The significance of fucosylated glycoconjugates of human milk in nutrition of newborns and infants
Jolanta Lis-Kuberka 1 , Magdalena Orczyk-Pawiłowicz 1Abstract
Human milk is extremely complex secretion rich in biologically active glycoconjugates including free oligosaccharides, glycoproteins, glycolipids, and glycosaminoglycans. Alpha1-2-fucosylated glycoconjugates of human milk are component of the innate immune system and provide an additional defense for infants. Participation of fucosylated glycotopes in the inhibition of infections caused by some bacteria and/or viruses rely on blocking of lectin-receptors of pathogen. Free fucosylated glycoconjugates present in milk are recognized and bound by the lectin-receptors of bacteria and/or viruses, and prevent pathogens adhesion to host epithelial cells and development of infection. So far, the efficacy of fucosylated glycoconjugates of human milk in the inhibition of adhesion has been confirmed for Escherichia coli, Campylobacter jejuni, Salmonella enterica, Rotaviruses, HIV, and Noroviruses. In this process the secretor/nonsecretor status of mother plays an important role. This is particularly important for the women who are nonsecretors and whose milk does not contain α1-2-fucosylated glycoconjugates and has reduced anti-microbial properties. Fucosylated glycoconjugates of milk are also one of the energy sources for physiological bacterial flora (Bifidobacterium), and have a positive impact on the intestinal peristalsis, and indirectly stimulate the central nervous system of infants. Furthermore, compared to human milk, the content of fucosylated glycoconjugates of cow’s milk is very low and does not provide adequate protection. This fact is particularly important in terms of nutrition and should be taken into consideration when artificial mixtures based on cows’ milk are used. The paper presents the current state of knowledge on human milk glycoconjugates, particularly on α1-2-fucosylated free oligosaccharides and glycoproteins, and discusses the significance of fucosylated glycoconjugates of human milk in the nutrition of newborns and infants.
References
- 1. Adamkin D.H.: Mother’s milk, feeding strategies, and lactoferrinto prevent necrotizing enterocolitis. JPEN J. Parenter. Enteral Nutr.,2012; 36: 25S-29S
Google Scholar - 2. Aldredge D.L., Geronimo M.R., Hua S., Nwosu C.C., Lebrilla C.B.,Barile D.: Annotation and structural elucidation of bovine milk oligosaccharidesand determination of novel fucosylated structures.Glycobiology, 2013; 23: 664-676
Google Scholar - 3. Artym J.: Udział laktoferryny w gospodarce żelazem w organizmie.Część II. Działanie przeciwmikrobiologiczne i przeciwzapalnepoprzez sekwestrację żelaza. Postępy Hig. Med. Dośw., 2010; 64:604-616
Google Scholar - 4. Artym J., Zimecki M.: Milk-derived proteins and peptides in clinicaltrials. Postępy Hig. Med. Dośw., 2013; 67: 800-816
Google Scholar - 5. Artym J., Zimecki M.: Rola laktoferryny w prawidłowym rozwojunoworodka. Postępy Hig. Med. Dośw., 2005; 59: 421-432
Google Scholar - 6. Asakuma S., Urashima T., Akahori M., Obayashi H., NakamuraT., Kimura K., Watanabe Y., Arai I., Sanai Y.: Variation of major neutraloligosaccharides levels in human colostrum. Eur. J. Clin. Nutr.,2008; 62: 488-494
Google Scholar - 7. Bakker-Zierikzee A.M., Alles M.S., Knol J., Kok F.J., Tolboom J.J.,Bindels J.G.: Effects of infant formula containing a mixture of galacto-and fructo-oligosaccharides or viable Bifidobacterium animalison the intestinal microflora during the first 4 months of life. Br. J.Nutr., 2005; 94: 783-790
