Reaction mechanism and substrate specificity for nucleotide sugar of mammalian α1,6-fucosyltransferase - A large-scale preparation and characterization of recombinant human FUT8

Glycobiology

Volumn 16, Issue 4, 2006, Pages 333-342

  Ihara, Hideyuki ^a   Ikeda, Yoshitaka ^b,c   Taniguchi, Naoyuki ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SAGA UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Fucosyltransferase FUT8 Baculovirus insect cell expression system Kinetic analysis Reaction mechanism

Indexed keywords

ALPHA 1,6 FUCOSYLTRANSFERASE; ARGININE; ASPARAGINE; FUCOSYLTRANSFERASE; GLYCOSYLTRANSFERASE; GUANOSINE DIPHOSPHATE FUCOSE; MEMBRANE PROTEIN; OLIGOSACCHARIDE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACULOVIRUS; CATALYSIS; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; ENZYME SYNTHESIS; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; SOLUBILITY; VIRUS INFECTION;

CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CATALYSIS; FUCOSE; FUCOSYLTRANSFERASES; HUMANS; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES, BRANCHED-CHAIN; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

ANIMALIA; INSECTA; MAMMALIA;

EID: 33645107042     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwj068     Document Type: Article

References (49)

1. Becker, D.J. and Lowe, J.B. (2003) Fucose: Biosynthesis and biological function in mammals. Glycobiology, 13, 41R-53R.
2. Beyer, T.A. and Hill, R.L. (1980) Enzymatic properties of the β-galactoside α1→2 fucosyltransferase from porcine submaxillary gland. J. Biol. Chem., 255, 5373-5379.
3. Breton, C., Oriol, R., and Imberty, A. (1998) Conserved structural features in eukaryotic and prokaryotic fucosyltransferases. Glycobiology, 8, 87-94.
4. Costache, M., Apoil, P.A., Cailleau, A., Elmgren, A., Larson, G., Henry, S., Blancher, A., Iordachescu, D., Oriol, R., and Mollicone, R. (1997) Evolution of fucosyltransferase genes in vertebrates. J. Biol. Chem., 272, 29721-29728.
5. Coullin, P., Crooijmans, R.P., Groenen, M.A., Heilig, R., Mollicone, R., Oriol, R., and Candelier, J.J. (2002) Assignment of FUT8 to chicken chromosome band 5q1.4 and to human chromosome 14q23.2→q24.1 by in situ hybridization. Conserved and compared synteny between human and chicken. Cytogenet. Genome Res., 97, 234-238.
6. Felgner, P.L., Gadek, T.R., Holm, M., Roman, R., Chan, H.W., Wenz, M., Northrop, J.P., Ringold, G.M., and Danielsen, M. (1987) Lipofection: A highly efficient, lipid-mediated DNA-transfection procedure. Proc. Natl. Acad. Sci. U. S. A., 84, 7413-7417.
7. Hayashi, H., Yoneda, A., Asada, M., Ikekita, M., and Imamura, T. (2000) Molecular cloning of mouse α-1,6-fucosyltransferase and expression of its mRNA in the developing cerebrum. DNA Seq., 11, 91-96.
8. Ihara, H., Ikeda, Y., Koyota, S., Endo, T., Honke, K., and Taniguchi, N. (2002) A catalytically inactive β1,4-N-acetylglucosaminyltransferase III (GnT-III) behaves as a dominant negative GnT-III inhibitor. Eur. J. Biochem., 269, 193-201.
9. Ikeda, Y., Koyota, S., Ihara, H., Yamaguchi, Y., Korekane, H., Tsuda, T., Sasai, K., and Taniguchi, N. (2000) Kinetic basis for the donor nucleotide-sugar specificity of β1,4-N-acetylglucosaminyltransferase III. J. Biochem. (Tokyo), 128, 609-619.
