Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheep

The energy intake of Tibetan sheep on the harsh Qinghai–Tibetan Plateau (QTP) varies greatly with seasonal forage fluctuations and is often below maintenance requirements, especially during the long, cold winter. The liver plays a crucial role in gluconeogenesis and skeletal muscle is the primary ti...

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Main Authors: X.P. Jing, W.J. Wang, A.A. Degen, Y.M. Guo, J.P. Kang, P.P. Liu, L.M. Ding, Z.H. Shang, J.W. Zhou, R.J. Long
Format: Article
Language:English
Published: Elsevier 2021-03-01
Series:Animal
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1751731120301646
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author X.P. Jing
W.J. Wang
A.A. Degen
Y.M. Guo
J.P. Kang
P.P. Liu
L.M. Ding
Z.H. Shang
J.W. Zhou
R.J. Long
author_facet X.P. Jing
W.J. Wang
A.A. Degen
Y.M. Guo
J.P. Kang
P.P. Liu
L.M. Ding
Z.H. Shang
J.W. Zhou
R.J. Long
author_sort X.P. Jing
collection DOAJ
description The energy intake of Tibetan sheep on the harsh Qinghai–Tibetan Plateau (QTP) varies greatly with seasonal forage fluctuations and is often below maintenance requirements, especially during the long, cold winter. The liver plays a crucial role in gluconeogenesis and skeletal muscle is the primary tissue of energy expenditure in mammals. Both play important roles in energy substrate metabolism and regulating energy metabolism homeostasis of the body. This study aimed to gain insight into how skeletal muscle and liver of Tibetan sheep regulate energy substrate metabolism to cope with low energy intake under the harsh environment of the QTP. Tibetan sheep (n = 24; 48.5 ± 1.89 kg BW) were compared with Small-tailed Han sheep (n = 24; 49.2 ± 2.21 kg BW), which were allocated randomly into one of four groups that differed in dietary digestible energy densities: 8.21, 9.33, 10.45 and 11.57 MJ /kg DM. The sheep were slaughtered after a 49-d feeding period, skeletal muscle and liver tissues were collected and measurements were made of the activities of the key enzymes of energy substrate metabolism and the expressions of genes related to energy homeostasis regulation. Compared with Small-tailed Han sheep, Tibetan sheep exhibited higher capacities of propionate to glucose conversion and fatty acid oxidation and ketogenesis in the liver, higher glucose utilization efficiency in both skeletal muscle and liver, but lower activities of fatty acid oxidation and protein mobilization in skeletal muscle, especially when in negative energy balance. However, the Small-tailed Han sheep exhibited higher capacities to convert amino acids and lactate to glucose and higher levels of glycolysis and lipogenesis in the liver than Tibetan sheep. These differences in gluconeogenesis and energy substrate metabolism conferred the Tibetan sheep an advantage over Small-tailed Han sheep to cope with low energy intake and regulate whole-body energy homeostasis under the harsh environment of the QTP.
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spelling doaj.art-eed09dee179b41a1995aeb2629969ca72022-12-21T22:53:15ZengElsevierAnimal1751-73112021-03-01153100162Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheepX.P. Jing0W.J. Wang1A.A. Degen2Y.M. Guo3J.P. Kang4P.P. Liu5L.M. Ding6Z.H. Shang7J.W. Zhou8R.J. Long9State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China; International Centre for Tibetan Plateau Ecosystem Management, School of Life Sciences, Lanzhou University, Lanzhou 730000, China; Laboratory for Animal Nutrition and Animal Product Quality, Department of Animal Sciences and Aquatic Ecology, Faculty of Bioscience Engineering, Ghent University, Ghent 9000, BelgiumInternational Centre for Tibetan Plateau Ecosystem Management, School of Life Sciences, Lanzhou University, Lanzhou 730000, ChinaDesert Animal Adaptations and Husbandry, Wyler Department of Dryland Agriculture, Blaustein Institutes for Desert Research, Ben-Gurion University of Negev, Beer Sheva 8410500, IsraelState Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, ChinaState Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, ChinaInternational Centre for Tibetan Plateau Ecosystem Management, School of Life Sciences, Lanzhou University, Lanzhou 730000, ChinaInternational Centre for Tibetan Plateau Ecosystem Management, School of Life Sciences, Lanzhou University, Lanzhou 730000, ChinaInternational Centre for Tibetan Plateau Ecosystem Management, School of Life Sciences, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China; Corresponding author.International Centre for Tibetan Plateau Ecosystem Management, School of Life Sciences, Lanzhou University, Lanzhou 730000, ChinaThe energy intake of Tibetan sheep on the harsh Qinghai–Tibetan Plateau (QTP) varies greatly with seasonal forage fluctuations and is often below maintenance requirements, especially during the long, cold winter. The liver plays a crucial role in gluconeogenesis and skeletal muscle is the primary tissue of energy expenditure in mammals. Both play important roles in energy substrate metabolism and regulating energy metabolism homeostasis of the body. This study aimed to gain insight into how skeletal muscle and liver of Tibetan sheep regulate energy substrate metabolism to cope with low energy intake under the harsh environment of the QTP. Tibetan sheep (n = 24; 48.5 ± 1.89 kg BW) were compared with Small-tailed Han sheep (n = 24; 49.2 ± 2.21 kg BW), which were allocated randomly into one of four groups that differed in dietary digestible energy densities: 8.21, 9.33, 10.45 and 11.57 MJ /kg DM. The sheep were slaughtered after a 49-d feeding period, skeletal muscle and liver tissues were collected and measurements were made of the activities of the key enzymes of energy substrate metabolism and the expressions of genes related to energy homeostasis regulation. Compared with Small-tailed Han sheep, Tibetan sheep exhibited higher capacities of propionate to glucose conversion and fatty acid oxidation and ketogenesis in the liver, higher glucose utilization efficiency in both skeletal muscle and liver, but lower activities of fatty acid oxidation and protein mobilization in skeletal muscle, especially when in negative energy balance. However, the Small-tailed Han sheep exhibited higher capacities to convert amino acids and lactate to glucose and higher levels of glycolysis and lipogenesis in the liver than Tibetan sheep. These differences in gluconeogenesis and energy substrate metabolism conferred the Tibetan sheep an advantage over Small-tailed Han sheep to cope with low energy intake and regulate whole-body energy homeostasis under the harsh environment of the QTP.http://www.sciencedirect.com/science/article/pii/S1751731120301646Energy homeostasis regulationFatty acids metabolismGlucose metabolismHepatic gluconeogenesisSkeletal muscle morphology
spellingShingle X.P. Jing
W.J. Wang
A.A. Degen
Y.M. Guo
J.P. Kang
P.P. Liu
L.M. Ding
Z.H. Shang
J.W. Zhou
R.J. Long
Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheep
Animal
Energy homeostasis regulation
Fatty acids metabolism
Glucose metabolism
Hepatic gluconeogenesis
Skeletal muscle morphology
title Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheep
title_full Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheep
title_fullStr Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheep
title_full_unstemmed Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheep
title_short Energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels: comparison between Tibetan and Small-tailed Han sheep
title_sort energy substrate metabolism in skeletal muscle and liver when consuming diets of different energy levels comparison between tibetan and small tailed han sheep
topic Energy homeostasis regulation
Fatty acids metabolism
Glucose metabolism
Hepatic gluconeogenesis
Skeletal muscle morphology
url http://www.sciencedirect.com/science/article/pii/S1751731120301646
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