1,3-1,4-α-L-Fucosynthase that specifically introduces Lewis a/x antigens into type-1/2 chains

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16709-16719

  Sakurama, Haruko ^a   Fushinobu, Shinya ^b   Hidaka, Masafumi ^b   Yoshida, Erina ^a   Honda, Yuji ^a   Ashida, Hisashi ^c   Kitaoka, Motomitsu ^d   Kumagai, Hidehiko ^a   Yamamoto, Kenji ^a   Katayama, Takane ^a  

^a ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE STRUCTURE; BIOLOGICAL PROCESS; CRYSTALLOGRAPHIC STUDIES; GLYCOCONJUGATES; GLYCOMICS; GLYCOSIDASES; GLYCOSIDE HYDROLASES; GLYCOSIDIC BOND; GLYCOSYL; GLYCOSYNTHASE; INDUCED FIT; REGIOSPECIFIC SYNTHESIS; STRUCTURAL BASIS;

CARBOHYDRATES; X RAY CRYSTALLOGRAPHY;

ANTIGENS;

ALPHA LEVO FUCOSIDASE; BLOOD GROUP ANTIGEN; DISACCHARIDE; EPITOPE; GALACTOSE; GLUCOSE; GLYCOCONJUGATE; GLYCOPROTEIN; GLYCOSIDASE; N ACETYLLACTOSAMINE SYNTHASE; SIALYL LEWIS X ANTIGEN; TRISACCHARIDE;

ARTICLE; BLOOD GROUP; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SPECIFICITY; LINKAGE ANALYSIS; NONHUMAN; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; BIFIDOBACTERIUM; CATALYTIC DOMAIN; EPITOPES; FUCOSE; FUCOSYLTRANSFERASES; HUMANS; OLIGOSACCHARIDES;

EID: 84860848800     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.333781     Document Type: Article

References (55)

