Time course analysis of candida albicans metabolites during biofilm development

Journal of Proteome Research

Volumn 12, Issue 6, 2013, Pages 2375-2385

  Zhu, Zhenyu ^a   Wang, Hui ^a   Shang, Qinghua ^a   Jiang, Yuanying ^a   Cao, Yingying ^a   Chai, Yifeng ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

biofilm; Candida albicans; drug resistance; metabolite; trehalose

Indexed keywords

4 AMINOBUTYRIC ACID; ALANINE; ARABINITOL; ASPARAGINE; ASPARTIC ACID; FUMARIC ACID; GALACTOSE; GLUCOSE; GLUTAMIC ACID; GLYCEROL; GLYCEROPHOSPHATE; GLYCINE; INOSITOL; ISOLEUCINE; LACTIC ACID; MALIC ACID; MANNOSE; MANNOSE PHOSPHATE; N ACETYLGLUTAMIC ACID; PHENYLALANINE; PHOSPHATE; PUTRESCINE; PYROGLUTAMIC ACID; SARCOSINE; SERINE; SUCCINIC ACID; THREONINE; TREHALOSE; TRICARBOXYLIC ACID; VALINE;

AMINO ACID METABOLISM; ANTIBIOTIC SENSITIVITY; ARTICLE; BIOFILM; CANDIDA ALBICANS; FUNGAL DEVELOPMENT; FUNGUS GROWTH; GLYCOLYSIS; GROWTH CURVE; LIPOGENESIS; MASS FRAGMENTOGRAPHY; METABOLITE; METABOLOMICS; NONHUMAN; OXIDATIVE STRESS; PLANKTON; PRIORITY JOURNAL;

CANDIDA ALBICANS;

EID: 84879400084     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300447k     Document Type: Article

References (51)

