Influence of Leptin and Adiponectin Supplementation on Intraepithelial Lymphocyte and Microbiota Composition in Suckling Rats

Dietary components in early life play a role in both microbiota and intestinal immune system maturation in mammalian species. Adipokines, as endogenously produced hormones from breast milk, may have an impact on this process. The aim of the present study was to establish the influence of leptin and...

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Main Authors: Blanca Grases-Pintó, Mar Abril-Gil, Margarida Castell, Maria J. Rodríguez-Lagunas, Stephen Burleigh, Frida Fåk Hållenius, Olena Prykhodko, Francisco J. Pérez-Cano, Àngels Franch
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-10-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/article/10.3389/fimmu.2019.02369/full
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author Blanca Grases-Pintó
Blanca Grases-Pintó
Mar Abril-Gil
Mar Abril-Gil
Margarida Castell
Margarida Castell
Maria J. Rodríguez-Lagunas
Maria J. Rodríguez-Lagunas
Stephen Burleigh
Stephen Burleigh
Frida Fåk Hållenius
Frida Fåk Hållenius
Olena Prykhodko
Olena Prykhodko
Francisco J. Pérez-Cano
Francisco J. Pérez-Cano
Àngels Franch
Àngels Franch
author_facet Blanca Grases-Pintó
Blanca Grases-Pintó
Mar Abril-Gil
Mar Abril-Gil
Margarida Castell
Margarida Castell
Maria J. Rodríguez-Lagunas
Maria J. Rodríguez-Lagunas
Stephen Burleigh
Stephen Burleigh
Frida Fåk Hållenius
Frida Fåk Hållenius
Olena Prykhodko
Olena Prykhodko
Francisco J. Pérez-Cano
Francisco J. Pérez-Cano
Àngels Franch
Àngels Franch
author_sort Blanca Grases-Pintó
collection DOAJ
description Dietary components in early life play a role in both microbiota and intestinal immune system maturation in mammalian species. Adipokines, as endogenously produced hormones from breast milk, may have an impact on this process. The aim of the present study was to establish the influence of leptin and adiponectin supplementation during suckling on the intraepithelial lymphocyte composition, intestinal barrier function, intestinal gene expression, and gut microbiota in rat. For this purpose, newborn Wistar rats were supplemented daily with leptin, adiponectin, or whey protein concentrate during the first 21 days of life. Lymphocyte composition was established by immunofluorescence staining and flow cytometry analysis; intestinal gene expression by real-time PCR and cecal microbiota were analyzed through 16S rRNA gene sequencing. Although leptin and adiponectin were able to increase the Tc TCRαβ+ and NKT cell proportion, they decreased the NK cell percentage in IEL. Moreover, adipokine supplementation differentially modified CD8+ IEL. While the supplementation of leptin increased the proportion of CD8αα+ IEL (associated to a more intestinal phenotype), adiponectin enhanced that of CD8αβ+ (related to a peripheral phenotype). Furthermore, both adipokines enhanced the gene expression of TNF-α, MUC-2, and MUC-3, and decreased that of FcRn. In addition, the adipokine supplementations decreased the abundance of the Proteobacteria phylum and the presence of Blautia. Moreover, leptin-supplemented animals had lower relative abundance of Sutterella and a higher proportion of Clostridium genus, among others. However, supplementation with adiponectin resulted in lower abundance of the Roseburia genus and a higher proportion of the Enterococcus genus. In conclusion, the supplementation with leptin and adiponectin throughout the suckling period had an impact on both the IEL composition and the gut microbiota pattern, suggesting a modulatory role of these adipokines on the development of intestinal functionality.
