The superoxide dismutases of Candida glabrata protect against oxidative damage and are required for lysine biosynthesis, DNA integrity and chronological life survival

Microbiology (United Kingdom)

Volumn 161, Issue 2, 2015, Pages 300-310

  Briones Martin Del Campo, Marcela ^a   Orta Zavalza, Emmanuel ^a   Cañas Villamar, Israel ^a   Gutiérrez Escobedo, Guadalupe ^a   Juárez Cepeda, Jacqueline ^a   Robledo Márquez, Karina ^a   Arroyo Helguera, Omar ^a,b   Castaño, Irene ^a   De Las Peñas, Alejandro ^a  

^a INSTITUTO POTOSINO DE INVESTIGACIÓN CIENTÍFICA Y TECNOLÓGICA   (Mexico)

^b UNIVERSIDAD VERACRUZANA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; DNA; LYSINE; MANGANESE SUPEROXIDE DISMUTASE; FUNGAL DNA; FUNGAL PROTEIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUXOTROPHY; CANDIDA GLABRATA; CARBON SOURCE; CELLULAR DISTRIBUTION; CHRONOLOGY; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; ENZYME ACTIVITY; FEMALE; FUNGAL CELL; FUNGAL GENOME; FUNGUS GROWTH; LIFESPAN; METABOLISM; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SEQUENCE HOMOLOGY; SPONTANEOUS MUTATION; SURVIVAL; SYNTENY; BIOSYNTHESIS; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIAL VIABILITY;

CANDIDA GLABRATA;

CANDIDA GLABRATA; DNA, FUNGAL; FUNGAL PROTEINS; LYSINE; MICROBIAL VIABILITY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 85052411615     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.000006     Document Type: Article

References (65)

