Bifidobacterial a-galactosidase with unique carbohydrate-binding module specifically acts on blood group B antigen

Glycobiology

Volumn 23, Issue 2, 2013, Pages 232-240

  Wakinaka, Takura ^a   Kiyohara, Masashi ^a   Kurihara, Shin ^a   Hirata, Akiko ^a   Chaiwangsri, Thida ^b   Ohnuma, Takayuki ^c   Fukamizo, Tamo ^c   Katayama, Takane ^d   Ashida, Hisashi ^c   Yamamoto, Kenji ^d  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF PHAYAO   (Thailand)

^c KINKI UNIVERSITY   (Japan)

^d ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

Author keywords

Bifidobacterium bifidum blood group antigen a galactosidase glycosidase probiotics

Indexed keywords

ALPHA GALACTOSIDASE; BLOOD GROUP B ANTIGEN; CARBOHYDRATE; MUCIN; OLIGOSACCHARIDE; RECOMBINANT ENZYME; BETA GALACTOSIDASE; BLOOD GROUP ANTIGEN; CELL SURFACE RECEPTOR; POLYSACCHARIDE; SACCHARIDE BINDING PROTEINS; SACCHARIDE-BINDING PROTEINS;

ARTICLE; BACTERIAL GENE; BIFIDOBACTERIACEAE; BINDING ASSAY; ENZYME SUBSTRATE; ERYTHROCYTE; ESCHERICHIA COLI; HYDROLYSIS; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SALIVA ANALYSIS; SOLID; XENOTRANSPLANTATION; BIFIDOBACTERIUM; BLOOD GROUP ABO SYSTEM; BREAST MILK; CHEMISTRY; ENZYMOLOGY; GENETICS; HUMAN; INFANT; INTESTINE; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; NEWBORN;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM LONGUM; ESCHERICHIA COLI;

ABO BLOOD-GROUP SYSTEM; ALPHA-GALACTOSIDASE; BETA-GALACTOSIDASE; BIFIDOBACTERIUM; BLOOD GROUP ANTIGENS; ESCHERICHIA COLI; HUMANS; INFANT; INFANT, NEWBORN; INTESTINES; MILK, HUMAN; MUCINS; POLYSACCHARIDES; RECEPTORS, CELL SURFACE;

EID: 84871983808     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cws142     Document Type: Article

References (36)