Google Scholar - 8. Barboza M., Pinzon J., Wickramasinghe S., Froehlich J.W., MoellerI., Smilowitz J.T., Ruhaak L.R., Huang J., Lönnerdal B., German J.B.,Medrano J.F., Weimer B.C., Lebrilla C.B.: Glycosylation of humanmilk lactoferrin exhibits dynamic changes during early lactationenhancing its role in pathogenic bacteria-host interactions. Mol.Cell. Proteomics, 2012; 11: M111
Google Scholar - 9. Becker D.J., Lowe J.B.: Fucose: biosynthesis and biologic functionin mammals. Glycobiology, 2003; 13: 41R-53R
Google Scholar - 10. Bertino E., Giuliani F., Occhi L., Coscia A., Tonetto P., MarchinoF., Fabris C.: Benefits of donor human milk for preterm infants: currentevidence. Early Hum. Dev., 2009; 85: S9-S10
Google Scholar - 11. Best T., Kemps E., Bryan J.: Effects of saccharides on brain functionand cognitive performance. Nutr. Rev., 2005; 63: 409-418
Google Scholar - 12. Bezirtzoglou E.: The intestinal microflora during the first weeksof life. Anaerobe, 1997; 3: 173-177
Google Scholar - 13. Bezirtzoglou E., Tsiotsias A., Welling G.W.: Microbiota profile infeces of breast- and formula-fed newborns by using fluorescence insitu hybridization (FISH). Anaerobe, 2011; 17: 478-482
Google Scholar - 14. Bienenstock J., Buck R.H., Linke H., Forsythe P., Stanisz A.M.,Kunze W.A.: Fucosylated but not sialylated milk oligosaccharidesdiminish colon motor contractions. PLoS One, 2013; 8: e76236
Google Scholar - 15. Bode L.: Human milk oligosaccharides: every baby needs a sugarmama. Glycobiology, 2012; 22: 1147-1162
Google Scholar - 16. Bode L.: Recent advances on structure, metabolism, and functionof human milk oligosaccharides. J. Nutr., 2006; 136: 2127-2130
Google Scholar - 17. Bode L., Jantscher-Krenn E.: Structure-function relationships ofhuman milk oligosaccharides. Adv. Nutr., 2012; 3: 383S-391SPiśmiennictwo
Google Scholar - 18. Canny G.O., McCormick B.A.: Bacteria in the intestine, helpfulresidents or enemies from within? Infect. Immun., 2008; 76: 3360-3373
Google Scholar - 19. Charlwood J., Hanrahan S., Tyldesley R., Langridge J., Dwek M.,Camilleri P.: Use of proteomic methodology for the characterizationof human milk fat globular membrane proteins. Anal. Biochem.,2002; 301: 314-324
Google Scholar - 20. Chaturvedi P., Warren C.D., Buescher C.R., Pickering L.K., NewburgD.S.: Survival of human milk oligosaccharides in the intestineof infants. Adv. Exp. Med. Biol., 2001; 501: 315-323
Google Scholar - 21. Coppa G.V., Bruni S., Morelli L., Soldi S., Gabrielli O.: The firstprebiotics in humans: human milk oligosaccharides. J. Clin. Gastroenterol.,2004; 38: S80-S83
Google Scholar - 22. Coppa G.V., Gabrielli O., Bertino E., Zampini L., Galeazzi T., PadellaL., Santoro L., Marchesiello R.L., Galeotti F., Maccari F., Volpi N.:Human milk glycosaminoglycans: the state of the art and futureperspectives. Ital. J. Pediatr., 2013; 39: 2
Google Scholar - 23. Coppa G.V., Pierani P., Zampini L., Carloni I., Carlucci A., GabrielliO.: Oligosaccharides in human milk during different phases oflactation. Acta Paediatr. Suppl. 430, 1999; 88: 89-94
Google Scholar - 24. Coppa G.V., Zampini L., Galeazzi T., Facinelli B., Ferrante L., CaprettiR., Orazio G.: Human milk oligosaccharides inhibit the adhesionto Caco-2 cells of diarrheal pathogens: Escherichia coli, Vibrio cholerae,and Salmonella fyris. Pediatr. Res., 2006; 59: 377-382
Google Scholar - 25. Crane J.K., Azar S.S., Stam A., Newburg D.S.: Oligosaccharidesfrom human milk block binding and activity of the Escherichia coliheat-stable enterotoxin (STa) in T84 intestinal cells. J. Nutr. 1994;124: 2358-2364
Google Scholar - 26. Cravioto A., Tello A., Villafán H., Ruiz J., del Vedovo S., Neeser J.R.:Inhibition of localized adhesion of enteropathogenic Escherichia colito HEp-2 cells by immunoglobulin and oligosaccharide fractions ofhuman colostrum and breast milk. J. Infect. Dis., 1991; 163: 1247-1255
