Trehalose-Mediated Protection of the Plasma Membrane H+-ATPase from Kluyveromyces lactis during Freeze-Drying and Rehydration

Cryobiology

Volumn 37, Issue 2, 1998, Pages 131-138

  Sampedro, José G ^a   Guerra, Guadalupe ^a   Pardo, Juan Pablo ^b   Uribe, Salvador ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Carbohydrates; Freeze drying; H+ atpase; Protein stabilization; Trehalose

Indexed keywords

KLUYVEROMYCES LACTIS;

CRYOPROTECTIVE AGENT; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; TREHALOSE;

ARTICLE; CELL MEMBRANE; DOSE RESPONSE; ENZYME ACTIVATION; FREEZE DRYING; KLUYVEROMYCES;

CELL MEMBRANE; CRYOPROTECTIVE AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; FREEZE DRYING; KLUYVEROMYCES; PROTON-TRANSLOCATING ATPASES; TREHALOSE;

EID: 0032161053     PISSN: 00112240     EISSN: None     Source Type: Journal    
DOI: 10.1006/cryo.1998.2109     Document Type: Article

References (36)

1. + translocating ATPase from the yeast Schizosaccharomyces pombe. J. Biol. Chem. 257, 4723-4730 (1982).
2. Argall, M. E., and Smith, G. D. The use of trehalose-stabilized lyophilized methanol dehydrogenase from Hyphomicrobium X for the detection of methanol. Biochem. Mol. Biol. Intl. 30, 491-497 (1993).
3. Belton, P. S., and Gil, A. M. IR and Raman spectroscopic studies of the interaction of trehalose with hen egg white lysozyme. Biopolymers 34, 957-961 (1994).
4. Bowman, B. J., and Slayman, C. W. The effects of vanadate on the plasma membrane ATPase of Neurospora crassa. J. Biol. Chem. 254, 2928-2934 (1979).
5. Butler, S. L., and Falke, J. J. Effects of protein stabilizing agents on thermal backbone motions: A disulfide trapping study. Biochemistry 35, 10595-10600 (1996).
6. Carpenter, J. F., and Crowe, J. H. An infrared spectroscopic study of the interactions of carbohydrates with dried proteins. Biochemistry 28, 3916-3922 (1989).
7. Carpenter, J. F., Crowe, L. M., and Crowe, J. H. Stabilization of phosphofructokinase with sugars during freeze-drying: Characterization of enhanced protection in the presence of divalent cations. Biochim. Biophys. Acta 923, 109-115 (1987).
8. Carpenter, J. F., Prestrelski, S. J., and Arakawa, T. Separation of freeze- and drying-induced denaturation of lyophilized proteins using stress-specific stabilization. Arch. Biochem. Biophys. 303, 456-464. (1993).
9. Colaco, C., Sen, S., Thangavelu, M., Pinder, S., and Roser, B. Extraordinary stability of enzymes dried in trehalose: Simplified molecular biology. Biotechnology 10, 1007-1011 (1992).
10. Crowe, J. H., Crowe L. M., and Jackson, S. Preservation of structural and functional activity in lyophilized sarcoplasmic reticulum. Arch. Biochem. Biophys. 220, 477-484 (1983).
11. Crowe, J. H., Crowe, L. M., Carpenter, J. F., and Aurell Wikstrom, C. Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J. 242, 1-10 (1987).
12. Crowe, J. H., Spargo, B. J., and Crowe, L. M. Preservation of dry liposomes does not require retention of residual water. Proc. Natl. Acad. Sci. USA 84, 1537-1540 (1987).
13. Crowe, L. M., Mouradian, R., Crowe, J. H., Jackson, S. A., and Womersley, C. Effects of carbohydrates on membrane stability at low water activities. Biochim. Biophys. Acta 769, 141-150 (1984).
14. Cyrklaff, M., Auer, M, Kuhlbrandt, W., and Scarborough, G. A. 2-D structure of the Neurospora crassa plasma membrane ATPase as determined by electron microscopy. EMBO J. 14, 1854-1857 (1995).
