Induction of Oral Tolerance in Neonatal Mice by Transfer of Food Allergens as IgA-Immune Complexes in Breast Milk
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Affiliation(s)
1Department of Life and Living, Osaka Seikei College, Osaka, Japan.
2Department of Food and Nutrition, Kyoto Women’s University, Kyoto, Japan.
3Department of Food Science and Nutrition, School of Human Cultures, The University of Shiga Prefecture, Hikone, Japan.
4Itayado Clinic, Kobe, Japan.
2Department of Food and Nutrition, Kyoto Women’s University, Kyoto, Japan.
3Department of Food Science and Nutrition, School of Human Cultures, The University of Shiga Prefecture, Hikone, Japan.
4Itayado Clinic, Kobe, Japan.
ABSTRACT
Various
opinions have been presented on the merits and demerits that
breastfeeding gives for the allergic onset of the babies. In this
report, we focused on whether food proteins eaten by mother mice and
secreted into breast milk as IgA-immune complexes contribute to the
allergy prevention through oral tolerance in infants who ingest the
milk. BALB/c mice were divided into two groups; E-group fed only egg
white proteins and M-group fed only cow’s milk proteins as a dietary
protein source. After immunizing M-group infants fed their own mother’s
milk with ovalbumin/alum, diarrhea associated with experimental Th2
intestinal inflammation was induced by oral administration of ovalbumin.
The diarrhea was dramatically suppressed in E-group infants.
Concomitantly, low level of serum anti-ovalbumin- and ovomucoid-IgG1 and
IgE, suppression of IL-4 synthesis by spleen cells, and low incidence
of anaphylactic death after intravenous injection of ovalbumin were
observed preferentially in E-infants. Immune complexes of respective
dietary proteins and IgA were found in the breast milk obtained from
each group of mother. Oral administration of pseudo immune complex
chemically synthesized with ovalbumin and monoclonal mouse IgA in
advance effectively suppressed anti-ovalbumin-IgG1 synthesis in adult
mice after immunization with ovalbumin. The tolerance induced by the
pseudo immune complex of ovalbumin diminished spontaneously while mice
did not take egg white proteins. Thus, immune tolerance and then
prevention of allergic disorder against dietary proteins were acquired
via breastfeeding by mothers feeding the relevant proteins, probably
through the immune complexes of dietary proteins and sIgAs secreted into
breast milk.
Cite this paper
References
Kizu,
K. , Matsunaga, A. , Hirose, J. , Kimura, A. and Narita, H. (2015)
Induction of Oral Tolerance in Neonatal Mice by Transfer of Food
Allergens as IgA-Immune Complexes in Breast Milk. Food and Nutrition Sciences, 6, 221-233. doi: 10.4236/fns.2015.62023.
| [1] | Gartner,
L.M., Morton, J., Lawrence, R.A., Naylor, A.J., O’Hare, D., Schanler,
R.J. and Eidelman, A.I. (2005) Breastfeeding and the Use of Human Milk.
Pediatrics, 115, 496-506. http://dx.doi.org/10.1542/peds.2004-2491 |
| [2] | Labbok,
M.H., Clark, D. and Goldman, A.S. (2004) Breastfeeding: Maintaining an
Irreplaceable Immunological Resource. Nature Reviews Immunology, 4,
565-572. http://dx.doi.org/10.1038/nri1393 |
| [3] | Ip,
S., Chung, M., Raman, G., Chew, P., Magula, N., DeVine, D., Trikalinos,
T. and Lau, J. (2007) Breastfeeding and Maternal and Infant Health
Outcomes in Developed Countries. Evidence Report—Technology Assessment,
153, 1-186. http://archive.ahrq.gov/downloads/pub/evidence/pdf/brfout/brfout.pdf |
| [4] | Brandtzaeg, P. (2003) Mucosal Immunity: Integration between Mother and the Breast-Fed Infant. Vaccine, 21, 33823388. 10.1016/S0264-410X(03)00338-4 |
| [5] | Geller-Bernstein, C., Weissglas, L., Dun, R., Tsur, S., Kahane, P. and Lahav, M. (1980) Immunoglobulin E and A Levels in Atopic and Anaphylactic Children. Annals of Allergy, 44, 29-33. |
| [6] | Aghamohammadi,
A., Cheraghi, T., Gharagozlou, M., Movahedi, M., Rezaei, N., Yeganeh,
M., Parvaneh, N., Abolhassani, H., Pourpak, Z. and Moin, M. (2009) IgA
Deficiency: Correlation between Clinical and Immunological Phenotypes.
