Browse > Article
http://dx.doi.org/10.4014/jmb.1712.12041

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

Lee, Heung-Shick (Department of Biotechnology and Bioinformatics, Korea University)
Kim, Younhee (Department of Korean Medicine, Semyung University)
Publication Information
Journal of Microbiology and Biotechnology / v.28, no.3, 2018 , pp. 482-490 More about this Journal
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 serum-containing 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 biofilm-associated infections.
Keywords
Biofilm; Candida albicans; hypha-specific gene; pseudohypha; qPCR; Paeonia lactiflora;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 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.   DOI
2 Thein ZM, Samaranayake YH, Samaranayake LP. 2007. In vitro biofilm formation of Candida albicans and non-albicans Candida species under dynamic and anaerobic conditions. Arch. Oral Biol. 52: 761-767.   DOI
3 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.   DOI
4 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   DOI
5 Kucharikova 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.   DOI
6 Sudbery P, Gow N, Berman J. 2004. The distinct morphogenic states of Candida albicans. Trends Microbiol. 12: 317-324.   DOI
7 Merson-Davies LA, Odds FC. 1989. A morphology index for characterization of cell shape in Candida albicans. J. Gen. Microbiol. 135: 3143-3152.
8 Hoyer LL. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9: 176-180.   DOI
9 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.   DOI
10 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.   DOI
11 Sundstrom P. 2002. Adhesion in Candida spp. Cell. Microbiol. 4: 461-469.   DOI
12 Schaller M, Borelli C, Korting HC, Hube B. 2005. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48: 365-377.   DOI
13 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.   DOI
14 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.   DOI
15 Gow NA, Brown AJ, Odds FC. 2002. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5: 366-371.   DOI
16 Ramage G, Martinez JP, Lopez-Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6: 979-986.   DOI
17 Thompson DS, Carlisle PL, Kadosh D. 2011. Coevolution of morphology and virulence in Candida species. Eukaryot. Cell 10: 1173-1182.   DOI
18 Pfaller MA, Pappas PG, Wingard JR. 2006. Invasive fungal pathogens: current epidemiological trends. Clin. Infect. Dis. 43: S3-S14.   DOI
19 Martinez LR, Fries BC. 2010. Fungal biofilms: relevance in the setting of human disease. Curr. Fungal Infect. Rep. 4: 266-275.   DOI
20 Ramage G, Rajendran R, Sherry L, Williams C. 2012. Fungal biofilm resistance. Int. J. Microbiol. 2012: 1-14.
21 Mathe L, Van Dijck P. 2013. Recent insights into Candida albicans biofilm resistance mechanisms. Curr. Genet. 59: 251-264.
22 Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, Kohler JR, et al. 2010. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog. 6: e1000828.   DOI
23 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.   DOI
24 Campbell BC, Chan KL, Kim JH. 2012. Chemosensitization as a means to augment commercial antifungal agents. Front. Microbiol. 3: 79.
25 Cowen LE. 2008. The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype. Nat. Rev. Microbiol. 6: 187-198.   DOI
26 Bink A, P ellens K , Cammue B PA, Thevissen K. 2 011. Anti-biofilm strategies: how to eradicate Candida biofilms? Open Mycol. J. 5: 29-38.   DOI
27 Lee HS, Kim Y. 2017. Paeonia lactiflora inhibits cell wall synthesis and triggers membrane depolarization in Candida albicans. J. Microbiol. Biotechnol. 27: 395-404.   DOI
28 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.   DOI
29 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.   DOI
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.   DOI
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.
32 Rameau RD, Jackson DN, Beaussart A, Dufrene YF, Lipke PN. 2016. The human disease-associated $A{\beta}$ amyloid core sequence forms functional amyloids in a fungal adhesin. MBio 7: e01815-15.
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: 393-404.   DOI