High-level expression of the Neisseria meningitidis lgtA gene in Escherichia coli and characterization of the encoded N-acetylglucosaminyltransferase as a useful catalyst in the synthesis of GlcNAcβ1→3Gal and GalNAcβ1→3Gal linkages

Glycobiology

Volumn 9, Issue 10, 1999, Pages 1061-1071

  Blixt, Ola ^a   Van Die, Irma ^b   Norberg, Thomas ^a   Van Den Eijnden, Dirk H ^b  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Enzyme assisted synthesis; Glycosid linkage; Oligosaccharide; Polylactosaminoglycan; Recombinant glycosyltransferase

Indexed keywords

LACTOSE; N ACETYLGLUCOSAMINE; N ACETYLGLUCOSAMINYLTRANSFERASE; RECOMBINANT ENZYME; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE;

ARTICLE; BACTERIAL GENE; CARBOHYDRATE SYNTHESIS; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION SYSTEM; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CLONING, MOLECULAR; DISACCHARIDES; DNA, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION; GENES, BACTERIAL; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MAMMALS; MOLECULAR SEQUENCE DATA; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEISSERIA MENINGITIDIS; OLIGOSACCHARIDES; RECOMBINANT PROTEINS; SPECIES SPECIFICITY; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEISSERIA MENINGITIDIS; PROKARYOTA;

EID: 0032824750     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/9.10.1061     Document Type: Article

References (45)

