1932

Abstract

In addition to providing complete postnatal nutrition, breast milk is a complex biofluid that delivers bioactive components for the growth and development of the intestinal and immune systems. Lactation is a unique opportunity to understand the role of diet in shaping the intestinal environment including the infant microbiome. Of considerable interest is the diversity and abundance of milk glycans that are energetically costly for the mammary gland to produce yet indigestible by infants. Milk glycans comprise free oligosaccharides, glycoproteins, glycopeptides, and glycolipids. Emerging technological advances are enabling more comprehensive, sensitive, and rapid analyses of these different classes of milk glycans. Understanding the impact of inter- and intraindividual glycan diversity on function is an important step toward interventions aimed at improving health and preventing disease. This review discusses the state of technology for glycan analysis and how specific structure-function knowledge is enhancing our understanding of early nutrition in the neonate.

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2014-07-17
2024-05-24
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Literature Cited

  1. Alfaleh K, Anabrees J, Bassler D, Al-Kharfi T. 1.  2011. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst. Rev. 3:CD005496 [Google Scholar]
  2. Alvarez-Manilla G, Atwood J III, Guo Y, Warren NL, Orlando R, Pierce M. 2.  2006. Tools for glycoproteomic analysis: size exclusion chromatography facilitates identification of tryptic glycopeptides with N-linked glycosylation sites. J. Proteome Res. 5:701–8 [Google Scholar]
  3. Am. Diabetes Assoc 2011. Diagnosis and classification of diabetes mellitus. Diabetes Care 34:S62–69 [Google Scholar]
  4. An HJ, Froehlich JW, Lebrilla CB. 4.  2009. Determination of glycosylation sites and site-specific heterogeneity in glycoproteins. Curr. Opin. Chem. Biol. 13:421–26 [Google Scholar]
  5. Andersson B, Porras O, Hanson , Lagergård T, Svanborg-Edén C. 5.  1986. Inhibition of attachment of Streptococcus pneumoniae and Haemophilus influenzae by human milk and receptor oligosaccharides. J. Infect. Dis. 153:232–37 [Google Scholar]
  6. Aoki-Kinoshita KF. 6.  2008. An introduction to bioinformatics for glycomics research. PLoS Comput. Biol. 4:e1000075 [Google Scholar]
  7. Ashline D, Singh S, Hanneman A, Reinhold V. 7.  2005. Congruent strategies for carbohydrate sequencing. 1. Mining structural details by MSn. Anal. Chem. 77:6250–62 [Google Scholar]
  8. Azuma N, Yamauchi K, Mitsuoka T. 8.  1984. Bifidus growth-promoting activity of a glycomacropeptide derived from human K-casein. Agric. Biol. Chem. 48:2159–62 [Google Scholar]
  9. Barboza M, Pinzon J, Wickramasinghe S, Froehlich JW, Moeller I. 9.  et al. 2012. Glycosylation of human milk lactoferrin exhibits dynamic changes during early lactation enhancing its role in pathogenic bacteria-host interactions. Mol. Cell Proteomics 11:M111.015248 [Google Scholar]
  10. Barboza M, Sela DA, Pirim C, Locascio RG, Freeman SL. 10.  et al. 2009. Glycoprofiling bifidobacterial consumption of galacto-oligosaccharides by mass spectrometry reveals strain-specific, preferential consumption of glycans. Appl. Environ. Microbiol. 75:7319–25 [Google Scholar]
  11. Barile D, Marotta M, Chu C, Mehra R, Grimm R. 11.  et al. 2010. Neutral and acidic oligosaccharides in Holstein-Friesian colostrum during the first 3 days of lactation measured by high performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry. J. Dairy Sci. 93:3940–49 [Google Scholar]
  12. Bellamy L, Casas JP, Hingorani AD, Williams D. 12.  2009. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet 373:1773–79 [Google Scholar]
  13. Blackburn D. 13.  1993. Lactation: historical patterns and potential for manipulation. J. Dairy Sci. 76:3195–212 [Google Scholar]
  14. Blank D, Dotz V, Geyer R, Kunz C. 14.  2012. Human milk oligosaccharides and Lewis blood group: individual high-throughput sample profiling to enhance conclusions from functional studies. Adv. Nutr. 3:440–49S [Google Scholar]