Journal of Clinical Immunology, 29, 130-136. http://dx.doi.org/10.1007/s10875-008-9229-9 |
| [7] | Kramer,
M.S. and Kakuma, R. (2014) Maternal Dietary Antigen Avoidance during
Pregnancy or Lactation, or Both, for Preventing or Treating Atopic
Disease in the Child. Evidence-Based Child Health, 9, 447-483. http://dx.doi.org/10.1002/ebch.1972 |
| [8] | Ehlayel,
M.S. and Bener, A. (2008) Duration of Breast-Feeding and the Risk of
Childhood Allergic Diseases in a Developing Country. Allergy and Asthma
Proceedings, 29, 386-391. http://dx.doi.org/10.2500/aap.2008.29.3138 |
| [9] | Sicherer,
S.H., Wood, R.A., Stablein, D., Lindblad, R., Burks, A.W., Liu, A.H.,
Jones, S.M., Fleischer, D.M., Leung, D.Y. and Sampson, H.A. (2010)
Maternal Consumption of Peanut during Pregnancy Is Associated with
Peanut Sensitization in Atopic Infants. Journal of Allergy and Clinical
Immunology, 126, 1191-1197. http://dx.doi.org/10.1016/j.jaci.2010.08.036 |
| [10] | Duncan,
J.M. and Sears, M.R. (2008) Breastfeeding and Allergies: Time for a
Change in Paradigm? Current Opinion in Allergy and Clinical Immunology,
8, 398-405. http://dx.doi.org/10.1097/ACI.0b013e32830d82ed |
| [11] | Verhasselt,
V., Milcent, V., Cazareth, J., Kanda, A., Fleury, S., Dombrowicz, D.,
Glaichenhaus, N. and Julia, V. (2008) Breast Milk-Mediated Transfer of
an Antigen Induces Tolerance and Protection from Allergic Asthma. Nature
Medicine, 14, 170-175. http://dx.doi.org/10.1038/nm1718 |
| [12] | Leme,
A.S., Hubeau, C., Xiang, Y., Goldman, A., Hamada, K., Suzaki, Y. and
Kobzik, L. (2006) Role of Breast Milk in a Mouse Model of Maternal
Transmission of Asthma Susceptibility. Journal of Immunology, 176,
762-769. http://dx.doi.org/10.4049/jimmunol.176.2.762 |
| [13] | Strobel,
S. (2001) Immunity Induced after a Feed of Antigen during Early Life:
Oral Tolerance v. Sensitisation. Proceedings of the Nutrition Society,
60, 437-442. http://dx.doi.org/10.1079/PNS2001119 |
| [14] | Lack, G. (2008) Epidemiologic Risks for Food Allergy. Journal of Allergy and Clinical Immunology, 121, 1331-1336. http://dx.doi.org/10.1016/j.jaci.2008.04.032 |
| [15] | Vance,
G.H., Lewis, S.A., Grimshaw, K.E., Wood, P.J., Briggs, R.A., Thornton,
C.A. and Warner, J.O. (2005) Exposure of the Fetus and Infant to Hens’
Egg Ovalbumin via the Placenta and Breast Milk in Relation to Maternal
Intake of Dietary Egg. Clinical & Experimental Allergy, 35,
1318-1326. http://dx.doi.org/10.1111/j.1365-2222.2005.02346.x |
| [16] | Greer,
F.R., Sicherer, S.H. and Burks, A.W. (2008) 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, 121, 183-191. http://dx.doi.org/10.1542/peds.2007-3022 |
| [17] | Hirose,
J., Ito, S., Hirata, N., Kido, S., Kitabatake, N. and Narita, H. (2001)
Occurrence of the Major Food Allergen, Ovomucoid, in Human Breast Milk
as an Immune Complex. Bioscience, Biotechnology, and Biochemistry, 65,
14381440. http://dx.doi.org/10.1271/bbb.65.1438 |
| [18] | Mantis,
N.J., Cheung, M.C., Chintalacharuvu, K.R., Rey, J., Corthésy, B. and
Neutra, M.R. (2002) Selective Adherence of IgA to Murine Peyer’s Patch M
Cells: Evidence for a Novel IgA Receptor. Journal of Immunology, 169,
1844-1851. http://dx.doi.org/10.4049/jimmunol.169.4.1844 |
| [19] | Weltzin,
R., Lucia-Jandris, P., Michetti, P., Fields, B.N., Kraehenbuhl, J.P.
and Neutra, M.R. (1989) Binding and Transepithelial Transport of
Immunoglobulins by Intestinal M Cells: Demonstration Using Monoclonal
IgA Antibodies against Enteric Viral Proteins. Journal of Cell Biology,
108, 1673-1685. http://dx.doi.org/10.1083/jcb.108.5.1673 |
| [20] | Kizu,
K., Hirose, J., Honjo, T. and Narita, H. (2012) Induction of Oral
Immune Tolerance through Breast-Feeding in Rats. Japan Society of
Nutrition and Food Science, 64, 13-19. http://dx.doi.org/10.4327/jsnfs.65.13 |
| [21] | Hirose,
J., Kitabatake, N., Kimura, A. and Narita, H. (2004) Recognition of
Native and/or Thermally Induced Denatured Forms of the Major Food
Allergen, Ovomucoid, by Human IgE and Mouse Monoclonal IgG Antibodies.