1. Fidel, P. L., Jr. Candida-host interactions in HIV disease: relationships in oropharyngeal candidiasis Adv. Dent. Res. 2006, 19 (1) 80-4
2. Redding, S. W.; Zellars, R. C.; Kirkpatrick, W. R.; McAtee, R. K.; Caceres, M. A.; Fothergill, A. W.; Lopez-Ribot, J. L.; Bailey, C. W.; Rinaldi, M. G.; Patterson, T. F. Epidemiology of oropharyngeal Candida colonization and infection in patients receiving radiation for head and neck cancer J. Clin. Microbiol. 1999, 37 (12) 3896-900
3. Perlroth, J.; Choi, B.; Spellberg, B. Nosocomial fungal infections: epidemiology, diagnosis, and treatment Med. Mycol. 2007, 45 (4) 321-46
4. O'Toole, G.; Kaplan, H. B.; Kolter, R. Biofilm formation as microbial development Annu. Rev. Microbiol. 2000, 54, 49-79
5. Nicastri, E.; Petrosillo, N.; Viale, P.; Ippolito, G. Catheter-related bloodstream infections in HIV-infected patients Ann. N.Y. Acad. Sci. 2001, 946, 274-90
6. Kuhn, D. M.; Chandra, J.; Mukherjee, P. K.; Ghannoum, M. A. Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces Infect. Immun. 2002, 70 (2) 878-88
7. Finkel, J. S.; Mitchell, A. P. Genetic control of Candida albicans biofilm development Nat. Rev. Microbiol. 2011, 9 (2) 109-18
8. Nobile, C. J.; Mitchell, A. P. Genetics and genomics of Candida albicans biofilm formation Cell. Microbiol. 2006, 8 (9) 1382-91
9. Costerton, J. W.; Stewart, P. S.; Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections Science 1999, 284 (5418) 1318-22
10. Davey, M. E.; O'Toole, G, A. Microbial biofilms: from ecology to molecular genetics Microbiol. Mol. Biol. Rev. 2000, 64 (4) 847-67
11. Chandra, J.; Mukherjee, P. K.; Leidich, S. D.; Faddoul, F. F.; Hoyer, L. L.; Douglas, L. J.; Ghannoum, M. A. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro J. Dent. Res. 2001, 80 (3) 903-8
12. Ramage, G.; Vandewalle, K.; Wickes, B. L.; Lopez-Ribot, J. L. Characteristics of biofilm formation by Candida albicans Rev. Iberoam Micol. 2001, 18 (4) 163-70
13. Perumal, P.; Mekala, S.; Chaffin, W. L. Role for cell density in antifungal drug resistance in Candida albicans biofilms Antimicrob. Agents Chemother. 2007, 51 (7) 2454-63
14. Ramage, G.; Bachmann, S.; Patterson, T. F.; Wickes, B. L.; Lopez-Ribot, J. L. Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms J. Antimicrob. Chemother. 2002, 49 (6) 973-80
15. Mukherjee, P. K.; Chandra, J.; Kuhn, D. M.; Ghannoum, M. A. Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols Infect. Immunol. 2003, 71 (8) 4333-40
16. 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) 510-20
17. Nett, J. E.; Sanchez, H.; Cain, M. T.; Andes, D. R. Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan J. Infect. Dis. 2010, 202 (1) 171-5
18. Kumamoto, C. A. A contact-activated kinase signals Candida albicans invasive growth and biofilm development Proc. Natl. Acad. Sci. U. S. A. 2005, 102 (15) 5576-81
19. Garcia-Sanchez, S.; Aubert, S.; Iraqui, I.; Janbon, G.; Ghigo, J. M.; d'Enfert, C. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns Eukaryot. Cell 2004, 3 (2) 536-45
20. Thomas, D. P.; Bachmann, S. P.; Lopez-Ribot, J. L. Proteomics for the analysis of the Candida albicans biofilm lifestyle Proteomics 2006, 6 (21) 5795-804
21. Yeater, K. M.; Chandra, J.; Cheng, G.; Mukherjee, P. K.; Zhao, X.; Rodriguez-Zas, S. L.; Kwast, K. E.; Ghannoum, M. A.; Hoyer, L. L. Temporal analysis of Candida albicans gene expression during biofilm development Microbiology 2007, 153 (Pt 8) 2373-85
22. Fiehn, O. Metabolomics-the link between genotypes and phenotypes Plant Mol. Biol. 2002, 48 (1-2) 155-71
23. Vaidyanathan, S. Profiling microbial metabolomes: what do we stand to gain? Metabolomics 2005, 1 (1) 17-28
24. Halouska, S.; Chacon, O.; Fenton, R. J.; Zinniel, D. K.; Barletta, R. G.; Powers, R. Use of NMR metabolomics to analyze the targets of D-cycloserine in mycobacteria: role of D-alanine racemase J. Proteome Res. 2007, 6 (12) 4608-14
25. Sadykov, M. R.; Zhang, B.; Halouska, S.; Nelson, J. L.; Kreimer, L. W.; Zhu, Y.; Powers, R.; Somerville, G. A. Using NMR metabolomics to investigate tricarboxylic acid cycle-dependent signal transduction in Staphylococcus epidermidis J. Biol. Chem. 2010, 285 (47) 36616-24
26. Tan, G.; Lou, Z.; Liao, W.; Zhu, Z.; Dong, X.; Zhang, W.; Li, W.; Chai, Y. Potential biomarkers in mouse myocardium of doxorubicin-induced cardiomyopathy: a metabonomic method and its application PLoS One 2011, 6 (11) e27683
27. Bolten, C. J.; Wittmann, C. Appropriate sampling for intracellular amino acid analysis in five phylogenetically different yeasts Biotechnol. Lett. 2008, 30 (11) 1993-2000
28. Canelas, A. B.; ten Pierick, A.; Ras, C.; Seifar, R. M.; van Dam, J. C.; van Gulik, W. M.; Heijnen, J. J. Quantitative evaluation of intracellular metabolite extraction techniques for yeast metabolomics Anal. Chem. 2009, 81 (17) 7379-89
