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      Transfer of Maternal Immune Cells by Breastfeeding: Maternal Cytotoxic T Lymphocytes Present in Breast Milk Localize in the Peyer’s Patches of the Nursed Infant

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          Abstract

          Despite our knowledge of the protective role of antibodies passed to infants through breast milk, our understanding of immunity transfer via maternal leukocytes is still limited. To emulate the immunological interface between the mother and her infant while breast-feeding, we used murine pups fostered after birth onto MHC-matched and MHC-mismatched dams. Overall, data revealed that: 1) Survival of breast milk leukocytes in suckling infants is possible, but not significant after the foster-nursing ceases; 2) Most breast milk lymphocytes establish themselves in specific areas of the intestine termed Peyer’s patches (PPs); 3) While most leukocytes in the milk bolus were myeloid cells, the majority of breast milk leukocytes localized to PPs were T lymphocytes, and cytotoxic T cells (CTLs) in particular; 4) These CTLs exhibit high levels of the gut-homing molecules α4β7 and CCR9, but a reduced expression of the systemic homing marker CD62L; 5) Under the same activation conditions, transferred CD8 T cells through breast milk have a superior capacity to produce potent cytolytic and inflammatory mediators when compared to those generated by the breastfed infant. It is therefore possible that maternal CTLs found in breast milk are directed to the PPs to compensate for the immature adaptive immune system of the infant in order to protect it against constant oral infectious risks during the postnatal phase.

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          Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium.

          The transcytosis of antigens across the gut epithelium by microfold cells (M cells) is important for the induction of efficient immune responses to some mucosal antigens in Peyer's patches. Recently, substantial progress has been made in our understanding of the factors that influence the development and function of M cells. This review highlights these important advances, with particular emphasis on: the host genes which control the functional maturation of M cells; how this knowledge has led to the rapid advance in our understanding of M-cell biology in the steady state and during aging; molecules expressed on M cells which appear to be used as "immunosurveillance" receptors to sample pathogenic microorganisms in the gut; how certain pathogens appear to exploit M cells to infect the host; and finally how this knowledge has been used to specifically target antigens to M cells to attempt to improve the efficacy of mucosal vaccines.
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            Transfer of antibody via mother's milk.

            Differing from humans, IgG from breast milk in many animal species (rodents, bovines, cats, ferrets, etc.) are transported across the intestinal epithelium into the neonatal circulation. This transport is located at the duodenal and jejunal level where enterocytes express a surface membrane receptor able to bind Fc of IgG and to facilitate transcytosis of these immunoglobulins. Fcgamma-R, which is very similar to the placenta receptor responsible for active transplacental transfer of IgG in humans, binds IgG but not other isotypes. Maternal milk antibodies represent an important part of circulating IgG in these animals, as they are involved in the negative feedback of endogenous IgG synthesis. This phenomenon stops abruptly as soon as weaning takes place. Neonatal calves that have a defect in such transfer of maternal immunoglobulins are at high risk of systemic infectious diseases. In humans, in whom gut closure occurs precociously, breast milk antibodies do not enter neonatal/infant circulation. A large part of immunoglobulins excreted in milk are IgA that protect mainly against enteric infections. The specificity of maternal milk IgA is driven by an entero-mammary cell circulation. Human milk also contains anti-idiotypic antibodies capable of enhancing infant antibody response. Maternal milk antibodies coat infant mucosal surfaces and some have a clear protective role. This has been studied extensively in infectious disease models such as rotavirus, E. coli, poliovirus, and retroviruses. In the rotavirus model, antirotaviral IgA can be detected in stools of breast-fed but not bottle-fed neonates. In a large cohort of lactating women infected with HIV-1 in Rwanda, anti-HIV milk antibodies of the IgG isotype were more frequently detected followed by secretory IgM. Surprisingly, anti-HIV-1 SIgA were less frequently found. The presence of milk SIgA at 15 days as well as the persistence of a SIgM response during the whole lactation period was associated with lower risk of HIV transmission from the mother to the infant. Recently, HIV-1 antibodies from maternal milk have been shown to block transcytosis in vitro in a monolayer enterocyte model. Among these antibodies, those directed against the ELDKWA epitope had higher neutralising activity than serum antibodies. In humans, milk excreted antibodies play a major role in protecting infants from infection by pathogens having a mucosal portal of entry.
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              Continued maturation of thymic emigrants in the periphery.

              Developing thymocytes are selected for recognition of molecules encoded by the major histocompatibility complex, purged of self-reactive cells and committed to either the CD4 or CD8 lineage. The 1% of thymocytes that complete these tasks emigrate and join the population of peripheral lymphocytes. Whether T cell maturation is complete at the time of thymic exit has been a subject of debate. Using mice transgenic for green fluorescent protein driven by the recombination activating gene 2 promoter to identify recent thymic emigrants, we now show that T cell differentiation continues post-thymically, with progressive maturation of both surface phenotype and immune function. In addition, the relative contribution of CD4 and CD8 recent thymic emigrants was modulated as they entered the peripheral T cell pool. Thus, T cell maturation and subset contribution are both finalized in the lymphoid periphery.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                10 June 2016
                2016
                : 11
                : 6
                : e0156762
                Affiliations
                [1 ]The Child Health Institute of New Jersey, Robert Wood Johnson Medical School, Rutgers University, New Brunswick, New Jersey, United States of America
                [2 ]Department of Microbiology and Immunology, University of Michigan School of Medicine, Ann Arbor, Michigan, United States of America
                INRA, UR1282, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AL YL. Performed the experiments: AC DS MT OZ HM AT YL AL. Analyzed the data: AC DS AT AL. Contributed reagents/materials/analysis tools: YL DSA. Wrote the paper: AL AC YL OZ.

                Author information
                http://orcid.org/0000-0002-3714-4628
                Article
                PONE-D-16-04319
                10.1371/journal.pone.0156762
                4902239
                27285085
                41ae2d8e-d66a-46f0-9523-ef69765ddf8a
                © 2016 Cabinian et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 February 2016
                : 19 May 2016
                Page count
                Figures: 3, Tables: 0, Pages: 18
                Funding
                Funded by: The Robert Wood Johnson Foundation for the Child Health Institute of New Jersey
                Award ID: Grant # 67038
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000867, Robert Wood Johnson Foundation;
                Award ID: Grant # 581534
                Award Recipient :
                Funded by: NIH NIAID
                Award ID: R01AI083642
                Award Recipient :
                Funded by: NIH NIAID
                Award ID: R01 AI083988
                Award Recipient :
                The authors would like to acknowledge the support of the Robert Wood Johnson Foundation (grant # 67038) for the Child Health Institute of New Jersey, NIH NIAID R01 AI083988 to DSA, NIH NIAID R01AI083642 to YL, and Robert Wood Johnson Foundation (grant # 581534) to AL.
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