1887

Abstract

produces and accumulates large amounts of the polyols -arabitol and glycerol in culture, and/or in infected mammalian tissues. However, the effects of environmental stresses on production and accumulation of these polyols, and the means by which polyol production and accumulation are regulated have not been studied. grown in glucose at 30 °C (i) produced maximal amounts of glycerol within 6 h, (ii) produced maximal amounts of -arabitol and ribitol within 12 h, and (iii) released most of these polyols into the extracellular environment. responded to osmotic and citric acid stress by producing and accumulating more glycerol, and to temperature and oxidative stresses by producing more -arabitol. The increase in intracellular glycerol was proportional to extracellular osmolarity, suggesting that glycerol functions as an osmolyte. The MAP kinase Hog1p is required for wild-type glycerol production in several fungal species subjected to osmotic stress, but it is not known if Hog1p plays a role in regulating -arabitol production. Therefore, two null mutants were constructed and tested for the ability to produce glycerol and -arabitol in response to environmental stresses. The ability to grow and produce glycerol when exposed to osmotic or citric acid stresses, and to produce -arabitol when exposed to oxidative stress, was partially dependent on Hog1p, but the ability to produce -arabitol when exposed to temperature stress was Hog1p independent. These results imply that multiple pathways regulate glycerol and -arabitol synthesis in .

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2005-09-01
2024-03-28
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References

  1. Albertyn J., Hohmann S., Thevelein J. M., Prior B. A. 1994; GPD1 , which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae , and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14:4135–4144
    [Google Scholar]
  2. Alonso-Monge R., Navarro-Garcia F., Molero G., Diez-Orejas R., Gustin M., Pla J., Sanchez M., Nombela C. 1999; Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans . J Bacteriol 181:3058–3068
    [Google Scholar]
  3. Alonso-Monge R., Negredo A. I., Eisman B., Nombela C., Pla J, Navarro-García F., Roman E. 2003; The Hog1 MAP kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans . Eukaryot Cell 2:351–361 [CrossRef]
    [Google Scholar]
  4. Ansell R., Granath K., Hohmann S., Thevelein J. M., Adler L. 1997; The two isoenzymes for yeast NAD+-dependent glycerol-3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaption and redox regulation. EMBO J 16:2179–2187 [CrossRef]
    [Google Scholar]
  5. Banuett F. 1998; Signalling in the yeasts: an informational cascade with links to the filamentous fungi. Microbiol Mol Biol Rev 62:249–274
    [Google Scholar]
  6. Bernard E. M., Christiansen L. J., Tsang S. F., Kiehn T. E., Armstrong D. 1981; Rate of arabinitol production by pathogenic yeast species. J Clin Microbiol 14:189–194
    [Google Scholar]
  7. Bernard E. M., Wong B., Armstrong D. 1985; Stereoisomeric configuration of arabinitol in serum, urine, and tissues in invasive candidiasis. J Infect Dis 151:711–715 [CrossRef]
    [Google Scholar]
  8. Bilsland E., Molin C., Swaminathan S., Ramne A., Sunnerhagen P. 2004; Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol Microbiol 53:1743–1756 [CrossRef]
    [Google Scholar]
  9. Brewster J. L., Dwyer N. D., Winter E., Gustin M. C, de Valoir T. 1993; An osmosensing signal transduction pathway in yeast. Science 259:1760–1763 [CrossRef]
    [Google Scholar]
  10. Brown A. D. 1978; Compatible solutes and extreme water stress in eukaryotic micro-organisms. Adv Microb Physiol 17:181–242
    [Google Scholar]
