Interrelationships of glycosylation and aggregation kinetics for Peniophora lycii phytase

Biochemistry

Volumn 45, Issue 15, 2006, Pages 5057-5066

  Høiberg Nielsen, Rasmus ^a   Fuglsang, Claus C ^b   Arleth, Lise ^c,d   Westh, Peter ^a  

^a ROSKILDE UNIVERSITY   (Denmark)

^b NOVOZYMES A S   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; CALORIMETRY; ENZYME KINETICS; ENZYMES; HYDRATION; IONIC STRENGTH; LIGHT SCATTERING; PH; PROTEINS; SCANNING; THERMODYNAMIC STABILITY;

AGGREGATION KINETICS; DEGLYCOSYLATED FORM (DGPHY); GLYCOSYLATION; PENIOPHORA LYCII PHYTASE;

GLYCOLS;

DEGLYCOSYLATED PHYTASE; FUNGAL ENZYME; GLYCAN; PHYTASE; UNCLASSIFIED DRUG;

ARTICLE; DIFFERENTIAL SCANNING CALORIMETRY; DYNAMIC LIGHT SCATTERING; ENZYME DENATURATION; ENZYME GLYCOSYLATION; ENZYME KINETICS; ENZYME STABILITY; FUNGUS; HYDRATION; IONIC STRENGTH; LIGHT SCATTERING; NONHUMAN; PENIOPHORA LYCII; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN INTERACTION; SECOND VIRIAL COEFFICIENT; STATIC LIGHT SCATTERING; STEREOSPECIFICITY; TEMPERATURE; THERMODYNAMICS;

6-PHYTASE; BASIDIOMYCOTA; CALORIMETRY, DIFFERENTIAL SCANNING; GLYCOSYLATION; HYDROGEN-ION CONCENTRATION; KINETICS; OSMOLAR CONCENTRATION; PEPTIDES; POLYSACCHARIDES; PROTEIN FOLDING; TEMPERATURE; THERMODYNAMICS; TIME FACTORS; WATER;

FUNGI; PENIOPHORA LYCII;

EID: 33645911471     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0522955     Document Type: Article

References (62)

