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Analysis and role of oligosaccharides in milk

  • Ruhaak, L. Renee ;
  • Lebrilla, Carlito B.
  • Received : 2012.07.30
  • Published : 2012.08.31

Abstract

Milk is an important fluid in glycobiology because it contains a number of short carbohydrate chains either free or as glycoconjugates. These compounds as a class are the most abundant component and benefit the infant by developing and maintaining the infant's gut flora. New and emerging methods for oligosaccharide analysis have been developed to study milk. These methods allow for the rapid profiling of oligosaccharide mixtures with quantitation. With these tools, the role of oligosaccharide in milk is being understood. They further point to how oligosaccharide analysis can be performed, which until now has been very difficult and have lagged significantly those of other biopolymers.

Keywords

Analysis;Bacterial consumption;High performance liquid chromatography;Lewis blood group;Mass spectrometry;Milk oligosaccharides;Secretor status

References

  1. Viverge, D., Grimmonprez, L., Cassanas, G., Bardet, L. and Solere, M. (1990) Variations in oligosaccharides and lactose in human milk during the first week of lactation. J. Pediatr. Gastroenterol. Nutr. 11, 361-364. https://doi.org/10.1097/00005176-199010000-00013
  2. Coppa, G. V., Gabrielli, O., Pierani, P., Catassi, C., Carlucci, A. and Giorgi, P. L. (1993) Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics 91, 637-641.
  3. Kunz, C., Rudloff, S., Baier, W., Klein, N. and Strobel, S. (2000) Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu. Rev. Nutr. 20, 699-722. https://doi.org/10.1146/annurev.nutr.20.1.699
  4. Wu, S., Grimm, R., German, J. B. and Lebrilla, C. B. (2011) Annotation and structural analysis of sialylated human milk oligosaccharides. J. Proteome Res. 10, 856-868. https://doi.org/10.1021/pr101006u
  5. Wu, S., Tao, N., German, J. B., Grimm, R. and Lebrilla, C. B. (2010) Development of an annotated library of neutral human milk oligosaccharides. J. Proteome Res. 9, 4138-4151. https://doi.org/10.1021/pr100362f
  6. Kobata, A. (2010) Structures and application of oligosaccharides in human milk. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 86, 731-747. https://doi.org/10.2183/pjab.86.731
  7. Marino, K., Lane, J. A., Abrahams, J. L., Struwe, W. B., Harvey, D. J., Marotta, M., Hickey, R. M. and Rudd, P. M. (2011) Method for milk oligosaccharide profiling by 2-aminobenzamide labeling and hydrophilic interaction chromatography. Glycobiology 21, 1317-1330. https://doi.org/10.1093/glycob/cwr067
  8. Thurl, S., Henker, J., Siegel, M., Tovar, K. and Sawatzki, G. (1997) Detection of four human milk groups with respect to Lewis blood group dependent oligosaccharides. Glycoconj. J. 14, 795-799. https://doi.org/10.1023/A:1018529703106
  9. Blank, D., Gebhardt, S., Maass, K., Lochnit, G., Dotz, V., Blank, J., Geyer, R. and Kunz, C. (2011) High-throughput mass finger printing and Lewis blood group assignment of human milk oligosaccharides. Anal. Bioanal. Chem. 401, 2495-2510. https://doi.org/10.1007/s00216-011-5349-9
