The cell wall protein Ecm33 of Candida albicans is involved in chronological life span, morphogenesis, cell wall regeneration, stress tolerance, and host-cell interaction

Frontiers in Microbiology

Volumn 7, Issue FEB, 2016, Pages

  Gil Bona, Ana ^a,b   Reales Calderon, Jose A ^a,b   Parra Giraldo, Claudia M ^a,c   Martinez Lopez, Raquel ^a   Monteoliva, Lucia ^a,b   Gil, Concha ^a,b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b INSTITUTO RAMÓN Y CAJAL DE INVESTIGACIÓN SANITARIA IRYCIS   (Spain)

^c PONTIFICIA UNIVERSIDAD JAVERIANA   (Colombia)

Author keywords

Candida albicans; Cell wall regeneration; Chronological lifespan; Ecm33; Host cell interaction; Stress response; Veil growth

Indexed keywords

CELL MEMBRANE PROTEIN; ECM33 PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANDIDA ALBICANS; CELL INTERACTION; CELL REGENERATION; CELL WALL; CYTOTOXICITY ASSAY; FLUORESCENCE; FUNGUS GROWTH; IMMUNOBLOTTING; LIFESPAN; MACROPHAGE; MICROSCOPY; MORPHOGENESIS; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PHAGOCYTOSIS; PHENOTYPE; SCANNING ELECTRON MICROSCOPY; TEMPERATURE STRESS; WESTERN BLOTTING;

EID: 84962129064     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00064     Document Type: Article

References (60)

