Neonatal tolerance under breastfeeding influence

Current Opinion in Immunology

Volumn 22, Issue 5, 2010, Pages 623-630

  Verhasselt, Valérie ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; EPIDERMAL GROWTH FACTOR; GAMMA INTERFERON; IMMUNOGLOBULIN A; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; LACTOFERRIN; LYSOZYME; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; OSTEOPONTIN; TOLL LIKE RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN ANTIBODY REACTION; ANTIGEN EXPRESSION; ANTIMICROBIAL ACTIVITY; ARTIFICIAL MILK; BIFIDOBACTERIUM; BREAST FEEDING; CELIAC DISEASE; FOOD ALLERGY; FOOD COMPOSITION; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOPATHOLOGY; IMMUNOSTIMULATION; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; LACTOBACILLUS; PROTEIN LOCALIZATION; REVIEW;

ANIMALS; BREAST FEEDING; FEMALE; HUMANS; IMMUNE TOLERANCE; INFANT, NEWBORN; MILK, HUMAN;

EID: 78049289417     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2010.08.008     Document Type: Review

References (82)

1. Labbok M.H., Clark D., Goldman A.S. Breastfeeding: maintaining an irreplaceable immunological resource. Nat Rev Immunol 2004, 4:565-572.
2. Brandtzaeg P. Mucosal immunity: integration between mother and the breast-fed infant. Vaccine 2003, 21:3382-3388.
3. Malcova H., Sumnik Z., Drevinek P., Venhacova J., Lebl J., Cinek O. Absence of breast-feeding is associated with the risk of type 1 diabetes: a case-control study in a population with rapidly increasing incidence. Eur J Pediatr 2006, 165:114-119.
4. Holmberg H., Wahlberg J., Vaarala O., Ludvigsson J. Short duration of breast-feeding as a risk-factor for beta-cell autoantibodies in 5-year-old children from the general population. Br J Nutr 2007, 97:111-116.
5. Akobeng A.K., Ramanan A.V., Buchan I., Heller R.F. Effect of breast feeding on risk of coeliac disease: a systematic review and meta-analysis of observational studies. Arch Dis Child 2006, 91:39-43.
6. Greer F.R., Sicherer S.H., Burks A.W. Effects of early nutritional interventions on the development of atopic disease in infants and children: the role of maternal dietary restriction, breastfeeding, timing of introduction of complementary foods, and hydrolyzed formulas. Pediatrics 2008, 121:183-191.
7. Campbell D.A., Lorber M.I., Sweeton J.C., Turcotte J.G., Niederhuber J.E., Beer A.E. Breast feeding and maternal-donor renal allografts. Possibly the original donor-specific transfusion. Transplantation 1984, 37:340-344.
8. Burlingham W.J., Grailer A.P., Heisey D.M., Claas F.H., Norman D., Mohanakumar T., Brennan D.C., de Fijter H., van Gelder T., Pirsch J.D., et al. The effect of tolerance to noninherited maternal HLA antigens on the survival of renal transplants from sibling donors. N Engl J Med 1998, 339:1657-1664.
9. Tiittanen M., Paronen J., Savilahti E., Virtanen S.M., Ilonen J., Knip M., Akerblom H.K., Vaarala O. Dietary insulin as an immunogen and tolerogen. Pediatr Allergy Immunol 2006, 17:538-543.
10. Chirdo F.G., Rumbo M., Anon M.C., Fossati C.A. Presence of high levels of non-degraded gliadin in breast milk from healthy mothers. Scand J Gastroenterol 1998, 33:1186-1192.
11. Palmer D.J., Makrides M. Diet of lactating women and allergic reactions in their infants. Curr Opin Clin Nutr Metab Care 2006, 9:284-288.
12. van Rood J.J., Claas F. Both self and non-inherited maternal HLA antigens influence the immune response. Immunol Today 2000, 21:269-273.
