Abstract
We measured the amino acid concentrations in the afferent and efferent vessels of the liver in anaesthetized fed adult rats and in fed suckling rat pups. A much higher content of glutamine in the portal vein and the aorta than in hepatic veins suggests that this amino acid is actively taken up by the liver of fed suckling rat pups, conversely to what is found in adult rats. In an attempt to characterize further the mechanism(s) contributing to this enhanced glutamine uptake, we monitored the time course of 1 mM-glutamine transport into plasma-membrane vesicles purified from the livers of either adult or suckling rats. The concentrative Na+-dependent uptake of glutamine was lower in those vesicles obtained from pups than in those obtained from adult rats. Glutaminase and glutamine synthetase activities in livers from both experimental groups were also measured. Glutaminase and glutamine synthetase activities in suckling rats were about 3-fold higher and 2-fold lower respectively than those in adult rats. It is concluded that glutamine is a main nitrogen carrier to the liver in fed suckling rats. A high availability of this amino acid and an enzyme imbalance between glutamine-synthesizing and -degrading activities may account for the net uptake found in vivo.
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- Aikawa T., Matsutaka H., Yamamoto H., Okuda T., Ishikawa E. Gluconeogenesis and amino acid metabolism. II. Inter-organal relations and roles of glutamine and alanine in the amino acid metabolism of fasted rats. J Biochem. 1973 Nov;74(5):1003–1017. [PubMed] [Google Scholar]
- Arola L., Palou A., Remesar X., Alemany M. Glutamine synthetase activity in the organs of fed and 24-hours fasted rats. Horm Metab Res. 1981 Apr;13(4):199–202. doi: 10.1055/s-2007-1019220. [DOI] [PubMed] [Google Scholar]
- Aronson N. N., Jr, Touster O. Isolation of rat liver plasma membrane fragments in isotonic sucrose. Methods Enzymol. 1974;31:90–102. doi: 10.1016/0076-6879(74)31009-9. [DOI] [PubMed] [Google Scholar]
- Bellemann P. Amino acid transport and rubidium-ion uptake in monolayer cultures of hepatocytes from neonatal rats. Biochem J. 1981 Sep 15;198(3):475–483. doi: 10.1042/bj1980475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bellemann P. Enhanced amino acid transport in cultured hepatocytes during liver development. J Biochem. 1981 Dec;90(6):1821–1824. doi: 10.1093/oxfordjournals.jbchem.a133661. [DOI] [PubMed] [Google Scholar]
- Carroll M. Characterization of proteins structurally related to human N-acetyl-beta-D-glucosaminidase. Biochem J. 1978 Jul 1;173(1):191–196. doi: 10.1042/bj1730191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Casado J., Pastor-Anglada M., Remesar X. Hepatic uptake of amino acids at mid-lactation in the rat. Biochem J. 1987 Jul 1;245(1):297–300. doi: 10.1042/bj2450297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Casado J., Remesar X., Pastor-Anglada M. Hepatic uptake of amino acids in late-pregnant rats. Effect of food deprivation. Biochem J. 1987 Nov 15;248(1):117–122. doi: 10.1042/bj2480117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Conde R. D., Scornik O. A. Faster synthesis and slower degradation of liver protein during developmental growth. Biochem J. 1977 Jul 15;166(1):115–121. doi: 10.1042/bj1660115. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Curthoys N. P., Lowry O. H. The distribution of glutaminase isoenzymes in the various structures of the nephron in normal, acidotic, and alkalotic rat kidney. J Biol Chem. 1973 Jan 10;248(1):162–168. [PubMed] [Google Scholar]
