Direct evidence for the presence of human milk oligosaccharides in the circulation of breastfed infants

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Goehring, Karen C ^a   Kennedy, Adam D ^b   Prieto, Pedro A ^a   Buck, Rachael H ^a  

^a ABBOTT LABORATORIES   (United States)

^b METABOLON INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2' FUCOSYLLACTOSE; 3' FUCOSYLLACTOSE; HUMAN MILK OLIGOSACCHARIDE; LACTO N NEOTETRAOSE; OLIGOSACCHARIDE; UNCLASSIFIED DRUG; 2'-FUCOSYLLACTOSE; LACTO-N-NEOTETRAOSE; TRISACCHARIDE;

ARTICLE; ARTIFICIAL MILK; BLOOD ANALYSIS; BREAST FEEDING; BREAST MILK; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; INFANT; LIQUID CHROMATOGRAPHY; MASS FRAGMENTOGRAPHY; NORMAL HUMAN; TANDEM MASS SPECTROMETRY; URINALYSIS; BLOOD; CHEMISTRY; FEMALE; MOTHER; PREGNANCY; URINE;

BREAST FEEDING; FEMALE; HUMANS; INFANT; MILK, HUMAN; MOTHERS; OLIGOSACCHARIDES; PREGNANCY; TRISACCHARIDES;

EID: 84904339148     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101692     Document Type: Article

References (54)

