Introduction of H-antigens into oligosaccharides and sugar chains of glycoproteins using highly efficient 1,2-α-L-fucosynthase

Glycobiology

Volumn 26, Issue 11, 2016, Pages 1235-1247

  Sugiyama, Yuta ^a   Gotoh, Aina ^a,b   Katoh, Toshihiko ^a,b   Honda, Yuji ^a   Yoshida, Erina ^a   Kurihara, Shin ^a   Ashida, Hisashi ^c   Kumagai, Hidehiko ^a   Yamamoto, Kenji ^a   Kitaoka, Motomitsu ^d   Katayama, Takane ^a,b  

^a ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KINKI UNIVERSITY   (Japan)

^d FOOD RESEARCH INSTITUTE   (Japan)

Author keywords

Glycoprotein; Glycosylation; Glycosynthase; H antigen; Oligosaccharide

Indexed keywords

1,2 ALPHA LEVO FUCOSIDASE; 1,2 ALPHA LEVO FUCOSYNTHASE; ALPHA LEVO FUCOSIDASE; BLOOD GROUP H ANTIGEN; CARBOHYDRATE DERIVATIVE; GLYCOPROTEIN; MONOSACCHARIDE; OLIGOSACCHARIDE; STOMACH MUCIN; SUGAR; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; CARBOHYDRATE; H ANTIGEN;

ARTICLE; CARBOHYDRATE ANALYSIS; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY; BIFIDOBACTERIUM BIFIDUM; BIOCATALYSIS; CHEMISTRY; CONFORMATION; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL;

ALPHA-L-FUCOSIDASE; ANTIGENS, BACTERIAL; BIFIDOBACTERIUM BIFIDUM; BIOCATALYSIS; CARBOHYDRATE CONFORMATION; GLYCOPROTEINS; MODELS, MOLECULAR; OLIGOSACCHARIDES; SUGARS;

EID: 85016155323     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cww085     Document Type: Article

References (56)