- DE DUVE C., PRESSMAN B. C., GIANETTO R., WATTIAUX R., APPELMANS F. Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J. 1955 Aug;60(4):604–617. doi: 10.1042/bj0600604. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferré P., Decaux J. F., Issad T., Girard J. Changes in energy metabolism during the suckling and weaning period in the newborn. Reprod Nutr Dev. 1986;26(2B):619–631. doi: 10.1051/rnd:19860413. [DOI] [PubMed] [Google Scholar]
- Gaasbeek Janzen J. W., Moorman A. F., Lamers W. H., Charles R. Development of the heterogeneous distribution of carbamoyl-phosphate synthetase (ammonia) in rat-liver parenchyma during postnatal development. J Histochem Cytochem. 1985 Dec;33(12):1205–1211. doi: 10.1177/33.12.4067274. [DOI] [PubMed] [Google Scholar]
- Hager S. E., Jones M. E. A glutamine-dependent enzyme for the synthesis of carbamyl phosphate for pyrimidine biosynthesis in fetal rat liver. J Biol Chem. 1967 Dec 25;242(24):5674–5680. [PubMed] [Google Scholar]
- Hayes M. R., McGivan J. D. Differential effects of starvation on alanine and glutamine transport in isolated rat hepatocytes. Biochem J. 1982 Apr 15;204(1):365–368. doi: 10.1042/bj2040365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herzfeld A., Estes N. A., 3rd The distinction between gamma-glutamylhydroxamate synthetase and L-glutamine-hydroxylamine glutamyltransferase activities in rat tissues. Biochem J. 1973 May;133(1):59–66. doi: 10.1042/bj1330059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Häussinger D. Hepatocyte heterogeneity in glutamine and ammonia metabolism and the role of an intercellular glutamine cycle during ureogenesis in perfused rat liver. Eur J Biochem. 1983 Jun 15;133(2):269–275. doi: 10.1111/j.1432-1033.1983.tb07458.x. [DOI] [PubMed] [Google Scholar]
- Häussinger D., Soboll S., Meijer A. J., Gerok W., Tager J. M., Sies H. Role of plasma membrane transport in hepatic glutamine metabolism. Eur J Biochem. 1985 Nov 4;152(3):597–603. doi: 10.1111/j.1432-1033.1985.tb09237.x. [DOI] [PubMed] [Google Scholar]
- Häussinger D. Structural-functional organization of hepatic glutamine and ammonium metabolism. Biochem Soc Trans. 1987 Jun;15(3):369–372. doi: 10.1042/bst0150369. [DOI] [PubMed] [Google Scholar]
- Issad T., Coupé C., Pastor-Anglada M., Ferré P., Girard J. Development of insulin-sensitivity at weaning in the rat. Role of the nutritional transition. Biochem J. 1988 May 1;251(3):685–690. doi: 10.1042/bj2510685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jacob R., Rosenthal N., Barrett E. J. Characterization of glutamine transport by liver plasma membrane vesicles. Am J Physiol. 1986 Nov;251(5 Pt 1):E509–E514. doi: 10.1152/ajpendo.1986.251.5.E509. [DOI] [PubMed] [Google Scholar]
- Jones C. T., Rolph T. P. Metabolism during fetal life: a functional assessment of metabolic development. Physiol Rev. 1985 Apr;65(2):357–430. doi: 10.1152/physrev.1985.65.2.357. [DOI] [PubMed] [Google Scholar]
- Joseph S. K., McGivan J. D. The effects of ammonium chloride and bicarbonate on the activity of glutaminase in isolated liver mitochondria. Biochem J. 1978 Dec 15;176(3):837–844. doi: 10.1042/bj1760837. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kadowaki H., Bibb P. C., Knox W. E. Capacity of cyclic urea synthesis in neonatal rat liver. Biol Neonate. 1983;44(1):21–27. doi: 10.1159/000241690. [DOI] [PubMed] [Google Scholar]
- Katz J., Golden S., Wals P. A. Glycogen synthesis by rat hepatocytes. Biochem J. 1979 May 15;180(2):389–402. doi: 10.1042/bj1800389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kilberg M. S. Amino acid transport in isolated rat hepatocytes. J Membr Biol. 1982;69(1):1–12. doi: 10.1007/BF01871236. [DOI] [PubMed] [Google Scholar]