1. Anderson KM, Ashida H, Maskos K, Dell A, Li SC, Li YT. 2005. A clostridial endo-β-galactosidase that cleaves both blood group A and B glycotopes: The first member of a new glycoside hydrolase family, GH98. J Biol Chem. 280: 7720-7728.
2. Anderson K, Li SC, Li YT. 2000. Diphenylamine-aniline-phosphoric acid reagent, a versatile spray reagent for revealing glycoconjugates on thinlayer chromatography plates. Anal Biochem. 287: 337-339.
3. 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.
4. Ashida H, Maki R, Ozawa H, Tani Y, Kiyohara M, Fujita M, Imamura A, Ishida H, Kiso M, Yamamoto K. 2008. Characterization of two different endo-α-N-acetylgalactosaminidases from probiotic and pathogenic enterobacteria, Bifidobacterium longum and Clostridium perfringens. Glycobiology. 18: 727-734.
5. Ashida H, Miyake A, Kiyohara M, Wada J, Yoshida E, Kumagai H, Katayama T, 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.
6. Benno Y, Sawada K, Mitsuoka T. 1984. The intestinal microflora of infants: Composition of fecal flora in breast-fed and bottle-fed infants. Microbiol Immunol. 28: 975-986.
7. Clausen H, Hakomori S. 1989. ABH and related histo-blood group antigens; immunochemical differences in carrier isotypes and their distribution. Vox Sang. 56: 1-20.
8. Fujita K, Oura F, Nagamine N, Katayama T, Hiratake J, Sakata K, Kumagai H, Yamamoto K. 2005. Identification and molecular cloning of a novel glycoside hydrolase family of core 1 type O-glycan-specific endo-α- Nacetylgalactosaminidase from Bifidobacterium longum. J Biol Chem. 280: 37415-37422.
9. Fujita M, Tsuchida A, Hirata A, Kobayashi N, Goto K, Osumi K, Hirose Y, Nakayama J, Yamanoi T, Ashida H, Mizuno M. 2011. Glycoside hydrolase family 89 α-N-acetylglucosaminidase from Clostridium perfringens specifically acts on GlcNAcα1,4Galβ1R at the non-reducing terminus of O-glycans in gastric mucin. J Biol Chem. 286: 6479-6489.
10. Goldstein J, Siviglia G, Hurst R, Lenny L, Reich L. 1982. Group B erythrocytes enzymatically converted to group O survive normally in A, B, and O individuals. Science. 215: 168-170.
11. Gregg KJ, Finn R, Abbott DW, Boraston AB. 2008. Divergent modes of glycan recognition by a new family of carbohydrate-binding modules. J Biol Chem. 283: 12604-12613.
12. Guillen D, Sanchez S, Rodriguez-Sanoja R. 2010. Carbohydrate-binding domains: Multiplicity of biological roles. Appl Microbiol Biotechnol. 85: 1241-1249.
13. Higgins MA, Ficko-Blean E, Meloncelli PJ, Lowary TL, Boraston AB. 2011. The overall architecture and receptor binding of pneumococcal carbohydrate-antigen-hydrolyzing enzymes. J Mol Biol. 411: 1017-1036.
14. Hoskins LC, Boulding ET. 1976. Degradation of blood group antigens in human colon ecosystems. I. In vitro production of ABH blood groupdegrading enzymes by enteric bacteria. J Clin Invest. 57: 63-73.
15. 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-α-l-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J Bacteriol. 186: 4885-4893.
16. 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.
17. Kiyohara M, Nakatomi T, Kurihara S, Fushinobu S, Suzuki H, Tanaka T, Shoda S, Kitaoka M, Katayama T, Yamamoto K, Ashida H. 2012. α-N- acetylgalactosaminidase from infant-associated bifidobacteria belonging to novel glycoside hydrolase family 129 is implicated in alternative mucin degradation pathway. J Biol Chem. 287: 693-700.
18. Kiyohara M, Tachizawa A, Nishimoto M, Kitaoka M, Ashida H, Yamamoto K. 2009. Prebiotic effect of lacto-N-biose I on bifidobacterial growth. Biosci Biotechnol Biochem. 73: 1175-1179.
19. Kiyohara M, Tanigawa K, Chaiwangsri T, Katayama T, Ashida H, Yamamoto K. 2011. An exo-α-sialidase from bifidobacteria involved in the degradation of sialyloligosaccharides in human milk and intestinal glycoconjugates. Glycobiology. 21: 437-447.
20. Liu QP, Sulzenbacher G, Yuan H, Bennett EP, Pietz G, Saunders K, Spence J, Nudelman E, Levery SB, White T, Neveu JM, Lane WS, Bourne Y, Olsson ML, Henrissat B, Clausen H. 2007. Bacterial glycosidases for the production of universal red blood cells. Nat Biotechnol. 25: 454-464.
21. Liu QP, Yuan H, Bennett EP, Levery SB, Nudelman E, Spence J, Pietz G, Saunders K, White T, Olsson ML, Henrissat B, Sulzenbacher G, Clausen H. 2008. Identification of a GH110 subfamily of α1,3-galactosidases: Novel enzymes for removal of the α3Gal xenotransplantation antigen. J Biol Chem. 283: 8545-8554.
22. Miwa M, Horimoto T, Kiyohara M, Katayama T, Kitaoka M, Ashida H, Yamamoto K. 2010. Cooperation of β-galactosidase and β-N-acetylhexosaminidase from bifidobacteria in assimilation of human milk oligosaccharides with type 2 structure. Glycobiology. 20: 1402-1409.
23. Olsson ML, Clausen H. 2008. Modifying the red cell surface: Towards an ABO-universal blood supply. Br J Haematol. 140: 3-12.
24. Olsson ML, Hill CA, de la Vega H, Liu QP, Stroud MR, Valdinocci J, Moon S, Clausen H, Kruskall MS. 2004. Universal red blood cells-enzymatic conversion of blood group A and B antigens. Transfus Clin Biol. 11: 33-39.
25. Picard C, Fioramonti J, Francois A, Robinson T, Neant F, Matuchansky C. 2005. Review article: Bifidobacteria as probiotic agents-physiological effects and clinical benefits. Aliment Pharmacol Ther. 22: 495-512.
26. Saitou N, Yamamoto F. 1997. Evolution of primate ABO blood group genes and their homologous genes. Mol Biol Evol. 14: 399-411.
27. Shoseyov O, Shani Z, Levy I. 2006. Carbohydrate binding modules: Biochemical properties and novel applications. Microbiol Mol Biol Rev. 70: 283-295.
28. Suzuki R, Katayama T, Kim BJ, Wakagi T, Shoun H, Ashida H, Yamamoto K, Fushinobu S. 2010. Crystal structures of phosphoketolase: Thiamine diphosphate-dependent dehydration mechanism. J Biol Chem. 285: 34279-34287.
29. Suzuki R, Wada J, Katayama T, Fushinobu S, Wakagi T, Shoun H, Sugimoto H, Tanaka A, Kumagai H, Ashida H, Kitaoka M, Yamamoto K. 2008. Structural and thermodynamic analyses of solute-binding protein from Bifidobacterium longum specific for core 1 disaccharide and lacto-N-biose I. J Biol Chem. 283: 13165-13173.
30. Trebichavsky I, Rada V, Splichalova A, Splichal I. 2009. Cross-talk of human gut with bifidobacteria. Nutr Rev. 67: 77-82.
31. Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A, Sanchez B, Bidossi A, Ferrarini A, Giubellini V, Delledonne M, Henrissat B, Coutinho P, Oggioni M, Fitzgerald GF, Mills D, Margolles A, Kelly D, van Sinderen D, Ventura M. 2010. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci USA. 107: 19514-19519.
32. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, Gueimonde M, Margolles A, De Bellis G, O'Toole PW, van Sinderen D, Marchesi JR, Ventura M. 2012. Diversity of Bifidobacteria within the Infant Gut Microbiota. PLoS One. 7: e36957.
33. Wacklin P, Makivuokko H, Alakulppi N, Nikkila J, Tenkanen H, Rabina J, Partanen J, Aranko K, Matto J. 2011. Secretor genotype (FUT2 gene) is strongly associated with the composition of bifidobacteria in the human intestine. PLoS One. 6: e20113.
34. Wada J, Ando T, Kiyohara M, Ashida H, Kitaoka M, Yamaguchi M, Kumagai H, Katayama T, Yamamoto K. 2008. 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.
35. Yamamoto F, Clausen H, White T, Marken J, Hakomori S. 1990. Molecular genetic basis of the histo-blood group ABO system. Nature. 345: 229-233.
36. Yoshida E, Sakurama H, Kiyohara M, Nakajima M, Kitaoka M, Ashida H, Hirose J, Katayama T, Yamamoto K, 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.