  15. Bode L. 15.  2012. Human milk oligosaccharides: Every baby needs a sugar mama. Glycobiology 22:1147–62 [Google Scholar]
  16. Bode L, Beermann C, Mank M, Kohn G, Boehm G. 16.  2004. Human and bovine milk gangliosides differ in their fatty acid composition. J. Nutr. 134:3016–20 [Google Scholar]
  17. Bode L, Jantscher-Krenn E. 17.  2012. Structure-function relationships of human milk oligosaccharides. Adv. Nutr. 3:383–91S [Google Scholar]
  18. Borén T, Falk P, Roth KA, Larson G, Normark S. 18.  1993. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262:1892–95 [Google Scholar]
  19. Brandtzaeg P. 19.  2010. The mucosal immune system and its integration with the mammary glands. J. Pediatr. 156:S8–15 [Google Scholar]
  20. Bricarello DA, Smilowitz JT, Zivkovic AM, German JB, Parikh AN. 20.  2011. Reconstituted lipoprotein: a versatile class of biologically-inspired nanostructures. ACS Nano 5:42–57 [Google Scholar]
  21. Brønnum H, Seested T, Hellgren L, Brix S, Frøkiær H. 21.  2005. Milk-derived GM3 and GD3 differentially inhibit dendritic cell maturation and effector functionalities. Scand. J. Immunol. 61:551–57 [Google Scholar]
  22. Bu H, Zuo X, Wang X, Ensslin MA, Koti V. 22.  et al. 2007. Milk fat globule-EGF factor 8/lactadherin plays a crucial role in maintenance and repair of murine intestinal epithelium. J. Clin. Invest. 117:3673–83 [Google Scholar]
  23. Charlwood J, Hanrahan S, Tyldesley R, Langridge J, Dwek M, Camilleri P. 23.  2002. Use of proteomic methodology for the characterization of human milk fat globular membrane proteins. Anal. Biochem. 301:314–24 [Google Scholar]
  24. Chaturvedi P, Warren CD, Altaye M, Morrow AL, Ruiz-Palacios G. 24.  et al. 2001. Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology 11:365–72 [Google Scholar]
  25. Chaturvedi P, Warren CD, Buescher CR, Pickering LK, Newburg DS. 25.  2001. Survival of human milk oligosaccharides in the intestine of infants. Bioactive Components of Human Milk DS Newburg 315–24 New York: Springer [Google Scholar]
  26. Chen Q, Cao J, Jia Y, Liu X, Yan Y, Pang G. 26.  2012. Modulation of mice fecal microbiota by administration of casein glycomacropeptide. Microbiol. Res. 3:e3 [Google Scholar]
  27. Chichlowski M, De Lartigue G, German JB, Raybould HE, Mills DA. 27.  2012. Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. J. Pediatr. Gastroenterol. Nutr. 55:321–27 [Google Scholar]
  28. Chirico G, Marzollo R, Cortinovis S, Fonte C, Gasparoni A. 28.  2008. Antiinfective properties of human milk. J. Nutr. 138:1801–6S [Google Scholar]
  29. Clausen TD, Mathiesen ER, Hansen T, Pedersen O, Jensen DM. 29.  et al. 2008. High prevalence of type 2 diabetes and pre-diabetes in adult offspring of women with gestational diabetes mellitus or type 1 diabetes. Diabetes Care 31:340–46 [Google Scholar]
  30. Coppa G, Pierani P, Zampini L, Bruni S, Carloni I, Gabrielli O. 30.  2001. Characterization of oligosaccharides in milk and feces of breast-fed infants by high-performance anion-exchange chromatography. Bioactive Components of Human Milk DS Newburg 307–14 New York: Springer [Google Scholar]
  31. Coppa GV, Gabrielli O, Pierani P, Catassi C, Carlucci A, Giorgi PL. 31.  1993. Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics 91:637–41 [Google Scholar]
  32. Coppa GV, Pierani P, Zampini L, Bruni S, Carloni I, Gabrielli O. 32.  2001. Characterization of oligosaccharides in milk and feces of breast-fed infants by high-performance anion-exchange chromatography. Adv. Exp. Med. Biol. 501:307–14 [Google Scholar]
  33. Coppa GV, Zampini L, Galeazzi T, Facinelli B, Ferrante L. 33.  et al. 2006. Human milk oligosaccharides inhibit the adhesion to Caco-2 cells of diarrheal pathogens: Escherichia coli, Vibrio cholerae, and Salmonella fyris. Pediatr. Res. 59:377–82 [Google Scholar]
