Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Open Life Sciences

formerly Central European Journal of Biology

Editor-in-Chief: Ratajczak, Mariusz

1 Issue per year


IMPACT FACTOR 2016 (Open Life Sciences): 0.448

CiteScore 2017: 0.88

SCImago Journal Rank (SJR) 2017: 0.271
Source Normalized Impact per Paper (SNIP) 2017: 0.545

Open Access
Online
ISSN
2391-5412
See all formats and pricing
More options …
Volume 6, Issue 6

Issues

Volume 10 (2015)

Biofilm formation and adhesive/invasive properties of Candida dubliniensis in comparison with Candida albicans

Anna Kolecka
  • Faculty of Natural Sciences, Department of Microbiology and Virology, Comenius University, 842 15, Bratislava, Slovakia
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Martin Zavrel / Rosa Hernandez-Barbado / Steffen Rupp / Helena Bujdakova
  • Faculty of Natural Sciences, Department of Microbiology and Virology, Comenius University, 842 15, Bratislava, Slovakia
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2011-11-23 | DOI: https://doi.org/10.2478/s11535-011-0087-8

Abstract

Candida dubliniensis and Candida albicans are closely related spp. exhibiting differences in their virulence potency. This study compared clinical isolates of C. dubliniensis with C. albicans from HIV patients with oropharyngeal candidiasis (OPC) and standard strains in power to form biofilm and their adhesive and invasive properties. Members of both spp. were able to form strong biofilms. However, SEM microscopy confirmed that C. albicans undergoes the more effective yeast-to-hyphae transition than C. dubliniensis with prevalent yeast form and limited ability to form filaments. Kinetic patterns indicated that while the first 30 min are critical for sufficient attachment to a polystyrene surface, adhesion to human carcinoma cell lines (Caco-2 and TR 146) needs additional time with maximal saturation observed at 240 min for both spp. The invasion process was tested on 3D RHE (reconstituted human epithelium) with Caco-2 or TR 146 on the collagen surface. C. albicans rapidly produced hyphae that penetrated the tissue layer, demonstrating substantive invasion within 21 h. In contrast, C. dubliniensis attached to the tissue surface and proliferated, suggesting the formation of a biofilm-like structure. After 21 h, C. dubliniensis was able to penetrate the RHE layer and invade unusually, with a cluster of the yeast cells.

Keywords: Candida dubliniensis; Candida albicans; Adhesive and invasive properties; Biofilm; RHE

  • [1] Sullivan D.J., Moran G.P., Coleman D.C., Candida dubliniensis: ten years on, FEMS Microbiol Lett., 2005, 253, 9–17 http://dx.doi.org/10.1016/j.femsle.2005.09.015CrossrefGoogle Scholar

  • [2] van Hal S.J., Stark D., Harkness J., Marriott D., Candida dubliniensis meningitis as delayed sequela of treated C. dubliniensis fungemia, Emerg Infect Dis., 2008, 14, 327–329 http://dx.doi.org/10.3201/eid1402.070985CrossrefGoogle Scholar

  • [3] Biasoli M.S., Tosello M.E., Luque A.G., Magaro H.M., Adherence, colonization and dissemination of Candida dubliniensis and other Candida species, Med Mycol., 2009, 22, 1–8 http://dx.doi.org/10.1080/13693780903114942CrossrefGoogle Scholar

  • [4] Pinjon E., Moran G.P., Coleman D.C., Sullivan D.J., Azole susceptibility and resistance in Candida dubliniensis, Biochem Soc Trans., 2005, 33, 1210–1214 http://dx.doi.org/10.1042/BST20051210CrossrefGoogle Scholar

  • [5] Moran G.P., MacCallum D.M., Spiering M.J., Coleman D.C., Sullivan D.J., Differential regulation of the transcriptional repressor NRG1 accounts for altered host-cell interactions in Candida albicans and Candida dubliniensis, Mol Microbiol., 2007, 66, 915–929 http://dx.doi.org/10.1111/j.1365-2958.2007.05965.xCrossrefGoogle Scholar

  • [6] Citiulo F., Moran G.P., Coleman D.C., Sullivan D.J., Purification and germination of Candida albicans and Candida dubliniensis chlamydospores cultured in liquid media, FEMS Yeast Res., 2009, 9, 1051–1060 http://dx.doi.org/10.1111/j.1567-1364.2009.00533.xCrossrefGoogle Scholar

  • [7] Henriques M., Azeredo J., Oliveira R., Candida species adhesion to oral epithelium: factors involved and experimental methodology used, Crit Rev Microbiol., 2006, 32, 217–226 http://dx.doi.org/10.1080/10408410601023524CrossrefGoogle Scholar

