Maternal intake restriction programs the energy metabolism, clock circadian regulator and mTOR signals in the skeletal muscles of goat offspring probably via the protein kinase A-cAMP-responsive element-binding proteins pathway

The biological mechanism by which maternal undernutrition increases the metabolic disorder risk of skeletal muscles in offspring is not fully understood. We hypothesize that maternal intake restriction influences metabolic signals in the skeletal muscles of offspring via a glucagon-mediated pathway....

Full description

Bibliographic Details
Main Authors: Xiaoling Zhou, Qiongxian Yan, Hong Yang, Ao Ren, Zhixiong He, Zhiliang Tan
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2021-12-01
Series:Animal Nutrition
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405654521001712
_version_ 1818871864601083904
author Xiaoling Zhou
Qiongxian Yan
Hong Yang
Ao Ren
Zhixiong He
Zhiliang Tan
author_facet Xiaoling Zhou
Qiongxian Yan
Hong Yang
Ao Ren
Zhixiong He
Zhiliang Tan
author_sort Xiaoling Zhou
collection DOAJ
description The biological mechanism by which maternal undernutrition increases the metabolic disorder risk of skeletal muscles in offspring is not fully understood. We hypothesize that maternal intake restriction influences metabolic signals in the skeletal muscles of offspring via a glucagon-mediated pathway. Twenty-four pregnant goats were assigned to the control group (100% of the nutrients requirement, n = 12) and restricted group (60% of the control feed allowance from pregnant days 45 to 100, n = 12). Blood and Longissimus thoracis muscle were sampled from dams (100 d of gestation), fetuses (100 d of gestation), and kids (90 d after birth) in each group. The data were analyzed using the linear MIXED model, with the multiple comparison method of SIDAK applied. Intake restriction reduced (P < 0.05) the total blood protein of dams and fetuses. Maternal restriction decreased (P < 0.05) the cAMP-responsive element-binding protein 1 (CREB1), CREB-binding protein (CREBBP), protein kinase A (PKA), aryl hydrocarbon receptor nuclear translocator-like protein 1 (BMAL1), protein kinase B (AKT1), mammalian target of rapamycin (mTOR), and regulatory-associated protein of mTOR (RPTOR) mRNA expression in the fetuses, and reduced (P < 0.05) the CREBBP, nuclear receptor subfamily 1 group H member 3 (NR1H3), D-box binding PAR bZIP transcription factor (DBP) and PKA mRNA levels in the kids, but increased (P < 0.05) the peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC1A) and tuberous sclerosis 2 (TSC2) mRNA levels in the fetuses. The mRNA expression of clock circadian regulator (CLOCK) and TSC2 genes was increased (P < 0.05) in the restricted kids. The protein expression of total PKA and phosphorylated PKA in the restricted fetuses and kids were downregulated (P < 0.05), and the protein expression of total mTOR and phosphorylated mTOR were reduced (P < 0.05) in the restricted fetuses and kids. Maternal intake restriction regulated fat oxidation, protein synthesis, and circadian clock expression in the muscles of the offspring probably via the glucagon-mediated PKA-CREB pathway, which reveals a noteworthy molecular pathway that maternal undernutrition leads to metabolic adaptation of skeletal muscle in offspring.
first_indexed 2024-12-19T12:29:42Z
format Article
id doaj.art-a3ca931192fe4b41b8bb1eefadd45da1
institution Directory Open Access Journal
issn 2405-6545
language English
last_indexed 2024-12-19T12:29:42Z
publishDate 2021-12-01
publisher KeAi Communications Co., Ltd.
record_format Article
series Animal Nutrition
spelling doaj.art-a3ca931192fe4b41b8bb1eefadd45da12022-12-21T20:21:27ZengKeAi Communications Co., Ltd.Animal Nutrition2405-65452021-12-017413031314Maternal intake restriction programs the energy metabolism, clock circadian regulator and mTOR signals in the skeletal muscles of goat offspring probably via the protein kinase A-cAMP-responsive element-binding proteins pathwayXiaoling Zhou0Qiongxian Yan1Hong Yang2Ao Ren3Zhixiong He4Zhiliang Tan5CAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutrition &amp; Physiology and Metabolism, South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China; University of the Chinese Academy of Science, Beijing, 100049, China; College of Animal Science, Tarim University, Alaer, 843300, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutrition &amp; Physiology and Metabolism, South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China; Hunan Co-Innovation Center for Utilization of Botanical Functional Ingredients, Changsha, 410128, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutrition &amp; Physiology and Metabolism, South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutrition &amp; Physiology and Metabolism, South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutrition &amp; Physiology and Metabolism, South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutrition &amp; Physiology and Metabolism, South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China; Corresponding author.The biological mechanism by which maternal undernutrition increases the metabolic disorder risk of skeletal muscles in offspring is not fully understood. We hypothesize that maternal intake restriction influences metabolic signals in the skeletal muscles of offspring via a glucagon-mediated