Bioscience, Biotechnology, and Biochemistry, 68, 2490-2497. http://dx.doi.org/10.1271/bbb.68.2490 |
| [22] | Brandt,
E.B., Strait, R.T., Hershko, D., Wang, Q., Muntel, E.E., Scribner,
T.A., Zimmermann, N., Finkelman, F.D. and Rothenberg, M.E. (2003) Mast
Cells Are Required for Experimental Oral Allergen-Induced Diarrhea.
Journal of Clinical Investigation, 112, 1666-1677. http://dx.doi.org/10.1172/JCI19785 |
| [23] | Bland, J.M. and Altman, D.G. (2004) The Logrank Test. British Medical Journal, 328, 1073. http://dx.doi.org/10.1136/bmj.328.7447.1073 |
| [24] | Chehade,
M. and Mayer, L. (2005) Oral Tolerance and Its Relation to Food
Hypersensitivities. Journal of Allergy and Clinical Immunology, 115,
3-12. http://dx.doi.org/10.1016/j.jaci.2004.11.008 |
| [25] | Saito,
S., Yoshida, M., Ichijo, M., Ishizaka, S. and Tsujii, T. (1993)
Transforming Growth Factor-Beta (TGF-β) in Human Milk. Clinical &
Experimental Immunology, 94, 220-224. http://dx.doi.org/10.1111/j.1365-2249.1993.tb06004.x |
| [26] | Ando,
T., Hatsushika, K., Wako, M., Ohba, T., Koyama, K., Ohnuma, Y., Katoh,
R., Ogawa, H., Okumura, K., Luo, J., Wyss-Coray, T. and Nakao, A. (2007)
Orally Administered TGF-β Is Biologically Active in the Intestinal
Mucosa and Enhances Oral Tolerance. Journal of Allergy and Clinical
Immunology, 120, 916-923. http://dx.doi.org/10.1016/j.jaci.2007.05.023 |
| [27] | Corthésy, B. (2007) Roundtrip Ticket for Secretory IgA: Role in Mucosal Homeostasis? Journal of Immunology, 178, 27-32. http://dx.doi.org/10.4049/jimmunol.178.1.27 |
| [28] | Duc,
M., Johansen, F.E. and Corthésy, B. (2010) Antigen Binding to Secretory
Immunoglobulin A Results in Decreased Sensitivity to Intestinal
Proteases and Increased Binding to Cellular Fc Receptors. Journal of
Biological Chemistry, 285, 953-960. http://dx.doi.org/10.1074/jbc.M109.059220 |
| [29] | Grimshaw,
K.E., Maskell, J., Oliver, E.M., Morris, R.C., Foote, K.D., Mills,
E.N., Roberts, G. and Margetts, B.M. (2013) Introduction of
Complementary Foods and the Relationship to Food Allergy. Pediatrics,
132, e1529-e1538. http://dx.doi.org/10.1542/peds.2012-3692 |
| [30] | Yoshida,
M., Claypool, S.M., Wagner, J.S., Mizoguchi, E., Mizoguchi, A.,
Roopenian, D.C., Lencer, W.I. and Blumberg, R.S. (2004) Human Neonatal
Fc Receptor Mediates Transport of IgG into Luminal Secretions for
Delivery of Antigens to Mucosal Dendritic Cells. Immunity, 20, 769-783. http://dx.doi.org/10.1016/j.immuni.2004.05.007 |
| [31] | Nakata,
K., Kobayashi, K., Ishikawa, Y., Yamamoto, M., Funada, Y., Kotani, Y.,
Blumberg, R.S., Karasuyama, H., Yoshida, M. and Nishimura, Y. (2010) The
Transfer of Maternal Antigen-Specific IgG Regulates the Development of
Allergic Airway Inflammation Early in Life in an FcRn-Dependent Manner.
Biochemical and Biophysical Research Communications, 395, 238-243. http://dx.doi.org/10.1016/j.bbrc.2010.03.170 |
| [32] | Mosconi,
E., Rekima, A., Seitz-Polski, B., Kanda, A., Fleury, S., Tissandie, E.,
Monteiro, R., Dombrowicz, D.D., Julia, V., Glaichenhaus, N. and
Verhasselt, V. (2010) Breast Milk Immune Complexes Are Potent Inducers
of Oral Tolerance in Neonates and Prevent Asthma Development. Mucosal
Immunology, 3, 461-474. http://dx.doi.org/10.1038/mi.2010.23 |
| [33] | Burks,
A.W., Laubach, S. and Jones, S.M. (2008) Oral Tolerance, Food Allergy,
and Immunotherapy: Implications for Future Treatment. Journal of Allergy
and Clinical Immunology, 121, 1344-1350. http://dx.doi.org/10.1016/j.jaci.2008.02.037 eww150212lx |
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