A compensatory increase in trehalose synthesis in response to desiccation stress in Saccharomyces cerevisiae cells lacking the heat shock protein Hsp12p

Canadian Journal of Microbiology

Volumn 54, Issue 7, 2008, Pages 559-568

  Shamrock, Vanessa J ^a   Lindsey, George G ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Desiccation; Flow cytometry; Malondialdehyde; Plasma membrane; Propidium iodide; Reactive oxygen species; TBARS

Indexed keywords

CELL MEMBRANES; CELLS; CHROMATOGRAPHIC ANALYSIS; FLOW CYTOMETRY; MICROSCOPIC EXAMINATION; OXYGEN; QUALITY ASSURANCE; RELIABILITY;

(ABIOTIC AND BIOTIC) STRESS; APPLIED (CO); CYTOMETRY; DESICCATION STRESS; DESICCATION TOLERANCE; EXPONENTIAL PHASE; HEAT SHOCK PROTEIN (HSP); PLASMA MEMBRANE (PM); PROPIDIUM IODIDE; REACTIVE OXYGEN SPECIES (ROS); REDUCED GLUTATHIONE; SACCHAROMYCES CEREVISIAE CELLS; STATIONARY PHASE (SP); STRAIN COMPENSATED; SYNTHESIS (OF CHIRAL IONIC LIQUIDS); WILD TYPE STRAIN; WILD-TYPE (WT); WILD-TYPE (WT) CELLS;

STRAIN;

GLUTATHIONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 12P; HYDROGEN PEROXIDE; PROPIDIUM IODIDE; REACTIVE OXYGEN METABOLITE; TREHALOSE;

COMPARATIVE STUDY; COMPENSATION; CONCENTRATION (COMPOSITION); CYTOLOGY; DESICCATION; ENVIRONMENTAL STRESS; HEAT SHOCK; MEMBRANE; PROTEIN; YEAST;

ARTICLE; CARBOHYDRATE SYNTHESIS; CELL MEMBRANE; CELL PROTECTION; CONTROLLED STUDY; DESICCATION; FLOW CYTOMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; WILD TYPE;

CELL MEMBRANE; DESICCATION; HEAT-SHOCK PROTEINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TREHALOSE;

SACCHAROMYCES CEREVISIAE;

EID: 46849103406     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W08-044     Document Type: Article

References (47)