  10. Newburg, D. S., Ruiz-Palacios, G. M., Altaye, M., Chaturvedi, P., Meinzen-Derr, J., Guerrero Mde, L. and Morrow, A. L. (2004) Innate protection conferred by fucosylated oligosaccharides of human milk against diarrhea in breastfed infants. Glycobiology 14, 253-263. https://doi.org/10.1093/glycob/cwh020
  11. Kobata, A. (1992) Structures and functions of the sugar chains of glycoproteins. Eur. J. Biochem. 209, 483-501. https://doi.org/10.1111/j.1432-1033.1992.tb17313.x
  12. Oriol, R., Le Pendu, J. and Mollicone, R. (1986) Genetics of ABO, H, Lewis, X and related antigens. Vox Sanguinis 51, 161-171. https://doi.org/10.1111/j.1423-0410.1986.tb01946.x
  13. Urashima, T., Saito, T., Nakamura, T. and Messer, M. (2001) Oligosaccharides of milk and colostrum in non-human mammals. Glycoconj. J. 18, 357-371. https://doi.org/10.1023/A:1014881913541
  14. Tao, N., Wu, S., Kim, J., An, H. J., Hinde, K., Power, M. L., Gagneux, P., German, J. B. and Lebrilla, C. B. (2011) Evolutionary glycomics: characterization of milk oligosaccharides in primates. J. Proteome Res. 10, 1548-1557. https://doi.org/10.1021/pr1009367
  15. Zivkovic, A. M., German, J. B., Lebrilla, C. B. and Mills, D. A. (2011) Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc. Natl. Acad. Sci. U.S.A. 108(Suppl 1), 4653-4658. https://doi.org/10.1073/pnas.1000083107
  16. German, J. B., Freeman, S. L., Lebrilla, C. B. and Mills, D. A. (2008) Human milk oligosaccharides: evolution, structures and bioselectivity as substrates for intestinal bacteria. Nestle Nutr. Workshop Ser. Pediatr. Program 62, 205-218. https://doi.org/10.1159/000146322
  17. Newburg, D. S., Ruiz-Palacios, G. M. and Morrow, A. L. (2005) Human milk glycans protect infants against enteric pathogens. Annu. Rev. Nutr. 25, 37-58. https://doi.org/10.1146/annurev.nutr.25.050304.092553
  18. Morrow, A. L., Meinzen-Derr, J., Huang, P., Schibler, K. R., Cahill, T., Keddache, M., Kallapur, S. G., Newburg, D. S., Tabangin, M., Warner, B. B. and Jiang, X. (2011) Fucosyltransferase 2 non-secretor and low secretor status predicts severe outcomes in premature infants. J. Pediatr. 158, 745-751. https://doi.org/10.1016/j.jpeds.2010.10.043
  19. Morrow, A. L., Ruiz-Palacios, G. M., Altaye, M., Jiang, X., Guerrero, M. L., Meinzen-Derr, J. K., Farkas, T., Chaturvedi, P., Pickering, L. K. and Newburg, D. S. (2004) Human milk oligosaccharide blood group epitopes and innate immune protection against campylobacter and calicivirus diarrhea in breastfed infants. Adv. Exp. Med. Biol. 554, 443-446. https://doi.org/10.1007/978-1-4757-4242-8_61
  20. Wang, B. (2009) Sialic acid is an essential nutrient for brain development and cognition. Annu. Rev. Nutr. 29, 177-222. https://doi.org/10.1146/annurev.nutr.28.061807.155515
  21. Hong, P., Ninonuevo, M. R., Lee, B., Lebrilla, C. and Bode, L. (2009) Human milk oligosaccharides reduce HIV- 1-gp120 binding to dendritic cell-specific ICAM3-grabbing non-integrin (DC-SIGN). Br. J. Nutr. 101, 482-486.
