2,105
Views
68
CrossRef citations to date
0
Altmetric
Award Review

Host-derived glycans serve as selected nutrients for the gut microbe: human milk oligosaccharides and bifidobacteriaFootnote

Pages 621-632 | Received 21 Oct 2015, Accepted 02 Dec 2015, Published online: 03 Feb 2016

References

  • Schloissnig S, Arumugam M, Sunagawa S, et al. Genomic variation landscape of the human gut microbiome. Nature. 2013;493:45–50.
  • Maslowski KM, Vieira AT, Ng A, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461:1282–1286.10.1038/nature08530
  • Furusawa Y, Obata Y, Fukuda S, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446–450.10.1038/nature12721
  • Tobisawa Y, Imai Y, Fukuda M, et al. Sulfation of colonic mucins by N-acetylglucosamine 6-O-sulfotransferase-2 and its protective function in experimental colitis in mice. J. Biol. Chem. 2010;285:6750–6760.10.1074/jbc.M109.067082
  • Hsiao EY, McBride SW, Hsien S, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013;155:1451–1463.10.1016/j.cell.2013.11.024
  • Nakayama J, Watanabe K, Jiang J, et al. Diversity in gut bacterial community of school-age children in Asia. Sci. Rep. 2015;5:8397.10.1038/srep08397
  • David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563.
  • Larsbrink J, Rogers TE, Hemsworth GR, et al. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature. 2014;506:498–502.10.1038/nature12907
  • Katayama T, Sakuma A, Kimura T, et al. Molecular cloning and characterization of Bifidobacterium bifidum 1,2-α-L-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J. Bacteriol. 2004;186:4885–4893.10.1128/JB.186.15.4885-4893.2004
  • Fujita K, Oura F, Nagamine N, et al. Identification and molecular cloning of a novel glycoside hydrolase family of core 1 type O-glycan-specific endo-α-N-acetylgalactosaminidase from Bifidobacterium longum. J. Biol. Chem. 2005;280:37415–37422.10.1074/jbc.M506874200
  • Katayama T, Fujita K, Yamamoto K. Novel bifidobacterial glycosidases acting on sugar chains of mucin glycoproteins. J. Biosci. Bioeng. 2005;99:457–465.10.1263/jbb.99.457
  • Lewis ZT, Totten SM, Smilowitz JT, et al. Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome. 2015;3:13.10.1186/s40168-015-0071-z
  • Mitsuoka T. Intestinal flora and host. Asian Med. J. 1988;31:400–409.
  • Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–227.
  • Sakata S, Tonooka T, Ishizeki S, et al. Culture-independent analysis of fecal microbiota in infants, with special reference to Bifidobacterium species. FEMS Microbiol. Lett. 2005;243:417–423.10.1016/j.femsle.2005.01.002
  • Penders J, Thijs C, Vink C, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511–521.10.1542/peds.2005-2824
  • Enomoto T, Sowa M, Nishimori K, et al. Effects of bifidobacterial supplementation to pregnant women and infants in the prevention of allergy development in infants and on fecal microbiota. Allergol. Int. 2014;63:575–585.10.2332/allergolint.13-OA-0683
  • Ishizuka S, Iwama A, Dinoto A, et al. Synbiotic promotion of epithelial proliferation by orally ingested encapsulated Bifidobacterium breve and raffinose in the small intestine of rats. Mol. Nutr. Food Res. 2009;53(S1):S62–S67.10.1002/mnfr.v53.5s
  • Groeger D, O’Mahony L, Murphy EF, et al. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes. 2013;4:325–339.10.4161/gmic.25487
  • György P, Norris RF, Rose CS. Bifidus factor. I. a variant of Lactobacillus bifidus requiring a special growth factor. Arch. Biochem. Biophys. 1954;48:193–201.10.1016/0003-9861(54)90323-9
  • György P, Kuhn R, Rose CS, et al. Bifidus factor. II. its occurrence in milk from different species and in other natural products. Arch. Biochem. Biophys. 1954;48:202–208.10.1016/0003-9861(54)90324-0
  • Gauhe A, György P, Hoover JR, et al. Bifidus factor. IV. preparations obtained from human milk. Arch. Biochem. Biophys. 1954;48:214–224.10.1016/0003-9861(54)90326-4
  • Glick MC, Sall T, Zilliken F, et al. Morphological changes of Lactobacillus bifidus var. pennsylvanicus produced by a cell-wall precursor. Biochim. Biophys. Acta. 1960;37:361–363.10.1016/0006-3002(60)90251-1
  • Asakuma S, Hatakeyama E, Urashima T, et al. Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. J. Biol. Chem. 2011;286:34583–34592.10.1074/jbc.M111.248138
  • Ruiz-Palacios GM, Cervantes LE, Ramos P, et al. Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J. Biol. Chem. 2003;278:14112–14120.10.1074/jbc.M207744200
  • Crane JK, Azar SS, Stam A, et al. Oligosaccharides from human milk block binding and activity of the Escherichia coli heat-stable enterotoxin (STa) in T84 intestinal cells. J. Nutr. 1994;124:2358–2364.