1. Attfield, P.V. 1987. Trehalose accumulates in Saccharomyces cerevisiae during exposure to agents that induce heat shock response. FEBS Lett. 225: 259-263. doi:10.1016/0014-5793(87)81170-5. PMID:2446923.
2. Benaroudj, N., Lee, D., and Goldberg, A. 2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276: 24261-24267. doi:10.1074/jbc. M101487200. PMID:11301331.
3. Berney, M., Weilenmann, H., and Egli, T. 2006. Flow-cytometric study of vital cellular functions in Escherichia coli during solar disinfection (SODIS). Microbiology (Reading, U.K.), 152: 1719-1729. doi:10.1099/mic.0.28617-0.
4. 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. doi:10.1016/0003-2697(76)90527-3. PMID:942051.
5. 2 in Saccharomyces cerevisiae. J. Biol. Chem. 279: 6501-6506. doi:10.1074/jbc.M311818200. PMID:14645222.
6. Chen, C., Dewaele, S., Braeckman, B., Desmyter, L., Verstraelen, J., Borgonie, G., et al. 2003. A high-throughput screening system for genes extending life-span. Exp. Gerontol. 38: 1051-1063. doi:10.1016/S0531- 5565(03)00186-4. PMID:14580858.
7. Cipak, A., Hasslacher, M., Tehlivets, O., Collinson, E., Zivkovic, M., Matijevic, T., et al. 2006. Saccharomyces cerevisiae strain expressing a plant fatty acid desaturase produces polyunsaturated fatty acids and is susceptible to oxidative stress induced by lipid peroxidation. Free Radic. Biol. Med. 40: 897-906. doi:10.1016/j.freeradbiomed.2005.10.039. PMID:16520241.
8. de Jesus Pereira, E., Panek, A., and Eleutherio, E. 2003. Protection against oxidation during dehydration of yeast. Cell Stress Chaperones, 8: 120-124. doi:10.1379/1466-1268(2003)008〈0120:PAODDO〉2.0.CO;2. PMID:14627197.
9. Eleutherio, E.C., de Araujo, P., and Panek, A. 1993. Role of the trehalose carrier in dehydration resistance of Saccharomyces cerevisiae. Biochim. Biophys. Acta, 1156: 263-266. PMID:8461315.
10. Espindola Ade, S., Gomes, D.S., Panek, A.D., and Eleutherio, E.C. 2003. The role of glutathione in yeast dehydration tolerance. Cryobiology, 47: 236-241. doi:10.1016/j.cryobiol.2003.10.003. PMID:14697735.
11. Garay-Arroyo, A., Colmenero-Flores, J., Garciarrubio, A., and Covarrubias, A.A. 2000. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J. Biol. Chem. 275: 5668-5674. doi:10.1074/jbc.275.8.5668. PMID:10681550.
12. Gasch, A.P., Spellman, P., Kao, C., Carmel-Harel, O., Eisen, M., Storz, G., et al. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell, 11: 4241-4257. PMID:11102521.
13. 2 stimulon in Saccharomyces cerevisiae. J. Biol. Chem. 273: 22480-22489. doi:10.1074/jbc.273.35. 22480. PMID:9712873.
14. Hayashi, M., and Maeda, T. 2006. Activation of the HOG pathway upon cold stress in Saccharomyces cerevisiae. J. Biochem. 139: 797-803. doi:10.1093/jb/mvj089. PMID:16672281.
15. Herdeiro, R.S., Pereira, M.D., Panek, A.D., and Eleutherio, E.C. 2006. Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochim. Biophys. Acta, 1760: 340-346. PMID:16510250.
16. Kandror, O., Bretschneider, N., Kreydin, E., Cavalieri, D., and Goldberg, A.L. 2004. Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependant induction of trehalose synthesis and certain molecular chaperones. Mol. Cell, 13: 771-781. doi:10.1016/S1097-2765(04)00148-0. PMID:15053871.
17. Karreman, R.J., and Lindsey, G.G. 2005. A rapid method to determine the stress status of Saccharomyces cerevisiae by monitoring the expression of a Hsp12:Green Fluorescent Protein (GFP) construct under the control of the Hsp12 promoter. J. Biomol. Screen. 10: 253-259. doi:10.1177/ 1087057104273485. PMID:15809321.
18. Karreman, R.J., and Lindsey, G.G. 2007. Modulation of Congored-induced aberrations in the yeast Saccharomyces cerevisiae by the general stress response protein Hsp12p. Can. J. Microbiol. 53: 1203-1210. doi:10.1139/W07-090. PMID:18026214.
19. Karreman, R.J., Brandt, W.F., and Lindsey, G.G. 2005. The yeast Saccharomyces cerevisiae stress response protein Hsp12p decreases the gel strength of agarose used as a model system for the b-glucan layer of the cell wall. Carbohydr. Polym. 60: 193-198. doi:10.1016/j.carbpol.2004.12.004.
20. Karreman, R.J., Dague, E., Gaboriaud, F., Quile's, F., Duval, J., and Lindsey, G.G. 2007. The stress response protein Hsp12p increases the flexibility of the yeast Saccharomyces cerevisiae cell wall. Biochim. Biophys. Acta, 1774: 131-137. PMID:17161030.
21. Kim, J., Alizadeh, P., Harding, T., Hefner-Gravink, A., and Klionsky, D. 1996. Disruption of the yeast ATH1 gene confers better survival after dehydration, freezing and ethanol shock: potential commercial applications. Appl. Environ. Microbiol. 62: 1563-1569. PMID:8633854.
22. Kitagawa, E., Akama, K., and Iwahashi, H. 2005. Effects of iodine on global gene expression in Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 69: 2285-2293. doi:10.1271/bbb.69.2285. PMID:16377885.
23. Kunst, A., Draeger, B., and Ziegenhorn, J. 1984. UV-methods with hexokinase and glucose-6-phosphate dehydrogenase. In Methods of enzyme analysis. Edited by H. Bergmeyer, J. Bergmeyer, and M. Grassl. Vol. VI. Verlag Chemie, GmbH, Weinheim, Germany. pp. 163-172.
24. Mansure, J.J., Panek, A., Crowe, L., and Crowe, J. 1994. Trehalose inhibits ethanol effects on intact yeast cells and liposomes. Biochim. Biophys. Acta, 1191: 309-316. doi:10.1016/0005-2736(94)90181-3. PMID:8172916.
