Host-microbe interactions in the neonatal intestine: Role of human milk oligosaccharides

Advances in Nutrition

Volumn 3, Issue 3, 2012, Pages

  Donovan, Sharon M ^a   Wang, Mei ^a   Li, Min ^a   Friedberg, Iddo ^b   Schwartz, Scott L ^c   Chapkin, Robert S ^c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b MIAMI UNIVERSITY   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGOSACCHARIDE; PREBIOTIC AGENT; TRANSCRIPTOME; VOLATILE FATTY ACID;

ANIMAL; ARTIFICIAL MILK; BACTERIAL GENE; BREAST FEEDING; BREAST MILK; CHEMISTRY; EPITHELIUM CELL; FECES; GENE EXPRESSION PROFILING; HUMAN; INFANT; INTESTINE; METABOLISM; METAGENOME; MICROBIOLOGY; MILK; PHYLOGENY; REVIEW; SWINE;

ANIMALS; BREAST FEEDING; EPITHELIAL CELLS; FATTY ACIDS, VOLATILE; FECES; GENE EXPRESSION PROFILING; GENES, BACTERIAL; HUMANS; INFANT; INFANT FORMULA; INTESTINES; METAGENOME; MILK; MILK, HUMAN; OLIGOSACCHARIDES; PHYLOGENY; PREBIOTICS; SWINE; TRANSCRIPTOME;

EID: 84866776469     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.112.001859     Document Type: Article

References (63)

