Cargando…

Maternal Undernutrition during Pregnancy Alters Amino Acid Metabolism and Gene Expression Associated with Energy Metabolism and Angiogenesis in Fetal Calf Muscle

To elucidate the mechanisms underlying maternal undernutrition (MUN)-induced fetal skeletal muscle growth impairment in cattle, the longissimus thoracis muscle of Japanese Black fetal calves at 8.5 months in utero was analyzed by an integrative approach with metabolomics and transcriptomics. The pre...

Descripción completa

Detalles Bibliográficos
Autores principales: Muroya, Susumu, Zhang, Yi, Kinoshita, Aoi, Otomaru, Kounosuke, Oshima, Kazunaga, Gotoh, Yuji, Oshima, Ichiro, Sano, Mitsue, Roh, Sanggun, Oe, Mika, Ojima, Koichi, Gotoh, Takafumi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8465837/
https://www.ncbi.nlm.nih.gov/pubmed/34564398
http://dx.doi.org/10.3390/metabo11090582
_version_ 1784572978229411840
author Muroya, Susumu
Zhang, Yi
Kinoshita, Aoi
Otomaru, Kounosuke
Oshima, Kazunaga
Gotoh, Yuji
Oshima, Ichiro
Sano, Mitsue
Roh, Sanggun
Oe, Mika
Ojima, Koichi
Gotoh, Takafumi
author_facet Muroya, Susumu
Zhang, Yi
Kinoshita, Aoi
Otomaru, Kounosuke
Oshima, Kazunaga
Gotoh, Yuji
Oshima, Ichiro
Sano, Mitsue
Roh, Sanggun
Oe, Mika
Ojima, Koichi
Gotoh, Takafumi
author_sort Muroya, Susumu
collection PubMed
description To elucidate the mechanisms underlying maternal undernutrition (MUN)-induced fetal skeletal muscle growth impairment in cattle, the longissimus thoracis muscle of Japanese Black fetal calves at 8.5 months in utero was analyzed by an integrative approach with metabolomics and transcriptomics. The pregnant cows were fed on 60% (low-nutrition, LN) or 120% (high-nutrition, HN) of their overall nutritional requirement during gestation. MUN markedly decreased the bodyweight and muscle weight of the fetus. The levels of amino acids (AAs) and arginine-related metabolites including glutamine, gamma-aminobutyric acid (GABA), and putrescine were higher in the LN group than those in the HN group. Metabolite set enrichment analysis revealed that the highly different metabolites were associated with the metabolic pathways of pyrimidine, glutathione, and AAs such as arginine and glutamate, suggesting that MUN resulted in AA accumulation rather than protein accumulation. The mRNA expression levels of energy metabolism-associated genes, such as PRKAA1, ANGPTL4, APLNR, CPT1B, NOS2, NOS3, UCP2, and glycolytic genes were lower in the LN group than in the HN group. The gene ontology/pathway analysis revealed that the downregulated genes in the LN group were associated with glucose metabolism, angiogenesis, HIF-1 signaling, PI3K-Akt signaling, pentose phosphate, and insulin signaling pathways. Thus, MUN altered the levels of AAs and expression of genes associated with energy expenditure, glucose homeostasis, and angiogenesis in the fetal muscle.
format Online
Article
Text
id pubmed-8465837
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-84658372021-09-27 Maternal Undernutrition during Pregnancy Alters Amino Acid Metabolism and Gene Expression Associated with Energy Metabolism and Angiogenesis in Fetal Calf Muscle Muroya, Susumu Zhang, Yi Kinoshita, Aoi Otomaru, Kounosuke Oshima, Kazunaga Gotoh, Yuji Oshima, Ichiro Sano, Mitsue Roh, Sanggun Oe, Mika Ojima, Koichi Gotoh, Takafumi Metabolites Article To elucidate the mechanisms underlying maternal undernutrition (MUN)-induced fetal skeletal muscle growth impairment in cattle, the longissimus thoracis muscle of Japanese Black fetal calves at 8.5 months in utero was analyzed by an integrative approach with metabolomics and transcriptomics. The pregnant cows were fed on 60% (low-nutrition, LN) or 120% (high-nutrition, HN) of their overall nutritional requirement during gestation. MUN markedly decreased the bodyweight and muscle weight of the fetus. The levels of amino acids (AAs) and arginine-related metabolites including glutamine, gamma-aminobutyric acid (GABA), and putrescine were higher in the LN group than those in the HN group. Metabolite set enrichment analysis revealed that the highly different metabolites were associated with the metabolic pathways of pyrimidine, glutathione, and AAs such as arginine and glutamate, suggesting that MUN resulted in AA accumulation rather than protein accumulation. The mRNA expression levels of energy metabolism-associated genes, such as PRKAA1, ANGPTL4, APLNR, CPT1B, NOS2, NOS3, UCP2, and glycolytic genes were lower in the LN group than in the HN group. The gene ontology/pathway analysis revealed that the downregulated genes in the LN group were associated with glucose metabolism, angiogenesis, HIF-1 signaling, PI3K-Akt signaling, pentose phosphate, and insulin signaling pathways. Thus, MUN altered the levels of AAs and expression of genes associated with energy expenditure, glucose homeostasis, and angiogenesis in the fetal muscle. MDPI 2021-08-28 /pmc/articles/PMC8465837/ /pubmed/34564398 http://dx.doi.org/10.3390/metabo11090582 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Muroya, Susumu
Zhang, Yi
Kinoshita, Aoi
Otomaru, Kounosuke
Oshima, Kazunaga
Gotoh, Yuji
Oshima, Ichiro
Sano, Mitsue
Roh, Sanggun
Oe, Mika
Ojima, Koichi
Gotoh, Takafumi
Maternal Undernutrition during Pregnancy Alters Amino Acid Metabolism and Gene Expression Associated with Energy Metabolism and Angiogenesis in Fetal Calf Muscle
title Maternal Undernutrition during Pregnancy Alters Amino Acid Metabolism and Gene Expression Associated with Energy Metabolism and Angiogenesis in Fetal Calf Muscle
title_full Maternal Undernutrition during Pregnancy Alters Amino Acid Metabolism and Gene Expression Associated with Energy Metabolism and Angiogenesis in Fetal Calf Muscle
title_fullStr Maternal Undernutrition during Pregnancy Alters Amino Acid Metabolism and Gene Expression Associated with Energy Metabolism and Angiogenesis in Fetal Calf Muscle
title_full_unstemmed Maternal Undernutrition during Pregnancy Alters Amino Acid Metabolism and Gene Expression Associated with Energy Metabolism and Angiogenesis in Fetal Calf Muscle
title_short Maternal Undernutrition during Pregnancy Alters Amino Acid Metabolism and Gene Expression Associated with Energy Metabolism and Angiogenesis in Fetal Calf Muscle
title_sort maternal undernutrition during pregnancy alters amino acid metabolism and gene expression associated with energy metabolism and angiogenesis in fetal calf muscle
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8465837/
https://www.ncbi.nlm.nih.gov/pubmed/34564398
http://dx.doi.org/10.3390/metabo11090582
work_keys_str_mv AT muroyasusumu maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT zhangyi maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT kinoshitaaoi maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT otomarukounosuke maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT oshimakazunaga maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT gotohyuji maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT oshimaichiro maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT sanomitsue maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT rohsanggun maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT oemika maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT ojimakoichi maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle
AT gotohtakafumi maternalundernutritionduringpregnancyaltersaminoacidmetabolismandgeneexpressionassociatedwithenergymetabolismandangiogenesisinfetalcalfmuscle