Breast milk and its impact on maturation of the neonatal immune system

Current Opinion in Infectious Diseases

Volumn 28, Issue 3, 2015, Pages 199-206

  Turfkruyer, Mathilde ^a   Verhasselt, Valerie ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

breast milk; gut mucosa; neonate; oral tolerance

Indexed keywords

CD103 ANTIGEN;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; BREAST MILK; DENDRITIC CELL; DIET; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOMODULATION; IMMUNOREGULATION; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; MUCOSAL IMMUNITY; NEONATOLOGY; REVIEW; BREAST FEEDING; FEMALE; GASTROINTESTINAL TRACT; IMMUNOLOGY; INFANT NUTRITION; INTESTINE MUCOSA; MALE; NEWBORN; PASSIVE IMMUNIZATION;

BREAST FEEDING; FEMALE; GASTROINTESTINAL TRACT; HOMEOSTASIS; HUMANS; IMMUNITY, MATERNALLY-ACQUIRED; INFANT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; INFANT, NEWBORN; INTESTINAL MUCOSA; MALE; MILK, HUMAN;

EID: 84929461448     PISSN: 09517375     EISSN: 14736527     Source Type: Journal    
DOI: 10.1097/QCO.0000000000000165     Document Type: Review

References (80)

1. Oza S, Lawn JE, Hogan DR, et al. Neonatal cause-of-death estimates for the early and late neonatal periods for 194 countries: 2000-2013. Bull World Health Organ 2015; 93:19-28.
2. Rona RJ, Keil T, Summers C, et al. The prevalence of food allergy: a metaanalysis. J Allergy Clin Immunol 2007; 120:638-646.
3. Lawrence RM. Pane CA: human breast milk: current concepts of immunology and infectious diseases. Curr Probl Pediatr Adolesc Healthcare 2007; 37: 7-36.
4. Labbok MH, Clark D, Goldman AS. Breastfeeding: maintaining an irreplaceable immunological resource. Nat Rev Immunol 2004; 4:565-572.
5. Brandtzaeg P. Mucosal immunity: integration between mother and the breastfed infant. Vaccine 2003; 21:3382-3388.
6. Hanson LA, Korotkova M, Lundin S, et al. The transfer of immunity from mother to child. Ann NY Acad Sci 2003; 987:199-206.
7. Muraro A, Halken S, Arshad SH, et al. EAACI food allergy and anaphylaxis guidelines. Primary prevention of food allergy. Allergy 2014; 69:590-601.
8. Verhasselt V. Neonatal tolerance under breastfeeding influence. Curr Opin Immunol 2010; 22:623-630.
9. Verhasselt V. Oral tolerance in neonates: from basics to potential prevention of allergic disease. Mucosal Immunol 2010; 3:326-333.
10. Barclay AR, Russell RK, Wilson ML, et al. Systematic review: the role of breastfeeding in the development of pediatric inflammatory bowel disease. J Pediatr 2009; 155:421-426.
11. Pereira PF, Alfenas Rita de CG, Araujo RM. Does breastfeeding influence the risk of developing diabetes mellitus in children? A review of current evidence. J Pediatr (Rio J) 2014; 90:7-15.
12. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012; 489:231-241.
13. Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014; 14:141-153.
14. Henning SJ. Postnatal development: coordination of feeding, digestion, and metabolism. Am J Physiol 1981; 241:G199-G214.
15. de Santa Barbara P, van den Brink GR, Roberts DJ. Development and differentiation of the intestinal epithelium. Cell Mol Life Sci 2003; 60: 1322-1332.
16. Harper J, Mould A, Andrews RM, et al. The transcriptional repressor Blimp1/Prdm1 regulates postnatal reprogramming of intestinal enterocytes. Proc Natl Acad Sci USA 2011; 108:10585-10590.
17. Muncan V, Heijmans J, Krasinski SD, et al. Blimp1 regulates the transition of neonatal to adult intestinal epithelium. Nat Commun 2011; 2:452.