  • [8] Thein Z.M., Samaranayake Y.H., Samaranayake L.P., In vitro biofilm formation of Candida albicans and non-albicans Candida species under dynamic and anaerobic conditions, Arch Oral Biol, 2007, 52, 761–767 http://dx.doi.org/10.1016/j.archoralbio.2007.01.009CrossrefGoogle Scholar

  • [9] Borecká-Melkusová S., Moran G.P., Sullivan D.J., Kucharíková S., Chorvát D. Jr., Bujdáková H., The expression of genes involved in the ergosterol biosynthesis pathway in Candida albicans and Candida dubliniensis biofilms exposed to fluconazole, Mycoses, 2009, 52, 118–128 http://dx.doi.org/10.1111/j.1439-0507.2008.01550.xCrossrefGoogle Scholar

  • [10] Stokes C., Moran G.P., Spiering M.J., Cole G.T., Coleman D.C., Sullivan D.J., Lower filamentation rates of Candida dubliniensis contribute to its lower virulence in comparison with Candida albicans, Fungal Genet Biol., 2007, 44, 920–931 http://dx.doi.org/10.1016/j.fgb.2006.11.014CrossrefGoogle Scholar

  • [11] Jackson A.P., Gamble J.A., Yeomans T., Moran G.P., Saunders D., Harris D., et al., The comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans, Genome Res., 2009, 19, 2231–2244 http://dx.doi.org/10.1101/gr.097501.109CrossrefGoogle Scholar

  • [12] Järvensivu A., Hietanen J., Rautemaa R., Sorsa T., Richardson M, Candida yeasts in chronic periodontitis tissues and subgingival microbial biofilms in vivo, Oral Dis., 2004, 10, 106–112 http://dx.doi.org/10.1046/j.1354-523X.2003.00978.xCrossrefGoogle Scholar

  • [13] Feller L., Buskin A., Blignaut E., A review of Candida and periodontal disease in immunocompetent and HIV-infected subjects, SADJ., 2005, 60, 152–154 Google Scholar

  • [14] Dieterich C., Schandar M., Noll M., Johannes F.J., Brunner H., Graeve T., et al., In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion, Microbiology, 2002, 148, 497–506 CrossrefGoogle Scholar

  • [15] Zakikhany K., Thewes S., Wilson D., Martin R., Albrecht A., Hube B., From attachment to invasion: infection associated genes of Candida albicans, Jap Journal Med Mycol, 2008, 49, 245–251 http://dx.doi.org/10.3314/jjmm.49.245CrossrefGoogle Scholar

  • [16] Martinez M., López-Ribot J.L., Kirkpatrick W.R., Coco B.J., Bachmann S.P., Patterson T.F., Replacement of Candida albicans with C. dubliniensis in human immunodeficiency virusinfected patients with oropharyngeal candidiasis treated with fluconazole, J Clin Microbiol., 2002, 40, 3135–3139 http://dx.doi.org/10.1128/JCM.40.9.3135-3139.2002CrossrefGoogle Scholar

  • [17] Chunchanur S.K., Nadgir S.D., Halesh L.H., Patil B.S., Kausar Y., Chandrasekhar M.R., Detection and antifungal susceptibility testing of oral Candida dubliniensis from human immunodeficiency virusinfected patients, Indian J Pathol Microbiol., 2009, 52, 501–504 http://dx.doi.org/10.4103/0377-4929.56138CrossrefGoogle Scholar

  • [18] Pinjon E., Sullivan D., Salkin I., Shanley D., Coleman D., Simple, inexpensive, reliable method for differentiation of Candida dubliniensis from Candida albicans, J Clin Microbiol., 1998, 36, 2093–2095 Google Scholar

  • [19] Gillum A.M., Tsay E.Y., Kirsch D.R., Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations, Mol Gen Genet., 1984, 198, 179–182 http://dx.doi.org/10.1007/BF00328721CrossrefGoogle Scholar

  • [20] Boucher H., Mercure S., Montplaisir S., Lemay G., A novel group I intron in Candida dubliniensis is homologous to a Candida albicans intron, Gene, 1996, 180, 189–196 http://dx.doi.org/10.1016/S0378-1119(96)00453-2CrossrefGoogle Scholar

  • [21] McCullough M.J., Clemons K.V., Stevens D.A., Molecular and phenotypic characterization of genotypic Candida albicans subgroups and comparison with Candida dubliniensis and Candida stellatoidea, J Clin Microbiol., 1999, 37, 417–421 Google Scholar

  • [22] Li X., Yan Z., Xu J., Quantitative variation of biofilms among strains in natural populations of Candida albicans, Microbiology, 2003, 149, 353–362 http://dx.doi.org/10.1099/mic.0.25932-0CrossrefGoogle Scholar

