Trehalose-mediated thermal stabilization of glucose oxidase from Aspergillus niger

Journal of Biotechnology

Volumn 141, Issue 3-4, 2009, Pages 130-136

  Paz Alfaro, Karina J ^a   Ruiz Granados, Yadira G ^b   Uribe Carvajal, Salvador ^b   Sampedro, José G ^a  

^a UNIVERSIDAD AUTÓNOMA DEL ESTADO DE HIDALGO   (Mexico)

^b INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

FAD dissociation; Fluorescence; Glucose oxidase; Thermal inactivation; Trehalose

Indexed keywords

ASPERGILLUS NIGER; COFACTOR; FAD DISSOCIATION; FOLDED STATE; HYDROPHOBIC REGIONS; INTRINSIC FLUORESCENCES; KINETICS ANALYSIS; MULTIPLE APPLICATIONS; RED SHIFTS; STABILIZING EFFECTS; STRUCTURAL CHANGES; THERMAL INACTIVATION; THERMAL STABILIZATIONS; TREHALOSE;

ASTROPHYSICS; DISSOCIATION; DOPPLER EFFECT; ENZYME KINETICS; ENZYMES; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; GLUCOSE; GLUCOSE SENSORS; POLYSACCHARIDES; RATE CONSTANTS;

GLUCOSE OXIDASE;

FLAVINE ADENINE NUCLEOTIDE; GLUCOSE OXIDASE; TREHALOSE;

ARTICLE; ASPERGILLUS NIGER; DISSOCIATION; ENZYME INACTIVATION; ENZYME KINETICS; ENZYME METABOLISM; ENZYME STABILITY; ENZYME STRUCTURE; HALF LIFE TIME; HYDROPHOBICITY; MICHAELIS CONSTANT; PRIORITY JOURNAL; SPECTROFLUOROMETRY; STRUCTURE ANALYSIS; THERMOSTABILITY; TRANSITION TEMPERATURE;

ASPERGILLUS NIGER; ENZYME STABILITY; FLAVIN-ADENINE DINUCLEOTIDE; GLUCOSE OXIDASE; KINETICS; PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; TEMPERATURE; TREHALOSE;

ASPERGILLUS NIGER;

EID: 67349271674     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2009.03.002     Document Type: Article

References (44)

