Crystal structures of Trichoderma reesei β-galactosidase reveal conformational changes in the active site

Journal of Structural Biology

Volumn 174, Issue 1, 2011, Pages 156-163

  Maksimainen, Mirko ^a   Hakulinen, Nina ^a   Kallio, Johanna M ^a   Timoharju, Tommi ^b   Turunen, Ossi ^b   Rouvinen, Juha ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b AALTO UNIVERSITY   (Finland)

Author keywords

Galactosidase; Conformational changes; Crystal structure; Glycosyl hydrolase; Octaserine

Indexed keywords

2 PHENYLETHYL BETA DEXTRO THIOGALACTOSIDE; BETA GALACTOSIDASE; GALACTOSE; GALACTOSIDE; GLYCEROL; ISOPROPYL BETA DEXTRO 1 THIOGALACTOPYRANOSIDE; LACTOSE; MONOSACCHARIDE; OCTASERINE; PYRANOSIDE; SERINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CATALYST; CRYSTAL STRUCTURE; ELECTRON; ENZYME CONFORMATION; GLYCOSYLATION; HYDROLYSIS; HYPOCREA JECORINA; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN MOTIF; STRUCTURE ANALYSIS;

BETA-GALACTOSIDASE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GLYCEROL; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; TRICHODERMA;

HYPOCREA JECORINA;

EID: 79952445041     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.11.024     Document Type: Article

References (41)

1. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombart V., Henrissat B. The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 2009, 37:D233-D238.
2. Davies G., Henrissat B. Structures and mechanisms of glycosyl hydrolases. Structure 1995, 3:853-859.
3. de Barros M.C., do Nascimento Silva R., Ramada M.H., Galdino A.S., de Moraes L.M., Torres F.A., Ulhoa C.J. The influence of N-glycosylation on biochemical properties of Amy1, an alpha-amylase from the yeast Cryptococcus flavus. Carbohydr. Res. 2009, 344:1682-1686.
4. Dickson R.C., Dickson L.R., Markin J.S. Purification and properties of an inducible beta-galactosidase isolated from the yeast Kluyveromyces lactis. J. Bacteriol. 1979, 137:51-61.
5. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Cryst. D 2004, 60:2126-2132.
6. Gamauf C., Marchetti M., Kallio J., Puranen T., Vehmaanperä J., Allmaier G., Kubicek C.P., Seiboth B. Characterization of the bga1-encoded glycoside hydrolase family 35 β-galactosidase of Hypocrea jecorina with galacto-d-galactanase activity. FEBS J. 2007, 274:1691-1700.
7. Gloster T.M., Roberts S., Ducros V.M.-A., Perugino G., Rossi M., Hoos R., Moracci M., Vasella A., Davies G.J. Structural studies of the β-glycosidase from Sulfolobus solfataricus in complex with covalently and noncovalently bound inhibitors. Biochemistry 2004, 43:6101-6109.
8. Griffith K.L., Wolf R.E. Measuring -galactosidase activity in bacteria: cell growth permeabilization and enzyme assays in 96-well arrays. Biochem. Biophys. Res. Commun. 2002, 290:397-402.
9. Harrington L.K., Mayberry J.F. A re-appraisal of lactose intolerance. Int. J. Clin. Pract. 2008, 62:1541-1546.
10. Hidaka M., Fushinobu S., Ohtsu N., Motoshima H., Matsuzawa H., Shoun H., Wakagi T. Trimeric crystal structure of the glycoside hydrolase family 42-galactosidase from Thermus thermophilus A4 and the structure of its complex with galactose. J. Mol. Biol. 2002, 322:79-91.
11. Higashiyama T., Watanabe H., Aga H., Nishimoto T., Kubota M., Fukuda S., Kurimoto M., Tsujisaka Y. Enzymatic synthesis of a β-d-galactopyranosyl cyclic tetrasaccharide by β-galactosidases. Carbohydr. Res. 2004, 339:1603-1608.
12. Howard M.B., Ekborg N.A., Taylor L.E., Hutcheson S.W., Weiner R.M. Identification and analysis of polyserine link domains in prokaryotic proteins with emphasis on the marine bacterium Microbulbifer degradans. Protein Sci. 2004, 13:1522-1525.
13. Jacobson R.H., Zhang X.-J., DuBose R.F., Matthews B.W. Three-dimensional structure of -galactosidase from E. coli. Nature 1994, 369:761-766.
14. Jones J., Krag S.S., Betenbaugh M.J. Controlling N-linked glycan site occupancy. Biochim. Biophys. Acta 2005, 1726:121-137.
15. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A 1991, 47:110-119.
16. Juers D.H., Heightman T.D., Vasella A., McCarter J.D., Mackenzie L., Withers S.G., Matthews B.W. A structural view of the action of Escherichia coli (lacZ) beta-galactosidase. Biochemistry 2001, 40:14781-14794.
17. Juers D.H., Jakobson R.H., Wigley D., Zhang X.J., Huber R.E., Tronrud D.E., Matthews B.W. High resolution refinement of β-galactosidase in a new crystal form reveals multiple metal-binding sites and provides a structural basis for -complementation. Protein Sci. 2000, 9:1685-1699.
18. Juers D.H., Rob B., Dugdale M.L., Rahimzadeh N., Giang C., Lee M., Matthews B.W., Huber R.E. Direct and indirect roles of His-418 in metal binding and in the cavity of β-galactosidase (E. coli. Protein Sci. 2009, 18:1281-1292.
19. Kabsch W.J. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constant. J. Appl. Cryst. 1993, 26:795-800.
20. Kestwal R.M., Bhide S.V. Purification of β-galactosidase from Erythina indica: Involvement of tryptophan in active site. Biochim. Biophys. Acta 2007, 1770:1506-1512.
21. Langer G.G., Cohen S.X., Lamzin V.S., Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 2008, 3:1171-1179.
22. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993, 26:283-291.
23. 13C-NMR study of Bacillus circulans xylanase. Biochemistry 1996, 35:9958-9966.
24. Maksimainen M., Timoharju T., Kallio J.M., Hakulinen N., Turunen O., Rouvinen J. Crystallization and preliminary diffraction analysis of a β-galactosidase from Trichoderma reesei. Acta Cryst. F 2009, 65:767-769.
25. Matsuura F., Ohta M., Murakami K., Matsuki Y. Structures of asparagine linked oligosaccharides of immunoglobulins (IgY) isolated from egg-yolk of Japanese quail. Glycoconj. J. 1993, 10:202-213.
26. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Cryst. D 1999, 55:247-255.
27. Potterton E., Briggs P., Turkenburg M., Dodson E. A graphical user interface to the CCP4 program suite. Acta Cryst. D 2003, 59:1131-1137.
28. Rojas A.L., Nagem R.A.P., Neustroev K.N., Arand M., Adamska M., Eneyskaya E.V., Kulminskaya A.A., Garratt R.C., Golubev A.M., Polikarpov I. Crystal structures of -galactosidase from Penicillium sp. and its complex with galactose. J. Mol. Biol. 2004, 343:1281-1292.
29. Seiboth B., Hartl L., Salovuori N., Lanthaler K., Robson G.D., Vehmaanperä J., Penttilä M.E., Kubicek C.P. Role of the bga1-encoded extracellular-galactosidase of Hypocrea jecorina in cellulase induction by lactose. Appl. Environ. Microbiol. 2005, 71:851-857.
30. Sener N., Kilic Apar D., Demirhan E., Özbek B. Milk lactose hydrolysis in a batch reactor: optimisation of process parameters, kinetics of hydrolysis and enzyme inactivation. Chem. Biochem. Eng. Q 2008, 22:185-193.
31. Shaikh S.A., Khire J.M., Khan M.I. Characterization of a thermostable extracellular β-galactosidase from thermophilic fungus Rhizomucor sp. Biochim. Biophys. Acta 1999, 1472:314-322.
32. Sheldrick G.M. A short history of SHELX. Acta Cryst. A 2008, 64:112-122.
33. Skalova T., Dohnalek J., Spiwok V., Lipovova P., Vondrackova E., Petrokova H., Strnad H., Kralova B., Hasek J. Cold-active β-galactosidase from Arthrobacter sp. C2-2 forms compact 660kDa hexamers: Crystal structure at 1.9Å resolution. J. Mol. Biol. 2005, 353:282-294.
34. Splechtna B., Nguyen T., Steinböck M., Kulbe K.D., Lorenz W., Haltrich D. Production of prebiotic galacto-oligosaccharides from lactose using β-galactosidases from Lactobacillus reuteri. J. Agric. Food Chem. 2006, 54:4999-5006.
35. The CCP4 suite Programs for Protein Crystallography. Acta Cryst. D 1994, 50:760-763.
36. Tsai C.-J., Ma B., Nussinov R. Folding and binding cascades: shifts in energy landscapes. Proc. Natl. Acad. Sci. USA 1999, 96:9970-9972.
37. Törrönen A., Harkki A., Rouvinen J. Crystallographic studies on endo-1, 4-β-xylanase II from Trichoderma reesei: two conformational states in the active site. EMBO J. 1994, 13:2493-2501.
38. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Cryst. 1997, 30:1022-1025.
39. Wang Z.H., Zeng B., Shibuya H., Johnson G.S., Alroy J., Pastores G.M., Raghavan S., Kolodny E.H. Isolation and characterization of the normal canine beta-galactosidase gene and its mutation in a dog model of GM1-gangliosidosis. J. Inherit. Metab. Dis. 2000, 23:593-606.
40. Zal F., Kuster B., Green B.N., Harvey D.J., Lallier F.H. Partially glucose-capped oligosaccharides are found on the hemoglobins of the deep-sea tube worm Riftia pachyptila. Glycobiology 1998, 8:663-673.
41. Zhou Q.Z., Chen X.D., Li X. Kinetics of lactose hydrolysis by beta-galactosidase of Kluyveromyces lactis immobilized on cotton fabric. Biotechnol. Bioeng. 2002, 81:127-133.