18. Tapper D, Klagsbrun M, Neumann J. The identification and clinical implications of human breast milk mitogen. J Pediatr Surg 1979; 14:803-808.
19. Berseth CL. Enhancement of intestinal growth in neonatal rats by epidermal growth factor in milk. Am J Physiol 1987; 253:G662-G665.
20. Dvorak B. Milk epidermal growth factor and gut protection. J Pediatr 2010; 156:S31-S35.
21. Blum JW, Baumrucker CR. Insulin-like growth factors (IGFs), IGF binding proteins, and other endocrine factors in milk: role in the newborn. Adv Exp Med Biol 2008; 606:397-422.
22. Garcia C, Duan RD, Brevaut-Malaty V, et al. Bioactive compounds in human milk and intestinal health and maturity in preterm newborn: an overview. Cell Mol Biol (Noisy-le-grand) 2013; 59:108-131.
23. McCullough FS, Northrop-Clewes CA, Thurnham DI. The effect of vitamin A on epithelial integrity. Proc Nutr Soc 1999; 58:289-293.
24. Haskell MJ, Brown KH. Maternal vitamin A nutriture and the vitamin A content of human milk. J Mammary Gland Biol Neoplasia 1999; 4:243-257.
25. Chappell JE, Francis T, Clandinin MT. Vitamin A and E content of human milk at early stages of lactation. Early Hum Dev 1985; 11:157-167.
26. Menard S, Cerf-Bensussan N, Heyman M. Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunol 2010; 3:247-259.
27. Groschwitz KR, Hogan SP. Intestinal barrier function: molecular regulation and disease pathogenesis. J Allergy Clin Immunol 2009; 124:3-20.
28. Persson EK, Scott CL, Mowat AM, Agace WW. Dendritic cell subsets in the intestinal lamina propria: ontogeny and function. Eur J Immunol 2013; 43:3098-3107.
29. McDole JR, Wheeler LW, McDonald KG, et al. Goblet cells deliver luminal antigen to CD103\+dendritic cells in the small intestine. Nature 2012; 483:345-349.
30. Catassi C, Bonucci A, Coppa GV, et al. Intestinal permeability changes during the first month: effect of natural versus artificial feeding. J Pediatr Gastroenterol Nutr 1995; 21:383-386.
31. Udall JN, Colony P, Fritze L, et al. Development of gastrointestinal mucosal barrier. II. The effect of natural versus artificial feeding on intestinal permeability to macromolecules. Pediatr Res 1981; 15:245-249.
32. Heyman M, Crain-Denoyelle AM, Corthier G, et al. Postnatal development of protein absorption in conventional and germ-free mice. Am J Physiol 1986; 251:G326-G331.
33. Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 2007; 7:715-725.
34. Qiao SW, Kobayashi K, Johansen FE, et al. Dependence of antibodymediated presentation of antigen on FcRn. Proc Natl Acad Sci USA 2008; 105:9337-9342.
35. Mosconi E, Rekima A, Seitz-Polski B, et al. Breast milk immune complexes are potent inducers of oral tolerance in neonates and prevent asthma development. Mucosal Immunol 2010; 3:461-474.
36. Verhasselt V, Milcent V, Cazareth J, et al. Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat Med 2008; 14:170-175.
37. Yoshida M, Claypool SM, Wagner JS, et al. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 2004; 20:769-783.
38. Yoshida M, Kobayashi K, Kuo TT, et al. Neonatal Fc receptor for IgG regulates mucosal immune responses to luminal bacteria. J Clin Invest 2006; 116: 2142-2151.
39. Harris NL, Spoerri I, Schopfer JF, et al. Mechanisms of neonatal mucosal antibody protection. J Immunol 2006; 177:6256-6262.
40. Israel EJ, Taylor S, Wu Z, et al. Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells. Immunology 1997; 92:69-74.
