Human Serum Promotes Candida albicans Biofilm Growth and Virulence Gene Expression on Silicone Biomaterial

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Samaranayake, Yuthika Hemamala ^a   Cheung, Becky P K ^a   Yau, Joyce Y Y ^a   Yeung, Shadow K W ^a   Samaranayake, Lakshman P ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROLASE; MESSENGER RNA; SILICONE;

ALS3 GENE; ARTICLE; BACTERIAL VIRULENCE; BIOFILM; CANDIDA ALBICANS; CONTROLLED STUDY; CULTURE MEDIUM; EAP1 GENE; ECE1 GENE; FUNGAL COLONIZATION; FUNGAL GENE; FUNGAL STRUCTURES; FUNGUS CULTURE; FUNGUS GROWTH; FUNGUS MUTANT; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HWP1 GENE; IN VITRO STUDY; INCUBATION TIME; NITROBLUE TETRAZOLIUM TEST; NONHUMAN; PLB1 GENE; PLB2 GENE; PLC GENE; PLD GENE; REAL TIME POLYMERASE CHAIN REACTION; SAP1 GENE; SAP10 GENE; SCANNING ELECTRON MICROSCOPY; SERUM; UPREGULATION; WILD TYPE;

BIOCOMPATIBLE MATERIALS; BIOFILMS; CANDIDA ALBICANS; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HUMANS; SERUM; SILICONES;

EID: 84877994942     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062902     Document Type: Article

References (72)