  22. Coppa, G. V., Zampini, L., Galeazzi, T., Facinelli, B., Ferrante, L., Capretti, R. and Orazio, G. (2006) Human milk oligosaccharides inhibit the adhesion to Caco-2 cells of diarrheal pathogens: Escherichia coli, Vibrio cholerae, and Salmonella fyris. Pediatr. Res. 59, 377-382. https://doi.org/10.1203/01.pdr.0000200805.45593.17
  23. Ruiz-Palacios, G. M., Cervantes, L. E., Ramos, P., Chavez- Munguia, B. and Newburg, D. S. (2003) 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. 278, 14112-14120. https://doi.org/10.1074/jbc.M207744200
  24. Morrow, A. L., Ruiz-Palacios, G. M., Altaye, M., Jiang, X., Guerrero, M. L., Meinzen-Derr, J. K., Farkas, T., Chaturvedi, P., Pickering, L. K. and Newburg, D. S. (2004) Human milk oligosaccharides are associated with protection against diarrhea in breast-fed infants. J. Pediatr. 145, 297-303. https://doi.org/10.1016/j.jpeds.2004.04.054
  25. Marcobal, A. and Sonnenburg, J. L. (2012) Human milk oligosaccharide consumption by intestinal microbiota. Clin. Microbiol. Infect. 18(Suppl 4), 12-15. https://doi.org/10.1111/j.1469-0691.2012.03863.x
  26. Marcobal, A., Barboza, M., Sonnenburg, E. D., Pudlo, N., Martens, E. C., Desai, P., Lebrilla, C. B., Weimer, B. C., Mills, D. A., German, J. B. and Sonnenburg, J. L. (2011) Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host. Microbe. 10, 507-514. https://doi.org/10.1016/j.chom.2011.10.007
  27. Sela, D. A., Li, Y., Lerno, L., Wu, S., Marcobal, A. M., German, J. B., Chen, X., Lebrilla, C. B. and Mills, D. A. (2011) An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J. Biol. Chem. 286, 11909-11918. https://doi.org/10.1074/jbc.M110.193359
  28. LoCascio, R. G., Ninonuevo, M. R., Freeman, S. L., Sela, D. A., Grimm, R., Lebrilla, C. B., Mills, D. A. and German, J. B. (2007) 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. 55, 8914-8919. https://doi.org/10.1021/jf0710480
  29. Marcobal, A., Barboza, M., Froehlich, J. W., Block, D. E., German, J. B., Lebrilla, C. B. and Mills, D. A. (2010) Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food Chem. 58, 5334-5340. https://doi.org/10.1021/jf9044205
  30. O'hara, A. M. and Shanahan, F. (2006) The gut flora as a forgotten organ. EMBO Rep. 7, 688-693. https://doi.org/10.1038/sj.embor.7400731
  31. Stahl, B., Thurl, S., Zeng, J., Karas, M., Hillenkamp, F., Steup, M. and Sawatzki, G. (1994) Oligosaccharides from human milk as revealed by matrix-assisted laser desorption/ ionization mass spectrometry. Anal. Biochem. 223, 218-226. https://doi.org/10.1006/abio.1994.1577
  32. Locascio, R. G., Ninonuevo, M. R., Kronewitter, S. R., Freeman, S. L., German, J. B., Lebrilla, C. B. and Mills, D. A. (2009) A versatile and scalable strategy for glycoprofiling bifidobacterial consumption of human milk oligosaccharides. Microb. Biotechnol. 2, 333-342. https://doi.org/10.1111/j.1751-7915.2008.00072.x
  33. Ninonuevo, M. R., Ward, R. E., LoCascio, R. G., German, J. B., Freeman, S. L., Barboza, M., Mills, D. A. and Lebrilla, C. B. (2007) Methods for the quantitation of human milk oligosaccharides in bacterial fermentation by mass spectrometry. Anal. Biochem. 361, 15-23. https://doi.org/10.1016/j.ab.2006.11.010
  34. Zauner, G., Deelder, A. M. and Wuhrer, M. (2011) Recent advances in hydrophilic interaction liquid chromatography (HILIC) for structural glycomics. Electrophoresis 32, 3456-3466. https://doi.org/10.1002/elps.201100247