  34. De Leoz ML, Wu S, Strum JS, Ninonuevo MR, Gaerlan SC. 34.  et al. 2013. A quantitative and comprehensive method to analyze human milk oligosaccharide structures in the urine and feces of infants. Anal. Bioanal. Chem. 405:4089–105 [Google Scholar]
  35. De Leoz MLA, Gaerlan SC, Strum JS, Dimapasoc LM, Mirmiran M. 35.  et al. 2012. Lacto-N-tetraose, fucosylation, and secretor status are highly variable in human milk oligosaccharides from women delivering preterm. J. Proteome Res. 11:4662–72 [Google Scholar]
  36. Desai PT, Walsh MK, Weimer BC. 36.  2008. Solid phase capture of pathogenic bacteria using gangliosides and detection with real time PCR. Appl. Environ. Microbiol. 74:2254–58 [Google Scholar]
  37. Dodds ED, Seipert RR, Clowers BH, German JB, Lebrilla CB. 37.  2009. Analytical performance of immobilized pronase for glycopeptide footprinting and implications for surpassing reductionist glycoproteomics. J. Proteome Res. 8:502–12 [Google Scholar]
  38. Du X-L, Edelstein D, Rossetti L, Fantus IG, Goldberg H. 38.  et al. 2000. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc. Natl. Acad. Sci. 97:12222–26 [Google Scholar]
  39. Engfer MB, Stahl B, Finke B, Sawatzki G, Daniel H. 39.  2000. Human milk oligosaccharides are resistant to enzymatic hydrolysis in the upper gastrointestinal tract. Am. J. Clin. Nutr. 71:1589–96 [Google Scholar]
  40. Ewaschuk JB, Diaz H, Meddings L, Diederichs B, Dmytrash A. 40.  et al. 2008. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 295:G1025–34 [Google Scholar]
  41. Falk P, Roth KA, Boren T, Westblom TU, Gordon JI, Normark S. 41.  1993. An in vitro adherence assay reveals that Helicobacter pylori exhibits cell lineage specific tropism in the human gastric epithelium. Proc. Natl. Acad. Sci. USA 90:2035–39 [Google Scholar]
  42. Ferrer-Admetlla A, Sikora M, Laayouni H, Esteve A, Roubinet F. 42.  et al. 2009. A natural history of FUT2 polymorphism in humans. Mol. Biol. Evol. 26:1993–2003 [Google Scholar]
  43. Fong B, Ma K, McJarrow P. 43.  2011. Quantification of bovine milk oligosaccharides using liquid chromatography-selected reaction monitoring-mass spectrometry. J. Agric. Food Chem. 59:9788–95 [Google Scholar]
  44. Froehlich J, Dodds E, Barboza M, McJimpsey E, Seipert R. 44.  et al. 2010. Glycoprotein expression in human milk during lactation. J. Agric. Food Chem. 58:6440–48 [Google Scholar]
  45. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y. 45.  et al. 2011. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469:543–47 [Google Scholar]
  46. Gabrielli O, Zampini L, Galeazzi T, Padella L, Santoro L. 46.  et al. 2011. Preterm milk oligosaccharides during the first month of lactation. Pediatrics 128:e1520–31 [Google Scholar]
  47. Ganguli K, Meng D, Rautava S, Lu L, Walker WA, Nanthakumar N. 47.  2013. Probiotics prevent necrotizing enterocolitis by modulating enterocyte genes that regulate innate immune-mediated inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 304:G132–41 [Google Scholar]
  48. Garrido D, Barile D, Mills DA. 48.  2012. A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract. Adv. Nutr. 3:415–21S [Google Scholar]
  49. Garrido D, Kim JH, German JB, Raybould HE, Mills DA. 49.  2011. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS ONE 6:e17315 [Google Scholar]
  50. Garrido D, Nwosu C, Ruiz-Moyano S, Aldredge D, German JB. 50.  et al. 2012. Endo-β-N-acetylglucosaminidases from infant gut-associated bifidobacteria release complex N-glycans from human milk glycoproteins. Mol. Cell Proteomics 11:775–85 [Google Scholar]
  51. Garrido D, Ruiz-Moyano S, Jimenez-Espinoza R, Eom HJ, Block DE, Mills DA. 51.  2013. Utilization of galactooligosaccharides by Bifidobacterium longum subsp. infantis isolates. Food Microbiol. 33:262–70 [Google Scholar]
  52. Garrido D, Ruiz-Moyano S, Mills DA. 52.  2012. Release and utilization of N-acetyl-D-glucosamine from human milk oligosaccharides by Bifidobacterium longum subsp. infantis. Anaerobe 18:430–35 [Google Scholar]
