Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1991 May;436:237–256. doi: 10.1113/jphysiol.1991.sp018548

Chemiosmotic control of renin release from isolated renin granules of rat kidneys.

D H Sigmon 1, J C Fray 1
PMCID: PMC1181503  PMID: 2061832

Abstract

1. Renin-containing granules were isolated, characterized, and used to gain insight into a possible chemiosmotic mechanism of renin secretion. 2. Renin granules were obtained by a modification of the sucrose gradient method, which yielded a 67-fold purification of renin granules as assessed by marker enzymes, or a modification of the Percoll gradient, which yielded a 230-fold enrichment of renin granules. 3. Granular renin content was increased by chronic sodium deprivation and hypophysectomy. 4. Renin release from granules was inversely related to osmotic strength (150-900 mosmol l-1). pH had a biphasic effect on renin release, with greater stimulation at both acidic (pH 5) and alkaline (pH 8 and 9) pH. The pH effect was dependent on Cl-; raising Cl- stimulated release. This effect was abolished by-oligomycin and N,N'-dicyclohexylcarbodiimide (DCCD) at pH 5, but not at pH 8; the effect was enhanced by NH4+. 5. Either valinomycin or carbonyl cyanide m-chlorophenylhydrazone (CCCP) alone was without effect; but in combination they caused a potent stimulation at all pHs. Nigericin stimulated renin release at all pHs, but its effect required K+. 6. Raising K+ stimulated renin release from granules, whereas raising Na+ was without effect. Lowering Ca2+ below 10(-6) M significantly stimulated renin release. 7. Taken together, the evidence is consistent with the chemiosmotic hypothesis for the control of renin release from granules and may have some implications for the regulation of renin secretion from juxtaglomerular cells.

