Overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp (Cyprinus carpio L.) fed a high-starch diet

Growth hormone (GH) is important for regulating insulin secretion and carbohydrate metabolism, and its role in mammalian models of diabetes is relatively worked out. Although some fish species were used as models for diabetes research, the effects of GH on insulin and glucose catabolism and anabolis...

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Main Authors: Yunya Wu, Rui Li, Xingxing Wu, Wei Guo, Wenrong Zhong, Yongming Li, Yanlong Song, Binbin Tao, Ji Chen, Dong Han, Shouqi Xie, Yaping Wang, Zuoyan Zhu, Wei Hu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Endocrinology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fendo.2022.1038479/full
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author Yunya Wu
Yunya Wu
Rui Li
Xingxing Wu
Xingxing Wu
Wei Guo
Wei Guo
Wenrong Zhong
Yongming Li
Yanlong Song
Binbin Tao
Ji Chen
Dong Han
Shouqi Xie
Yaping Wang
Zuoyan Zhu
Wei Hu
Wei Hu
Wei Hu
author_facet Yunya Wu
Yunya Wu
Rui Li
Xingxing Wu
Xingxing Wu
Wei Guo
Wei Guo
Wenrong Zhong
Yongming Li
Yanlong Song
Binbin Tao
Ji Chen
Dong Han
Shouqi Xie
Yaping Wang
Zuoyan Zhu
Wei Hu
Wei Hu
Wei Hu
author_sort Yunya Wu
collection DOAJ
description Growth hormone (GH) is important for regulating insulin secretion and carbohydrate metabolism, and its role in mammalian models of diabetes is relatively worked out. Although some fish species were used as models for diabetes research, the effects of GH on insulin and glucose catabolism and anabolism in these models remain to be clarified. In this study, we investigated the effect of GH on insulin and glucose catabolism and anabolism in an omnivorous fish using GH transgenic (T) common carp that consistently overexpressed GH and wild-type (WT) common carp. We compared the intestinal morphology, and digestive and absorptive capacity of fish fed commercial feed. We also analyzed the growth performance, insulin level, glucose catabolism and anabolism, lipid deposition, and lipid catabolism and anabolism in T carp and WT carp fed diets containing either 30% or 40% starch. In the intestine of T carp, α-amylase activity was enhanced, the number of goblet cells and intestinal villi surface area was increased, and the expression level of glucose transport protein-related genes (glut2 and sglt1) was upregulated when compared to these indicators in WT carp. When fed either a normal or high-starch diet, the growth performance of T carp was better than that of WT carp. Compared with WT carp, serum insulin was increased and glucose was decreased, hepatic expression level of igf-1 and glycolysis-related genes was increased, and the activity level of a hepatic enzyme related to glycolysis was enhanced in T carp. When fed with a high-starch diet, the serum alanine aminotransferase activity, hepatic lipid content, and malondialdehyde content were significantly lower in T carp than in WT carp. These results indicated that overexpression of GH (1) enhanced carbohydrate digestion and absorption in the carp intestine, (2) did not induce insulin resistance and improved glucose catabolism and utilization in carp, and (3) relieved liver lipid deposition. Our data might provide new insights into potential ways to improve glucose utilization in fish and diabetes treatments.
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spelling doaj.art-ee266ceb25cb4a10b9e03091825208d02022-12-22T04:39:59ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922022-12-011310.3389/fendo.2022.10384791038479Overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp (Cyprinus carpio L.) fed a high-starch dietYunya Wu0Yunya Wu1Rui Li2Xingxing Wu3Xingxing Wu4Wei Guo5Wei Guo6Wenrong Zhong7Yongming Li8Yanlong Song9Binbin Tao10Ji Chen11Dong Han12Shouqi Xie13Yaping Wang14Zuoyan Zhu15Wei Hu16Wei Hu17Wei Hu18State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaSchool of Basic Medical Science, Wuhan University, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaQingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaGrowth hormone (GH) is important for regulating insulin secretion and carbohydrate metabolism, and its role in mammalian models of diabetes is relatively worked out. Although some fish species were used as models for diabetes research, the effects of GH on insulin and glucose catabolism and anabolism in these models remain to be clarified. In this study, we investigated the effect of GH on insulin and glucose catabolism and anabolism in an omnivorous fish using GH transgenic (T) common carp that consistently overexpressed GH and wild-type (WT) common carp. We compared the intestinal morphology, and digestive and absorptive capacity of fish fed commercial feed. We also analyzed the growth performance, insulin level, glucose catabolism and anabolism, lipid deposition, and lipid catabolism and anabolism in T carp and WT carp fed diets containing either 30% or 40% starch. In the intestine of T carp, α-amylase activity was enhanced, the number of goblet cells and intestinal villi surface area was increased, and the expression level of glucose transport protein-related genes (glut2 and sglt1) was upregulated when compared to these indicators in WT carp. When fed either a normal or high-starch diet, the growth performance of T carp was better than that of WT carp. Compared with WT carp, serum insulin was increased and glucose was decreased, hepatic expression level of igf-1 and glycolysis-related genes was increased, and the activity level of a hepatic enzyme related to glycolysis was enhanced in T carp. When fed with a high-starch diet, the serum alanine aminotransferase activity, hepatic lipid content, and malondialdehyde content were significantly lower in T carp than in WT carp. These results indicated that overexpression of GH (1) enhanced carbohydrate digestion and absorption in the carp intestine, (2) did not induce insulin resistance and improved glucose catabolism and utilization in carp, and (3) relieved liver lipid deposition. Our data might provide new insights into potential ways to improve glucose utilization in fish and diabetes treatments.https://www.frontiersin.org/articles/10.3389/fendo.2022.1038479/fullgrowth hormone overexpressioninsulin sensitivityglucose utilizationliver lipid depositioncommon carp (Cyprinus carpio L.)
spellingShingle Yunya Wu
Yunya Wu
Rui Li
Xingxing Wu
Xingxing Wu
Wei Guo
Wei Guo
Wenrong Zhong
Yongming Li
Yanlong Song
Binbin Tao
Ji Chen
Dong Han
Shouqi Xie
Yaping Wang
Zuoyan Zhu
Wei Hu
Wei Hu
Wei Hu
Overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp (Cyprinus carpio L.) fed a high-starch diet
Frontiers in Endocrinology
growth hormone overexpression
insulin sensitivity
glucose utilization
liver lipid deposition
common carp (Cyprinus carpio L.)
title Overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp (Cyprinus carpio L.) fed a high-starch diet
title_full Overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp (Cyprinus carpio L.) fed a high-starch diet
title_fullStr Overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp (Cyprinus carpio L.) fed a high-starch diet
title_full_unstemmed Overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp (Cyprinus carpio L.) fed a high-starch diet
title_short Overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp (Cyprinus carpio L.) fed a high-starch diet
title_sort overexpression of growth hormone improved hepatic glucose catabolism and relieved liver lipid deposition in common carp cyprinus carpio l fed a high starch diet
topic growth hormone overexpression
insulin sensitivity
glucose utilization
liver lipid deposition
common carp (Cyprinus carpio L.)
url https://www.frontiersin.org/articles/10.3389/fendo.2022.1038479/full
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