Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1988 Oct;82(4):1383–1390. doi: 10.1172/JCI113742

Atrial natriuretic factor inhibits vasopressin-stimulated osmotic water permeability in rat inner medullary collecting duct.

H Nonoguchi 1, J M Sands 1, M A Knepper 1
PMCID: PMC442695  PMID: 2844855

Abstract

The inner medullary collecting duct (IMCD) has been proposed to be a site of atrial natriuretic factor (ANF) action. We carried out experiments in isolated perfused terminal IMCDs to determine whether ANF (rat ANF 1-28) affects either osmotic water permeability (Pf) or urea permeability. In the presence of a submaximally stimulating concentration of vasopressin (10(-11) M), ANF (100 nM) significantly reduced Pf by an average of 46%. Lower concentrations of ANF also significantly inhibited vasopressin-stimulated Pf by the following percentages: 0.01 nM ANF, 18%; 0.1 nM, 46%; 1 nM, 48%. Addition of exogenous cyclic GMP (0.1 mM) mimicked the effect of ANF, decreasing Pf by an average of 48%. ANF also inhibited cyclic AMP-stimulated Pf by an average of 31%. ANF did not affect urea permeability, nor did it alter vasopressin-stimulated cyclic AMP accumulation. We conclude that ANF at physiological concentrations causes a large inhibition of vasopressin-stimulated Pf in the rat terminal IMCD, and that cyclic GMP is the second messenger mediating the effect. ANF appears to act at a site distal to cyclic AMP generation in the chain of events linking vasopressin receptor binding to an increase in osmotic water permeability.