1. Murgas Torrazza R, Neu J. The developing intestinal microbiome and its relationship to health and disease in the neonate. J Perinatol. 2011;31:Suppl 1:S29-34.
2. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5:e177.
3. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107:11971-5.
4. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, Welling GW. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification band detection methods. J Pediatr Gastroenterol Nutr. 2000;30:61-7.
5. Spor A, Koren O, Ley R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol. 2011;9:279-90.
6. Zivkovic AM, German JB, Lebrilla CB, Mills DA. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci U S A. 2011;108:Suppl 1:4653-8.
7. Donovan SM. Role of human milk components in gastrointestinal development: current knowledge and future needs. J Pediatr. 2006;149:S49-61.
8. Palmer AC. Nutritionally mediated programming of the developing immune system. Adv Nutr. 2011;2:377-95.
9. Newburg DS. Neonatal protection by an innate immune system of human milk consisting of oligosaccharides and glycans. J Anim Sci. 2009; 87:13 Suppl:26-34.
10. Kaplan JL, Shi HN, Walker WA. The role of microbes in developmental immunologic programming. Pediatr Res. 2011;69:465-72.
11. Gartner LM, Morton J, Lawrence RA, Naylor AJ, O'Hare D, Schanler RJ, Eidelman AI; American Academy of PediatricsSection on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics. 2005; 115:496-506.
12. Dewey KG, Heinig MJ, Nommsen-Rivers LA. Differences in morbidity between breast fed and formula-fed infants. J Pediatr. 1995;126:696-702.
13. Heinig MJ. Host defense benefits of breastfeeding for the infant. Effect of breastfeeding duration and exclusivity. Pediatr Clin North Am. 2001; 48:105-23.
14. Yoshioka H, Iseki K, Fujita K. Development and differences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants. Pediatrics. 1983;72:317-21.
15. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A. 2011;108:Suppl 1:4578-85.
16. Boesten R, Schuren F, Ben AmoreK,HaarmanM, Know J, deVosWM. Bifidobacterium population analysis in the infant gut by direct mapping of genomic hybridization patterns:potential for monitoring temporal development and effects of dietary regimens. Microb Biotechnol. 2011;4:417-27.
17. Gauhe A, Gyorgy P, Hoover JR, Kuhn R, Rose CS, Ruelius HW, Zilliken F. Bifidus factor. IV. Preparations obtained from human milk. Arch Biochem Biophys. 1954;48:214-24.
18. Niñonuevo MR, Park Y, Yin H, Zhang J, Ward RE, Clowers BH, German JB, Freeman SL, Killeen K, Grimm R, et al. A strategy for annotating the human milk glycome. J Agric Food Chem. 2006;54:7471-80.
19. Urashima T, Saito T, Nakamura T, Messer M. Oligosaccharides of milk and colostrum in non-human mammals. Glycoconj J. 2001;18:357-71.
20. Warren CD, Chaturvedi P, Newburg AR, Oftedal OT, Tilden CD, Newburg DS. Comparison of oligosaccharides in milk specimens from humans and twelve other species. Adv Exp Med Biol. 2001;501:325-32.
21. Bode L. Recent advances on structure, metabolism, and function of human milk oligosaccharides. J Nutr. 2006;136:2127-30.
22. Sela DA, Mills DA. Nursing our microbiota:molecular linkages between biofidobacteria and milk oligosaccharides. Trends Microbiol. 2010;18:298-307.
23. Donovan SM. Promoting bifidobacteria in the human infant intestine: why, how, and which one? J Pediatr Gastroenterol Nutr. 2011;52:648-9.
24. Kuntz S, Rudloff S, Kunz C. Oligosaccharides from human milk influence growth-related characteristics of intestinally transformed and non-transformed intestinal cells. Br J Nutr. 2008;99:462-71.
25. Kuntz S, Rudloff S, Kunz C. Oligosaccharides from human milk induce growth arrest via G2/M by influencing growth-related cell cycle genes in intestinal epithelial cells. Br J Nutr. 2009;101:1306-15.
26. Shen Q, Tuohy KM, Gibson GR, Ward RE. In vitro measurement of the impact of human milk oligosaccharides on the faecal microbiota of weaned formula-fed infants compared to a mixture of prebiotic fructooligosaccharies and galactooligosaccharides. Lett Appl Microbiol. 2011;52:337-43.
27. Vael C, Desager K. The importance of the development of the intestinal microbiota in infancy. Curr Opin Pediatr. 2009;21:794-800.
28. Rahman MM, Kim WS, Ito T, Kumura H, Shimazaki K. Growth promotion and cell binding ability of bovine lactoferrin to Bifidobacterium longum. Anaerobe. 2009;15:133-7.
29. Roberts AK, Chierici R, Sawatzki G, Hill MJ, Volpato S, Vigi V. Supplementation of an adapted formula with bovine lactoferrin:1. Effect on the infant faecal flora. Acta Paediatr. 1992;81:119-24.
30. Liepke C, Adermann K, Raida M, Mägert HJ, Forssmann WG, Zucht HD. Human milk provides peptides highly stimulating the growth of bifidobacteria. Eur J Biochem. 2002;269:712-8.
31. LoCascio RG, Niñonuevo MR, Kronewitter SR, Freeman SL, German JB, Lebrilla CB, Mills DA. A versatile and scalable strategy for glycoprofiling bifidobacterial consumption of human milk oligosaccharides. Microb Biotechnol. 2009;2:333-42.
32. LoCascio RG, Desai P, Sela DA, Weimer B, Mills DA. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Appl Environ Microbiol. 2010;76:7373-81.
33. Ruhaak LR, Lebrilla CB. Advances in the analysis of free milk oligosaccharides. Adv Nutr. 2012;3:406S-14S.
