Mutation of arginine 228 to lysine enhances the glucosyltransferase activity of bovine β-1,4-galactosyltransferase I

Biochemistry

Volumn 44, Issue 9, 2005, Pages 3202-3210

  Ramakrishnan, Boopathy ^a,b   Boeggeman, Elizabeth ^a,b   Qasba, Pradman K ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; COMPLEXATION; CONFORMATIONS; CRYSTAL ORIENTATION; DISSOCIATION; GLUCOSE; HYDROGEN BONDS;

Α-LACTALBUMIN (LA); GLUCOSYLTRANSFERASE; HYDROXYL GROUP; MUTATION;

ENZYME KINETICS;

ALPHA LACTALBUMIN; ARGININE; BETA 1,4 GALACTOSYLTRANSFERASE 1; GLUCOSYLTRANSFERASE; LYSINE; MANGANESE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE; URIDINE DIPHOSPHATE GALACTOSE; URIDINE DIPHOSPHATE GLUCOSE;

ARTICLE; CATALYSIS; COW; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME CONFORMATION; HYDROGEN BOND; KINETICS; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; STEREOSPECIFICITY; WILD TYPE;

ANIMALS; ARGININE; CATTLE; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; GALACTOSYLTRANSFERASES; GLUCOSYLTRANSFERASES; KINETICS; LACTALBUMIN; LYSINE; MACROMOLECULAR SUBSTANCES; MANGANESE; MUTAGENESIS, SITE-DIRECTED; URIDINE DIPHOSPHATE GALACTOSE; URIDINE DIPHOSPHATE GLUCOSE;

EID: 14644434401     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0479454     Document Type: Article

References (36)

