Three-dimensional structures of thermophilic β-1,4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa: Comparison of twelve xylanases in relation to their thermal stability

European Journal of Biochemistry

Volumn 270, Issue 7, 2003, Pages 1399-1412

  Hakulinen, Nina ^a   Turunen, Ossi ^b   Jänis, Janne ^a   Leisola, Matti ^b   Rouvinen, Juha ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b AALTO UNIVERSITY   (Finland)

Author keywords

Family 11; Glycoside hydrolases; Thermostability; Xylanase

Indexed keywords

ARGININE; BETA 1,4 XYLANASE; ENZYME; THREONINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ARTICLE; CHAETOMIUM THERMOPHILUM; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME MODIFICATION; ENZYME STABILITY; ENZYME STRUCTURE; FUNGUS; GENE SEQUENCE; HYDROGEN BOND; HYDROPHOBICITY; NONHUMAN; NONOMURAEA FLEXUOSA; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; THERMOSTABILITY; TRICHODERMA REESEI;

ACTINOMYCETALES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHAETOMIUM; CRYSTALLOGRAPHY, X-RAY; DISULFIDES; FUNGAL PROTEINS; HYDROGEN BONDING; HYDROPHOBICITY; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; XYLAN ENDO-1,3-BETA-XYLOSIDASE; XYLOSIDASES;

CHAETOMIUM THERMOPHILUM; FUNGI; HYPOCREA JECORINA; NONOMURAEA FLEXUOSA; THERMOPHILUM; TRICHODERMA;

EID: 0344406096     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03496.x     Document Type: Article

References (57)