  35. Wuhrer, M., de Boer, A. R. and Deelder, A. M. (2009) Structural glycomics using hydrophilic interaction chromatography (HILIC) with mass spectrometry. Mass Spectrom. Rev. 28, 192-206. https://doi.org/10.1002/mas.20195
  36. Ruhaak, L. R., Deelder, A. M. and Wuhrer, M. (2009) Oligosaccharide analysis by graphitized carbon liquid chromatography-mass spectrometry. Anal. Bioanal. Chem. 394, 163-174. https://doi.org/10.1007/s00216-009-2664-5
  37. Pabst, M. and Altmann, F. (2011) Glycan analysis by modern instrumental methods. Proteomics 11, 631-643. https://doi.org/10.1002/pmic.201000517
  38. Ruhaak, L. R., Zauner, G., Huhn, C., Bruggink, C., Deelder, A. M. and Wuhrer, M. (2010) Glycan labeling strategies and their use in identification and quantification. Anal. Bioanal. Chem. 397, 3457-3481. https://doi.org/10.1007/s00216-010-3532-z
  39. Costello, C. E., Contado-Miller, J. M. and Cipollo, J. F. (2007) A glycomics platform for the analysis of permethylated oligosaccharide alditols. J. Am. Soc. Mass Spectrom. 18, 1799-1812. https://doi.org/10.1016/j.jasms.2007.07.016
  40. Asakuma, S., Urashima, T., Akahori, M., Obayashi, H., Nakamura, T., Kimura, K., Watanabe, Y., Arai, I. and Sanai, Y. (2008) Variation of major neutral oligosaccharides levels in human colostrum. Eur. J. Clin. Nutr. 62, 488-494. https://doi.org/10.1038/sj.ejcn.1602738
  41. Sumiyoshi, W., Urashima, T., Nakamura, T., Arai, I., Saito, T., Tsumura, N., Wang, B., Brand-Miller, J., Watanabe, Y. and Kimura, K. (2003) Determination of each neutral oligosaccharide in the milk of Japanese women during the course of lactation. Br. J. Nutr. 89, 61-69. https://doi.org/10.1079/BJN2002746
  42. Leo, F., Asakuma, S., Fukuda, K., Senda, A. and Urashima, T. (2010) Determination of sialyl and neutral oligosaccharide levels in transition and mature milks of Samoan women, using anthranilic derivatization followed by reverse phase high performance liquid chromatography. Biosci. Biotechnol. Biochem. 74, 298-303. https://doi.org/10.1271/bbb.90614
  43. Leo, F., Asakuma, S., Nakamura, T., Fukuda, K., Senda, A. and Urashima, T. (2009) Improved determination of milk oligosaccharides using a single derivatization with anthranilic acid and separation by reversed-phase high-performance liquid chromatography. J. Chrom. A 1216, 1520-1523. https://doi.org/10.1016/j.chroma.2009.01.015
  44. Royle, L., Campbell, M. P., Radcliffe, C. M., White, D. M., Harvey, D. J., Abrahams, J. L., Kim, Y. G., Henry, G. W., Shadick, N. A., Weinblatt, M. E., Lee, D. M., Rudd, P. M. and Dwek, R. A. (2008) HPLC-based analysis of serum N-glycans on a 96-well plate platform with dedicated database software. Anal. Biochem. 376, 1-12. https://doi.org/10.1016/j.ab.2007.12.012
  45. Royle, L., Mattu, T. S., Hart, E., Langridge, J. I., Merry, A. H., Murphy, N., Harvey, D. J., Dwek, R. A. and Rudd, P. M. (2002) An analytical and structural database provides a strategy for sequencing O-glycans from microgram quantities of glycoproteins. Anal. Biochem. 304, 70-90. https://doi.org/10.1006/abio.2002.5619
  46. Ruhaak, L. R., Huhn, C., Waterreus, W. J., de Boer, A. R., Neususs, C., Hokke, C. H., Deelder, A. M. and Wuhrer, M. (2008) Hydrophilic interaction chromatography-based high-throughput sample preparation method for N-glycan analysis from total human plasma glycoproteins. Anal. Chem. 80, 6119-6126. https://doi.org/10.1021/ac800630x
