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Oxidation of amino acids, glucose, and fatty acids as metabolic fuels in enterocytes of developing pigs

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Abstract

Enterocytes of young pigs are known to use glutamine, glutamate, and glucose as major metabolic fuels. However, little is known about the roles of aspartate, alanine, and fatty acids as energy sources for these cells. Therefore, this study simultaneously determined the oxidation of the amino acids and glucose as well as short- and long-chain fatty acids in enterocytes of developing pigs. Jejunal enterocytes were isolated from 0-, 7-, 14- and 21-day-old piglets, and incubated at 37 °C for 30 min in Krebs–Henseleit bicarbonate buffer (pH 7.4) containing 5 mM d-glucose and one of the following: d-[U-14C]glucose, 0.5–5 mM l-[U-14C]glutamate, 0.5–5 mM l-[U-14C]glutamine, 0.5–5 mM l-[U-14C]aspartate, 0.5–5 mM l-[U-14C]alanine, 0.5–2 mM l-[U-14C]palmitate, 0.5–5 mM [U-14C]propionate, and 0.5–5 mM [1-14C]butyrate. At the end of the incubation, 14CO2 produced from each 14C-labeled substrate was collected. Rates of oxidation of each substrate by enterocytes from all age groups of piglets increased (P < 0.05) gradually with increasing its extracellular concentrations. The rates of oxidation of glutamate, glutamine, aspartate, and glucose by enterocytes from 0- to 21-day-old pigs and of alanine from newborn pigs were much greater (P < 0.05) than those for the same concentrations of palmitate, propionate, and butyrate. Compared with 0-day-old pigs, the rates of oxidation of glutamate, aspartate, glutamine, alanine, and glucose by enterocytes from 21-day-old pigs decreased (P < 0.05) markedly, without changes in palmitate oxidation. Oxidation of alanine, propionate, butyrate and palmitate by enterocytes of pigs was limited during their postnatal growth. At each postnatal age, the oxidation of glutamate, glutamine, aspartate, and glucose produced much more ATP than alanine, propionate, butyrate and palmitate. The degradation of glutamate was initiated primarily by glutamate-pyruvate and glutamate-oxaloacetate transaminases. Our results indicated that amino acids (glutamate plus glutamine plus aspartate) are the major metabolic fuels in enterocytes of 0- to 21-day-old pigs.

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Abbreviations

CPT-1:

Carnitine palmitoyltransferase-1

GDH:

Glutamate dehydrogenase

GOT:

Glutamate–oxaloacetate transaminase

GPT:

Glutamate-pyruvate transaminase

KHB:

Krebs–Henseleit bicarbonate

PFK:

Phosphofructokinase

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Acknowledgements

This work was supported by Texas A&M AgriLife Research (H-8200). We thank Dr. Gayan Nawaratna for helpful technical assistance. He et al. (2019) presented the findings from the current study at the 2019 Annual Meeting of the American Society of Animal Science.

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Correspondence to Guoyao Wu.

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He, W., Wu, G. Oxidation of amino acids, glucose, and fatty acids as metabolic fuels in enterocytes of developing pigs. Amino Acids 54, 1025–1039 (2022). https://doi.org/10.1007/s00726-022-03151-7

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