  53. Georgieff M, Petry C, Mills M, McKay H, Wobken J. 53.  1997. Increased N-glycosylation and reduced transferrin-binding capacity of transferrin receptor isolated from placentae of diabetic women. Placenta 18:563–68 [Google Scholar]
  54. Gordon JI, Dewey KG, Mills DA, Medzhitov RM. 54.  2012. The human gut microbiota and undernutrition. Sci. Transl. Med. 4:137ps12 [Google Scholar]
  55. Grollman EF, Ginsburg V. 55.  1967. Correlation between secretor status and the occurrence of 2′-fucosyllactose in human milk. Biochem. Biophys. Res. Commun. 28:50–53 [Google Scholar]
  56. Gross SJ, Geller J, Tomarelli R. 56.  1981. Composition of breast milk from mothers of preterm infants. Pediatrics 68:490–93 [Google Scholar]
  57. György P, Norris RF, Rose CS. 57.  1954. Bifidus factor. I. A variant of Lactobacillus bifidus requiring a special growth factor. Arch. Biochem. Biophys. 48:193–201 [Google Scholar]
  58. Haarman M, Knol J. 58.  2005. Quantitative real-time PCR assays to identify and quantify fecal Bifidobacterium species in infants receiving a prebiotic infant formula. Appl. Environ. Microbiol. 71:2318–24 [Google Scholar]
  59. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. 59.  2002. Identification of a factor that links apoptotic cells to phagocytes. Nature 417:182–87 [Google Scholar]
  60. Hanson LA. 60.  1998. Breastfeeding provides passive and likely long-lasting active immunity. Ann. Allergy Asthma Immunol. 81:523–37 [Google Scholar]
  61. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N. 61.  et al. 2000. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30:61–67 [Google Scholar]
  62. Hebert LF Jr, Daniels MC, Zhou J, Crook ED, Turner RL. 62.  et al. 1996. Overexpression of glutamine:fructose-6-phosphate amidotransferase in transgenic mice leads to insulin resistance. J. Clin. Invest. 98:930–36 [Google Scholar]
  63. Hernandez-Hernandez O, Sanz ML, Kolida S, Rastall RA, Moreno FJ. 63.  2011. In vitro fermentation by human gut bacteria of proteolytically digested caseinomacropeptide nonenzymatically glycosylated with prebiotic carbohydrates. J. Agric. Food Chem. 59:11949–55 [Google Scholar]
  64. Hong P, Ninonuevo MR, Lee B, Lebrilla C, Bode L. 64.  2009. Human milk oligosaccharides reduce HIV-1-gp120 binding to dendritic cell-specific ICAM3-grabbing non-integrin (DC-SIGN). Br. J. Nutr. 101:482–86 [Google Scholar]
  65. Huang P, Xia M, Tan M, Zhong W, Wei C. 65.  et al. 2012. Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J. Virol. 86:4833–43 [Google Scholar]
  66. Ip S, Chung M, Raman G, Chew P, Magula N. 66.  et al. 2007. Breastfeeding and maternal and infant health outcomes in developed countries. Evid. Rep. Technol. Assess. 153:1–186 [Google Scholar]
  67. Iwamori M, Takamizawa K, Momoeda M, Iwamori Y, Taketani Y. 67.  2008. Gangliosides in human, cow and goat milk, and their abilities as to neutralization of cholera toxin and botulinum type A neurotoxin. Glycoconj. J. 25:675–83 [Google Scholar]
  68. Jantscher-Krenn E, Lauwaet T, Bliss LA, Reed SL, Gillin FD, Bode L. 68.  2012. Human milk oligosaccharides reduce Entamoeba histolytica attachment and cytotoxicity in vitro. Br. J. Nutr. 108:1839–46 [Google Scholar]
  69. Kavanaugh DW, O'Callaghan J, Buttó LF, Slattery H, Lane J. 69.  et al. 2013. Exposure of Bifidobacterium longum subsp. infantis to milk oligosaccharides increases adhesion to epithelial cells and induces a substantial transcriptional response. PLoS ONE 8:e67224 [Google Scholar]
  70. Kim W-S, Ohashi M, Tanaka T, Kumura H, Kim G-Y. 70.  et al. 2004. Growth-promoting effects of lactoferrin on L. acidophilus and Bifidobacterium spp. Biometals 17:279–83 [Google Scholar]
  71. Kitaoka M. 71.  2012. Bifidobacterial enzymes involved in the metabolism of human milk oligosaccharides. Adv. Nutr. 3:422–29S [Google Scholar]
  72. Kiyohara M, Nakatomi T, Kurihara S, Fushinobu S, Suzuki H. 72.  et al. 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 [Google Scholar]
  73. Kumar R, Ouyang F, Story RE, Pongracic JA, Hong X. 73.  et al. 2009. Gestational diabetes, atopic dermatitis, and allergen sensitization in early childhood. J. Allergy Clin. Immunol. 124:1031–38.e4 [Google Scholar]