  47. Shen, Z., Warren, C. D. and Newburg, D. S. (2000) High-performance capillary electrophoresis of sialylated oligosaccharides of human milk. Anal. Biochem. 279, 37-45. https://doi.org/10.1006/abio.1999.4448
  48. Bao, Y., Zhu, L. and Newburg, D. S. (2007) Simultaneous quantification of sialyloligosaccharides from human milk by capillary electrophoresis. Anal. Biochem. 370, 206-214. https://doi.org/10.1016/j.ab.2007.07.004
  49. Albrecht, S., Schols, H. A., van den Heuvel, E. G., Voragen, A. G. and Gruppen, H. (2010) CE-LIF-MS n profiling of oligosaccharides in human milk and feces of breast-fed babies. Electrophoresis 31, 1264-1273. https://doi.org/10.1002/elps.200900646
  50. Albrecht, S., Schols, H. A., van den Heuvel, E. G., Voragen, A. G. and Gruppen, H. (2011) Occurrence of oligosaccharides in feces of breast-fed babies in their first six months of life and the corresponding breast milk. Carbohydr. Res. 346, 2540-2550. https://doi.org/10.1016/j.carres.2011.08.009
  51. Albrecht, S., Schols, H. A., van Zoeren, D., van Lingen, R. A., Groot Jebbink, L. J., van den Heuvel, E. G., Voragen, A. G. and Gruppen, H. (2011) Oligosaccharides in feces of breast- and formula-fed babies. Carbohydr. Res. 346, 2173-2181. https://doi.org/10.1016/j.carres.2011.06.034
  52. Huhn, C., Ramautar, R., Wuhrer, M. and Somsen, G. W. (2010) Relevance and use of capillary coatings in capillary electrophoresis-mass spectrometry. Anal. Bioanal. Chem. 396, 297-314. https://doi.org/10.1007/s00216-009-3193-y
  53. Ninonuevo, M., An, H., Yin, H., Killeen, K., Grimm, R., Ward, R., German, B. and Lebrilla, C. (2005) Nanoliquid chromatography-mass spectrometry of oligosaccharides employing graphitized carbon chromatography on microchip with a high-accuracy mass analyzer. Electrophoresis 26, 3641-3649. https://doi.org/10.1002/elps.200500246
  54. Anraku, T., Fukuda, K., Saito, T., Messer, M. and Urashima, T. (2012) Chemical characterization of acidic oligosaccharides in milk of the red kangaroo (Macropus rufus). Glycoconj. J. 29, 147-156. https://doi.org/10.1007/s10719-012-9372-7
  55. Taufik, E., Fukuda, K., Senda, A., Saito, T., Williams, C., Tilden, C., Eisert, R., Oftedal, O. and Urashima, T. (2012) Structural characterization of neutral and acidic oligosaccharides in the milks of strepsirrhine primates: greater galago, aye-aye, Coquerel's sifaka and mongoose lemur. Glycoconj. J. 29, 119-134. https://doi.org/10.1007/s10719-012-9370-9
  56. Amano, J., Osanai, M., Orita, T., Sugahara, D. and Osumi, K. (2009) Structural determination by negative-ion MALDI-QIT-TOFMSn after pyrene derivatization of variously fucosylated oligosaccharides with branched decaose cores from human milk. Glycobiology 19, 601-614. https://doi.org/10.1093/glycob/cwp026
  57. Suzuki, Y., Suzuki, M., Ito, E., Ishii, H., Miseki, K. and Suzuki, A. (2005) Convenient and rapid analysis of linkage isomers of fucose-containing oligosaccharides by matrix- assisted laser desorption/ionization quadrupole ion trap time-of-flight mass spectrometry. Glycoconj. J. 22, 427-431. https://doi.org/10.1007/s10719-005-4173-x