1. Atanasova, R., Angoulvant, A., Tefit, M., Gay, F., Guitard, J., Mazier, D., Fairhead, C. & Hennequin, C. (2013). A mouse model for Candida glabrata hematogenous disseminated infection starting from the gut: evaluation of strains with different adhesion properties. PLoS ONE 8, e69664.
2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (editors) (2000). Current Protocols in Molecular Biology. New York: John Wiley.
3. Beauchamp, C. & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44, 276-287.
4. Biliński, T., Krawiec, Z., Liczmański, A. & Litwińska, J. (1985). Is hydroxyl radical generated by the Fenton reaction in vivo? Biochem Biophys Res Commun 130, 533-539.
5. Boeke, J. D., LaCroute, F. & Fink, G. R. (1984). A positive selection for mutants lacking orotidine-59-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 197, 345-346.
6. Bonatto, D. (2007). A systems biology analysis of protein-protein interactions between yeast superoxide dismutases and DNA repair pathways. Free Radic Biol Med 43, 557-567.
7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
8. Branzei, D. & Foiani, M. (2007). Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst) 6, 994-1003.
9. Castano, I., Kaur, R., Pan, S., Cregg, R., Penas, A. L., Guo, N., Biery, M. C., Craig, N. L. & Cormack, B. P. (2003). Tn7-based genome-wide random insertional mutagenesis of Candida glabrata. Genome Res 13, 905-915.
10. Claros, M. G. & Vincens, P. (1996). Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241, 779-786.
11. Cormack, B. P., Ghori, N. & Falkow, S. (1999). An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285, 578-582.
12. Cué llar-Cruz, M., Briones-Martin-del-Campo, M., Cañas-Villamar, I., Montalvo-Arredondo, J., Riego-Ruiz, L., Castaño, I. & De Las Peñas, A. (2008). High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot Cell 7, 814-825.
13. Cué llar-Cruz, M., Castaño, I., Arroyo-Helguera, O. & De Las Peñas, A. (2009). Oxidative stress response to menadione and cumene hydroperoxide in the opportunistic fungal pathogen Candida glabrata. Mem Inst Oswaldo Cruz 104, 649-654.
14. David, S. S., O'Shea, V. L. & Kundu, S. (2007). Base-excision repair of oxidative DNA damage. Nature 447, 941-950.
15. Dukan, S. & Nyström, T. (1999). Oxidative stress defense and deterioration of growth-arrested Escherichia coli cells. J Biol Chem 274, 26027-26032.
16. Fabrizio, P. & Longo, V. D. (2003). The chronological life span of Saccharomyces cerevisiae. Aging Cell 2, 73-81.
17. Farr, S. B., D'Ari, R. & Touati, D. (1986). Oxygen-dependent mutagenesis in Escherichia coli lacking superoxide dismutase. Proc Natl Acad Sci U S A 83, 8268-8272.
18. Fazius, F., Shelest, E., Gebhardt, P. & Brock, M. (2012). The fungal aaminoadipate pathway for lysine biosynthesis requires two enzymes of the aconitase family for the isomerization of homocitrate to homoisocitrate. Mol Microbiol 86, 1508-1530.
19. Fink, R. C. & Scandalios, J. G. (2002). Molecular evolution and structure-function relationships of the superoxide dismutase gene families in angiosperms and their relationship to other eukaryotic and prokaryotic superoxide dismutases. Arch Biochem Biophys 399, 19-36.
20. Flint, D. H., Tuminello, J. F. & Emptage, M. H. (1993). The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 268, 22369-22376.
21. Fridovich, I. (1995). Superoxide radical and superoxide dismutases. Annu Rev Biochem 64, 97-112.
22. Gangloff, S. P., Marguet, D. & Lauquin, G. J. (1990). Molecular cloning of the yeast mitochondrial aconitase gene (ACO1) and evidence of a synergistic regulation of expression by glucose plus glutamate. Mol Cell Biol 10, 3551-3561.
23. Gralla, E. B. & Kosman, D. J. (1992). Molecular genetics of superoxide dismutases in yeasts and related fungi. Adv Genet 30, 251-319.
24. Gralla, E. B. & Valentine, J. S. (1991). Null mutants of Saccharomyces cerevisiae Cu, Zn superoxide dismutase: characterization and spontaneous mutation rates. J Bacteriol 173, 5918-5920.
25. Gutié rrez-Escobedo, G., Orta-Zavalza, E., Castaño, I. & De Las Peñas, A. (2013). Role of glutathione in the oxidative stress response in the fungal pathogen Candida glabrata. Curr Genet 59, 91-106.
26. Hall, B. M., Ma, C. X., Liang, P. & Singh, K. K. (2009). Fluctuation analysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 25, 1564-1565.
27. Hampsey, M. (1997). A review of phenotypes in Saccharomyces cerevisiae. Yeast 13, 1099-1133.
28. Herker, E., Jungwirth, H., Lehmann, K. A., Maldener, C., Fröhlich, K. U., Wissing, S., Büttner, S., Fehr, M., Sigrist, S. & Madeo, F. (2004). Chronological aging leads to apoptosis in yeast. J Cell Biol 164, 501-507.
29. Higgins, D. G., Thompson, J. D. & Gibson, T. J. (1996). Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266, 383-402.
30. Huang, M. E., Rio, A. G. I., Nicolas, A. & Kolodner, R. D. (2003). A genomewide screen in Saccharomyces cerevisiae for genes that suppress the accumulation of mutations. Proc Natl Acad Sci U S A 100, 11529-11534.
31. Hwang, C. S., Rhie, G. E., Oh, J. H., Huh, W. K., Yim, H. S. & Kang, S. O. (2002). Copper-and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148, 3705-3713.
32. Jacobsen, I. D., Grosse, K., Berndt, A. & Hube, B. (2011). Pathogenesis of Candida albicans infections in the alternative chorio-allantoic membrane chicken embryo model resembles systemic murine infections. PLoS ONE 6, e19741.
33. Kaur, R., Domergue, R., Zupancic, M. L. & Cormack, B. P. (2005). A yeast by any other name: Candida glabrata and its interaction with the host. Curr Opin Microbiol 8, 378-384.
34. Kaur, R., Ma, B. & 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.