13. Verhasselt V., Milcent V., Cazareth J., Kanda A., Fleury S., Dombrowicz D., Glaichenhaus N., Julia V. Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat Med 2008, 14:170-175.
14. Mosconi E., Rekima A., Seitz-Polski B., Kanda A., Fleury S., Tissandie E., Monteiro R., Dombrowicz D.D., Julia V., Glaichenhaus N., et al. Breast milk immune complexes are potent inducers of oral tolerance in neonates and prevent asthma development. Mucosal Immunol 2010, 3:461-474.
15. Willoughby J.B., Willoughby W.F. In vivo responses to inhaled proteins. I. Quantitative analysis of antigen uptake, fate, and immunogenicity in a rabbit model system. J Immunol 1977, 119:2137-2146.
16. Michael J.G. The role of digestive enzymes in orally induced immune tolerance. Immunol Invest 1989, 18:1049-1054.
17. Untersmayr E., Scholl I., Swoboda I., Beil W.J., Forster-Waldl E., Walter F., Riemer A., Kraml G., Kinaciyan T., Spitzauer S., et al. Antacid medication inhibits digestion of dietary proteins and causes food allergy: a fish allergy model in BALB/c mice. J Allergy Clin Immunol 2003, 112:616-623.
18. Agunod M., Yamaguchi N., Lopez R., Luhby A.L., Glass G.B. Correlative study of hydrochloric acid, pepsin, and intrinsic factor secretion in newborns and infants. Am J Dig Dis 1969, 14:400-414.
19. Palmer D.J., Gold M.S., Makrides M. Effect of cooked and raw egg consumption on ovalbumin content of human milk: a randomized, double-blind, cross-over trial. Clin Exp Allergy 2005, 35:173-178.
20. Benn C.S., Bottcher M.F., Pedersen B.V., Filteau S.M., Duchen K. Mammary epithelial paracellular permeability in atopic and non-atopic mothers versus childhood atopy. Pediatr Allergy Immunol 2004, 15:123-126.
21. Hanson D.G. Ontogeny of orally induced tolerance to soluble proteins in mice. I. Priming and tolerance in newborns. J Immunol 1981, 127:1518-1524.
22. Strobel S. Neonatal oral tolerance. Ann N Y Acad Sci 1996, 778:88-102.
23. Telemo E., Jakobsson I., Westrom B.R., Folkesson H. Maternal dietary antigens and the immune response in the offspring of the guinea-pig. Immunology 1987, 62:35-38.
24. Komatsu T., Okao M., Miyamoto H., Chen T., Shinka S. Effects of early antigen exposure through lactation on later specific antibody responses in mice. J Immunol 1988, 141:2895-2906.
25. Korotkova M., Telemo E., Yamashiro Y., Hanson L.A., Strandvik B. 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.
26. Andrassy J., Kusaka S., Jankowska-Gan E., Torrealba J.R., Haynes L.D., Marthaler B.R., Tam R.C., Illigens B.M., Anosova N., Benichou G., et al. Tolerance to noninherited maternal MHC antigens in mice. J Immunol 2003, 171:5554-5561.
27. Aoyama K., Koyama M., Matsuoka K., Hashimoto D., Ichinohe T., Harada M., Akashi K., Tanimoto M., Teshima T. Improved outcome of allogeneic bone marrow transplantation due to breastfeeding-induced tolerance to maternal antigens. Blood 2009, 113:1829-1833.
28. Penttila I.A., van Spriel A.B., Zhang M.F., Xian C.J., Steeb C.B., Cummins A.G., Zola H., Read L.C. Transforming growth factor-beta levels in maternal milk and expression in postnatal rat duodenum and ileum. Pediatr Res 1998, 44:524-531.
29. Penttila I.A., Flesch I.E., McCue A.L., Powell B.C., Zhou F.H., Read L.C., Zola H. Maternal milk regulation of cell infiltration and interleukin 18 in the intestine of suckling rat pups. Gut 2003, 52:1579-1586.