  • Hong P, Ninonuevo MR, Lee B, et al. Human milk oligosaccharides reduce HIV-1-gp120 binding to dendritic cell-specific ICAM3-grabbing non-integrin (DC-SIGN). Br. J. Nutr. 2009;101:482–486.
  • Jantscher-Krenn E, Zherebtsov M, Nissan C, et al. The human milk oligosaccharide disialyllacto-N-tetraose prevents necrotising enterocolitis in neonatal rats. Gut. 2012;61:1417–1425.10.1136/gutjnl-2011-301404
  • Urashima T, Kitaoka M, Terabayashi T, et al. Milk oligosaccharides. New York, NY: Nova Science Publishers; 2011. p. 1–93.
  • Ninonuevo MR, Park Y, Yin H, et al. A strategy for annotating the human milk glycome. J. Agric. Food Chem. 2006;54:7471–7480.10.1021/jf0615810
  • Kobata A. Structures and application of oligosaccharides in human milk. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2010;86:731–747.10.2183/pjab.86.731
  • Kunz C, Rudloff S, Baier W, et al. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu. Rev. Nutr. 2000;20:699–722.10.1146/annurev.nutr.20.1.699
  • Brand-Miller JC, McVeagh P, McNeil Y, et al. Digestion of human milk oligosaccharides by healthy infants evaluated by the lactulose hydrogen breath test. J. Pediatr. 1998;133:95–98.10.1016/S0022-3476(98)70185-4
  • Dotz V, Rudloff S, Meyer C, et al. Metabolic fate of neutral human milk oligosaccharides in exclusively breast-fed infants. Mol. Nutr. Food Res. 2015;59:355–364.10.1002/mnfr.201400160
  • Ruhaak LR, Stroble C, Underwood MA, et al. Detection of milk oligosaccharides in plasma of infants. Anal. Bioanal. Chem. 2014;406:5775–5784.10.1007/s00216-014-8025-z
  • He Y, Liu S, Kling DE, et al, The human milk oligosaccharide 2′-fucosyllactose modulates CD14 expression in human enterocytes, thereby attenuating LPS-induced inflammation, Gut 2016;65:33–46.
  • Tannock GW, Lawley B, Munro K, et al. Comparison of the compositions of the stool microbiotas of infants fed goat milk formula, cow milk-based formula, or breast milk, Appl. Environ. Microbiol. 2013;79:3040–3048.10.1128/AEM.03910-12
  • Derensy-Dron D, Krzewinski F, Brassart C, et al. Beta-1,3-galactosyl-N-acetylhexosamine phosphorylase from Bifidobacterium bifidum DSM 20082: characterization, partial purification and relation to mucin degradation. Biotechnol. Appl. Biochem. 1999;29(Pt 1):3–10.