15. Fiske, C. H., and Subbarow, Y. The colorimetric determination of phosphorus. J. Biol. Chem. 66, 375-400 (1925).
16. Gadd, G. M., Chalmers, K., and Reed, R. H. The role of trehalose in dehydration resistance of Saccharomyces cerevisiae. FEMS Microbiol. Lett. 48, 249-254 (1987).
17. Goormaghtigh, E., Chadwick, C., and Scarborough, G. A. Monomers of the Neurospora plasma membrane proton ATPase catalyze efficient proton translocation. J. Biol. Chem. 261, 7466-7471 (1986).
18. +-ATPase from Kluyveromyces lactis to sulfhydryl reagents. Arch. Biochem. Biophys. 321, 101-107 (1995).
19. Hottiger, T., Boller, T., and Wiemken, A. Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEMS Lett. 220, 113-115 (1987).
20. Hottiger, T., De Virgilio, C., Hall, M. N., Boller, T., and Wiemken, A. The role of trehalose synthesis for the acquisition of thermotolerance in yeast II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro. Eur. J. Biochem. 219, 187-193 (1994).
21. Hottiger, T., Schmutz, P., and Wiemken, A. Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J. Bacteriol. 169, 5518-5522 (1987).
22. Leslie, S. B., Teter, S. A., Crowe, L. M., and Crowe, J. H. Trehalose lowers membrane phase transitions in dry yeast cells. Biochim. Biophys. Acta 1192, 7-13 (1994).
23. Lin, Y., and Timasheff, S. N. On the role of surface tension in the stabilization of globular proteins. Protein Sci. 5, 372-381 (1996).
24. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275 (1951).
25. + uptake. J. Bacteriol. 177, 2360-2367 (1995).
26. Mouradian, R., Womersley, C., Crowe, L. M., and Crowe, J. H. Preservation of functional integrity during long term storage of a biological membrane. Biochim. Biophys. Acta 778, 615-617 (1984).
27. Peña, A., Uribe, S., Clemente, S. M., and Sánchez, N. Rehydration temperature is critical for metabolic competence and for membrane integrity in active dry yeast (ADY). Arch. Microbiol. 158, 75-80 (1992).
28. Prestrelski, S. J., Tedeschi, N., Arakawa, T., and Carpenter, J. F. Dehydration induced conformational transitions in proteins and their inhibition by stabilizers. Biophys J. 65, 661-671 (1993).
29. Sola-Penna, M., Ferreira-Pereira, A., Lemos, A., and Meyer-Fernandez, J. R. Carbohydrate protection of enzyme structure and function against guanidinium chloride treatment depends on the nature of carbohydrate and enzyme. Eur. J. Biochem. 248, 24-29 (1997).
30. Sola-Penna, M., and Meyer-Fernandez, J. R. Protective role of trehalose in thermal denaturation of yeast pyrophosphatase. Z. Naturforsch. 49c, 327-330 (1994).
31. Sola-Penna, M., and Meyer-Fernandez, J. R. Trehalose protects yeast pyrophosphatase against structural and functional damage induced by guanidinium chloride. Z. Naturforsch. 51c, 160-164 (1996).
32. Sun, W. Q., Leopold, A. C., Crowe, L. M., and Crowe, J. H. Stability of dry liposomes in sugar glasses. Biophys J. 70, 1769-1776 (1996).
33. Takahashi, H., Ohmae, H., and Hatta, I. Trehalose-induced destabilization of interdigitated gel phase in dihexadecylphosphatidylcholine. Biophys. J. 73, 3030-3038 (1997).
34. Uritani, M., Takai, M., and Yoshinaga, K. Protective effect of disaccharides on restriction endonucleases during drying under vacuum. J. Biochem. 117, 774-779 (1995).
35. +-ATPase by dicyclohexylcarbodiimide: binding stoichiometry and effect of nucleophiles. Arch. Biochem. Biophys. 346, 294-302 (1997).
36. Wiemken, A. Trehalose in yeast, stress protectant rather than reserve carbohydrate. Antonie Van Leeuwenhoek. 58, 209-217 (1990).