1. Brew, K., Vanaman, T. C., and Hill, R. L. (1968) The role of α-lactalbumin and the A protein in lactose synthetase: A unique mechanism for the control of a biological reaction, Proc. Natl. Acad. Sci. U.S.A. 59, 491-497.
2. Brodbeck, U., Denton, W. L., Tanahashi, N., and Ebner, K. E. (1967) The isolation and identification of the B protein of lactose synthetase as α-lactalbumin, J. Biol. Chem. 242, 1391-1397.
3. Andree, P. J., and Berliner, L. J. (1978) Glucosyltransferase activity of bovine galactosyl-transferase, Biochim. Biophys. Acta 544, 489-495.
4. Palcic, M. M., and Hindsgaul, O. (1991) Flexibility in the donor substrate specificity of β-1,4-galactosyltransferase: Application in the synthesis of complex carbohydrates, Glycobiology 1, 205-209.
5. Do, K. Y., Do, S. I., and Cummings, R. D. (1995) α-Lactalbumin induces bovine milk β-1,4-galactosyltransferase to utilize UDP-GalNAc, J. Biol. Chem. 270, 18447-18451.
6. Gastinel, L. N., Cambillau, C., and Bourne, Y. (1999) Crystal structures of the bovine β-4-galactosyltransferase catalytic domain and its complex with uridine diphosphogalactose, EMBO J. 18, 3546-3557.
7. Ramakrishnan, B., and Qasba, P. K. (2001) Crystal structure of lactose synthase reveals a large conformational change in its catalytic component, the β-1,4-galactosyltransferase-I, J. Mol. Biol. 310, 205-218.
8. Ramakrishnan, B., Balaji, P. V., and Qasba, P. K. (2002) Crystal structure of β-1,4-galactosyltransferase complex with UDP-Gal reveals an oligosaccharide acceptor binding site, J. Mol. Biol. 318, 491-502.
9. Ramakrishnan, B., and Qasba, P. K. (2003) Comparison of the closed conformation of the β-1,4-galactosyltransferase-1 (β4Gal-T1) in the presence and absence of α-lactalbumin (LA), J. Biomol. Struct. Dyn. 21, 1-8.
10. Ramakrishnan, B., Boeggeman, E., and Qasba, P. K. (2004) Effect of the Met344His mutation on the conformational dynamics of bovine 1,4- galactosyltransferase: Crystal structure of the Met344His mutant in complex with chitobiose, Biochemistry 43, 12513-12522.
11. Ramakrishnan, B., Boeggeman, E., and Qasba, P. K. (2002) β-1,4-Galactosyltransferase and lactose synthase: Molecular mechanical devices, Biochem. Biophys. Res. Commun. 291, 1113-1118.
12. Ramakrishnan, B., Boeggeman, E., Ramasamy, V., and Qasba, P. K. (2004) Structure and catalytic cycle of β-1,4-galactosyltransferase, Curr. Opin. Struct. Biol. 14, 593-600.
13. Ramakrishnan, B., and Qasba, P. K. (2002) Structure-based design of β-1,4-galactosyltransferase I (β4Gal-T1) with equally efficient N-acetylgalactosaminyltransferase activity: Point mutation broadens β4Gal-T1 donor specificity, J. Biol. Chem. 277, 20833-20839.
14. Ramakrishnan, B., Shah, P. S., and Qasba, P. K. (2001) α-Lactalbumin (LA) stimulates milk β-1,4-galactosyltransferase I (β4Gal-T1) to transfer glucose from UDP-glucose to N-acetylglucosamine. Crystal structure of β4Ga1-T1·LA complex with UDP-Glc, J. Biol. Chem. 276, 37665-37671.
15. Marcus, S. L., Polakowski, R., Seto, N. O. L., Leinala, E., Borisova, S., Blancher, A., Roubinet, F., Evans, S. V., and Palcic, M. M. (2003) A Single Point Mutation Reverses the Donor Specificity of Human Blood Group B-synthesizing Galactosyltransferase, J. Biol. Chem. 278, 12403-12405.
16. Seto, N. O., Compston, C. A., Evans, S. V., Bundle, D. R., Narang, S. A., and Palcic, M. M. (1999) Donor substrate specificity of recombinant human blood group A, B and hybrid A/B, Eur. J. Biochem. 259, 770-775.
17. Ouzzine, M., Gulberti, S., Levoin, N., Netter, P., Magdalou, J., and Fournel-Gigleux, S. (2002) The donor substrate specificity of the human β-1,3-glucuronosyltransferase I toward UDP-glucuronic acid is determined by two crucial histidine and arginine residues, J. Biol. Chem. 277, 25439-25445.
18. Wu, K., Marks, D. I., Watanabe, R., Paul, P., Rajan, N., and Pagano, R. (1999) Histidine-193 of rat glucosylceramide synthase resides in a UDP-Glucose and inhibitor (D-threo-1-phenyl-2-decanoylamino-3-morpholinopropan-1-ol)-binding region: A biochemical and mutational study, Biochem. J. 341, 395-400.
19. Sprong, H., Kruithof, B., Leijendekker, R., Slot, J. W., van Meer, G., and van der Sluijis, P. (1998) UDP-galactose:ceramide galactosyltransferase is a class I integral membrane protein of the endoplasmic reticulum, J. Biol. Chem. 273, 25880-25888.
20. Qasba, P. K., Ramakrishnan, B., and Boeggeman, E. (2005) Substrate induced conformational changes in glycosyltransferases, Trends Biochem. Sci. 30, 53-62.
21. Khidekel, N., Arndt, S., Lamarre-Vincent, N., Lippert, A., Poulin-Kerstien, K. G., Ramakrishnan, B., Qasba, P. K., and Hsieh-Wilson, L. C. (2003) A chemoenzymatic approach toward the rapid and sensitive detection of O-GlcNAc posttranslational modifications, J. Am. Chem. Soc. 125, 16162-16163.
22. Khidekel, N., Ficarro, S. B., Peters, E. C., and Hsieh-Wilson, L. C. (2004) Exploring the O-GlcNAc proteome: Direct identification of O-GlcNAc-modified proteins from the brain, Proc. Natl. Acad. Sci. U.S.A. 101, 13132-13137.
23. Boeggeman, E., and Qasba, P. K. (2002) Studies on the metal binding sites in the catalytic domain of β-1,4-galactosyltransferase, Glycobiology 12, 395-407.
24. Boeggeman, E., Balaji, P. V., Sethi, N., Masibay, A. S., and Qasba, P. K. (1993) Expression of deletion constructs of bovine β-1,4- galactosyltransferase in Escherichia coli: Importance of Cys134 for its activity, Protein Eng. 6, 779-785.
25. Herbert, J. F. (1975) Initial Rate Enzyme Kinetics, Springer-Verlag, New York.
26. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
27. Navaza, J. (2001) Implementation of molecular replacement in AMoRe, Acta Crystallogr. D57, 1367-1372.
28. 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., and Warren, G. L. Crystallography & NMR system: A new software suite for macromolecular structure determination (1998) Acta Crystallogr. D54, 905-921.
29. Kraulis, P. J. (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
30. Esnouf, R. M. (1999) Further additions to MolScript version 1.4, including reading and contouring of electron-density maps, Acta Crystallogr. D55, 938-940.
31. Morrison, J. F., and Ebner, K. E. (1971) Studies on galactosyltransferase. Kinetic investigations with N-acetylglucosamine as the galactosyl group acceptor, J. Biol. Chem. 246, 3977-3984.
32. Khatra, B. S., Herries, D. G., and Brew, K. (1974) Some kinetic properties of human-milk galactosyl transferase, Eur. J. Biochem. 44, 537-560.
33. Ramasamy, V., Ramakrishnan, B., Boeggeman, E., and Qasba, P. K. (2003) The role of tryptophan 314 in the conformational changes of β-1,4- galactosyltransferase-I, J. Mol. Biol. 331, 1065-1076.
34. Zhang, Y., Malinovskii, V. A., Fiedler, T. J., and Brew, K. (1999) Role of a conserved acidic cluster in bovine β-1,4-galactosyltransferase-1 probed by mutagenesis of a bacterially expressed recombinant enzyme, Glycobiology 8, 815-822.
35. Bakker, H., Agterberg, M., Van Tetering, A., Koeleman, C. A., van den Eijnden, D. H., and Van Die, I. (1994) A Lymnaea stagnalis gene, with sequence similarity to that of mammalian β-1→4-galactosyltransferases, encodes a novel UDP-GlcNAc: GlcNAcβ-Rβ-1→4-N- acetylglucosaminyltransferase, J. Biol. Chem. 269, 30326-30333.
36. Kawar, Z. S., Van Die, I., and Cummings, R. D. (2002) Molecular cloning and enzymatic characterization of a UDP-GalNAc: GlcNAcβ-R β-1,4-N-acetylgalactosaminyltransferase from Caenorhabditis elegans, J. Biol. Chem. 277, 34924-34932.