Oxidation of amino acids, glucose, and fatty acids as metabolic fuels in enterocytes of post-hatching developing chickens

Because chicken enterocytes do not take up glutamate from the arterial blood, our results support the notion that dietary glutamate is essential for the integrity and function of the chicken small intestine. This finding also has important implications for developing new nutritional strategies to improve the small-intestinal and whole-body growth and health of post-hatching chickens. This study determined the oxidation of amino acids, glucose and fatty acid in enterocytes of developing chickens. Jejunal enterocytes were isolated from 0-, 7-, 21-, and 42-d-old broiler chickens, and incubated at 40 degrees C for 30 min in Krebs-Henseleit bicarbonate buffer (pH 7.4) containing 5 mM D-glucose and one of the following: 0.5-5 mM L-[U-C-14]glutamate, 0.5-5 mM L-[U-C-14]glutamine, 0.5-5 mM L-[U-C-14]aspartate, 0.5-5 mM L-[U-C-14]alanine, 0.5-2 mM [U-C-14]palmitate, D-[U-C-14]glucose, 0.5-5 mM [U-C-14]propionate, and 0.5-5 mM [1-C-14]butyrate. (CO2)-C-14 produced from each C-14-labeled substrate was collected for determination of radioactivity. Among all the substrates studied, glutamate had the greatest rate of oxidation in enterocytes from 0- to 42-d-old chickens. Glutamate transaminases, rather than glutamate dehydrogenase, may be primarily responsible for initiating glutamate degradation. Rates of amino acid and fatty acid oxidation by cells increased (P < 0.05) with increasing their extracellular concentrations from 0.5 to 5 mM. Rates of glutamate and glucose oxidation in enterocytes decreased (P < 0.05) with increasing age, and rates of glutamine, aspartate, propionate, and butyrate oxidation were lower (P < 0.05) in 42-d-old chickens than in 0-d-old chickens. By contrast, oxidation of palmitate at 2 mM increased (P < 0.05) by 118% in cells from 42-d-old chickens, compared with 0-d-old chickens. Compared with glutamate, oxidation of glutamine, aspartate, alanine, propionate, butyrate, and palmitate was limited in cells from all age groups of chickens. Collectively, these results indicate that glutamate is the major metabolic fuel in enterocytes of 0- to 42-d-old chickens. Lay Summary Glucose and fatty acids have long been regarded as the primary sources of energy for the absorptive epithelial cells (enterocytes) of the avian small intestine. However, little is known about the use of amino acids for ATP production in these cells. Based on studies with mammalian enterocytes, we hypothesize that aspartate, glutamate, and glutamine provide the bulk of energy for the enterocytes of post-hatching developing chickens. To test this hypothesis, we isolated jejunal enterocytes from 0-, 7-, 21-, and 42-d-old male broiler chickens and performed metabolic studies. Our results indicated that: (1) glutamate (an amino acid) was the major energy source for the enterocytes of post-hatching chickens, (2) the biological oxidation of other amino acids (glutamine, aspartate, and alanine) was limited in chicken enterocytes, (3) glucose was the second most important metabolic fuel in chicken enterocytes, and (4) chicken enterocytes had a limited ability to degrade fatty acids but oxidized more long-chain fatty acids than short-chain fatty acids. We conclude that glutamate is the major source of energy in the enterocytes of post-hatching developing chickens.

Automated summary

This study found that chicken enterocytes do not uptake glutamate from arterial blood, confirming the importance of dietary glutamate for the chicken small intestine. These findings have implications for improving the growth and health of post-hatching chickens and developing new nutritional strategies.