  11. Calderone R. A. 2002; Introduction and historical perspectives. In Candida and Candidiasiss pp 3–13 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  12. Chaturvedi V., Flynn T., Niehaus W. G., Wong B. 1996a; Stress tolerance and pathogenesis potential of a mannitol mutant of Cryptococcus neoformans . Microbiology 142:937–943 [CrossRef]
    [Google Scholar]
  13. Chaturvedi V., Wong B., Newman S. L. 1996b; Oxidative killing of Cryptococcus neoformans by human neutrophils. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediates. J Immunol 156:3836–3840
    [Google Scholar]
  14. Davis D., Ibrahim A. S, Edwards J. E. Jr, Mitchell A. P. 2000; Candida albicans RIM101 pH response pathway is required for host-pathogen interactions. Infect Immun 68:5953–5959 [CrossRef]
    [Google Scholar]
  15. de Jong J. C., McCormack B. J., Smirnoff N., Talbot N. J. 1997; Glycerol generates turgor in rice blast. Nature 389:244–245 [CrossRef]
    [Google Scholar]
  16. Dixon K. P., Xu J. R., Smirnoff N., Talbot N. J. 1999; Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea . Plant Cell 11:2045–2058 [CrossRef]
    [Google Scholar]
  17. Edgley M., Brown A. D. 1983; Yeast water relations: physiological changes induced by solute stress in Saccharomyces cerevisiae and Saccharomyces rouxii . J Gen Microbiol 129:3453–3463
    [Google Scholar]
  18. Enjalbert B., Nantel A., Whiteway M. 2003; Stress-induced gene expression in Candida albicans : absence of a general stress response. Mol Biol Cell 14:1460–1467 [CrossRef]
    [Google Scholar]
  19. Fan J., Whiteway M., Shen S. H. 2005; Disruption of a gene encoding glycerol 3-phosphatase from Candida albicans impairs intracellular glycerol accumulation-mediated salt-tolerance. FEMS Microbiol Lett 245:107–116 [CrossRef]
    [Google Scholar]
  20. Fonzi W. A., Irwin M. Y. 1993; Isogenic strain construction and gene mapping in Candida albicans . Genetics 134:717–728
    [Google Scholar]
  21. Gillum A. M., Tsay E. Y., Kirsch D. R. 1984; Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura 3 and E. coli pyrF mutations. Mol Gen Genet 198:179–182 [CrossRef]
    [Google Scholar]
  22. Gustin M. C., Albertyn J., Alexander M., Davenport K. 1998; MAP kinase pathways in the yeast Saccharomyces cerevisiae . Microbiol Mol Biol Rev 62:1264–1300
    [Google Scholar]
  23. Haghnazari E., Heyer W.-D. 2004; The Hog1 MAP kinase pathway and the Mec1 DNA damage checkpoint pathway independently control the cellular responses to hydrogen peroxide. DNA Repair 3:769–776 [CrossRef]
    [Google Scholar]
  24. Herskowitz I. 1995; MAP kinase pathways in yeast: for mating and more. Cell 80:187–197 [CrossRef]
    [Google Scholar]
  25. Hohmann S. 2002; Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66:300–372 [CrossRef]
    [Google Scholar]
  26. Jennings D. B., Ehrenshaft M., Pharr D. M., Williamson J. D. 1998; Roles for mannitol and mannitol dehydrogenases in active oxygen-mediated plant defense. Proc Natl Acad Sci U S A 95:15129–15133 [CrossRef]
    [Google Scholar]
  27. Kayingo G., Kilian S. G., Prior B. A. 2001; Conservation and release of osmolytes by yeasts during hypo-osmotic stress. Arch Microbiol 177:29–55 [CrossRef]
    [Google Scholar]
  28. Kiehn T. E., Bernard M., Gold J. W. M., Armstrong D. 1979; Candidiasis detection by gas-liquid chromatography of d-arabinitol, a fungal metabolite in human serum. Science 206:577–580 [CrossRef]
    [Google Scholar]
  29. Lawrence C. L., Botting C. H., Antrobus R., Coote P. J. 2004; Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol Cell Biol 24:3307–3323 [CrossRef]
    [Google Scholar]
  30. Lee L. K., Buckley H. R., Campbell C. C. 1975; An amino acid liquid synthetic medium for the development of mycelial and yeast form of Candida albicans . Sabouraudia 13:148–153 [CrossRef]
    [Google Scholar]