29. Schneider, K.; Kromer, J. O.; Wittmann, C.; Alves-Rodrigues, I.; Meyerhans, A.; Diez, J.; Heinzle, E. Metabolite profiling studies in Saccharomyces cerevisiae: an assisting tool to prioritize host targets for antiviral drug screening Microb. Cell Fact 2009, 8, 12
30. Bonhomme, J.; Chauvel, M.; Goyard, S.; Roux, P.; Rossignol, T.; d'Enfert, C. Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans Mol. Microbiol. 2011, 80 (4) 995-1013
31. Seneviratne, C. J.; Wang, Y.; Jin, L.; Abiko, Y.; Samaranayake, L. P. Candida albicans biofilm formation is associated with increased anti-oxidative capacities Proteomics 2008, 8 (14) 2936-47
32. Abu-Elteen, K. H.; Whittaker, P. A. Effect of sub-inhibitory concentration of chlorhexidine on lipid and sterol composition of Candida albicans Mycopathologia 1997, 140 (2) 69-76
33. Hitchcock, C. A.; Barrett-Bee, K. J.; Russell, N. J. The lipid composition and permeability to azole of an azole- and polyene-resistant mutant of Candida albicans J. Med. Vet. Mycol. 1987, 25 (1) 29-37
34. Reynolds, T. B. Strategies for acquiring the phospholipid metabolite inositol in pathogenic bacteria, fungi and protozoa: making it and taking it Microbiology 2009, 155 (Pt 5) 1386-96
35. Cao, Y. Y.; Cao, Y. B.; Xu, Z.; Ying, K.; Li, Y.; Xie, Y.; Zhu, Z. Y.; Chen, W. S.; Jiang, Y. Y. cDNA microarray analysis of differential gene expression in Candida albicans biofilm exposed to farnesol Antimicrob. Agents Chemother. 2005, 49 (2) 584-9
36. Lattif, A. A.; Mukherjee, P. K.; Chandra, J.; Roth, M. R.; Welti, R.; Rouabhia, M.; Ghannoum, M. A. Lipidomics of Candida albicans biofilms reveals phase-dependent production of phospholipid molecular classes and role for lipid rafts in biofilm formation Microbiology 2011, 157 (Pt 11) 3232-42
37. Nett, J. E.; Lepak, A. J.; Marchillo, K.; Andes, D. R. Time course global gene expression analysis of an in vivo Candida biofilm J. Infect. Dis. 2009, 200 (2) 307-13
38. Baillie, G. S.; Douglas, L. J. Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents J. Antimicrob. Chemother. 2000, 46 (3) 397-403
39. Murillo, L. A.; Newport, G.; Lan, C. Y.; Habelitz, S.; Dungan, J.; Agabian, N. M. Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans Eukaryot. Cell 2005, 4 (9) 1562-73
40. Zhu, J.; Krom, B. P.; Sanglard, D.; Intapa, C.; Dawson, C. C.; Peters, B. M.; Shirtliff, M. E.; Jabra-Rizk, M. A. Farnesol-induced apoptosis in Candida albicans is mediated by Cdr1-p extrusion and depletion of intracellular glutathione PLoS One 2011, 6 (12) e28830
41. Tabor, C. W.; Tabor, H. Polyamines in microorganisms Microbiol. Rev. 1985, 49 (1) 81-99
42. Martinez, J. P.; Lopez-Ribot, J. L.; Gil, M. L.; Sentandreu, R.; Ruiz-Herrera, J. Inhibition of the dimorphic transition of Candida albicans by the ornithine decarboxylase inhibitor 1,4-diaminobutanone: alterations in the glycoprotein composition of the cell wall J. Gen. Microbiol. 1990, 136 (10) 1937-43
43. Herrero, A. B.; Lopez, M. C.; Garcia, S.; Schmidt, A.; Spaltmann, F.; Ruiz-Herrera, J.; Dominguez, A. Control of filament formation in Candida albicans by polyamine levels Infect. Immun. 1999, 67 (9) 4870-8
44. Elbein, A. D.; Pan, Y. T.; Pastuszak, I.; Carroll, D. New insights on trehalose: a multifunctional molecule Glycobiology 2003, 13 (4) 17R-27R
45. Arguelles, J. C. Physiological roles of trehalose in bacteria and yeasts: a comparative analysis Arch. Microbiol. 2000, 174 (4) 217-24
46. Richards, A. B.; Krakowka, S.; Dexter, L. B.; Schmid, H.; Wolterbeek, A. P.; Waalkens-Berendsen, D. H.; Shigoyuki, A.; Kurimoto, M. Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies Food Chem. Toxicol. 2002, 40 (7) 871-98
47. Alvarez-Peral, F. J.; Zaragoza, O.; Pedreno, Y.; Arguelles, J. C. Protective role of trehalose during severe oxidative stress caused by hydrogen peroxide and the adaptive oxidative stress response in Candida albicans Microbiology 2002, 148 (Pt 8) 2599-606
48. Zaragoza, O.; Blazquez, M. A.; Gancedo, C. Disruption of the Candida albicans TPS1 gene encoding trehalose-6-phosphate synthase impairs formation of hyphae and decreases infectivity J. Bacteriol. 1998, 180 (15) 3809-15
49. Gonzalez-Parraga, P.; Sanchez-Fresneda, R.; Zaragoza, O.; Arguelles, J. C. Amphotericin B induces trehalose synthesis and simultaneously activates an antioxidant enzymatic response in Candida albicans Biochim. Biophys. Acta 2011, 1810 (8) 777-83
50. Gillum, A. M.; Tsay, E. Y. H.; Kirsch, D. R. Isolation of the Candida albicans genes for orotidine-59-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations Mol. Gen. Genet. 1984, 198, 179-182
51. Lu, H.; Zhu, Z.; Dong, L.; Jia, X.; Sun, X.; Yan, L.; Chai, Y.; Jiang, Y.; Cao, Y. Lack of trehalose accelerates H2O2-induced Candida albicans apoptosis through regulating Ca2+ signaling pathway and caspase activity PLoS One 2011, 6 (1) e15808