  74. Kunz C, Rudloff S, Baier W, Klein N, Strobel S. 74.  2000. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu. Rev. Nutr. 20:699–722 [Google Scholar]
  75. Lee CL, Chiu PCN, Pang PC, Chu IK, Lee KF. 75.  et al. 2011. Glycosylation failure extends to glycoproteins in gestational diabetes mellitus. Diabetes 60:909–17 [Google Scholar]
  76. Lee H, An HJ, Lerno LA, German JB, Lebrilla CB. 76.  2011. Rapid profiling of bovine and human milk gangliosides by matrix-assisted laser desorption/ionization Fourier transform ion cyclotron resonance mass spectrometry. Int. J. Mass Spectrom. 305:138–50 [Google Scholar]
  77. Legrand D, Pierce A, Elass E, Carpentier M, Mariller C, Mazurier J. 77.  2008. Lactoferrin structure and functions. Adv. Exp. Med. Biol. 606:163–94 [Google Scholar]
  78. Liao Y, Alvarado R, Phinney B, Lönnerdal B. 78.  2011. Proteomic characterization of human milk whey proteins during a twelve-month lactation period. J. Proteome Res. 10:1746–54 [Google Scholar]
  79. Liepke C, Adermann K, Raida M, Mägert HJ, Forssmann WG, Zucht HD. 79.  2002. Human milk provides peptides highly stimulating the growth of bifidobacteria. Eur. J. Biochem. 269:712–18 [Google Scholar]
  80. Lin H-C, Hsu C-H, Chen H-L, Chung M-Y, Hsu J-F. 80.  et al. 2008. Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics 122:693–700 [Google Scholar]
  81. Lin H-C, Su B-H, Chen A-C, Lin T-W, Tsai C-H. 81.  et al. 2005. Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics 115:1–4 [Google Scholar]
  82. LoCascio R, Ninonuevo M, Freeman S, Sela D, Grimm R. 82.  et al. 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. 55:8914–19 [Google Scholar]
  83. Locascio RG, Ninonuevo MR, Kronewitter SR, Freeman SL, German JB. 83.  et al. 2009. A versatile and scalable strategy for glycoprofiling bifidobacterial consumption of human milk oligosaccharides. Microb. Biotechnol. 2:333–42 [Google Scholar]
  84. Lönnerdal B. 84.  2010. Bioactive proteins in human milk: mechanisms of action. J. Pediatr. 156:S26–30 [Google Scholar]
  85. Marcobal A, Barboza M, Froehlich J, Block D, German JB. 85.  et al. 2010. Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food Chem. 58:5334–40 [Google Scholar]
  86. Marcobal A, Barboza M, Sonnenburg ED, Pudlo N, Martens EC. 86.  et al. 2011. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10:507–14 [Google Scholar]
  87. Marth JD, Grewal PK. 87.  2008. Mammalian glycosylation in immunity. Nat. Rev. Immunol. 8:874–87 [Google Scholar]
  88. Martin-Sosa S, Martin MJ, Hueso P. 88.  2002. The sialylated fraction of milk oligosaccharides is partially responsible for binding to enterotoxigenic and uropathogenic Escherichia coli human strains. J. Nutr. 132:3067–72 [Google Scholar]
  89. Mechref Y, Chen P, Novotny MV. 89.  1999. Structural characterization of the N-linked oligosaccharides in bile salt-stimulated lipase originated from human breast milk. Glycobiology 9:227–34 [Google Scholar]
  90. Molinari CE, Casadio YS, Hartmann BT, Arthur PG, Hartmann PE. 90.  2013. Longitudinal analysis of protein glycosylation and β-casein phosphorylation in term and preterm human milk during the first 2 months of lactation. Br. J. Nutr. 110:105–15 [Google Scholar]
  91. Molinari CE, Casadio YS, Hartmann BT, Livk A, Bringans S. 91.  et al. 2012. Proteome mapping of human skim milk proteins in term and preterm milk. J. Proteome Res. 11:1696–714 [Google Scholar]
  92. Morrow AL, Meinzen-Derr J, Huang P, Schibler KR, Cahill T. 92.  et al. 2011. Fucosyltransferase 2 non-secretor and low secretor status predicts severe outcomes in premature infants. J. Pediatr. 158:745–51 [Google Scholar]
  93. Morrow AL, Ruiz-Palacios GM, Jiang X, Newburg DS. 93.  2005. Human-milk glycans that inhibit pathogen binding protect breast-feeding infants against infectious diarrhea. J. Nutr. 135:1304–7 [Google Scholar]