30. Penttila I. Effects of transforming growth factor-beta and formula feeding on systemic immune responses to dietary beta-lactoglobulin in allergy-prone rats. Pediatr Res 2006, 59:650-655.
31. Oddy W.H., Halonen M., Martinez F.D., Lohman I.C., Stern D.A., Kurzius-Spencer M., Guerra S., Wright A.L. TGF-beta in human milk is associated with wheeze in infancy. J Allergy Clin Immunol 2003, 112:723-728.
32. Kalliomaki M., Ouwehand A., Arvilommi H., Kero P., Isolauri E. Transforming growth factor-beta in breast milk: a potential regulator of atopic disease at an early age. J Allergy Clin Immunol 1999, 104:1251-1257.
33. Prescott S.L., Wickens K., Westcott L., Jung W., Currie H., Black P.N., Stanley T.V., Mitchell E.A., Fitzharris P., Siebers R., et al. Supplementation with Lactobacillus rhamnosus or Bifidobacterium lactis probiotics in pregnancy increases cord blood interferon-gamma and breast milk transforming growth factor-beta and immunoglobin A detection. Clin Exp Allergy 2008, 38:1606-1614.
34. Bottcher M.F., Abrahamsson T.R., Fredriksson M., Jakobsson T., Bjorksten B. Low breast milk TGF-beta2 is induced by Lactobacillus reuteri supplementation and associates with reduced risk of sensitization during infancy. Pediatr Allergy Immunol 2008, 19:497-504.
35. Garofalo R. Cytokines in human milk. J Pediatr 2010, 156:S36-S40.
36. Ngom P.T., Collinson A.C., Pido-Lopez J., Henson S.M., Prentice A.M., Aspinall R. Improved thymic function in exclusively breastfed infants is associated with higher interleukin 7 concentrations in their mothers' breast milk. Am J Clin Nutr 2004, 80:722-728.
37. Schack L., Lange A., Kelsen J., Agnholt J., Christensen B., Petersen T.E., Sorensen E.S. Considerable variation in the concentration of osteopontin in human milk, bovine milk, and infant formulas. J Dairy Sci 2009, 92:5378-5385.
38. Cantor H., Shinohara M.L. Regulation of T-helper-cell lineage development by osteopontin: the inside story. Nat Rev Immunol 2009, 9:137-141.
39. Strober W. Vitamin A rewrites the ABCs of oral tolerance. Mucosal Immunol 2008, 1:92-95.
40. Ishikawa H., Tanaka K., Maeda Y., Aiba Y., Hata A., Tsuji N.M., Koga Y., Matsumoto T. Effect of intestinal microbiota on the induction of regulatory CD25+ CD4+ T cells. Clin Exp Immunol 2008, 153:127-135.
41. Moreau M.C., Gaboriau-Routhiau V. The absence of gut flora, the doses of antigen ingested and aging affect the long-term peripheral tolerance induced by ovalbumin feeding in mice. Res Immunol 1996, 147:49-59.
42. Sudo N., Sawamura S., Tanaka K., Aiba Y., Kubo C., Koga Y. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol 1997, 159:1739-1745.
43. Ostman S., Rask C., Wold A.E., Hultkrantz S., Telemo E. Impaired regulatory T cell function in germ-free mice. Eur J Immunol 2006, 36:2336-2346.
44. Wen L., Ley R.E., Volchkov P.Y., Stranges P.B., Avanesyan L., Stonebraker A.C., Hu C., Wong F.S., Szot G.L., Bluestone J.A., et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008, 455:1109-1113.
45. Lonnqvist A., Ostman S., Almqvist N., Hultkrantz S., Telemo E., Wold A.E., Rask C. Neonatal exposure to staphylococcal superantigen improves induction of oral tolerance in a mouse model of airway allergy. Eur J Immunol 2009, 39:447-456.
46. Bjorksten B. Effects of intestinal microflora and the environment on the development of asthma and allergy. Springer Semin Immunopathol 2004, 25:257-270.