  58. Li, B., An, H. J., Hedrick, J. L. and Lebrilla, C. B. (2009) Infrared multiphoton dissociation mass spectrometry for structural elucidation of oligosaccharides. Methods Mol. Biol. 534, 23-35. https://doi.org/10.1007/978-1-59745-022-5_2
  59. Li, B., Russell, S. C., Zhang, J., Hedrick, J. L. and Lebrilla, C. B. (2011) Structure determination by MALDI-IRMPD mass spectrometry and exoglycosidase digestions of O-linked oligosaccharides from Xenopus borealis egg jelly. Glycobiology 21, 877-894. https://doi.org/10.1093/glycob/cwr003
  60. Zhang, J., Schubothe, K., Li, B., Russell, S. and Lebrilla, C. B. (2005) Infrared multiphoton dissociation of O-linked mucin-type oligosaccharides. Anal. Chem. 77, 208-214. https://doi.org/10.1021/ac0489824
  61. Pfenninger, A., Karas, M., Finke, B. and Stahl, B. (2002) Structural analysis of underivatized neutral human milk oligosaccharides in the negative ion mode by nano-electrospray MS(n) (part 1: methodology). J. Am. Soc. Mass Spectrom. 13, 1331-1340. https://doi.org/10.1016/S1044-0305(02)00645-1
  62. Pfenninger, A., Karas, M., Finke, B. and Stahl, B. (2002) Structural analysis of underivatized neutral human milk oligosaccharides in the negative ion mode by nano-electrospray MS(n) (part 2: application to isomeric mixtures). J. Am. Soc. Mass Spectrom. 13, 1341-1348. https://doi.org/10.1016/S1044-0305(02)00646-3
  63. Wuhrer, M., Deelder, A. M. and van der Burgt, Y. E. (2011) Mass spectrometric glycan rearrangements. Mass Spectrom. Rev. 30, 664-680. https://doi.org/10.1002/mas.20337
  64. Han, L. and Costello, C. E. (2011) Electron transfer dissociation of milk oligosaccharides. J. Am. Soc. Mass Spectrom. 22, 997-1013. https://doi.org/10.1007/s13361-011-0117-9
  65. Hua, S., An, H. J., Ozcan, S., Ro, G. S., Soares, S., DeVere-White, R. and Lebrilla, C. B. (2011) Comprehen.- sive native glycan profiling with isomer separation and quantitation for the discovery of cancer biomarkers. Analyst 136, 3663-3671. https://doi.org/10.1039/c1an15093f
  66. Hua, S., Lebrilla, C. and An, H. J. (2011) Application of nano-LC-based glycomics towards biomarker discovery. Bioanalysis 3, 2573-2585. https://doi.org/10.4155/bio.11.263
  67. Blank, D., Dotz, V., Geyer, R. and Kunz, C. (2012) Human milk oligosaccharides and Lewis blood group: individual high-throughput sample profiling to enhance conclusions from functional studies. Adv. Nutr. 3, 440S-449S https://doi.org/10.3945/an.111.001446
  68. Newburg, D. S., Ruiz-Palacios, G. M., Altaye, M., Chaturvedi, P., Guerrero, M. L., Meinzen-Derr, J. K. and Morrow, A. L. (2004) Human milk alphal,2-linked fucosylated oligosaccharides decrease risk of diarrhea due to stable toxin of E. coli in breastfed infants. Adv. Exp. Med. Biol. 554, 457-461. https://doi.org/10.1007/978-1-4757-4242-8_64
  69. Stepans, M. B., Wilhelm, S. L., Hertzog, M., Rodehorst, T. K., Blaney, S., Clemens, B., Polak, J. J. and Newburg, D. S. (2006) Early consumption of human milk oligosaccharides is inversely related to subsequent risk of respiratory and enteric disease in infants. Breastfeed. Med. 1, 207-215. https://doi.org/10.1089/bfm.2006.1.207
  70. Kindberg, E., Hejdeman, B., Bratt, G., Wahren, B., Lindblom, B., Hinkula, J. and Svensson, L. (2006) A nonsense mutation (428G${\rightarrow}$A) in the fucosyltransferase FUT2 gene affects the progression of HIV-1 infection. AIDS 20, 685-689. https://doi.org/10.1097/01.aids.0000216368.23325.bc