1. Ahmad A., Akhtar M.S., and Bhakuni V. Monovalent cation-induced conformational change in glucose oxidase leading to stabilization of the enzyme. Biochemistry 40 (2001) 1945-1955
2. Akhtar M.S., Ahmad A., and Bhakuni V. Divalent cation induced changes in structural properties of the dimeric enzyme glucose oxidase: dual effect of dimer stabilization and dissociation with loss of cooperative interactions in enzyme monomer. Biochemistry 41 (2002) 7142-7149
3. Auton M., Bolen D.W., and Rösgen J. Structural thermodynamics of protein preferential solvation: osmolyte solvation of proteins, aminoacids, and peptides. Proteins 73 (2008) 802-813
4. Benaroudj N., Lee D.H., and Goldberg A.L. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276 (2001) 24261-24267
5. Betancor L., López-Gallego F., Hidalgo A., Alonso-Morales N., Dellamora-Ortiz G., Guisán J.M., and Fernández-Lafuente R. Preparation of a very stable immobilized biocatalyst of glucose oxidase from Aspergillus niger. J. Biotech. 121 (2006) 284-289
6. Bourdillon C., Lortie R., and Laval J.M. Gluconic acid production by an immobilized glucose oxidase reactor with electrochemical regeneration of an artificial electron acceptor. Biotechnol. Bioeng. 31 (1988) 553-558
7. Chen L.Y., Ferreira J.A.B., Costa S.M.B., Cabrita G.J.M., Otzen D.E., and Melo E.P. Compaction of ribosomal protein S6 by sucrose occurs only under native conditions. Biochemistry 45 (2006) 2189-2199
8. 2+ pump. Eur. J. Biochem. 221 (1994) 1103-1110
9. Cordone L., Cottone G., Giuffrida S., Palazzo G., Venturoli G., and Viappiani C. Internal dynamics and protein-matrix coupling in trehalose-coated proteins. Biochim. Biophys. Acta 1749 (2005) 252-281
10. Dashnau J.L., Zelent B., and Vanderkooi J.M. Tryptophan interactions with glycerol/water and trehalose/sucrose cryosolvents: infrared and fluorescence spectroscopy and ab initio calculations. Biophys. Chem. 114 (2005) 71-83
11. Dumoulin M., Ueno H., Hayashi R., and Balny C. Contribution of the carbohydrate moiety to conformational stability of the carboxypeptidase Y. High pressure study. Eur. J. Biochem. 262 (1999) 475-483
12. Frederick K.R., Tung J., Emerick M.S., Masiarz F.R., Chamberlain S.H., Vasavada A., and Rosenberg S. Glucose oxidase from Aspergillus niger. Cloning, gene sequencing, secretion from Saccharomyces cerevisiae and kinetic analysis of a yeast-derived enzyme. J. Biol. Chem. 265 (1990) 3793-3802
13. Gouda M.D., Singh S.A., Rao A.G.A., Thakur M.S., and Karanth N.G. Thermal inactivation of glucose oxidase mechanism and stabilization using additives. J. Biol. Chem. 278 (2003) 24324-24333
14. Gulla K.C., Gouda M.D., Thakur M.S., and Karanth N.G. Enhancement of stability of immobilized glucose oxidase by modification of free thiols generated by reducing disulfide bonds and using additives. Biosens. Bioelectron. 19 (2004) 621-625
15. Haouz A., Glandières J.M., and Alpert B. Involvement of protein dynamics in enzyme stability the case of glucose oxidase. FEBS Lett. 506 (2001) 216-220
16. Henley J.P., and Sadana A. Deactivation theory. Biotechnol. Bioeng. 73 (1986) 1277-1285
17. 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 (1994) 187-193
18. Iyer P.V., and Ananthanarayan L. Enzyme stability and stabilization-aqueous and non-aqueous environment. Process Biochem. 43 (2008) 1019-1032
19. Jaenicke R. Stability and stabilization of globular proteins in solution. J. Biotechnol. 79 (2000) 193-203
20. Jain N.K., and Roy I. Effect of trehalose on protein structure. Protein Sci. 18 (2008) 24-36
21. Johnson J.L., London R.E., and Rajagopalan K.V. Covalently bound phosphate residues in bovine milk xanthine oxidase and in glucose oxidase from Aspergillus niger. Proc. Natl. Acad. Sci. USA 86 (1989) 6493-6497
22. Kalish H.M., Hech H.J., Schomburg D., and Schmid R.D. Effect of carbohydrate depletion on the structure, stability and activity of glucose oxidase from Aspergillus niger. Biochim. Biophys. Acta 1080 (1991) 138-142
23. Lowry O.H., Nira J.N., Rosebrough J., Farr A.L., and Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
24. Moschou E.A., Sharma B.V., Deo S.K., and Daunert S. Fluorescence glucose detection: advances toward the ideal in vivo biosensor. J. Fluoresc. 14 (2007) 537-547
25. Nakamura S., and Koga K. Alteration of thermal stability of glucose oxidase associated with the redox states. Biochem. Biophys. Res. Comm. 78 (1976) 806-810
26. Pace C.N., Treviño S., Prabhakaran E., and Scholtz J.M. Protein structure, stability and solubility in water and other solvents. Phil. Trans. R. Soc. Lond. B Biol. Sci. 359 (2004) 1225-1235
27. Pradeep L., and Udgaonkar J.B. Diffusional barrier in the unfolding of a small protein. J. Mol. Biol. 366 (2007) 1016-1028
28. Rao V.B., Sastri N.V.S., and Rao P.V.S. Thermal stabilization of glucose oxidase and glucoamylase by physical entrapment. Biochem. J. 193 (1981) 389-394
29. Rauf S., Ihsan A., Akhtar K., Ghauri M.A., Rahman M., Anwar M.A., and Khalid A.M. Glucose oxidase immobilization on a novel cellulose acetate-polymethylmethacrylate membrane. J. Biotechnol. 121 (2006) 351-360
30. Ruan K., Tian S., Lange R., and Balny C. Pressure effects on tryptophan and its derivatives. Biochem. Biophys. Res. Comm. 269 (2000) 681-686
31. Rubio-Retama J., Sánchez-Paniagua López M., Hervás Péreza J.P., Frutos Cabanillas G., López-Cabarcos E., and López-Ruiz B. Biosensors based on acrylic microgels: a comparative study of immobilized glucose oxidase and tyrosinase. Biosens. Bioelectron. 20 (2005) 2268-2275
32. +-ATPase from Kluyveromyces lactis. Protection by trehalose. Biochim. Biophys. Acta 1544 (2001) 64-73
33. +-ATPase from Kluyveromyces lactis. Biochemistry 46 (2007) 5616-5622
34. Sampedro J.G., and Uribe S. Trehalose-enzyme interactions result in structure stabilization and activity inhibition. The role of viscosity. Mol. Cell. Biochem. 256/257 (2004) 319-327
35. Seymour S.L., and Klinman J.P. Comparison of rates and kinetic isotope effects using PEGmodified variants and glicoforms of glucose oxidase: the relationship of modification of the protein envelope to C-H activation and tunneling. Biochemistry 41 (2002) 8747-8758
36. Shimizu S., and Smith D.J. Preferential hydration and the exclusion of cosolvents from protein surfaces. J. Chem. Phys. 121 (2004) 1148-1154
37. Singer M.A., and Lindquist S. Thermotolerance in Saccharomyces cerevisiae: the yin and yang of trehalose. Trends Biotechnol. 16 (1998) 460-468
38. Swodoba B.E.P., and Macey V. Purification and properties of glucose oxidase from Aspergillus niger. J. Biol. Chem. 240 (1965) 2209-2215
39. Teramoto N., Sachinvala N.D., and Shibata N. Trehalose and trehalose-based polymers for environmentally benign, biocompatible and bioactive materials. Molecules 13 (2008) 1773-1816
40. Tzanov T., Costa S.A., Gübitz G.M., and Cavaco-Paulo A. Hydrogen peroxide generation with immobilized glucose oxidase for textile bleaching. J. Biotechnol. 93 (2002) 87-94
41. Wang S., Yoshimoto M., Fukunaga K., and Nakao K. Optimal covalent immobilization of glucose oxidase-containing liposomes for highly stable biocatalyst bioreactor. Biotechnol. Bioeng. 84 (2003) 444-453
42. Wong C.M., Wong K.H., and Chen X.D. Glucose oxidase: natural occurrence, function, properties and industrial applications. Appl. Microbiol. Biotechnol. 78 (2008) 927-938
43. Zoldák G., Zubrik A., Musatov A., Stupák M., and Sedlák E. Irreversible thermal denaturation of glucose oxidase from Aspergillus niger is the transition to the denatured state with residual structure. J. Biol. Chem. 279 (2004) 47601-47609
44. Zhu Z., Momeu C., Zakhartsev M., and Schwaneberg U. Making glucose oxidase fit for biofuel cell applications by directed protein evolution. Biosens. Bioelectron. 21 (2006) 2046-2051