47. Adlerberth I., Wold A.E. Establishment of the gut microbiota in Western infants. Acta Paediatr 2009, 98:229-238.
48. Morelli L. Postnatal development of intestinal microflora as influenced by infant nutrition. J Nutr 2008, 138:1791S-1795S.
49. Gaboriau-Routhiau V., Rakotobe S., Lecuyer E., Mulder I., Lan A., Bridonneau C., Rochet V., Pisi A., De Paepe M., Brandi G., et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009, 31:677-689.
50. Labeta M.O., Vidal K., Nores J.E., Arias M., Vita N., Morgan B.P., Guillemot J.C., Loyaux D., Ferrara P., Schmid D., et al. Innate recognition of bacteria in human milk is mediated by a milk-derived highly expressed pattern recognition receptor, soluble CD14. J Exp Med 2000, 191:1807-1812.
51. LeBouder E., Rey-Nores J.E., Rushmere N.K., Grigorov M., Lawn S.D., Affolter M., Griffin G.E., Ferrara P., Schiffrin E.J., Morgan B.P., et al. Soluble forms of Toll-like receptor (TLR)2 capable of modulating TLR2 signaling are present in human plasma and breast milk. J Immunol 2003, 171:6680-6689.
52. Martin R., Heilig H.G., Zoetendal E.G., Jimenez E., Fernandez L., Smidt H., Rodriguez J.M. Cultivation-independent assessment of the bacterial diversity of breast milk among healthy women. Res Microbiol 2007, 158:31-37.
53. Perez P.F., Dore J., Leclerc M., Levenez F., Benyacoub J., Serrant P., Segura-Roggero I., Schiffrin E.J., Donnet-Hughes A. Bacterial imprinting of the neonatal immune system: lessons from maternal cells?. Pediatrics 2007, 119:e724-732.
54. Brandtzaeg P.E. Current understanding of gastrointestinal immunoregulation and its relation to food allergy. Ann N Y Acad Sci 2002, 964:13-45.
55. Menezes J.S., Mucida D.S., Cara D.C., Alvarez-Leite J.I., Russo M., Vaz N.M., de Faria A.M. Stimulation by food proteins plays a critical role in the maturation of the immune system. Int Immunol 2003, 15:447-455.
56. Mucida D.S., Rodriguez D., Keller A.C., Gomes E., Menezes J.S., de Faria A.M., Russo M. Decreased nasal tolerance to allergic asthma in mice fed an amino acid-based protein-free diet. Ann N Y Acad Sci 2004, 1029:361-365.
57. Vaarala O. Leaking gut in type 1 diabetes. Curr Opin Gastroenterol 2008, 24:701-706.
58. Heyman M. Gut barrier dysfunction in food allergy. Eur J Gastroenterol Hepatol 2005, 17:1279-1285.
59. Menard S., Cerf-Bensussan N., Heyman M. Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunol 2010, 3:247-259.
60. Cummins A.G., Thompson F.M. Effect of breast milk and weaning on epithelial growth of the small intestine in humans. Gut 2002, 51:748-754.
61. Dvorak B. Milk epidermal growth factor and gut protection. J Pediatr 2010, 156:S31-S35.
62. Beck P.L., Rosenberg I.M., Xavier R.J., Koh T., Wong J.F., Podolsky D.K. Transforming growth factor-beta mediates intestinal healing and susceptibility to injury in vitro and in vivo through epithelial cells. Am J Pathol 2003, 162:597-608.
63. Cario E. Barrier-protective function of intestinal epithelial Toll-like receptor 2. Mucosal Immunol 2008, 1(Suppl. 1):S62-S66.
64. Levinsky R.J. Factors influencing intestinal uptake of food antigens. Proc Nutr Soc 1985, 44:81-86.
65. Andre C., Heremans J.F., Vaerman J.P., Cambiaso C.L. A mechanism for the induction of immunological tolerance by antigen feeding: antigen-antibody complexes. J Exp Med 1975, 142:1509-1519.
