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. 1986 Mar;83(5):1513–1517. doi: 10.1073/pnas.83.5.1513

Permissive effect of dexamethasone on the increase of proenkephalin mRNA induced by depolarization of chromaffin cells.

J R Naranjo, I Mocchetti, J P Schwartz, E Costa
PMCID: PMC323107  PMID: 2869487

Abstract

In cultured bovine chromaffin cells, changes in the dynamic state of enkephalin stores elicited experimentally were studied by measuring cellular proenkephalin mRNA, as well as enkephalin precursors and authentic enkephalin content of cells and culture media. In parallel, tyrosine hydroxylase mRNA and catecholamine cell content were also determined. Low concentrations (0.5-100 pM) of dexamethasone increased the cell contents of proenkephalin mRNA and enkephalin-containing peptides. High concentrations of the hormone (1 microM) were required to increase the cell contents of tyrosine hydroxylase mRNA and catecholamines. Depolarization of the cells with 10 microM veratridine resulted in a depletion of enkephalin and catecholamine stores after 24 hr. The enkephalin, but not the catecholamine, content was restored by 48 hr. An increase in proenkephalin mRNA content might account for the recovery; this increase was curtailed by tetrodotoxin and enhanced by 10 pM dexamethasone. Tyrosine hydroxylase mRNA content was not significantly modified by depolarization, even in the presence of 1 microM dexamethasone. Aldosterone, progesterone, testosterone, or estradiol (1 microM) failed to change proenkephalin mRNA. Hence, dexamethasone appears to exert a specific permissive action on the stimulation of the proenkephalin gene elicited by depolarization. Though the catecholamines and enkephalins are localized in the same chromaffin granules and are coreleased by depolarization, the genes coding for the processes that are rate limiting in the production of these neuromodulators can be differentially regulated.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bohn M. C., Kessler J. A., Golightly L., Black I. B. Appearance of enkephalin-immunoreactivity in rat adrenal medulla following treatment with nicotinic antagonists or reserpine. Cell Tissue Res. 1983;231(3):469–479. doi: 10.1007/BF00218106. [DOI] [PubMed] [Google Scholar]
  2. Eiden L. E., Giraud P., Affolter H. U., Herbert E., Hotchkiss A. J. Alternative modes of enkephalin biosynthesis regulation by reserpine and cyclic AMP in cultured chromaffin cells. Proc Natl Acad Sci U S A. 1984 Jul;81(13):3949–3953. doi: 10.1073/pnas.81.13.3949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Eiden L. E., Giraud P., Dave J. R., Hotchkiss A. J., Affolter H. U. Nicotinic receptor stimulation activates enkephalin release and biosynthesis in adrenal chromaffin cells. Nature. 1984 Dec 13;312(5995):661–663. doi: 10.1038/312661a0. [DOI] [PubMed] [Google Scholar]
  4. Glaser T., Hübner K., Hamprecht B. Glucocorticoids elevate the level of enkephalin-like peptides in neuroblastoma x glioma hybrid cells. FEBS Lett. 1981 Aug 17;131(1):63–67. doi: 10.1016/0014-5793(81)80888-5. [DOI] [PubMed] [Google Scholar]
  5. Hexum T. D., Yang H. Y., Costa E. Biochemical characterization of enkephalin-like immunoreactive peptides of adrenal glands. Life Sci. 1980 Sep 29;27(13):1211–1216. doi: 10.1016/0024-3205(80)90474-9. [DOI] [PubMed] [Google Scholar]
  6. Kumakura K., Guidotti A., Costa E. Primary cultures of chromaffin cells: molecular mechanisms for the induction of tyrosine hydroxylase mediated by 8-Br-cyclic AMP. Mol Pharmacol. 1979 Nov;16(3):865–876. [PubMed] [Google Scholar]
  7. Lewis E. J., Tank A. W., Weiner N., Chikaraishi D. M. Regulation of tyrosine hydroxylase mRNA by glucocorticoid and cyclic AMP in a rat pheochromocytoma cell line. Isolation of a cDNA clone for tyrosine hydroxylase mRNA. J Biol Chem. 1983 Dec 10;258(23):14632–14637. [PubMed] [Google Scholar]
  8. Lewis R. V., Stern A. S. Biosynthesis of the enkephalins and enkephalin-containing polypeptides. Annu Rev Pharmacol Toxicol. 1983;23:353–372. doi: 10.1146/annurev.pa.23.040183.002033. [DOI] [PubMed] [Google Scholar]
  9. Livett B. G., Day R., Elde R. P., Howe P. R. Co-storage of enkephalins and adrenaline in the bovine adrenal medulla. Neuroscience. 1982 May;7(5):1323–1332. doi: 10.1016/0306-4522(82)91138-1. [DOI] [PubMed] [Google Scholar]