1. Appelmelk, B.J., Simoonssmit, I., Negrini, R., Moran, A.P. Aspinall, G.O., Forte, J.G., De Vries, T., Quan, H., Verboom, T., Maaskant, J.J., Ghiara, P., Kuipers, E.J., Bloemena, E., Tadema, T.M., Townsend, R.R., Tyagarajan, K., Crothers, J.M., Monteiro, M.A., Savio, A. and De Graaff, J. (1996) Potential role of molecular mimicry between Helicobacter pylori lipopolysaccharide and host Lewis blood group antigens in autoimmunity. Infect. Immun., 64, 2031-2040.
2. Bakker, H., van Tetering, A., Agterberg, M., Smit, A.B., Van den Eijnden, D.H. and van Die, I. (1997) Deletion of two exons from the Lymnaea stagnalis β1→4-N-acetylglucosaminyltransferase gene elevates the kinetic efficiency of the encoded enzyme for both UDP-sugar donor and acceptor substrates. J. Biol. Chem., 212, 18580-18585.
3. Blanken, W.M. and Van den Eijnden, D.H. (1985) Biosynthesis of terminal Galα1→3Galβ1→4GlcNAc-R oligosaccharide sequences on glycoconjugates. Purification and acceptor specificity of a UDP-Gal:N-acetyllactosaminide α1→3-galactosyltransferase from calf thymus. J. Biol. Chem., 260, 12927-12934.
4. Blanken, W.M., Hooghwinkel, G.J.M. and Van den Eijnden, D.H. (1982) Biosynthesis of blood-group I and i substances. Specificity of bovine colostrum β-N-acetyl-D-glucosaminide β1 →4-galactosyltransferase. Eur. J. Biochem., 127, 547-552.
5. a trisaccharide using an acceptor reversibly bound to Sepharose. J. Carbohydr. Chem., 16, 143-154.
6. x tetrasaccharide on a Sepharose matrix. J. Org. Chem., 63, 2705-2710.
7. Brockhausen, I., Williams, D., Matta, K.L., Orr, J. and Schachter, H. (1983) Mucin synthesis. III. UDP-GlcNAc:Galβ1-3 (GlcNAcβ1-6)GalNAc-R (GlcNAc to Gal) β3-N-acetylglucosaminyltransferase, an enzyme in porcine gastric mucosa involved in the elongation of mucin-type oligosaccharides. Can. J. Biochem. Cell Biol., 61, 1322-1333.
8. Brockhausen, I., Orr, J. and Schachter, H. (1984) Mucin synthesis. The action of pig gastric mucosal UDP-GlcNAc:Galβ1-3 (R1)GalNAc-R2 (GIcNAc to Gal) β3-N-acetylglucosaminyltransferase on high molecular weight substrates. Can. J. Biochem. Cell Biol., 62, 1081-1090.
9. Chou, D.K. and Jungalwala, F.B. (1993) N-Acetylglucosaminyltransferase regulates the expression of neolactoglycolipids including sulfoglucuronylglycolipids in the developing nervous system. J. Biol. Chem., 268, 21727-21733.
10. Del Sal, G., Manfioletti, G. and Schneider, C. (1988) A one-tube plasmid DNA mini-preparation suitable for sequencing. Nucleic Acids Res., 16, 9878-9878.
11. Eklind, K., Gustafsson, R., Tide'n, A.-K., Norberg, T. and Åberg, P.-M. (1996) Large-scale synthesis of a Lewis B tetrasaccharide derivative, its acrylamide copolymer and related di- and trisaccharides for use in adhesion inhibition studies with Helicobacter pylori. J. Carbohydr. Chem., 15, 1161-1178.
12. Feizi, T. (1985) Demonstration by monoclonal antibodies that carbohydrate structures of glycoproteins and glycolipids are onco-developmental antigens. Nature, 314. 53-57.
13. Fukuda, M. (1985) Cell surface glycoconjugates as onco-differentiation markers in hematopoietic cells. Biochim. Biophys. Acta, 780, 119-150.
14. Fukuda, M. (1996) Possible roles of tumor-associated carbohydrate antigens. Cancer Res., 56, 2237-2244.
15. Garegg, P.J., Lindberg, B. and Norberg, T. (1979) Synthesis of β-D-galactopyranosyl-(1-3)-β-D-galactopyranosyl-(1-4)-β-D- xylopyranosyl-(1-3)-L-serine. Acta Chem. Scand. B, 33, 449-452.
16. Gilbert, M., Watson, D.C., Cunningham, A.M., Jennings, M.P., Young, N.M. and Wakarchuk, W.W. (1996) Cloning of the lipooligosaccharide α-2,3-sialyl-transferase from the bacterial pathogens Neisseria meningitidis and Neisseria gonorrhoeae. J. Biol. Chem., 271, 28271-28276.
17. Gilbert, M., Cunningham, A.M., Watson, D.C., Martin, A., Richards, J.C. and Wakarchuk, W.W. (1997) Characterization of a recombinant Neisseria meningitidis α-2,3-sialyltransferase and its acceptor specificity. Eur. J. Biochem., 249, 187-194.
18. Gotschlich, E.C. (1994) Genetic locus for the biosynthesis of the variable portion of Neisseria gonorrhoeae lipooligosaccharide. J. Exp. Med., 180, 2181-2190.
19. Guo, Z. and Wang, P.G. (1997) Utilization of glycosyltransferases to change oligosaccharide structures. Appl. Biochem. Biotechnol., 68, 1-20.
20. l-acid glycoprotein. Biochim. Biophys. Acta. 322, 99-108.
21. Hill, H.D., Reynolds, J.A. and Hill, R.L. (1977) Purification, composition, molecular weight and subunit structure of ovine submaxillary mucin. J. Biol. Chem., 252, 3791-3798.
22. Hokke, C.H., Zervosen, A., Elling, L., Joziasse, D.H. and Van den Eijnden, D.H. (1996) One-pot enzymatic synthesis of the Galα1→3Galβ1→4GlcNAc sequence with in situ UDP-Gal regeneration. Glycoconjugate J., 13, 687-692.