10. Inamori, K., Endo, T., Gu, J., Matsuo, I., Ito, Y., Fujii, S., Iwasaki, H., Narimatsu, H., Miyoshi, E., Honke, K., and Taniguchi, N. (2004) N-Acetylglucosaminyltransferase IX acts on the GlcNAc β1,2-Man α1-Ser/ Thr moiety, forming a 2,6-branched structure in brain O-mannosyl glycan. J. Biol. Chem., 279, 2337-2340.
11. Javaud, C., Dupuy, F., Maftah, A., Michalski, J.C., Oriol, R., Petit, J.M., and Julien, R. (2000) Ancestral exonic organization of FUT8, the gene encoding the α6-fucosyltransferase, reveals successive peptide domains which suggest a particular three-dimensional core structure for the α6-fucosyltransferase family. Mol. Biol. Evol., 17, 1661-1672.
12. Kunkel, T.A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. U. S. A., 82, 488-492.
13. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
14. Longmore, G.D. and Schachter, H. (1982) Product-identification and substrate-specificity studies of the GDP-L-fucose: 2-acetamido-2-deoxy-β-D-glucoside (FUC goes to Asn-linked GlcNAc) 6-α-L-fucosyltransferase in a Golgi-rich fraction from porcine liver. Carbohydr. Res., 100, 365-392.
15. Martinez-Duncker, I., Michalski, J.C., Bauvy, C., Candelier, J.J., Mennesson, B., Codogno, P., Oriol, R., and Mollicone, R. (2004) Activity and tissue distribution of splice variants of α6-fucosyltransferase in human embryogenesis. Glycobiology, 14, 13-25.
16. Martinez-Duncker, I., Mollicone, R., Candelier, J.J., Breton, C., and Oriol, R. (2003) A new superfamily of protein-O-fucosyltransferases, α2-fucosyltransferases, and α6-fucosyltransferases: Phylogeny and identification of conserved peptide motifs. Glycobiology, 13, 1C-5C.
17. Mita, Y., Aoyagi, Y., Suda, T., and Asakura, H. (2000) Plasma fucosyltransferase activity in patients with hepatocellular carcinoma, with special reference to correlation with fucosylated species of α-fetoprotein. J. Hepatol., 32, 946-954.
18. Miyoshi, E., Noda, K., Ko, J.H., Ekuni, A., Kitada, T., Uozumi, N., Ikeda, Y., Matsuura, N., Sasaki, Y., Hayashi, N., and others. (1999) Overexpression of α1-6 fucosyltransferase in hepatoma cells suppresses intrahepatic metastasis after splenic injection in athymic mice. Cancer Res., 59, 2237-2243.
19. Miyoshi, E., Noda, K., Yamaguchi, Y., Inoue, S., Ikeda, Y., Wang, W., Ko, J.H., Uozumi, N., Li, W., and Taniguchi, N. (1999) The α1-6-fucosyltransferase gene and its biological significance. Biochem. Biophys. Acta, 1473, 9-20.
20. Miyoshi, E., Uozumi, N., Noda, K., Hayashi, N., Hori, M., and Taniguchi, N. (1997) Expression of α1-6 fucosyltransferase in rat tissues and human cancer cell lines. Int. J. Cancer, 72, 1117-1121.
21. Morais, V.A., Costa, M.T., and Costa, J. (2003) N-glycosylation of recombinant human fucosyltransferase III is required for its in vivo folding in mammalian and insect cells. Biochem Biophys. Acta., 1619, 133-138.
22. Morais, V.A., Serpa, J., Palma, A.S., Costa, T., Maranga, L., and Costa, J. (2001) Expression and characterization of recombinant human α-3/ 4-fucosyltransferase III from Spodoptera frugiperda (Sf9) and Trichoplusia ni (Tn) cells using the baculovirus expression system. Biochem. J., 353, 719-725.
23. Murray, B.W., Takayama, S., Schultz, J., and Wong, C.H. (1996) Mechanism and specificity of human α-1,3-fucosyltransferase V. Biochemistry, 35, 11183-11195.
