Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-17T18:04:40.319Z Has data issue: false hasContentIssue false

Uptake and metabolism of propionate in the liver isolated from sheep treated with glucagon

Published online by Cambridge University Press:  09 March 2007

Abdulhamid Mohamed Ali
Affiliation:
School of Agriculture, Faculty of Science and Technology, La Trobe University, Bundoora, Victoria, Australia3083
Markandeya Jois
Affiliation:
School of Agriculture, Faculty of Science and Technology, La Trobe University, Bundoora, Victoria, Australia3083
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The uptake and metabolism of propionate in the isolated perfused caudal lobe of the liver and in isolated hepatocytes were examined following treatment of sheep with glucagon or saline. Glucagon or sterile saline was infused at 9·8 µg/min for 3 h into the jugular vein and then the caudal lobe of the liver was removed surgically under anaesthesia. The caudal lobe was used either to prepare hepatocytes or in a non-recirculating perfusion experiment. Uptake and metabolism of propionate were studied using [2-14C]propionate. In studies using the non-recirculation perfusion of the caudal lobe of the sheep liver it was shown that the treatment of sheep with glucagon resulted in an increased rate of gluconeogenesis from propionate and in an increased net uptake of propionate by the caudal lobe. The uptake of propionate into the hepatocytes was saturable, concentrative and exhibited a Km for propionate of 0·24 (SE 0·07) mM and a maximal rate of uptake (Vmax) of 6·7 (SE 0·6) nmol/mg dry cells per min and was unaffected by glucagon treatment of sheep. After incubation of cells in medium containing 0·5 mM-[2-14C]propionate for 10 min, the rate of gluconeogenesis from propionate was 22 % higher in the hepatocytes isolated from glucagon-treated sheep. Concentrations in the medium of 1·35 mM butyrate and 1 mM-caproate inhibited propionate uptake by about 50 % and abolished the glucagon-induced stimulation of gluconeogenesis from propionate. The results are consistent with a regulatory role for glucagon in the gluconeogenesis from propionate in the sheep liver.