25. Mavis, R.D., and Stellwagen, E. 1968. Purification and subunit structure of glutathione reductase from bakers' yeast. J. Biol. Chem. 243: 809-814. PMID:5638597.
26. Motshwene, P., Karreman, R.J., Kgari, G., Brandt, W.F., and Lindsey, G.G. 2004. LEA (late embryonic abundant)-like protein Hsp12p (heat-shock protein 12) is present in the cell wall and enhances the barotolerance of the yeast Saccharomyces cerevisiae. Biochem. J. 377: 769-774. doi:10.1042/BJ20031301. PMID:14570591.
27. Mtwisha, L., Brandt, W.F., McCready, S.A., and Lindsey, G.G. 1998. HSP 12 is a LEA-like protein in yeast (Saccharomyces cerevisiae). Plant Mol. Biol. 37: 513-521. doi:10.1023/A:1005904219201. PMID:9617818.
28. Nwaka, S., Kopp, M., Burgert, M., Deuchler, I., Kienle, I., and Holzer, H. 1994. Is thermotolerance of yeast dependent on trehalose accumulation? FEBS Lett. 344: 225-228. doi:10.1016/0014-5793(94)00385-8. PMID:8187889.
29. Park, J.I., Grant, C., Attfield, P., and Dawes, I. 1997. The freeze thaw stress response of the yeast Saccharomyces cerevisiae is growth phase specific and is controlled by the nutritional state via the RAS-cyclic AMP signal transduction pathway. Appl. Environ. Microbiol. 63: 3818-3824. PMID:9327544.
30. Parrou, J., Teste, M., and 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. Microbiology (Reading, U.K.), 142: 1891-1900.
31. Pereira, M.D., Elutherio, E.C., and Panek, A.D. 2001. Acquisition of tolerance against oxidative damage in Saccharomyces cerevisiae. BMC Microbiol. 1: 11-20. doi:10.1186/1471-2180-1-11. PMID:11483159.
32. Piper, P.W. 1995. The heat shock and ethanol stress responses of yeast exhibit extensive similarity and functional overlap. FEMS Microbiol. Lett. 134: 121-127. doi:10.1111/j.1574-6968.1995.tb07925.x. PMID:8586257.
33. Praekelt, U.M., and Meacock, P. 1990. HSP12, a new small heat shock gene of Saccharomyces cerevisiae: analysis of structure, regulation and function. Mol. Gen. Genet. 223: 97-106. doi:10.1007/BF00315801. PMID:2175390.
34. Ribeiro, M.J., Silva, J., and Panek, A. 1994. Trehalose metabolism in Saccharomyces cerevisiae during heat-shock. Biochim. Biophys. Acta, 1200: 139-147. PMID:8031833.
35. Sales, K., Brandt, W., Rumbak, E., and Lindsey, G.G. 2000. The LEA-like protein HSP12 in Saccharomyces cerevisiae has a plasma membrane location and protects membranes against desiccation and ethanol-induced lysis. Biochim. Biophys. Acta, 1463: 267-278. doi:10.1016/S0005-2736(99)00215-1. PMID:10675505.
36. Sano, F., Asakawa, N., Inoue, Y., and Sakurai, M. 1999. A dual role for intracellular trehalose in the resistance of yeast cells to water stress. Cryobiology, 39: 80-87. doi:10.1006/cryo.1999.2188. PMID:10458903.
37. Scandalios, J.G. 2002. Oxidative stress responses - What have genome-scale studies taught us? Genome Biol. 3: 1019.1-1019.6. doi:10.1186/gb-2002-3-7-reviews1019.
38. Schade, B., Jansen, G., Whiteway, M., Entian, K., and Thomas, D. 2004. Cold adaptation in budding yeast. Mol. Biol. Cell, 15: 5492-5502. doi:10.1091/mbc.E04-03-0167. PMID:15483057.
39. Sharma, S.C. 1997. A possible role of trehalose in osmotolerance and ethanol tolerance in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 152: 11-15. doi:10.1111/j.1574-6968.1997.tb10402.x. PMID:9228764.
40. Singh, J., Kumar, D., Ramakrishnan, N., Singhal, V., Jervis, J., Garst, J., et al. 2005. Transcriptional response of Saccharomyces cerevisiae to desiccation and rehydration. Appl. Environ. Microbiol. 71: 8752-8763. doi:10.1128/AEM.71.12.8752-8763.2005. PMID:16332871.
41. 2 protects Saccharomyces cerevisiae cells in stationary phase against oxidative stress. FEBS Lett. 578: 152-156. doi:10.1016/j.febslet.2004.10.090. PMID:15581633.
42. Steels, E.L., Learmonth, R.P., and Watson, K. 1994. Stress tolerance and membrane lipid unsaturation in Saccharomyces cerevisiae grown aerobically or anaerobically. Microbiology (Reading, U.K.), 140: 569-576. PMID:8012580.
43. Toledano, M., Delaunay, A., Biteau, B., Spector, D., and Azevedo, D. 2003. Oxidative stress response in yeast. In Yeast stress responses. Topics in current genetics, Vol. 1. Edited by S. Hohmann and P.W.H. Manger. Springer-Verlag, Berlin Heidelberg. pp. 241-303.
44. van Bakel, H., Strengman, E., Wijmenga, C., and Holstege, F. 2005. Gene expression profiling and phenotype analysis of S. cerevisiae in response to changing copper reveals six genes with new roles in copper and iron metabolism. Physiol. Genomics, 22: 356-367. doi:10.1152/physiolgenomics. 00055.2005. PMID:15886332.
45. Varela, J.C., Preakelt, U., Meacock, P., Planta, R., and Mager, W. 1995. The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol. Cell. Biol. 15: 6232-6245. PMID:7565776.
46. Yang, Y., Cheng, J., Singhal, S., Saini, M., Pandya, U., Awasthi, S., and Awasthi, Y. 2001. Role of glutathione S-transferase in protection against lipid peroxidation. Overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation. J. Biol. Chem. 276: 19220-19230. doi:10.1074/jbc.M100551200. PMID:11279091.
47. Zähringer, H., Burgert, M., Holzer, H., and 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. doi:10.1016/S0014-5793(97)00868-5. PMID:9276477.