Candida glabrata susceptibility to antifungals and phagocytosis is modulated by acetate

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Mota, Sandra ^a,b   Alves, Rosana ^a   Carneiro, Catarina ^a   Silva, Sónia ^a   Brown, Alistair J ^c   Istel, Fabian ^d   Kuchler, Karl ^d   Sampaio, Paula ^a   Casal, Margarida ^a   Henriques, Mariana ^a   Paiva, Sandra ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Acetate; Antifungal drug resistance; Candida glabrata; Candidiasis; Fluconazole; Phagocytosis; Transporters

Indexed keywords

ACETIC ACID; ANTIFUNGAL AGENT; FLUCONAZOLE; TUMOR NECROSIS FACTOR ALPHA;

ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BIOFILM; CANDIDA GLABRATA; CELL VIABILITY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; FOOD DEPRIVATION; FUNGAL STRAIN; FUNGUS GROWTH; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHAGOCYTOSIS; REAL TIME POLYMERASE CHAIN REACTION; SERIAL ANALYSIS OF GENE EXPRESSION;

EID: 84946741757     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00919     Document Type: Article

References (65)

1. Baillie, G. S., and Douglas, L. J. (1998). Effect of growth rate on resistance of Candida albicans biofilms to antifungal agents. Antimicrob. Agents Chemother. 42, 1900-1905.
2. Barelle, C. J., Priest, C. L., Maccallum, D. M., Gow, N. A. R., Odds, F. C., and Brown, A. J. P. (2006). Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell. Microbiol. 8, 961-971. doi: 10.1111/j.1462-5822.2005.00676.x
3. Beese-Sims, S. E., Pan, S. J., Lee, J., Hwang-Wong, E., Cormack, B. P., and Levin, D. E. (2012). Mutants in the Candida glabrata glycerol channels are sensitized to cell wall stress. Eukaryot. Cell 11, 1512-1519. doi: 10.1128/EC.00231-12EC.00231-12
4. Brown, A. J., Brown, G. D., Netea, M. G., and Gow, N. A. (2014). Metabolism impacts upon Candida immunogenicity and pathogenicity at multiple levels. Trends Microbiol. 22, 614-622. doi: 10.1016/j.tim.2014.07.001
5. Calderone, R. A., and Clancy, C. J. (2012). Candida and Candidiasis. Washington, DC: ASM Press.
6. Carneiro, C., Vaz, C., Carvalho-Pereira, J., Pais, C., and Sampaio, P. (2014). A new method for yeast phagocytosis analysis by flow cytometry. J. Microbiol. Methods 101, 56-62. doi: 10.1016/j.mimet.2014.03.013
7. Casal, M., Cardoso, H., and Leao, C. (1996). Mechanisms regulating the transport of acetic acid in Saccharomyces cerevisiae. Microbiology 142(Pt 6), 1385-1390. doi: 10.1099/13500872-142-6-1385
8. Casal, M., Paiva, S., Queiros, O., and Soares-Silva, I. (2008). Transport of carboxylic acids in yeasts. FEMS Microbiol. Rev. 32, 974-994. doi: 10.1111/j.1574-6976.2008.00128.x
9. Chandra, J., Kuhn, D. M., Mukherjee, P. K., Hoyer, L. L., Mccormick, T., and Ghannoum, M. A. (2001a). Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183, 5385-5394. doi: 10.1128/JB.183.18.5385-5394.2001
10. Chandra, J., Mukherjee, P. K., Leidich, S. D., Faddoul, F. F., Hoyer, L. L., Douglas, L. J., et al. (2001b). Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J. Dent. Res. 80, 903-908. doi: 10.1177/00220345010800031101
11. Costa, C., Henriques, A., Pires, C., Nunes, J., Ohno, M., Chibana, H., et al. (2013). The dual role of candida glabrata drug:H+ antiporter CgAqr1 (ORF CAGL0J09944g) in antifungal drug and acetic acid resistance. Front. Microbiol. 4:170. doi: 10.3389/fmicb.2013.00170
12. CLSI. (2008). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard CLSI document M27-A3, 3rd Edn. Wayne, PA: Clinical and Laboratory Standards Institute.
13. Douglas, L. J. (2003). Candida biofilms and their role in infection. Trends Microbiol. 11, 30-36. doi: 10.1016/S0966-842X(02)00002-1