24. Nakakita, S., Menon, K.K., Natsuka, S., Ikenaka, K., and Hase, S. (1999) β1-4Galactosyltransferase activity of mouse brain as revealed by analysis of brain-specific complex-type N-linked sugar chains. J. Biochem. (Tokyo), 126, 1161-1169.
25. Noda, K., Miyoshi, E., Uozumi, N., Gao, C.X., Suzuki, K., Hayashi, N., Hori, M., and Taniguchi, N. (1998) High expression of α-1-6 fucosyltransferase during rat hepatocarcinogenesis. Int. J. Cancer, 75, 444-450.
26. Noda, K., Miyoshi, E., Uozumi, N., Yanagidani, S., Ikeda, Y., Gao, C., Suzuki, K., Yoshihara, H., Yoshikawa, K., Kawano, K., and others. (1998) Gene expression of α1-6 fucosyltransferase in human hepatoma tissues: A possible implication for increased fucosylation of α-fetoprotein [erratum in: Hepatology 1999;29:301]. Hepatology, 28, 944-952.
27. Okajima, T., Xu, A., Lei, L., and Irvine, K.D. (2005) Chaperone activity of protein O-fucosyltransferase 1 promotes notch receptor folding. Science, 307, 1599-1603.
28. Oriol, R., Mollicone, R., Cailleau, A., Balanzino, L., and Breton, C. (1999) Divergent evolution of fucosyltransferase genes from vertebrates, invertebrates, and bacteria. Glycobiology, 9, 324-334.
29. Piwnica-Worms, H. (1987) Expression of proteins in insect cells using baculovirus vectors. In Ausebel, F.M., Brent, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (eds), Current Protocols in Molecular Biology. Greene Publishing Associates and Wiley-Interscience, NY, pp. 16.8.1-16.11.7.
30. Qiao, L., Murray, B.W., Shimazaki, M., Schuultz, J., and Wong, C.H. (1996) Synergistic inhibition of human α-1,3-fucosyltransferase V. J. Am. Chem. Soc., 118, 7653-7662.
31. Seko, A., Koketsu, M., Nishizono, M., Enoki, Y., Ibrahim, H.R., Juneja, L.R., Kim, M., and Yamamoto, T. (1997) Occurrence of a sialylglycopeptide and free sialylglycans in hen's egg yolk. Biochim. Biophys. Acta, 1335, 23-32.
32. Shao, M.C., Sokolik, C.W., and Wold, F. (1994) Specificity studies of the GDP-[L]-fucose: 2-acetamido-2-deoxy-β-[D]-glucoside (Fuc→Asn-linked GlcNAc) 6-α-[L]-fucosyltransferase from rat-liver Golgi membranes. Carbohydr. Res., 251, 163-173.
33. Shields, R.L., Lai, J., Keck, R., O'Connell, L.Y., Hong, K., Meng, Y.G., Weikert, S.H., and Presta, L.G. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. J. Biol. Chem., 277, 26733-26740.
34. Shinkai, A., Shinoda, K., Sasaki, K., Morishita, Y., Nishi, T., Matsuda, Y., Takahashi, I., and Anazawa, H. (1997) High-level expression and purification of a recombinant human α-1,3-fucosyltransferase in baculovirus-infected insect cells. Protein Expr. Purif., 10, 379-385.
35. Shinkawa, T., Nakamura, K., Yamane, N., Shoji-Hosaka, E., Kanda, Y., Sakurada, M., Uchida, K., Anazawa, H., Satoh, M., Yamasaki, M., and others. (2003) The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. J. Biol. Chem., 278, 3466-3473.
36. Smithers, N., Kelly, V.A., Witham, S.J., Edbrooke, M.R., and Britten, C.J. (1997) Expression of a secreted form of human α1,3 fucosyltransferase VII from insect cells. Biochem. Soc. Trans., 25, 426S.
37. Staudacher, E., Altmann, F., Wilson, I.B., and Marz, L. (1999) Fucose in N-glycans: From plant to man. Biochim. Biophys. Acta, 1473, 216-236.