Type
Animal Nutrition
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

Adams, A. J. A. & Haynes, R. C. Jr (1969). Control of hepatic mitochondrial CO2 fixation by glucagon, epinephrine, and cortisol. Journal of Biological Chemistry 244, 64446450.CrossRefGoogle Scholar
Aiello, R. J., Armentano, L. E., Bertics, S. J. & Murphy, A. T. (1989). Volatile fatty acid uptake and propionate metabolism in ruminant hepatocytes. Journal of Dairy Science 72, 942949.CrossRefGoogle ScholarPubMed
Bassett, J. M. (1972). Plasma glucagon concentrations in sheep: their regulation and relation to concentration of insulin and growth hormone. Australian Journal of Biological Chemistry 25, 12771287.Google ScholarPubMed
Bergman, E. N. (1990). Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567590.CrossRefGoogle ScholarPubMed
Bergman, E. N., Roe, W. E. & Kon, K. (1966). Quantitative aspects of propionate metabolism and gluconeogenesis in sheep. American Journal of Physiology 211, 793799.CrossRefGoogle ScholarPubMed
Bergman, E. N. & Wolff, J. E. (1971). Metabolism of fatty acids by liver and portal-drained viscera in sheep. American Journal of Physiology 221, 586592.CrossRefGoogle ScholarPubMed
Bergmeyer, H. U. & Bernt, E. (1974). Determination of glucose with glucose oxidase and peroxidase. In Methods of Enzymatic Analysis, vol. 3, pp. 12051215 [Bergmeyer, H. U., editor]. New York: Academic Press.Google Scholar
Brass, E. P., Fennessey, P. V. & Miller, L. V. (1986). Inhibition of oxidative metabolism by propionic acid and its reversal by carnitine in isolated hepatocytes. Biochemical Journal 236, 131136.CrossRefGoogle Scholar
Brockman, R. P. & Bergman, E. N. (1975). Effect of glucagon on plasma alanine and glutamine metabolism and hepatic gluconeogenesis in sheep. American Journal of Physiology 228, 16271633.CrossRefGoogle ScholarPubMed
Brockman, R. P. & Greer, C. (1980). Effects of somatostatin and glucagon on the utilization of [2-14C] propionate in glucose production in vivo in sheep. Australian Journal of Biological Sciences 33, 457464.CrossRefGoogle ScholarPubMed
Chow, J. C. & Jesse, B. W. (1992). Interactions between gluconeogenesis and fatty acid oxidation in isolated sheep hepatocytes. Journal of Dairy Science 75, 21422149.CrossRefGoogle ScholarPubMed
Clark, M. G., Filsell, O. H. & Jarrett, I. G. (1976). Gluconeogenesis in isolated intact lamb liver cells: effects of glucagon and butyrate. Biochemical Journal 156, 671680.CrossRefGoogle ScholarPubMed
Demigné, C., Yacoub, C., Morand, C. & Rémésy, C. (1991). Interactions between propionate and amino acid metabolism in isolated sheep hepatocytes. British Journal of Nutrition 65, 301317.CrossRefGoogle ScholarPubMed
Demigné, C., Yacoub, C., Rémésy, C. & Fafournoux, P. (1986). Propionate and butyrate metabolism in rat or sheep hepatocytes. Biochimica et Biophysica Acta 875, 535542.CrossRefGoogle ScholarPubMed
Donkin, S. S. & Armentano, L. (1995). Insulin and glucagon regulation of gluconeogenesis in preruminating and ruminating bovine. Journal of Animal Science 73, 546551.CrossRefGoogle ScholarPubMed
Fafournoux, P., Rémésy, C. & Demigné, C. (1985). Propionate transport in rat liver cells. Biochimica et Biophysica Acta 818, 7380.CrossRefGoogle ScholarPubMed
Faulkner, A. & Pollock, H. T. (1986). Propionate metabolism and its regulation by fatty acids in ovine hepatocytes. Comparative Biochemistry and Physiology 84B, 559563.Google ScholarPubMed
Faulkner, A. & Pollock, H. T. (1990). Effects of glucagon and α- and β-agonists on glycogenolysis and gluconeogenesis in isolated ovine hepatocytes. Biochimica et Biophysica Acta 1052, 229234.CrossRefGoogle ScholarPubMed
Garrison, J. C., Johnsen, D. E. & Campanile, C. P. (1984). Evidence for the role of phosphorylase kinase, protein kinase C and other Ca2+-sensitive protein kinases in response of hepatocytes to angiotensin II and vasopressin. Journal of Biological Chemistry 259, 32833292.CrossRefGoogle ScholarPubMed
Gill, W., Mitchell, G. E., Boling, J. A., Tucker, R. E., Schelling, G. T. & De Gregorio, R. M. (1985). Glucagon influence on gluconeogenesis and oxidation of propionic acid and threonine by perfused ovine liver. Journal of Dairy Science 68, 28862894.CrossRefGoogle ScholarPubMed
Halestrap, A. P. (1989). The regulation of the matrix volume of mammalian mitochondria in vivo and in vitro and its role in the control of mitochondrial metabolism. Biochimica et Biophysica Acta 973, 355382.CrossRefGoogle ScholarPubMed
Hampson, R. K., Baron, L. L. & Olson, M. S. (1984). Stimulation of the glycine cleavage system by short-chain fatty acids in isolated rat liver mitochondria. Biochemistry 23, 46044610.CrossRefGoogle ScholarPubMed
Jensen, C. B., Sistare, F. D., Hamman, H. C. & Haynes, R. C. Jr (1983). Stimulation of mitochondrial functions by glucagon treatment. Evidence that effects are artifacts of mitochondrial isolation. Biochemical Journal 210, 819827.CrossRefGoogle ScholarPubMed
Jois, M. & Brosnan, J. T. (1993). Hormonal regulation of hepatic glycine metabolism. Australian Journal of Agricultural Research 44, 473478.CrossRefGoogle Scholar
Jois, M., Bunnage, A. P. & Egan, A. R. (1993). Non-recirculating perfusion of caudal lobe sheep liver to study hepatic metabolism of propionate. Proceedings of XV International Congress of Nutrition, Adelaide, p. 114 Abstr.Adelaide:Smith-Gordon.Google Scholar
Jois, M., Hall, B., Fewer, K. & Brosnan, J. T. (1989). Regulation of hepatic glycine catabolism by glucagon. Journal of Biological Chemistry 264, 33473351.CrossRefGoogle ScholarPubMed
Judson, G. J., Anderson, E. E., Luick, J. R. & Leng, R. A. (1968). The contribution of propionate to glucose synthesis in sheep given different diets of different grain contents. British Journal of Nutrition 22, 6974.CrossRefGoogle Scholar
Krebs, H. A., Cornell, N. W., Lund, P. & Hems, R. (1974). Isolated liver cells as an experimental material. In Regulation of Hepatic Metabolism, pp. 726750 [Lundquist, F. and Tygstrup, N., editors]. New York: Academic Press.Google Scholar
Looney, M. C., Baldwin, R. L. & Calvert, C. C. (1987). Gluconeogenesis in isolated lamb hepatocytes. Journal of Animal Science 64, 283294.CrossRefGoogle ScholarPubMed
Pethick, D. W., Lindsay, D. B., Barker, P. J. & Northop, A. J. (1981). Acetate supply and utilization by the tissues of sheep in vivo. British Journal of Nutrition 46, 97110.CrossRefGoogle ScholarPubMed
Ricks, C. A. & Cook, R. M. (1981). Regulation of volatile fatty acid uptake by mitochondrial acylCoA synthases of bovine liver. Journal of Dairy Science 64, 23242335.CrossRefGoogle Scholar
Savan, P. M., Jeacock, M. E. & Shepherd, D. A. L. (1986). Gluconeogenesis in foetal, suckling and weaned lambs: the effects of glucagon. Journal of Agricultural Science, Cambridge 106, 259264.CrossRefGoogle Scholar
Siess, H. (1978). The use of perfusion of liver and other organs for the study of microsomal electron-transport and cytochrome P-450 systems. Methods in Enzymology 52, 4859.CrossRefGoogle Scholar