  10. Livett B. G., Dean D. M., Whelan L. G., Udenfriend S., Rossier J. Co-release of enkephalin and catecholamines from cultured adrenal chromaffin cells. Nature. 1981 Jan 22;289(5795):317–319. doi: 10.1038/289317a0. [DOI] [PubMed] [Google Scholar]
  11. Mecham R. P., Morris S. L., Levy B. D., Wrenn D. S. Glucocorticoids stimulate elastin production in differentiated bovine ligament fibroblasts but do not induce elastin synthesis in undifferentiated cells. J Biol Chem. 1984 Oct 25;259(20):12414–12418. [PubMed] [Google Scholar]
  12. Milner R. J., Sutcliffe J. G. Gene expression in rat brain. Nucleic Acids Res. 1983 Aug 25;11(16):5497–5520. doi: 10.1093/nar/11.16.5497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mocchetti I., Giorgi O., Schwartz J. P., Costa E. A reduction of the tone of 5-hydroxytryptamine neurons decreases utilization rates of striatal and hypothalamic enkephalins. Eur J Pharmacol. 1984 Nov 13;106(2):427–430. doi: 10.1016/0014-2999(84)90734-9. [DOI] [PubMed] [Google Scholar]
  14. Mulvihill E. R., LePennec J. P., Chambon P. Chicken oviduct progesterone receptor: location of specific regions of high-affinity binding in cloned DNA fragments of hormone-responsive genes. Cell. 1982 Mar;28(3):621–632. doi: 10.1016/0092-8674(82)90217-3. [DOI] [PubMed] [Google Scholar]
  15. Nawata H., Yanase T., Higuchi K., Kato K., Ibayashi H. Epinephrine and norepinephrine syntheses are regulated by a glucocorticoid receptor-mediated mechanism in the bovine adrenal medulla. Life Sci. 1985 May 20;36(20):1957–1966. doi: 10.1016/0024-3205(85)90445-x. [DOI] [PubMed] [Google Scholar]
  16. Nyborg J. K., Nguyen A. P., Spindler S. R. Relationship between thyroid and glucocorticoid hormone receptor occupancy, growth hormone gene transcription, and mRNA accumulation. J Biol Chem. 1984 Oct 25;259(20):12377–12381. [PubMed] [Google Scholar]
  17. Payvar F., Wrange O., Carlstedt-Duke J., Okret S., Gustafsson J. A., Yamamoto K. R. Purified glucocorticoid receptors bind selectively in vitro to a cloned DNA fragment whose transcription is regulated by glucocorticoids in vivo. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6628–6632. doi: 10.1073/pnas.78.11.6628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Quach T. T., Tang F., Kageyama H., Mocchetti I., Guidotti A., Meek J. L., Costa E., Schwartz J. P. Enkephalin biosynthesis in adrenal medulla. Modulation of proenkephalin mRNA content of cultured chromaffin cells by 8-bromo-adenosine 3',5'-monophosphate. Mol Pharmacol. 1984 Sep;26(2):255–260. [PubMed] [Google Scholar]
  19. Saiani L., Guidotti A. Opiate receptor-mediated inhibition of catecholamine release in primary cultures of bovine adrenal chromaffin cells. J Neurochem. 1982 Dec;39(6):1669–1676. doi: 10.1111/j.1471-4159.1982.tb08001.x. [DOI] [PubMed] [Google Scholar]
  20. Schultzberg M., Lundberg J. M., Hökfelt T., Terenius L., Brandt J., Elde R. P., Goldstein M. Enkephalin-like immunoreactivity in gland cells and nerve terminals of the adrenal medulla. Neuroscience. 1978;3(12):1169–1186. doi: 10.1016/0306-4522(78)90137-9. [DOI] [PubMed] [Google Scholar]
  21. Udenfriend S., Kilpatrick D. L. Biochemistry of the enkephalins and enkephalin-containing peptides. Arch Biochem Biophys. 1983 Mar;221(2):309–323. doi: 10.1016/0003-9861(83)90149-2. [DOI] [PubMed] [Google Scholar]
  22. Viveros O. H., Diliberto E. J., Jr, Hazum E., Chang K. J. Opiate-like materials in the adrenal medulla: evidence for storage and secretion with catecholamines. Mol Pharmacol. 1979 Nov;16(3):1101–1108. [PubMed] [Google Scholar]
  23. Wilson S. P., Kirshner N. Effects of ascorbic acid, dexamethasone, and insulin on the catecholamine and opioid peptide stores of cultured adrenal medullary chromaffin cells. J Neurosci. 1983 Oct;3(10):1971–1978. doi: 10.1523/JNEUROSCI.03-10-01971.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wilson S. P., Unsworth C. D., Viveros O. H. Regulation of opioid peptide synthesis and processing in adrenal chromaffin cells by catecholamines and cyclic adenosine 3':5'-monophosphate. J Neurosci. 1984 Dec;4(12):2993–3001. doi: 10.1523/JNEUROSCI.04-12-02993.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yanase T., Nawata H., Higuchi K., Kato K., Ibayashi H. Dexamethasone increases both catecholamines and methionine-enkephalin in cultured bovine adrenal chromaffin cells and human extramedullary pheochromocytoma cells. Life Sci. 1984 Oct 29;35(18):1869–1875. doi: 10.1016/0024-3205(84)90538-1. [DOI] [PubMed] [Google Scholar]

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