1. Trombetta, E. S. (2003) The contribution of N-glycans and their Processing in the Endoplasmic Reticulum to Glycoprotein Biosynthesis, Glycobiology 13, 77-91.
2. Helenius, A. (1994) How N-linked Oligosaccharides Affect Glycoprotein Folding in the Endoplasmic Reticulum, Mol. Biol. Cell 5, 253-265.
3. Paulson, J. C. (1989) Glycoprotiens: What are the sugar chains for? Trends Biochem. Sci. 14, 272-276.
4. Tams, J. W., and Welinder, K. G. (1998) Glycosylation and thermodynamic versus kinetic stability of horseradish peroxidase, FEBS Lett. 421, 234-236.
5. Tams, J. W., and Welinder, K. G. (2001) Kinetic stability of designed glycosylation mutants of Coprinus cinereus peroxidase, Biochem. Biophys. Res. Commun. 286, 701-706.
6. Kwon, K. S., and Yu, M. H. (1997) Effect of glycosylation on the stability of α1-antitrypsin toward urea denaturation and thermal deactivation, Biochim. Biophys. Acta 1335, 265-272.
7. Price, N. J., Pinheiro, C., Soares, C. M., Ashford, D. A., Ricardo, C. P., and Jackson, P. A. (2003) A biochemical and molecular characterization of LEP1, an extensin peroxidase from lupin, J. Biol. Chem. 278, 41389-41399.
8. Cruz, M. A., Handin, R. I., and Wise, R. J. (1993) The interaction of the von Willebrand factor-A1 domain with platelet glycoprotein Ib/IX. The role of glycosylation and disulfide bonding in a monomeric recombinant A1 domain protein, J. Biol. Chem. 268, 21238-21245.
9. Maruyama, N., Katsube, T., Wada, Y., Oh, M. H., Barba De La Rosa, A. P., Okuda, E., Nakagawa, S., and Utsumi, S. (1998) The roles of the N-linked glycans and extension regions of soybean β-conglycinin in folding, assembly and structural features, Eur. J. Biochem. 258, 854-862.
10. Kern, G., Schulke, N., Schmid, F. X., and Jaenicke, R. (1992) Stability, quaternary structure, and folding of internal, external, and core-glycosylated invertase from yeast, Protein Sci. 1, 120-131.
11. Schulke, N., and Schmid, F. X. (1988) Effect of glycosylation on the mechanism of renaturation of invertase from yeast, J. Biol. Chem. 263, 8832-8837.
12. Ioannou, Y. A., Zeidner, K. M., Grace, M. E., and Desnick, R. J. (1998) Human α-galactosidase A: Glycosylation site 3 is essential for enzyme solubility, Biochem. J. 332, 789-797.
13. Haki, G. D., and Rakshit, S. K. (2003) Developments in Industrially Important Thermostable Enzymes: A review, Bioresour. Technol. 89, 17-34.
14. Kendrick, B. S., Carpenter, J. F., Cleland, J. L., and Randolph, T. W. (1998) A Transient Expansion of the Native State Precedes Aggregation of Recombinant Human Interferon-γ, Proc. Natl. Acad. Sci. U.S.A. 94, 14142-14146.
15. Eijsink, V. G., Bjork, A., Gaseidnes, S., Sirevag, R., Synstad, B., van den Burg, B., and Vriend, G. (2004) Rational Engineering of Enzyme Stability, J. Biotechnol. 113, 105-120.
16. Bagger, H. L., Fuglsang, C. C., and Westh, P. (2003) Preferential binding of two compatible solutes to the glycan moieties of Peniophora lycii phytase, Biochemistry 42, 10295-10300.
17. Lei, X. G., and Stahl, C. H. (2001) Biotechnological development of effective phytases for mineral nutrition and environmental protection, Appl. Microbiol. Biotechnol. 57, 474-481.
18. Lassen, S. F., Breinholt, J., Ostergaard, P. R., Brugger, R., Bischoff, A., Wyss, M., and Fuglsang, C. C. (2001) Expression, gene cloning, and characterization of five novel phytases from four basidiomycete fungi: Peniophora lycii, Agrocybe pediades, a Ceriporia sp., and Trametes pubescens, Appl. Environ. Microbiol. 67, 4701-4707.
19. Trimble, R. B., and Tarentino, A. L. (1991) Identification of distinct endoglycosidase (endo) activities in Flavobacterium meningosepticum: endo F4, endo F2, and endo F3. Endo F1 and endo H hydrolyze only high mannose and hybrid glycans, J. Biol. Chem. 266, 1646-1651.
20. Zimm, B. H. (1948) The scattering of light and the radial distribution function of high polymer solutions, J. Chem. Phys. 16, 1093-1099.
