Saccharomyces cerevisiae biofilm tolerance towards systemic antifungals depends on growth phase

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Bojsen, Rasmus ^a   Regenberg, Birgitte ^b   Folkesson, Anders ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Amphotericin B; Antifungal agent; Biofilm; Caspofungin; Drug tolerance; Flucytosine; Fungicide; Resistance; Voriconazole; Yeast

Indexed keywords

AMPHOTERICIN B; CASPOFUNGIN; FLUCYTOSINE; VORICONAZOLE; ANTIFUNGAL AGENT;

ANTIFUNGAL ACTIVITY; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BIOFILM; CANDIDA GLABRATA; CELL COUNT; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; FUNGAL STRAIN; FUNGUS GROWTH; GROWTH CURVE; NONHUMAN; SACCHAROMYCES CEREVISIAE; BACTERIAL COUNT; CONFOCAL MICROSCOPY; DRUG EFFECTS; DRUG TOLERANCE; GROWTH, DEVELOPMENT AND AGING; MICROBIAL VIABILITY;

CANDIDA; CANDIDA GLABRATA; SACCHAROMYCES CEREVISIAE;

ANTIFUNGAL AGENTS; BIOFILMS; COLONY COUNT, MICROBIAL; DRUG TOLERANCE; MICROBIAL VIABILITY; MICROSCOPY, CONFOCAL; SACCHAROMYCES CEREVISIAE;

EID: 84924147113     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/s12866-014-0305-4     Document Type: Article

References (69)