  • Kitaoka M, Tian J, Nishimoto M. Novel putative galactose operon involving lacto-N-biose phosphorylase in Bifidobacterium longum. Appl. Environ. Microbiol. 2005;71:3158–3162.10.1128/AEM.71.6.3158-3162.2005
  • Wada J, Ando T, Kiyohara M, et al. Bifidobacterium bifidum Lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Appl. Environ. Microbiol. 2008;74:3996–4004.10.1128/AEM.00149-08
  • Sano M, Hayakawa K, Kato I. An enzyme releasing lacto-N-biose from oligosaccharides. Proc. Natl. Acad. Sci. USA. 1992;89:8512–8516.10.1073/pnas.89.18.8512
  • Henrissat B, Davies G. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 1997;7:637–644.10.1016/S0959-440X(97)80072-3
  • Mark BL, Mahuran DJ, Cherney MM, et al. Crystal structure of human β-hexosaminidase B: understanding the molecular basis of Sandhoff and Tay–Sachs disease. J. Mol. Biol. 2003;327:1093–1109.10.1016/S0022-2836(03)00216-X
  • Mark BL, Vocadlo DJ, Knapp S, et al. Crystallographic evidence for substrate-assisted catalysis in a bacterial β-hexosaminidase. J. Biol. Chem. 2001;276:10330–10337.10.1074/jbc.M011067200
  • Lemieux MJ, Mark BL, Cherney MM, et al. Crystallographic structure of human beta-hexosaminidase A: interpretation of Tay-Sachs mutations and loss of GM2 ganglioside hydrolysis. J. Mol. Biol. 2006;359:913–929.10.1016/j.jmb.2006.04.004
  • Ito T, Katayama T, Hattie M, et al. Crystal structures of a glycoside hydrolase family 20 lacto-N-biosidase from Bifidobacterium bifidum. J. Biol. Chem. 2013;288:11795–11806.10.1074/jbc.M112.420109
  • Hattie M, Ito T, Debowski AW, et al. Gaining insight into the catalysis by GH20 lacto-N-biosidase using small molecule inhibitors and structural analysis. Chem. Commun. (Camb). 2015;51:15008–15011.10.1039/C5CC05494J
  • Fukuda S, Toh H, Taylor TD, et al. Acetate-producing bifidobacteria protect the host from enteropathogenic infection via carbohydrate transporters. Gut Microbes. 2012;3:449–454.10.4161/gmic.21214
  • Honda Y, Nishimoto M, Katayama T, et al, Characterization of the cytosolic β-N-acetylglucosaminidase from bifidobacterium longum subsp. longum. J. Appl. Glycosci, 60, 141–146 (2013).10.5458/jag.jag.JAG-2013_001
  • Sakurama H, Kiyohara M, Wada J, et al. 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. 2013;288:25194–25206.10.1074/jbc.M113.484733
  • Gotoh A, Katoh T, Sugiyama Y, et al. Novel substrate specificities of two lacto-N-biosidases towards beta-linked galacto-N-biose-containing oligosaccharides of globo H, Gb5, and GA1. Carbohydr. Res. 2015;408:18–24.10.1016/j.carres.2015.03.005
  • Altschul SF, Gish W, Miller W, et al. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410.10.1016/S0022-2836(05)80360-2
  • Suzuki R, Wada J, Katayama T, et al. Structural and thermodynamic analyses of solute-binding protein from Bifidobacterium longum specific for core 1 disaccharide and lacto-N-biose I. J. Biol. Chem. 2008;283:13165–13173.10.1074/jbc.M709777200
  • Tam R, Saier MH Jr. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 1993;57:320–346.
  • Sela DA, Chapman J, Adeuya A, et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. USA. 2008;105:18964–18969.10.1073/pnas.0809584105
  • Yoshida E, Sakurama H, Kiyohara M, et al. Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology. 2012;22:361–368.10.1093/glycob/cwr116
  • Viborg AH, Fredslund F, Katayama T, et al, A beta1-6/beta1-3 galactosidase from Bifidobacterium animalis subsp. lactis Bl-04 gives insight into sub-specificities of beta-galactoside catabolism within Bifidobacterium, Mol. Microbiol 2014;94:1024–1040.