  94. Newburg DS. 94.  2013. Glycobiology of human milk. Biochemistry (Moscow) 78:771–85 [Google Scholar]
  95. Newburg DS, Ruiz-Palacios GM, Morrow AL. 95.  2005. Human milk glycans protect infants against enteric pathogens. Annu. Rev. Nutr. 25:37–58 [Google Scholar]
  96. Newburg DS, Walker WA. 96.  2007. Protection of the neonate by the innate immune system of developing gut and of human milk. Pediatr. Res. 61:2–8 [Google Scholar]
  97. Ninonuevo MR, Park Y, Yin H, Zhang J, Ward RE. 97.  et al. 2006. A strategy for annotating the human milk glycome. J. Agric. Food Chem. 54:7471–80 [Google Scholar]
  98. Ninonuevo MR, Perkins PD, Francis J, Lamotte LM, LoCascio RG. 98.  et al. 2008. Daily variations in oligosaccharides of human milk determined by microfluidic chips and mass spectrometry. J. Agric. Food Chem. 56:618–26 [Google Scholar]
  99. Ninonuevo MR, Ward RE, LoCascio RG, German JB, Freeman SL. 99.  et al. 2007. Methods for the quantitation of human milk oligosaccharides in bacterial fermentation by mass spectrometry. Anal. Biochem. 361:15–23 [Google Scholar]
  100. Nusrat A, Turner J, Madara J. 100.  2000. IV. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. Am. J. Physiol. Gastrointest. Liver Physiol. 279:G851–57 [Google Scholar]
  101. Nwosu CC, Huang J, Aldredge DL, Strum JS, Hua S. 101.  et al. 2012. In-gel nonspecific proteolysis for elucidating glycoproteins: a method for targeted protein-specific glycosylation analysis in complex protein mixtures. Anal. Chem. 85:956–63 [Google Scholar]
  102. Ochoa TJ, Noguera-Obenza M, Ebel F, Guzman CA, Gomez HF, Cleary TG. 102.  2003. Lactoferrin impairs type III secretory system function in enteropathogenic Escherichia coli. Infect. Immun. 71:5149–55 [Google Scholar]
  103. Oda H, Wakabayashi H, Yamauchi K, Sato T, Xiao J-Z. 103.  et al. 2013. Isolation of a bifidogenic peptide from the pepsin hydrolysate of bovine lactoferrin. Appl. Environ. Microbiol. 79:1843–49 [Google Scholar]
  104. Pan XL, Izumi T. 104.  2000. Variation of the ganglioside compositions of human milk, cow's milk and infant formulas. Early Hum. Dev. 57:25–31 [Google Scholar]
  105. Peterson R, Cheah WY, Grinyer J, Packer N. 105.  2013. Glycoconjugates in human milk: protecting infants from disease. Glycobiology 23:1425–38 [Google Scholar]
  106. Petshow BW, Talbottt RD, Batema RP. 106.  1999. Ability of lactoferrin to promote the growth of Bifidobacterium spp. in vitro is independent of receptor binding capacity and iron saturation level. J. Med. Microbiol. 48:541–49 [Google Scholar]
  107. Qiu J, Hendrixson DR, Baker EN, Murphy TF, Geme JWS, Plaut AG. 107.  1998. Human milk lactoferrin inactivates two putative colonization factors expressed by Haemophilus influenzae. Proc. Natl. Acad. Sci. 95:12641–46 [Google Scholar]
  108. Reinhold V, Zhang H, Hanneman A, Ashline D. 108.  2013. Toward a platform for comprehensive glycan sequencing. Mol. Cell. Proteomics 12:866–73 [Google Scholar]
  109. Roger LC, McCartney AL. 109.  2010. Longitudinal investigation of the faecal microbiota of healthy full-term infants using fluorescence in situ hybridization and denaturing gradient gel electrophoresis. Microbiology 156:3317–28 [Google Scholar]
  110. Rueda R. 110.  2007. The role of dietary gangliosides on immunity and the prevention of infection. Br. J. Nutr. 98:S68–73 [Google Scholar]
  111. Ruiz-Moyano S, Totten SM, Garrido DA, Smilowitz JT, German JB. 111.  et al. 2013. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl. Environ. Microbiol. 79:6040–49 [Google Scholar]
  112. Rumbo M, Schiffrin EJ. 112.  2005. Ontogeny of intestinal epithelium immune functions: developmental and environmental regulation. Cell Mol Life Sci 62:1288–96 [Google Scholar]
  113. Ruvoën-Clouet N, Le Pendu J, Mas E, Marionneau S, Guillon P, Lombardo D. 113.  2006. Bile-salt-stimulated lipase and mucins from milk of “secretor” mothers inhibit the binding of Norwalk virus capsids to their carbohydrate ligands. Biochem. J 393:627–34 [Google Scholar]
