Maternal undernutrition during pregnancy alters amino acid metabolism and gene expression associated with energy metabolism and angiogenesis in fetal calf muscle

Susumu Muroya, Yi Zhang, Aoi Kinoshita, Kounosuke Otomaru, Kazunaga Oshima, Yuji Gotoh, Ichiro Oshima, Mitsue Sano, Sanggun Roh, Mika Oe, Koichi Ojima, Takafumi Gotoh

Research output: Contribution to journalArticlepeer-review

Abstract

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 tran-scriptomics. 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, 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 glu-tamate, 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.

Original languageEnglish
Article number582
JournalMetabolites
Volume11
Issue number9
DOIs
Publication statusPublished - 2021 Sep

Keywords

  • Amino acid
  • Angiogenesis
  • Energy metabolism
  • Fetal growth re-striction
  • Fetal programming
  • Maternal nutrient restriction
  • Skeletal muscle

ASJC Scopus subject areas

  • Endocrinology, Diabetes and Metabolism
  • Biochemistry
  • Molecular Biology

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