1887

Abstract

The cellular response to the oxidative stress caused by hydrogen peroxide and its putative correlation with the stress protector trehalose was investigated in CAI.4 and the / double mutant, which is deficient in trehalose synthesis. When exponential wild-type blastoconidia were exposed to high concentrations of hydrogen peroxide, they displayed a high cell survival, accompanied by a marked rise of intracellular trehalose. The latter is due to a moderate activation of trehalose synthase and the concomitant inactivation of neutral trehalase. Identical challenge in the / double mutant severely reduced cell viability, a phenotype which was suppressed by overexpression of the gene. Pretreatment of growing cultures from both strains with either a low, non-lethal concentration of HO (05 mM) or a preincubation at 37 °C, induced an adaptive response that protected cells from being killed by a subsequent exposure to oxidative stress. During these mild oxidative preincubations, trehalose was not induced in CAI.4 cells and remained undetectable in their / counterpart. Blastoconidia from the two strains exhibited a similar degree of cell protection during the adaptive response. The induction of trehalose accumulation by HO was not due to an increased expression of mRNA. These results are consistent with a mainly protective role of trehalose in during direct oxidative stress but not during acquired oxidative tolerance.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-8-2599
2002-08-01
2019-12-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/8/1482599a.html?itemId=/content/journal/micro/10.1099/00221287-148-8-2599&mimeType=html&fmt=ahah