14. Ene, I. V., Adya, A. K., Wehmeier, S., Brand, A. C., Maccallum, D. M., Gow, N. A. R., et al. (2012a). Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell. Microbiol. 14, 1319-1335. doi: 10.1111/j.1462-5822.2012.01813.x
15. Ene, I. V., Heilmann, C. J., Sorgo, A. G., Walker, L. A., De Koster, C. G., Munro, C. A., et al. (2012b). Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans. Proteomics 12, 3164-3179. doi: 10.1002/pmic.201200228
16. Ene, I. V., Cheng, S. C., Netea, M. G., and Brown, A. J. (2013). Growth of Candida albicans cells on the physiologically relevant carbon source lactate affects their recognition and phagocytosis by immune cells. Infect. Immun. 81, 238-248. doi: 10.1128/IAI.01092-12IAI.01092-12
17. Fradin, C., De Groot, P., Maccallum, D., Schaller, M., Klis, F., Odds, F. C., et al. (2005). Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 56, 397-415. doi: 10.1111/j.1365-2958.2005.04557.x
18. Fradin, C., Kretschmar, M., Nichterlein, T., Gaillardin, C., D'enfert, C., and Hube, B. (2003). Stage-specific gene expression of Candida albicans in human blood. Mol. Microbiol. 47, 1523-1543. doi: 10.1046/j.1365-2958.2003.03396.x
19. Fukuda, Y., Tsai, H. F., Myers, T. G., and Bennett, J. E. (2013). Transcriptional profiling of Candida glabrata during phagocytosis by neutrophils and in the infected mouse spleen. Infect. Immun. 81, 1325-1333. doi: 10.1128/IAI.00851-12IAI.00851-12
20. Gow, N. A., Van De Veerdonk, F. L., Brown, A. J., and Netea, M. G. (2012). Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat. Rev. Microbiol. 10, 112-122. doi: 10.1038/nrmicro2711nrmicro2711
21. Han, T. L., Cannon, R. D., and Villas-Boas, S. G. (2011). The metabolic basis of Candida albicans morphogenesis and quorum sensing. Fungal Genet. Biol. 48, 747-763. doi: 10.1016/j.fgb.2011.04.002
22. Huggins, G. R., and Preti, G. (1976). Volatile constituents of human vaginal secretions. Am. J. Obstet. Gynecol. 126, 129-136.
23. Jacobsen, I. D., Brunke, S., Seider, K., Schwarzmuller, T., Firon, A., D'enfert, C., et al. (2010). Candida glabrata persistence in mice does not depend on host immunosuppression and is unaffected by fungal amino acid auxotrophy. Infect. Immun. 78, 1066-1077. doi: 10.1128/IAI.01244-09IAI.01244-09
24. Kaur, R., Ma, B., and Cormack, B. P. (2007). A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. U.S.A. 104, 7628-7633. doi: 10.1073/pnas.0611195104
25. Li, Q. Q., Skinner, J., and Bennett, J. E. (2012). Evaluation of reference genes for real-time quantitative PCR studies in Candida glabrata following azole treatment. BMC Mol. Biol. 13:22. doi: 10.1186/1471-2199-13-221471-2199-13-22
26. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
27. Lodi, T., Diffels, J., Goffeau, A., and Baret, P. V. (2007). Evolution of the carboxylate Jen transporters in fungi. FEMS Yeast Res. 7, 646-656. doi: 10.1111/j.1567-1364.2007.00245.x
28. Lorenz, M. C., Bender, J. A., and Fink, G. R. (2004). Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3, 1076-1087. doi: 10.1128/ec.3.5.1075-1087.2004
29. Lorenz, M. C., and Fink, G. R. (2001). The glyoxylate cycle is required for fungal virulence. Nature 412, 83-86. doi: 10.1038/35083594
30. Lorenz, M. C., and Fink, G. R. (2002). Life and death in a macrophage: role of the glyoxylate cycle in virulence. Eukaryot. Cell 1, 657-662. doi: 10.1128/ec.1.5657-662.2002
31. Mollapour, M., and Piper, P. W. (2007). Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistant to acetic acid. Mol. Cell. Biol. 27, 6446-6456. doi: 10.1128/MCB.02205-06
32. Moosa, M. Y., Sobel, J. D., Elhalis, H., Du, W., and Akins, R. A. (2004). Fungicidal activity of fluconazole against Candida albicans in a synthetic vagina-simulative medium. Antimicrob. Agents Chemother. 48, 161-167. doi: 10.1128/AAC.48.1.161-167.2004
