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....
Main Authors: | , , , , , |
---|---|
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 & 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 & 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 & 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 & 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 & 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 & 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 |