Engineering the pattern of protein glycosylation modulates the thermostability of a GH11 xylanase

Journal of Biological Chemistry

Volumn 288, Issue 35, 2013, Pages 25522-25534

  Fonseca Maldonado, Raquel ^a   Vieira, Davi Serradella ^a   Alponti, Juliana Sanchez ^a   Bonneil, Eric ^b   Thibault, Pierre ^b   Ward, Richard John ^a,c  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^c BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS SUBTILIS; CONCEPTUAL FRAMEWORKS; MOLECULAR BASIS; N-GLYCOSYLATION; PROTEIN GLYCOSYLATION; PROTEIN STABILITY; PROTEIN THERMOSTABILITIES; XYLANASE A;

ESTERIFICATION; GLYCOSYLATION; POLYSACCHARIDES; STABILITY;

PROTEINS;

ASPARAGINE; GLYCAN; UNCLASSIFIED DRUG; XYLAN ENDO 1,3 BETA XYLOSIDASE; XYLANASE A;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME REGULATION; ENZYME STABILITY; ESCHERICHIA COLI; GLYCOSYLATION; HETEROLOGOUS EXPRESSION; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NONHUMAN; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN MODIFICATION; RESIDUE ANALYSIS; SITE DIRECTED MUTAGENESIS; THERMOSTABILITY;

GLYCOSIDE HYDROLASES; GLYCOSYLATION; MASS SPECTROMETRY (MS); MOLECULAR DYNAMICS SIMULATION; PROTEIN DESIGN; PROTEIN ENGINEERING; PROTEIN THERMOSTABILITY;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; ENDO-1,4-BETA XYLANASES; ENZYME STABILITY; ESCHERICHIA COLI; GLYCOSYLATION; HOT TEMPERATURE; MUTAGENESIS; PICHIA; PROTEIN ENGINEERING; RECOMBINANT PROTEINS;

EID: 84883426663     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.485953     Document Type: Article

References (50)