41. Lindsey B, Kampmann B, Jones C. Maternal immunization as a strategy to decrease susceptibility to infection in newborn infants. Curr Opin Infect Dis 2013; 26:248-253.
42. Pott J, Hornef M. Innate immune signalling at the intestinal epithelium in homeostasis and disease. EMBO Rep 2012; 13:684-698.
43. Menard S, Forster V, Lotz M, et al. Developmental switch of intestinal antimicrobial peptide expression. J Exp Med 2008; 205:183-193.
44. Gaboriau-Routhiau V, Lecuyer E, Cerf-Bensussan N. Role of microbiota in postnatal maturation of intestinal T-cell responses. Curr Opin Gastroenterol 2011; 27:502-508.
45. Jiang HQ, Bos NA, Cebra JJ. Timing, localization, and persistence of colonization by segmented filamentous bacteria in the neonatal mouse gut depend on immune status of mothers and pups. Infect Immun 2001; 69:3611-3617.
46. Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 2012; 22:1147-1162.
47. Maslowski KM, Mackay CR. Diet, gut microbiota and immune responses. Nat Immunol 2011; 12:5-9.
48. Walker A. Breast milk as the gold standard for protective nutrients. J Pediatr 2010; 156:S3-S7.
49. Lotz M, Gutle D, Walther S, et al. Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J Exp Med 2006; 203:973-984.
50. Penttila IA, van Spriel AB, Zhang MF, et al. Transforming growth factor-beta levels in maternal milk and expression in postnatal rat duodenum and ileum. Pediatr Res 1998; 44:524-531.
51. Lantier L, Lacroix-Lamande S, Potiron L, et al. Intestinal CD103\+dendritic cells are key players in the innate immune control of Cryptosporidium parvum infection in neonatal mice. PLoS Pathog 2013; 9:e1003801.
52. Chapkin RS, Zhao C, Ivanov I, et al. Noninvasive stool-based detection of infant gastrointestinal development using gene expression profiles from exfoliated epithelial cells. Am J Physiol Gastrointest Liver Physiol 2010; 298:G582-G589.
53. LeBouder E, Rey-Nores JE, Raby AC, et al. Modulation of neonatal microbial recognition: TLR-mediated innate immune responses are specifically and differentially modulated by human milk. J Immunol 2006; 176:3742-3752.
54. Chatterton DE, Nguyen DN, Bering SB, Sangild PT. Anti-inflammatory mechanisms of bioactive milk proteins in the intestine of newborns. Int J Biochem Cell Biol 2013; 45:1730-1747.
55. Penttila IA, Flesch IE, McCue AL, et al. Maternal milk regulation of cell infiltration and interleukin 18 in the intestine of suckling rat pups. Gut 2003; 52:1579-1586.
56. Penttila IA. Milk-derived transforming growth factor-beta and the infant immune response. J Pediatr 2010; 156:S21-S25.
57. He Y, Liu S, Leone S, Newburg DS. Human colostrum oligosaccharides modulate major immunologic pathways of immature human intestine. Mucosal Immunol 2014; 7:1326-1339.
58. Cassani B, Villablanca EJ, De Calisto J, et al. Vitamin A and immune regulation: role of retinoic acid in gut-associated dendritic cell education, immune protection and tolerance. Mol Aspects Med 2012; 33:63-76.
59. Hall JA, Grainger JR, Spencer SP, Belkaid Y. The role of retinoic acid in tolerance and immunity. Immunity 2011; 35:13-22.
60. Agace WW, Persson EK. How vitamin A metabolizing dendritic cells are generated in the gut mucosa. Trends Immunol 2012; 33:42-48.
61. Cassani B, Villablanca EJ, De Calisto J, et al. Vitamin A and immune regulation: role of retinoic acid in gut-associated dendritic cell education, immune protection and tolerance. Mol Aspects Med 2012; 33:63-76.