Google Scholar - 27. Crost E.H., Tailford L.E., Le Gall G., Fons M., Henrissat B., Juge N.:Utilisation of mucin glycans by the human gut symbiont Ruminococcusgnavus is strain-dependent. PLoS One, 2013; 8: e76341
Google Scholar - 28. Dallas D.C., Martin W.F., Strum J.S., Zivkovic A.M., Smilowitz J.T.,Underwood M.A., Affolter M., Lebrilla C.B., German J.B.: N-linkedglycan profiling of mature human milk by high-performance microfluidicchip liquid chromatography time-of-flight tandem massspectrometry. J. Agric. Food Chem., 2011; 59: 4255-4263
Google Scholar - 29. Dallas D.C., Sela D., Underwood M.A., German J.B., Lebrilla C.:Protein-linked glycan degradation in infants fed human milk. J. GlycomicsLipidomics, 2012; Suppl. 1: 002
Google Scholar - 30. Darwin K.H., Miller V.L.: Molecular basis of the interaction ofSalmonella with the intestinal mucosa. Clin. Microbiol. Rev., 1999;12, 405-428
Google Scholar - 31. Day C.J., Semchenko E.A., Korolik V.: Glycoconjugates play a keyrole in Campylobacter jejuni infection: interactions between host andpathogen. Front. Cell. Infect. Microbiol., 2012; 2: 9
Google Scholar - 32. De Leoz M.L., Gaerlan S.C., Strum J.S., Dimapasoc L.M., MirmiranM., Tancredi D.J., Smilowitz J.T., Kalanetra K.M., Mills D.A., GermanJ.B., Lebrilla C.B., Underwood M.A.: Lacto-N-tetraose, fucosylation, and secretor status are highly variable in human milk oligosaccharidesfrom women delivering preterm. J. Proteome Res., 2012;11: 4662-4672
Google Scholar - 33. DiBiasie A.: Evidence-based review of retinopathy of prematurityprevention in VLBW and ELBW infants. Neonatal Netw., 2006;25: 393-403
Google Scholar - 34. Duska-McEwen G., Senft A.P, Ruetschilling T.L, Barrett E.G., BuckR.H.: Human milk oligosaccharides enhance innate immunity torespiratory syncytial virus and influenza in vitro. Food Nutr. Sci.,2014; 5: 1387-1398
Google Scholar - 35. Eidelman A.I.: Breastfeeding and the use of human milk: ananalysis of the American Academy of Pediatrics 2012 BreastfeedingPolicy Statement. Breastfeed. Med., 2012; 7: 323-324
Google Scholar - 36. Eiwegger T., Stahl B., Haidl P., Schmitt J., Boehm G., DehlinkE., Urbanek R., Szépfalusi Z.: Prebiotic oligosaccharides: in vitroevidence for gastrointestinal epithelial transfer and immunomodulatoryproperties. Pediatr. Allergy Immunol., 2010; 21: 1179-1188
Google Scholar - 37. Engfer M.B., Stahl B., Finke B., Sawatzki G., Daniel H.: Humanmilk oligosaccharides are resistant to enzymatic hydrolysis in theupper gastrointestinal tract. Am. J. Clin. Nutr., 2000; 71: 1589-1596
Google Scholar - 38. ESPGHAN Committee on Nutrition, Agostoni C., Braegger C., DecsiT., Kolacek S., Koletzko B., Michaelsen K.F., Mihatsch W., MorenoL.A., Puntis J., Shamir R., Szajewska H., Turck D., van Goudoever J.:Breast-feeding: a commentary by the ESPGHAN Committee on Nutrition.J. Pediatr. Gastroenterol. Nutr., 2009; 49: 112-125
Google Scholar - 39. Falk P., Roth K.A., Boren T., Westblom T.U., Gordon J.I., NormarkS.: An in vitro adherence assay reveals that Helicobacter pylori exhibitscell lineage-specific tropism in the human gastric epithelium. Proc.Natl. Acad. Sci. USA, 1993; 90: 2035-2039
Google Scholar - 40. Froehlich J.W., Dodds E.D., Barboza M., McJimpsey E.L., SeipertR.R., Francis J., An H.J., Freeman S., German J.B., Lebrilla C.B.: Glycoproteinexpression in human milk during lactation. J. Agric. FoodChem., 2010; 58: 6440-6448
Google Scholar - 41. Ganguli K., Walker W.A.: Probiotics in the prevention of necrotizingenterocolitis. J. Clin. Gastroenterol., 2011; 45: S133-S138