  • Viborg AH, Katayama T, Abou Hachem M, et al. Distinct substrate specificities of three glycoside hydrolase family 42 beta-galactosidases from Bifidobacterium longum subsp. infantis ATCC 15697. Glycobiology. 2014;24:208–216.10.1093/glycob/cwt104
  • Nagae M, Tsuchiya A, Katayama T, et al. Structural basis of the catalytic reaction mechanism of novel 1,2-α-L-fucosidase from Bifidobacterium bifidum. J. Biol. Chem. 2007;282:18497–18509.10.1074/jbc.M702246200
  • Wada J, Honda Y, Nagae M, et al. 1,2-alpha-l-Fucosynthase: a glycosynthase derived from an inverting alpha-glycosidase with an unusual reaction mechanism. FEBS Lett. 2008;582:3739–3743.10.1016/j.febslet.2008.09.054
  • Ashida H, Miyake A, Kiyohara M, et al. Two distinct α-L-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology. 2009;19:1010–1017.10.1093/glycob/cwp082
  • Sakurama H, Fushinobu S, Hidaka M, et al. 1,3-1,4-α-L-fucosynthase that specifically introduces Lewis a/x antigens into type-1/2 chains. J. Biol. Chem. 2012;287:16709–16719.10.1074/jbc.M111.333781
  • Sakurama H, Tsutsumi E, Ashida H, et al. Differences in the substrate specificities and active-site structures of two α-L-fucosidases (glycoside hydrolase family 29) from bacteroides thetaiotaomicron. Biosci. Biotechnol. Biochem. 2012;76:1022–1024.10.1271/bbb.111004
  • Rodriguez-Diaz J, Rubio-del-Campo A, Yebra MJ. Lactobacillus casei ferments the N-Acetylglucosamine moiety of fucosyl-alpha-1,3-N-acetylglucosamine and excretes L-fucose. Appl. Environ. Microbiol. 2012;78:4613–4619.10.1128/AEM.00474-12
  • Kitaoka M. Bifidobacterial enzymes involved in the metabolism of human milk oligosaccharides. Adv. Nutr. 2012;3:422S–429S.10.3945/an.111.001420
  • Odamaki T, Horigome A, Sugahara H, et al. Comparative genomics revealed genetic diversity and species/strain-level differences in carbohydrate metabolism of three probiotic bifidobacterial species. Int. J. Genomics. 2015:567809.
  • Ward RE, Niñonuevo M, Mills DA, et al. In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria. Mol. Nutr. Food Res. 2007;51:1398–1405.10.1002/(ISSN)1613-4133
  • LoCascio RG, Ninonuevo MR, Freeman SL, et al. Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J. Agric. Food Chem. 2007;55:8914–8919.10.1021/jf0710480
  • Marcobal A, Barboza M, Froehlich JW, et al. Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food Chem. 2010;58:5334–5340.10.1021/jf9044205
  • Garrido D, Kim JH, German JB, et al. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One. 2011;6:e17315.10.1371/journal.pone.0017315
  • Kiyohara M, Tachizawa A, Nishimoto M, et al. Prebiotic effect of lacto-N-biose I on bifidobacterial growth. Biosci. Biotechnol. Biochem. 2009;73:1175–1179.10.1271/bbb.80697
  • Xiao JZ, Takahashi S, Nishimoto M, et al. Distribution of in vitro fermentation ability of lacto-N-biose I, a major building block of human milk oligosaccharides, in bifidobacterial strains. Appl. Environ. Microbiol. 2010;76:54–59.10.1128/AEM.01683-09
  • Miwa M, Horimoto T, Kiyohara M, et al. Cooperation of β-galactosidase and β-N-acetylhexosaminidase from bifidobacteria in assimilation of human milk oligosaccharides with type 2 structure. Glycobiology. 2010;20:1402–1409.10.1093/glycob/cwq101
  • Albrecht S, Schols HA, van den Heuvel EG, et al. Occurrence of oligosaccharides in feces of breast-fed babies in their first six months of life and the corresponding breast milk. Carbohydr. Res. 2011;346:2540–2550.10.1016/j.carres.2011.08.009
  • De Leoz ML, Kalanetra KM, Bokulich NA, et al. Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota: a proof-of-concept study. J. Proteome Res. 2015;14:491–502.10.1021/pr500759e
  • Urashima T, Inamori H, Fukuda K, et al. 4-O-Acetyl-sialic acid (Neu4,5Ac2) in acidic milk oligosaccharides of the platypus (Ornithorhynchus anatinus) and its evolutionary significance. Glycobiology. 2015;25:683–697.10.1093/glycob/cwv010
  • Larkin MA, Blackshields G, Brown NP, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–2948.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.