The mechanism of inactivation of glucose oxidase from Penicillium amagasakiense under ambient storage conditions

Enzyme and Microbial Technology

Volumn 49, Issue 1, 2011, Pages 79-87

  Caves, Michael S ^a   Derham, Barry K ^b   Jezek, Jan ^b   Freedman, Robert B ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b Arecor Limited   (United Kingdom)

Author keywords

Aggregation; Denaturation; Glucose oxidase (GOx); Inactivation; Molten globule; Stability

Indexed keywords

AGGREGATION; AMBIENT STORAGE; ASPERGILLUS NIGER; COFACTORS; FLUORIMETRY; INACTIVATION; MOLTEN GLOBULE; NIGER; SALT EFFECT; SECONDARY STRUCTURES; SOLUBLE AGGREGATES; SPECIFIC ACTIVITY; TERTIARY STRUCTURES;

ASPERGILLUS; CIRCULAR DICHROISM SPECTROSCOPY; DICHROISM; GLUCOSE; GLUCOSE SENSORS; INDUSTRIAL APPLICATIONS; SIZE EXCLUSION CHROMATOGRAPHY; SODIUM CHLORIDE;

GLUCOSE OXIDASE;

GLUCOSE OXIDASE;

ARTICLE; CIRCULAR DICHROISM; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME DENATURATION; ENZYME INACTIVATION; ENZYME STABILITY; ENZYME SUBUNIT; FLUORESCENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; PENICILLIUM; PENICILLIUM AMAGASAKIENSE; PH; PROTEIN SECONDARY STRUCTURE; SPECTROSCOPY;

ASPERGILLUS NIGER; ENZYME STABILITY; FLAVIN-ADENINE DINUCLEOTIDE; FUNGAL PROTEINS; GLUCOSE OXIDASE; KINETICS; OSMOLAR CONCENTRATION; PENICILLIUM; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

ASPERGILLUS NIGER; PENICILLIUM AMAGASAKIENSE;

EID: 79957542417     PISSN: 01410229     EISSN: 18790909     Source Type: Journal    
DOI: 10.1016/j.enzmictec.2011.03.004     Document Type: Article

References (41)

1. Turner A., Pickup J. Diabetes mellitus: biosensors for research and management. Biosensors 1985, 1:85-115.
2. Babu V., Kumar M., Karanth N., Thakur M. Stabilization of immobilized glucose oxidase against thermal inactivation by silanization for biosensor applications. Biosens Bioelectron 2004, 19:1337-1341.
3. Gouda M., Kumar M., Thakur M., Karanth N. Enhancement of operational stability of an enzyme biosensor for glucose and sucrose using protein based stabilizing agents. Biosens Bioelectron 2002, 17:503-507.
4. Gulla K., Gouda M., Thakur M., Karanth N. Enhancement of stability of immobilized glucose oxidase by modification of free thiols generated by reducing disulfide bonds and using additives. Biosens Bioelectron 2004, 19:621-625.
5. Li J., Du Y., Boullanger L., Jiang L. The folding and enzymatic activity of glucose oxidase in the glycolipid matrixes of different charges. Thin Solid Films 1999, 352:213-217.
6. Liu S.-N., Yin Y.-J., Cai C.-X. Immobilization and characterization of glucose oxidase on single-walled carbon nanotubes and its application to sensing glucose. Chin J Chem 2007, 25:439-447.
7. Rodriguez-Nogales J. Kinetic behaviour and stability of glucose oxidase entrapped in liposomes. J Chem Technol Biotechnol 2004, 79:72-78.
8. Vikartovska A., Bucko M., Mislovicova D., Patoprsty V., Lacik I., Gemeiner P. Improvement of the stability of glucose oxidase via encapsulation in sodium alginate-cellulose sulphate-poly(methylene-co-guanidine) capsules. Enzyme Microb Technol 2007, 41:748-755.
9. Yoshimoto M., Sato M., Wang S., Fukunaga K., Nakao K. Structural stability of glucose oxidase encapsulated in liposomes to inhibition by hydrogen peroxide produced during glucose oxidation. Biochem Eng J 2006, 30:158-163.
10. Hatzinikolaou D., Hansen O., Macris B., Tingey A., Kekos D., Goodenough P., et al. A new glucose oxidase from Aspergillus niger: characterization and regulation studies of enzyme and gene. Appl Microbiol Biotechnol 1996, 46:371-381.
11. O'Malley J., Weaver J. Subunit structure of glucose oxidase from Aspergillus niger. Biochemistry 1972, 11:3527-3532.
12. Kiess M., Hecht H., Kalisz H. Glucose oxidase from Penicillium amagasakiense. Primary structure and comparison with other glucose-methanol-choline (GMC) oxidoreductases. Eur J Biochem 1998, 252:90-99.
13. Chi Q., Zhang J., Dong S., Wang E. Direct observation of native and unfolded glucose oxidase structures by scanning tunnelling microscopy. J Chem Soc, Faraday Trans 1994, 90:2057-2060.
14. Hecht H., Schomburg D., Kalisz H., Schmid R. The 3D structure of glucose oxidase from Aspergillus niger. Implications for the use of GOD as a biosensor enzyme. Biosens Bioelectron 1993, 8:197-203.
15. Swoboda B., Massey V. Purification and properties of the glucose oxidase from Aspergillus niger. J Biol Chem 1965, 240:2209-2215.
16. Tsuge H., Suzuki M., Kito N., Nakanishi Y., Ohashi K., Aoki K. Inactivation of glucose oxidase by the cationic detergent, hexadecyltrimethylammonium bromide. Agric Biol Chem 1984, 48:19-28.
17. Ye W., Combes D. The relationship between the glucose oxidase subunit structure and its thermostability. Biochim Biophys Acta 1989, 999:86-93.
18. Gouda M., Singh S., Rao A., Thakur M., Karanth N. Thermal inactivation of glucose oxidase. Mechanism and stabilization using additives. J Biol Chem 2003, 278:24324-24333.
19. Zoldák G., Zubrik A., Musatov A., Stupák M., Sedlák E. Irreversible thermal denaturation of glucose oxidase from Aspergillus niger is the transition to the denatured state with residual structure. J Biol Chem 2004, 279:47601-47609.
20. Eremin A., Metelitsa D., Shishko Z., Mikhailova R., Yasenko M., Lobanok A. Thermal stability of glucose oxidase from Penicillium adametzii. Appl Biochem Microbiol 2001, 37:578-586.
21. Wohlfahrt G., Witt S., Hendle J., Schomburg D., Kalisz H., Hecht H. 1.8 and 1.9Å resolution structures of the Penicillium amagasakiense and Aspergillus niger glucose oxidases as a basis for modelling substrate complexes. Acta Crystallogr Sect D: Biol Crystallogr 1999, 55:969-977.
22. Hayashi S., Nakamura S. Comparison of fungal glucose oxidases. Chemical, physicochemical and immunological studies. Biochim Biophys Acta 1976, 438:37-48.
23. Sisak C., Csanadi Z., Ronay E., Szajani B. Elimination of glucose in egg white using immobilized glucose oxidase. Enzyme Microb Technol 2006, 39:1002-1007.
24. Godjevargova T., Dayal R., Turmanova S. Gluconic acid production in bioreactor with immobilized glucose oxidase plus catalase on polymer membrane adjacent to anion-exchange membrane. Macromol Biosci 2004, 4:950-956.
25. Thorn R., Greenman J., Austin A. In vitro method to assess the antimicrobial activity and potential efficacy of novel types of wound dressings. J Appl Microbiol 2005, 99:895-901.
26. Pickup J., Shaw G., Claremont D. In vivo molecular sensing in diabetes mellitus: an implantable glucose sensor with direct electron transfer. Diabetologia 1989, 32:213-217.
27. Pickup J., Hussain F., Evans N., Sachedina N. In vivo glucose monitoring: the clinical reality and the promise. Biosens Bioelectron 2005, 20:1897-1902.
28. Whitmore L., Wallace B. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 2004, 32:W668-W673.
29. Hennessey J.J., Johnson W.J. Information content in the circular dichroism of proteins. Biochemistry 1981, 20:1085-1094.
30. Lees J., Miles A., Wien F., Wallace B. A reference database for circular dichroism spectroscopy covering fold and secondary structure space. Bioinformatics 2006, 22:1955-1962.
31. Kelly S., Jess T., Price N. How to study proteins by circular dichroism. Biochim Biophys Acta 2005, 1751:119-139.
32. Zhong D., Zewail A. Femtosecond dynamics of flavoproteins: charge separation and recombination in riboflavine (vitamin B2)-binding protein and in glucose oxidase enzyme. Proc Natl Acad Sci USA 2001, 98:11867-11872.
33. Stryer L. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of non-polar binding sites. J Mol Biol 1965, 13:482-495.
34. Dolgikh D., Gilmanshin R., Brazhnikov E., Bychkova V., Semisotnov G., Venyaminov S.Yu., et al. Alpha-Lactalbumin: compact state with fluctuating tertiary structure?. FEBS Lett 1981, 136:311-315.
35. Hayashi S., Nakamura S. Multiple forms of glucose oxidase with different carbohydrate compositions. Biochim Biophys Acta 1981, 657:40-51.
36. Pace C. Conformational stability of globular proteins. Trends Biochem Sci 1990, 15:14-17.
37. Hecht H., Kalisz H., Hendle J., Schmid R., Schomburg D. Crystal structure of glucose oxidase from Aspergillus niger refined at 2.3Å resolution. J Mol Biol 1993, 229:153-172.
38. Yoshimura T., Isemura T. Subunit structure of glucose oxidase from Penicillium amagasakiense. J Biochem 1971, 69:839-846.
39. Ahmad A., Akhtar M., Bhakuni V. Monovalent cation-induced conformational change in glucose oxidase leading to stabilization of the enzyme. Biochemistry 2001, 40:1945-1955.
40. Dominy B., Perl D., Schmid F., Brooks C.r. The effects of ionic strength on protein stability: the cold shock protein family. J Mol Biol 2002, 319:541-554.
41. Bolen D., Baskakov I. The osmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol 2001, 310:955-963.