 3143-3152.
    CrossRef
  21. Hoyer LL. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9: 176-180.
    CrossRef
  22. Li F, Svarovsky MJ, Karlsson AJ, Wagner JP, Marchillo K, Oshel P, et al. 2007. Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot. Cell 6: 931-939.
    Pubmed PMC CrossRef
  23. 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. Nat. 532: 64-68.
    Pubmed PMC CrossRef
  24. Sundstrom P. 2002. Adhesion in Candida spp. Cell. Microbiol. 4: 461-469.
    Pubmed CrossRef
  25. Schaller M, Borelli C, Korting HC, Hube B. 2005. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48:365-377.
    Pubmed CrossRef
  26. Schaller M, Schackert C, Korting HC, Januschke E, Hube B. 2000. Invasion of Candida albicans correlates with expression of secreted aspartic proteinases during experimental infection of human epidermis. J. Invest. Dermatol. 114: 712-717.
    Pubmed CrossRef
  27. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J. 2012. Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol. Rev. 36: 288-305.
    Pubmed CrossRef
  28. Gow NA, Brown AJ, Odds FC. 2002. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5: 366-371.
    CrossRef
  29. Thompson DS, Carlisle PL, Kadosh D. 2011. Coevolution of morphology and virulence in Candida species. Eukaryot. Cell 10: 1173-1182.
    Pubmed PMC CrossRef
  30. Hoyer LL, Scherer S, Shatzman AR, Livi GP. 1995. Candida albicans ALS1: domains related to a Saccharomyces cerevisiae sexual agglutinin separated by a repeating motif. Mol. Microbiol. 15: 39-54.
    Pubmed CrossRef
  31. 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
  32. Rameau RD, Jackson DN, Beaussart A, Dufrêne YF, Lipke PN. 2016. The human disease-associated Aβ amyloid core sequence forms functional amyloids in a fungal adhesin. MBio 7: e01815-15.
    Pubmed PMC CrossRef
  33. Ram sook CB, T an C , Garcia M C, F ung R, S oybelm an G, Henry R, et al. 2010. Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot. Cell 9: 393404.

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Article

Research article

J. Microbiol. Biotechnol. 2018; 28(3): 482-490

Published online March 28, 2018 https://doi.org/10.4014/jmb.1712.12041

Copyright © The Korean Society for Microbiology and Biotechnology.

Development of Candida albicans Biofilms Is Diminished by Paeonia lactiflora via Obstruction of Cell Adhesion and Cell Lysis

Heung-Shick Lee 1 and Younhee Kim 2*

1Department of Biotechnology and Bioinformatics, Korea University, Sejongsi 30019, Republic of Korea, 2Department of Korean Medicine, Semyung University, Jecheon 27136, Republic of Korea

Correspondence to:Younhee  Kim
ykim@semyung.ac.kr

Received: December 20, 2017; Accepted: January 3, 2018

Abstract

Candida albicans infections are often problematic to treat owing to antifungal resistance, as such infections are mostly associated with biofilms. The ability of C. albicans to switch from a budding yeast to filamentous hyphae and to adhere to host cells or various surfaces supports biofilm formation. Previously, the ethanol extract from Paeonia lactiflora was reported to inhibit cell wall synthesis and cause depolarization and permeabilization of the cell membrane in C. albicans. In this study, the P. lactiflora extract was found to significantly reduce the initial stage of C. albicans biofilms from 12 clinical isolates by 38.4%. Thus, to assess the action mechanism, the effect of the P. lactiflora extract on the adhesion of C. albicans cells to polystyrene and germ tube formation was investigated using a microscopic analysis. The density of the adherent cells was diminished following incubation with the P. lactiflora extract in an acidic medium. Additionally, the P. lactiflora-treated C. albicans cells were mostly composed of less virulent pseudohyphae, and ruptured debris was found in the serumcontaining medium. A quantitative real-time PCR analysis indicated that P. lactiflora downregulated the expression of C. albicans hypha-specific genes: ALS3 by 65% (p = 0.004), ECE1 by 34.9% (p = 0.001), HWP1 by 29.2% (p = 0.002), and SAP1 by 37.5% (p = 0.001), matching the microscopic analysis of the P. lactiflora action on biofilm formation. Therefore, the current findings demonstrate that the P. lactiflora ethanol extract is effective in inhibiting C. albicans biofilms in vitro, suggesting its therapeutic potential for the treatment of biofilmassociated infections.

