1887

Abstract

Oral candidiasis is a disease caused by opportunistic species of that normally reside on human mucosal surfaces. The transition of from budding yeast to filamentous hyphae allows for covalent attachment to oral epithelial cells, followed by biofilm formation, invasion and tissue damage. In this study, combinations of SD5870, CBS N116411 and DSM 14685 were assessed for their ability to inhibit the formation of and disrupt biofilms. Co-incubation with probiotic supernatants under hyphae-inducing conditions reduced biofilm formation by >75 % in all treatment groups. Likewise, combinations of live probiotics reduced biofilm formation of by >67 %. When live probiotics or their supernatants were overlaid on preformed biofilms, biofilm size was reduced by >63 and >65 % respectively. Quantitative real-time PCR results indicated that the combined supernatants of SD5870 and CBS N116411 significantly reduced the expression of several genes involved in the yeast–hyphae transition: (adhesin/invasin) by 70 % ( < 0.0001), (hyphae-specific gene activator) by 47 % ( = 0.0061), (secreted protease) by 49 % ( < 0.0001) and (hyphal wall protein critical to biofilm formation) by >99 % ( < 0.0001). These findings suggest the combination of SD5870, CBS N116411 and DSM 14685 is effective at both preventing the formation of and removing preformed biofilms. Our novel results point to the downregulation of several genes critical to the yeast–hyphae transition, biofilm formation, tissue invasion and cellular damage.

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2016-04-01
2019-11-21
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References

  1. Abe S., Satoh T., Tokuda Y., Tansho S., Yamaguchi H.. ( 1994;). A rapid colorimetric assay for determination of leukocyte-mediated inhibition of mycelial growth of Candida albicans. Microbiol Immunol 38: 385–388 [CrossRef] [PubMed].
    [Google Scholar]
  2. Andes D.. ( 2003;). In vivo pharmacodynamics of antifungal drugs in treatment of candidiasis. Antimicrob Agents Chemother 47: 1179–1186 [CrossRef] [PubMed].
    [Google Scholar]
  3. Baillie G. S., Douglas L. J.. ( 1999;). Role of dimorphism in the development of Candida albicans biofilms. J Med Microbiol 48: 671–679 [CrossRef] [PubMed].
    [Google Scholar]
  4. Bal A. M.. ( 2010;). The echinocandins: three useful choices or three too many?. Int J Antimicrob Agents 35: 13–18 [CrossRef] [PubMed].
    [Google Scholar]
  5. Burton J. P., Drummond B. K., Chilcott C. N., Tagg J. R., Thomson W. M., Hale J.D.F., Wescombe P. A.. ( 2013;). Influence of the probiotic Streptococcus salivarius strain M18 on indices of dental health in children: a randomized double-blind, placebo-controlled trial. J Med Microbiol 62: 875–884 [CrossRef] [PubMed].
    [Google Scholar]
  6. Campisi G., Panzarella V., Matranga D., Calvino F., Pizzo G., Lo Muzio L., Porter S.. ( 2008;). Risk factors of oral candidosis: a twofold approach of study by fuzzy logic and traditional statistic. Arch Oral Biol 53: 388–397 [CrossRef] [PubMed].
    [Google Scholar]
  7. Cotter G., Kavanagh K.. ( 2000;). Adherence mechanisms of Candida albicans. Br J Biomed Sci 57: 241–249 [PubMed].
    [Google Scholar]
  8. Drago L., Mombelli B., De Vecchi E., Bonaccorso C., Fassina M. C., Gismondo M. R.. ( 2000;). Candida albicans cellular internalization: a new pathogenic factor?. Int J Antimicrob Agents 16: 545–547 [CrossRef] [PubMed].
    [Google Scholar]
  9. Egusa H., Soysa N. S., Ellepola A. N., Yatani H., Samaranayake L. P.. ( 2008;). Oral candidosis in HIV-infected patients. Curr HIV Res 6: 485–499 [CrossRef] [PubMed].