23. Jennnings, M.P., Hood, D.W., Peak, I.R.A., Virji, M. and Moxon, E.R. (1995) Molecular analysis of a locus for the biosynthesis and phase-variable expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. Mol. Microbiol., 18, 729-740.
24. Kawashima, H., Yamamoto, K., Osawa, T. and Irimura, T. (1993) Purification and characterization of UDP-GlcNAc.:Galβ1-4Glc (NAc) β-1,3-N-acetylglucosaminyltransferase (poly-N-acetyllactosamine extension enzyme) from calf serum. J. Biol. Chem., 268, 27118-27126.
25. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227, 680-685.
26. McEver, R.P. and Cummings, R.D. (1997) Role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Invest., 100, 485-492.
27. Narimatsu, H. (1994) Recent progress in molecular cloning of glycosyltransferase genes of eukaryotes. Microbiol. Immunol., 38, 489-504.
28. Palcic, M.M. and Hindsgaul, O. (1991) Flexibility in the donor substrate specificity of β1,4-galactosyltransferase: application in the synthesis of complex carbohydrates. Glycobiology, 1, 205-209.
29. Palcic, M.M., Heerze, L.D., Pierce, M. and Hindsgaul, O. (1988) The use of hydrophobic synthetic glycosides as acceptors in glycosyltransferase assays. Glycoconjugate J., 5, 49-63.
30. Peterson, G.L. (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem., 83, 346-356.
31. Piller, F. and Cartron, J.P. (1983) UDP-GlcNAc:Galβ1-4Glc (NAc) β1-3-N-Ace-tylglucosaminyltransferase. Identification and characterization in human serum. J. Biol. Chem., 258, 12293-12299.
32. Rastan, S., Thorpe, S.J., Scudder, R, Brown, S., Gooi, H.C. and Feizi, T. (1985) Cell interactions in preimplantation embryos: evidence for involvement of saccharides of the poly-N-acetyllactosamine series. J. Embryol. Exp. Morphol., 87, 115-128.
33. Renkonen, O., Toppila, S., Penttila, L., Salminen, H., Helin, J., Maaheimo, H., Costello, C.E., Turunen, J.P. and Renkonen, R. (1997) Synthesis of a new nanomolar saccharide inhibitor of lymphocyte adhesion - different polylactosamine backbones present multiple sialyl Lewis x determinants to L-selectin in high-affinity mode. Glycobiology, 7, 453-461.
34. Sanger, E. Nicklen, S. and Coulson, A. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA, 74, 5463-5467.
35. Sasaki, K., Kuratamiura, K., Ujita, M., Angata, K., Nakagawa, S., Sekine, S., Nishi, T. and Fukuda, M. (1997) Expression cloning of cDNA encoding a human β-1,3-N-acetylglucosaminyltransferase that is essential for poly-N-acetyllactosamine synthesis. Proc. Natl. Acad. Sci. USA, 94, 14294-14299.
36. Studier, F.W., Rosenberg, A.H., Dunn, J.J. and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol., 185, 60-89.
37. Van den Eijnden, D.H., Winterwerp.H., Smeeman, P. and Schiphorst, W.E.C.M. (1983) Novikoff ascites tumor cells contain N-acetyllactosaminide β1→3 and β→6 N-acetylglucosaminyltransferase activity. J. Biol. Chem., 258, 3435-3437.
38. Van den Eijnden, D.H., Koenderman, A.H.L. and Schiphorst, W.E.C.M. (1988) Biosynthesis of blood group i-active polylactosaminoglycans. Partial purification and properties of an UDP-GlcNAc:N-acetyllactosaminide β1→3-N-acetylglucosaminyltransferase from Novikoff tumor cell ascites fluid. J. Biol. Chem., 263, 12461-12471.
39. Van der Ley, R., Kramer, M., Martin, A., Richards, J.C. and Poolman, J.T. (1997) Analysis of the icsBA locus required for biosynthesis of the inner core region from Neisseria meningitidis lipopolysaccharide. FEMS Microbiol. Lett., 146, 247-253.
40. Wakarchuk, W., Martin, A., Jennings, M.P., Moxon, E.R. and Richards, J.C. (1996) Functional relationships of the genetic locus encoding the glycosyltransferase enzymes involved in expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. J. Biol. Chem., 271, 19166-19173.
41. Wilkins, P.P., McEver, R.P. and Cummings, R.D. (1996) Structures of the O-glycans on P-selectin glycoprotein ligand-1 from HL-60 CELLS. J. Biol. Chem., 271, 18732-18742.
42. Wong, C.-H. and Whitesides, G.M. (1994) Synthesis of glycoside bonds. In Enzymes in Synthetic Organic Chemistry. Tetrahedron Organic Chemistry Series, Vol. 12. Elsevier Science, Amsterdam, The Netherlands, pp. 252-297.
43. Yamamoto, F. and Hakomori, S. (1990) Sugar-nucleotide donor specificity of histo-blood group A and B transferases is based on amino acid substitutions. J. Biol. Chem., 265, 19257-19262.
44. Yates, A.D., Greenwell, P. and Watkins, W.M. (1983) Overlapping specificities of the glycosyltransferases specified by the blood-group A and B genes: a possible explanation for aberrant blood group expression in malignant tissues. Biochem. Soc. Trans., 11, 300-301.
45. Yates, A.D. and Watkins, W.M. (1983) Enzymes involved in the biosynthesis of glycoconjugates. A UDP-2-acetamido-2-deoxy-D-glucose: β-D-galactopyranosyl-(1→4)-saccharide (1→3)-2-2-deoxy-β-D-glucopyranosyltransferase in human serum. Carbohydr. Res., 120, 251-268.