1. Ninonuevo MR, Lebrilla CB (2009) Mass spectrometric methods for analysis of oligosaccharides in human milk. Nutr Rev 67 Suppl 2: S216-S226.
2. Fong B, Ma K, McJarrow P (2011) Quantification of bovine milk oligosaccharides using liquid chromatography-selected reaction monitoring-mass spectrometry. J Agric Food Chem 59: 9788-9795.
3. Chaturvedi P, Warren CD, Altaye M, Morrow AL, Ruiz-Palacios G, et al. (2001) Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology 11: 365-372. (Pubitemid 32685211)
4. Thurl S, Henker J, Taut H, Tovar K, Sawatzki G (1993) Variations of neutral oligosaccharides and lactose in human milk during the feeding. Z Ernahrungswiss 32: 262-269. (Pubitemid 24011305)
5. Asakuma S, Urashima T, Akahori M, Obayashi H, Nakamura T, et al. (2008) Variation of major neutral oligosaccharides levels in human colostrum. Eur J Clin Nutr 62: 488-494.
6. Thurl S, Munzert M, Henker J, Boehm G, Muller-Werner B, et al. (2010) Variation of human milk oligosaccharides in relation to milk groups and lactational periods. Br J Nutr 104: 1261-1271.
7. De Leoz ML, Gaerlan SC, Strum JS, Dimapasoc LM, Mirmiran M, 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: 4662-4672.
8. Kunz C, Rudloff S, Baier W, Klein N, Strobel S (2000) Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr 20: 699-722.
9. Totten SM, Zivkovic AM, Wu S, Ngyuen U, Freeman SL, 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: 6124-6133.
10. Erney RM, Malone WT, Skelding MB, Marcon AA, Kleman-Leyer KM, et al. (2000) Variability of human milk neutral oligosaccharides in a diverse population. J Pediatr Gastroenterol Nutr 30: 181-192. (Pubitemid 30366196)
11. Prieto PA (2012) Profiles of human milk oligosaccharides and production of some human milk oligosaccharides in transgenic animals. Adv Nutr 3: 456S-464S.
12. Blaymore Bier JA, Oliver T, Ferguson A, Vohr BR (2002) Human milk reduces outpatient upper respiratory symptoms in premature infants during their first year of life. J Perinatol 22: 354-359.
13. Duijts L, Jaddoe VW, Hofman A, Moll HA (2010) Prolonged and exclusive breastfeeding reduces the risk of infectious diseases in infancy. Pediatrics 126: e18-e25.
14. Ip S, Chung M, Raman G, Chew P, Magula N, et al. (2007) Breastfeeding and maternal and infant health outcomes in developed countries. Evid Rep Technol Assess (Full Rep) 1-186.
15. Kramer MS, Guo T, Platt RW, Sevkovskaya Z, Dzikovich I, et al. (2003) Infant growth and health outcomes associated with 3 compared with 6 mo of exclusive breastfeeding. Am J Clin Nutr 78: 291-295. (Pubitemid 39655234)
16. Quigley MA, Kelly YJ, Sacker A (2007) Breastfeeding and hospitalization for diarrheal and respiratory infection in the United Kingdom Millennium Cohort Study. Pediatrics 119: e837-e842. (Pubitemid 46556646)
17. Labbok MH, Clark D, Goldman AS (2004) Breastfeeding: maintaining an irreplaceable immunological resource. Nat Rev Immunol 4: 565-572. (Pubitemid 38931771)
18. Penttila IA (2010) Milk-derived transforming growth factor-beta and the infant immune response. J Pediatr 156: S21-S25.
19. Stepans MB, Wilhelm SL, Hertzog M, Rodehorst TK, Blaney S, et al. (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.
20. Yu ZT, Chen C, Kling DE, Liu B, McCoy JM, et al. (2013) The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology 23: 169-177.
21. Yang B, Chuang H, Chen RF (2012) Protection from Viral Infections by Human Milk Oligosaccharides: Direct Blockade and Indirect Modulation of Intestinal Ecology and Immune Reactions. Open Glycoscience 5: 19-25.
22. LoCascio RG, Ninonuevo MR, Freeman SL, Sela DA, Grimm R, 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: 8914-8919. (Pubitemid 350105536)
23. Marcobal A, Barboza M, Froehlich JW, Block DE, German JB, et al. (2010) Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem 58: 5334-5340.
24. Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, et al. (2011) Physiology of consumption of human milk oligosaccharides by infant gutassociated bifidobacteria. J Biol Chem 286: 34583-34592.
25. Espinosa RM, Tamez M, Prieto P (2007) Efforts to emulate human milk oligosaccharides. Br J Nutr 98 Suppl 1: S74-S79. (Pubitemid 47543482)
26. Bode L (2012) Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 22: 1147-1162.
27. Kuntz S, Rudloff S, Kunz C (2008) Oligosaccharides from human milk influence growth-related characteristics of intestinally transformed and non-transformed intestinal cells. Br J Nutr 99: 462-471. (Pubitemid 351223413)
28. Rabinovich GA, van Kooyk Y, Cobb BA (2012) Glycobiology of immune responses. Ann N Y Acad Sci 1253: 1-15.
29. de Kivit S, Kraneveld AD, Garssen J, Willemsen LE (2011) Glycan recognition at the interface of the intestinal immune system: target for immune modulation via dietary components. Eur J Pharmacol 668 Suppl 1: S124-S132.
30. Rudloff S, Pohlentz G, Borsch C, Lentze MJ, Kunz C (2012) Urinary excretion of in vivo 13C-labelled milk oligosaccharides in breastfed infants. Br J Nutr 107: 957-963.
31. Gnoth MJ, Rudloff S, Kunz C, Kinne RK (2001) Investigations of the in vitro transport of human milk oligosaccharides by a Caco-2 monolayer using a novel high performance liquid chromatography-mass spectrometry technique. J Biol Chem 276: 34363-34370.
32. Gall WE, Beebe K, Lawton KA, Adam KP, Mitchell MW, et al. (2010) alpha-hydroxybutyrate is an early biomarker of insulin resistance and glucose intolerance in a nondiabetic population. PLoS One 5: e10883.
33. Takei M, Ando Y, Saitoh W, Tanimoto T, Kiyosawa N, et al. (2010) Ethylene glycol monomethyl ether-induced toxicity is mediated through the inhibition of flavoprotein dehydrogenase enzyme family. Toxicol Sci 118: 643-652.
34. Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E (2009) Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem 81: 6656-6667.
35. DeHaven CD, Evans AM, Dai H, Lawton KA (2010) Organization of GC/MS and LC/MS metabolomics data into chemical libraries. J Cheminform 2: 9.
36. Thurl S, Muller-Werner B, Sawatzki G (1996) Quantification of individual oligosaccharide compounds from human milk using high-pH anion-exchange chromatography. Anal Biochem 235: 202-206.
37. Radzanowski G, Garrett P, Li X, Anita M (2013) Short-chain milk oligosaccharide levels in human milk and infant plasma. FASEB J 27: Abstract 629.16.
38. De Leoz ML, Wu S, Strum JS, Ninonuevo MR, Gaerlan SC, et al. (2013) A quantitative and comprehensive method to analyze human milk oligosaccharide structures in the urine and feces of infants. Anal Bioanal Chem.
39. Martin-Sosa S, Martin MJ, Garcia-Pardo LA, Hueso P (2003) Sialyloligosaccharides in human and bovine milk and in infant formulas: variations with the progression of lactation. J Dairy Sci 86: 52-59. (Pubitemid 39067160)
40. Matrosovich M, Klenk HD (2003) Natural and synthetic sialic acid-containing inhibitors of influenza virus receptor binding. Rev Med Virol 13: 85-97. (Pubitemid 36323672)
41. Yamamoto K (2012) Biological analysis of the microbial metabolism of heterooligosaccharides in application to glycotechnology. Biosci Biotechnol Biochem 76: 1815-1827.
42. Prieto PA (2005) In Vitro and Clinical Experiences with a Human Milk Oligosaccharide, Lacto-N-neoTetraose, and Fructooligosaccharides. Foods Foods Ingredient J JAPAN 219: 1018-1030.
43. Fanaro S, Boehm G, Garssen J, Knol J, Mosca F, et al. (2005) Galactooligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: a review. Acta Paediatr Suppl 94: 22-26.
44. Eiwegger T, Stahl B, Haidl P, Schmitt J, Boehm G, et al. (2010) Prebiotic oligosaccharides: in vitro evidence for gastrointestinal epithelial transfer and immunomodulatory properties. Pediatr Allergy Immunol 21: 1179-1188.
45. Zivkovic AM, Barile D (2011) Bovine milk as a source of functional oligosaccharides for improving human health. Adv Nutr 2: 284-289.
46. Dotz V, Rudloff S, Blank D, Lochnit G, Geyer R, et al. (2014) 13C-labeled oligosaccharides in breastfed infants' urine: Individual-, structure- and time-dependent differences in the excretion. Glycobiology 24: 185-194.
47. Rudloff S, Obermeier S, Borsch C, Pohlentz G, Hartmann R, et al. (2006) Incorporation of orally applied (13)C-galactose into milk lactose and oligosaccharides. Glycobiology 16: 477-487. (Pubitemid 43779044)
48. Rudloff S, Pohlentz G, Diekmann L, Egge H, Kunz C (1996) Urinary excretion of lactose and oligosaccharides in preterm infants fed human milk or infant formula. Acta Paediatr 85: 598-603. (Pubitemid 26178509)
49. Jantscher-Krenn E, Bode L (2012) Human milk oligosaccharides and their potential benefits for the breast-fed neonate. Minerva Pediatr 64: 83-99.
50. Eiwegger T, Stahl B, Schmitt J, Boehm G, Gerstmayr M, et al. (2004) Human milk - derived oligosaccharides and plant-derived oligosaccharides stimulate cytokine production of cord blood T-cells in vitro. Pediatr Res 56: 536-540. (Pubitemid 39280905)
51. Bode L, Rudloff S, Kunz C, Strobel S, Klein N (2004) Human milk oligosaccharides reduce platelet-neutrophil complex formation leading to a decrease in neutrophil beta 2 integrin expression. J Leukoc Biol 76: 820-826. (Pubitemid 39313718)
52. Bode L, Kunz C, Muhly-Reinholz M, Mayer K, Seeger W, et al. (2004) Inhibition of monocyte, lymphocyte, and neutrophil adhesion to endothelial cells by human milk oligosaccharides. Thromb Haemost 92: 1402-1410. (Pubitemid 39642553)
53. Sotgiu S, Arru G, Fois ML, Sanna A, Musumeci M, et al. (2006) Immunomodulation of fucosyl-lactose and lacto-N-fucopentaose on mononuclear cells from multiple sclerosis and healthy subjects. International Journal of Biomedical Science 2: 114-120.
54. Naarding MA, Ludwig IS, Groot F, Berkhout B, Geijtenbeek TB, et al. (2005) Lewis X component in human milk binds DC-SIGN and inhibits HIV-1 transfer to CD4+ T lymphocytes. J Clin Invest 115: 3256-3264. (Pubitemid 41567590)