33. Netea, M. G., and Marodi, L. (2010). Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol. 31, 346-353. doi: 10.1016/j.it.2010.06.007S1471-4906(10)00105-5
34. Noble, S. M., and Johnson, A. D. (2005). Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot. Cell 4, 298-309. doi: 10.1128/EC.4.2.298-309.2005
35. Otto, V., and Howard, D. H. (1976). Further studies on the intracellular behavior of Torulopsis glabrata. Infect. Immun. 14, 433-438.
36. Pacheco, A., Talaia, G., Sa-Pessoa, J., Bessa, D., Goncalves, M. J., Moreira, R., et al. (2012). Lactic acid production in Saccharomyces cerevisiae is modulated by expression of the monocarboxylate transporters Jen1 and Ady2. FEMS Yeast Res. 12, 375-381. doi: 10.1111/j.1567-1364.2012.00790.x
37. Paiva, S., Devaux, F., Barbosa, S., Jacq, C., and Casal, M. (2004). Ady2p is essential for the acetate permease activity in the yeast Saccharomyces cerevisiae. Yeast 21, 201-210. doi: 10.1002/yea.1056
38. Palkova, Z., Devaux, F., Icicova, M., Minarikova, L., Le Crom, S., and Jacq, C. (2002). Ammonia pulses and metabolic oscillations guide yeast colony development. Mol. Biol. Cell 13, 3901-3914. doi: 10.1091/mbc.E01-12-0149
39. Pfaller, M. A. (2012). Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am. J. Med. 125, S3-S13. doi: 10.1016/j.amjmed.2011.11.001S0002-9343(11)00913-2
40. Pfaller, M. A., Chaturvedi, V., Espinel-Ingroff, A., Ghannoum, M. A., Linda, L., Gosey, M. T., et al. (2008). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts:Approved Standard, 2nd Edn. Wayne, PA: Clinical and Laboratory Standards Institute.
41. Pfaller, M. A., Diekema, D. J., Jones, R. N., Sader, H. S., Fluit, A. C., Hollis, R. J., et al. (2001). International surveillance of bloodstream infections due to Candida species: frequency of occurrence and in vitro susceptibilities to fluconazole, ravuconazole, and voriconazole of isolates collected from 1997 through 1999 in the SENTRY antimicrobial surveillance program. J. Clin. Microbiol. 39, 3254-3259.
42. Pfaller, M. A., Moet, G. J., Messer, S. A., Jones, R. N., and Castanheira, M. (2011). Candida bloodstream infections: comparison of species distributions and antifungal resistance patterns in community-onset and nosocomial isolates in the SENTRY Antimicrobial Surveillance Program, 2008-2009. Antimicrob. Agents Chemother. 55, 561-566. doi: 10.1128/AAC.01079-10AAC.01079-10
43. Piekarska, K., Mol, E., Van Den Berg, M., Hardy, G., Van Den Burg, J., Van Roermund, C., et al. (2006). Peroxisomal fatty acid beta-oxidation is not essential for virulence of Candida albicans. Eukaryot. Cell 5, 1847-1856. doi: 10.1128/ec.00093-06
44. Preti, G., Huggins, G. R., and Silverberg, G. D. (1979). Alterations in the organic compounds of vaginal secretions caused by sexual arousal. Fertil. Steril. 32, 47-54.
45. Prigneau, O., Porta, A., Poudrier, J. A., Colonna-Romano, S., Noel, T., and Maresca, B. (2003). Genes involved in β-oxidation, energy metabolism and glyoxylate cycle are induced by Candida albicans during macrophage infection. Yeast 20, 723-730. doi: 10.1002/yea.998
46. Ramage, G., Saville, S. P., Thomas, D. P., and Lopez-Ribot, J. L. (2005). Candida biofilms: an update. Eukaryot. Cell 4, 633-638. doi: 10.1128/EC.4.4.633-638.2005
47. Ramage, G., Vande Walle, K., Wickes, B. L., and Lopez-Ribot, J. L. (2001). Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob. Agents Chemother. 45, 2475-2479. doi: 10.1128/AAC.45.9.2475-2479.2001
48. Ramirez, M. A., and Lorenz, M. C. (2007). Mutations in alternative carbon utilization pathways in Candida albicans attenuate virulence and confer pleiotropic phenotypes. Eukaryot. Cell 6, 280-290. doi: 10.1128/ec.00372-06
49. Reuss, O., Vik, A., Kolter, R., and Morschhauser, J. (2004). The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341, 119-127. doi: 10.1016/j.gene.2004.06.021