38. Staudacher, E. and Marz, L. (1998) Strict order of (Fuc to Asn-linked GlcNAc) fucosyltransferases forming core-difucosylated structures. Glycoconj. J., 15, 355-360.
39. Struppe, E. and Staudacher, E. (2000) Occurrence of GDP-L-fucose: β-N-acetylglucosamine (Fuc to Asn-linked GlcNAc) α1,6-fucosyltransferases in porcine, sheep, bovine, rabbit and chicken tissues. Biochim. Biophys. Acta, 1475, 360-368.
40. Takahashi, T., Ikeda, Y., Miyoshi, E., Yaginuma, Y., Ishikawa, M., and Taniguchi, N. (2000) α1,6Fucosyltransferase is highly and specifically expressed in human ovarian serous adenocarcinomas. Int. J. Cancer, 88, 914-919.
41. Takahashi, T., Ikeda, Y., Tateishi, A., Yamaguchi, Y., Ishikawa, M., and Taniguchi, N. (2000) A sequence motif involved in the donor substrate binding by α1,6-fucosyltransferase: The role of the conserved arginine residues. Glycobiology, 10, 503-510.
42. Uozumi, N., Teshima, T., Yamamoto, T., Nishikawa, A., Gao, Y.E., Miyoshi, E., Gao, C.X., Noda, K., Islam, K.N., Ihara, Y., and others. (1996) A fluorescent assay method for GDP-L-Fuc: N-acetyl-β-D-glucosaminide α1-6fucosyltransferase activity, involving high performance liquid chromatography. J. Biochem. (Tokyo), 120, 385-392.
43. Uozumi, N., Yanagidani, S., Miyoshi, E., Ihara, Y., Sakuma, T., Gao, C.X., Teshima, T., Fujii, S., Shiba, T., and Taniguchi, N. (1996) Purification and cDNA cloning of porcine brain GDP-L-Fuc: N-acetyl-β-D-glucosaminide α1→6fucosyltransferase. J. Biol. Chem., 271, 27810-27817.
44. Voynow, J.A., Kaiser, R.S., Scanlin, T.F., and Glick, M.C. (1991) Purification and characterization of GDP-L-fucose-N-acetyl beta-D-glucosaminide alpha 1-6fucosyltransferase from cultured human skin fibroblasts. Requirement of a specific biantennary oligosaccharide as substrate. J. Biol. Chem., 266, 21572-21577.
45. Wang, X., Inoue, S., Gu, J., Miyoshi, E., Noda, K., Li, W., Mizuno-Horikawa, Y., Nakano, M., Asahi, M., Takahashi, M., and others. (2005) Dysregulation of TGF-β1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc. Natl. Acad. Sci. U. S. A., 102, 15791-15796.
46. Wilson, J.R., Williams, D., and Schachter, H. (1976) The control of glycoprotein synthesis: N-acetylglucosamine linkage to a mannose residue as a signal for the attachment of L-fucose to the asparagine-linked N-acetylglucosamine residue of glycopeptide from alpha1-acid glycoprotein. Biochem. Biophys. Res. Commun., 72, 909-916.
47. Yamaguchi, Y., Fujii, J., Inoue, S., Uozumi, N., Yanagidani, S., Ikeda, Y., Egashira, M., Miyoshi, O., Niikawa, N., and Taniguchi, N. (1999) Mapping of the α-1,6-fucosyltransferase gene, FUT8, to human chromosome 14q24.3. Cytogenet. Cell Genet., 84, 58-60.
48. Yamaguchi, Y., Ikeda, Y., Takahashi, T., Ihara, H., Tanaka, T., Sasho, C., Uozumi, N., Yanagidani, S., Inoue, S., Fujii, J., and Taniguchi, N. (2000) Genomic structure and promoter analysis of the human α1,6-fucosyltransferase gene (FUT8). Glycobiology, 10, 637-643.
49. Yanagidani, S., Uozumi, N., Ihara, Y., Miyoshi, E., Yamaguchi, N., and Taniguchi, N. (1997) Purification and cDNA cloning of GDP-L-Fuc: N-acetyl-β-D-glucosaminide: α1-6 fucosyltransferase (α1-6 FucT) from human gastric cancer MKN45 cells. J. Biochem. (Tokyo), 121, 626-632.