  114. Sakata S, Tonooka T, Ishizeki S, Takada M, Sakamoto M. 114.  et al. 2005. Culture-independent analysis of fecal microbiota in infants, with special reference to Bifidobacterium species. FEMS Microbiol. Lett. 243:417–23 [Google Scholar]
  115. Schroten H, Stapper C, Plogmann R, Köhler H, Hacker J, Hanisch FG. 115.  1998. Fab-independent antiadhesion effects of secretory immunoglobulin A on S-fimbriated Escherichia coli are mediated by sialyloligosaccharides. Infect. Immun. 66:3971–73 [Google Scholar]
  116. Seipert RR, Dodds ED, Clowers BH, Beecroft SM, German JB, Lebrilla CB. 116.  2008. Factors that influence fragmentation behavior of N-linked glycopeptide ions. Anal. Chem. 80:3684–92 [Google Scholar]
  117. Sela DA, Chapman J, Adeuya A, Kim J, Chen F. 117.  et al. 2008. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. USA 105:18964–69 [Google Scholar]
  118. Sela DA, Garrido D, Lerno L, Wu S, Tan K. 118.  et al. 2012. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl. Environ. Microbiol. 78:795–803 [Google Scholar]
  119. Sela DA, Li Y, Lerno L, Wu S, Marcobal AM. 119.  et al. 2011. An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J. Biol. Chem. 286:11909–18 [Google Scholar]
  120. Shen L, Grollman EF, Ginsburg V. 120.  1968. An enzymatic basis for secretor status and blood group substance specificity in humans. Proc. Natl. Acad. Sci. USA 59:224–30 [Google Scholar]
  121. Shen Z, Warren CD, Newburg DS. 121.  2000. High-performance capillary electrophoresis of sialylated oligosaccharides of human milk. Anal. Biochem. 279:37–45 [Google Scholar]
  122. Smilowitz JT, O'Sullivan A, Barile D, German JB, Lönnerdal B, Slupsky CM. 122.  2013. The human milk metabolome reveals diverse oligosaccharide profiles. J. Nutr. 143:1709–18 [Google Scholar]
  123. Smilowitz JT, Totten SM, Huang J, Grapov D, Durham HA. 123.  et al. 2013. Human milk secretory immunoglobulin A and lactoferrin N-glycans are altered in women with gestational diabetes mellitus. J. Nutr. 143:1906–12 [Google Scholar]
  124. Strum JS, Kim J, Wu S, De Leoz ML, Peacock K. 124.  et al. 2012. Identification and accurate quantitation of biological oligosaccharide mixtures. Anal. Chem. 84:7793–801 [Google Scholar]
  125. Strum JS, Nwosu CC, Hua S, Kronewitter SR, Seipert RR. 125.  et al. 2013. Automated assignments of N- and O-site specific glycosylation with extensive glycan heterogeneity of glycoprotein mixtures. Anal. Chem. 85:5666–75 [Google Scholar]
  126. Tao N, Ochonicky KL, German JB, Donovan SM, Lebrilla CB. 126.  2010. Structural determination and daily variations of porcine milk oligosaccharides. J. Agric. Food Chem. 58:4653–59 [Google Scholar]
  127. Tao N, Wu S, Kim J, An HJ, Hinde K. 127.  et al. 2011. Evolutionary glycomics: characterization of milk oligosaccharides in primates. J. Proteome Res. 10:1548–57 [Google Scholar]
  128. Thakkar SK, Giuffrida F, Cristina CH, Castro CA, Mukherjee R. 128.  et al. 2013. Dynamics of human milk nutrient composition of women from Singapore with a special focus on lipids. Am. J. Hum. Biol. 25:770–79 [Google Scholar]
  129. Thurl S, Munzert M, Henker J, Boehm G, Muller-Werner B. 129.  et al. 2010. Variation of human milk oligosaccharides in relation to milk groups and lactational periods. Br. J. Nutr. 104:1261–71 [Google Scholar]
  130. Tissier H. 130.  1900. Recherches sur la flore intestinale des nourrissons: état normal et pathologique Paris: G. Carré et C. Naud
  131. Totten SM, Zivkovic AM, Wu S, Ngyuen U, Freeman SL. 131.  et al. 2012. Comprehensive profiles of human milk oligosaccharides yield highly sensitive and specific markers for determining secretor status in lactating mothers. J. Proteome Res. 11:6124–33 [Google Scholar]
  132. Tseng K, Hedrick JL, Lebrilla CB. 132.  1999. Catalog-library approach for the rapid and sensitive structural elucidation of oligosaccharides. Anal. Chem. 71:3747–54 [Google Scholar]
  133. Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH. 133.  et al. 2010. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc. Natl. Acad. Sci. USA 107:19514–19 [Google Scholar]