1. Kojic EM, Darouiche RO, (2004) Candida infections of medical devices. Clin Microbiol Rev 17: 255-267.
2. Cauda R, (2009) Candidaemia in patients with an inserted medical device. Drugs 69: 33-38.
3. Li F, Svarovsky MJ, Karlsson AJ, Wagner JP, Marchillo K, et al. (2007) Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell 6: 931-939.
4. Al-Fattani MA, Douglas LJ, (2006) Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55: 999-1008.
5. Nailis H, Kucharikova S, Ricicova M, Van Dijck P, Deforce D, et al. (2010) Real-time PCR expression profiling of genes encoding potential virulence factors in Candida albicans biofilms: identification of model-dependent and -independent gene expression. BMC Microbiol 10: 114-125.
6. Denstedt JD, Wollin TA, Rede G, (1998) Biomaterials used in urology: current issues of biocompatibility, infection and encrustation. J Endourol 12: 493-500.
7. Nett JE, Lepak AJ, Marchillo K, Andes DR, (2009) Time course global gene expression analysis of an in vivo Candida biofilm. J Infect Dis 200: 307-313.
8. Ramage G, Martinez JP, Lopez-Ribot JL, (2006) Minireview: Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6: 979-986.
9. Hoyer LL, (2001) The ALS gene family of Candida albicans. Trends Microbiol 9: 176-180.
10. Fu Y, Ibrahim AS, Sheppard DC, Chen YC, French SW, et al. (2002) Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol Microbiol 44: 61-72.
11. Zhao X, Oh SH, Yeater KM, Hoyer LL, (2005) Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function with the Als family. Microbiol 151: 1619-1630.
12. Tronchin G, Pihet M, Lopes-Bezerra LM, Bouchara JP, (2008) Adherence mechanisms in human pathogenic fungi. Med Mycol 46: 749-772.
13. Garcia-Sanchez S, Aubert S, Iraqui I, Janbon G, Ghigo J-M, et al. (2004) Candida albicans Biofilms: A developmental state associated with specific and stable gene expression patterns. Eukaryot Cell 3: 536-545.
14. Marchais V, Kempf M, Licznar P, Lefrancois C, Bouchara JP, et al. (2005) DNA array analysis of Candida albicans gene expression in response to adherence to polystyrene. FEMS Microbiol Lett 245: 25-32.
15. Staab JF, Bradway SD, Fidel PL, Sundstrom P, (1999) Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283: 1535-1538.
16. Li F, Palecek SP, (2003) EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot Cell 2: 1266-1273.
17. Kunze D, Melzer I, Bennett D, Sanglard D, MacCallum D, et al. (2005) Functional analysis of the phospholipase C gene CaPLC1 and two unusual phospholipase C genes, CaPLC2 and CaPLC3, of Candida albicans. Microbiol 151: 3381-3394.
18. Aoki W, Kitahara N, Miura N, Morisaka H, Yamamoto Y, et al. (2011) Comprehensive characterization of secreted aspartic proteases encoded by a virulence gene famiy in Candida albicans. J Biochem 150: 431-438.
19. Mendes A, Mores AU, Carvalho AP, Rosa RT, Samaranayake LP, et al. (2007) Candida albicans biofilms produce more secreted aspartyl protease than the planktonic cells. Biol Pharm Bull 30: 1813-1815.
20. Dolan JW, Bell AC, Hube B, Schaller M, Warner TF, et al. (2004) Candida albicans PLD1 activity is required for full virulence. Med Mycol 42: 439-447.
21. Gow NA, Brown AJ, Odds FC, (2002) Fungal morphogenesis and host invasion. Curr Opin Microbiol 5: 366-371.
22. Kumamoto CA, Vinces MD, (2005) Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol 7: 1546-1554.
23. Sharkey LL, McNemar MD, Saporito-Irwin SM, Sypherd PS, Fonzi WA, (1999) HWP1 functions in the morphological development of Candida albicans downstream of EFG1, TUP1 and RBF1. J Bacteriol 181: 5273-5279.
24. 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.
25. Sohn K, Urban C, Brunner H, Rupp S, (2003) EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol Microbiol 47: 89-102.
26. Hilmioglu S, Ilkit M, Badak Z, (2007) Comparison of 12 liquid media for germ tube production of Candida albicans and C. tropicalis. Mycoses 50: 282-285.
27. Thein ZM, Samaranayake YH, Samaranayake LP, (2007) Characteristics of dual species Candida biofilms on denture acrylic surfaces. Arch Oral Biol 52: 1200-1208.
28. Jin Y, Yip HK, Samaranayake YH, Yau JY, Samaranayake LP, (2003) Biofilm forming ability of Candida albicans is unlikely to contribute to high oral yeast carriage in human immunodeficiency virus-infection. J Clin Microbiol 41: 2961-7.
29. Samaranayake YH, Dassanayake RS, Jayatilake JAMS, Cheung BPK, Yau JYY, et al. (2005) Phospholipase B enzyme expression is not associated with other virulence attributes in Candida albicans isolates from patients with human immunodeficiency virus infection. J Med Microbiol 54: 583-593.
30. Samaranayake YH, Dassanayake RS, Cheung BPK, Jayatilake JAMS, Yeung KWS, et al. (2006) Differential phospholipase gene expression by Candida albicans in artificial media and cultured human oral epithelium. APMIS 2006 114: 857-866.
31. Lachke SA, Srikantha T, Tsai LK, Daniels K, Soll DR, (2000) Phenotypic switching in Candida glabrata involves phase-specific regulation of the metallothionein gene MT-II and the newly discovered haemolysin gene HLP. Infect Immun 68: 884-895.
32. Finkel JS, Mitchell AP, (2011) Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 9: 109-118.
33. Raad I, Costerton W, Sabharwal U, Sacilowski M, Anaissie E, et al. (1993) Ultrastructural analysis of indwelling vascular catheters: a quantitative relationship between luminal colonization and duration of placement. J Infect Dis 168: 400-407.
34. Francois P, Vaudaux P, Lew PD, (1998) Role of plasma and extracellular matrix proteins in the physiopathology of foreign body infections. Ann Vasc Surg 12: 34-40.
35. Samaranayake LP, McCourtie J, MacFarlane TW, (1980) Factors affecting the in vitro adherence to Candida albicans to acrylic surfaces. Arch Oral Biol 25: 611-615.
36. Nikawa H, Nishimura H, Makihira S, Hamada T, Sadamori S, et al. (2000) Effect of serum concentration on Candida biofilm formation on acrylic surfaces. Mycoses 43: 139-143.
37. Shepherd MG, Yin CY, Ram SP, Sullivan PA, (1980) Germ tube induction in Candida albicans. Can J Microbiol 26: 21-26.