Full text

PDF
1383

Selected References

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

  1. Al-Zahid G., Schafer J. A., Troutman S. L., Andreoli T. E. Effect of antidiuretic hormone on water and solute permeation, and the activation energies for these processes, in mammalian cortical collecting tubules: evidence for parallel ADH-sensitive pathways for water and solute diffusion in luminal plasma membranes. J Membr Biol. 1977 Feb 24;31(1-2):103–129. doi: 10.1007/BF01869401. [DOI] [PubMed] [Google Scholar]
  2. Ballermann B. J. A highly sensitive radioreceptor assay for atrial natriuretic peptide in rat plasma. Am J Physiol. 1988 Jan;254(1 Pt 2):F159–F163. doi: 10.1152/ajprenal.1988.254.1.F159. [DOI] [PubMed] [Google Scholar]
  3. Ballermann B. J., Brenner B. M. George E. Brown memorial lecture. Role of atrial peptides in body fluid homeostasis. Circ Res. 1986 May;58(5):619–630. doi: 10.1161/01.res.58.5.619. [DOI] [PubMed] [Google Scholar]
  4. Briggs J. P., Steipe B., Schubert G., Schnermann J. Micropuncture studies of the renal effects of atrial natriuretic substance. Pflugers Arch. 1982 Dec;395(4):271–276. doi: 10.1007/BF00580789. [DOI] [PubMed] [Google Scholar]
  5. Burg M. B. Perfusion of isolated renal tubules. Yale J Biol Med. 1972 Jun-Aug;45(3-4):321–326. [PMC free article] [PubMed] [Google Scholar]
  6. Camargo M. J., Kleinert H. D., Atlas S. A., Sealey J. E., Laragh J. H., Maack T. Ca-dependent hemodynamic and natriuretic effects of atrial extract in isolated rat kidney. Am J Physiol. 1984 Apr;246(4 Pt 2):F447–F456. doi: 10.1152/ajprenal.1984.246.4.F447. [DOI] [PubMed] [Google Scholar]
  7. Chai S. Y., Sexton P. M., Allen A. M., Figdor R., Mendelsohn F. A. In vitro autoradiographic localization of ANP receptors in rat kidney and adrenal gland. Am J Physiol. 1986 Apr;250(4 Pt 2):F753–F757. doi: 10.1152/ajprenal.1986.250.4.F753. [DOI] [PubMed] [Google Scholar]
  8. Cogan M. G. Atrial natriuretic factor can increase renal solute excretion primarily by raising glomerular filtration. Am J Physiol. 1986 Apr;250(4 Pt 2):F710–F714. doi: 10.1152/ajprenal.1986.250.4.F710. [DOI] [PubMed] [Google Scholar]
  9. Dillingham M. A., Anderson R. J. Inhibition of vasopressin action by atrial natriuretic factor. Science. 1986 Mar 28;231(4745):1572–1573. doi: 10.1126/science.3006248. [DOI] [PubMed] [Google Scholar]
  10. Dunn F. L., Brennan T. J., Nelson A. E., Robertson G. L. The role of blood osmolality and volume in regulating vasopressin secretion in the rat. J Clin Invest. 1973 Dec;52(12):3212–3219. doi: 10.1172/JCI107521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gunning M. E., Ballermann B. J., Silva P., Brenner B. M., Zeidel M. L. Characterization of ANP receptors in rabbit inner medullary collecting duct cells. Am J Physiol. 1988 Aug;255(2 Pt 2):F324–F330. doi: 10.1152/ajprenal.1988.255.2.F324. [DOI] [PubMed] [Google Scholar]
  12. Hartzell H. C., Fischmeister R. Opposite effects of cyclic GMP and cyclic AMP on Ca2+ current in single heart cells. Nature. 1986 Sep 18;323(6085):273–275. doi: 10.1038/323273a0. [DOI] [PubMed] [Google Scholar]
  13. Healy D. P., Fanestil D. D. Localization of atrial natriuretic peptide binding sites within the rat kidney. Am J Physiol. 1986 Mar;250(3 Pt 2):F573–F578. doi: 10.1152/ajprenal.1986.250.3.F573. [DOI] [PubMed] [Google Scholar]
  14. Huang C. L., Cogan M. G. Atrial natriuretic factor inhibits maximal tubuloglomerular feedback response. Am J Physiol. 1987 May;252(5 Pt 2):F825–F828. doi: 10.1152/ajprenal.1987.252.5.F825. [DOI] [PubMed] [Google Scholar]
  15. Knepper M. A., Good D. W., Burg M. B. Ammonia and bicarbonate transport by rat cortical collecting ducts perfused in vitro. Am J Physiol. 1985 Dec;249(6 Pt 2):F870–F877. doi: 10.1152/ajprenal.1985.249.6.F870. [DOI] [PubMed] [Google Scholar]
  16. Koseki C., Hayashi Y., Torikai S., Furuya M., Ohnuma N., Imai M. Localization of binding sites for alpha-rat atrial natriuretic polypeptide in rat kidney. Am J Physiol. 1986 Feb;250(2 Pt 2):F210–F216. doi: 10.1152/ajprenal.1986.250.2.F210. [DOI] [PubMed] [Google Scholar]
  17. Lang R. E., Thölken H., Ganten D., Luft F. C., Ruskoaho H., Unger T. Atrial natriuretic factor--a circulating hormone stimulated by volume loading. Nature. 1985 Mar 21;314(6008):264–266. doi: 10.1038/314264a0. [DOI] [PubMed] [Google Scholar]
  18. Leitman D. C., Andresen J. W., Kuno T., Kamisaki Y., Chang J. K., Murad F. Identification of multiple binding sites for atrial natriuretic factor by affinity cross-linking in cultured endothelial cells. J Biol Chem. 1986 Sep 5;261(25):11650–11655. [PubMed] [Google Scholar]
  19. Maack T., Camargo M. J., Kleinert H. D., Laragh J. H., Atlas S. A. Atrial natriuretic factor: structure and functional properties. Kidney Int. 1985 Apr;27(4):607–615. doi: 10.1038/ki.1985.54. [DOI] [PubMed] [Google Scholar]
  20. Morgan T., Berliner R. W. Permeability of the loop of Henle, vasa recta, and collecting duct to water, urea, and sodium. Am J Physiol. 1968 Jul;215(1):108–115. doi: 10.1152/ajplegacy.1968.215.1.108. [DOI] [PubMed] [Google Scholar]
  21. Moss J., Manganiello V. C., Vaughan M. Substrate and effector specificity of a guanosine 3':5'-monophosphate phosphodiesterase from rat liver. J Biol Chem. 1977 Aug 10;252(15):5211–5215. [PubMed] [Google Scholar]