1. Tortorano AM, Tortorano AM, Peman J, Bernhardt H, Klingspor L, Kibbler CC, Faure O, Biraghi E, Canton E, Zimmermann K, Seaton S, Grillot R: Epidemiology of candidaemia in Europe: results of 28-month European Confederation of Medical Mycology (ECMM) hospital-based surveillance study. Eur J Clin Microbiol Infect Dis 2004, 23(4):317-322.
2. Ramage G, Williams C: The clinical importance of fungal biofilms. Adv Appl Microbiol 2013, 84:27-83.
3. Ramage G, Martinez JP, Lopez-Ribot JL: Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 2006, 6(7):979-986.
4. Costerton JW, Stewart PS, Greenberg EP: Bacterial biofilms: a common cause of persistent infections. Science 1999, 284(5418):1318-1322.
5. Vanden Bossche H, Koymans L, Moereels H: P450 inhibitors of use in medical treatment: focus on mechanisms of action. Pharmacol Ther 1995, 67(1):79-100.
6. Kanafani ZA, Perfect JR: Antimicrobial resistance: resistance to antifungal agents: mechanisms and clinical impact. Clin Infect Dis 2008, 46(1):120-128.
7. Horn DL, Neofytos D, Anaissie EJ, Fishman JA, Steinbach WJ, Olyaei AJ, Marr KA, Pfaller MA, Chang CH, Webster KM: Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin Infect Dis 2009, 48(12):1695-1703.
8. Deresinski SC, Stevens DA: Caspofungin. Clin Infect Dis 2003, 36(11):1445-1457.
9. Mesa-Arango AC, Scorzoni L, Zaragoza O: It only takes one to do many jobs: Amphotericin B as antifungal and immunomodulatory drug. Front Microbiol 2012, 3:286.
10. Waldorf AR, Polak A: Mechanisms of action of 5-fluorocytosine. Antimicrob Agents Chemother 1983, 23(1):79-85.
11. Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA: Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother 2002, 46(6):1773-1780.
12. Martins M, Uppuluri P, Thomas DP, Cleary IA, Henriques M, Lopez-Ribot JL, Oliveira R: Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. Mycopathologia 2010, 169(5):323-331.
13. Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, Hoff B, VanHandel M, Andes D: Putative role of beta-1,3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother 2007, 51(2):510-520.
14. Martins M, Henriques M, Lopez-Ribot JL, Oliveira R: Addition of DNase improves the in vitro activity of antifungal drugs against Candida albicans biofilms. Mycoses 2012, 55(1):80-85.
15. Al-Fattani MA, Douglas LJ: Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother 2004, 48(9):3291-3297.
16. Vediyappan G, Rossignol T, D'Enfert C: Interaction of Candida albicans biofilms with antifungals: transcriptional response and binding of antifungals to beta-glucans. Antimicrob Agents Chemother 2010, 54(5):2096-2111.
17. Song JW, Shin JH, Kee SJ, Kim SH, Shin MG, Suh SP, Ryang DW: Expression of CgCDR1, CgCDR2, and CgERG11 in Candida glabrata biofilms formed by bloodstream isolates. Med Monde 2009, 47(5):545-548.
18. Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA: Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun 2003, 71(8):4333-4340.
19. Ramage G, Bachmann S, Patterson TF, Wickes BL, Lopez-Ribot JL: Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J Antimicrob Chemother 2002, 49(6):973-980.
20. Cannon RD, Lamping E, Holmes AR, Niimi K, Baret PV, Keniya MV, Tanabe K, Niimi M, Goffeau A, Monk BC: Efflux-mediated antifungal drug resistance. Clin Microbiol Rev 2009, 22(2):291-321. Table of Content.
21. Botstein D, Fink GR: Yeast: an experimental organism for 21st Century biology. Genetics 2011, 189(3):695-704.
22. Shapiro RS, Robbins N, Cowen LE: Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev: MMBR 2011, 75(2):213-267.
23. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, De Montigny J, Marck C, Neuveglise C, Talla E, Goffard N, Frangeul L, Aigle M, Anthouard V, Babour A, Barbe V, Barnay S, Blanchin S, Beckerich JM, Beyne E, Bleykasten C, Boisrame A, Boyer J, Cattolico L, Confanioleri F, De Daruvar A, Despons L, Fabre E, Fairhead C, Ferry-Dumazet H, et al: Genome evolution in yeasts. Nature 2004, 430(6995):35-44.
24. Verstrepen KJ, Klis FM: Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 2006, 60(1):5-15.
25. Seneviratne CJ, Silva WJ, Jin LJ, Samaranayake YH, Samaranayake LP: Architectural analysis, viability assessment and growth kinetics of Candida albicans and Candida glabrata biofilms. Arch Oral Biol 2009, 54(11):1052-1060.
26. Hawser SP, Douglas LJ: Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun 1994, 62(3):915-921.
27. Ryan O, Shapiro RS, Kurat CF, Mayhew D, Baryshnikova A, Chin B, Lin ZY, Cox MJ, Vizeacoumar F, Cheung D, Bahr S, Tsui K, Tebbji F, Sellam A, Istel F, Schwarzmuller T, Reynolds TB, Kuchler K, Gifford DK, Whiteway M, Giaever G, Nislow C, Costanzo M, Gingras AC, Mitra RD, Andrews B, Fink GR, Cowen LE, Boone C: Global gene deletion analysis exploring yeast filamentous growth. Science 2012, 337(6100):1353-1356.
28. Reynolds TB, Fink GR: Bakers' yeast, a model for fungal biofilm formation. Science 2001, 291(5505):878-881.
29. Vachova L, Stovicek V, Hlavacek O, Chernyavskiy O, Stepanek L, Kubinova L, Palkova Z: Flo11p, drug efflux pumps, and the extracellular matrix cooperate to form biofilm yeast colonies. J Cell Biol 2011, 194(5):679-687.
30. Weiss Nielsen M, Sternberg C, Molin S, Regenberg B: Pseudomonas aeruginosa and Saccharomyces cerevisiae biofilm in flow cells. J Vis Exp 2011, 47:pii: 2383.
31. Granek JA, Murray D, Kayrkci O, Magwene PM: The genetic architecture of biofilm formation in a clinical isolate of Saccharomyces cerevisiae. Genetics 2013, 193(2):587-600.
32. Vandenbosch D, De Canck E, Dhondt I, Rigole P, Nelis HJ, Coenye T: Genomewide screening for genes involved in biofilm formation and miconazole susceptibility in Saccharomyces cerevisiae. FEMS Yeast Res 2013, 13(8):720-730.
33. Scherz K, Andersen Bojsen R, Gro L, Rejkjaer S, Weiss M, Nielsen Lisby M, Folkesson A, Regenberg B: Genetic basis for Saccharomyces cerevisiae biofilm in liquid medium. G3 (Bethesda) 2014, 4(9):1671-1680.