  71. Le Pendu, J., Ruvoen-Clouet, N., Kindberg, E. and Svensson, L. (2006) Mendelian resistance to human norovirus infections. Semin. Immunol. 18, 375-386. https://doi.org/10.1016/j.smim.2006.07.009
  72. Coppa, G. V., Bruni, S., Morelli, L., Soldi, S. and Gabrielli, O. (2004) The first prebiotics in humans: human milk oligosaccharides. J. Clin. Gastroenterol. 38, S80-83. https://doi.org/10.1097/01.mcg.0000128926.14285.25
  73. Coppa, G. V., Zampini, L., Galeazzi, T. and Gabrielli, O. (2006) Prebiotics in human milk: a review. Dig. Liver Dis. 38(Suppl 2), S291-294. https://doi.org/10.1016/S1590-8658(07)60013-9
  74. Barboza, M., Sela, D. A., Pirim, C., Locascio, R. G., Freeman, S. L., German, J. B., Mills, D. A. and Lebrilla, C. B. (2009) Glycoprofiling bifidobacterial consumption of galacto-oligosaccharides by mass spectrometry reveals strain-specific, preferential consumption of glycans. Appl. Environ. Microbiol. 75, 7319-7325. https://doi.org/10.1128/AEM.00842-09
  75. Fukuda, K., Yamamoto, A., Ganzorig, K., Khuukhenbaatar, J., Senda, A., Saito, T. and Urashima, T. (2010) Chemical characterization of the oligosaccharides in Bactrian camel (Camelus bactrianus) milk and colostrum. J. Dairy Sci. 93, 5572-5587. https://doi.org/10.3168/jds.2010-3151
  76. Nakamura, T., Urashima, T., Mizukami, T., Fukushima, M., Arai, I., Senshu, T., Imazu, K., Nakao, T., Saito, T., Ye, Z., Zuo, H. and Wu, K. (2003) Composition and oligosaccharides of a milk sample of the giant panda, Ailuropoda melanoleuca. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 135, 439-448. https://doi.org/10.1016/S1096-4959(03)00093-9
  77. Osthoff, G., Dickens, L., Urashima, T., Bonnet, S. L., Uemura, Y. and van der Westhuizen, J. H. (2008) Structural characterization of oligosaccharides in the milk of an African elephant (Loxodonta africana africana). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 150, 74-84. https://doi.org/10.1016/j.cbpb.2008.01.010
  78. Uemura, Y., Asakuma, S., Yon, L., Saito, T., Fukuda, K., Arai, I. and Urashima, T. (2006) Structural determination of the oligosaccharides in the milk of an Asian elephant (Elephas maximus). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 145, 468-478. https://doi.org/10.1016/j.cbpa.2006.08.001
  79. Uemura, Y., Takahashi, S., Senda, A., Fukuda, K., Saito, T., Oftedal, O. T. and Urashima, T. (2009) Chemical characterization of milk oligosaccharides of a spotted hyena (Crocuta crocuta). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 152, 158-161. https://doi.org/10.1016/j.cbpa.2008.09.013
  80. Urashima, T., Kobayashi, M., Asakuma, S., Uemura, Y., Arai, I., Fukuda, K., Saito, T., Mogoe, T., Ishikawa, H. and Fukui, Y. (2007) Chemical characterization of the oligosaccharides in Bryde's whale (Balaenoptera edeni) and Sei whale (Balaenoptera borealis lesson) milk. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 146, 153-159. https://doi.org/10.1016/j.cbpb.2006.10.094
  81. Urashima, T., Odaka, G., Asakuma, S., Uemura, Y., Goto, K., Senda, A., Saito, T., Fukuda, K., Messer, M. and Oftedal, O. T. (2009) Chemical characterization of oligosaccharides in chimpanzee, bonobo, gorilla, orangutan, and siamang milk or colostrum. Glycobiology 19, 499-508. https://doi.org/10.1093/glycob/cwp006

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