1. Rothman, J. E., and Lodish, H. F. (1977) Synchronised transmembrane insertion and glycosylation of a nascent membrane protein. Nature 269, 775-780
2. Apweiler, R., Hermjakob, H., and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473, 4-8
3. Burda, P., and Aebi, M. (1999) The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1426, 239-257
4. Taylor, M. E., Drickamer, K. (2011) Introduction to Glycobiology, Oxford University Press, United Kingdom
5. Ohtsubo, K., and Marth, J. D. (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126, 855-867
6. Jefferis, R. (2009) Recombinant antibody therapeutics. The impact of glycosylation on mechanisms of action. Trends Pharmacol. Sci. 30, 356-362
7. Mulloy, B., and Corfield, A. P. (2010) Structural glycobiology and human health. Biochem. Soc. Trans. 38, 1329-1332
8. Hecht, M. L., Stallforth, P., Silva, D. V., Adibekian, A., and Seeberger, P. H. (2009) Recent advances in carbohydrate-based vaccines. Curr. Opin. Chem. Biol. 13, 354-359
9. Jaeken, J., and Matthijs, G. (2007) Congenital disorders of glycosylation. A rapidly expanding disease family. Annu. Rev. Genomics Hum. Genet. 8, 261-278
10. Marth, J. D., and Grewal, P. K. (2008) Mammalian glycosylation in immunity. Nat. Rev. Immunol. 8, 874-887
11. Kawasaki, N., Itoh, S., Hashii, N., Takakura, D., Qin, Y., Huang, X., and Yamaguchi, T. (2009) The significance of glycosylation analysis in development of biopharmaceuticals. Biol. Pharm. Bull. 32, 796-800
12. Molinari, M., Eriksson, K. K., Calanca, V., Galli, C., Cresswell, P., Michalak, M., and Helenius, A. (2004) Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol. Cell 13, 125-135
13. Sitia, R., and Braakman, I. (2003) Quality control in the endoplasmic reticulum protein factory. Nature 426, 891-894
14. Helenius, A., and Aebi, M. (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev. Biochem. 73, 1019-1049
15. Helenius, A., and Aebi, M. (2001) Intracellular functions of N-linked glycans. Science 291, 2364-2369
16. Wang, C., Eufemi, M., Turano, C., and Giartosio, A. (1996) Influence of the carbohydrate moiety on the stability of glycoproteins. Biochemistry 35, 7299-7307
17. Shental-Bechor, D., and Levy, Y. (2008) Effect of glycosylation on protein folding. A close look at thermodynamic stabilization. Proc. Natl. Acad. Sci. U.S.A. 105, 8256-8261
18. Straumann, N., Wind, A., Leuenberger, T., and Wallimann, T. (2006) Effects of N-linked glycosylation on the creatine transporter. Biochem. J. 393, 459-469
19. Yi, W., Clark, P. M., Mason, D. E., Keenan, M. C., Hill, C., Goddard, W. A., 3rd, Peters, E. C., Driggers, E. M., and Hsieh-Wilson, L. C. (2012) Phosphofructokinase 1 glycosylation regulates cell growth and metabolism. Science 337, 975-980
20. Wyss, D. F., Choi, J. S., Li, J., Knoppers, M. H., Willis, K. J., Arulanandam, A. R., Smolyar, A., Reinherz, E. L., and Wagner, G. (1995) Conformation and function of the N-linked glycan in the adhesion domain of human CD2. Science 269, 1273-1278
21. Sinha, S., and Surolia, A. (2007) Attributes of glycosylation in the establishment of the unfolding pathway of soybean agglutinin. Biophys. J. 92, 208-216
22. Shental-Bechor, D., and Levy, Y. (2011) Communication. Folding of glycosylated proteins under confinement. J. Chem. Phys. 135, 141104
23. Cheng, S., Edwards, S. A., Jiang, Y., and Gräter, F. (2010) Glycosylation enhances peptide hydrophobic collapse by impairing solvation. Chemphyschem. 11, 2367-2374
24. Petrescu, A. J., Wormald, M. R., and Dwek, R. A. (2006) Structural aspects of glycomes with a focus on N-glycosylation and glycoprotein folding. Curr. Opin. Struct. Biol. 16, 600-607
25. Petrescu, A. J., Petrescu, S. M., Dwek, R. A., and Wormald, M. R. (1999) A statistical analysis of N- and O-glycan linkage conformations from crystallographic data. Glycobiology 9, 343-352
26. Woods, R. J. (1998) Computational carbohydrate chemistry. What theoretical methods can tell us. Glycoconj. J. 15, 209-216
27. Yuried, E., Ramsland, P. A. (2012) Structural Glycobiology, CRC Press, Inc., Boca Raton, FL
28. von der Lieth, C., Luetteke, T., Frank, M. (2010) Bioinformatics for Glycobilogy and Glycomics: An Introduction, John Wiley&Sons, Inc., New York
29. Woods, R. J., Edge, C. J., and Dwek, R. A. (1994) Protein surface oligosaccharides and protein function. Nat. Struct. Biol. 1, 499-501
30. Lu, D., Yang, C., and Liu, Z. (2012) How hydrophobicity and the glycosylation site of glycans affect protein folding and stability. A molecular dynamics simulation. J. Phys. Chem. B 116, 390-400
31. Daly, R., and Hearn, M. T. (2005) Expression of heterologous proteins in Pichia pastoris. A useful experimental tool in protein engineering and production. J. Mol. Recognit. 18, 119-138
32. Bretthauer, R. K., and Castellino, F. J. (1999) Glycosylation of Pichia pastoris- derived proteins. Biotechnol. Appl. Biochem. 30, 193-200
33. Kukuruzinska, M. A., Bergh, M. L., and Jackson, B. J. (1987) Protein glycosylation in yeast. Annu. Rev. Biochem. 56, 915-944
34. Vieira, D. S., and Degrève, L. (2009) An insight into the thermostability of a pair of xylanases. The role of hydrogen bonds. Mol. Phys. 107, 59-69
35. Georis, J., de Lemos Esteves, F., Lamotte-Brasseur, J., Bougnet, V., Devreese, B., Giannotta, F., Granier, B., and Frère, J. M. (2000) An additional aromatic interaction improves the thermostability and thermophilicity of a mesophilic family 11 xylanase. Structural basis and molecular study. Protein Sci. 9, 466-475
36. Torrez, M., Schultehenrich, M., and Livesay, D. R. (2003) Conferring thermostability to mesophilic proteins through optimized electrostatic surfaces. Biophys. J. 85, 2845-2853
37. Ruller, R., Deliberto, L., Ferreira, T. L., and Ward, R. J. (2008) Thermostable variants of the recombinant xylanase A from Bacillus subtilis produced by directed evolution show reduced heat capacity changes. Proteins 70, 1280-1293
38. Nelson, R. M., and Long, G. L. (1989) A general method of site-specific mutagenesis using a modification of the Thermus aquaticus polymerase chain reaction. Anal. Biochem. 180, 147-151
39. Ruller, R., Rosa, J. C., Faça, V. M., Greene, L. J., and Ward, R. J. (2006) Efficient constitutive expression of Bacillus subtilis xylanase A in Escherichia coli DH5α under the control of the Bacillus BsXA promoter. Biotechnol. Appl. Biochem. 43, 9-15
40. Miller, G. L. (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31, 426-428
41. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
42. Bohne-Lang, A., and von der Lieth, C. W. (2005) GlyProt. In silico glycosylation of proteins. Nucleic Acids Res. 33, W214-W219
43. Arfken, G. (1985) The Method of Steepest Descents in Mathematical Methods for Physicists. 3rd Ed., pp. 428-436, Academic Press, Orlando, FL
44. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., Hermans, J. (1981) Interaction models for water in relation to protein hydration. in Intermolecular Forces (Pullman, B., and Reidel, D., eds) pp. 331-334, Dordrecht, The Netherlands
45. Gordon, J. C., Myers, J. B., Folta, T., Shoja, V., Heath, L. S., and Onufriev, A. (2005) H++. A server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Res. 33, W368-W371
46. Miyamo, S., Kollman, P. A. (2002) SETTLE. An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 13, 952-962
47. van Gunsteren, W. F., Berendsen, H. J. C. (1988) A leap-frog algorithm for stochastic dynamics. Mol. Simul. 1, 173-185
48. Darden, T., York, D., Pedersen, L. (1993) Particle mesh Ewald. AnN.log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
49. Hess, B., Kutzner, C., van der Spoel, D., Lindahl, E. (2008) GROMACS 4. Algorithms for highly efficient, load-balanced and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
50. van Gunsteren, W. F., Billeter, S. R., Eising, A. A., Hünenberger, P. H., Krüger, P., Mark, A. E., Scott, W. R. P., Tironi, I. G. (1996) The GROMOS96 Manual and User Guide. in Biomolecular Simulation, Biomos, Groningen, The Netherlands