1887

Abstract

Trehalose accumulation is a common response to several stresses in the yeast . This metabolite protects proteins and membrane lipids from structural damage and helps cells to maintain integrity. Based on genetic studies, degradation of trehalose has been proposed as a required mechanism for growth recovery after stress, and the neutral trehalase Nth1p as the unique degradative activity involved. Here we constructed a collection of mutants for several trehalose metabolism and transport genes and analysed their growth and trehalose mobilization profiles during experiments of saline stress recovery. The behaviour of the triple ΔΔΔ and quadruple ΔΔΔΔ mutant strains in these experiments demonstrates the participation of the three known yeast trehalases Nth1p, Nth2p and Ath1p in the mobilization of intracellular trehalose during growth recovery after saline stress, rules out the participation of the Agt1p H-disaccharide symporter, and allows us to propose the existence of additional new mechanisms for trehalose mobilization after saline stress.

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2009-09-01
2020-04-04
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References

  1. Alizadeh P., Klionsky D. J.. 1996; Purification and biochemical characterization of the ATH1 gene product, vacuolar acid trehalase, from Saccharomyces cerevisiae. FEBS Lett391:273–278
    [Google Scholar]
  2. Basu A., Bhattacharyya S., Chaudhuri P., Sengupta S., Ghosh A. K.. 2006; Extracellular trehalose utilization by Saccharomyces cerevisiae. Biochim Biophys Acta 1760;134–140
    [Google Scholar]
  3. Blomberg A.. 2000; Metabolic surprises in Saccharomyces cerevisiae during adaptation to saline conditions: questions, some answers and a model. FEMS Microbiol Lett182:1–8
    [Google Scholar]
  4. Crowe J. H., Hoekstra F. A., Crowe L. M.. 1992; Anhydrobiosis. Annu Rev Physiol54:579–599
    [Google Scholar]
  5. De Mesquita J. F., Paschoalin V. M., Panek A. D.. 1997; Modulation of trehalase activity in Saccharomyces cerevisiae by an intrinsic protein. Biochim Biophys Acta 1334;233–239
    [Google Scholar]
  6. De Mesquita J. F., Panek A. D., de Araujo P. S.. 2003; In silico and in vivo analysis reveal a novel gene in Saccharomyces cerevisiae trehalose metabolism. BMC Genomics4:45
    [Google Scholar]
  7. Destruelle M., Holzer H., Klionsky D. J.. 1995; Isolation and characterization of a novel yeast gene, ATH1, that is required for vacuolar acid trehalase activity. Yeast11:1015–1025
    [Google Scholar]
  8. Garre E., Pérez-Torrado R., Gimeno-Alcañiz J. V., Matallana E.. 2009; Acid trehalase is involved in intracellular trehalose mobilization during postdiauxic growth and severe saline stress in Saccharomyces cerevisiae. FEMS Yeast Res9:52–62
    [Google Scholar]
  9. Gietz R. D., Schiestl R. H., Willems A. R., Woods R. A.. 1995; Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast11:355–360
    [Google Scholar]
  10. González-Hernández J. C., Jiménez-Estrada M., Pena A.. 2005; Comparative analysis of trehalose production by Debaryomyces hansenii and Saccharomyces cerevisiae under saline stress. Extremophiles9:7–16
    [Google Scholar]
  11. Güldener U., Heck S., Fielder T., Beinhauer J., Hegemann J. H.. 1996; A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res24:2519–2524
    [Google Scholar]
  12. Harris S. D., Cotter D. A.. 1988; Transport of yeast vacuolar trehalase to the vacuole. Can J Microbiol34:835–838
    [Google Scholar]
  13. Hottiger T., Schmutz P., Wiemken A.. 1987; Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J Bacteriol169:5518–5522
    [Google Scholar]
  14. Huang J., Reggiori F., Klionsky D. J.. 2007; The transmembrane domain of acid trehalase mediates ubiquitin-independent multivesicular body pathway sorting. Mol Biol Cell18:2511–2524
    [Google Scholar]
  15. Jules M., Guillou V., François J., Parrou J. L.. 2004; Two distinct pathways for trehalose assimilation in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol70:2771–2778
    [Google Scholar]
  16. Jules M., Beltrán G., François J., Parrou J. L.. 2008; New insights in yeast trehalose metabolism: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals a Ath1p-dependent trehalose mobilization. Appl Environ Microbiol74:605–614
    [Google Scholar]
  17. Jung Y. J., Park H. D.. 2005; Antisense-mediated inhibition of acid trehalase ( ATH1) gene expression promotes ethanol fermentation and tolerance in Saccharomyces cerevisiae. Biotechnol Lett27:1855–1859
    [Google Scholar]
  18. Keller F., Schellenberg M., Wiemken A.. 1982; Localization of trehalase in vacuoles and of trehalose in the cytosol of yeast ( Saccharomyces cerevisiae. Arch Microbiol131:298–301
