Anti-Candida albicans biofilm effect of novel heterocyclic compounds

Journal of Antimicrobial Chemotherapy

Volumn 69, Issue 2, 2014, Pages 416-427

  Kagan, Sarah ^a   Jabbour, Adel ^b,c   Sionov, Edward ^a   Alquntar, Abed A ^b,c   Steinberg, Doron ^b   Srebnik, Morris ^c   Nir paz, Ran ^a   Weiss, Aryeh ^d   Polacheck, Itzhack ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d BAR ILAN UNIVERSITY   (Israel)

Author keywords

Antifungal; C. albicans; Quorum sensing; TZD

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; FLUORESCENT DYE; HETEROCYCLIC COMPOUND; PROPIDIUM IODIDE; STEROL; SUCCINIMIDE DERIVATIVE; SULFUR;

ARTICLE; ATOM; BIOFILM; CANDIDA ALBICANS; CELL STRUCTURE; CELL VIABILITY; CELL WALL; CONTROLLED STUDY; DRUG ACTIVITY; FUNGUS HYPHAE; NONHUMAN; STRUCTURE ACTIVITY RELATION; TRANSMISSION ELECTRON MICROSCOPY; XTT ASSAY; YEAST;

ANTIFUNGAL; C. ALBICANS; QUORUM SENSING; TZD;

ANIMALS; ANTIFUNGAL AGENTS; BIOFILMS; CANDIDA ALBICANS; HETEROCYCLIC COMPOUNDS; SHEEP; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84892469135     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkt365     Document Type: Article

References (54)