pathway. Twenty-four pregnant goats were assigned to the control group (100% of the nutrients requirement, n = 12) and restricted group (60% of the control feed allowance from pregnant days 45 to 100, n = 12). Blood and Longissimus thoracis muscle were sampled from dams (100 d of gestation), fetuses (100 d of gestation), and kids (90 d after birth) in each group. The data were analyzed using the linear MIXED model, with the multiple comparison method of SIDAK applied. Intake restriction reduced (P < 0.05) the total blood protein of dams and fetuses. Maternal restriction decreased (P < 0.05) the cAMP-responsive element-binding protein 1 (CREB1), CREB-binding protein (CREBBP), protein kinase A (PKA), aryl hydrocarbon receptor nuclear translocator-like protein 1 (BMAL1), protein kinase B (AKT1), mammalian target of rapamycin (mTOR), and regulatory-associated protein of mTOR (RPTOR) mRNA expression in the fetuses, and reduced (P < 0.05) the CREBBP, nuclear receptor subfamily 1 group H member 3 (NR1H3), D-box binding PAR bZIP transcription factor (DBP) and PKA mRNA levels in the kids, but increased (P < 0.05) the peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC1A) and tuberous sclerosis 2 (TSC2) mRNA levels in the fetuses. The mRNA expression of clock circadian regulator (CLOCK) and TSC2 genes was increased (P < 0.05) in the restricted kids. The protein expression of total PKA and phosphorylated PKA in the restricted fetuses and kids were downregulated (P < 0.05), and the protein expression of total mTOR and phosphorylated mTOR were reduced (P < 0.05) in the restricted fetuses and kids. Maternal intake restriction regulated fat oxidation, protein synthesis, and circadian clock expression in the muscles of the offspring probably via the glucagon-mediated PKA-CREB pathway, which reveals a noteworthy molecular pathway that maternal undernutrition leads to metabolic adaptation of skeletal muscle in offspring.http://www.sciencedirect.com/science/article/pii/S2405654521001712Maternal effectSkeletal muscleFat oxidationProtein synthesisCircadian clockGoat
spellingShingle Xiaoling Zhou
Qiongxian Yan
Hong Yang
Ao Ren
Zhixiong He
Zhiliang Tan
Maternal intake restriction programs the energy metabolism, clock circadian regulator and mTOR signals in the skeletal muscles of goat offspring probably via the protein kinase A-cAMP-responsive element-binding proteins pathway
Animal Nutrition
Maternal effect
Skeletal muscle
Fat oxidation
Protein synthesis
Circadian clock
Goat
title Maternal intake restriction programs the energy metabolism, clock circadian regulator and mTOR signals in the skeletal muscles of goat offspring probably via the protein kinase A-cAMP-responsive element-binding proteins pathway
title_full Maternal intake restriction programs the energy metabolism, clock circadian regulator and mTOR signals in the skeletal muscles of goat offspring probably via the protein kinase A-cAMP-responsive element-binding proteins pathway
title_fullStr Maternal intake restriction programs the energy metabolism, clock circadian regulator and mTOR signals in the skeletal muscles of goat offspring probably via the protein kinase A-cAMP-responsive element-binding proteins pathway
title_full_unstemmed Maternal intake restriction programs the energy metabolism, clock circadian regulator and mTOR signals in the skeletal muscles of goat offspring probably via the protein kinase A-cAMP-responsive element-binding proteins pathway
title_short Maternal intake restriction programs the energy metabolism, clock circadian regulator and mTOR signals in the skeletal muscles of goat offspring probably via the protein kinase A-cAMP-responsive element-binding proteins pathway
title_sort maternal intake restriction programs the energy metabolism clock circadian regulator and mtor signals in the skeletal muscles of goat offspring probably via the protein kinase a camp responsive element binding proteins pathway
topic Maternal effect
Skeletal muscle
Fat oxidation
Protein synthesis
Circadian clock
Goat
url http://www.sciencedirect.com/science/article/pii/S2405654521001712
work_keys_str_mv AT xiaolingzhou maternalintakerestrictionprogramstheenergymetabolismclockcircadianregulatorandmtorsignalsintheskeletalmusclesofgoatoffspringprobablyviatheproteinkinaseacampresponsiveelementbindingproteinspathway
AT qiongxianyan maternalintakerestrictionprogramstheenergymetabolismclockcircadianregulatorandmtorsignalsintheskeletalmusclesofgoatoffspringprobablyviatheproteinkinaseacampresponsiveelementbindingproteinspathway
AT hongyang maternalintakerestrictionprogramstheenergymetabolismclockcircadianregulatorandmtorsignalsintheskeletalmusclesofgoatoffspringprobablyviatheproteinkinaseacampresponsiveelementbindingproteinspathway
AT aoren maternalintakerestrictionprogramstheenergymetabolismclockcircadianregulatorandmtorsignalsintheskeletalmusclesofgoatoffspringprobablyviatheproteinkinaseacampresponsiveelementbindingproteinspathway
AT zhixionghe maternalintakerestrictionprogramstheenergymetabolismclockcircadianregulatorandmtorsignalsintheskeletalmusclesofgoatoffspringprobablyviatheproteinkinaseacampresponsiveelementbindingproteinspathway
AT zhiliangtan maternalintakerestrictionprogramstheenergymetabolismclockcircadianregulatorandmtorsignalsintheskeletalmusclesofgoatoffspringprobablyviatheproteinkinaseacampresponsiveelementbindingproteinspathway