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Changes in lamina propria dendritic cells on the oral administration of exogenous protein antigens during weaning

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Abstract

Two critical periods of maximum exposure to antigens occur in young mammals, immediately after birth and at weaning, as a result of colonization by commensal bacteria and the ingestion of new diets. At weaning, active immune responses of antibody production against dietary proteins are known to occur, but simultaneously, oral tolerance is acquired for harmless food proteins. However, regulated mechanisms of the immune system at weaning remain to be elucidated although its immune responses may be somewhat similar to those in adulthood. Considering that tolerogenic antigen-presenting cells (APCs) are likely to be a key factor in the acquisition of oral tolerance, in the present study, we examined the changes of dendritic cells (DCs) in the lamina propria (LP) on exposure to food proteins at weaning. C57BL/6 female mice were weaned at the age of 3 weeks and orally administered 10 mg of ovalbumin (OVA) for ten consecutive days after weaning. The administration led to a decrease in the plasma level of immunoglobulin specific for OVA, suggesting the acquisition of oral tolerance. The uptake of fluorescence-labeled OVA was significantly observed for CD11c+LPDCs. When we analyzed the changes of two types of LPDCs, PDCA-1+ MHC II+ DCs and CD103+ MHC II+ DCs, ten consecutive gavages of OVA marginally, but not significantly, augmented only the frequency of PDCA-1+ MHC II+ DCs. Considering that the change of APCs likely appears immediately on the response to antigen intake, we found the statistically significant increase in the frequency of PDCA-1+ DCs, but not in that of CD103+ DCs, even after two treatments, indicating PDCA-1+ DCs to be recruited in the LP within 2 days of exposure to food proteins. These results suggest that the behavior of tolerogenic PDCA-1+ DCs may change at weaning with the removal of the immunoprotective components of maternal milk.

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Abbreviations

APC:

Antigen-presenting cell

DC:

Dendritic cell

LP:

Lamina propria

MLN:

Mesenteric lymph node

OVA:

Ovalbumin

PP:

Peyer’s patch

pDC:

Plasmacytoid dendritic cell

Treg:

Regulatory T

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Acknowledgments

This work was supported in part by a Grant-in-Aid for Exploratory Research (No. 15658108) to F. T. from the Ministry of Education, Science, Sports, and Culture of Japan, and also in part by a Grant to F. T. from Japan Dairy Association.

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Authors and Affiliations

  1. Laboratory of Food Environmental Science, Division of Food Science and Biotechnology, Graduate School of Agriculture, Kyoto University, Kitashirakawa-Oiwake-cho, Sakyo-ku, Kyoto, Kyoto, 606-8502, Japan

    Ryuji Ohue, Masahiro Nakamoto, Naofumi Kitabatake & Fumito Tani

  2. Laboratory of Global Food Science, Department of Natural Resources, Graduate School of Global Environmental Studies, Kyoto University, Kitashirakawa-Oiwake-cho, Sakyo-ku, Kyoto, Kyoto, 606-8502, Japan

    Naofumi Kitabatake & Fumito Tani

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  1. Ryuji Ohue
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  2. Masahiro Nakamoto
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  3. Naofumi Kitabatake
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  4. Fumito Tani
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Correspondence to Fumito Tani.

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Ohue, R., Nakamoto, M., Kitabatake, N. et al. Changes in lamina propria dendritic cells on the oral administration of exogenous protein antigens during weaning. Cytotechnology 64, 221–230 (2012). https://doi.org/10.1007/s10616-011-9351-z

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  • DOI: https://doi.org/10.1007/s10616-011-9351-z

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