    [Google Scholar]
  10. Fukushima C., Matsuse H., Saeki S., Kawano T., Machida I., Kondo Y., Kohno S.. ( 2005;). Salivary IgA and oral candidiasis in asthmatic patients treated with inhaled corticosteroid. J Asthma 42: 601–604 [CrossRef] [PubMed].
    [Google Scholar]
  11. Gow N.A.R., van de Veerdonk F. L., Brown A.J.P., Netea M. G.. ( 2012;). Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 10: 112–122 [PubMed].
    [Google Scholar]
  12. Gropp K., Schild L., Schindler S., Hube B., Zipfel P. F., Skerka C.. ( 2009;). The yeast Candida albicans evades human complement attack by secretion of aspartic proteases. Mol Immunol 47: 465–475 [CrossRef] [PubMed].
    [Google Scholar]
  13. Harriott M. M., Noverr M. C.. ( 2011;). Importance of Candida-bacterial polymicrobial biofilms in disease. Trends Microbiol 19: 557–563 [CrossRef] [PubMed].
    [Google Scholar]
  14. Hatakka K., Ahola A. J., Yli-Knuuttila H., Richardson M., Poussa T., Meurman J. H., Korpela R.. ( 2007;). Probiotics reduce the prevalence of oral candida in the elderly - a randomized controlled trial. J Dent Res 86: 125–130 [CrossRef] [PubMed].
    [Google Scholar]
  15. Herzberg M. C., Meyer M. W., Kiliç A., Tao L.. ( 1997;). Host-pathogen interactions in bacterial endocarditis: streptococcal virulence in the host. Adv Dent Res 11: 69–74 [CrossRef] [PubMed].
    [Google Scholar]
  16. Hoyer L. L.. ( 2001;). The ALS gene family of Candida albicans. Trends Microbiol 9: 176–180 [CrossRef] [PubMed].
    [Google Scholar]
  17. Ishijima S. A., Hayama K., Burton J. P., Reid G., Okada M., Matsushita Y., Abe S.. ( 2012;). Effect of Streptococcus salivarius K12 on the in vitro growth of Candida albicans and its protective effect in an oral candidiasis model. Appl Environ Microbiol 78: 2190–2199 [CrossRef] [PubMed].
    [Google Scholar]
  18. Jenkinson H. F., Lala H. C., Shepherd M. G.. ( 1990;). Coaggregation of Streptococcus sanguis and other streptococci with Candida albicans. Infect Immun 58: 1429–1436 [PubMed].
    [Google Scholar]
  19. Jiang Q., Stamatova I., Kari K., Meurman J. H.. ( 2015;). Inhibitory activity in vitro of probiotic lactobacilli against oral Candida under different fermentation conditions. Benef Microbes 6: 361–368 [CrossRef] [PubMed].
    [Google Scholar]
  20. Kamagata-Kiyoura Y., Abe S., Yamaguchi H., Nitta T.. ( 2003;). Detachment activity of human saliva in vitro for Candida albicans cells attached to a plastic plate. J Infect Chemother 9: 215–220 [CrossRef] [PubMed].
    [Google Scholar]
  21. Li F., Palecek S. P.. ( 2003;). EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot Cell 2: 1266–1273 [CrossRef] [PubMed].
    [Google Scholar]
  22. Liu Y., Filler S. G.. ( 2011;). Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryot Cell 10: 168–173 [CrossRef] [PubMed].
    [Google Scholar]
  23. Lo H. J., Köhler J. R., DiDomenico B., Loebenberg D., Cacciapuoti A., Fink G. R.. ( 1997;). Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939–949 [CrossRef] [PubMed].