Google Scholar - 42. García-Montoya I.A., Cendón T.S., Arévalo-Gallegos S., RascónCruzQ.: Lactoferrin a multiple bioactive protein: an overview. Biochim.Biophys. Acta, 2012; 1820: 226-236
Google Scholar - 43. Garrido D., Dallas D.C., Mills D.A.: Consumption of human milkglycoconjugates by infant-associated bifidobacteria: mechanismsand implications. Microbiology, 2013; 159: 649-664
Google Scholar - 44. Georgi G., Bartke N., Wiens F., Stahl B.: Functional glycans andglycoconjugates in human milk. Am. J. Clin. Nutr., 2013; 98: 578S-585S
Google Scholar - 45. Gnoth M.J., Kunz C., Kinne-Saffran E., Rudloff S.: Human milkoligosaccharides are minimally digested in vitro. J. Nutr., 2000; 130:3014-3020
Google Scholar - 46. Goehring K.C., Kennedy A.D., Prieto P.A., Buck R.H.: Direct evidencefor the presence of human milk oligosaccharides in the circulationof breastfed infants. PLoS One, 2014; 9: e101692
Google Scholar - 47. Goldman A.S.: The immune system in human milk and the developinginfant. Breastfeed. Med., 2007; 2: 195-204
Google Scholar - 48. Goldman A.S., Chheda S., Garofalo R.: Evolution of immunologicfunctions of the mammary gland and the postnatal development ofimmunity. Pediatr. Res., 1998; 43: 155-162
Google Scholar - 49. Górska S., Jarząb A., Gamian A.: Bakterie probiotyczne w przewodziepokarmowym człowieka jako czynnik stymulujący układodpornościowy. Postępy Hig. Med. Dośw., 2009; 63: 653-667
Google Scholar - 50. Hanisch F.G., Müller S.: MUC1: the polymorphic appearance ofa human mucin. Glycobiology, 2000; 10: 439-449
Google Scholar - 51. Harmsen H.J., Wildeboer-Veloo A.C., Raangs G.C., WagendorpA.A., Klijn N., Bindels J.G., Welling G.W.: Analysis of intestinal floradevelopment in breast-fed and formula-fed infants by using molecularidentification and detection methods. J. Pediatr. Gastroenterol.Nutr., 2000; 30: 61-67
Google Scholar - 52. Hart G.W.: Sweet insights into learning and memory. Nat. Chem.Biol., 2006; 2: 67-68
Google Scholar - 53. Hylander M.A., Strobino D.M., Dhanireddy R.: Human milk feedingsand infection among very low birth weight infants. Pediatrics,1998; 102: E38
Google Scholar - 54. Jiang X., Huang P., Zhong W., Tan M., Farkas T., Morrow A.L.,Newburg D.S., Ruiz-Palacios G.M., Pickering L.K.: Human milk containselements that block binding of noroviruses to human histobloodgroup antigens in saliva. J. Infect. Dis., 2004; 190: 1850-1859
Google Scholar - 55. Katayama T., Sakuma A., Kimura T., Makimura Y., Hiratake J.,Sakata K., Yamanoi T., Kumagai H., Yamamoto K.: Molecular cloningand characterization of Bifidobacterium bifidum 1,2-α-L-fucosidase(AfcA), a novel inverting glycosidase (glycoside hydrolase family95). J. Bacteriol., 2004; 186: 4885-4893
Google Scholar - 56. Kątnik-Prastowska I., Orczyk-Pawiłowicz M.: Expression andpotential biological role of α(1,2)fucosylated glycotopes on amnioticand seminal fibronectins. Biochem. Soc. Trans., 2011; 39: 355-359
Google Scholar - 57. Koning N., Kessen S.F., Van Der Voorn J.P., Appelmelk B.J., JeurinkP.V., Knippels L.M., Garssen J., Van Kooyk Y.: Human milk blocks DCSIGN-pathogeninteraction via MUC1. Front. Immunol., 2015; 6: 112
Google Scholar - 58. Landberg E., Huang Y., Strömqvist M., Mechref Y., Hansson L.,Lundblad A., Novotny M.V., Påhlsson P.: Changes in glycosylation ofhuman bile-salt-stimulated lipase during lactation. Arch. Biochem.Biophys., 2000; 377: 246-254
Google Scholar - 59. Lesman-Movshovich E., Lerrer B., Gilboa-Garber N.: Blockingof Pseudomonas aeruginosa lectins by human milk glycans. Can. J.Microbiol., 2003; 49: 230-235