1. Anderson K, Li SC, Li YT. 2000. Diphenylamine-aniline-phosphoric acid reagent, a versatile spray reagent for revealing glycoconjugates on thin-layer chromatography plates. Anal Biochem. 287:337-339.
2. Angyal SJ, Pickles V. 1972. Equilibria between pyranoses and furanoses. II. Aldoses. Aust J Chem. 25:1695-1710.
3. Anumula KR, Taylor PB. 1992. A comprehensive procedure for preparation of partially methylated alditol acetates from glycoprotein carbohydrates. Anal Biochem. 203:101-108.
4. Aoki K, PorterfieldM, Lee SS, Dong B, Nguyen K, McGlamry KH, Tiemeyer M. 2008. The diversity of O-linked glycans expressed during Drosophila melanogaster development reflects stage-and tissue-specific requirements for cell signaling. J BiolChem. 283:30385-30400.
5. Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, Yamamoto K, Kumagai H, Ashida H, Hirose J, Kitaoka M. 2011. Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. J Biol Chem. 286:34583-34592.
6. Ashida H, Miyake A, Kiyohara M, Wada J, Yoshida E, Kumagai H, Katayama T, Yamamoto K. 2009. Two distinct alpha-L-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology. 19:1010-1017.
7. Baumgartner F, Seitz L, Sprenger GA, Albermann C. 2013. Construction of Escherichia coli strains with chromosomally integrated expression cassettes for the synthesis of 2'-fucosyllactose. Microb Cell Fact. 12:40.
8. Brand-Miller JC, McVeagh P, McNeil Y, Messer M. 1998. Digestion of human milk oligosaccharides by healthy infants evaluated by the lactulose hydrogen breath test. J Pediatr. 133:95-98.
9. Bry L, Falk PG, Midtvedt T, Gordon JI. 1996. A model of host-microbial interactions in an open mammalian ecosystem. Science. 273:1380-1383.
10. Ceroni A, Maass K, Geyer H, Geyer R, Dell A, Haslam SM. 2008. GlycoWorkbench: A tool for the computer-assisted annotation of mass spectra of glycans. J Proteome Res. 7:1650-1659.
11. Drouillard S, Driguez H, Samain E. 2006. Large-scale synthesis of H-antigen oligosaccharides by expressing Helicobacter pylori alpha1, 2-fucosyltransferase in metabolically engineered Escherichia coli cells. Angew Chem Int Ed Engl. 45:1778-1780.
12. Goto Y, Obata T, Kunisawa J, Sato S, Ivanov II, Lamichhane A, Takeyama N, Kamioka M, Sakamoto M, Matsuki T, et al. 2014. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science. 345:1254009.
13. Gotoh A, Katoh T, Sugiyama Y, Kurihara S, Honda Y, Sakurama H, Kambe T, Ashida H, KitaokaM, Yamamoto K, et al. 2015. Novel substrate specificities of two lacto-N-biosidases towards beta-linked galacto-N-biose-containing oligosaccharides of globo H, Gb5, and GA1. Carbohydr Res. 408:18-24.
14. Hakomori S. 1999. Antigen structure and genetic basis of histo-blood groups A, B and O: Their changes associated with human cancer. Biochim Biophys Acta. 1473:247-266.
15. He Y, Liu S, Kling DE, Leone S, Lawlor NT, Huang Y, Feinberg SB, Hill DR, Newburg DS. 2016. The human milk oligosaccharide 2'-fucosyllactose modulates CD14 expression in human enterocytes, thereby attenuating LPS-induced inflammation. Gut. 65:33-46.
16. Hehre EJ, Brewer CF, Genghof DS. 1979. Scope and mechanism of carbohydrase action. Hydrolytic and nonhydrolytic actions of beta-amylase on alpha-and beta-maltosyl fluoride. J Biol Chem. 254:5942-5950.
17. Heimburg-Molinaro J, Lum M, Vijay G, Jain M, Almogren A, Rittenhouse-Olson K. 2011. Cancer vaccines and carbohydrate epitopes. Vaccine. 29:8802-8826.
18. Helland R, Larsen RL, Finstad S, Kyomuhendo P, Larsen AN. 2009. Crystal structures of g-type lysozyme from Atlantic cod shed new light on substrate binding and the catalytic mechanism. Cell Mol Life Sci. 66: 2585-2598.
19. Hidaka M, Fushinobu S, Honda Y, Wakagi T, Shoun H, Kitaoka M. 2010. Structural explanation for the acquisition of glycosynthase activity. J Biochem. 147:237-244.