62. Ruckwardt TJ, Malloy AM, Morabito KM, Graham BS. Quantitative and qualitative deficits in neonatal lung-migratory dendritic cells impact the generation of the CD8\+T cell response. PLoS Pathog 2014; 10:e1003934.
63. Garcia AL, Ruhl R, Schweigert FJ. Retinoid concentrations in the mouse during postnatal development and after maternal vitamin A supplementation. Ann Nutr Metab 2005; 49:333-341.
64. Olson JA, Gunning DB, Tilton RA. Liver concentrations of vitamin A and carotenoids, as a function of age and other parameters, of American children who died of various causes. Am J Clin Nutr 1984; 39:903-910.
65. Malvy DJ, Burtschy B, Dostalova L, Amedee-Manesme O. Serum retinol, betacarotene, alpha-tocopherol and cholesterol in healthy French children. Int J Epidemiol 1993; 22:237-246.
66. Delvin EE, Salle BL, Reygrobellet B, et al. Vitamin A and E supplementation in breast-fed newborns. J Pediatr Gastroenterol Nutr 2000; 31:562-565.
67. Shenai JP, Chytil F, Jhaveri A, Stahlman MT. Plasma vitamin A and retinolbinding protein in premature and term neonates. J Pediatr 1981; 99:302-305.
68. Mitchell GV, Young M, Seward CR. Vitamin A and carotene levels of a selected population in metropolitan Washington, D.C. Am J Clin Nutr 1973; 26:992-997.
69. Pesonen M, Kallio MJ, Siimes MA, Ranki A. Retinol concentrations after birth are inversely associated with atopic manifestations in children and young adults. Clin Exp Allergy 2007; 37:54-61.
70. Rothman KJ, Moore LL, Singer MR, et al. Teratogenicity of high vitamin A intake. N Engl J Med 1995; 333:1369-1373.
71. Tilg H, Moschen AR. Food, immunity, and the microbiome. Gastroenterology 2015. [Epub ahead of print]
72. Korotkova M, Telemo E, Yamashiro Y, et al. The ratio of n-6 to n-3 fatty acids in maternal diet influences the induction of neonatal immunological tolerance to ovalbumin. Clin Exp Immunol 2004; 137:237-244.
73. Duchen K, Yu G, Bjorksten B. Atopic sensitization during the first year of life in relation to long chain polyunsaturated fatty acid levels in human milk. Pediatr Res 1998; 44:478-484.
74. Dunstan JA, Mori TA, Barden A, et al. Fish oil supplementation in pregnancy modifies neonatal allergen-specific immune responses and clinical outcomes in infants at high risk of atopy: a randomized, controlled trial. J Allergy Clin Immunol 2003; 112:1178-1184.
75. D'Vaz N, Meldrum SJ, Dunstan JA, et al. Postnatal fish oil supplementation in high-risk infants to prevent allergy: randomized controlled trial. Pediatrics 2012; 130:674-682.
76. Pierre M, Husson MO, Le Berre R, et al. Omega-3 polyunsaturated fatty acids improve host response in chronic Pseudomonas aeruginosa lung infection in mice. Am J Physiol Lung Cell Mol Physiol 2007; 292:L1422-1431.
77. Anderson M, Fritsche KL. (n-3) Fatty acids and infectious disease resistance. J Nutr 2002; 132:3566-3576.
78. Macchiaverni P, Tulic MK, Verhasselt V. Antigens in breast milk: possible impact on immune system education. In: Zibadi S, Watson RR, Preedy VR, editors. Dietary and nutritional aspects of human milk. Wageningen, The Netherlands: Wageningen Academic Publishers; 2013. vol 5. pp. 447-460.
79. Macchiaverni P, Rekima A, Turfkruyer M, et al. Respiratory allergen from house dust mite is present in human milk and primes for allergic sensitization in a mouse model of asthma. Allergy 2014; 69:395-398.
80. Gregory LG, Lloyd CM. Orchestrating house dust mite-associated allergy in the lung. Trends Immunol 2011; 32:402-411.