  • [23] Sohn K., Senyürek I., Fertey J., Königsdorfer A., Joffroy C, Hauser N., et al., An in vitro assay to study the transcriptional response during adherence of Candida albicans to different human epithelia, FEMS Yeast Res., 2006, 6, 1085–1093 http://dx.doi.org/10.1111/j.1567-1364.2006.00130.xCrossrefGoogle Scholar

  • [24] Hernandez R., Rupp S., Human epithelial model system for the study of Candida infections in vitro: Part II. Histologic methods for studying fungal invasion, Methods Mol Biol., 2009, 470, 105–123 http://dx.doi.org/10.1007/978-1-59745-204-5_10CrossrefGoogle Scholar

  • [25] Sohn K., Rupp S., Human epithelial model systems for the study of Candida infections in vitro: part I. Adhesion to epithelial models, Methods Mol Biol., 2009, 470, 95–104 http://dx.doi.org/10.1007/978-1-59745-204-5_9CrossrefGoogle Scholar

  • [26] Sullivan D.J., Westerneng T.J., Haynes K.A., Bennett D.E., Coleman D.C., Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals, Microbiology, 1995, 141, 1507–1521 http://dx.doi.org/10.1099/13500872-141-7-1507CrossrefGoogle Scholar

  • [27] Moran G., Stokes C., Thewes S., Hube B., Coleman D.C., Sullivan D., Comparative genomics using Candida albicans DNA microarrays reveals absence and divergence of virulence-associated genes in Candida dubliniensis, Microbiology, 2004, 150, 3363–3382 http://dx.doi.org/10.1099/mic.0.27221-0CrossrefGoogle Scholar

  • [28] Kuhn D.M., Balkis M., Chandra J., Mukherjee P.K., Ghannoum M.A., Uses and limitations of the XTT assay in studies of Candida growth and metabolism, J Clin Microbiol., 2003, 41, 506–508 http://dx.doi.org/10.1128/JCM.41.1.506-508.2003CrossrefGoogle Scholar

  • [29] Borecká-Melkusová S., Bujdáková H., Variation of cell surface hydrophobicity and biofilm formation among genotypes of Candida albicans and Candida dubliniensis under antifungal treatment, Can J Microbiol., 2008, 54, 718–724 http://dx.doi.org/10.1139/W08-060CrossrefGoogle Scholar

  • [30] Blankenship J.R., Mitchell A.P., How to build a biofilm: a fungal perspective, Curr Opin Microbiol., 2006, 9, 588–594 http://dx.doi.org/10.1016/j.mib.2006.10.003CrossrefGoogle Scholar

  • [31] Ramage G., Mowat E., Jones B., Williams C., Lopez-Ribot J., Our current understanding of fungal biofilms, Crit Rev Microbiol., 2009, 35, 340–355 http://dx.doi.org/10.3109/10408410903241436CrossrefGoogle Scholar

  • [32] Bujdáková H., Paulovičová E., Paulovičová L., Šimová Z., Participation of the Candida albicans surface antigen in adhesion, the first phase of biofilm development, FEMS Immunol Med Microbiol., 2010, 59, 485–92 CrossrefGoogle Scholar

  • [33] Hazen K.C., Wu J.G., Masuoka J., Comparison of the hydrophobic properties of Candida albicans and Candida dubliniensis, Infect Immun., 2001, 69, 779–786 http://dx.doi.org/10.1128/IAI.69.2.779-786.2001CrossrefGoogle Scholar

  • [34] Jabra-Rizk M.A., Falkler W.A. Jr., Merz W.G., Baqui A.A., Kelley J.I., Meiller T.F., Cell surface hydrophobicity-associated adherence of Candida dubliniensis to human buccal epithelial cells, Rev Iberoam Micol., 2001, 18, 17–22 Google Scholar

  • [35] Blanco M.T., Sacristán B., Beteta A., Fernández-Calderón M.C., Hurtado C., Pérez-Giraldo C., et al., Cellular surface hydrophobicity as an additional phenotypic criterion applied to differentiate strains of Candida albicans and Candida dubliniensis, Diagn Microbiol Infect Dis., 2008, 60, 129–131 http://dx.doi.org/10.1016/j.diagmicrobio.2007.07.013CrossrefGoogle Scholar

  • [36] Cotter G., Kavanagh K., Adherence mechanisms of Candida albicans, Br J Biomed Sci., 2000, 57, 241–249 Google Scholar

About the article

Published Online: 2011-11-23

Published in Print: 2011-12-01


Citation Information: Open Life Sciences, Volume 6, Issue 6, Pages 893–901, ISSN (Online) 2391-5412, DOI: https://doi.org/10.2478/s11535-011-0087-8.

Export Citation

© 2011 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Comments (0)

Please log in or register to comment.
Log in