38. Jayatilake JAMS, Samaranayake YH, Cheung LK, Samaranayake LP, (2006) Quantitative evaluation of tissue invasion by wild type, hyphal and SAP mutants of Candida albicans, and non-albicans Candida species in reconstituted human oral epithelium. J Oral Pathol Med 35: 484-491.
39. Chandra J, Mukherjee PK, Leidich SD, Faddoul FF, Hoyer LL, et al. (2001) Antifungal resistance of Candida biofilms formed on denture acrylic in vitro. J Dent Res 80: 903-908.
40. Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA, (2002) Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother 46: 1773-1780.
41. Ramage G, Wickes BL, Lopez-Ribot JL, (2001) Biofilms of Candida albicans and their associated resistance to antifungal agents. Am Clin Lab 20: 42-44.
42. Andes D, Nett J, Oschel P, Albrecht R, Marchillo K, et al. (2004) Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun 72: 6023-6031.
43. Zhang L, Mah TF, (2008) Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J Bacteriol 190: 4447-4452.
44. Cao YY, Cao YB, Xu Z, Ying K, Li Y, et al. (2005) cDNA microarray analysis of differential gene expression in Candida albicans biofilm exposed to farnesol. Antimicrob Agents Chemother 49: 584-589.
45. Nobile CJ, Nett JE, Andes DR, Mitchell AP, (2006) Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukarot Cell 5: 1604-1610.
46. Yeater KM, Chandra J, Cheung G, Mukherjee PK, Zhao X, et al. (2007) Temporal analysis of Candida albicans gene expression during biofilm development. Microbiol 153: 2373-2385.
47. Zhao X, Daniels KJ, Oh SH, Green CB, Yeater KM, et al. (2006) Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiol 152: 2287-2299.
48. Coleman DA, Oh SH, Zhao X, Zhao H, Hutchins JT, et al. (2009) Monoclonal antibodies specific for Candida albicans Als3 that immunolabel fungal cells in vitro and in vivo and block adhesion to host surfaces. J Microbiol Methods 78: 71-78.
49. Green CB, Zhao X, Yeater KM, Hoyer LL, (2005) Construction and real-time RT-PCR validation of Candida albicans PALS-GFP reporter strains and their use in flow cytometry analysis of ALS gene expression in budding and filamenting cells. Microbiol 151: 1051-1060.
50. O'Connor L, Lahiff S, Casey F, Glennon M, Cormican M, et al. (2005) Quantification of ALS1 gene expression in Candida albicans biofilms by RT-PCR using hybridization probes on the Light Cycler. Mol Cell Probes 19: 153-162.
51. Sundstrom P, (2002) Adhesion in Candida spp. Cell Microbiol 4: 461-469.
52. Snide JL, Sundstrom P (2006) Characterisation of HWP1 promoter activation in pseudohyhal cells in Candida albicans. Presentation at the Eighth ASM Conference on Candida and Candidiasis, Denver, CO. Washington, DC: American Society for Microbiology.
53. Odds FC, (1994) Candida species and virulence. ASM News 60: 313-318.
54. Liu Y, Filler SG, (2011) Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryot Cell 10: 168-173.
55. 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.
56. Stoldt VR, Sonneborn A, Leuker CE, Ernst JF, (1997) Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J 16: 1982-1991.
57. Felk A, Kretschmar M, Albrecht A, Schaller M, Beinhauer S, et al. (2002) Candida albicans hyphal formation and the expression of the Efg1-regulated proteinases Sap4 to Sap6 are required for the invasion of parenchymal organs. Infect Immun 70: 3689-3700.
58. Schaller M, Borelli C, Korting HC, Hube B, (2005) Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 48: 365-377.
59. Hube B, Naglik J, (2001) Candida albicans proteinases: resolving the mystery of a gene family. Microbiol 147: 1997-2005.
60. Naglik JR, Challacombe SJ, Hube B, (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67: 400-428.
61. Chen YC, Wu CC, Chung WL, Lee FJ, (2002) Differential secretion of Sap4-6 proteins in Candida albicans during hyphae formation. Microbiol 148: 3743-3754.
62. Borg-von Zepelin M, Meyer I, Thomssen R, Wurzner R, Sanglard D, et al. (1999) HIV-Protease inhibitors reduce cell adherence of Candida albicans strains by inhibition of yeast secreted aspartic proteases. J Invest Dermatol 113: 747-751.
63. Kvaal CS, Lachke SA, Srikantha T, Daniels K, McCoy J, et al. (1999) Misexpression of the opaque-phase-specific gene PEP1 (SAP1) in the white phase of Candida albicnas confers increased virulence in a mouse model of cutaneous infection. Infect Immun 67: 6652-6662.
64. Hube B, Monod M, Schofield DA, Brown AJ, Gow NA, (1994) Expression of seven members of the gene family encoding secretory aspartyl proteinases in Candida albicans. Mol Microbiol 14: 87-99.
65. White TC, Agabian N, (1995) Candida albicans secreted aspartyl proteinases: isoenzyme pattern is determined by cell type, and levels are determined by environmental factors. J Bacteriol 177: 5214-5221.
66. Liu H, (2002) Co-regulation of pathogenesis with dimorphism and phenotypic switching in Candida albicans, a commensal and a pathogen. Int J Med Microbiol 292: 299-311.
67. Ibrahim AS, Filler SG, Sanglard D, Edwards JE Jr, Hube B, (1998) Secreted aspartyl proteinases and interactions of Candida albicans with human endothelial cells. Infect Immun 66: 3003-3005.
68. Schaller M, Korting HC, Schafer W, Bastert J, Chen W, et al. (1999) Secreted aspartic proteinase (Sap) activity contributes to tissue damage in a model of human oral candidosis. Mol Microbiol 34: 169-180.
69. Schaller M, Bein M, Korting HC, Baur S, Hamm G, et al. (2003) The secreted aspartyl proteinases Sap1 and Sap2 cause tissue damage in an in vitro model of vaginal candidiasis based on reconstituted human vaginal epithelium. Infect Immun 71: 3227-3234.
70. Albrecht A, Felk A, Pichova I, Naglik JR, Schaller M, et al. (2006) glycosylphosphatidyl-inositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host pathogen interactions. J Biol Chem 281: 688-694.
71. Taylor BN, Hannemann H, Sehnal M, Biesemeier A, Schweizer A, et al. (2005) Induction of SAP 7 correlates with virulence in an intravenous infection model of candidiasis but not in a vaginal infection model in mice. Infect Immun 73: 7061-7063.
72. Taniguchi L, de Fatima Faria B, Rosa RT, de Paula E, Carvalho A, et al. (2009) Proposal of a low cost protocol for colorimetric semi-quantification of secretory phospholipase by Candida albicans grown in planktonic and biofilm phases. J Microbiol Methods 78: 171-174.