Oxidation of energy substrates in tissues of largemouth bass (Micropterus salmoides)
This study tested the hypothesis that amino acids are oxidized at higher rates than glucose and palmitate for ATP production in tissues of largemouth bass (LMB, a carnivorous fish). Slices (10 to 50 mg) of liver, proximal intestine, kidney, and skeletal muscle isolated from LMB were incubated at 26 ...
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Published in | Amino acids Vol. 52; no. 6-7; pp. 1017 - 1032 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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Springer Vienna
01.07.2020
Springer Nature B.V |
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Abstract | This study tested the hypothesis that amino acids are oxidized at higher rates than glucose and palmitate for ATP production in tissues of largemouth bass (LMB, a carnivorous fish). Slices (10 to 50 mg) of liver, proximal intestine, kidney, and skeletal muscle isolated from LMB were incubated at 26 °C for 2 h in oxygenated Krebs–Henseleit bicarbonate buffer (pH 7.4, with 5 mM
d
-glucose) containing either
d
-[U-
14
C]glucose, 2 mM
l
-alanine plus
l
-[U-
14
C]alanine, 2 mM
l
-aspartate plus
l
-[U-
14
C]aspartate, 2 mM
l
-glutamate plus
l
-[U-
14
C]glutamate, 2 mM
l
-glutamine plus
l
-[U-
14
C]glutamine, 2 mM
l
-leucine plus
l
-[U-
14
C]leucine, or 2 mM palmitate plus [U-
14
C]palmitate. In parallel experiments, tissues were incubated with a [U-
14
C]-labeled tracer and a mixture of unlabeled substrates [alanine, aspartate, glutamate, glutamine, leucine, and palmitate (2 mM each) plus 5 mM glucose].
14
CO
2
was collected to calculate the rates of substrate oxidation. In separate experiments, O
2
consumption by each tissue was measured in the presence of individual or a mixture of substrates. The activities of key metabolic enzymes were also measured. Results indicated that the liver and skeletal muscle had a limited ability to oxidize glucose and palmitate to CO
2
for ATP production in the presence of individual or a mixture of substrates due to low activities of carnitine palmitoyltransferase-I, hexokinase and pyruvate dehydrogenase. In the presence of individual substrates, each amino acid was actively oxidized by all the tissues. In the presence of a mixture of substrates, glutamine and glutamate were the major metabolic fuels in the proximal intestine and kidney, as glutamine for the liver and aspartate for skeletal muscle. All the tissues had high activities of glutaminase, glutamate dehydrogenase, and transaminases. At the same extracellular concentration of amino acids (2 mM) in a mixture of energy substrates, glutamine was the major metabolic fuel for the liver of the LMB, glutamine and glutamate for the proximal intestine and kidneys, and aspartate for the skeletal muscle. Glutamine plus glutamate plus aspartate generated 60–70% of ATP in LMB tissues. |
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AbstractList | This study tested the hypothesis that amino acids are oxidized at higher rates than glucose and palmitate for ATP production in tissues of largemouth bass (LMB, a carnivorous fish). Slices (10 to 50 mg) of liver, proximal intestine, kidney, and skeletal muscle isolated from LMB were incubated at 26 °C for 2 h in oxygenated Krebs–Henseleit bicarbonate buffer (pH 7.4, with 5 mM d-glucose) containing either d-[U-14C]glucose, 2 mM l-alanine plus l-[U-14C]alanine, 2 mM l-aspartate plus l-[U-14C]aspartate, 2 mM l-glutamate plus l-[U-14C]glutamate, 2 mM l-glutamine plus l-[U-14C]glutamine, 2 mM l-leucine plus l-[U-14C]leucine, or 2 mM palmitate plus [U-14C]palmitate. In parallel experiments, tissues were incubated with a [U-14C]-labeled tracer and a mixture of unlabeled substrates [alanine, aspartate, glutamate, glutamine, leucine, and palmitate (2 mM each) plus 5 mM glucose]. 14CO2 was collected to calculate the rates of substrate oxidation. In separate experiments, O2 consumption by each tissue was measured in the presence of individual or a mixture of substrates. The activities of key metabolic enzymes were also measured. Results indicated that the liver and skeletal muscle had a limited ability to oxidize glucose and palmitate to CO2 for ATP production in the presence of individual or a mixture of substrates due to low activities of carnitine palmitoyltransferase-I, hexokinase and pyruvate dehydrogenase. In the presence of individual substrates, each amino acid was actively oxidized by all the tissues. In the presence of a mixture of substrates, glutamine