References

  1. Argüelles, J. C. ( 1997; ). Thermotolerance and trehalose accumulation induced by heat shock in yeast cells of Candida albicans. FEMS Microbiol Lett 146, 65-71.[CrossRef]
    [Google Scholar]
  2. Argüelles, J. C. ( 2000; ). Physiological roles of trehalose in bacteria and yeast: a comparative analysis. Arch Microbiol 174, 217-224.[CrossRef]
    [Google Scholar]
  3. Argüelles, J. C., Rodrı́guez, T. & Alvarez-Peral, F. J. ( 1999; ). Trehalose hydrolysis is not required for human serum-induced dimorphic transition in Candida albicans: evidence from a tps1/tps1 mutant deficient in trehalose synthesis. Res Microbiol 150, 521-529.[CrossRef]
    [Google Scholar]
  4. Berlett, B. S. & Stadtman, E. R. ( 1997; ). Protein oxidation in aging, disease and oxidative stress. J Biol Chem 272, 20313-20316.[CrossRef]
    [Google Scholar]
  5. Blázquez, M. A., Stucka, R., Feldmann, H. & Gancedo, C. ( 1994; ). Trehalose-6-P synthase is dispensable for growth on glucose but not for spore germination in Schizosaccharomyces pombe. J Bacteriol 176, 3895-3902.
    [Google Scholar]
  6. Brewster, J. L., de Valoir, T., Dwyer, N. D. & Gustin, M. C. ( 1993; ). An osmosensing transduction pathway in yeast. Science 259, 1760-1763.[CrossRef]
    [Google Scholar]
  7. Brown, A. J. P. & Gow, N. A. R. ( 1999; ). Regulatory networks controlling Candida albicans morphogenesis. Trends Microbiol 7, 333-338.[CrossRef]
    [Google Scholar]
  8. Coleman, D. C., Bennett, D. J., Sullivan, P. J., Gallagher, M. C., Henman, D. B., Shanley, D. & Russell, R. J. ( 1993; ). Oral Candida in HIV infection and AIDS: new perspectives and new approaches. Crit Rev Microbiol 19, 61-82.[CrossRef]
    [Google Scholar]
  9. Cutler, J. E. ( 1991; ). Putative virulence factors of Candida albicans. Annu Rev Microbiol 45, 187-218.[CrossRef]
    [Google Scholar]
  10. Elliot, B., Haltiwanger, R. S. & Fuchter, B. ( 1996; ). Synergy between trehalose and hsp104 for thermotolerance in Saccharomyces cerevisiae. Genetics 144, 923-933.
    [Google Scholar]
  11. Ernst, J. F. ( 2000; ). Transcription factors in Candida albicans – environmental control of morphogenesis. Microbiology 146, 1763-1774.
    [Google Scholar]
  12. Estruch, F. ( 2000; ). Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24, 469-486.[CrossRef]
    [Google Scholar]
  13. Fonzi, W. A. & Irwin, M. Y. ( 1993; ). Isogenic strain construction and gene mapping in Candida albicans. Genetics 134, 717-728.
    [Google Scholar]
  14. Hottiger, T., Schmutz, P. & Wiemken, A. ( 1987; ). Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J Bacteriol 169, 5518-5522.
    [Google Scholar]
  15. Jamieson, D. J. ( 1998; ). Oxidative stress responses of yeast Saccharomyces cerevisiae. Yeast 14, 1511-1527.[CrossRef]
    [Google Scholar]
  16. Jamieson, D. J., Stephen, D. W. S. & Terriere, E. C. ( 1996; ). Analysis of the adaptive oxidative stress response of Candida albicans. FEMS Microbiol Lett 138, 83-88.[CrossRef]
    [Google Scholar]
  17. Kurtz, M. B., Cortelyou, M. W. & Kirsch, D. R. ( 1986; ). Integrative transformation of Candida albicans using a cloned Candida ADE2 gene. Mol Cell Biol 6, 142-149.
    [Google Scholar]
  18. Lewis, J. G., Learmonth, R. P. & Watson, K. ( 1995; ). Induction of heat, freezing and salt tolerance by heat and salt shock in Saccharomyces cerevisiae. Microbiology 141, 687-694.[CrossRef]
    [Google Scholar]
  19. Lewis, J. G., Learmonth, R. P., Attfield, P. V. & Watson, K. ( 1997; ). Stress co-tolerance and trehalose content in baking strains of Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 18, 30-36.[CrossRef]
    [Google Scholar]
  20. Lo, H. J., Köhler, J. R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A. & Fink, G. R. ( 1997; ). Nonfilamentous Candida albicans mutants are avirulent. Cell 90, 939-949.[CrossRef]
    [Google Scholar]
  21. Mager, W. H. & Moradas-Ferreira, P. ( 1993; ). Stress response of yeast. Biochem J 290, 1-13.
    [Google Scholar]
  22. Molero, G., Dı́ez-Orejas, R., Navarro, F., Monteoliva, L., Pla, J., Gil, C., Sanchez-Perez, M. & Nombela, C. ( 1998; ). Candida albicans: genetics, dimorphism and pathogenicity. Int Microbiol 1, 95-106.
    [Google Scholar]
  23. Murphy, J. W. ( 1991; ). Mechanisms of natural resistance to human pathogenic fungi. Annu Rev Microbiol 45, 509-538.[CrossRef]
    [Google Scholar]
  24. Nwaka, S. & Holzer, H. ( 1998; ). Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Prog Nucleic Acids Res Mol Biol 58, 199-224.
    [Google Scholar]
  25. Nwaka, S., Kopp, M. & Holzer, H. ( 1995; ). Expression and function of the trehalase genes NTH1 and YBR106 in Saccharomyces cerevisiae. J Biol Chem 270, 10193-10198.[CrossRef]
    [Google Scholar]
  26. Odds, F. C. (1988). Candida and Candidiosis, a Review and Bibliography. London: Baillière Tindall.
  27. Odds, F. C. ( 1994; ). Candida species and virulence. ASM News 60, 313-318.
    [Google Scholar]
  28. Plá, J., Pérez-Dı́az, M., Navarro-Garcı́a, F., Sánchez, M. & Nombela, C. ( 1995; ). Cloning of Candida albicans HIS1 gene by direct homologous complementation of a histidine auxotroph using an improved double-ARS shuttle vector. Gene 165, 115-120.[CrossRef]
    [Google Scholar]
  29. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  30. Shepherd, M. G., Poulter, R. M. & Sullivan, P. A. ( 1985; ). Candida albicans: biology, genetics and pathogenicity. Annu Rev Microbiol 39, 579-614.[CrossRef]
    [Google Scholar]
  31. Shimokawa, O. & Nakayama, H. ( 1992; ). Increased sensitivity of Candida albicans cells accumulating 14 alpha-methylated sterols to active oxygen: possible relevance to in vivo efficacies of azole antifungal agents. Antimicrob Agents Chemother 36, 1626-1629.[CrossRef]
    [Google Scholar]
  32. Singer, M. A. & Lindquist, S. ( 1998; ). Multiple effects of trehalose on protein folding in vivo and in vitro. Mol Cell 1, 639-648.[CrossRef]
    [Google Scholar]
  33. Storz, G., Christman, M. F., Sies, H. & Ames, B. N. ( 1987; ). Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. Proc Natl Acad Sci USA 84, 8917-8921.[CrossRef]
    [Google Scholar]
  34. Thevelein, J. M. ( 1996; ). Regulation of trehalose metabolism and its relevance to cell growth and function. In The Mycota , pp. 395-414. Edited by R. Brambl & G. A. Marzluf. Heidelberg:Springer.
  35. Werner-Washburne, M., Braun, E., Johnston, G. C. & Singer, R. A. ( 1993; ). Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev 57, 383-401.
    [Google Scholar]
  36. Wiemken, A. ( 1990; ). Trehalose in yeast, stress protectant rather than reserve carbohydrate. Antonie Leeuwenhoek 58, 209-217.[CrossRef]
    [Google Scholar]
  37. Zähringer, H., Burgert, M., Holzer, H. & Nwaka, S. ( 1997; ). Neutral trehalase Nth1p of Saccharomyces cerevisiae encoded by the NTH1 gene is a multiple stress responsive protein. FEBS Lett 412, 615-620.[CrossRef]
    [Google Scholar]
  38. Zähringer, H., Thevelein, J. M. & Nwaka, S. ( 2000; ). Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: variations of PKA effect during stress and growth. Mol Microbiol 35, 397-406.[CrossRef]
    [Google Scholar]
  39. Zaragoza, O., Blázquez, M. A. & Gancedo, C. ( 1998; ). Disruption of the Candida albicans TPS1 gene encoding trehalose-6P-synthase impairs formation of hyphae and decreases infectivity. J Bacteriol 180, 3809-3815.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-8-2599
Loading
/content/journal/micro/10.1099/00221287-148-8-2599
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error