21. Bloomfield, V. A. (2000) Static and dynamic light scattering from aggregating particles, Biopolymers 54, 168-172.
22. Webb, J. N., Webb, S. D., Cleland, J. L., Carpenter, J. F., and Randolph, T. W. (2001) Partial molar volume, surface area, and hydration changes for equilibrium unfolding and formation of aggregation transition state: High-pressure and cosolute studies on recombinant human IFN-γ, Proc. Natl. Acad. Sci. U.S.A. 98, 7259-7264.
23. Chang, S. T., Tobler, S. A., and Fernandez, E. J. (2001) Unfolding and conformational distributions during protein precipitation, Biotechnol. Prog. 17, 583-585.
24. Rochet, J. C., and Lansbury, P. T., Jr. (2000) Amyloid fibrillogenesis: Themes and variations, Curr. Opin. Struct. Biol. 10, 60-68.
25. Kim, Y. S., Cape, S. P., Chi, E., Raffen, R., Wilkins-Stevens, P., Stevens, F. J., Manning, M. C., Randolph, T. W., Solomon, A., and Carpenter, J. F. (2001) Counteracting effects of renal solutes on amyloid fibril formation by immunoglobulin light chains, J. Biol. Chem. 276, 1626-1633.
26. Chi, E. Y., Krishnan, S., Kendrick, B. S., Chang, B. S., Carpenter, J. F., and Randolph, T. W. (2003) Roles of conformational stability and colloidal stability in the aggregation of recombinant human granulocyte colony-stimulating factor, Protein Sci. 12, 903-913.
27. Lumry, R., and Eyring, H. (1954) Conformation changes of proteins, J. Phys. Chem. 58, 110-120.
28. Sanchez-Ruiz, J. M., Lopez-Lacomba, J. L., Cortijo, M., and Mateo, P. L. (1988) Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin, Biochemistry 27, 1648-1652.
29. Kreimer, D. I., Shnyrov, V. L., Villa, R. E., Silman, I., and Weiner, L. (1995) Irreversible thermal denaturation of Torpedo californica acetylcholinesterase, Protein Sci. 4, 2349-2357.
30. Lyubarev, A. E., Kurganov, B. I., Orlov, V. N., and Zhou, H. M. (1999) Two-state irreversible thermal denaturation of muscle creatine kinase, Biophys. Chem. 79, 199-204.
31. Creveld, L. D., Meijberg, W., Berendsen, H. J. C., and Pepermans, H. A. M. (2001) DSC studies of Fusarium solani pisi cutinase: Consequences for stability in the presence of surfactants, Biophys. Chem. 92, 65-75.
32. Weijers, M., Barneveld, P. A., Cohen Stuart, M. A., and Visschers, R. W. (2003) Heat-induced denaturation and aggregation of ovalbumin at neutral pH described by irreversible first-order kinetics, Protein Sci. 12, 2693-2703.
33. Gouda, M. D., Singh, S. A., Rao, A. G., Thakur, M. S., and Karanth, N. G. (2003) Thermal inactivation of glucose oxidase. Mechanism and stabilization using additives, J. Biol. Chem. 278, 24324-24333.
34. Kurganov, B. I., Rafikova, E. R., and Dobrov, E. N. (2002) Kinetics of thermal aggregation of tobacco mosaic virus coat protein, Biochemistry (Moscow) 67 (5), 525-533.
35. Kendrick, B. S., Cleland, J. L., Lam, X., Nguyen, T., Randolph, T. W., Manning, M. C., and Carpenter, J. F. (1998) Aggregation of recombinant human interferon γ: Kinetics and structural transitions, J. Pharm. Sci. 87, 1069-1076.
36. Kurganov, B. I. (2002) Kinetics of protein aggregation. Quantitative estimation of the chaperone-like activity in test-systems based on suppression of protein aggregation, Biochemistry (Moscow) 67, 409-422.
37. Wang, K., and Kurganov, B. I. (2003) Kinetics of heat- and acidification-induced aggregation of firefly luciferase, Biophys. Chem. 106, 97-109.
38. Finke, J. M., Gross, L. A., Ho, H. M., Sept, D., Zimm, B. H., and Jennings, P. A. (2000) Commitment to folded and aggregated states occurs late in interleukin-1/9 folding, Biochemistry 39, 15633-15642.
39. Duy, C., and Fitter, J. (2005) Thermostability of irreversible unfolding of α-amylases analyzed by unfolding kinetics, J. Biol. Chem. 280, 37360-37365.
40. Hinrichs, J., and Rademacher, B. (2004) High pressure thermal denaturation kinetics of whey proteins, J. Dairy Res. 71, 480-488.
