Microbial Exposure During Early Life Has Persistent Effects on Natural Killer T Cell Function

Exposure to microbes during early childhood is associated with protection from immune-mediated diseases such as inflammatory bowel disease (IBD) and asthma. Here, we show that in germ-free (GF) mice, invariant natural killer T (iNKT) cells accumulate in the colonic lamina propria and lung, resulting...

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Published in	Science (American Association for the Advancement of Science) Vol. 336; no. 6080; pp. 489 - 493
Main Authors	Olszak, Torsten, An, Dingding, Zeissig, Sebastian, Vera, Miguel Pinilla, Richter, Julia, Franke, Andre, Glickman, Jonathan N., Siebert, Reiner, Baron, Rebecca M., Kasper, Dennis L., Blumberg, Richard S.
Format	Journal Article
Language	English
Published	Washington, DC American Association for the Advancement of Science 27.04.2012 The American Association for the Advancement of Science
Subjects	Aging Animal models Animals Animals, Newborn Antigens, CD1d - immunology Asthma Asthma - immunology Bacteria - growth & development Biological and medical sciences Chemokine CXCL16 Chemokine CXCL6 - genetics Chemokine CXCL6 - metabolism Children & youth Colitis Colitis, Ulcerative - chemically induced Colitis, Ulcerative - immunology Colon - immunology Colon - microbiology Disease Models, Animal Disease Susceptibility DNA DNA Methylation Epidemiology Fundamental and applied biological sciences. Psychology Fundamental immunology Genetics of the immune response Germ-Free Life Ileum Immune system Immunobiology Inflammatory bowel diseases Inflammatory diseases Intestinal Mucosa - immunology Intestines - immunology Intestines - microbiology Lung - immunology Lungs Lymphocytes Mice Mice, Inbred C57BL Microbiota Microorganisms Natural killer T cells Natural Killer T-Cells - immunology Oxazolone Pathology Receptors, CXCR - genetics Receptors, CXCR - metabolism Receptors, CXCR6 Specific Pathogen-Free Organisms Young Children Immunoprotection Vertebrata Mammalia Mouse Rodentia Early Exposure NKT cell
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Abstract	Exposure to microbes during early childhood is associated with protection from immune-mediated diseases such as inflammatory bowel disease (IBD) and asthma. Here, we show that in germ-free (GF) mice, invariant natural killer T (iNKT) cells accumulate in the colonic lamina propria and lung, resulting in increased morbidity in models of IBD and allergic asthma as compared with that of specific pathogen-free mice. This was associated with increased intestinal and pulmonary expression of the chemokine ligand CXCL16, which was associated with increased mucosal iNKT cells. Colonization of neonatal—but not adult—GF mice with a conventional microbiota protected the animals from mucosal iNKT accumulation and related pathology. These results indicate that age-sensitive contact with commensal microbes is critical for establishing mucosal iNKT cell tolerance to later environmental exposures.
AbstractList	Microbes: Early and OftenEpidemiological studies have suggested that the increase in the incidence of asthma and other inflammatory diseases seen in many parts of the world may be due to a reduced exposure to microbes during early childhood. Olszak et al. (p. 489, published online 22 March) now show that commensal microflora help to regulate the numbers and functions of natural killer T (NKT) cells in the colon and lung in mice. Germ-free mice had elevated numbers of NKT cells in these tissues and were more susceptible to chemically induced colitis and allergic asthma. Neonatal recolonization of germ-free mice with microflora prevented enhanced colitis and asthma sensitivity; however, exposure of adult mice to these conditions was not effective. Thus, early exposure to microbes has important, lasting effects on the immune system's sensitivity to inflammation. Exposure to microbes during early childhood is associated with protection from immune-mediated diseases such as inflammatory bowel disease (IBD) and asthma. Here, we show that in germ-free (GF) mice, invariant natural killer T (iNKT) cells accumulate in the colonic lamina propria and lung, resulting in increased morbidity in models of IBD and allergic asthma as compared with that of specific pathogen-free mice. This was associated with increased intestinal and pulmonary expression of the chemokine ligand CXCL16, which was associated with increased mucosal iNKT cells. Colonization of neonatal-but not