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Mode of Delivery Shapes Gut Colonization Pattern and Modulates Regulatory Immunity in Mice

Camilla H. F. Hansen, Line S. F. Andersen, Łukasz Krych, Stine B. Metzdorff, Jane P. Hasselby, Søren Skov, Dennis S. Nielsen, Karsten Buschard, Lars H. Hansen and Axel K. Hansen
J Immunol June 20, 2014, 1400085; DOI: https://doi.org/10.4049/jimmunol.1400085
Camilla H. F. Hansen
*Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg C, Denmark;
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Line S. F. Andersen
*Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg C, Denmark;
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Łukasz Krych
†Department of Food Science, Faculty of Science, University of Copenhagen, 1958 Frederiksberg C, Denmark;
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Stine B. Metzdorff
*Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg C, Denmark;
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Jane P. Hasselby
‡Department of Pathology, Rigshospitalet, 2100 Copenhagen, Denmark;
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Søren Skov
*Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg C, Denmark;
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Dennis S. Nielsen
†Department of Food Science, Faculty of Science, University of Copenhagen, 1958 Frederiksberg C, Denmark;
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Karsten Buschard
§Bartholin Institute, Rigshospitalet, 2100 Copenhagen, Denmark;
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Lars H. Hansen
¶Department of Biology, Faculty of Science, University of Copenhagen, 1307 Copenhagen, Denmark; and
‖Department of Environmental Science, Faculty of Science and Technology, Aarhus University, 4000 Roskilde, Denmark
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Axel K. Hansen
*Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg C, Denmark;
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Abstract

Delivery mode has been associated with long-term changes in gut microbiota composition and more recently also with changes in the immune system. This has further been suggested to link Cesarean section (C-section) with an increased risk for development of immune-mediated diseases such as type 1 diabetes. In this study, we demonstrate that both C-section and cross-fostering with a genetically distinct strain influence the gut microbiota composition and immune key markers in mice. Gut microbiota profiling by denaturing gradient gel electrophoresis and 454/FLX-based 16S rRNA gene amplicon sequencing revealed that mice born by C-section had a distinct bacterial profile at weaning characterized by higher abundance of Bacteroides and Lachnospiraceae, and less Rikenellaceae and Ruminococcus. No clustering according to delivery method as determined by principal component analysis of denaturing gradient gel electrophoresis profiles was evident in adult mice. However, the adult C-section–born mice had lower proportions of Foxp3+ regulatory T cells, tolerogenic CD103+ dendritic cells, and less Il10 gene expression in mesenteric lymph nodes and spleens. This demonstrates long-term systemic effect on the regulatory immune system that was also evident in NOD mice, a model of type 1 diabetes, born by C-section. However, no effect of delivery mode was seen on diabetes incidence or insulitis development. In conclusion, the first exposure to microorganisms seems to be crucial for the early life gut microbiota and priming of regulatory immune system in mice, and mode of delivery strongly influences this.

Footnotes

  • This work was supported by the Chemometric Analysis Centre at the University of Copenhagen and the Center for Applied Laboratory Animal Research.

  • The online version of this article contains supplemental material.

  • Received January 13, 2014.
  • Accepted June 2, 2014.
  • Copyright © 2014 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (5)
The Journal of Immunology
Vol. 206, Issue 5
1 Mar 2021
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Mode of Delivery Shapes Gut Colonization Pattern and Modulates Regulatory Immunity in Mice
Camilla H. F. Hansen, Line S. F. Andersen, Łukasz Krych, Stine B. Metzdorff, Jane P. Hasselby, Søren Skov, Dennis S. Nielsen, Karsten Buschard, Lars H. Hansen, Axel K. Hansen
The Journal of Immunology June 20, 2014, 1400085; DOI: 10.4049/jimmunol.1400085

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Mode of Delivery Shapes Gut Colonization Pattern and Modulates Regulatory Immunity in Mice
Camilla H. F. Hansen, Line S. F. Andersen, Łukasz Krych, Stine B. Metzdorff, Jane P. Hasselby, Søren Skov, Dennis S. Nielsen, Karsten Buschard, Lars H. Hansen, Axel K. Hansen
The Journal of Immunology June 20, 2014, 1400085; DOI: 10.4049/jimmunol.1400085
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