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. 1995 Sep;96(3):1375–1381. doi: 10.1172/JCI118172

Study of the rat adrenal renin-angiotensin system at a cellular level.

C Y Chiou 1, G H Williams 1, I Kifor 1
PMCID: PMC185759  PMID: 7657812

Abstract

To address the question as to how zona glomerulosa (ZG) cell angiotensin II (Ang II) secretion is regulated, we developed an immuno-cell blot assay to measure its secretion from single cells. We compared these results with those obtained from population studies using a superfusion system. Modulation of Ang II secretion was investigated acutely (by administrating potassium [K+] or captopril) and chronically (by feeding the animals low or high sodium diets). The area of secretory cells, halo areas, and halo intensities varied widely but were highly significantly correlated (P < 0.001) with each other. A disproportionate amount of Ang II was secreted by a small number of large cells. When K+ concentration was increased from 3.6 to 0 mM, superfused ZG cells increased their Ang II secretion 2.32 +/- 0.59-fold. Administration of captopril reduced the K(+)-stimulated Ang II secretion 1.24 +/- 0.07 fold. These findings were reflected in the cell blot assay as a change in the frequency distribution of halo area by K+ and captopril in the same direction as in the population study. In both conditions, the percentage of secretory cells did not change significantly from control. Superfused ZG cells from rats on a low sodium diet secreted 1.85 +/- 0.58-fold more Ang II than cells from sodium-loaded rats (p < 0.05, n = 6). The cell blot assay confirmed these findings with sodium restriction significantly increasing (P < 0.001) both the halo area and its frequency distribution to a larger portion of high secreting cells. However, in contrast to acute treatment with K+ or captopril, the number of secretory cells also doubled. Thus, the individual ZG cell uses two mechanisms to modify Ang II production. In response to acute stimulation and suppression, the amount of Ang II secreted per cell is modified without changing the number of secretary cells. With chronic stimulation, both the amount of Ang II secreted per cell and the number of secretary cells increase.