adult-GF mice with a conventional microbiota protected the animals from mucosal iNKT accumulation and related pathology. These results indicate that age-sensitive contact with commensal microbes is critical for establishing mucosal iNKT cell tolerance to later environmental exposures. Epidemiological studies have suggested that the increase in the incidence of asthma and other inflammatory diseases seen in many parts of the world may be due to a reduced exposure to microbes during early childhood. Olszak et al. (p. 489, published online 22 March) now show that commensal microflora help to regulate the numbers and functions of natural killer T (NKT) cells in the colon and lung in mice. Germ-free mice had elevated numbers of NKT cells in these tissues and were more susceptible to chemically induced colitis and allergic asthma. Neonatal recolonization of germ-free mice with microflora prevented enhanced colitis and asthma sensitivity; however, exposure of adult mice to these conditions was not effective. Thus, early exposure to microbes has important, lasting effects on the immune system's sensitivity to inflammation. Early exposure of germ-free mice to microbes keeps later inflammation in check by modulating immune cells. Exposure to microbes during early childhood is associated with protection from immune-mediated diseases such as inflammatory bowel disease (IBD) and asthma. Here, we show that in germ-free (GF) mice, invariant natural killer T (iNKT) cells accumulate in the colonic lamina propria and lung, resulting in increased morbidity in models of IBD and allergic asthma as compared with that of specific pathogen-free mice. This was associated with increased intestinal and pulmonary expression of the chemokine ligand CXCL16, which was associated with increased mucosal iNKT cells. Colonization of neonatal—but not adult—GF mice with a conventional microbiota protected the animals from mucosal iNKT accumulation and related pathology. These results indicate that age-sensitive contact with commensal microbes is critical for establishing mucosal iNKT cell tolerance to later environmental exposures. Epidemiological studies have suggested that the increase in the incidence of asthma and other inflammatory diseases seen in many parts of the world may be due to a reduced exposure to microbes during early childhood. Olszak et al. (p. 489, published online 22 March) now show that commensal microflora help to regulate the numbers and functions of natural killer T (NKT) cells in the colon and lung in mice. Germ-free mice had elevated numbers of NKT cells in these tissues and were more susceptible to chemically induced colitis and allergic asthma. Neonatal recolonization of germ-free mice with microflora prevented enhanced colitis and asthma sensitivity; however, exposure of adult mice to these conditions was not effective. Thus, early exposure to microbes has important, lasting effects on the immune system's sensitivity to inflammation. Exposure to microbes during early childhood is associated with protection from immune-mediated diseases such as inflammatory bowel disease (IBD) and asthma. Here, we show that in germ-free (GF) mice, invariant natural killer T (iNKT) cells accumulate in the colonic lamina propria and lung, resulting in increased morbidity in models of IBD and allergic asthma as compared with that of specific pathogen-free mice. This was associated with increased intestinal and pulmonary expression of the chemokine ligand CXCL16, which was associated with increased mucosal iNKT cells. Colonization of neonatal--but not adult--GF mice with a conventional microbiota protected the animals from mucosal iNKT accumulation and related pathology. These results indicate that age-sensitive contact with commensal microbes is critical for establishing mucosal iNKT cell tolerance to later environmental exposures. [PUBLICATION ABSTRACT]
Author	Glickman, Jonathan N. Siebert, Reiner Baron, Rebecca M. Zeissig, Sebastian An, Dingding Richter, Julia Franke, Andre Vera, Miguel Pinilla Blumberg, Richard S. Kasper, Dennis L. Olszak, Torsten
AuthorAffiliation	6 Institute of Clinical Molecular Biology, Christian-Albrechts University, Kiel 24105, Germany 7 GI Pathology, Caris Diagnostics, Caris Life Sciences, Newton, MA 02464, USA 5 Institute of Human Genetics, Christian-Albrechts University Kiel and University Medical Center Schleswig-Holstein, Kiel 24105, Germany 3 Department of Internal Medicine I, University Medical Center Schleswig-Holstein, Kiel 24105, Germany 1 Division of Gastroenterology, Hepatology, and Endoscopy, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA 4 Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA 2 Channing Laboratory, Brigham and Women's Hospital and Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115, USA