1. Becker, D. J., and Lowe, J. B. (2003) Fucose: biosynthesis and biological function in mammals. Glycobiology 13, 41R-53R (Pubitemid 36850123)
2. Gooi, H. C., Feizi, T., Kapadia, A., Knowles, B. B., Solter, D., and Evans, M. J. (1981) Stage-specific embryonic antigen involves α1 goes to 3 fucosylated type 2 blood group chains. Nature 292, 156-158 (Pubitemid 11050742)
3. Inoue, M., Sasagawa, T., Saito, J., Shimizu, H., Ueda, G., Tanizawa, O., and Nakayama, M. (1987) Expression of blood group antigens A, B, H, Lewis-a, and Lewis-b in fetal, normal, and malignant tissues of the uterine endometrium. Cancer 60, 2985-2993 (Pubitemid 18013183)
4. Phillips, M. L., Nudelman, E., Gaeta, F. C., Perez, M., Singhal, A. K., Hakomori, S., and Paulson, J. C. (1990) ELAM-1 mediates cell adhesion by recognition of a carbohydrate ligand, sialyl-Lex. Science 250, 1130-1132 (Pubitemid 120031820)
5. Walz, G., Aruffo, A., Kolanus, W., Bevilacqua, M., and Seed, B. (1990) Recognition by ELAM-1 of the sialyl-Lex determinant on myeloid and tumor cells. Science 250, 1132-1135 (Pubitemid 120031821)
6. Nilsson, C., Skoglund, A., Moran, A. P., Annuk, H., Engstrand, L., and Normark, S. (2006) An enzymatic ruler modulates Lewis antigen glycosylation of Helicobacter pylori LPS during persistent infection. Proc. Natl. Acad. Sci. U.S.A. 103, 2863-2868
7. Liu, T. W., Ho, C. W., Huang, H. H., Chang, S. M., Popat, S. D., Wang, Y. T., Wu, M. S., Chen, Y. J., and Lin, C. H. (2009) Role for α-L-fucosidase in the control of Helicobacter pylori-infected gastric cancer cells. Proc. Natl. Acad. Sci. U.S.A. 106, 14581-14586
8. Bergman, M. P., Engering, A., Smits, H. H., van Vliet, S. J., van Bodegraven, A. A., Wirth, H. P., Kapsenberg, M. L., Vandenbroucke-Grauls, C. M., van Kooyk, Y., and Appelmelk, B. J. (2004) Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J. Exp. Med. 200, 979-990 (Pubitemid 39431123)
9. Hancock, S. M., Vaughan, M. D., and Withers, S. G. (2006) Engineering of glycosidases and glycosyltransferases. Curr. Opin. Chem. Biol. 10, 509-519 (Pubitemid 44375059)
10. Wang, L. X., and Huang, W. (2009) Enzymatic transglycosylation for glycoconjugate synthesis. Curr. Opin. Chem. Biol. 13, 592-600
11. Wang, W., Hu, T., Frantom, P. A., Zheng, T., Gerwe, B., Del Amo D. S., Garret, S., Seidel, R. D., 3rd, and Wu, P. (2009) Chemoenzymatic synthesis of GDP-L-fucose and the Lewis X glycan derivatives. Proc. Natl. Acad. Sci. U.S.A. 106, 16096-16101
12. Dumon, C., Bosso, C., Utille, J. P., Heyraud, A., and Samain, E. (2006) Production of Lewis x tetrasaccharides by metabolically engineered Escherichia coli. Chembiochem 7, 359-365 (Pubitemid 43220951)
13. Drouillard, S., Driguez, H., and Samain, E. (2006) Large-scale synthesis of H-antigen oligosaccharides by expressing Helicobacter pylori α1,2-fucosyltransferase in metabolically engineered Escherichia coli cells. Angew. Chem. Int. Ed. Engl. 45, 1778-1780 (Pubitemid 44105254)
14. Mackenzie, L. F., Wang, Q., Warren, R. A. J., and Withers, S. G. (1998) Glycosynthases: mutant glycosidases for oligosaccharide synthesis. J. Am. Chem. Soc. 120, 5583-5584
15. Malet, C., and Planas, A. (1998) From β-glucanase to β-glucansynthase: glycosyl transfer to α-glycosyl fluorides catalyzed by a mutant endoglucanase lacking its catalytic nucleophile. FEBS Lett. 440, 208-212 (Pubitemid 28558766)
16. Honda, Y., and Kitaoka, M. (2006) The first glycosynthase derived from an inverting glycoside hydrolase. J. Biol. Chem. 281, 1426-1431
17. Cobucci-Ponzano, B., Strazzulli, A., Rossi, M., and Moracci, M. (2011) Glycosynthases in biocatalysis. Adv. Synth. Catal. 353, 2284-2300