Google Scholar - 60. Liao Y., Alvarado R., Phinney B., Lönnerdal B.: Proteomic characterizationof human milk fat globule membrane proteins duringa 12 month lactation period. J. Proteome Res., 2011; 10: 3530-3541
Google Scholar - 61. Lin A.E, Autran C.A., Espanola S.D., Bode L., Nizet V.: Humanmilk oligosaccharides protect bladder epithelial cells against uropathogenicEscherichia coli invasion and cytotoxicity. J. Infect. Dis.,2014; 209: 389-398
Google Scholar - 62. Lis J., Orczyk-Pawiłowicz M., Kątnik-Prastowska I.: Białka mlekaludzkiego zaangażowane w procesy immunologiczne. Postępy Hig.Med. Dośw., 2013; 67: 529-547
Google Scholar - 63. Liu B., Newburg D.S.: Human milk glycoproteins protect infantsagainst human pathogens. Breastfeed. Med., 2013; 8: 354-362
Google Scholar - 64. Liu B., Yu Z., Chen C., Kling D.E., Newburg D.S.: Human milk mucin 1 and mucin 4 inhibit Salmonella enterica serovar Typhimurium invasionof human intestinal epithelial cells in vitro. J. Nutr., 2012; 142: 1504-1509
Google Scholar - 65. LoCascio R.G., Ninonuevo M.R., Freeman S.L., Sela D.A., Grimm R.,Lebrilla C.B., Mills D.A., German J.B.: Glycoprofiling of bifidobacterialconsumption of human milk oligosaccharides demonstrates strainspecific, preferential consumption of small chain glycans secretedin early human lactation. J. Agric. Food Chem., 2007; 55: 8914-8919
Google Scholar - 66. Lorenzini C.G., Baldi E., Bucherelli C., Sacchetti B., Tassoni G.:2-Deoxy-D-galactose effects on passive avoidance memorization inthe rat. Neurobiol. Learn. Mem., 1997; 68: 317-324
Google Scholar - 67. Macpherson A.J., Harris N.L.: Interactions between commensalintestinal bacteria and the immune system. Nat. Rev. Immunol.,2004; 4: 478-485
Google Scholar - 68. Marcobal A., Barboza M., Froehlich J.W., Block D.E., GermanJ.B., Lebrilla C.B., Mills D.A.: Consumption of human milk oligosaccharidesby gut-related microbes. J. Agric. Food Chem., 2010; 58:5334-5340
Google Scholar - 69. Martin-Sosa S., Martin M.J., Hueso P.: The sialylated fraction ofmilk oligosaccharides is partially responsible for binding to enterotoxigenic and uropathogenic Escherichia coli human strains. J. Nutr.,2002; 132: 3067-3072
Google Scholar - 70. Matthies H., Staak S., Krug M.: Fucose and fucosyllactose enhancein-vitro hippocampal long-term potentiation. Brain Res., 1996;725: 276-280
Google Scholar - 71. McGuire W., Anthony M.Y.: Donor human milk versus formulafor preventing necrotising enterocolitis in preterm infants: systematicreview. Arch. Dis. Child. Fetal Neonatal Ed., 2003; 88: F11-F14
Google Scholar - 72. Mehra R., Barile D., Marotta M., Lebrilla C.B., Chu C., GermanJ.B.: Novel high-molecular weight fucosylated milk oligosaccharidesidentified in dairy streams. PLoS One, 2014; 9: e96040
Google Scholar - 73. Molinari C.E., Casadio Y.S., Hartmann B.T., Livk A., BringansS., Arthur P.G., Hartmann P.E.: Proteome mapping of human skimmilk proteins in term and preterm milk. J. Proteome Res., 2012; 11:1696-1714
Google Scholar - 74. Morowitz M.J., Poroyko V., Caplan M., Alverdy J., Liu D.C.: Redefiningthe role of intestinal microbes in the pathogenesis of necrotizingenterocolitis. Pediatrics, 2010; 125: 777-785
Google Scholar - 75. Morrow A.L., Ruiz-Palacios G.M., Jiang X., Newburg D.S.: Humanmilkglycans that inhibit pathogen binding protect breast-feedinginfants against infectious diarrhea. J. Nutr., 2005; 135: 1304-1307
Google Scholar - 76. Murrey H.E., Gama C.I., Kalovidouris S.A., Luo W.I., Driggers E.M.,Porton B., Hsieh-Wilson L.C.: Protein fucosylation regulates synapsinIa/Ib expression and neuronal morphology in primary hippocampalneurons. Proc. Natl. Acad. Sci. USA, 2006; 103: 21-26