- Lavoinne A., Baquet A., Hue L. Stimulation of glycogen synthesis and lipogenesis by glutamine in isolated rat hepatocytes. Biochem J. 1987 Dec 1;248(2):429–437. doi: 10.1042/bj2480429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Linder-Horowitz M. Changes in glutaminase activities of rat liver and kidney during pre- and post-natal development. Biochem J. 1969 Aug;114(1):65–70. doi: 10.1042/bj1140065. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meijer A. J. Channeling of ammonia from glutaminase to carbamoyl-phosphate synthetase in liver mitochondria. FEBS Lett. 1985 Oct 28;191(2):249–251. doi: 10.1016/0014-5793(85)80018-1. [DOI] [PubMed] [Google Scholar]
- Moule S. K., Bradford N. M., McGivan J. D. Short-term stimulation of Na+-dependent amino acid transport by dibutyryl cyclic AMP in hepatocytes. Characteristics and partial mechanism. Biochem J. 1987 Feb 1;241(3):737–743. doi: 10.1042/bj2410737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pastor-Anglada M., Remesar X., Bourdel G. Alanine uptake by liver at midpregnancy in rats. Am J Physiol. 1987 Mar;252(3 Pt 1):E408–E413. doi: 10.1152/ajpendo.1987.252.3.E408. [DOI] [PubMed] [Google Scholar]
- Pausch J., Rasenack J., Häussinger D., Gerok W. Hepatic carbamoyl phosphate metabolism. Role of cytosolic and mitochondrial carbamoyl phosphate in de novo pyrimidine synthesis. Eur J Biochem. 1985 Jul 1;150(1):189–194. doi: 10.1111/j.1432-1033.1985.tb09006.x. [DOI] [PubMed] [Google Scholar]
- Peterson G. L. Review of the Folin phenol protein quantitation method of Lowry, Rosebrough, Farr and Randall. Anal Biochem. 1979 Dec;100(2):201–220. doi: 10.1016/0003-2697(79)90222-7. [DOI] [PubMed] [Google Scholar]
- Remesar X., López-Tejero D., Pastor-Anglada M. Some aspects of amino acid metabolism in the rat fetus. Comp Biochem Physiol B. 1987;88(3):719–725. doi: 10.1016/0305-0491(87)90234-3. [DOI] [PubMed] [Google Scholar]
- Remesy C., Fafournoux P., Demigne C. Control of hepatic utilization of serine, glycine and threonine in fed and starved rats. J Nutr. 1983 Jan;113(1):28–39. doi: 10.1093/jn/113.1.28. [DOI] [PubMed] [Google Scholar]
- Richards T. C., Greengard O. Distribution of glutamine hexosephosphate aminotransferase in rat tissues; changes with state of differentiation. Biochim Biophys Acta. 1973 May 28;304(3):842–850. doi: 10.1016/0304-4165(73)90231-6. [DOI] [PubMed] [Google Scholar]
- Russell S. M., Burgess R. J., Mayer R. J. Protein degradation in rat liver during post-natal development. Biochem J. 1980 Oct 15;192(1):321–330. doi: 10.1042/bj1920321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rémésey C., Demigné C., Aufrère J. Inter-organ relationships between glucose, lactate and amino acids in rats fed on high-carbohydrate or high-protein diets. Biochem J. 1978 Feb 15;170(2):321–329. doi: 10.1042/bj1700321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sips H. J., Van Amelsvoort J. M., Van Dam K. Amino acid transport in plasma-membrane vesicles from rat liver. Characterization of L-alanine transport. Eur J Biochem. 1980 Apr;105(2):217–224. doi: 10.1111/j.1432-1033.1980.tb04492.x. [DOI] [PubMed] [Google Scholar]
- Tremblay G. S., Crandall D. E., Knott C. E., Alfant M. Orotic acid biosynthesis in rat liver: studies on the source of carbamoylphosphate. Arch Biochem Biophys. 1977 Jan 15;178(1):264–277. doi: 10.1016/0003-9861(77)90191-6. [DOI] [PubMed] [Google Scholar]
- Windmueller H. G., Spaeth A. E. Respiratory fuels and nitrogen metabolism in vivo in small intestine of fed rats. Quantitative importance of glutamine, glutamate, and aspartate. J Biol Chem. 1980 Jan 10;255(1):107–112. [PubMed] [Google Scholar]