18. Cobucci-Ponzano, B., Conte, F., Bedini, E., Corsaro, M. M., Parrilli, M., Sulzenbacher, G., Lipski, A., Dal Piaz, F., Lepore, L., Rossi, M., and Moracci, M. (2009) β-Glycosyl azides as substrates for α-glycosynthases: preparation of efficient α-L-fucosynthases. Chem. Biol. 16, 1097-1108
19. Cobucci-Ponzano, B., Zorzetti, C., Strazzulli, A., Carillo, S., Bedini, E., Corsaro, M. M., Comfort, D. A., Kelly, R. M., Rossi, M., and Moracci, M. (2011) A novel α-D-galactosynthase from Thermotoga maritima converts β-D-galactopyranosyl azide to α-galacto-oligosaccharides. Glycobiology 21, 448-456
20. Umekawa, M., Huang, W., Li, B., Fujita, K., Ashida, H., Wang, L. X., and Yamamoto, K. (2008) Mutants of Mucor hiemalis endo-β-N- acetylglucosaminidase show enhanced transglycosylation and glycosynthase-like activities. J. Biol. Chem. 283, 4469-4479
21. Shaikh, F. A., and Withers, S. G. (2008) Teaching old enzymes new tricks: engineering and evolution of glycosidases and glycosyl transferases for improved glycoside synthesis. Biochem. Cell Biol. 86, 169-177 (Pubitemid 351536497)
22. Ajisaka, K., Fujimoto, H., and Miyasato, M. (1998) An α-L-fucosidase from Penicillium multicolor as a candidate enzyme for the synthesis of α(1→3)-linked fucosyl oligosaccharides by transglycosylation. Carbohydr. Res. 309, 125-129 (Pubitemid 28349933)
23. Murata, T., Morimoto, S., Zeng, X., Watanabe, S., and Usui, T. (1999) Enzymatic synthesis of α-L-fucosyl-N-acetyllactosamines and 3′-O-α-L-fucosyllactose utilizing α-L-fucosidases. Carbohydr. Res. 320, 192-199 (Pubitemid 29488501)
24. Farkas, E., Thiem, J., and Ajisaka, K. (2000) Enzymatic synthesis of fucose-containing disaccharides employing the partially purified α-L-fucosidase from Penicillium multicolor. Carbohydr. Res. 328, 293-299
25. Osanjo, G., Dion, M., Drone, J., Solleux, C., Tran, V., Rabiller, C., and Tellier, C. (2007) Directed evolution of the α-L-fucosidase from Thermotoga maritima into an α-L-transfucosidase. Biochemistry 46, 1022-1033 (Pubitemid 46184990)
26. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
27. Katayama, T., Sakuma, A., Kimura, T., Makimura, Y., Hiratake, J., Sakata, K., Yamanoi, T., Kumagai, H., and Yamamoto, K. (2004) Molecular cloning and characterization of Bifidobacterium bifidum 1,2-α-L-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J. Bacteriol. 186, 4885-4893 (Pubitemid 38970815)
28. Nagae, M., Tsuchiya, A., Katayama, T., Yamamoto, K., Wakatsuki, S., and Kato, R. (2007) Structural basis of the catalytic reaction mechanism of novel 1,2-α-L-fucosidase from Bifidobacterium bifidum. J. Biol. Chem. 282, 18497-18509 (Pubitemid 47100222)
29. Ashida, H., Miyake, A., Kiyohara, M., Wada, J., Yoshida, E., Kumagai, H., Katayama, T., and Yamamoto, K. (2009) Two distinct α-L-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology 19, 1010-1017
30. Wada, J., Honda, Y., Nagae, M., Kato, R., Wakatsuki, S., Katayama, T., Taniguchi, H., Kumagai, H., Kitaoka, M., and Yamamoto, K. (2008) 1,2-α-L-Fucosynthase: a glycosynthase derived from an inverting α-glycosidase with an unusual reaction mechanism. FEBS Lett. 582, 3739-3743
31. Nishimoto, M., and Kitaoka, M. (2007) Practical preparation of lacto-N-biose I, a candidate for the bifidus factor in human milk. Biosci. Biotechnol. Biochem. 71, 2101-2104 (Pubitemid 350113147)
32. Nishimoto, M., and Kitaoka, M. (2009) One-pot enzymatic production of β-D-galactopyranosyl-(1→3)-2-acetamido-2-deoxy-F-galactose (galacto-N-biose) from sucrose and 2-acetamido-2-deoxy-D-galactose (N-acetylgalactosamine). Carbohydr. Res. 344, 2573-2576
33. Honda, Y., Kitaoka, M., and Hayashi, K. (2004) Reaction mechanism of chitobiose phosphorylase from Vibrio proteolyticus: identification of family 36 glycosyltransferase in Vibrio. Biochem. J. 377, 225-232 (Pubitemid 38114449)
34. Cohenford, M. A., Abraham, A., Abraham, J., and Dain, J. A. (1989) Colorimetric assay for free and bound L-fucose. Anal. Biochem. 177, 172-177 (Pubitemid 19081742)
35. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
36. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025 (Pubitemid 127485985)
37. Sela, D. A., Garrido, D., Lerno, L., Wu, S., Tan, K., Eom, H. J., Joachimiak, A., Lebrilla, C. B., and Mills, D. A. (2012) Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl. Environ. Microbiol. 78, 795-803
38. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
39. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
40. Suzuki, R., Katayama, T., Kitaoka, M., Kumagai, H., Wakagi, T., Shoun, H., Ashida, H., Yamamoto, K., and Fushinobu, S. (2009) Crystallographic and mutational analyses of substrate recognition of endo-α-N- acetylgalactosaminidase from Bifidobacterium longum. J. Biochem. 146, 389-398
41. Bohne, A., Lang, E., and von der Lieth, C. W. (1999) SWEET-WWW-based rapid 3D construction of oligo- and polysaccharides. Bioinformatics 15, 767-768 (Pubitemid 29484341)
42. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19, 1639-1662 (Pubitemid 128590223)
43. McCarter, J. D., and Withers, S. G. (1994) Mechanisms of enzymatic glycoside hydrolysis. Curr. Opin. Struct. Biol. 4, 885-892
44. Sulzenbacher, G., Bignon, C., Nishimura, T., Tarling, C. A., Withers, S. G., Henrissat, B., and Bourne, Y. (2004) Crystal structure of Thermotoga maritima α-L-fucosidase. Insights into the catalytic mechanism and the molecular basis for fucosidosis. J. Biol. Chem. 279, 13119-13128 (Pubitemid 38445890)
45. Tarling, C. A., He, S., Sulzenbacher, G., Bignon, C., Bourne, Y., Henrissat, B., and Withers, S. G. (2003) Identification of the catalytic nucleophile of the family 29 α-L-fucosidase from Thermotoga maritima through trapping of a covalent glycosyl-enzyme intermediate and mutagenesis. J. Biol. Chem. 278, 47394-47399 (Pubitemid 37523179)
46. Sela, D. A., Chapman, J., Adeuya, A., Kim, J. H., Chen, F., Whitehead, T. R., Lapidus, A., Rokhsar, D. S., Lebrilla, C. B., German, J. B., Price, N. P., Richardson, P. M., and Mills, D. A. (2008) The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. U.S.A. 105, 18964-18969
47. Liu, S. W., Chen, C. S., Chang, S. S., Mong, K. K., Lin, C. H., Chang, C. W., Tang, C. Y., and Li, Y. K. (2009) Identification of essential residues of human α-L-fucosidase and tests of its mechanism. Biochemistry 48, 110-120
48. Rodríguez-Díaz, J., Monedero, V., and Yebra, M. J. (2011) Utilization of natural fucosylated oligosaccharides by three novel α-L-fucosidases from a probiotic Lactobacillus casei strain. Appl. Environ. Microbiol. 77, 703-705
49. Sano, M., Hayakawa, K., and Kato, I. (1992) Purification and characterization of α-L-fucosidase from Streptomyces species. J. Biol. Chem. 267, 1522-1527
50. Zeleny, R., Leonard, R., Dorfner, G., Dalik, T., Kolarich, D., and Altmann, F. (2006) Molecular cloning and characterization of a plant α1,3/4-fucosidase based on sequence tags from almond fucosidase I. Phytochemistry 67, 641-648
51. Fisher, K. J., and Aronson, N. N. Jr. (1989) Isolation and sequence analysis of a cDNA encoding rat liver α-L-fucosidase. Biochem. J. 264, 695-701 (Pubitemid 20023438)
52. ivalues in the micro- to picomolar range. Angew. Chem. Int. Ed. Engl. 49, 337-340
53. Yoshida, E., Sakurama, H., Kiyohara, M., Nakajima, M., Kitaoka, M., Ashida, H., Hirose, J., Katayama, T., Yamamoto, K., and Kumagai, H. (2012) Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology 22, 361-368
54. Asakuma, S., Hatakeyama, E., Urashima, T., Yoshida, E., Katayama, T., Yamamoto, K., Kumagai, H., Ashida, H., Hirose, J., and Kitaoka, M. (2011) Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. J. Biol. Chem. 286, 34583-34592
55. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425