Google Scholar - 77. Naarding M.A., Dirac A.M., Ludwig I.S., Speijer D., LindquistS., Vestman E.L., Stax M.J., Geijtenbeek T.B., Pollakis G., Hernell O.,Paxton W.A.: Bile salt-stimulated lipase from human milk binds DCSIGNand inhibits human immunodeficiency virus type 1 transferto CD4+ T cells. Antimicrob. Agents Chemother., 2006; 50: 3367-3374
Google Scholar - 78. Naarding M.A., Ludwig I.S., Groot F., Berkhout B., GeijtenbeekT.B., Pollakis G., Paxton W.A.: Lewis X component in human milkbinds DC-SIGN and inhibits HIV-1 transfer to CD4+ T lymphocytes.J. Clin. Invest., 2005; 115: 3256-3264
Google Scholar - 79. Newburg D.S.: Neonatal protection by an innate immune systemof human milk consisting of oligosaccharides and glycans. J. Anim.Sci., 2009; 87, Suppl. 1: 26-34
Google Scholar - 80. Newburg D.S., Pickering L.K., McCluer R.H., Cleary T.G.: Fucosylatedoligosaccharides of human milk protect suckling mice fromheat-stabile enterotoxin of Escherichia coli. J. Infect. Dis., 1990; 162:1075-1080
Google Scholar - 81. Nwosu C.C., Aldredge D.L., Lee H., Lerno L.A., Zivkovic A.M., GermanJ.B., Lebrilla C.B.: Comparison of the human and bovine milkN-glycome via high-performance microfluidic chip liquid chromatographyand tandem mass spectrometry. J. Proteome Res., 2012;11: 2912-2924
Google Scholar - 82. Orczyk-Pawiłowicz M.: Znaczenie fukozylacji glikokoniugatóww zdrowiu i chorobie. Postępy Hig. Med. Dośw., 2007; 61: 240-252
Google Scholar - 83. Orczyk-Pawiłowicz M., Hirnle L., Berghausen-Mazur M., KątnikPrastowskaI.: Lactation stage-related expression of sialylated andfucosylated glycotopes of human milk α-1-acid glycoprotein. Breastfeed.Med., 2014; 9: 313-319
Google Scholar - 84. Orczyk-Pawiłowicz M., Hirnle L., Berghausen-Mazur M., KątnikPrastowskaI.: Terminal glycotope expression on milk fibronectindiffers from plasma fibronectin and changes over lactation. Clin.Biochem., 2015; 48: 167-173
Google Scholar - 85. Pan F., Zhao X., Waigh T.A., Lu J.R., Miano F.: Interfacial adsorptionand denaturization of human milk and recombinant rice lactoferrin.Biointerphases, 2008; 3: FB36
Google Scholar - 86. Parry S., Hanisch F.G., Leir S.H., Sutton-Smith M., Morris H.R.,Dell A., Harris A.: N-Glycosylation of the MUC1 mucin in epithelialcells and secretions. Glycobiology, 2006; 16: 623-634
Google Scholar - 87. Patton S.: Detection of large fragments of the human milk mucinMUC-1 in feces of breast-fed infants. J. Pediatr. Gastroenterol.Nutr., 1994; 18: 225-230
Google Scholar - 88. Patton S., Gendler S.J., Spicer A.P.: The epithelial mucin, MUC1,of milk, mammary gland and other tissues. Biochim. Biophys. Acta,1995; 1241: 407-423
Google Scholar - 89. Penders J., Thijs C., Vink C., Stelma F.F., Snijders B., KummelingI., van den Brandt P.A., Stobberingh E.E.: Factors influencing thecomposition of the intestinal microbiota in early infancy. Pediatrics,2006; 118: 511-521
Google Scholar - 90. Perret S., Sabin C., Dumon C., Pokorná M., Gautier C., GalaninaO., Ilia S., Bovin N., Nicaise M., Desmadril M., Gilboa-Garber N., WimmerováM., Mitchell E.P., Imberty A.: Structural basis for the interactionbetween human milk oligosaccharides and the bacterial lectinPA-IIL of Pseudomonas aeruginosa. Biochem. J., 2005; 389: 325-332
Google Scholar - 91. Peterson R., Cheah W.Y., Grinyer J., Packer N.: Glycoconjugatesin human milk: protecting infants from disease. Glycobiology, 2013;23: 1425-1438
Google Scholar - 92. Pohle W., Acosta L., Rüthrich H., Krug M., Matthies H.: Incorporationof [3H]fucose in rat hippocampal structures after conditioningby perforant path stimulation and after LTP-producing tetanization.Brain Res., 1987; 410: 245-256