1. Alexandre, H. (2013). Flor yeasts of Saccharomyces cerevisiae-their ecology, genetics and metabolism. Int. J. Food Microbiol. 167, 269-275. doi: 10.1016/j.ijfoodmicro.2013.08.021
2. Alexandre, H., Blanchet, S., and Charpentier, C. (2000). Identification of a 49-kDa hydrophobic cell wall mannoprotein present in velum yeast which may be implicated in velum formation. FEMS Microbiol. Lett. 185, 147-150. doi: 10.1111/j.1574-6968.2000.tb09053.x
3. Alvarez, F. J., Douglas, L. M., Rosebrock, A., and Konopka, J. B. (2008). The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol. Biol. Cell 19, 5214-5225. doi: 10.1091/mbc. E08-05-0479
4. Aronova, S., Wedaman, K., Anderson, S., Yates, J. III, and Powers, T. (2007). Probing the membrane environment of the TOR kinases reveals functional interactions between TORC1, actin, and membrane trafficking in Saccharomyces cerevisiae. Mol. Biol. Cell 18, 2779-2794. doi: 10.1091/mbc. E07-030274
5. Bonawitz, N. D., Chatenay-Lapointe, M., Pan, Y., and Shadel, G. S. (2007). Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell Metab. 5, 265-277. doi: 10.1016/j.cmet.2007.02.009
6. Cabezón, V., Llama-Palacios, A., Nombela, C., Monteoliva, L., and Gil, C. (2009). Analysis of Candida albicans plasma membrane proteome. Proteomics 9, 4770-4786. doi: 10.1002/pmic.200800988
7. Carmona-Gutierrez, D., Eisenberg, T., Buttner, S., Meisinger, C., Kroemer, G., and Madeo, F. (2010). Apoptosis in yeast: triggers, pathways, subroutines. Cell Death. Differ. 17, 763-773. doi: 10.1038/cdd.2009.219
8. Castillo, L., Calvo, E., Martinez, A. I., Ruiz-Herrera, J., Valentin, E., Lopez, J. A., et al. (2008). A study of the Candida albicans cell wall proteome. Proteomics 8, 3871-3881. doi: 10.1002/pmic.200800110
9. Chaffin, W. L. (2008). Candida albicans cell wall proteins. Microbiol. Mol. Biol. Rev. 72, 495-544. doi: 10.1128/MMBR.00032-07
10. Chen, Y., Zhu, J., Ying, S. H., and Feng, M. G. (2014). The GPI-anchored protein Ecm33 is vital for conidiation, cell wall integrity, and multi-stress tolerance of two filamentous entomopathogens but not for virulence. Appl. Microbiol. Biotechnol. 98, 5517-5529. doi: 10.1007/s00253-014-5577-y
11. Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E. D., Sevier, C. S., et al. (2010). The genetic landscape of a cell. Science 327, 425-431. doi: 10.1126/science.1180823
12. Douglas, L. M., Wang, H. X., Keppler-Ross, S., Dean, N., and Konopka, J. B. (2012). Sur7 promotes plasma membrane organization and is needed for resistance to stressful conditions and to the invasive growth and virulence of Candida albicans. MBio 3:piie254-11. doi: 10.1128/mBio.00254-11
13. Fabrizio, P., Battistella, L., Vardavas, R., Gattazzo, C., Liou, L. L., Diaspro, A., et al. (2004). Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J. Cell Biol. 166, 1055-1067. doi: 10.1083/jcb.200404002
14. Fabrizio, P., Gattazzo, C., Battistella, L., Wei, M., Cheng, C., Mcgrew, K., et al. (2005). Sir2 blocks extreme life-span extension. Cell 123, 655-667. doi: 10.1016/j.cell.2005.08.042
15. Fernández-Arenas, E., Cabezón, V., Bermejo, C., Arroyo, J., Nombela, C., Diez-Orejas, R., et al. (2007). Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol. Cell Proteom. 6, 460-478. doi: 10.1074/mcp. M600210-MCP200
16. Fontana, L., Partridge, L., and Longo, V. D. (2010). Extending healthy life span-from yeast to humans. Science 328, 321-326. doi: 10.1126/science.1172539
17. Free, S. J. (2013). Fungal cell wall organization and biosynthesis. Adv. Genet. 81, 33-82. doi: 10.1016/B978-0-12-407677-8.00002-6
18. Fuchs, B. B., and Mylonakis, E. (2009). Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot. Cell 8, 1616-1625. doi: 10.1128/EC.00193-09
19. Gil-Bona, A., Llama-Palacios, A., Parra, C. M., Vivanco, F., Nombela, C., Monteoliva, L., et al. (2015a). Proteomics unravels extracellular vesicles as carriers of classical cytoplasmic proteins in Candida albicans. J. Proteome Res. 14, 142-153. doi: 10.1021/pr5007944
20. Gil-Bona, A., Monteoliva, L., and Gil, C. (2015b). Global proteomic profiling of the secretome of Candida albicans ecm33 cell wall mutant reveals the involvement of ecm33 in sap2 secretion. J. Proteome Res. 14, 4270-4281. doi: 10.1021/acs.jproteome.5b00411