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spelling doaj.art-44d66c4b09704fea93d0fb6a20e8ce902022-12-21T17:50:26ZengFrontiers Media S.A.Frontiers in Immunology1664-32242019-10-011010.3389/fimmu.2019.02369463571Influence of Leptin and Adiponectin Supplementation on Intraepithelial Lymphocyte and Microbiota Composition in Suckling RatsBlanca Grases-Pintó0Blanca Grases-Pintó1Mar Abril-Gil2Mar Abril-Gil3Margarida Castell4Margarida Castell5Maria J. Rodríguez-Lagunas6Maria J. Rodríguez-Lagunas7Stephen Burleigh8Stephen Burleigh9Frida Fåk Hållenius10Frida Fåk Hållenius11Olena Prykhodko12Olena Prykhodko13Francisco J. Pérez-Cano14Francisco J. Pérez-Cano15Àngels Franch16Àngels Franch17Physiology 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, SpainPhysiology 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, SpainPhysiology 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, SpainPhysiology 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, SpainFood for Health Science Centre, Lund University, Lund, SwedenDepartment of Food Technology, Engineering and Nutrition, Lund University, Lund, SwedenFood for Health Science Centre, Lund University, Lund, SwedenDepartment of Food Technology, Engineering and Nutrition, Lund University, Lund, SwedenFood for Health Science Centre, Lund University, Lund, SwedenDepartment of Food Technology, Engineering and Nutrition, Lund University, Lund, SwedenPhysiology 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, SpainPhysiology 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, SpainDietary components in early life play a role in both microbiota and intestinal immune system maturation in mammalian species. Adipokines, as endogenously produced hormones from breast milk, may have an impact on this process. The aim of the present study was to establish the influence of leptin and adiponectin supplementation during suckling on the intraepithelial lymphocyte composition, intestinal barrier function, intestinal gene expression, and gut microbiota in rat. For this purpose, newborn Wistar rats were supplemented daily with leptin, adiponectin, or whey protein concentrate during the first 21 days of life. Lymphocyte composition was established by immunofluorescence staining and flow cytometry analysis; intestinal gene expression by real-time PCR and cecal microbiota were analyzed through 16S rRNA gene sequencing. Although leptin and adiponectin were able to increase the Tc TCRαβ+ and NKT cell proportion, they decreased the NK cell percentage in IEL. Moreover, adipokine supplementation differentially modified CD8+ IEL. While the supplementation of leptin increased the proportion of CD8αα+ IEL (associated to a more intestinal phenotype), adiponectin enhanced that of CD8αβ+ (related to a peripheral phenotype). Furthermore, both adipokines enhanced the gene expression of TNF-α, MUC-2, and MUC-3, and decreased that of FcRn. In addition, the adipokine supplementations decreased the abundance of the Proteobacteria phylum and the presence of Blautia. Moreover, leptin-supplemented animals had lower relative abundance of Sutterella and a higher proportion of Clostridium genus, among others. However, supplementation with adiponectin resulted in lower abundance of the Roseburia genus and a higher proportion of the Enterococcus genus. In conclusion, the supplementation with leptin and adiponectin throughout the suckling period had an impact on both the IEL composition and the gut microbiota pattern, suggesting a modulatory role of these adipokines on the development of intestinal functionality.https://www.frontiersin.org/article/10.3389/fimmu.2019.02369/fullleptinadiponectinsuckling ratIELmicrobiota
spellingShingle Blanca Grases-Pintó
Blanca Grases-Pintó
Mar Abril-Gil
Mar Abril-Gil
Margarida Castell
Margarida Castell
Maria J. Rodríguez-Lagunas
Maria J. Rodríguez-Lagunas
Stephen Burleigh
Stephen Burleigh
Frida Fåk Hållenius
Frida Fåk Hållenius
Olena Prykhodko
Olena Prykhodko
Francisco J. Pérez-Cano
Francisco J. Pérez-Cano
Àngels Franch
Àngels Franch
Influence of Leptin and Adiponectin Supplementation on Intraepithelial Lymphocyte and Microbiota Composition in Suckling Rats
Frontiers in Immunology
leptin
adiponectin
suckling rat
IEL
microbiota
title Influence of Leptin and Adiponectin Supplementation on Intraepithelial Lymphocyte and Microbiota Composition in Suckling Rats
title_full Influence of Leptin and Adiponectin Supplementation on Intraepithelial Lymphocyte and Microbiota Composition in Suckling Rats
title_fullStr Influence of Leptin and Adiponectin Supplementation on Intraepithelial Lymphocyte and Microbiota Composition in Suckling Rats
title_full_unstemmed Influence of Leptin and Adiponectin Supplementation on Intraepithelial Lymphocyte and Microbiota Composition in Suckling Rats
title_short Influence of Leptin and Adiponectin Supplementation on Intraepithelial Lymphocyte and Microbiota Composition in Suckling Rats
title_sort influence of leptin and adiponectin supplementation on intraepithelial lymphocyte and microbiota composition in suckling rats
topic leptin
adiponectin
suckling rat
IEL
microbiota
url https://www.frontiersin.org/article/10.3389/fimmu.2019.02369/full
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