  31. Minard K. I., McAlister-Henn L. 2001; Antioxidant function of cytosolic sources of NADPH in yeast. Free Radic Biol Med 31:832–843 [CrossRef]
    [Google Scholar]
  32. Norbeck J., Blomberg A., Adler L, Påhlman A.-K., Akhtar N. 1996; Purification and characterization of two isoenzymes of dl-glycerol-3-phosphatase from Saccharomyces cerevisiae . Identification of the corresponding GPP1 and GPP2 genes and evidence for osmotic regulation of Gpp2p expression by the osmosensing mitogen-activated protein kinase signal transduction pathway. J Biol Chem 271:13875–13881 [CrossRef]
    [Google Scholar]
  33. O'Rourke S. M., Herskowitz I. 2004; Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis. Mol Biol Cell 15:532–532
    [Google Scholar]
  34. Pfaller M. A., Jones R. N., Doern G. V., Sader H. S., Hollis R. J., Messer S. A. for The SENTRY Participant Group 1998; International surveillance of bloodstream infections due to Candida species: frequency of occurrence and antifungal susceptibilities of isolates collected in 1997 in the United States, Canada, and South America for the SENTRY Program. J Clin Microbiol 36:1886–1889
    [Google Scholar]
  35. Posas F., Chamabers J. R., Heyman J. A., Hoeffler J. P., Arino J, de Nadal E. 2000; The transcriptional response of yeast to saline stress. J Biol Chem 275:17249–17255 [CrossRef]
    [Google Scholar]
  36. Rep M., Krantz M., Thevelein J. M., Hohmann S. 2000; The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J Biol Chem 275:8290–8300 [CrossRef]
    [Google Scholar]
  37. San José C., Alonso R., Pérez-Díaz R. M., Pla J., Nombela C. 1996; The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans . J Bacteriol 178:5850–5852
    [Google Scholar]
  38. Smith D. A., Nicholls S., Morgan B. A., Brown A. J. P., Quinn J. 2004; A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans . Mol Biol Cell 15:4179–4190 [CrossRef]
    [Google Scholar]
  39. Van Eck J. H., Prior B. A., Brandt E. V. 1989; Accumulation of polyhydroxy alcohols by Hansenula anomala in response to water stress. J Gen Microbiol 135:1047–1054
    [Google Scholar]
  40. Wilson R. B., Davis D., Mitchell A. P. 1999; Rapid hypothesis testing in Candida albicans through gene disruption with short homology regions. J Bacteriol 181:1868–1874
    [Google Scholar]
  41. Wilson R. B., Davis D., Enloe B. M., Mitchell A. P. 2000; A recyclable Candida albicans URA3 cassette for PCR product-directed gene disruptions. Yeast 16:65–70 [CrossRef]
    [Google Scholar]
  42. Winkler A., Arkind C., Mattison C. P., Burkholder A., Knoche K., Ota I. 2002; Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phosphatases are essentail under heat stress. Eukaryot Cell 1:163–173 [CrossRef]
    [Google Scholar]
  43. Wong B., Bernard E. M., Gold J. W., Fong D., Armstrong D. 1982; The arabinitol appearance rate in laboratory animals and humans: estimation from the arabinitol/creatinine ratio and relevance to the diagnosis of candidiasis. J Infect Dis 146:353–359 [CrossRef]
    [Google Scholar]
  44. Wong B., Murray J. S., Castellanos M., Croen K. D. 1993; d-arabitol metabolism in Candida albicans : studies of the biosynthetic pathway and the gene that encodes NAD-dependent d-arabitol dehydrogenase. J Bacteriol 175:6314–6320
    [Google Scholar]
  45. Wong B., Leeson S., Grindle S., Magee B., Brooks E., Magee P. T. 1995; d-arabitol metabolism in Candida albicans : construction and analysis of mutants lacking d-arabitol dehydrogenase. J Bacteriol 177:2971–2976
    [Google Scholar]
  46. Yancey P. H., Clark M. E., Hand S. C., Bowlus R. D., Somero G. N. 1982; Living with water stress: evolution of osmolyte systems. Science 217:1214–1222 [CrossRef]
    [Google Scholar]
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