50. Roetzer, A., Gratz, N., Kovarik, P., and Schuller, C. (2010). Autophagy supports Candida glabrata survival during phagocytosis. Cell. Microbiol. 12, 199-216. doi: 10.1111/j.1462-5822.2009.01391.x
51. Rozen, S., and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365-386.
52. Schwarzmuller, T., Ma, B., Hiller, E., Istel, F., Tscherner, M., Brunke, S., et al. (2014). Systematic phenotyping of a large-scale Candida glabrata deletion collection reveals novel antifungal tolerance genes. PLoS Pathog. 10:e1004211. doi: 10.1371/journal.ppat.1004211
53. Seider, K., Brunke, S., Schild, L., Jablonowski, N., Wilson, D., Majer, O., et al. (2011). The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J. Immunol. 187, 3072-3086. doi: 10.4049/jimmunol.1003730
54. Seider, K., Heyken, A., Luttich, A., Miramon, P., and Hube, B. (2010). Interaction of pathogenic yeasts with phagocytes: survival, persistence and escape. Curr. Opin. Microbiol. 13, 392-400. doi: 10.1016/j.mib.2010.05.001
55. Shen, J., Guo, W., and Kohler, J. R. (2005). CaNAT1, a heterologous dominant selectable marker for transformation of Candida albicans and other pathogenic Candida species. Infect. Immun. 73, 1239-1242. doi: 10.1128/IAI.73.2.1239-1242.2005
56. Silva, S., Henriques, M., Martins, A., Oliveira, R., Williams, D., and Azeredo, J. (2009). Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Med. Mycol. 47, 681-689. doi: 10.3109/13693780802549594
57. Soares-Silva, I., Paiva, S., Kotter, P., Entian, K. D., and Casal, M. (2004). The disruption of JEN1 from Candida albicans impairs the transport of lactate. Mol. Membr. Biol. 21, 403-411. doi: 10.1080/09687860400011373
58. Stratford, M., Nebe-Von-Caron, G., Steels, H., Novodvorska, M., Ueckert, J., and Archer, D. B. (2013). Weak-acid preservatives: pH and proton movements in the yeast Saccharomyces cerevisiae. Int. J. Food Microbiol. 161, 164-171. doi: 10.1016/j.ijfoodmicro.2012.12.013
59. Turcotte, B., Liang, X. B., Robert, F., and Soontorngun, N. (2010). Transcriptional regulation of nonfermentable carbon utilization in budding yeast. FEMS Yeast Res. 10, 2-13. doi: 10.1111/j.1567-1364.2009.00555.xFYR555
60. Ueno, K., Matsumoto, Y., Uno, J., Sasamoto, K., Sekimizu, K., Kinjo, Y., et al. (2011). Intestinal resident yeast candida glabrata requires cyb2p-mediated lactate assimilation to adapt in mouse intestine. PLoS ONE 6:e24759. doi: 10.1371/journal.pone.0024759
61. Vachova, L., Chernyavskiy, O., Strachotova, D., Bianchini, P., Burdikova, Z., Fercikova, I., et al. (2009). Architecture of developing multicellular yeast colony: spatio-temporal expression of Ato1p ammonium exporter. Environ. Microbiol. 11, 1866-1877. doi: 10.1111/j.1462-2920.2009.01911.xEMI1911
62. Vieira, N., Casal, M., Johansson, B., Maccallum, D. M., Brown, A. J. P., and Paiva, S. (2010). Functional specialization and differential regulation of short-chain carboxylic acid transporters in the pathogen Candida albicans. Mol. Microbiol. 75, 1337-1354. doi: 10.1111/j.1365-2958.2009.07003.x
63. Wilson, D., Thewes, S., Zakikhany, K., Fradin, C., Albrecht, A., Almeida, R., et al. (2009). Identifying infection-associated genes of Candida albicans in the postgenomic era. FEMS Yeast Res. 9, 688-700. doi: 10.1111/j.1567-1364.2009.00524.xFYR524
64. Yamaguchi, N., Sonoyama, K., Kikuchi, H., Nagura, T., Aritsuka, T., and Kawabata, J. (2005). Gastric colonization of Candida albicans differs in mice fed commercial and purified diets. J. Nutr. 135, 109-115.
65. Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., and Madden, T. L. (2012). Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134. doi: 10.1186/1471-2105-13-134