1. Viikari, L., Kantelinen, A., Sundquist, J. & Linko, M. (1994) Xylanases in bleaching: from an idea to the industry. FEMS Microbiol. Rev. 13, 335-350.
2. Prade, R.A. (1996) Xylanases: from biology to biotechnology. Biotechnol. Genet. Eng. Rev. 13, 101-131.
3. Biely, P. (1985) Microbial xylanolytic systems. Trends Biotechnol. 3, 286-290.
4. Henrissat, B. & Davies, G. (1997) Structural and sequence based classification of glycosyl hydrolases. Curr. Opin. Struct. Biol. 7, 637-644.
5. Campbell, R.L., Rose, D.R., Wakarchuk, W.W., To, R., Sung, W. & Yaguchi, M. (1993) Trichoderma Reesei Cellulases and Other Hydrolases. (Suominen, P. & Reinikainen, T., eds) pp. 63-72, Foundation for Biochemical and Industrial Fermentation Research, Espoo, Finland.
6. Wakarchuk, W.W., Campbell, R.L., Sung, W.L., Davoodi, J. & Yaguchi, M. (1994) Mutational and crystallographic analyses of the active-site residues of the Bacillus circulans xylanase. Protein Sci. 3, 467-475.
7. Sidhu, G., Withers, S.G., Nguyen, N.T., McIntosh, L.P., Ziser, L. & Brayeer, G.D. (1999) Biochemistry 38, 5346-5354.
8. Törrönen, A., Harkki, A. & Rouvinen, J. (1994) Three-dimensional structure of endo-1,4-β-xylanase II from Trichoderma reesei: two conformation states in the active site. EMBO J. 13, 2493-2501.
9. Törrönen, A. & Rouvinen, J. (1995) Structural comparison of two major endo-1,4-xylanases from Trichoderma reesei. Biochemistry 34, 847-856.
10. Krengel, U. & Dijkstra, B.W. (1996) Three-dimensional structure of endo-1,4-β-xylanase I from Aspergillus niger: Molecular basis for its low pH optimum. J. Mol. Biol. 263, 70-78.
11. Gruber, K., Klintschar, G., Hayn, M., Schlacher, A., Steiner, W. & Kratky, C. (1998) Thermophilic xylanase from Thermomyces lanuginosus: High-resolution X-ray structure and modeling studies. Biochemistry 37, 13475-13485.
12. Fushinobu, S., Ito, K., Konno, M., Wakagi, T. & Matsuzawa, H. (1998) Crystallographic and mutational analyses of an extremely acidophilic and acid-stable xylanase: Biased distribution of acidic residues and importance of Asp37 for catalysis at low pH. Protein Eng. 11, 1121-1128.
13. Sabini, E., Sulzenbacher, G., Dauter, M., Dauter, Z., Jorgensen, P.L., Schulein, M., Dupont, C., Davies, G.J. & Wilson, K.S. (1999) Catalysis and specificity in enzymatic glycoside hydrolysis: a 2,5B conformation for the glycosyl-enzyme intermediate revealed by the structure of the Bacillus agaradhaerens family 11 xylanase. Chem. Biol. 6, 448-455.
14. Kumar, P.R., Eswaramoorthy, S., Vithayathil, P.J. & Viswamitra, M.A. (2000) The tertiary structure at 1.59 Å resolution and the proposed amino acid sequence of a family-11 xylanase from the thermophilic fungus Paecilomyces varioti Bainier. J. Mol. Biol. 295, 581-593.
15. McCarthy, A.A., Morris, D.D., Bergquist, P.L. & Baker, E.N. (2000) Structure of TRX IB, a highly thermostable β-1,4-xylanase from Dictyoglomus thermophilum Rt46B.1, at 1.8 Å resolution. Acta Cryst. D56, 1367-1375.
16. Harris, G.W., Pickersgill, R.W., Connerton, I., Debeire, P., Touzel, J.P., Breton, C. & Perez, S. (1997) Structural basis of the properties of an industrially relevant thermophilic xylanase. Proteins 29, 77-86.
17. Wouters, J., Georis, J., Engher, D., Vandenhaute, J., Dusart, J., Frere, J.M. & Charlier, P. (2001) Crystallographic analysis of family 11 endo-β-1,4-xylanases Xy11 from Streptomyces sp. S38. Acta Cryst. D57, 1813-1819.
18. Dunlop, R.W., Wang, B., Ball, D., Ruollo, A.B. & Falk, C.J. (1996) Bacterial protein with xylanase activity. Patent US-6200797, Biotech International Limited, Australia.
19. Morris, D.D., Gibbs, M.D., Chin, C.W., Koh, M.H., Wong, K.K.Y., Allison, R.W., Nelson, P.J. & Bergquist, P.L. (1998) Cloning of the TRX IB gene from Dictyoglomus thermophilum Rt46B.1 and action of the gene product on Kraft pulp. Appl. Environ. Microb. 64, 1759-1765.
20. Turunen, O., Etuaho, K., Fenel, F., Vehmaanperä, J., Wu, X., Rouvinen, J. & Leisola, M. (2001) Combination of weakly stabilizing mutations with a disulfide-bridge in the α-helix region of Trichoderma reesei endo-1,4-β-xylanase II increases the thermal stability through synergism. J. Biotechnol. 88, 37-46.
21. Bailey, M.J., Biely, P. & Poutanen, K. (1992) Interlaboratory testing of methods for assay of xylanase activity. J. Biotechnol. 23, 257-270.
22. Otwinowski, Z. & Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
23. Navaza, J. (1994) AmoRe: An automated package for molecular replacement. Acta Cryst. A50, 157-163.
24. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., Read, R.J., Rice, L.M., Simonson, T. & Warren, G.L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Cryst. D54, 905-921.
25. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjelgaard, M. (1991) Improved methods for binding protein models on electron density maps and the location of errors in these models. Acta Cryst. A47, 110-119.
26. Perrakis, A., Sixma, T.K., Wilson, K.S. & Lamzin, V.S. (1997) wARP: Improvement end extension of crystallographic phases by weighted averaging of multiple refined dummy atomic models. Acta Cryst. D53, 448-455.
27. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993) PROCHECK: a program to check stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291.
28. Russel, R.B. & Barton, G.J. (1992) Multiple protein sequence alignment from tertiary structure comparison: Assignment of global and residue confidence levels. Proteins: Struct. Funct. Genet. 14, 309-323.
29. Kabsch, W. & Sander, C. (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen bonded and geometrical features. Biopolymers 22, 2577-2637.
30. Hubbard, S.J. & Thonton, J.M. (1993) NACCESS, Computer Program, available from http://wolf.bms.umist.ac.uk/naccess/
31. Kleywegt, G.J. & Jones, T.A. (1994) Detection, delineation, measurement and display of cavities. Acta Cryst. D50, 178-185.
32. McDonald, I. & Thornton, J. (1994) Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777-793.
33. Barlow, D.J. & Thornton, J.M. (1983) Ion-pairs in proteins. J. Mol. Biol. 168, 867-885.
34. Wang, C., Eufemi, M., Turano, C. & Giartosio, A. (1996) Influence of the carbohydrate moiety on the stability of glycoproteins. Biochemistry 35, 7299-7307.
35. Havukainen, R., Törrönen, A., Laitinen, T. & Rouvinen, J. (1996) Covalent binding of three epoxyalkyl xylosides to the active site of endo-1,4-xylanase II from Trichoderma reesei. Biochemistry 35, 9617-9624.
36. Menendez-Arias, L. & Argos, P. (1989) Engineering protein thermal stability. Sequence statitistics point to residue substitutions in alpha-helices. J. Mol. Biol. 206, 397-406.
37. Vogt, G., Woell, S. & Argos, P. (1997) Protein thermal stability, hydrogen bonds, and ion pairs. J. Mol. Biol. 269, 631-643.
38. Kumar, S., Tsai, C.J. & Nussinov, R. (2000) Factors enhancing protein thermostability. Protein Eng. 13, 179-191.
39. Turunen, O., Vuorio, M., Fenel, F. & Leisola, M. (2002) Engineering of multiple arginines into the Ser/Thr surface of Trichoderma reesei endo-1,4-beta-xylanase II increases the thermotolerance and shifts the pH optimum towards alkaline pH. Protein Eng. 15, 141-145.
40. Argos, P., Rossman, M.G., Grau, U.M., Zuber, H., Frank, G. & Tratschin, J.D. (1979) Thermal stability and protein structure. Biochemistry 18, 5698-5703.
41. Facchiano, A.M., Colonna, G. & Ragone, R. (1998) Helix stabilizing factors and stabilization of thermophilic proteins: an X-ray based study. Protein Eng. 11, 753-760.
42. Scholtz, J.M., Qian, H., Robbins, V.H. & Baldwin, R.L. (1993) The energetic of ion-pair and hydrogen-bonding interactions in a helical peptide. Biochemistry 32, 9668-9676.
43. Viguera, A.R. & Serrano, L. (1995) Side-chain interactions between sulfur-containing amino acids and phenylalanine in α-helices. Biochemistry 34, 8771-8779.
44. Richardson, J.S. & Richardson, D.C. (1988) Science 240, 1648-1652.
45. Muilu, J., Törrönen, A., Peräkylä, M. & Rouvinen, J. (1998) Functional conformational changes of endo-154-xylanase II from Trichoderma reesei: a molecular dynamics study. Proteins 31, 434-444.
46. Daggett, V. & Levitt, M. (1993) Protein unfolding pathways explored through molecular dynamics simulations. J. Mol. Biol. 232, 600-619.
47. Wakarchuk, W.W., Sung, W.L., Campbell, R.L., Cunningham, A., Watson, D.C. & Yaguchi, M. (1994) Thermostabilization of the Bacillus circulans xylanase by the introduction of disulfide bonds. Protein Eng. 7, 1379-1386.
48. Sung, W.L. & Tolan, J.S. (2000) Thermostable xylanases. WO Patent 00/29587.
49. Russell, R.J.M., Ferguson, J.M.C., Hough, D.W., Danson, M.J. & Taylor, G.L. (1997) The crystal structure of citrate synthase from hyperthermophilic archaeon Pyrococcus furiosus at 1.9 resolution. Biochemistry 36, 9983-9994.
50. DeDecker, B.S., O'Brien, R., Fleming, P.J., Geiger, J.H., Jackson, S.P. & Sigler, P.B. (1996) The crystal stucture of a hyperthermophilic archael TATA-box binding protein. J. Mol. Biol. 264, 1072-1084.
51. Karshikoff, A. & Ladenstein, R. (1998) Proteins from thermophilic and mesophilic organisms essentially do not differ in packing. Protein Eng. 11, 867-872.
52. Chen, J., Lu, Z., Sakon, J. & Stites, W.E. (2000) Increasing thermostability of staphylococcal nuclease: implications for the origin of protein thermostability. J. Mol. Biol. 303, 125-130.
53. Chan, M.K., Mukund, S., Kletzin, A., Adams, M.W.W. & Rees, D.C. (1995) Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science 267, 1463-1469.
54. Burley, S.K. & Petsko, G.A. (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229, 23-28.
55. Kannan, N. & Vishveshwara, S. (2000) Aromatic clusters: a determinant of thermal stability of thermophilic proteins. Protein Eng. 13, 753-761.
56. Georis, J., de Lemos Esteves, F., Lamotte-Brasseur, J., Bougnet, V., Devreese, B., Giannotta, F., Granier, B. & Frère, J.-M. (2000) An additional aromatic interaction improves the therrnostability and thermophilicity of a mesophilic family 11 xylanase: Structural basis and molecular study. Protein Sci. 9, 466-475.
57. Sung, W.L., Yaguchi, M. & Ishikawa, K. (1998) Modification of xylanase to improve thermophilicity, alkophilicity and thermostability for pulp bleaching. Patent US-5759840, National Research Council of Canada, Canada