Glucagon Stimulation of Ruthenium Red-insensitive Calcium Ion Transport in Developing Rat Liver

Overview

Journal Biochem J

Specialty Biochemistry

Date 1981 Feb 15

PMID 6171260

Citations 10

Authors

P H Reinhart

F L. Bygrave

Affiliations

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Abstract

The maturation of glucagon-stimulated Ruthenium Red-insensitive Ca2+-transport activity was determined in livers of rats ranging in age from 5 days preterm to 10 weeks of adult life. Previous indications are that this activity is confined to vesicles derived mainly from the endoplasmic reticulum. Perinatal-rat liver contains near-adult values of Ruthenium Red-insensitive Ca2+-transport activity, and exhibits large transient increases in the rate of this activity at two stages of development, immediately after birth, and at 2-5 days after birth. The administration of glucagon to foetal rats, at developmental stages after 19.5 days of gestation (2.5 days before birth), results in a large stable increase (greater than 100%) of Ca2+-transport activity in a subsequently isolated 'heavy' microsomal fraction. That this fraction was enriched in vesicles derived from the rough endoplasmic reticulum was indicated by both an electron-microscopic examination and a marker-enzyme analysis of the subcellular fractions. The administration of glucagon into newborn animals only hours old does not enhance further the initial rate of Ca2+-transport activity, and from day 1 to 10 weeks after birth the administration of the hormone results in the moderate enhancement of Ca2+ transport. Experiments with cyclic AMP and inhibitors of phosphodiesterase activity suggest that cyclic AMP plays a key role in the enhancement by glucagon of Ruthenium Red-insensitive Ca2+ transport, and arguments are presented that this transport system has an important metabolic role in the redistribution of intracellular Ca2+ in liver tissue.

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References

Hughes B, Barritt G . Effects of glucagon and N6O2'-dibutyryladenosine 3':5'-cyclic monophosphate on calcium transport in isolated rat liver mitochondria. Biochem J. 1978; 176(1):295-304. PMC: 1186228. DOI: 10.1042/bj1760295. View

Bygrave F, Tranter C . The subcellular location, maturation and response to increased plasma glucagon of ruthenium red-insensitive calcium-ion transport in rat liver. Biochem J. 1978; 174(3):1021-30. PMC: 1186008. DOI: 10.1042/bj1741021. View

Walsh D, Clippinger M, Sivaramakrishnan S, McCullough T . Cyclic adenosine monophosphate dependent and independent phosphorylation of sarcolemma membrane proteins in perfused rat heart. Biochemistry. 1979; 18(5):871-7. DOI: 10.1021/bi00572a021. View

SANDS H, Mascali J . Effects of cyclic AMP and of protein kinase on the calcium uptake by various tracheal smooth muscle organelles. Arch Int Pharmacodyn Ther. 1978; 236(2):180-91. View

Prpic V, Spencer T, Bygrave F . Stable enhancement of calcium retention in mitochondria isolated from rat liver after the administration of glucagon to the intact animal. Biochem J. 1978; 176(3):705-14. PMC: 1186292. DOI: 10.1042/bj1760705. View

Blackmore P, Dehaye J, EXTON J . Studies on alpha-adrenergic activation of hepatic glucose output. The role of mitochondrial calcium release in alpha-adrenergic activation of phosphorylase in perfused rat liver. J Biol Chem. 1979; 254(15):6945-50. View

Taylor W, Bygrave F, Blackmore P, EXTON J . Stable enhancement of ruthenium red-insensitive calcium transport in an endoplasmic reticulum-rich fraction following the exposure of isolated rat liver cells to glucagon. FEBS Lett. 1979; 104(1):31-4. DOI: 10.1016/0014-5793(79)81079-0. View

Rylatt D, Embi N, Cohen P . The role of calmodulin in regulation of glycogen metabolism. Biochem Soc Trans. 1979; 7(4):622-4. DOI: 10.1042/bst0070622. View

Bashan N, Gross Y, Moses S, Gutman A . Rat liver glycogen metabolism in the perinatal period. Biochim Biophys Acta. 1979; 587(2):145-54. DOI: 10.1016/0304-4165(79)90349-0. View

10.

Le Peuch C, Haiech J, Demaille J . Concerted regulation of cardiac sarcoplasmic reticulum calcium transport by cyclic adenosine monophosphate dependent and calcium--calmodulin-dependent phosphorylations. Biochemistry. 1979; 18(23):5150-7. DOI: 10.1021/bi00590a019. View

11.

Taylor W, Reinhart P, Hunt N, Bygrave F . Role of 3',5'-cyclic AMP in glucagon-induced stimulation of ruthenium red-insensitive calcium transport in an endoplasmic reticulum-rich fraction of rat liver. FEBS Lett. 1980; 112(1):92-6. DOI: 10.1016/0014-5793(80)80136-0. View

12.

Lam A, Hummel L, Friedmann N . Characterization of the hormone-sensitive Ca2+ uptake activity of the hepatic endoplasmic reticulum. Biochim Biophys Acta. 1980; 630(2):165-75. DOI: 10.1016/0304-4165(80)90418-3. View

13.

Prpic V, Bygrave F . On the inter-relationship between glucagon action, the oxidation-reduction state of pyridine nucleotides, and calcium retention by rat liver mitochondria. J Biol Chem. 1980; 255(13):6193-9. View

14.

Taylor W, Prpic V, EXTON J, Bygrave F . Stable changes to calcium fluxes in mitochondria isolated from rat livers perfused with alpha-adrenergic agonists and with glucagon. Biochem J. 1980; 188(2):443-50. PMC: 1161887. DOI: 10.1042/bj1880443. View

15.

Greengard O, Dewey H . The premature deposition or lysis of glycogen in livers of fetal rats injected with hydrocortisone or glucagon. Dev Biol. 1970; 21(3):452-61. DOI: 10.1016/0012-1606(70)90135-1. View

16.

Moore C . Specific inhibition of mitochondrial Ca++ transport by ruthenium red. Biochem Biophys Res Commun. 1971; 42(2):298-305. DOI: 10.1016/0006-291x(71)90102-1. View

17.

Butcher F, Scott D, POTTER V . Effect of glucagon on the level of adenosine 3',5'-monophosphate in rat liver: dependence on the route of administration. Endocrinology. 1971; 89(1):130-4. DOI: 10.1210/endo-89-1-130. View

18.

Christoffersen T, Morland J, Osnes J, Oye I . Development of cyclic AMP metabolism in rat liver. A correlative study of tissue levels of cyclic AMP, accumulation of cyclic AMP in slices, adenylate cyclase activity and cyclic nucleotide phosphodiesterase activity. Biochim Biophys Acta. 1973; 313(2):338-49. DOI: 10.1016/0304-4165(73)90033-0. View

19.

Pollak J . Changes in rat liver mitochondria and endoplasmic reticulum during development and differentiation. Enzyme. 1973; 15(1):139-60. View

20.

Girard J, Kervran A, Soufflet E, Assan R . Factors affecting the secretion of insulin and glucagon by the rat fetus. Diabetes. 1974; 23(4):310-7. DOI: 10.2337/diab.23.4.310. View