Google Scholar - 93. Pytrus T., Iwańczak F.: Leczenie ostrych biegunek u dzieci. NowaPediatria, 2002; 3: 149-158
Google Scholar - 94. Reynolds J.D.: The management of retinopathy of prematurity.Paediatr. Drugs, 2001; 3: 263-272
Google Scholar - 95. Royle L., Roos A., Harvey D.J., Wormald M.R., van Gijlswijk-JanssenD., Redwan el-R.M., Wilson I.A., Daha M.R., Dwek R.A., Rudd P.M.:Secretory IgA N- and O-glycans provide a link between the innateand adaptive immune systems. J. Biol. Chem., 2003; 278: 20140-20153
Google Scholar - 96. Ruiz-Moyano S., Totten S.M., Garrido D.A., Smilowitz J.T., GermanJ.B., Lebrilla C.B., Mills D.A.: Variation in consumption of humanmilk oligosaccharides by infant gut-associated strains of Bifidobacteriumbreve. Appl. Environ. Microbiol., 2013; 79: 6040-6049
Google Scholar - 97. Ruiz-Palacios G.M., Cervantes L.E., Ramos P., Chavez-MunguiaB., Newburg D.S.: Campylobacter jejuni binds intestinal H(O) antigen(Fucα1,2Galβ1,4GlcNAc), and fucosyloligosaccharides of humanmilk inhibit its binding and infection. J. Biol. Chem., 2003; 278:14112-14120
Google Scholar - 98. Ruvoën-Clouet N., Mas E., Marionneau S., Guillon P., LombardoD., Le Pendu J.: Bile-salt-stimulated lipase and mucins from milk of‚secretor’ mothers inhibit the binding of Norwalk virus capsids totheir carbohydrate ligands. Biochem. J., 2006; 393: 627-634
Google Scholar - 99. Saeland E., de Jong M.A., Nabatov A.A., Kalay H., GeijtenbeekT.B., van Kooyk Y.: MUC1 in human milk blocks transmission of humanimmunodeficiency virus from dendritic cells to T cells. Mol.Immunol., 2009; 46: 2309-2316
Google Scholar - 100. Savino F., Cordisco L., Tarasco V., Locatelli E., Di Gioia D., OggeroR., Matteuzzi D.: Antagonistic effect of Lactobacillus strains againstgas-producing coliforms isolated from colicky infants. BMC Microbiol.,2011; 11: 157
Google Scholar - 101. Savino F., Cresi F., Pautasso S., Palumeri E., Tullio V., Roana J.,Silvestro L., Oggero R.: Intestinal microflora in breastfed colicky andnon-colicky infants. Acta Paediatr., 2004; 93: 825-829
Google Scholar - 102. Sela D.A., Garrido D., Lerno L., Wu S., Tan K., Eom H.J., JoachimiakA., Lebrilla C.B., Mills D.A.: Bifidobacterium longum subsp.infantis ATCC 15697 α-fucosidases are active on fucosylated humanmilk oligosaccharides. Appl. Environ. Microbiol., 2012; 78: 795-803
Google Scholar - 103. Sharon N., Ofek I.: Safe as mother’s milk: carbohydrates as futureanti-adhesion drugs for bacterial diseases. Glycoconj. J., 2000;17: 659-664
Google Scholar - 104. Sheinfeld J., Schaeffer A.J., Cordon-Cardo C., Rogatko A., FairW.R.: Association of the Lewis blood-group phenotype with recurrenturinary tract infections in women. N. Engl. J. Med., 1989; 320: 773-777
Google Scholar - 105. Smilowitz J.T., Totten S.M., Huang J., Grapov D., Durham H.A.,Lammi-Keefe C.J., Lebrilla C., German J.B.: Human milk secretoryimmunoglobulin A and lactoferrin N-glycans are altered in womenwith gestational diabetes mellitus. J. Nutr., 2013; 143: 1906-1912
Google Scholar - 106. Staudacher E., Altmann F., Wilson I.B., März L.: Fucose in N-glycans:from plant to man. Biochim. Biophys. Acta, 1999; 1473: 216-236
Google Scholar - 107. Thum C., Cookson A.L., Otter D.E., McNabb W.C., HodgkinsonA.J., Dyer J., Roy N.C.: Can nutritional modulation of maternal intestinalmicrobiota influence the development of the infant gastrointestinaltract? J. Nutr., 2012; 142: 1921-1928
Google Scholar - 108. Totten S.M., Zivkovic A.M., Wu S., Ngyuen U., Freeman S.L.,Ruhaak L.R., Darboe M.K., German J.B., Prentice A.M., Lebrilla C.B.:Comprehensive profiles of human milk oligosaccharides yield highlysensitive and specific markers for determining secretor status inlactating mothers. J. Proteome Res., 2012; 11: 6124-6133