    [Google Scholar]
  19. Kim J., Alizadeh P., Harding T., Hefner-Gravink A., Klionsky D. J.. 1996; Disruption of the yeast ATH1 gene confers better survival after dehydration, freezing, and ethanol shock: potential commercial applications. Appl Environ Microbiol62:1563–1569
    [Google Scholar]
  20. Mahmud S. A., Nagahisa K., Hirasawa T., Yoshikawa K., Ashitani K., Shimizu H.. 2009; Effect of trehalose accumulation on response to saline stress in Sacccharomyces cerevisiae. Yeast26:17–30
    [Google Scholar]
  21. Malluta E. F., Decker P., Stambuk B. U.. 2000; The Kluyver effect for trehalose in Saccharomyces cerevisiae. J Basic Microbiol40:199–205
    [Google Scholar]
  22. Nwaka S., Holzer H.. 1998; Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Prog Nucleic Acid Res Mol Biol58:197–237
    [Google Scholar]
  23. Nwaka S., Mechler B., Destruelle M., Holzer H.. 1995a; Phenotypic features of trehalase mutants in Saccharomyces cerevisiae. FEBS Lett360:286–290
    [Google Scholar]
  24. Nwaka S., Kopp M., Holzer H.. 1995b; Expression and function of the trehalase genes NTH1 and YBR0106 in Saccharomyces cerevisiae. J Biol Chem270:10193–10198
    [Google Scholar]
  25. Nwaka S., Mechler B., Holzer H.. 1996; Deletion of the ATH1 gene in Saccharomyces cerevisiae prevents growth on trehalose. FEBS Lett386:235–238
    [Google Scholar]
  26. Panadero J., Pallotti C., Rodríguez-Vargas S., Randez-Gil F., Prieto J. A.. 2006; A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J Biol Chem281:4638–4645
    [Google Scholar]
  27. Parrou J. L., François J.. 1997; A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells. Anal Biochem248:186–188
    [Google Scholar]
  28. Parrou J. L., Teste M. A., François J.. 1997; Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose. Microbiology143:1891–1900
    [Google Scholar]
  29. Pedreño Y., Gimeno-Alcañiz J. V., Matallana E., Argüelles J. C.. 2002; Response to oxidative stress caused by H2O2 in Saccharomyces cerevisiae mutants deficient in trehalase genes. Arch Microbiol177:494–499
    [Google Scholar]
  30. Plourde-Owobi L., Durner S., Parrou J. L., Wieczorke R., Goma G., François J.. 1999; AGT1, encoding an alpha-glucoside transporter involved in uptake and intracellular accumulation of trehalose in Saccharomyces cerevisiae. J Bacteriol181:3830–3832
    [Google Scholar]
  31. San Miguel P. F., Argüelles J. C.. 1994; Differential changes in the activity of cytosolic and vacuolar trehalases along the growth cycle of Saccharomyces cerevisiae. Biochim Biophys Acta1200:155–160
    [Google Scholar]
  32. Sebollela A., Louzada P. R., Sola-Penna M., Sarone-Williams V., Coelho-Sampaio T., Ferreira S. T.. 2004; Inhibition of yeast glutathione reductase by trehalose: possible implications in yeast survival and recovery from stress. Int J Biochem Cell Biol36:900–908
    [Google Scholar]
  33. Singer M. A., Lindquist S.. 1998a; Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell1:639–648
    [Google Scholar]
  34. Singer M. A., Lindquist S.. 1998b; Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol16:460–468
    [Google Scholar]
  35. Van Dijck P., Colavizza D., Smet P., Thevelein J. M.. 1995; Differential importance of trehalose in stress resistance in fermenting and nonfermenting Saccharomyces cerevisiae cells. Appl Environ Microbiol61:109–115
    [Google Scholar]
  36. Wera S., De Schrijver E., Geyskens I., Nwaka S., Thevelein J. M.. 1999; Opposite roles of trehalase activity in heat-shock recovery and heat-shock survival in Saccharomyces cerevisiae. Biochem J343:621–626
    [Google Scholar]
  37. Winderickx J., de Winde J. H., Crauwels M., Hino A., Hohmann S., Van Dijck P., Thevelein J. M.. 1996; Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control?. Mol Gen Genet252:470–482
    [Google Scholar]
  38. Wolfe K. H., Lohan A. J.. 1994; Sequence around the centromere of Saccharomyces cerevisiae chromosome II: similarity of CEN2 to CEN4. Yeast10:Suppl AS41–S46
    [Google Scholar]
  39. Zahringer 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 Lett412:615–620
    [Google Scholar]
  40. Zahringer H., Holzer H., Nwaka S.. 1998; Stability of neutral trehalase during heat stress in Saccharomyces cerevisiae is dependent on the activity of the catalytic subunits of cAMP-dependent protein kinase, Tpk1 and Tpk2. Eur J Biochem255:544–551
    [Google Scholar]
  41. Zahringer 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 Microbiol35:397–406
    [Google Scholar]
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