66. Corthesy B. Roundtrip ticket for secretory IgA: role in mucosal homeostasis?. J Immunol 2007, 178:27-32.
67. Hirose J., Ito S., Hirata N., Kido S., Kitabatake N., Narita H. Occurrence of the major food allergen, ovomucoid, in human breast milk as an immune complex. Biosci Biotechnol Biochem 2001, 65:1438-1440.
68. Juto P., Holm S. Gliadin-specific and cow's milk protein-specific IgA in human milk. J Pediatr Gastroenterol Nutr 1992, 15:159-162.
69. Savilahti E., Siltanen M., Kajosaari M., Vaarala O., Saarinen K.M. IgA antibodies, TGF-beta1 and -beta2, and soluble CD14 in the colostrum and development of atopy by age 4. Pediatr Res 2005, 58:1300-1305.
70. Jarvinen K.M., Laine S.T., Jarvenpaa A.L., Suomalainen H.K. Does low IgA in human milk predispose the infant to development of cow's milk allergy?. Pediatr Res 2000, 48:457-462.
71. Matysiak-Budnik T., Moura I.C., Arcos-Fajardo M., Lebreton C., Menard S., Candalh C., Ben-Khalifa K., Dugave C., Tamouza H., van Niel G., et al. Secretory IgA mediates retrotranscytosis of intact gliadin peptides via the transferrin receptor in celiac disease. J Exp Med 2008, 205:143-154.
72. Karlsson M.R., Johansen F.E., Kahu H., Macpherson A., Brandtzaeg P. Hypersensitivity and oral tolerance in the absence of a secretory immune system. Allergy 2010, 65:561-570.
73. Haddad Z.H., Vetter M., Friedmann J., Sainz C., Brunner E. Detection and kinetics of antigen-specific IgE and IgG immune complexes in food allergy. Ann Allergy 1983, 51:255.
74. Casas R., Bjorksten B. Detection of Fel d 1-immunoglobulin G immune complexes in cord blood and sera from allergic and non-allergic mothers. Pediatr Allergy Immunol 2001, 12:59-64.
75. Cianga P., Medesan C., Richardson J.A., Ghetie V., Ward E.S. Identification and function of neonatal Fc receptor in mammary gland of lactating mice. Eur J Immunol 1999, 29:2515-2523.
76. Kim Y.W., Halsey J.F. Metabolism and clearance of antibody-excess immune complexes in lactating mice. J Immunol 1982, 129:619-622.
77. Qiao S.W., Lencer W.I., Blumberg R.S. How the controller is controlled-neonatal Fc receptor expression and immunoglobulin G homeostasis. Immunology 2007, 120:145-147.
78. Yoshida M., Claypool S.M., Wagner J.S., Mizoguchi E., Mizoguchi A., Roopenian D.C., Lencer W.I., Blumberg R.S. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 2004, 20:769-783.
79. Yoshida M., Kobayashi K., Kuo T.T., Bry L., Glickman J.N., Claypool S.M., Kaser A., Nagaishi T., Higgins D.E., Mizoguchi E., et al. Neonatal Fc receptor for IgG regulates mucosal immune responses to luminal bacteria. J Clin Invest 2006, 116:2142-2151.
80. Caulfield M.J., Shaffer D. Immunoregulation by antigen/antibody complexes. I. Specific immunosuppression induced in vivo with immune complexes formed in antibody excess. J Immunol 1987, 138:3680-3683.
81. Machiels J.J., Somville M.A., Lebrun P.M., Lebecque S.J., Jacquemin M.G., Saint-Remy J.M. Allergic bronchial asthma due to Dermatophagoides pteronyssinus hypersensitivity can be efficiently treated by inoculation of allergen-antibody complexes. J Clin Invest 1990, 85:1024-1035.
82. Nimmerjahn F., Ravetch J.V. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 2008, 8:34-47.