34. Tristezza M, Lourenco A, Barata A, Brito L, Malfeito-Ferreira M, Loureiro V: Susceptibility of wine spoilage yeasts and bacteria in the planktonic state and in biofilms to disinfectants. Ann Microbiol 2010, 60(3):549-556.
35. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA: Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 2001, 183(18):5385-5394.
36. Enache-Angoulvant A, Hennequin C: Invasive Saccharomyces infection: a comprehensive review. Clin Infect Dis 2005, 41(11):1559-1568.
37. Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J: Our current understanding of fungal biofilms. Crit Rev Microbiol 2009, 35(4):340-355.
38. Mah TF, O'Toole GA: Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001, 9(1):34-39.
39. Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, Beer K, McKay G, Siehnel R, Schafhauser J, Wang Y, Britigan BE, Singh PK: Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 2011, 334(6058):982-986.
40. Spoering AL, Lewis K: Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 2001, 183(23):6746-6751.
41. Anderl JN, Zahller J, Roe F, Stewart PS: Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 2003, 47(4):1251-1256.
42. Millard PJ, Roth BL, Thi HP, Yue ST, Haugland RP: Development of the FUN-1 family of fluorescent probes for vacuole labeling and viability testing of yeasts. Appl Environ Microbiol 1997, 63(7):2897-2905.
43. Haagensen JA, Regenberg B, Sternberg C: Advanced microscopy of microbial cells. Adv Biochem Eng Biotechnol 2011, 124:21-54.
44. Beauvais A, Loussert C, Prevost MC, Verstrepen K, Latge JP: Characterization of a biofilm-like extracellular matrix in FLO1-expressing Saccharomyces cerevisiae cells. FEMS Yeast Res 2009, 9(3):411-419.
45. Verstrepen KJ, Reynolds TB, Fink GR: Origins of variation in the fungal cell surface. Nat Rev Microbiol 2004, 2(7):533-540.
46. Guo B, Styles CA, Feng Q, Fink GR: A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci U S A 2000, 97(22):12158-12163.
47. Mitchell KF, Taff HT, Cuevas MA, Reinicke EL, Sanchez H, Andes DR: Role of matrix beta-1,3 glucan in antifungal resistance of non-albicans Candida biofilms. Antimicrob Agents Chemother 2013, 57(4):1918-1920.
48. Nett JE, Crawford K, Marchillo K, Andes DR: Role of Fks1p and matrix glucan in Candida albicans biofilm resistance to an echinocandin, pyrimidine, and polyene. Antimicrob Agents Chemother 2010, 54(8):3505-3508.
49. Baillie GS, Douglas LJ: Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. J Antimicrob Chemother 2000, 46(3):397-403.
50. Pamp SJ, Gjermansen M, Johansen HK, Tolker-Nielsen T: Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol Microbiol 2008, 68(1):223-240.
51. Martinez LR, Casadevall A: Susceptibility of Cryptococcus neoformans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother 2006, 50(3):1021-1033.
52. Levin BR, Rozen DE: Non-inherited antibiotic resistance. Nat Rev Microbiol 2006, 4(7):556-562.
53. Lewis RE, Klepser ME, Pfaller MA: In vitro pharmacodynamic characteristics of flucytosine determined by time-kill methods. Diagn Microbiol Infect Dis 2000, 36(2):101-105.
54. Bartizal K, Gill CJ, Abruzzo GK, Flattery AM, Kong L, Scott PM, Smith JG, Leighton CE, Bouffard A, Dropinski JF, Balkovec J: In vitro preclinical evaluation studies with the echinocandin antifungal MK-0991 (L-743,872). Antimicrob Agents Chemother 1997, 41(11):2326-2332.
55. Frost DJ, Brandt K, Capobianco J, Goldman R: Characterization of (1,3)-beta-glucan synthase in Candida albicans: microsomal assay from the yeast or mycelial morphological forms and a permeabilized whole-cell assay. Microbiology 1994, 140(Pt 9):2239-2246.
56. Perlin DS: Current perspectives on echinocandin class drugs. Future Microbiol 2011, 6(4):441-457.
57. Klepser ME, Malone D, Lewis RE, Ernst EJ, Pfaller MA: Evaluation of voriconazole pharmacodynamics using time-kill methodology. Antimicrob Agents Chemother 2000, 44(7):1917-1920.
58. Anderson JB: Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat Rev Microbiol 2005, 3(7):547-556.
59. Folkesson A, Haagensen JA, Zampaloni C, Sternberg C, Molin S: Biofilm induced tolerance towards antimicrobial peptides. PLoS One 2008, 3(4):e1891.
60. Liu Y, Knapp KM, Yang L, Molin S, Franzyk H, Folkesson A: High in vitro antimicrobial activity of beta-peptoid-peptide hybrid oligomers against planktonic and biofilm cultures of Staphylococcus epidermidis. Int J Antimicrob Agents 2013, 41(1):20-27.
61. Zuroff TR, Bernstein H, Lloyd-Randolfi J, Jimenez-Taracido L, Stewart PS, Carlson RP: Robustness analysis of culturing perturbations on Escherichia coli colony biofilm beta-lactam and aminoglycoside antibiotic tolerance. BMC Microbiol 2010, 10:185.
62. Partow S, Siewers V, Bjorn S, Nielsen J, Maury J: Characterization of different promoters for designing a new expression vector in Saccharomyces cerevisiae. Yeast 2010, 27(11):955-964.
63. Andersen JB, Sternberg C, Poulsen LK, Bjorn SP, Givskov M, Molin S: New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 1998, 64(6):2240-2246.
64. Geu-Flores F, Nour-Eldin HH, Nielsen MT, Halkier BA: USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCR products. Nucleic Acids Res 2007, 35(7):e55.
65. Nour-Eldin HH, Hansen BG, Norholm MH, Jensen JK, Halkier BA: Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 2006, 34(18):e122.
66. Mikkelsen MD, Buron LD, Salomonsen B, Olsen CE, Hansen BG, Mortensen UH, Halkier BA: Microbial production of indolylglucosinolate through engineering of a multi-gene pathway in a versatile yeast expression platform. Metab Eng 2012, 14(2):104-111.
67. Gietz RD, Woods RA: Yeast transformation by the LiAc/SS Carrier DNA/PEG method. Methods Mol Biol 2006, 313:107-120.
68. Sherman F: Getting started with yeast. Methods Enzymol 1991, 194:3-21.
69. EUCAST: EUCAST definitive document EDef 7.1: method for the determination of broth dilution MICs of antifungal agents for fermentative yeasts. Clin Microbiol Infect 2008, 14(4):398-405.