20. Honda Y, Arai S, Suzuki K, Kitaoka M, Fushinobu S. 2016. The crystal structure of an inverting glycoside hydrolase family 9 exo-beta-D-glucosaminidase and the design of glycosynthase. Biochem J. 473:463-472.
21. Honda Y, Kitaoka M. 2006. The first glycosynthase derived from an inverting glycoside hydrolase. J Biol Chem. 281:1426-1431.
22. Karlsson NG, Herrmann A, Karlsson H, Johansson ME, Carlstedt I, Hansson GC. 1997. The glycosylation of rat intestinal Muc2 mucin varies between rat strains and the small and large intestine. A study of O-linked oligosaccharides by a mass spectrometric approach. J Biol Chem. 272: 27025-27034.
23. Katayama T. 2016. Host-derived glycans serve as selected nutrients for the gut microbe: Human milk oligosaccharides and bifidobacteria. Biosci Biotechnol Biochem. 80:621-632.
24. Katayama T, Sakuma A, Kimura T, Makimura Y, Hiratake J, Sakata K, Yamanoi T, Kumagai H, Yamamoto K. 2004. Molecular cloning and characterization of Bifidobacterium bifidum 1, 2-alpha-L-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J Bacteriol. 186:4885-4893.
25. Kitaoka M, Tian J, Nishimoto M. 2005. Novel putative galactose operon involving lacto-N-biose phosphorylase in Bifidobacterium longum. Appl Environ Microbiol. 71:3158-3162.
26. Kobata A. 2010. Structures and application of oligosaccharides in human milk. Proc Jpn Acad Ser B Phys Biol Sci. 86:731-747.
27. Kunz C, Rudloff S, Baier W, Klein N, Strobel S. 2000. Oligosaccharides in human milk: Structural, functional, and metabolic aspects. Annu Rev Nutr. 20:699-722.
28. Lewis ZT, Totten SM, Smilowitz JT, Popovic M, Parker E, Lemay DG, Van Tassell ML, Miller MJ, Jin YS, German JB, et al. 2015. Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome. 3:13.
29. Liu J, Zheng M, Zhang C, Xu D. 2013. "Amide resonance" in the catalysis of 1, 2-alpha-L-fucosidase from Bifidobacterium bifidum. J Phys Chem B. 117:10080-10092.
30. Mackenzie LF, Wang Q, Warren RAJ, Withers SG. 1998. Glycosynthases: Mutant Glycosidases for Oligosaccharide Synthesis. J. Am. Chem. Soc. 120:5583-5584.
31. Malet C, Planas A. 1998. From beta-glucanase to beta-glucansynthase: Glycosyl transfer to alpha-glycosyl fluorides catalyzed by a mutant endoglucanase lacking its catalytic nucleophile. FEBS Lett. 440: 208-212.
32. McGovern DP, Jones MR, Taylor KD, Marciante K, Yan X, Dubinsky M, Ippoliti A, Vasiliauskas E, Berel D, Derkowski C, et al. 2010. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet. 19:3468-3476.
33. Mollicone R, Candelier JJ, Reguigne I, Couillin P, Fletcher A, Oriol R. 1994. Molecular genetics of alpha-L-fucosyltransferase genes (H, Se, Le, FUT4, FUT5 and FUT6). Transfus Clin Biol. 1:91-97.
34. Nagae M, Tsuchiya A, Katayama T, Yamamoto K, Wakatsuki S, Kato R. 2007. Structural basis of the catalytic reaction mechanism of novel 1, 2-alpha-L-fucosidase from Bifidobacterium bifidum. J Biol Chem. 282: 18497-18509.
35. Nakajima M, Nishimoto M, Kitaoka M. 2010. Practical preparation of D-galactosyl-beta1→4-L-rhamnose employing the combined action of phosphorylases. Biosci Biotechnol Biochem. 74:1652-1655.
36. Nishimoto M, 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.
37. Nishimoto M, Kitaoka M. 2009. One-pot enzymatic production of beta-D-galactopyranosyl-(1→3)-2-acetamido-2-deoxy-D-galactose (galacto-N-biose) from sucrose and 2-acetamido-2-deoxy-D-galactose (N-acetylgalactosamine). Carbohydr Res. 344:2573-2576.
38. Ohnuma T, Fukuda T, Dozen S, Honda Y, Kitaoka M, Fukamizo T. 2012. A glycosynthase derived from an inverting GH19 chitinase from the moss Bryum coronatum. Biochem J. 444:437-443.
39. Osanjo G, Dion M, Drone J, Solleux C, Tran V, Rabiller C, Tellier C. 2007. Directed evolution of the alpha-L-fucosidase from Thermotoga maritima into an alpha-L-transfucosidase. Biochemistry. 46:1022-1033.