    [Google Scholar]
  24. Mendonça F. H., Santos S. S., Faria I. S., Gonçalves e Silva R., Jorge A. O., Leão M. V.. ( 2012;). Effects of probiotic bacteria on Candida presence and IgA anti-Candida in the oral cavity of elderly. Braz Dent J 23: 534–538 [CrossRef] [PubMed].
    [Google Scholar]
  25. Naglik J. R., Challacombe S. J., Hube B.. ( 2003;). Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67: 400–428 [CrossRef] [PubMed].
    [Google Scholar]
  26. Nett J. E., Sanchez H., Cain M. T., Andes D. R.. ( 2010;). Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J Infect Dis 202: 171–175 [CrossRef] [PubMed].
    [Google Scholar]
  27. Nobile C. J., Nett J. E., Andes D. R., Mitchell A. P.. ( 2006;). Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot Cell 5: 1604–1610 [CrossRef] [PubMed].
    [Google Scholar]
  28. Paturi G., Phillips M., Kailasapathy K.. ( 2008;). Effect of probiotic strains Lactobacillus acidophilus LAFTI L10 and Lactobacillus paracasei LAFTI L26 on systemic immune functions and bacterial translocation in mice. J Food Prot 71: 796–801 [PubMed].
    [Google Scholar]
  29. Phan Q. T., Myers C. L., Fu Y., Sheppard D. C., Yeaman M. R., Welch W. H., Ibrahim A. S., Edwards J. E. Jr., Filler S. G.. ( 2007;). Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 5: e64 [CrossRef] [PubMed].
    [Google Scholar]
  30. Radfar L., Shea Y., Fischer S. H., Sankar V., Leakan R. A., Baum B. J., Pillemer S. R.. ( 2003;). Fungal load and candidiasis in Sjögren's syndrome. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 96: 283–287 [CrossRef] [PubMed].
    [Google Scholar]
  31. Rajendran R., Robertson D. P., Hodge P. J., Lappin D. F., Ramage G.. ( 2010;). Hydrolytic enzyme production is associated with Candida albicans biofilm formation from patients with type 1 diabetes. Mycopathologia 170: 229–235 [CrossRef] [PubMed].
    [Google Scholar]
  32. Ramage G., VandeWalle K., López-Ribot J. L., Wickes B. L.. ( 2002;). The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol Lett 214: 95–100 [CrossRef] [PubMed].
    [Google Scholar]
  33. Ramage G., Martínez J. P., López-Ribot J. L.. ( 2006;). Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6: 979–986 [CrossRef] [PubMed].
    [Google Scholar]
  34. Reinholdt J., Krogh P., Holmstrup P.. ( 1987;). Degradation of IgA1, IgA2, and S-IgA by Candida and Torulopsis species. Acta Pathol Microbiol Immunol Scand C 95: 265–274 [PubMed].
    [Google Scholar]
  35. Rüchel R.. ( 1986;). Cleavage of immunoglobulins by pathogenic yeasts of the genus Candida. Microbiol Sci 3: 316–319 [PubMed].
    [Google Scholar]
  36. Sardi J. C., Duque C., Mariano F. S., Peixoto I. T., Höfling J. F., Gonçalves R. B.. ( 2010;). Candida spp. in periodontal disease: a brief review. J Oral Sci 52: 177–185 [CrossRef] [PubMed].
    [Google Scholar]
  37. Schauer F., Hanschke R.. ( 1999;). [Taxonomy and ecology of the genus Candida]. Mycoses 42: (Suppl 1), 12–21 (in German) [CrossRef] [PubMed].
    [Google Scholar]
  38. Shapiro R. S., Robbins N., Cowen L. E.. ( 2011;). Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev 75: 213–267 [CrossRef] [PubMed].
    [Google Scholar]
  39. Silverman R. J., Nobbs A. H., Vickerman M. M., Barbour M. E., Jenkinson H. F.. ( 2010;). Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun 78: 4644–4652 [CrossRef] [PubMed].