AuthorAffiliation_xml	– name: 4 Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 1 Division of Gastroenterology, Hepatology, and Endoscopy, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 7 GI Pathology, Caris Diagnostics, Caris Life Sciences, Newton, MA 02464, USA – name: 6 Institute of Clinical Molecular Biology, Christian-Albrechts University, Kiel 24105, Germany – name: 3 Department of Internal Medicine I, University Medical Center Schleswig-Holstein, Kiel 24105, Germany – name: 5 Institute of Human Genetics, Christian-Albrechts University Kiel and University Medical Center Schleswig-Holstein, Kiel 24105, Germany – name: 2 Channing Laboratory, Brigham and Women's Hospital and Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115, USA
Author_xml	– sequence: 1 givenname: Torsten surname: Olszak fullname: Olszak, Torsten – sequence: 2 givenname: Dingding surname: An fullname: An, Dingding – sequence: 3 givenname: Sebastian surname: Zeissig fullname: Zeissig, Sebastian – sequence: 4 givenname: Miguel Pinilla surname: Vera fullname: Vera, Miguel Pinilla – sequence: 5 givenname: Julia surname: Richter fullname: Richter, Julia – sequence: 6 givenname: Andre surname: Franke fullname: Franke, Andre – sequence: 7 givenname: Jonathan N. surname: Glickman fullname: Glickman, Jonathan N. – sequence: 8 givenname: Reiner surname: Siebert fullname: Siebert, Reiner – sequence: 9 givenname: Rebecca M. surname: Baron fullname: Baron, Rebecca M. – sequence: 10 givenname: Dennis L. surname: Kasper fullname: Kasper, Dennis L. – sequence: 11 givenname: Richard S. surname: Blumberg fullname: Blumberg, Richard S.
BackLink	http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25861825$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/22442383$$D View this record in MEDLINE/PubMed
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References	22498779 - Nat Rev Immunol. 2012 Apr 13;12(5):319. doi: 10.1038/nri3213 e_1_3_2_26_2 e_1_3_2_27_2 e_1_3_2_28_2 e_1_3_2_29_2 Roark J. H. (e_1_3_2_17_2) 1998; 160 e_1_3_2_20_2 e_1_3_2_21_2 e_1_3_2_22_2 e_1_3_2_23_2 e_1_3_2_24_2 e_1_3_2_25_2 e_1_3_2_9_2 e_1_3_2_15_2 e_1_3_2_38_2 e_1_3_2_8_2 e_1_3_2_16_2 e_1_3_2_37_2 e_1_3_2_7_2 e_1_3_2_6_2 e_1_3_2_18_2 e_1_3_2_19_2 e_1_3_2_30_2 e_1_3_2_32_2 e_1_3_2_10_2 e_1_3_2_31_2 e_1_3_2_5_2 e_1_3_2_11_2 e_1_3_2_34_2 e_1_3_2_4_2 e_1_3_2_12_2 e_1_3_2_33_2 e_1_3_2_3_2 e_1_3_2_13_2 e_1_3_2_36_2 e_1_3_2_2_2 e_1_3_2_14_2 e_1_3_2_35_2
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Snippet	Exposure to microbes during early childhood is associated with protection from immune-mediated diseases such as inflammatory bowel disease (IBD) and asthma.... Epidemiological studies have suggested that the increase in the incidence of asthma and other inflammatory diseases seen in many parts of the world may be due... Microbes: Early and OftenEpidemiological studies have suggested that the increase in the incidence of asthma and other inflammatory diseases seen in many parts...
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SubjectTerms	Aging Animal models Animals Animals, Newborn Antigens, CD1d - immunology Asthma Asthma - immunology Bacteria - growth & development Biological and medical sciences Chemokine CXCL16 Chemokine CXCL6 - genetics Chemokine CXCL6 - metabolism Children & youth Colitis Colitis, Ulcerative - chemically induced Colitis, Ulcerative - immunology Colon - immunology Colon - microbiology Disease Models, Animal Disease Susceptibility DNA DNA Methylation Epidemiology Fundamental and applied biological sciences. Psychology Fundamental immunology Genetics of the immune response Germ-Free Life Ileum Immune system Immunobiology Inflammatory bowel diseases Inflammatory diseases Intestinal Mucosa - immunology Intestines - immunology Intestines - microbiology Lung - immunology Lungs Lymphocytes Mice Mice, Inbred C57BL Microbiota Microorganisms Natural killer T cells Natural Killer T-Cells - immunology Oxazolone Pathology Receptors, CXCR - genetics Receptors, CXCR - metabolism Receptors, CXCR6 Specific Pathogen-Free Organisms Young Children
Title	Microbial Exposure During Early Life Has Persistent Effects on Natural Killer T Cell Function
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