Google Scholar - 109. Tu Z., Lin Y.N., Lin C.H.: Development of fucosyltransferase andfucosidase inhibitors. Chem. Soc. Rev., 2013; 42: 4459-4475
Google Scholar - 110. Urashima T., Asakuma S., Leo F., Fukuda K., Messer M., OftedalO.T.: The predominance of type I oligosaccharides is a feature specificto human breast milk. Adv. Nutr., 2012; 3: 473S-482S
Google Scholar - 111. van Berkel P.H., van Veen H.A., Geerts M.E., de Boer H.A.,Nuijens J.H.: Heterogeneity in utilization of N-glycosylation sitesAsn624 and Asn138 in human lactoferrin: a study with glycosylation-sitemutants. Biochem. J., 1996; 319: 117-122
Google Scholar - 112. van Neerven R.J., Knol E.F., Heck J.M., Savelkoul H.F.: Whichfactors in raw cow’s milk contribute to protection against allergies?J. Allergy Clin. Immunol., 2012; 130: 853-858
Google Scholar - 113. Wacklin P., Mäkivuokko H., Alakulppi N., Nikkilä J., Tenkanen H.,Räbinä J., Partanen J., Aranko K., Mättö J.: Secretor genotype (FUT2gene) is strongly associated with the composition of Bifidobacteriain the human intestine. PLoS One, 2011; 6: e20113
Google Scholar - 114. Wang B., Mao Y.K., Diorio C., Pasyk M., Wu R.Y., BienenstockJ., Kunze W.A.: Luminal administration ex vivo of a live Lactobacillusspecies moderates mouse jejunal motility within minutes. FASEB J.,2010; 24: 4078-4088
Google Scholar - 115. Wang C.S., Dashti A., Jackson K.W., Yeh J.C., Cummings R.D.,Tang J.: Isolation and characterization of human milk bile salt-activatedlipase C-tail fragment. Biochemistry, 1995; 34: 10639-10644
Google Scholar - 116. Weichert S., Jennewein S., Hüfner E., Weiss C., Borkowski J.,Putze J., Schroten H.: Bioengineered 2’-fucosyllactose and 3-fucosyllactoseinhibit the adhesion of Pseudomonas aeruginosa and entericpathogens to human intestinal and respiratory cell lines. Nutr.Res., 2013; 33: 831-838
Google Scholar - 117. Wiederschain G.Y., Newburg D.S.: Glycoconjugate stability inhuman milk: glycosidase activities and sugar release. J. Nutr. Biochem.,2001; 12: 559-564
Google Scholar - 118. Wilson N.L., Robinson L.J., Donnet A., Bovetto L., Packer N.H.,Karlsson N.G.: Glycoproteomics of milk: differences in sugar epitopeson human and bovine milk fat globule membranes. J. ProteomeRes., 2008; 7: 3687-3696
Google Scholar - 119. World Health Organizationhttp://www.who.int/nutrition/publications/infantfeeding/nut_adequacy_of_exc_bfeeding_eng (07.10.2014)
Google Scholar - 120. Wu S., Grimm R., German J.B., Lebrilla C.B.: Annotation andstructural analysis of sialylated human milk oligosaccharides. J.Proteome Res., 2011; 10: 856-868
Google Scholar - 121. Wu S., Tao N., German J.B., Grimm R., Lebrilla C.B.: Developmentof an annotated library of neutral human milk oligosaccharides. J.Proteome Res., 2010; 9: 4138-4151
Google Scholar - 122. Yen M.H., Wu A.M., Yang Z., Gong Y.P., Chang E.T.: Recognitionroles of the carbohydrate glycotopes of human and bovine lactofer rins in lectin-N-glycan interactions. Biochim. Biophys. Acta, 2011;1810: 139-149
Google Scholar - 123. Yu Z.T., Chen C., Kling D.E., Liu B., McCoy J.M., Merighi M., HeidtmanM., Newburg D.S.: The principal fucosylated oligosaccharidesof human milk exhibit prebiotic properties on cultured infantmicrobiota. Glycobiology, 2013; 23: 169-177
Google Scholar - 124. Yu Z.T., Chen C., Newburg D.S.: Utilization of major fucosylatedand sialylated human milk oligosaccharides by isolated human gutmicrobes. Glycobiology, 2013; 23: 1281-1292
Google Scholar - 125. Zimecki M., Artym J.: Therapeutic properties of proteins andpeptides from colostrum and milk. Postępy Hig. Med. Dośw., 2005;59: 309-323
Google Scholar