    [Google Scholar]
  40. Soysa N. S., Samaranayake L. P., Ellepola A. N.. ( 2008;). Antimicrobials as a contributory factor in oral candidosis - a brief overview. Oral Dis 14: 138–143 [CrossRef] [PubMed].
    [Google Scholar]
  41. Staab J. F., Bradway S. D., Fidel P. L., Sundstrom P.. ( 1999;). Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283: 1535–1538 [CrossRef] [PubMed].
    [Google Scholar]
  42. Staib P., Kretschmar M., Nichterlein T., Hof H., Morschhäuser J.. ( 2002;). Transcriptional regulators Cph1p and Efg1p mediate activation of the Candida albicans virulence gene SAP5 during infection. Infect Immun 70: 921–927 [CrossRef] [PubMed].
    [Google Scholar]
  43. Sudbery P. E.. ( 2011;). Growth of Candida albicans hyphae. Nat Rev Microbiol 9: 737–748 [CrossRef] [PubMed].
    [Google Scholar]
  44. Sudbery P., Gow N., Berman J.. ( 2004;). The distinct morphogenic states of Candida albicans. Trends Microbiol 12: 317–324 [CrossRef] [PubMed].
    [Google Scholar]
  45. Theberge S., Semlali A., Alamri A., Leung K. P., Rouabhia M.. ( 2013;). C. albicans growth, transition, biofilm formation, and gene expression modulation by antimicrobial decapeptide KSL-W. BMC Microbiol 13: 246–260 [CrossRef] [PubMed].
    [Google Scholar]
  46. Thompson G. R. III, Patel P. K., Kirkpatrick W. R., Westbrook S. D., Berg D., Erlandsen J., Redding S. W., Patterson T. F.. ( 2010;). Oropharyngeal candidiasis in the era of antiretroviral therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 109: 488–495 [CrossRef] [PubMed].
    [Google Scholar]
  47. Ujaoney S., Chandra J., Faddoul F., Chane M., Wang J., Taifour L., Mamtani M. R., Thakre T. P., Kulkarni H., other authors. ( 2014;). In vitro effect of over-the-counter probiotics on the ability of Candida albicans to form biofilm on denture strips. J Dent Hyg 88: 183–189 [PubMed].
    [Google Scholar]
  48. Uppuluri P., Pierce C. G., Thomas D. P., Bubeck S. S., Saville S. P., López-Ribot J. L.. ( 2010;). The transcriptional regulator Nrg1p controls Candida albicans biofilm formation and dispersion. Eukaryot Cell 9: 1531–1537 [CrossRef] [PubMed].
    [Google Scholar]
  49. Vazquez J. A.. ( 2010;). Invasive fungal infections in the intensive care unit. Semin Respir Crit Care Med 31: 79–86 [CrossRef] [PubMed].
    [Google Scholar]
  50. Weerasuriya N., Snape J.. ( 2008;). Oesophageal candidiasis in elderly patients: risk factors, prevention and management. Drugs Aging 25: 119–130 [CrossRef] [PubMed].
    [Google Scholar]
  51. Williams D., Lewis M.. ( 2011;). Pathogenesis and treatment of oral candidosis. J Oral Microbiol 3: 1–11 [CrossRef] [PubMed].
    [Google Scholar]
  52. Wu H., Downs D., Ghosh K., Ghosh A. K., Staib P., Monod M., Tang J.. ( 2013;). Candida albicans secreted aspartic proteases 4-6 induce apoptosis of epithelial cells by a novel Trojan horse mechanism. FASEB J 27: 2132–2144 [CrossRef] [PubMed].
    [Google Scholar]
  53. Zomorodian K., Haghighi N. N., Rajaee N., Pakshir K., Tarazooie B., Vojdani M., Sedaghat F., Vosoghi M.. ( 2011;). Assessment of Candida species colonization and denture-related stomatitis in complete denture wearers. Med Mycol 49: 208–211 [CrossRef] [PubMed].
    [Google Scholar]
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