40. Pacheco AR, Curtis MM, Ritchie JM, Munera D, Waldor MK, Moreira CG, Sperandio V. 2012. Fucose sensing regulates bacterial intestinal colonization. Nature. 492:113-117.
41. Pham TA, Clare S, Goulding D, Arasteh JM, Stares MD, Browne HP, Keane JA, Page AJ, Kumasaka N, Kane L, et al. 2014. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe. 16:504-516.
42. Pickard JM, Maurice CF, Kinnebrew MA, Abt MC, Schenten D, Golovkina TV, Bogatyrev SR, Ismagilov RF, Pamer EG, Turnbaugh PJ, et al. 2014. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature. 514:638-641.
43. Rouquier S, Lowe JB, Kelly RJ, Fertitta AL, Lennon GG, Giorgi D. 1995. Molecular cloning of a human genomic region containing the H blood group alpha(1, 2)fucosyltransferase gene and two H locus-related DNA restriction fragments. Isolation of a candidate for the human Secretor blood group locus. J Biol Chem. 270:4632-4639.
44. Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS. 2003. Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2 Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem. 278: 14112-14120.
45. Sakurama H, Fushinobu S, Hidaka M, Yoshida E, Honda Y, Ashida H, Kitaoka M, Kumagai H, Yamamoto K, Katayama T. 2012. 1, 3-1, 4-alpha-L-fucosynthase that specifically introduces Lewis a/x antigens into type-1/2 chains. J Biol Chem. 287:16709-16719.
46. Sakurama H, Kiyohara M, Wada J, Honda Y, Yamaguchi M, Fukiya S, Yokota A, Ashida H, Kumagai H, Kitaoka M, et al. 2013. Lacto-N-biosidase encoded by a novel gene of Bifidobacterium longum subspecies longum shows unique substrate specificity and requires a designated chaperone for its active expression. J Biol Chem. 288: 25194-25206.
47. Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebrilla CB, German JB, et al. 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.
48. Shaikh FA, Withers SG. 2008. Teaching old enzymes new tricks: Engineering and evolution of glycosidases and glycosyl transferases for improved glycoside synthesis. Biochem Cell Biol. 86:169-177.
49. Smyth DJ, Cooper JD, Howson JM, Clarke P, Downes K, Mistry T, Stevens H, Walker NM, Todd JA. 2011. FUT2 nonsecretor status links type 1 diabetes susceptibility and resistance to infection. Diabetes. 60: 3081-3084.
50. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, et al. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A. 101:6062-6067.
51. Tateno H, Matsushima A, Hiemori K, Onuma Y, Ito Y, Hasehira K, Nishimura K, Ohtaka M, Takayasu S, Nakanishi M, et al. 2013. Podocalyxin is a glycoprotein ligand of the human pluripotent stem cell-specific probe rBC2LCN. Stem Cells Transl Med. 2:265-273.
52. Urashima T, Asakuma S, Leo F, Fukuda K, Messer M, Oftedal OT. 2012. The predominance of type I oligosaccharides is a feature specific to human breast milk. Adv Nutr. 3:473S-482S.
53. Vasiliu D, Razi N, Zhang Y, Jacobsen N, Allin K, Liu X, Hoffmann J, Bohorov O, Blixt O. 2006. Large-scale chemoenzymatic synthesis of blood group and tumor-associated poly-N-acetyllactosamine antigens. Carbohydr Res. 341:1447-1457.
54. Wada J, Ando T, Kiyohara M, Ashida H, Kitaoka M, Yamaguchi M, Kumagai H, Katayama T, Yamamoto K. 2008a. Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Appl Environ Microbiol. 74: 3996-4004.
55. Wada J, Honda Y, Nagae M, Kato R, Wakatsuki S, Katayama T, Taniguchi H, Kumagai H, Kitaoka M, Yamamoto K. 2008b. 1, 2-alpha-l-Fucosynthase: A glycosynthase derived from an inverting alpha-glycosidase with an unusual reaction mechanism. FEBS Lett. 582:3739-3743.
56. Zhao C, Wu Y, Yu H, Shah IM, Li Y, Zeng J, Liu B, Mills DA, Chen X. 2016. The one-pot multienzyme (OPME) synthesis of human blood group H antigens and a human milk oligosaccharide (HMOS) with highly active Thermosynechococcus elongates alpha1-2-fucosyltransferase. Chem Commun (Camb). 52:3899-3902.