  22. Murad F. Cyclic guanosine monophosphate as a mediator of vasodilation. J Clin Invest. 1986 Jul;78(1):1–5. doi: 10.1172/JCI112536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Murray R. D., Itoh S., Inagami T., Misono K., Seto S., Scicli A. G., Carretero O. A. Effects of synthetic atrial natriuretic factor in the isolated perfused rat kidney. Am J Physiol. 1985 Oct;249(4 Pt 2):F603–F609. doi: 10.1152/ajprenal.1985.249.4.F603. [DOI] [PubMed] [Google Scholar]
  24. Needleman P., Adams S. P., Cole B. R., Currie M. G., Geller D. M., Michener M. L., Saper C. B., Schwartz D., Standaert D. G. Atriopeptins as cardiac hormones. Hypertension. 1985 Jul-Aug;7(4):469–482. doi: 10.1161/01.hyp.7.4.469. [DOI] [PubMed] [Google Scholar]
  25. Nonoguchi H., Knepper M. A., Manganiello V. C. Effects of atrial natriuretic factor on cyclic guanosine monophosphate and cyclic adenosine monophosphate accumulation in microdissected nephron segments from rats. J Clin Invest. 1987 Feb;79(2):500–507. doi: 10.1172/JCI112840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ogawa K., Henry M. A., Tange J., Woodcock E. A., Johnston C. I. Atrial natriuretic peptide in dehydrated Long-Evans rats and Brattleboro rats. Kidney Int. 1987 Mar;31(3):760–765. doi: 10.1038/ki.1987.63. [DOI] [PubMed] [Google Scholar]
  27. Paul R. V., Kirk K. A., Navar L. G. Renal autoregulation and pressure natriuresis during ANF-induced diuresis. Am J Physiol. 1987 Sep;253(3 Pt 2):F424–F431. doi: 10.1152/ajprenal.1987.253.3.F424. [DOI] [PubMed] [Google Scholar]
  28. Pollock D. M., Arendshorst W. J. Effect of atrial natriuretic factor on renal hemodynamics in the rat. Am J Physiol. 1986 Nov;251(5 Pt 2):F795–F801. doi: 10.1152/ajprenal.1986.251.5.F795. [DOI] [PubMed] [Google Scholar]
  29. Rocha A. S., Kudo L. H. Water, urea, sodium, chloride, and potassium transport in the in vitro isolated perfused papillary collecting duct. Kidney Int. 1982 Nov;22(5):485–491. doi: 10.1038/ki.1982.201. [DOI] [PubMed] [Google Scholar]
  30. Salazar F. J., Fiksen-Olsen M. J., Opgenorth T. J., Granger J. P., Burnett J. C., Jr, Romero J. C. Renal effects of ANP without changes in glomerular filtration rate and blood pressure. Am J Physiol. 1986 Sep;251(3 Pt 2):F532–F536. doi: 10.1152/ajprenal.1986.251.3.F532. [DOI] [PubMed] [Google Scholar]
  31. Samson W. K., Vanatta J. C. Atrial natriuretic factor inhibits vasotocin-induced water reabsorption in the toad urinary bladder. Proc Soc Exp Biol Med. 1986 Jan;181(1):169–172. doi: 10.3181/00379727-181-rc1. [DOI] [PubMed] [Google Scholar]
  32. Sands J. M., Knepper M. A. Urea permeability of mammalian inner medullary collecting duct system and papillary surface epithelium. J Clin Invest. 1987 Jan;79(1):138–147. doi: 10.1172/JCI112774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sands J. M., Nonoguchi H., Knepper M. A. Vasopressin effects on urea and H2O transport in inner medullary collecting duct subsegments. Am J Physiol. 1987 Nov;253(5 Pt 2):F823–F832. doi: 10.1152/ajprenal.1987.253.5.F823. [DOI] [PubMed] [Google Scholar]
  34. Schmidt-Nielsen B. The renal pelvis. Kidney Int. 1987 Feb;31(2):621–628. doi: 10.1038/ki.1987.43. [DOI] [PubMed] [Google Scholar]
  35. Sonnenberg H., Cupples W. A., de Bold A. J., Veress A. T. Intrarenal localization of the natriuretic effect of cardiac atrial extract. Can J Physiol Pharmacol. 1982 Sep;60(9):1149–1152. doi: 10.1139/y82-166. [DOI] [PubMed] [Google Scholar]
  36. Sonnenberg H., Honrath U., Chong C. K., Wilson D. R. Atrial natriuretic factor inhibits sodium transport in medullary collecting duct. Am J Physiol. 1986 Jun;250(6 Pt 2):F963–F966. doi: 10.1152/ajprenal.1986.250.6.F963. [DOI] [PubMed] [Google Scholar]
  37. Star R. A., Nonoguchi H., Balaban R., Knepper M. A. Calcium and cyclic adenosine monophosphate as second messengers for vasopressin in the rat inner medullary collecting duct. J Clin Invest. 1988 Jun;81(6):1879–1888. doi: 10.1172/JCI113534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tremblay J., Gerzer R., Pang S. C., Cantin M., Genest J., Hamet P. ANF stimulation of detergent-dispersed particulate guanylate cyclase from bovine adrenal cortex. FEBS Lett. 1986 Jan 6;194(2):210–214. doi: 10.1016/0014-5793(86)80086-2. [DOI] [PubMed] [Google Scholar]
  39. Tremblay J., Gerzer R., Vinay P., Pang S. C., Béliveau R., Hamet P. The increase of cGMP by atrial natriuretic factor correlates with the distribution of particulate guanylate cyclase. FEBS Lett. 1985 Feb 11;181(1):17–22. doi: 10.1016/0014-5793(85)81105-4. [DOI] [PubMed] [Google Scholar]
  40. Winquist R. J., Faison E. P., Waldman S. A., Schwartz K., Murad F., Rapoport R. M. Atrial natriuretic factor elicits an endothelium-independent relaxation and activates particulate guanylate cyclase in vascular smooth muscle. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7661–7664. doi: 10.1073/pnas.81.23.7661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Zeidel M. L., Seifter J. L., Lear S., Brenner B. M., Silva P. Atrial peptides inhibit oxygen consumption in kidney medullary collecting duct cells. Am J Physiol. 1986 Aug;251(2 Pt 2):F379–F383. doi: 10.1152/ajprenal.1986.251.2.F379. [DOI] [PubMed] [Google Scholar]
  42. de Bold A. J., Borenstein H. B., Veress A. T., Sonnenberg H. A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci. 1981 Jan 5;28(1):89–94. doi: 10.1016/0024-3205(81)90370-2. [DOI] [PubMed] [Google Scholar]
  43. van de Stolpe A., Jamison R. L. Micropuncture study of the effect of ANP on the papillary collecting duct in the rat. Am J Physiol. 1988 Apr;254(4 Pt 2):F477–F483. doi: 10.1152/ajprenal.1988.254.4.F477. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES