N-glycosylation enhances functional and structural stability of recombinant β-glucuronidase expressed in Pichia pastoris

Journal of Biotechnology

Volumn 164, Issue 1, 2013, Pages 75-81

  Zou, Shuping ^b   Huang, Shen ^a   Kaleem, Imdad ^a   Li, Chun ^a  

^a BEIJING INSTITUTE OF TECHNOLOGY   (China)

^b ZHEJIANG UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Glucuronidase; N glycosylation; Pichia pastoris; Stability; Unfolding equilibrium

Indexed keywords

CONFORMATIONAL STABILITIES; FUNCTIONAL ENHANCEMENTS; GLUCURONIDASE; N-GLYCOSYLATION; N-GLYCOSYLATION SITES; N-LINKED CARBOHYDRATES; PICHIA PASTORIS; STRUCTURAL STABILITIES;

CHLORINE COMPOUNDS; CONVERGENCE OF NUMERICAL METHODS; ESTERIFICATION; GLYCOSYLATION; ORGANIC SOLVENTS; SOAPS (DETERGENTS); YEAST;

STABILITY;

BETA GLUCOSIDASE; CARBOHYDRATE; GUANIDINE; SOLVENT;

ARTICLE; CONTROLLED STUDY; DEGLYCOSYLATION; ENZYME GLYCOSYLATION; ENZYME STABILITY; NONHUMAN; PH; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TEMPERATURE;

BIOTECHNOLOGY; DETERGENTS; ENZYME STABILITY; FUNGAL PROTEINS; GLUCURONIDASE; GLYCOSYLATION; HYDROGEN-ION CONCENTRATION; OCTOXYNOL; PEPTIDE-N4-(N-ACETYL-BETA-GLUCOSAMINYL) ASPARAGINE AMIDASE; PICHIA; PROTEIN UNFOLDING; RECOMBINANT PROTEINS; SODIUM DODECYL SULFATE;

PICHIA PASTORIS;

EID: 84875106219     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2012.12.015     Document Type: Article

References (36)

1. Akao T. Differences in the metabolism of glycyrrhizin, glycyrrhetic acid and glycyrrhetic acid monoglucuronide by human intestinal flora. Biological and Pharmaceutical Bulletin 2000, 23:1418-1423.
2. Apweiler R., Hermjakob H., Sharon N. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. BBA - General Subjects 1999, 1473:4-8.
3. Bradford M.M. A rapid and sensitivemethod for the quantitation ofmicrogram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
4. Chilukuri N., Parikh K., Sun W., Naik R., Tipparaju P., Doctor B.R., Saxena A. Polyethylene glycosylation prolongs the circulatory stability of recombinant human butyrylcholinesterase. Chemico-Biological Interactions 2005, 157:115-121.
5. Fatima A., Husain Q. A role of glycosyl moieties in the stabilization of bitter gourd (Momordica charantia) peroxidase. International Journal of Biological Macromolecules 2007, 41:56-63.
6. Feng S.J., Li C., Xu X.L., Wang X.Y. Screening strains for directed biosynthesis of beta-d-mono-glucuronide-glycyrrhizin and kinetics of enzyme production. Journal of Molecular Catalysis B: Enzymatic 2006, 43:63-67.
7. Fujihara J., Yasuda T., Kunito T., Fujii Y., Takatsuka H., Moritani T., Takeshita H. Two N-Linked glycosylation sites (Asn18 and Asn106) are both required for full enzymatic activity, thermal stability, and resistance to proteolysis in mammalian deoxyribonuclease. I. Bioscience, Biotechnology, and Biochemistry 2008, 72:3197-3205.
8. Haga Y., Ishii K., Suzuki T. N-glycosylation is critical for the stability and intracellular trafficking of glucose transporter GLUT4. Journal of Biological Chemistry 2011, 286:31320-31327.
9. Han Y.M., Lei X.G. Role of glycosylation in the functional expression of an Aspergillus niger phytase (phyA) in Pichia pastoris. Archives of Biochemistry and Biophysics 1999, 364:83-90.
10. Hirai-Fujita Y., Yamamoto-Hino M., Kanie O., Goto S. N-glycosylation of the Drosophila neural protein Chaoptin is essential for its stability, cell surface transport and adhesive activity. FEBS Letters 2008, 582:2572-2576.
11. Jafari-Aghdam J., Khajeh K., Ranjbar B., Nemat-Gorgani M. Deglycosylation of glucoamylase from Aspergillus niger: effects on structure, activity and stability. BBA - Proteins and Proteomics 2005, 1750:61-68.
12. Kim D.H., Lee S.W., Han M.J. Biotransformation of glycyrrhizin to 18 beta-glycyrrhetinic acid-3-O-beta-d-glucuronide by Streptococcus LJ-22, a human intestinal bacterium. Biological and Pharmaceutical Bulletin 1999, 22:320-322.
13. Kuramoto T., Ito Y., Oda M., Tamura Y., Kitahata S. Microbial-production of glycyrrhetic acid 3-O-mono-beta-d-glucuronide from glycyrrhizin by Cryptococcus magnus Mg-27. Bioscience, Biotechnology, and Biochemistry 1994, 58:455-458.
14. Li J.S.S., Cu L.W., Rock D.L., Li J.Y. Novel glycosidic linkage in Aedes aegypti chorion peroxidase N-mannosyl tryptophan. Journal of Biological Chemistry 2005, 280:38513-38521.
15. Li T.G., Nana W., Heng D., Min Z. Polyethylene glycosylation prolongs the stability of recombinant human paraoxonase-1. Toxicology Letters 2012, 210:366-371.
16. Miyata T., Harakuni T., Taira T., Matsuzaki G., Arakawa T. Merozoite surface protein-1 of Plasmodium yoelii fused via an oligosaccharide moiety of cholera toxin B subunit glycoprotein expressed in yeast induced protective immunity against lethal malaria infection in mice. Vaccine 2012, 30:948-958.
17. Mizutani K., Kuramoto T., Tamura Y., Ohtake N., Doi S., Nakaura M., Tanaka O. Sweetness of glycyrrhetic acid 3-O-beta-d-monoglucuronide and the related glycosides. Bioscience, Biotechnology, and Biochemistry 1994, 58:554-555.
18. Muller-Steffner H., Kuhn I., Argentini M., Schuber F. Identification of the N-glycosylation sites on recombinant bovine CD38 expressed in Pichia pastoris: their impact on enzyme stability and catalytic activity. Protein Expression and Purification 2010, 70:151-157.
19. Nestl B.M., Nebel B.A., Hauer B. Recent progress in industrial biocatalysis. Current Opinion in Chemical Biology 2011, 15:187-193.
20. Park H.Y., Kim N.Y., Han M.J., Bae E.A., Kim D.H. Purification and characterization of two novel beta-d-glucuronidases converting glycyrrhizin to 18 beta-glycyrrhetinic acid-3-O-beta-d-glucuronide from Streptococcus LJ-22. Journal of Microbiology and Biotechnology 2005, 15:792-799.
21. Pham V.T., Ewing E., Kaplan H., Choma C., Hefford M.A. Glycation improves the thermostability of trypsin and chymotrypsin. Biotechnology and Bioengineering 2008, 101:452-459.
22. Price J.L., Shental-Bechor D., Dhar A., Turner M.J., Powers E.T., Gruebele M., Levy Y., Kelly J.W. Context-dependent effects of asparagine glycosylation on pin WW folding kinetics and thermodynamics. Journal of the American Chemical Society 2010, 132:15359-15367.
23. Qi F., Dai D.Z., Liu Y.L., Kaleem I., Li C. Effects of low-shear modeled microgravity on the characterization of recombinant beta-d-glucuronidase expressed in Pichia pastoris. Applied Biochemistry and Biotechnology 2011, 163:162-172.
24. Rudd P.M., Joao H.C., Coghill E., Fiten P., Saunders M.R., Opdenakker G., Dwek R.A. Glycoforms modify the dynamic stability and functional-activity of an enzyme. Biochemistry 1994, 33:17-22.
25. Sarkar A., Wintrode P.L. Effects of glycosylation on the stability and flexibility of a metastable protein: the human serpin alpha(1)-antitrypsin. International Journal of Mass Spectrometry 2011, 302:69-75.
26. Sheldon R.A. Cross-linked enzyme aggregates as industrial biocatalysts. Organic Process Research and Development 2011, 15:213-223.
27. Shental-Bechor D., Levy Y. Effect of glycosylation on protein folding: a dose book at thermodynamic stabilization. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:8256-8261.
28. Skropeta D. The effect of individual N-glycans on enzyme activity. Bioorganic & Medicinal Chemistry 2009, 17:2645-2653.
29. Sola R.J., Griebenow K. Effects of Glycosylation on the Stability of Protein Pharmaceuticals. Journal of Pharmaceutical Science 2009, 98:1223-1245.
30. Somera A.F., Pereira M.G., Souza Guimarães L.H., Polizeli Mde L., Terenzi H.F., Melo Furriel R.P., Jorge J.A. Effect of glycosylation on the biochemical properties of beta-xylosidases from Aspergillus versicolor. Journal of Microbiology 2009, 47:270-276.
31. Srimathi S., Jayaraman G. Effect of glycosylation on the catalytic and conformational stability of homologous alpha-amylases. The Protein Journal 2005, 24:79-88.
32. Stahl C.H., Wilson D.B., Lei X.G. Comparison of extracellular Escherichia coli AppA phytases expressed in Streptomyces lividans and Pichia pastoris. Biotechnology Letters 2003, 25:827-831.
33. Tey L.H., Loveridge E.J., Swanwick R.S., Flitsch S.L., Allemann R.K. Highly site-selective stability increases by glycosylation of dihydrofolate reductase. The FEBS Journal 2010, 277:2171-2179.
34. Waetzig G.H., Chalaris A., Rosenstiel P., Suthaus J., Holland C., Karl N., Uriarte L.V., Till A., Scheller J., Grotzinger J., Schreiber S., Rose-John S., Seegert D. N-linked glycosylation is essential for the stability but not the signaling function of the interleukin-6 signal transducer glycoprotein 130. The Journal of Biological Chemistry 2010, 285:1781-1789.
35. Yoshimasu M.A., Tanaka T., Ahn J.K., Yada R.Y. Effect of N-linked glycosylation on the aspartic proteinase porcine pepsin expressed from Pichia pastoris. Glycobiology 2004, 14:417-429.
36. Zou S.P., Xie L.P., Liu Y.L., Kaleem I., Zhang G.F., Li C. N-linked glycosylation influences on the catalytic and biochemical properties of Penicillium purpurogenum beta-d-glucuronidase. Journal of Biotechnology 2012, 157:399-404.