Gastric bypass surgery weight loss-independently induces gut Il-22 release in association with improved glycemic control in obese Zucker fatty rats

Background: Roux-en-Y gastric bypass surgery (RYGB) improves glycemic control in individuals with severe obesity beyond the effects of weight loss alone. To identify potential underlying mechanisms, we asked how equivalent weight loss from RYGB and from chronic caloric restriction impact gut release...

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Main Authors: Florian Seyfried, Rebecca Springer, Annett Hoffmann, Maximilian Gruber, Christoph Otto, Nicolas Schlegel, Mohammed K. Hankir
Format: Article
Language:English
Published: Elsevier 2023-03-01
Series:Metabolism Open
Online Access:http://www.sciencedirect.com/science/article/pii/S2589936822000500
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author Florian Seyfried
Rebecca Springer
Annett Hoffmann
Maximilian Gruber
Christoph Otto
Nicolas Schlegel
Mohammed K. Hankir
author_facet Florian Seyfried
Rebecca Springer
Annett Hoffmann
Maximilian Gruber
Christoph Otto
Nicolas Schlegel
Mohammed K. Hankir
author_sort Florian Seyfried
collection DOAJ
description Background: Roux-en-Y gastric bypass surgery (RYGB) improves glycemic control in individuals with severe obesity beyond the effects of weight loss alone. To identify potential underlying mechanisms, we asked how equivalent weight loss from RYGB and from chronic caloric restriction impact gut release of the metabolically beneficial cytokine interleukin-22 (Il-22). Methods: Obese male Zucker fatty rats were randomized into sham-operated (Sham), RYGB, and sham-operated, body weight-matched to RYGB (BWM) groups. Food intake and body weight were measured regularly for 4 weeks. An oral glucose tolerance test (OGTT) was performed on postoperative day 27. Portal vein plasma, systemic plasma, and whole-wall samples from throughout the gut were collected on postoperative day 28. Gut Il-22 mRNA expression was determined by real-time quantitative PCR. Plasma Il-22 levels were determined by enzyme-linked immunosorbant assay (ELISA). Results: RYGB and BWM rats had lower food intake and body weight as well as superior blood glucose clearing capability compared with Sham rats. RYGB rats also had superior blood glucose clearing capability compared with BWM rats despite having similar body weights and higher food intake. Il-22 mRNA expression was approximately 100-fold higher specifically in the upper jejunum in RYGB rats compared with Sham rats. Il-22 protein was only detectable in portal vein (34.1 ± 9.4 pg/mL) and systemic (46.9 ± 10.5 pg/mL) plasma in RYGB rats. Area under the curve of blood glucose during the OGTT, but not food intake or body weight, negatively correlated with portal vein and systemic plasma Il-22 levels in RYGB rats. Conclusions: These results suggest that induction of gut Il-22 release might partly account for the weight loss-independent improvements in glycemic control after RYGB, and further support the use of this cytokine for the treatment of metabolic disease.
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spelling doaj.art-652b33a937b54bfa962fac2a7ee4ecef2023-03-18T04:42:38ZengElsevierMetabolism Open2589-93682023-03-0117100212Gastric bypass surgery weight loss-independently induces gut Il-22 release in association with improved glycemic control in obese Zucker fatty ratsFlorian Seyfried0Rebecca Springer1Annett Hoffmann2Maximilian Gruber3Christoph Otto4Nicolas Schlegel5Mohammed K. Hankir6Department of General, Visceral, Vascular and Pediatric Surgery, University Hospital Wuerzburg, Wuerzburg, 97080, GermanyDepartment of General, Visceral, Vascular and Pediatric Surgery, University Hospital Wuerzburg, Wuerzburg, 97080, GermanyDepartment of General, Visceral, Vascular and Pediatric Surgery, University Hospital Wuerzburg, Wuerzburg, 97080, GermanyDepartment of General, Visceral, Vascular and Pediatric Surgery, University Hospital Wuerzburg, Wuerzburg, 97080, GermanyDepartment of General, Visceral, Vascular and Pediatric Surgery, University Hospital Wuerzburg, Wuerzburg, 97080, GermanyDepartment of General, Visceral, Vascular and Pediatric Surgery, University Hospital Wuerzburg, Wuerzburg, 97080, GermanyCorresponding author. Center of Operative Medicine, Oberduerrbacherstrasse 6, 97080, Wuerzburg, Germany.; Department of General, Visceral, Vascular and Pediatric Surgery, University Hospital Wuerzburg, Wuerzburg, 97080, GermanyBackground: Roux-en-Y gastric bypass surgery (RYGB) improves glycemic control in individuals with severe obesity beyond the effects of weight loss alone. To identify potential underlying mechanisms, we asked how equivalent weight loss from RYGB and from chronic caloric restriction impact gut release of the metabolically beneficial cytokine interleukin-22 (Il-22). Methods: Obese male Zucker fatty rats were randomized into sham-operated (Sham), RYGB, and sham-operated, body weight-matched to RYGB (BWM) groups. Food intake and body weight were measured regularly for 4 weeks. An oral glucose tolerance test (OGTT) was performed on postoperative day 27. Portal vein plasma, systemic plasma, and whole-wall samples from throughout the gut were collected on postoperative day 28. Gut Il-22 mRNA expression was determined by real-time quantitative PCR. Plasma Il-22 levels were determined by enzyme-linked immunosorbant assay (ELISA). Results: RYGB and BWM rats had lower food intake and body weight as well as superior blood glucose clearing capability compared with Sham rats. RYGB rats also had superior blood glucose clearing capability compared with BWM rats despite having similar body weights and higher food intake. Il-22 mRNA expression was approximately 100-fold higher specifically in the upper jejunum in RYGB rats compared with Sham rats. Il-22 protein was only detectable in portal vein (34.1 ± 9.4 pg/mL) and systemic (46.9 ± 10.5 pg/mL) plasma in RYGB rats. Area under the curve of blood glucose during the OGTT, but not food intake or body weight, negatively correlated with portal vein and systemic plasma Il-22 levels in RYGB rats. Conclusions: These results suggest that induction of gut Il-22 release might partly account for the weight loss-independent improvements in glycemic control after RYGB, and further support the use of this cytokine for the treatment of metabolic disease.http://www.sciencedirect.com/science/article/pii/S2589936822000500
spellingShingle Florian Seyfried
Rebecca Springer
Annett Hoffmann
Maximilian Gruber
Christoph Otto
Nicolas Schlegel
Mohammed K. Hankir
Gastric bypass surgery weight loss-independently induces gut Il-22 release in association with improved glycemic control in obese Zucker fatty rats
Metabolism Open
title Gastric bypass surgery weight loss-independently induces gut Il-22 release in association with improved glycemic control in obese Zucker fatty rats
title_full Gastric bypass surgery weight loss-independently induces gut Il-22 release in association with improved glycemic control in obese Zucker fatty rats
title_fullStr Gastric bypass surgery weight loss-independently induces gut Il-22 release in association with improved glycemic control in obese Zucker fatty rats
title_full_unstemmed Gastric bypass surgery weight loss-independently induces gut Il-22 release in association with improved glycemic control in obese Zucker fatty rats
title_short Gastric bypass surgery weight loss-independently induces gut Il-22 release in association with improved glycemic control in obese Zucker fatty rats
title_sort gastric bypass surgery weight loss independently induces gut il 22 release in association with improved glycemic control in obese zucker fatty rats
url http://www.sciencedirect.com/science/article/pii/S2589936822000500
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