1. Gomes PN, da Silva WJ, Pousa CC et al. Bioactivity and cellular structure of Candida albicans and Candida glabrata biofilms grown in the presence of fluconazole. Arch Oral Biol 2011; 56: 1274-81.
2. Mayer FL, Wilson D, Hube B. Candida albicans pathogenicity mechanisms. Virulence 2013; 4: 119-28.
3. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 2007; 20: 133-63.
4. Finkel JS, Mitchell AP. Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 2011; 9: 109-18.
5. Blankenship JR, Mitchell AP. How to build a biofilm: a fungal perspective. Curr Opin Microbiol 2006; 9: 588-94.
6. Ramage G, Saville SP, Thomas DP et al. Candida biofilms: an update. Eukaryot Cell 2005; 4: 633-8.
7. Srinivasan A, Uppuluri P, Lopez-Ribot J et al. Development of a high-throughput Candida albicans biofilm chip. PLoS One 2011; 6: e19036.
8. Ajesh K, Sreejith K. Cryptococcus laurentii biofilms: structure, development and antifungal drug resistance. Mycopathologia 2012; 174:409-19.
9. Nunes JM, Bizerra FC, Ferreira RC et al. Molecular identification, antifungal susceptibility profile, and biofilm formation of clinical and environmental Rhodotorula species isolates. Antimicrob Agents Chemother 2013; 57:382-9.
10. Ramage G, Mowat E, Jones B et al. Our current understanding of fungal biofilms. Crit Rev Microbiol 2009; 35: 340-55.
11. Ramage G, Rajendran R, Gutierrez-Correa M et al. Aspergillus biofilms: clinical and industrial significance. FEMS Microbiol Lett 2011; 324: 89-97.
12. Ramage G, Rajendran R, Sherry L et al. Fungal biofilm resistance. Int J Microbiol 2012; 2012: 528521.
13. Deveau A, Hogan DA. Linking quorum sensing regulation and biofilm formation by Candida albicans. Methods Mol Biol 2011; 692: 219-33.
14. Han TL, Cannon RD, Villas-Boas SG. The metabolic basis of Candida albicans morphogenesis and quorum sensing. Fungal Genet Biol 2011; 48:747-63.
15. Ramage G, Saville SP, Wickes BL et al. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 2002; 68: 5459-63.
16. Weber K, Schulz B, Ruhnke M. The quorum-sensing molecule E, E-farnesol-its variable secretion and its impact on the growth and metabolism of Candida species. Yeast 2010; 27: 727-39.
17. Alem MA, Oteef MD, Flowers TH et al. Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot Cell 2006; 5: 1770-9.
18. Chen H, Fujita M, Feng Q et al. Tyrosol is a quorum-sensing molecule in Candida albicans. Proc Natl Acad Sci USA 2004; 101: 5048-52.
19. Angel-Moreno A, Boronat M, BolanosMet al. Candida glabratafungemia cured byantibiotic-lock therapy: case report and short review. J Infect 2005;51: e85-7.
20. Bugli F, Posteraro B, Papi M et al. In vitro interaction between alginate lyase and amphotericin B against Aspergillus fumigatus biofilm determined by different methods. Antimicrob Agents Chemother 2013;57: 1275-82.
21. de Aguiar Cordeiro R, Mourao CI, Rocha MF et al. Antifolates inhibit Cryptococcus biofilms and enhance susceptibility of planktonic cells to amphotericin B. Eur J Clin Microbiol Infect Dis 2013; 32: 557-64.
22. Kucharikova S, Sharma N, Spriet I et al. Activity of systemically administered echinocandins against in vivo mature Candida albicans biofilms developed in a rat subcutaneous model. Antimicrob Agents Chemother 2013; 57: 2365-8.
23. Ramage G, Jose A, Sherry L et al. Liposomal amphotericin B displays rapid dose dependent activity against Candida albicans biofilms. Antimicrob Agents Chemother 2013; 57: 2369-71.
24. Wu CY, Lee PI. Antibiotic-lock therapyanderythromycinfor treatmentof catheter-related Candida parapsilosis and Staphylococcus aureus infections. J Antimicrob Chemother 2007; 60: 706-7.
25. You J, Du L, King JB et al. Small-molecule suppressors of Candida albicans biofilm formation synergistically enhance the antifungal activity of amphotericin B against clinical Candida isolates. ACS Chem Biol 2013; 8:840-8.
26. De Sordi L, Muhlschlegel FA. Quorum sensing and fungal-bacterial interactions in Candida albicans: a communicative network regulating microbial coexistence and virulence. FEMS Yeast Res 2009; 9: 990-9.
27. Bandara HM, Cheung BP, Watt RM et al. Secretory products of Escherichia coli biofilm modulate Candida biofilm formation and hyphal development. J Investig Clin Dent 2013; 4: 186-99.
28. Cruz MR, Graham CE, Gagliano BC et al. Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infect Immun 2013; 81: 189-200.
29. Morales DK, Grahl N, Okegbe C et al. Control of Candida albicans metabolism and biofilm formation by Pseudomonas aeruginosa phenazines. MBio 2013; 4: e00526-12.
30. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts-Third Edition: Approved Standard M27-A3. CLSI, Wayne, PA, USA, 2008.
31. Falk R, Domb AJ, Polacheck I. A novel injectable water-soluble amphotericin B-arabinogalactan conjugate. Antimicrob Agents Chemother 1999; 43: 1975-81.
32. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 2012; 9: 671-5.
33. Schindelin J, Arganda-Carreras I, Frise E. Fiji: an open-source platform for biological-image analysis. Nature Methods 2012; 9: 676-82.
34. Chaffin WL, Lopez-Ribot JL, Casanova M et al. Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 1998; 62: 130-80.
35. Alvarez FJ, Douglas LM, Konopka JB. The Sur7 protein resides in punctate membrane subdomains and mediates spatial regulation of cell wall synthesis in Candida albicans. Commun Integr Biol 2009; 2: 76-7.
36. Alvarez FJ, Douglas LM, Rosebrock A et al. The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol Biol Cell 2008; 19: 5214-25.
37. Douglas LM, Wang HX, Keppler-Ross S et al. Sur7 promotes plasma membrane organization and is needed for resistance to stressful conditions and to the invasive growth and virulence of Candida albicans. MBio 2011; 3: e00254-11.
38. Lettner T, Zeidler U, Gimona M et al. Candida albicans AGE3, the ortholog of the S. cerevisiae ARF-GAP-encoding gene GCS1, is required for hyphal growth and drug resistance. PLoS One 2010;5: e11993.
39. Martin SW, Konopka JB. Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot Cell 2004; 3: 675-84.
40. Oberholzer U, Nantel A, Berman J et al. Transcript profiles of Candida albicans cortical actin patch mutants reflect their cellular defects: contribution of the Hog1p and Mkc1p signaling pathways. Eukaryot Cell 2006; 5: 1252-65.
41. Ragni E, Calderon J, Fascio U et al. Phr1p, a glycosylphosphatidylinsitolanchored b(1,3)-glucanosyltransferase critical for hyphal wall formation, localizes to the apical growth sites and septa in Candida albicans. Fungal Genet Biol 2011; 48: 793-805.
42. Wang HX, Douglas LM, Aimanianda V et al. The Candida albicans Sur7 protein is needed for proper synthesis of the fibrillar component of the cell wall that confers strength. Eukaryot Cell 2011; 10: 72-80.
43. Lattif AA, Mukherjee PK, Chandra J et al. Lipidomics of Candida albicans biofilms reveals phase-dependent production of phospholipid molecular classes and role for lipid rafts in biofilm formation. Microbiology 2011;157: 3232-42.
44. Insenser M, Nombela C, Molero G et al. Proteomic analysis of detergent-resistant membranes from Candida albicans. Proteomics 2006;6 Suppl 1: S74-81.
45. Bernardo SM, Lee SA. Candida albicans SUR7 contributes to secretion, biofilm formation, and macrophage killing. BMC Microbiol 2010;10: 133.
46. Douglas LM, Alvarez FJ, McCreary C et al. Septin function in yeast model systems and pathogenic fungi. Eukaryot Cell 2005; 4: 1503-12.
47. Li L, Zhang C, Konopka JB. A Candida albicans temperature-sensitive cdc12-6 mutant identifies roles for septins in selection of sites of germ tube formation and hyphal morphogenesis. Eukaryot Cell 2012; 11:1210-8.
48. Li F, Palecek SP. EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot Cell 2003; 2: 1266-73.
49. Li F, Svarovsky MJ, Karlsson AJ et al. Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell 2007;6: 931-9.
50. Nobile CJ, Schneider HA, Nett JE et al. Complementary adhesin function in C. albicans biofilm formation. Curr Biol 2008; 18: 1017-24.
51. Nobile CJ, Andes DR, Nett JE et al. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2006; 2: e63.
52. Nobile CJ, Mitchell AP. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol 2005; 15:1150-5.
53. Chaffin WL. Candida albicans cell wall proteins. Microbiol Mol Biol Rev 2008; 72: 495-544.
54. Richard ML, Plaine A. Comprehensive analysis of glycosylphosphatidylinositol- anchored proteins in Candida albicans. Eukaryot Cell 2007; 6:119-33.