Full text

PDF
237

Selected References

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

  1. AMADOR E., ZIMMERMAN T. S., WACKER W. E. URINARY ALKALINE PHOSPHATASE ACTIVITY. I. ELEVATED URINARY LDH AND ALKALINE PHOSPHATASE ACTIVITIES FOR THE DIAGNOSIS OF RENAL ADENOCARCINOMAS. JAMA. 1963 Sep 7;185:769–775. doi: 10.1001/jama.1963.03060100049016. [DOI] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  3. Chiappelli F., Vasil A., Haggerty D. F. The protein concentration of crude cell and tissue extracts as estimated by the method of dye binding: comparison with the Lowry method. Anal Biochem. 1979 Apr 1;94(1):160–165. doi: 10.1016/0003-2697(79)90805-4. [DOI] [PubMed] [Google Scholar]
  4. Cidon S., Ben-David H., Nelson N. ATP-driven proton fluxes across membranes of secretory organelles. J Biol Chem. 1983 Oct 10;258(19):11684–11688. [PubMed] [Google Scholar]
  5. Finkelstein A., Zimmerberg J., Cohen F. S. Osmotic swelling of vesicles: its role in the fusion of vesicles with planar phospholipid bilayer membranes and its possible role in exocytosis. Annu Rev Physiol. 1986;48:163–174. doi: 10.1146/annurev.ph.48.030186.001115. [DOI] [PubMed] [Google Scholar]
  6. Fray J. C., Lush D. J., Share D. S., Valentine A. N. Possible role of calmodulin in renin secretion from isolated rat kidneys and renal cells: studies with trifluoperazine. J Physiol. 1983 Oct;343:447–454. doi: 10.1113/jphysiol.1983.sp014903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fray J. C. Mechanism of increased renin release during sodium deprivation. Am J Physiol. 1978 May;234(5):F376–F380. doi: 10.1152/ajprenal.1978.234.5.F376. [DOI] [PubMed] [Google Scholar]
  8. Fray J. C., Park C. S., Valentine A. N. Calcium and the control of renin secretion. Endocr Rev. 1987 Feb;8(1):53–93. doi: 10.1210/edrv-8-1-53. [DOI] [PubMed] [Google Scholar]
  9. Fray J. C., Russo S. M. Mechanism for low renin in blacks: studies in hypophysectomised rat model. J Hum Hypertens. 1990 Apr;4(2):160–162. [PubMed] [Google Scholar]
  10. Fray J. C. Stretch receptor model for renin release with evidence from perfused rat kidney. Am J Physiol. 1976 Sep;231(3):936–944. doi: 10.1152/ajplegacy.1976.231.3.936. [DOI] [PubMed] [Google Scholar]
  11. Frederiksen O., Leyssac P. P., Skinner S. L. Sensitive osmometer function of juxtaglomerular cells in vitro. J Physiol. 1975 Nov;252(3):669–679. doi: 10.1113/jphysiol.1975.sp011164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Funakawa S., Higashio T., Yamamoto K. Renin release from renin granules in the dog. Clin Sci Mol Med. 1978 Jul;55(1):11–14. doi: 10.1042/cs0550011. [DOI] [PubMed] [Google Scholar]
  13. Geisow M. J., Burgoyne R. D. Cation-dependent lysis of chromaffin granules - an alternative hypothesis fro osmotically-driven exocytosis. Cell Biol Int Rep. 1982 Apr;6(4):353–359. doi: 10.1016/0309-1651(82)90037-6. [DOI] [PubMed] [Google Scholar]
  14. Grinstein S., Vander Meulen J., Furuya W. Possible role of H+--alkali cation countertransport in secretory granule swelling during exocytosis. FEBS Lett. 1982 Nov 1;148(1):1–4. [PubMed] [Google Scholar]
  15. Honeyman T. W., Goodman H. M., Fray J. C. The effects of growth hormone on blood pressure and renin secretion in hypophysectomized rats. Endocrinology. 1983 May;112(5):1613–1617. doi: 10.1210/endo-112-5-1613. [DOI] [PubMed] [Google Scholar]
  16. Hruban Z., Slesers A., Hopkins E. Drug-induced and naturally occurring myeloid bodies. Lab Invest. 1972 Jul;27(1):62–70. [PubMed] [Google Scholar]
  17. Hutton J. C., Peshavaria M. Proton-translocating Mg2+-dependent ATPase activity in insulin-secretory granules. Biochem J. 1982 Apr 15;204(1):161–170. doi: 10.1042/bj2040161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Johnson R. G., Scarpa A. Ion permeability of isolated chromaffin granules. J Gen Physiol. 1976 Dec;68(6):601–631. doi: 10.1085/jgp.68.6.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kawamura M., McKenzie J. C., Hoffman L. H., Tanaka I., Parmentier M., Inagami T. The storage form of renin in renin granules from rat kidney cortex. Hypertension. 1986 Aug;8(8):706–711. doi: 10.1161/01.hyp.8.8.706. [DOI] [PubMed] [Google Scholar]
  20. LOWRY O. H., ROBERTS N. R., WU M. L., HIXON W. S., CRAWFORD E. J. The quantitative histochemistry of brain. II. Enzyme measurements. J Biol Chem. 1954 Mar;207(1):19–37. [PubMed] [Google Scholar]
  21. Lorenson M. Y., Jacobs L. S. Inhibitor studies with adenohypophyseal granule membrane ATPase. Evidence for a membrane environment which modulates sensitivity to inhibitors. Biochim Biophys Acta. 1984 Jan 25;769(2):479–485. doi: 10.1016/0005-2736(84)90333-x. [DOI] [PubMed] [Google Scholar]