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Selected References

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  1. Bennett M. K., Wandinger-Ness A., Simons K. Release of putative exocytic transport vesicles from perforated MDCK cells. EMBO J. 1988 Dec 20;7(13):4075–4085. doi: 10.1002/j.1460-2075.1988.tb03301.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bianchi C., Gutkowska J., De Léan A., Ballak M., Anand-Srivastava M. B., Genest J., Cantin M. Fate of [125I]angiotensin II in adrenal zona glomerulosa cells. Endocrinology. 1986 Jun;118(6):2605–2607. doi: 10.1210/endo-118-6-2605. [DOI] [PubMed] [Google Scholar]
  3. Campbell D. J., Habener J. F. Angiotensinogen gene is expressed and differentially regulated in multiple tissues of the rat. J Clin Invest. 1986 Jul;78(1):31–39. doi: 10.1172/JCI112566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chiou C. Y., Kifor I., Moore T. J., Williams G. H. The effect of losartan on potassium-stimulated aldosterone secretion in vitro. Endocrinology. 1994 Jun;134(6):2371–2375. doi: 10.1210/endo.134.6.8194463. [DOI] [PubMed] [Google Scholar]
  5. Doi Y., Atarashi K., Franco-Saenz R., Mulrow P. Adrenal renin: a possible regulator of aldosterone production. Clin Exp Hypertens A. 1983;5(7-8):1119–1126. doi: 10.3109/10641968309048845. [DOI] [PubMed] [Google Scholar]
  6. Ganten D., Hermann K., Unger T., Lang R. E. The tissue renin-angiotensin systems: focus on brain angiotensin, adrenal gland and arterial wall. Clin Exp Hypertens A. 1983;5(7-8):1099–1118. doi: 10.3109/10641968309048844. [DOI] [PubMed] [Google Scholar]
  7. Hackenthal E., Paul M., Ganten D., Taugner R. Morphology, physiology, and molecular biology of renin secretion. Physiol Rev. 1990 Oct;70(4):1067–1116. doi: 10.1152/physrev.1990.70.4.1067. [DOI] [PubMed] [Google Scholar]
  8. Haning R., Tait S. A., Tait J. F. In vitro effects of ACTH, angiotensins, serotonin and potassium on steroid output and conversion of corticosterone to aldosterone by isolated adrenal cells. Endocrinology. 1970 Dec;87(6):1147–1167. doi: 10.1210/endo-87-6-1147. [DOI] [PubMed] [Google Scholar]
  9. Hunt M. K., Ramos S. P., Geary K. M., Norling L. L., Peach M. J., Gomez R. A., Carey R. M. Colocalization and release of angiotensin and renin in renal cortical cells. Am J Physiol. 1992 Sep;263(3 Pt 2):F363–F373. doi: 10.1152/ajprenal.1992.263.3.F363. [DOI] [PubMed] [Google Scholar]
  10. Husain A., DeSilva P., Speth R. C., Bumpus F. M. Regulation of angiotensin II in rat adrenal gland. Circ Res. 1987 May;60(5):640–648. doi: 10.1161/01.res.60.5.640. [DOI] [PubMed] [Google Scholar]
  11. Inagami T., Mizuno K., Naruse M., Nakamaru M., Naruse K., Hoffman L. H., McKenzie J. C. Active and inactive renin in the adrenal. Am J Hypertens. 1989 Apr;2(4):311–319. doi: 10.1093/ajh/2.4.311. [DOI] [PubMed] [Google Scholar]
  12. Kendall M. E., Hymer W. C. Cell blotting: a new approach to quantify hormone secretion from individual rat pituitary cells. Endocrinology. 1987 Dec;121(6):2260–2262. doi: 10.1210/endo-121-6-2260. [DOI] [PubMed] [Google Scholar]
  13. Kifor I., Moore T. J., Fallo F., Sperling E., Chiou C. Y., Menachery A., Williams G. H. Potassium-stimulated angiotensin release from superfused adrenal capsules and enzymatically dispersed cells of the zona glomerulosa. Endocrinology. 1991 Aug;129(2):823–831. doi: 10.1210/endo-129-2-823. [DOI] [PubMed] [Google Scholar]
  14. Kifor I., Moore T. J., Fallo F., Sperling E., Menachery A., Chiou C. Y., Williams G. H. The effect of sodium intake on angiotensin content of the rat adrenal gland. Endocrinology. 1991 Mar;128(3):1277–1284. doi: 10.1210/endo-128-3-1277. [DOI] [PubMed] [Google Scholar]
  15. Knight D. E., Baker P. F. Calcium-dependence of catecholamine release from bovine adrenal medullary cells after exposure to intense electric fields. J Membr Biol. 1982;68(2):107–140. doi: 10.1007/BF01872259. [DOI] [PubMed] [Google Scholar]
  16. Kurtz A., Scholz H., della Bruna R. Molecular mechanisms of renin release. J Cardiovasc Pharmacol. 1990;16 (Suppl 4):S1–S7. doi: 10.1097/00005344-199016004-00002. [DOI] [PubMed] [Google Scholar]
  17. Mendelsohn F. A. Angiotensin II is concentrated or locally produced in rat adrenal gland. Clin Exp Pharmacol Physiol Suppl. 1982;7:3–7. [PubMed] [Google Scholar]
  18. Oetting M., LeBoff M. S., Levy S., Swiston L., Preston J., Chen C., Brown E. M. Permeabilization reveals classical stimulus-secretion coupling in bovine parathyroid cells. Endocrinology. 1987 Oct;121(4):1571–1576. doi: 10.1210/endo-121-4-1571. [DOI] [PubMed] [Google Scholar]
  19. Peters J., Münter K., Bader M., Hackenthal E., Mullins J. J., Ganten D. Increased adrenal renin in transgenic hypertensive rats, TGR(mREN2)27, and its regulation by cAMP, angiotensin II, and calcium. J Clin Invest. 1993 Mar;91(3):742–747. doi: 10.1172/JCI116292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Racz K., Pinet F., Gasc J. M., Guyene T. T., Corvol P. Coexpression of renin, angiotensinogen, and their messenger ribonucleic acids in adrenal tissues. J Clin Endocrinol Metab. 1992 Sep;75(3):730–737. doi: 10.1210/jcem.75.3.1381371. [DOI] [PubMed] [Google Scholar]

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