  134. Turroni F, Van Sinderen D, Ventura M. 134.  2011. Genomics and ecological overview of the genus Bifidobacterium. Int. J. Food Microbiol. 149:37–44 [Google Scholar]
  135. Uchiyama S-i, Sekiguchi K, Akaishi M, Anan A, Maeda T, Izumi T. 135.  2011. Characterization and chronological changes of preterm human milk gangliosides. Nutrition 27:998–1001 [Google Scholar]
  136. Underwood MA, Kalanetra KM, Bokulich NA, Lewis ZT, Mirmiran M. 136.  et al. 2013. A comparison of two probiotic strains of bifidobacteria in premature infants. J. Pediatr. 163:1585–91 [Google Scholar]
  137. Van Berkel P, Geerts M, Van Veen H, Kooiman P, Pieper F. 137.  et al. 1995. Glycosylated and unglycosylated human lactoferrins both bind iron and show identical affinities towards human lysozyme and bacterial lipopolysaccharide, but differ in their susceptibilities towards tryptic proteolysis. Biochem. J. 312:107–14 [Google Scholar]
  138. Van Berkel P, Van Veen H, Geerts M, De Boer H, Nuijens J. 138.  1996. Heterogeneity in utilization of N-glycosylation sites Asn624 and Asn138 in human lactoferrin: a study with glycosylation-site mutants. Biochem. J. 319:117–22 [Google Scholar]
  139. van Veen H, Geerts M, van Berkel P, Nuijens J. 139.  2004. The role of N-linked glycosylation in the protection of human and bovine lactoferrin against tryptic proteolysis. Eur. J. Biochem. 271:678–84 [Google Scholar]
  140. Varki A. 140.  2011. Evolutionary forces shaping the Golgi glycosylation machinery: why cell surface glycans are universal to living cells. Cold Spring Harb. Perspect. Biol. 3:6 [Google Scholar]
  141. Wang Y-Z, Shan T-Z, Xu Z-R, Feng J, Wang Z-Q. 141.  2007. Effects of the lactoferrin (LF) on the growth performance, intestinal microflora and morphology of weanling pigs. Anim. Feed Sci. Technol. 135:263–72 [Google Scholar]
  142. Ward RE, Ninonuevo M, Mills DA, Lebrilla CB, German JB. 142.  2006. In vitro fermentation of breast milk oligosaccharides by Bifidobacterium infantis and Lactobacillus gasseri. Appl. Environ. Microbiol. 72:4497–99 [Google Scholar]
  143. Ward RE, Ninonuevo M, Mills DA, Lebrilla CB, German JB. 143.  2007. In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria. Mol. Nutr. Food Res. 51:1398–405 [Google Scholar]
  144. Weber A, Loui A, Jochum F, Bührer C, Obladen M. 144.  2001. Breast milk from mothers of very low birthweight infants: variability in fat and protein content. Acta Paediatr. 90:772–75 [Google Scholar]
  145. Westerbeek EA, van den Berg A, Lafeber HN, Knol J, Fetter WP, van Elburg RM. 145.  2006. The intestinal bacterial colonisation in preterm infants: a review of the literature. Clin. Nutr. 25:361–68 [Google Scholar]
  146. Wold AE, Mestecky J, Tomana M, Kobata A, Ohbayashi H. 146.  1990. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infect. Immun. 58:3073–77 [Google Scholar]
  147. Wu S, Tao N, German JB, Grimm R, Lebrilla CB. 147.  2010. Development of an annotated library of neutral human milk oligosaccharides. J. Proteome Res. 9:4138–51 [Google Scholar]
  148. Wu SA, Grimm R, German JB, Lebrilla CB. 148.  2011. Annotation and structural analysis of sialylated human milk oligosaccharides. J. Proteome Res. 10:856–68 [Google Scholar]
  149. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG. 149.  et al. 2012. Human gut microbiome viewed across age and geography. Nature 486:222–27 [Google Scholar]
  150. Yu Z-T, Chen C, Kling DE, Liu B, McCoy JM. 150.  et al. 2013. The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology 23:169–77 [Google Scholar]
  151. Zauner G, Selman MHJ, Bondt A, Rombouts Y, Blank D. 151.  et al. 2013. Glycoproteomic analysis of antibodies. Mol. Cell. Proteomics 12:856–65 [Google Scholar]
  152. Zivkovic AM, Lewis ZT, German JB, Mills DA. 152.  2013. Establishment of a milk-oriented microbiota (MOM) in early life: how babies meet their MOMs. Funct. Food Rev. 5:3–12 [Google Scholar]
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