Keywords: Biofilm, Candida albicans, hypha-specific gene, pseudohypha, qPCR, Paeonia lactiflora

References

  1. Pfaller MA, Pappas PG, Wingard JR. 2006. Invasive fungal pathogens: current epidemiological trends. Clin. Infect. Dis. 43: S3-S14.
    CrossRef
  2. Martinez LR, Fries BC. 2010. Fungal biofilms: relevance in the setting of human disease. Curr. Fungal Infect. Rep. 4: 266-275.
    Pubmed KoreaMed CrossRef
  3. Ramage G, Martinez JP, Lopez-Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6: 979-986.
    Pubmed CrossRef
  4. Ramage G, Rajendran R, Sherry L, Williams C. 2012. Fungal biofilm resistance. Int. J. Microbiol. 2012: 1-14.
    Pubmed KoreaMed CrossRef
  5. Mathé L, Van Dijck P. 2013. Recent insights into Candida
  6. Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, Köhler JR, et al. 2010. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog. 6: e1000828.
    Pubmed KoreaMed CrossRef
  7. Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA. 2003. Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect. Immun. 71: 4333-4340.
    Pubmed KoreaMed CrossRef
  8. Campbell BC, Chan KL, Kim JH. 2012. Chemosensitization as a means to augment commercial antifungal agents. Front. Microbiol. 3: 79.
    Pubmed KoreaMed CrossRef
  9. Cowen LE. 2008. The evolution of fungal drug resistance:modulating the trajectory from genotype to phenotype. Nat. Rev. Microbiol. 6: 187-198.
    Pubmed CrossRef
  10. Bink A, P ellens K , Cammue B PA, Thevissen K. 2 011. A ntibiofilm strategies: how to eradicate Candida biofilms? Open Mycol. J. 5: 29-38.
  11. Lee HS, Kim Y. 2017. Paeonia lactiflora inhibits cell wall synthesis and triggers membrane depolarization in Candida albicans. J. Microbiol. Biotechnol. 27: 395-404.
    Pubmed CrossRef
  12. 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
  13. 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
  14. 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
  15. Thein ZM, Samaranayake YH, Samaranayake LP. 2007. In vitro biofilm formation of Candida albicans and non-albicans Candida s pecies u nder d ynam ic a nd a naerobic c onditions. Arch. Oral Biol. 52: 761-767.
    Pubmed CrossRef
  16. Skrzypek MS, Binkley J, Binkley G, Miyasato SR, Simison M, Sherlock G. 2017. The Candida Genome Database (CGD):incorporation of Assembly 22, systematic identifiers and visualization of high throughput sequencing data. Nucleic Acids Res. 45: D592-D596.
    Pubmed KoreaMed CrossRef
  17. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. 2012. Primer3 - new capabilities and interfaces. Nucleic Acids Res. 40: e115
    Pubmed KoreaMed CrossRef
  18. 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
  19. Sudbery P, Gow N, Berman J. 2004. The distinct morphogenic states of Candida albicans. Trends Microbiol. 12: 317-324.
    Pubmed CrossRef
  20. Merson-Davies LA, Odds FC. 1989. A morphology index for characterization of cell shape in Candida albicans. J. Gen. Microbiol. 135: 3143-3152.
    CrossRef
  21. Hoyer LL. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9: 176-180.
    CrossRef
  22. Li F, Svarovsky MJ, Karlsson AJ, Wagner JP, Marchillo K, Oshel P, et al. 2007. Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot. Cell 6: 931-939.
    Pubmed KoreaMed CrossRef
  23. 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. Nat. 532: 64-68.
    Pubmed KoreaMed CrossRef
  24. Sundstrom P. 2002. Adhesion in Candida spp. Cell. Microbiol. 4: 461-469.
    Pubmed CrossRef
  25. Schaller M, Borelli C, Korting HC, Hube B. 2005. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48:365-377.
    Pubmed CrossRef
  26. Schaller M, Schackert C, Korting HC, Januschke E, Hube B. 2000. Invasion of Candida albicans correlates with expression of secreted aspartic proteinases during experimental infection of human epidermis. J. Invest. Dermatol. 114: 712-717.
    Pubmed CrossRef
  27. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J. 2012. Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol. Rev. 36: 288-305.
    Pubmed CrossRef
  28. Gow NA, Brown AJ, Odds FC. 2002. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5: 366-371.
    CrossRef
  29. Thompson DS, Carlisle PL, Kadosh D. 2011. Coevolution of morphology and virulence in Candida species. Eukaryot. Cell 10: 1173-1182.
    Pubmed KoreaMed CrossRef
  30. Hoyer LL, Scherer S, Shatzman AR, Livi GP. 1995. Candida albicans ALS1: domains related to a Saccharomyces cerevisiae sexual agglutinin separated by a repeating motif. Mol. Microbiol. 15: 39-54.
    Pubmed CrossRef
  31. 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
  32. Rameau RD, Jackson DN, Beaussart A, Dufrêne YF, Lipke PN. 2016. The human disease-associated Aβ amyloid core sequence forms functional amyloids in a fungal adhesin. MBio 7: e01815-15.
    Pubmed KoreaMed CrossRef
  33. Ram sook CB, T an C , Garcia M C, F ung R, S oybelm an G, Henry R, et al. 2010. Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot. Cell 9: 393404.