34. Garrido D, Barile D, Mills DA. A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract. Adv Nutr. 2012;3:415S-21S.
35. Leser TD, Mølbak L. Better living through microbial action:the benefits of the mammalian gastrointestinal microbiota on the host. Environ Microbiol. 2009;11:2194-206.
36. Hrncir T, Stepankova R, Kozakova H, Hudcovic T, Tlaskalova-Hogenova H. Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T cells:studies in germ-free mice. BMC Immunol. 2008;9:65 .
37. Claus SP, Ellero SL, Berger B, Krause L, Bruttin A, Molina J, Paris A, Want EJ, de Waziers I, Cloarec O, et al. Colonization-induced hostgut microbial metabolic interaction. MBio. 2011;2:e00271-10.
38. Moore AM, Munck M, Sommer MOA, Dantas G. Functional metagenomic investigations of the human intestinal microbiota. Front Microbiol. 2011;2:188. doi:10.3389/fmicb.2011.00188.
39. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027-31.
40. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome:a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009;1(6):6ra14.
41. McNulty NP, The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med 2011;3:106ra106.
42. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334: 105-8.
43. Shulzhenko N, Morgun A, Hsiao W, Battle M, Yao M, Gavrilova O, Orandle M, Mayer L, Macpherson AJ, McCoy KD, et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat Med. 2011;17:1585-93.
44. Poroyko V, White JR, Wang M, Donovan SM, Alverdy JC, Liu DC, Morowitz MJ. Gut microbial gene expression in mother-fed and formula fed neonatal piglets. PLoS ONE. 2010;5:e12459.
45. Tao N, Ochonicky KL, German JB, Donovan SM, Lebrilla CB. Structural determination and daily variations of porcine milk oligosaccharides. J Agric Food Chem. 2010;58:4653-9.
46. Martín-Sosa S, Martín MJ, García-Pardo LA, Hueso P. Sialyloligosaccharides in human and bovine milk and in infant formulas:variations with the progression of lactation. J Dairy Sci. 2003;86:52-9.
47. Shah P, Shah V. Arginine supplementation for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev. 2007; 3:CD004339.
48. Morales Y, Schanler RJ. Human milk and clinical outcomes in VLBW infants:How compelling is the evidence of benefit? Semin Perinatol. 2007;31:83-8.
49. Poroyko V, MorowitzM, Bell T, Ulanov A, WangM, Donovan S, BaoN, Gu A, Hong L, Alverdy JC, et al. Diet creates metabolic niches in the "immature gut" that shape microbial communities. Nutr Hosp. 2011;26:1283-95.
50. Morowitz MJ, Poroyko V, Caplan M, Alverdy JC, Liu DC. Redefining the role of intestinal microbes in the pathogenesis of necrotizing enterocolitis. Pediatrics. 2010;125:777-85.
51. Falk PG, Hooper LV, Midtvedt T, Gordon JI. Creating and maintaining the gastrointestinal ecosystem:what we know and need to know from gnotobiology. Microbiol Mol Biol Rev. 1998;62:1157-70.
52. Chowdhury SR, King DE, Willing BP, Band MR, Beever JE, Lane AB, Loor JJ, Marini JC, Rund LA, Schook LB, et al. Transcriptome profiling of the small intestinal epithelium in germfree versus conventional piglets. BMC Genomics. 2007;8:215.
53. Willing BP, Van Kessel AG. Enterocyte proliferation and apoptosis in the caudal small intestine is influenced by the composition of colonizing commensal bacteria in the neonatal gnotobiotic pig. J Anim Sci. 2007;85:3256-66.
54. Willing BP, Van Kessel AG. Intestinal microbiota differentially affect brush border enzyme activity and gene expression in the neonatal gnotobiotic pig. J Anim Physiol Anim Nutr (Berl). 2009;93:586-95.
55. Meurens F, Berri M, Siggers RH, Willing BP, Salmon H, Van Kessel AG, Gerdts V. Commensal bacteria and expression of two major intestinal chemokines, TECK/CCL25 and MEC/CCL28, and their receptors. PLoS ONE. 2007;2:e677.
56. Chapkin RS, Zhao C, Ivanov I, Davidson LA, Goldsby JS, Lupton JR, Mathai RA, Monaco MH, Rai D, Russell WM, et al. Stool-based detection of infant gastrointestinal development using gene expression profiles from exfoliated epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2010;298:G582-9.
57. Favier J, Kempf H, Corvol P, Gasc JM. Coexpression of endothelial PAS protein 1 with essential angiogenic factors suggests its involvement in human vascular development. Dev Dyn. 2001;222:377-88.
58. Zamora R, Vodovotz Y, Betten B, Wong C, Zuckerbraun B, Gibson KF, Ford HR. Intestinal and hepatic expression of BNIP3 in necrotizing enterocolitis: regulation by nitric oxide peroxynitrite. Am J Physiol Gastrointest Liver Physiol. 2005;289:G822-30.
59. Wu S, Tao N, German JB, Grimm R, Lebrilla CB. Development of an annotated library of neutral human milk oligosaccharides. J Proteome Res. 2010;9:4138-51.
60. Wu S, Wu S, Grimm R, German JB, Lebrilla CB. Annotation and structural analysis of sialylated human milk oligosaccharides. J Proteome Res. 2011;10:856-68.
61. Erney RM, Malone WT, Skelding MB, Marcon AA, Kleman-Leyer KM, O'Ryan ML, Ruiz-Palacios G, Hilty MD, Pickering LK, Prieto PA. Variability of human milk neutral oligosaccharides in a diverse population. J Pediatr Gastroenterol Nutr. 2000;30:181-92.
62. Renz H, Brandtzaeg P, Hornef M. The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol. 2012;12:9-23.
63. Mothur project. [Cited 2012 Jan 31. Available from:http://www.mothur.org/.