41. Weijers, M., Barneveld, P. A., Stuart, M. A. C., and Visschers, R. W. (2003) Heat-induced denaturation and aggregation of ovalbumin at neutral pH described by irreversible first-order kinetics, Protein Sci. 12, 2693-2703.
42. LeBon, C., Nicolai, T., and Durand, D. (1999) Kinetics of aggregation and gelation of globular proteins after heat induced denaturation, Macromolecules 32, 6120-6127.
43. Nohara, D., Mizutani, A., and Sakai, T. (1999) Kinetic study on the thermal denaturation of hen egg-white lysozyme involving precipitation, J. Biosci. Bioeng. 87, 199-205.
44. Collins, K. D., and Washabaugh, M. W. (1985) The Hofmeister effect and the behaviour of water at interfaces, Q. Rev. Biophys. 18, 323-422.
45. Baldwin, R. L. (1996) How Hofmeister ion interactions affect protein stability, Biophys. J. 71, 2056-2063.
46. Militello, V., Casarino, C., Emanuele, A., Giostra, A., Pullara, F., and Leone, M. (2004) Aggregation kinetics of bovine serum albumin studied by FTIR spectroscopy and light scattering, Biophys. Chem. 107, 175-187.
47. Durbin, S. D., and Feher, G. (1996) Protein crystallization, Annu. Rev. Phys. Chem. 47, 171-204.
48. van Holde, K. E., Johnson, W. C., and Ho, P. S. (1998) Principles of Physical Biochemistry, Prentice Hall, Upper Saddle River, NJ.
49. Bagger, H. L., Fuglsang, C. C., and Westh, P. (2005) Hydration of a glycoprotein: Relative water affinity of peptide and glycan moieties, Eur. Biophus. J. (in press).
50. Tams, J. W., Vind, J., and Welinder, K. G. (1999) Adapting protein solubility by glycosylation. N-Glycosylation mutants of Coprinus cinereus peroxidase in salt and organic solutions, Biochim. Biophys. Acta 1432, 214-221.
51. Tams, J. W., and Welinder, K. G. (1995) Mild chemical deglycosylation of horseradish peroxidase yields a fully active, homogeneous enzyme, Anal. Biochem. 228, 48-55.
52. Mimura, Y., Church, S., Ghirlando, R., Ashton, P. R., Dong, S., Goodall, M., Lund, J., and Jefferis, R. (2000) The influence of glycosylation on the thermal stability and effector function expression of human IgG1-Fc: Properties of a series of truncated glycoforms, Mol. Immunol. 37, 697-706.
53. Wang, C., Eufemi, M., Turano, C., and Giartosio, A. (1996) Influence of the carbohydrate moiety on the stability of glycoproteins, Biochemistry 35, 7299-7307.
54. Srinivas, V. R., Singha, N. C., Schwarz, F. P., and Surolia, A. (1998) Differential scanning calorimetric studies of the glycoprotein, winged bean acidic lectin, isolated from the seeds of Psophocarpus tetrogonolobus, FEBS Lett. 425, 57-60.
55. van Zuylen, C. W., Kamerling, J. P., and Vliegenthart, J. F. (1997) Glycosylation beyond the Asn78-linked G1cNAc residue has a significant enhancing effect on the stability of the α subunit of human chorionic gonadotropin, Biochem. Biophys. Res. Commun. 232, 117-120.
56. Hashimoto, Y., Munemura, O., Masumoto, K., Ueda, T., and Imoto, T. (2001) Thermostability of Doubly Glycosylated Recombinant Lysosyme, Biol. Pharm. Bull. 24, 1102-1107.
57. Pfeil, W. (2002) The influence of glycosylation on the thermal stability of ribonuclease, Thermochim. Acta 382, 169-174.
58. Cumming, D. A., and Carver, J. P. (1987) Virtual and solution conformations of oligosaccharides, Biochemistry 26, 6664-6676.
59. Rutherford, T. J., Partridge, J., Weller, C. T., and Homans, S. W. (1993) Characterization of the extent of internal motions in oligosaccharides, Biochemistry 32, 12715-12724.
60. Lommerse, J. P., Kroon-Batenburg, L. M., Kamerling, J. P., and Vliegenthart, J. F. (1995) Conformational analysis of the xylose-containing N-glycan of pineapple stem bromelain as part of the intact glycoprotein, Biochemistry 34, 8196-8206.
61. 1H NMR ROESY and NOESY spectroscopy in combination with MD simulations, Carbohydr. Res. 337, 2279-2299.
62. Imberty, A., and Perez, S. (1995) Stereochemistry of the N-glycosylation sites in glycoproteins, Protein Eng. 8, 699-709.