35. Keppler-Ross, S., Douglas, L., Konopka, J. B. & Dean, N. (2010). Recognition of yeast by murine macrophages requires mannan but not glucan. Eukaryot Cell 9, 1776-1787.
36. Keyer, K. & Imlay, J. A. (1996). Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci U S A 93, 13635-13640.
37. Kuwayama, H., Obara, S., Morio, T., Katoh, M., Urushihara, H. & Tanaka, Y. (2002). PCR-mediated generation of a gene disruption construct without the use of DNA ligase and plasmid vectors. Nucleic Acids Res 30, e2.
38. Kwon, E. S., Jeong, J. H. & Roe, J. H. (2006). Inactivation of homocitrate synthase causes lysine auxotrophy in copper/zinccontaining superoxide dismutase-deficient yeast Schizosaccharomyces pombe. J Biol Chem 281, 1345-1351.
39. Lang, G. I. & Murray, A. W. (2008). Estimating the per-base-pair mutation rate in the yeast Saccharomyces cerevisiae. Genetics 178, 67-82.
40. Langford, P. R., Sansone, A., Valenti, P., Battistoni, A. & Kroll, J. S. (2002). Bacterial superoxide dismutase and virulence. Methods Enzymol 349, 155-166.
41. Li, Y., Huang, T. T., Carlson, E. J., Melov, S., Ursell, P. C., Olson, J. L., Noble, L. J., Yoshimura, M. P., Berger, C. & other authors (1995). Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11, 376-381.
42. Liochev, S. I. & Fridovich, I. (1999). Superoxide and iron: partners in crime. IUBMB Life 48, 157-161.
43. Longo, V. D., Gralla, E. B. & Valentine, J. S. (1996). Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 271, 12275-12280.
44. Longo, V. D., Liou, L. L., Valentine, J. S. & Gralla, E. B. (1999). Mitochondrial superoxide decreases yeast survival in stationary phase. Arch Biochem Biophys 365, 131-142.
45. Miller, R. A. & Britigan, B. E. (1997). Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 10, 1-18.
46. Murakami, C. J., Burtner, C. R., Kennedy, B. K. & Kaeberlein, M. (2008). A method for high-throughput quantitative analysis of yeast chronological life span. J Gerontol A Biol Sci Med Sci 63, 113-121.
47. Mutoh, N., Nakagawa, C. W. & Yamada, K. (2002). Characterization of Cu, Zn-superoxide dismutase-deficient mutant of fission yeast Schizosaccharomyces pombe. Curr Genet 41, 82-88.
48. Narasipura, S. D., Ault, J. G., Behr, M. J., Chaturvedi, V. & Chaturvedi, S. (2003). Characterization of Cu, Zn superoxide dismutase (SOD1) gene knock-out mutant of Cryptococcus neoformans var. gattii: role in biology and virulence. Mol Microbiol 47, 1681-1694.
49. Narasipura, S. D., Chaturvedi, V. & Chaturvedi, S. (2005). Characterization of Cryptococcus neoformans variety gattii SOD2 reveals distinct roles of the two superoxide dismutases in fungal biology and virulence. Mol Microbiol 55, 1782-1800.
50. Orta-Zavalza, E., Guerrero-Serrano, G., Gutié rrez-Escobedo, G., Cañas-Villamar, I., Juárez-Cepeda, J., Castaño, I. & De Las Peñas, A. (2013). Local silencing controls the oxidative stress response and the multidrug resistance in Candida glabrata. Mol Microbiol 88, 1135-1148.
51. Pfaller, M. A. & Diekema, D. J. (2007). Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20, 133-163.
52. Rasmussen, A. K., Chatterjee, A., Rasmussen, L. J. & Singh, K. K. (2003). Mitochondria-mediated nuclear mutator phenotype in Saccharomyces cerevisiae. Nucleic Acids Res 31, 3909-3917.
53. Roetzer, A., Klopf, E., Gratz, N., Marcet-Houben, M., Hiller, E., Rupp, S., Gabaldón, T., Kovarik, P. & Schüller, C. (2011). Regulation of Candida glabrata oxidative stress resistance is adapted to host environment. FEBS Lett 585, 319-327.
54. Seider, K., Brunke, S., Schild, L., Jablonowski, N., Wilson, D., Majer, O., Barz, D., Haas, A., Kuchler, K. & other authors (2011). The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J Immunol 187, 3072-3086.
55. Sherman, F., Fink, G. R. & Hicks, J. B. (1986). Methods in Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
56. Slupphaug, G., Kavli, B. & Krokan, H. E. (2003). The interacting pathways for prevention and repair of oxidative DNA damage. Mutat Res 531, 231-251.
57. Smith, M. W. & Doolittle, R. F. (1992). A comparison of evolutionary rates of the two major kinds of superoxide dismutase. J Mol Evol 34, 175-184.
58. Srinivasan, C., Liba, A., Imlay, J. A., Valentine, J. S. & Gralla, E. B. (2000). Yeast lacking superoxide dismutase(s) show elevated levels of "free iron" as measured by whole cell electron paramagnetic resonance. J Biol Chem 275, 29187-29192.
59. Sturtz, L. A., Diekert, K., Jensen, L. T., Lill, R. & Culotta, V. C. (2001). A fraction of yeast Cu, Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J Biol Chem 276, 38084-38089.
60. Toyn, J. H., Gunyuzlu, P. L., White, W. H., Thompson, L. A. & Hollis, G. F. (2000). A counterselection for the tryptophan pathway in yeast: 5-fluoroanthranilic acid resistance. Yeast 16, 553-560.
61. Wallace, M. A., Liou, L. L., Martins, J., Clement, M. H., Bailey, S., Longo, V. D., Valentine, J. S. & Gralla, E. B. (2004). Superoxide inhibits 4Fe-4S cluster enzymes involved in amino acid biosynthesis. Cross-compartment protection by CuZn-superoxide dismutase. J Biol Chem 279, 32055-32062.
62. Weisiger, R. A. & Fridovich, I. (1973). Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 248, 4793-4796.
63. Xiao, W., Chow, B. L. & Rathgeber, L. (1996). The repair of DNA methylation damage in Saccharomyces cerevisiae. Curr Genet 30, 461-468.
64. Youseff, B. H., Holbrook, E. D., Smolnycki, K. A. & Rappleye, C. A. (2012). Extracellular superoxide dismutase protects Histoplasma yeast cells from host-derived oxidative stress. PLoS Pathog 8, e1002713.
65. Zordan, R. E., Ren, Y., Pan, S. J., Rotondo, G., De Las Peñas, A., Iluore, J. & Cormack, B. P. (2013). Expression plasmids for use in Candida glabrata. G3 (Bethesda) 3, 1675-1686.