and glutamate were the major metabolic fuels in the proximal intestine and kidney, as glutamine for the liver and aspartate for skeletal muscle. All the tissues had high activities of glutaminase, glutamate dehydrogenase, and transaminases. At the same extracellular concentration of amino acids (2 mM) in a mixture of energy substrates, glutamine was the major metabolic fuel for the liver of the LMB, glutamine and glutamate for the proximal intestine and kidneys, and aspartate for the skeletal muscle. Glutamine plus glutamate plus aspartate generated 60–70% of ATP in LMB tissues. This study tested the hypothesis that amino acids are oxidized at higher rates than glucose and palmitate for ATP production in tissues of largemouth bass (LMB, a carnivorous fish). Slices (10 to 50 mg) of liver, proximal intestine, kidney, and skeletal muscle isolated from LMB were incubated at 26 °C for 2 h in oxygenated Krebs–Henseleit bicarbonate buffer (pH 7.4, with 5 mM d -glucose) containing either d -[U- 14 C]glucose, 2 mM l -alanine plus l -[U- 14 C]alanine, 2 mM l -aspartate plus l -[U- 14 C]aspartate, 2 mM l -glutamate plus l -[U- 14 C]glutamate, 2 mM l -glutamine plus l -[U- 14 C]glutamine, 2 mM l -leucine plus l -[U- 14 C]leucine, or 2 mM palmitate plus [U- 14 C]palmitate. In parallel experiments, tissues were incubated with a [U- 14 C]-labeled tracer and a mixture of unlabeled substrates [alanine, aspartate, glutamate, glutamine, leucine, and palmitate (2 mM each) plus 5 mM glucose]. 14 CO 2 was collected to calculate the rates of substrate oxidation. In separate experiments, O 2 consumption by each tissue was measured in the presence of individual or a mixture of substrates. The activities of key metabolic enzymes were also measured. Results indicated that the liver and skeletal muscle had a limited ability to oxidize glucose and palmitate to CO 2 for ATP production in the presence of individual or a mixture of substrates due to low activities of carnitine palmitoyltransferase-I, hexokinase and pyruvate dehydrogenase. In the presence of individual substrates, each amino acid was actively oxidized by all the tissues. In the presence of a mixture of substrates, glutamine and glutamate were the major metabolic fuels in the proximal intestine and kidney, as glutamine for the liver and aspartate for skeletal muscle. All the tissues had high activities of glutaminase, glutamate dehydrogenase, and transaminases. At the same extracellular concentration of amino acids (2 mM) in a mixture of energy substrates, glutamine was the major metabolic fuel for the liver of the LMB, glutamine and glutamate for the proximal intestine and kidneys, and aspartate for the skeletal muscle. Glutamine plus glutamate plus aspartate generated 60–70% of ATP in LMB tissues. |
Author | Jia, Sichao Li, Xinyu Zhou, Chuanpeng Wu, Guoyao Shixuan Zheng Song, Fei |
Author_xml | – sequence: 1 givenname: Xinyu surname: Li fullname: Li, Xinyu organization: Department of Animal Science, Texas A&M University – sequence: 2 surname: Shixuan Zheng fullname: Shixuan Zheng organization: Guangdong Yuehai Feeds Group Co., Ltd – sequence: 3 givenname: Sichao surname: Jia fullname: Jia, Sichao organization: Department of Animal Science, Texas A&M University – sequence: 4 givenname: Fei surname: Song fullname: Song, Fei organization: Department of Animal Science, Texas A&M University – sequence: 5 givenname: Chuanpeng surname: Zhou fullname: Zhou, Chuanpeng organization: Department of Animal Science, Texas A&M University – sequence: 6 givenname: Guoyao orcidid: 0000-0001-8058-6969 surname: Wu fullname: Wu, Guoyao email: g-wu@tamu.edu organization: Department of Animal Science, Texas A&M University |
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SubjectTerms | Alanine Amino acids Analytical Chemistry Bass Bicarbonates Biochemical Engineering Biochemistry Biomedical and Life Sciences Carbon dioxide Carnitine Carnitine palmitoyltransferase Dehydrogenases Energy resources Glucose Glutamate dehydrogenase Glutamic acid Glutaminase Glutamine Hexokinase Intestine Kidneys L-Alanine Leucine Life Sciences Liver Metabolism Micropterus salmoides Muscles Musculoskeletal system Neurobiology Original Article Oxidation Oxygen consumption Palmitic acid Palmitoyltransferase Proteomics Pyruvic acid Skeletal muscle Substrates Transaminases |
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Title | Oxidation of energy substrates in tissues of largemouth bass (Micropterus salmoides) |
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