21. Gil-Bona, A., Parra-Giraldo, C. M., Hernaez, M. L., Reales-Calderon, J. A., Solis, N. V., Filler, S. G., et al. (2015c). Candida albicans cell shaving uncovers new proteins involved in cell wall integrity, yeast to hypha transition, stress response and host-pathogen interaction. J. Proteom. 127(Pt B), 340-351. doi: 10.1016/j.jprot.2015.06.006
22. Gillum, A. M., Tsay, E. Y. H., and Kirsch, D. R. (1984). Isolation of the Candida albicans gene for orotidine-5'-phosphate decarboxilase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198, 179-182. doi: 10.1007/BF00328721
23. Hausauer, D. L., Gerami-Nejad, M., Kistler-Anderson, C., and Gale, C. A. (2005). Hyphal guidance and invasive growth in Candida albicans require the Ras-like GTPase Rsr1p and its GTPase-activating protein Bud2p. Eukaryot. Cell 4, 1273-1286. doi: 10.1128/EC.4.7.1273-1286.2005
24. Kaeberlein, M., Burtner, C. R., and Kennedy, B. K. (2007). Recent developments in yeast aging. PLoS Genet. 3:e84. doi: 10.1371/journal.pgen.0030084
25. Kaeberlein, M., Powers, R. W. III, Steffen, K. K., Westman, E. A., Hu, D., Dang, N., et al. (2005). Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310, 1193-1196. doi: 10.1126/science.1115535
26. Keppler-Ross, S., Douglas, L., Konopka, J. B., and Dean, N. (2010). Recognition of yeast by murine macrophages requires mannan but not glucan. Eukaryot. Cell 9, 1776-1787. doi: 10.1128/EC.00156-10
27. Klis, F. M., Sosinska, G. J., De Groot, P. W., and Brul, S. (2009). Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. FEMS Yeast Res. 9, 1013-1028. doi: 10.1111/j.1567-1364.2009.00541.x
28. Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., et al. (2009). Classification of cell death: recommendations of the nomenclature committee on cell death 2009. Cell Death. Differ. 16, 3-11. doi: 10.1038/cdd.2008.150
29. Kuranda, K., Leberre, V., Sokol, S., Palamarczyk, G., and Francois, J. (2006). Investigating the caffeine effects in the yeast Saccharomyces cerevisiae brings new insights into the connection between TOR, PKC and Ras/cAMP signalling pathways. Mol. Microbiol. 61, 1147-1166. doi: 10.1111/j.1365-2958.2006.05300.x
30. Lagorce, A., Hauser, N. C., Labourdette, D., Rodriguez, C., Martin-Yken, H., Arroyo, J., et al. (2003). Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 278, 20345-20357. doi: 10.1074/jbc. M211604200
31. Lee, K. L., Buckley, H. R., and Campbell, C. C. (1975). An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans. Sabouraudia 13, 148-153. doi: 10.1080/00362177585190271
32. Li, D., Chen, H., Florentino, A., Alex, D., Sikorski, P., Fonzi, W. A., et al. (2011). Enzymatic dysfunction of mitochondrial complex I of the Candida albicans goa1 mutant is associated with increased reactive oxidants and cell death. Eukaryot. Cell 10, 672-682. doi: 10.1128/EC.00303-10
33. Li, X., Huang, X., Zhao, J., Zhao, J., Wei, Y., and Jiang, L. (2008). The MAP kinase-activated protein kinase Rck2p plays a role in rapamycin sensitivity in Saccharomyces cerevisiae and Candida albicans. FEMS Yeast Res. 8, 715-724. doi: 10.1111/j.1567-1364.2008.00402.x
34. Longo, V. D., and Fabrizio, P. (2002). Regulation of longevity and stress resistance: a molecular strategy conserved from yeast to humans? Cell Mol. Life Sci. 59, 903-908. doi: 10.1007/s00018-002-8477-8
35. Marek, A., and Korona, R. (2013). Restricted pleiotropy facilitates mutational erosion of major life-history traits. Evolution 67, 3077-3086. doi: 10.1111/evo.12196
36. Martin, H., Rodriguez-Pachon, J. M., Ruiz, C., Nombela, C., and Molina, M. (2000). Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J. Biol. Chem. 275, 1511-1519. doi: 10.1074/jbc.275.2.1511
37. Martínez-Lopez, R., Monteoliva, L., Diez-Orejas, R., Nombela, C., and Gil, C. (2004). The GPI-anchored protein CaEcm33p is required for cell wall integrity, morphogenesis and virulence in Candida albicans. Microbiology 150, 3341-3354. doi: 10.1099/mic.0.27320-0
38. Martínez-Lopez, R., Park, H., Myers, C. L., Gil, C., and Filler, S. G. (2006). Candida albicans Ecm33p is important for normal cell wall architecture and interactions with host cells. Eukaryot. Cell. 5, 140-147. doi: 10.1128/EC.5.1.140-147.2006
39. McCluskey, K., Wiest, A., and Plamann, M. (2010). The Fungal genetics stock center: a repository for 50 years of fungal genetics research. J. Biosci. 35, 119-126. doi: 10.1007/s12038-010-0014-6
40. Navarro-Garcia, F., Eisman, B., Fiuza, S. M., Nombela, C., and Pla, J. (2005). The MAP kinase Mkc1p is activated under different stress conditions in Candida albicans. Microbiology 151, 2737-2749. doi: 10.1099/mic.0.28038-0
41. Nishiyama, Y., Aoki, Y., and Yamaguchi, H. (1995). Morphological aspects of cell wall formation during protoplast regeneration in Candida albicans. J. Electron. Microsc. (Tokyo) 44, 72-78.
42. Noble, S. M., French, S., Kohn, L. A., Chen, V., and Johnson, A. D. (2010). Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42, 590-598. doi: 10.1038/ng.605
43. Pardo, M., Monteoliva, L., Vazquez, P., Martinez, R., Molero, G., Nombela, C., et al. (2004). PST1 and ECM33 encode two yeast cell surface GPI proteins important for cell wall integrity. Microbiology 150, 4157-4170. doi: 10.1099/mic.0.26924-0
44. Park, J. I., Collinson, E. J., Grant, C. M., and Dawes, I. W. (2005). Rom2p, the Rho1 GTP/GDP exchange factor of Saccharomyces cerevisiae, can mediate stress responses via the Ras-cAMP pathway. J. Biol. Chem. 280, 2529-2535. doi: 10.1074/jbc. M407900200
45. Pericolini, E., Gabrielli, E., Amacker, M., Kasper, L., Roselletti, E., Luciano, E., et al. (2015). Secretory aspartyl proteinases cause vaginitis and can mediate vaginitis caused by Candida albicans in mice. MBio 6, 724-725. doi: 10.1128/mBio.00724-15
46. Pitarch, A., Jimenez, A., Nombela, C., and Gil, C. (2006). Decoding serological response to Candida cell wall immunome into novel diagnostic, prognostic, and therapeutic candidates for systemic candidiasis by proteomic and bioinformatic analyses. Mol. Cell. Proteom. 5, 79-96. doi: 10.1074/mcp. M500243-MCP200
47. Pollack, J. D., and Benham, R. W. (1957). The chlamydospores of Candida albicans: comparison of three media for their induction. J. Lab. Clin. Med. 50, 313-317.
48. Powers, R. W. III, Kaeberlein, M., Caldwell, S. D., Kennedy, B. K., and Fields, S. (2006). Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 20, 174-184. doi: 10.1101/gad.1381406
49. Reinke, A., Chen, J. C., Aronova, S., and Powers, T. (2006). Caffeine targets TOR complex I and provides evidence for a regulatory link between the FRB and kinase domains of Tor1p. J. Biol. Chem. 281, 31616-31626. doi: 10.1074/jbc. M603107200
50. Senn, H., Shapiro, R. S., and Cowen, L. E. (2012). Cdc28 provides a molecular link between Hsp90, morphogenesis, and cell cycle progression in Candida albicans. Mol. Biol. Cell 23, 268-283. doi: 10.1091/mbc. E11-08-0729
51. Sharon, A., Finkelstein, A., Shlezinger, N., and Hatam, I. (2009). Fungal apoptosis: function, genes and gene function. FEMS Microbiol. Rev. 33, 833-854. doi: 10.1111/j.1574-6976.2009.00180.x
52. Sorgo, A. G., Heilmann, C. J., Dekker, H. L., Bekker, M., Brul, S., De Koster, C. G., et al. (2011). Effects of fluconazole on the secretome, the wall proteome, and wall integrity of the clinical fungus Candida albicans. Eukaryot. Cell 10, 1071-1081. doi: 10.1128/EC.05011-11
53. 2 sensing to suppress hyphal morphogenesis in Candida albicans. Eukaryot. Cell 10, 502-511. doi: 10.1128/EC.00289-10
54. Su, C., Lu, Y., and Liu, H. (2013). Reduced TOR signaling sustains hyphal development in Candida albicans by lowering Hog1 basal activity. Mol. Biol. Cell 24, 385-397. doi: 10.1091/mbc. E12-06-0477
55. Torres, J., Di Como, C. J., Herrero, E., and De La Torre-Ruiz, M. A. (2002). Regulation of the cell integrity pathway by rapamycin-sensitive TOR function in budding yeast. J. Biol. Chem. 277, 43495-43504. doi: 10.1074/jbc. M205408200
56. Vialas, V., Perumal, P., Gutierrez, D., Ximenez-Embun, P., Nombela, C., Gil, C., et al. (2012). Cell surface shaving of Candida albicans biofilms, hyphae, and yeast form cells. Proteomics 12, 2331-2339. doi: 10.1002/pmic.201100588
57. Vida, T. A., and Emr, S. D. (1995). A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779-792. doi: 10.1083/jcb.128.5.779
58. Wei, M., Fabrizio, P., Hu, J., Ge, H., Cheng, C., Li, L., et al. (2008). Life span extension by calorie restriction depends on Rim15 and transcription factors downstream of Ras/PKA, Tor, and Sch9. PLoS Genet. 4:e13. doi: 10.1371/journal.pgen.0040013
59. Wullschleger, S., Loewith, R., and Hall, M. N. (2006). TOR signaling in growth and metabolism. Cell 124, 471-484. doi: 10.1016/j.cell.2006.01.016
60. Yan, J., Du, T., Zhao, W., Hartmann, T., Lu, H., Lu, Y., et al. (2013). Transcriptome and biochemical analysis reveals that suppression of GPI-anchor synthesis leads to autophagy and possible necroptosis in Aspergillus fumigatus. PLoS ONE 8:e59013. doi: 10.1371/journal.pone.0059013