The Immature Gut Barrier and Its Importance in Establishing Immunity in Newborn Mammals
The gut is an efficient barrier which protects against the passage of pathogenic microorganisms and potential harmful macromolecules into the body, in addition to its primary function of nutrient digestion and absorption. Contrary to the restricted macromolecular passage in adulthood, enhanced trans...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-06-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fimmu.2020.01153/full |
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| author | Björn Weström Ester Arévalo Sureda Kateryna Pierzynowska Kateryna Pierzynowska Stefan G. Pierzynowski Stefan G. Pierzynowski Francisco-José Pérez-Cano Francisco-José Pérez-Cano |
| author_facet | Björn Weström Ester Arévalo Sureda Kateryna Pierzynowska Kateryna Pierzynowska Stefan G. Pierzynowski Stefan G. Pierzynowski Francisco-José Pérez-Cano Francisco-José Pérez-Cano |
| author_sort | Björn Weström |
| collection | DOAJ |
| description | The gut is an efficient barrier which protects against the passage of pathogenic microorganisms and potential harmful macromolecules into the body, in addition to its primary function of nutrient digestion and absorption. Contrary to the restricted macromolecular passage in adulthood, enhanced transfer takes place across the intestines during early life, due to the high endocytic capacity of the immature intestinal epithelial cells during the fetal and/or neonatal periods. The timing and extent of this enhanced endocytic capacity is dependent on animal species, with a prominent non-selective intestinal macromolecular transfer in newborn ungulates, e.g., pigs, during the first few days of life, and a selective transfer of mainly immunoglobulin G (IgG), mediated by the FcRn receptor, in suckling rodents, e.g., rats and mice. In primates, maternal IgG is transferred during fetal life via the placenta, and intestinal macromolecular transfer is largely restricted in human neonates. The period of intestinal macromolecular transmission provides passive immune protection through the transfer of IgG antibodies from an immune competent mother; and may even have extra-immune beneficial effects on organ maturation in the offspring. Moreover, intestinal transfer during the fetal/neonatal periods results in increased exposure to microbial and food antigens which are then presented to the underlying immune system, which is both naïve and immature. This likely stimulates the maturation of the immune system and shifts the response toward tolerance induction instead of activation or inflammation, as usually seen in adulthood. Ingestion of mother's milk and the dietary transition to complex food at weaning, as well as the transient changes in the gut microbiota during the neonatal period, are also involved in the resulting immune response. Any disturbances in timing and/or balance of these parallel processes, i.e., intestinal epithelial maturation, luminal microbial colonization and mucosal immune maturation due to, e.g., preterm birth, infection, antibiotic use or nutrient changes during the neonatal period, might affect the establishment of the immune system in the infant. This review will focus on how differing developmental processes in the intestinal epithelium affect the macromolecular passage in different species and the possible impact of such passage on the establishment of immunity during the critical perinatal period in young mammals. |
| first_indexed | 2024-12-18T10:57:30Z |
| format | Article |
| id | doaj.art-c437a26820e04afea177d592126006c9 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-18T10:57:30Z |
| publishDate | 2020-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-c437a26820e04afea177d592126006c92022-12-21T21:10:18ZengFrontiers Media S.A.Frontiers in Immunology1664-32242020-06-011110.3389/fimmu.2020.01153531569The Immature Gut Barrier and Its Importance in Establishing Immunity in Newborn MammalsBjörn Weström0Ester Arévalo Sureda1Kateryna Pierzynowska2Kateryna Pierzynowska3Stefan G. Pierzynowski4Stefan G. Pierzynowski5Francisco-José Pérez-Cano6Francisco-José Pérez-Cano7Department of Biology, Lund University, Lund, SwedenPrecision Livestock and Nutrition Unit, TERRA Teaching and Research Centre, Gembloux Agro-Biotech, University of Liège, Gembloux, BelgiumDepartment of Biology, Lund University, Lund, SwedenDepartment of Animal Physiology, Kielanowski Institute of Animal Physiology and Nutrition, Jablonna, PolandDepartment of Biology, Lund University, Lund, SwedenDepartment of Medical Biology, Institute of Rural Health, Lublin, PolandPhysiology Section, Department of Biochemistry and Physiology, Faculty of Pharmacy and Food Science, University of Barcelona, Barcelona, SpainResearch Institute of Nutrition and Food Safety of the University of Barcelona (INSA-UB), Santa Coloma de Gramenet, SpainThe gut is an efficient barrier which protects against the passage of pathogenic microorganisms and potential harmful macromolecules into the body, in addition to its primary function of nutrient digestion and absorption. Contrary to the restricted macromolecular passage in adulthood, enhanced transfer takes place across the intestines during early life, due to the high endocytic capacity of the immature intestinal epithelial cells during the fetal and/or neonatal periods. The timing and extent of this enhanced endocytic capacity is dependent on animal species, with a prominent non-selective intestinal macromolecular transfer in newborn ungulates, e.g., pigs, during the first few days of life, and a selective transfer of mainly immunoglobulin G (IgG), mediated by the FcRn receptor, in suckling rodents, e.g., rats and mice. In primates, maternal IgG is transferred during fetal life via the placenta, and intestinal macromolecular transfer is largely restricted in human neonates. The period of intestinal macromolecular transmission provides passive immune protection through the transfer of IgG antibodies from an immune competent mother; and may even have extra-immune beneficial effects on organ maturation in the offspring. Moreover, intestinal transfer during the fetal/neonatal periods results in increased exposure to microbial and food antigens which are then presented to the underlying immune system, which is both naïve and immature. This likely stimulates the maturation of the immune system and shifts the response toward tolerance induction instead of activation or inflammation, as usually seen in adulthood. Ingestion of mother's milk and the dietary transition to complex food at weaning, as well as the transient changes in the gut microbiota during the neonatal period, are also involved in the resulting immune response. Any disturbances in timing and/or balance of these parallel processes, i.e., intestinal epithelial maturation, luminal microbial colonization and mucosal immune maturation due to, e.g., preterm birth, infection, antibiotic use or nutrient changes during the neonatal period, might affect the establishment of the immune system in the infant. This review will focus on how differing developmental processes in the intestinal epithelium affect the macromolecular passage in different species and the possible impact of such passage on the establishment of immunity during the critical perinatal period in young mammals.https://www.frontiersin.org/article/10.3389/fimmu.2020.01153/fullintestinepermeabilityfetaltranscytosisFcRntolerance |
| spellingShingle | Björn Weström Ester Arévalo Sureda Kateryna Pierzynowska Kateryna Pierzynowska Stefan G. Pierzynowski Stefan G. Pierzynowski Francisco-José Pérez-Cano Francisco-José Pérez-Cano The Immature Gut Barrier and Its Importance in Establishing Immunity in Newborn Mammals Frontiers in Immunology intestine permeability fetal transcytosis FcRn tolerance |
| title | The Immature Gut Barrier and Its Importance in Establishing Immunity in Newborn Mammals |
| title_full | The Immature Gut Barrier and Its Importance in Establishing Immunity in Newborn Mammals |
| title_fullStr | The Immature Gut Barrier and Its Importance in Establishing Immunity in Newborn Mammals |
| title_full_unstemmed | The Immature Gut Barrier and Its Importance in Establishing Immunity in Newborn Mammals |
| title_short | The Immature Gut Barrier and Its Importance in Establishing Immunity in Newborn Mammals |
| title_sort | immature gut barrier and its importance in establishing immunity in newborn mammals |
| topic | intestine permeability fetal transcytosis FcRn tolerance |
| url | https://www.frontiersin.org/article/10.3389/fimmu.2020.01153/full |
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