  22. Lüllmann-Rauch B. Lipidosislike renal changes in rats treated with chlorphentermine or with tricyclic antidepressants. Virchows Arch B Cell Pathol. 1975;18(1):51–60. doi: 10.1007/BF02889233. [DOI] [PubMed] [Google Scholar]
  23. Morimoto S., Abe R., Fukuhara A., Tanaka K., Yamamoto K. Effect of sodium restriction on plasma renin activity and renin granules in rat kidney. Am J Physiol. 1979 Nov;237(5):F367–F371. doi: 10.1152/ajprenal.1979.237.5.F367. [DOI] [PubMed] [Google Scholar]
  24. Männistö P. T., Poisner A. M. Different isotonic density gradients in separation of renin granules from rat kidney cortex. Med Biol. 1983 Jun;61(3):172–178. [PubMed] [Google Scholar]
  25. Männistö P. T., Poisner A. M. Further studies on properties of renin granules isolated from rat kidney cortex. Acta Physiol Scand. 1981 Aug;112(4):365–371. doi: 10.1111/j.1748-1716.1981.tb06832.x. [DOI] [PubMed] [Google Scholar]
  26. Park C. S., Honeyman T. W., Chung E. S., Lee J. S., Sigmon D. H., Fray J. C. Involvement of calmodulin in mediating inhibitory action of intracellular Ca2+ on renin secretion. Am J Physiol. 1986 Dec;251(6 Pt 2):F1055–F1062. doi: 10.1152/ajprenal.1986.251.6.F1055. [DOI] [PubMed] [Google Scholar]
  27. Pazoles C. J., Creutz C. E., Ramu A., Pollard H. B. Permeant anion activation of MgATPase activity in chromaffin granules. Evidence for direct coupling of proton and anion transport. J Biol Chem. 1980 Aug 25;255(16):7863–7869. [PubMed] [Google Scholar]
  28. Pollard H. B., Pazoles C. J., Creutz C. E. Mechanism of calcium action and release of vesicle-bound hormones during exocytosis. Recent Prog Horm Res. 1981;37:299–332. doi: 10.1016/b978-0-12-571137-1.50010-4. [DOI] [PubMed] [Google Scholar]
  29. Pollard H. B., Pazoles C. J., Creutz C. E., Ramu A., Strott C. A., Ray P., Brown E. M., Aurbach G. D., Tack-Goldman K. M., Shulman N. R. A role for anion transport in the regulation of release from chromaffin granules and exocytosis from cells. J Supramol Struct. 1977;7(3-4):277–285. doi: 10.1002/jss.400070302. [DOI] [PubMed] [Google Scholar]
  30. Pollard H. B., Tack-Goldman K., Pazoles C. J., Creutz C. E., Shulman N. R. Evidence for control of serotonin secretion from human platelets by hydroxyl ion transport and osmotic lysis. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5295–5299. doi: 10.1073/pnas.74.12.5295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rothman S. S., Liebow C. Permeability of zymogen granule membrane to protein. Am J Physiol. 1985 Apr;248(4 Pt 1):G385–G392. doi: 10.1152/ajpgi.1985.248.4.G385. [DOI] [PubMed] [Google Scholar]
  32. SOMMER A. J. The determination of acid and alkaline phosphatase using p-nitrophenyl phosphate as substrate. Am J Med Technol. 1954 Jul-Aug;20(4):244–253. [PubMed] [Google Scholar]
  33. Sagnella G. A., Peart W. S. Studies on the isolation and properties of renin granules from the rat kidney cortex. Biochem J. 1979 Aug 15;182(2):301–309. doi: 10.1042/bj1820301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Simon C. D., Honeyman T. W., Fray J. C. Renin-angiotensin system in hypophysectomized rats. I. Control of blood pressure. Am J Physiol. 1984 Jan;246(1 Pt 1):E84–E88. doi: 10.1152/ajpendo.1984.246.1.E84. [DOI] [PubMed] [Google Scholar]
  35. Skøtt O. Calcium and osmotic stimulation in renin release from isolated rat glomeruli. Pflugers Arch. 1986 May;406(5):485–491. doi: 10.1007/BF00583371. [DOI] [PubMed] [Google Scholar]
  36. Skøtt O. Effects of amines, monensin and nigericin on the renin release from isolated superfused rat glomeruli. Pflugers Arch. 1987 Jun;409(1-2):93–99. doi: 10.1007/BF00584754. [DOI] [PubMed] [Google Scholar]
  37. Skøtt O. Effects of osmolality and calcium on renin release from superfused rat glomeruli treated with nigericin or monensin. Pflugers Arch. 1988 Oct;412(5):503–508. doi: 10.1007/BF00582539. [DOI] [PubMed] [Google Scholar]
  38. Skøtt O. Episodic release of renin from single isolated superfused rat afferent arterioles. Pflugers Arch. 1986 Jul;407(1):41–45. doi: 10.1007/BF00580718. [DOI] [PubMed] [Google Scholar]
  39. Taugner R., Bührle C. P., Nobiling R. Ultrastructural changes associated with renin secretion from the juxtaglomerular apparatus of mice. Cell Tissue Res. 1984;237(3):459–472. doi: 10.1007/BF00228430. [DOI] [PubMed] [Google Scholar]
  40. Taugner R., Whalley A., Angermüller S., Bührle C. P., Hackenthal E. Are the renin-containing granules of juxtaglomerular epithelioid cells modified lysosomes? Cell Tissue Res. 1985;239(3):575–587. doi: 10.1007/BF00219236. [DOI] [PubMed] [Google Scholar]
  41. Zimmerberg J., Whitaker M. Irreversible swelling of secretory granules during exocytosis caused by calcium. Nature. 1985 Jun 13;315(6020):581–584. doi: 10.1038/315581a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES