Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1983 Jun;71(6):1588–1601. doi: 10.1172/JCI110915

Interactions among prostaglandin E2, antidiuretic hormone, and cyclic adenosine monophosphate in modulating Cl- absorption in single mouse medullary thick ascending limbs of Henle.

R M Culpepper, T E Andreoli
PMCID: PMC370365  PMID: 6306052

Abstract

This paper describes the inhibitory effect of prostaglandin E2 (PGE2) on antidiuretic hormone (ADH)-stimulated net Cl- absorption and spontaneous transepithelial voltage (Ve) in single medullary thick ascending limbs of Henle (TALH, thick ascending limb; mTALH, medullary segment; cTALH, cortical segment) obtained from mouse kidney. The experimental data indicate that PGE2 reduced the ADH-dependent values of net Cl- absorption (JnetCl, eq cm-2 s-1) and Ve (mV) in a dose-dependent manner; that increasing concentrations of peritubular ADH reversed the PGE2-mediated reductions in the ADH-dependent moiety of Ve in the mouse mTALH; that PGE2 had no effect on cyclic AMP-stimulated increments in Ve in the mouse mTALH; and that PGE2 had no effect on Ve in the cTALH, where Ve is unaffected either by ADH or by cyclic AMP. These effects might be obtained because of a direct competition between ADH and PGE2 for receptor binding on basolateral membranes. Alternatively, PGE2 might have reduced the affinities between ADH-receptor units and a component(s) of the series of processes leading to adenyl cyclase activation. The latter argument requires that basolateral membranes of the mouse mTALH exhibit receptor reserve, i.e., at the minimum concentration of ADH required to enhance Ve and JnetCl maximally, a fraction of basolateral membrane ADH receptors were unoccupied. According to this view, increasing peritubular ADH concentrations might reverse the PGE2-mediated reduction in ADH-dependent salt transport by increasing the number of basolateral membrane receptors occupied by ADH.

Full text

PDF
1588

Selected References

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

  1. Altsheler P., Klahr S., Rosenbaum R., Slatopolsky E. Effects of inhibitors of prostaglandin synthesis on renal sodium excretion in normal dogs and dogs with decreased renal mass. Am J Physiol. 1978 Oct;235(4):F338–F344. doi: 10.1152/ajprenal.1978.235.4.F338. [DOI] [PubMed] [Google Scholar]
  2. Anderson R. J., Berl T., McDonald K. D., Schrier R. W. Evidence for an in vivo antagonism between vasopressin and prostaglandin in the mammalian kidney. J Clin Invest. 1975 Aug;56(2):420–426. doi: 10.1172/JCI108108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Andreoli T. E., Schafer J. A. Effective luminal hypotonicity: the driving force for isotonic proximal tubular fluid absorption. Am J Physiol. 1979 Feb;236(2):F89–F96. doi: 10.1152/ajprenal.1979.236.2.F89. [DOI] [PubMed] [Google Scholar]
  4. Bennett C. M., Clapp J. R., Berliner R. W. Micropuncture study of the proximal and distal tubule in the dog. Am J Physiol. 1967 Nov;213(5):1254–1262. doi: 10.1152/ajplegacy.1967.213.5.1254. [DOI] [PubMed] [Google Scholar]
  5. Berl T., Raz A., Wald H., Horowitz J., Czaczkes W. Prostaglandin synthesis inhibition and the action of vasopressin: studies in man and rat. Am J Physiol. 1977 Jun;232(6):F529–F537. doi: 10.1152/ajprenal.1977.232.6.F529. [DOI] [PubMed] [Google Scholar]
  6. Bisordi J. E., Schlondorff D., Hays R. M. Interaction of vasopressin and prostaglandins in the toad urinary bladder. J Clin Invest. 1980 Dec;66(6):1200–1210. doi: 10.1172/JCI109971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brummer H. C. Storage life of prostaglandin E 2 in ethanol and saline. J Pharm Pharmacol. 1971 Oct;23(10):804–805. doi: 10.1111/j.2042-7158.1971.tb08611.x. [DOI] [PubMed] [Google Scholar]
  8. Burg M. B., Green N. Function of the thick ascending limb of Henle's loop. Am J Physiol. 1973 Mar;224(3):659–668. doi: 10.1152/ajplegacy.1973.224.3.659. [DOI] [PubMed] [Google Scholar]
  9. Carvounis C. P., Franki N., Levine S. D., Hays R. M. Membrane pathways for water and solutes in the toad bladder: I. Independent activation of water and urea transport. J Membr Biol. 1979 Sep;49(3):253–268. doi: 10.1007/BF01871121. [DOI] [PubMed] [Google Scholar]
  10. Chabardés D., Imbert-Teboul M., Gagnan-Brunette M., Morel F. Different hormonal target sites along the mouse and rabbit nephrons. Curr Probl Clin Biochem. 1977 Oct 23;8:447–454. [PubMed] [Google Scholar]
  11. Clapp J. R., Robinson R. R. Osmolality of distal tubular fluid in the dog. J Clin Invest. 1966 Dec;45(12):1847–1853. doi: 10.1172/JCI105488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Edwards R. M., Jackson B. A., Dousa T. P. ADH-sensitive cAMP system in papillary collecting duct: effect of osmolality and PGE2. Am J Physiol. 1981 Apr;240(4):F311–F318. doi: 10.1152/ajprenal.1981.240.4.F311. [DOI] [PubMed] [Google Scholar]
  13. Eggena P., Schwartz I. L., Walter R. Threshold and receptor reserve in the action of neurohypophyseal peptides. A study of synergists and antagonists of the hydroosmotic response of the toad urinary bladder. J Gen Physiol. 1970 Aug;56(2):250–271. doi: 10.1085/jgp.56.2.250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fejes-Tóth G., Magyar A., Walter J. Renal response to vasopressin after inhibition of prostaglandin synthesis. Am J Physiol. 1977 May;232(5):F416–F423. doi: 10.1152/ajprenal.1977.232.5.F416. [DOI] [PubMed] [Google Scholar]
  15. Fine L. G., Trizna W. Influence of prostaglandins on sodium transport of isolated medullary nephron segments. Am J Physiol. 1977 Apr;232(4):F383–F390. doi: 10.1152/ajprenal.1977.232.4.F383. [DOI] [PubMed] [Google Scholar]
  16. Friedman P. A., Andreoli T. E. CO2-stimulated NaCl absorption in the mouse renal cortical thick ascending limb of Henle. Evidence for synchronous Na +/H+ and Cl-/HCO3- exchange in apical plasma membranes. J Gen Physiol. 1982 Nov;80(5):683–711. doi: 10.1085/jgp.80.5.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fülgraff G., Brandenbusch G. Comparison of the effects of the prostaglandins A1, E2, and F2alpha on kidney function in dogs. Pflugers Arch. 1974 May 24;349(1):9–17. doi: 10.1007/BF00587912. [DOI] [PubMed] [Google Scholar]
  18. GOTTSCHALK C. W., MYLLE M. Micropuncture study of the mammalian urinary concentrating mechanism: evidence for the countercurrent hypothesis. Am J Physiol. 1959 Apr;196(4):927–936. doi: 10.1152/ajplegacy.1959.196.4.927. [DOI] [PubMed] [Google Scholar]
  19. Grantham J. J., Orloff J. Effect of prostaglandin E1 on the permeability response of the isolated collecting tubule to vasopressin, adenosine 3',5'-monophosphate, and theophylline. J Clin Invest. 1968 May;47(5):1154–1161. doi: 10.1172/JCI105804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Greger R. Cation selectivity of the isolated perfused cortical thick ascending limb of Henle's loop of rabbit kidney. Pflugers Arch. 1981 Apr;390(1):30–37. doi: 10.1007/BF00582707. [DOI] [PubMed] [Google Scholar]
  21. Greger R., Schlatter E. Presence of luminal K+, a prerequisite for active NaCl transport in the cortical thick ascending limb of Henle's loop of rabbit kidney. Pflugers Arch. 1981 Nov;392(1):92–94. doi: 10.1007/BF00584588. [DOI] [PubMed] [Google Scholar]
  22. Gross J. B., Barter F. C. Effects of prostaglandins E 1 , A 1 , and F 2 on renal handling of salt and water. Am J Physiol. 1973 Jul;225(1):218–224. doi: 10.1152/ajplegacy.1973.225.1.218. [DOI] [PubMed] [Google Scholar]
  23. Hall D. A., Varney D. M. Effect of vasopressin on electrical potential difference and chloride transport in mouse medullary thick ascending limb of Henle's loop. J Clin Invest. 1980 Oct;66(4):792–802. doi: 10.1172/JCI109917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hebert S. C., Culpepper R. M., Andreoli T. E. NaCl transport in mouse medullary thick ascending limbs. I. Functional nephron heterogeneity and ADH-stimulated NaCl cotransport. Am J Physiol. 1981 Oct;241(4):F412–F431. doi: 10.1152/ajprenal.1981.241.4.F412. [DOI] [PubMed] [Google Scholar]
  25. Hebert S. C., Culpepper R. M., Andreoli T. E. NaCl transport in mouse medullary thick ascending limbs. II. ADH enhancement of transcellular NaCl cotransport; origin of transepithelial voltage. Am J Physiol. 1981 Oct;241(4):F432–F442. doi: 10.1152/ajprenal.1981.241.4.F432. [DOI] [PubMed] [Google Scholar]
  26. Hebert S. C., Culpepper R. M., Andreoli T. E. NaCl transport in mouse medullary thick ascending limbs. III. Modulation of the ADH effect by peritubular osmolality. Am J Physiol. 1981 Oct;241(4):F443–F451. doi: 10.1152/ajprenal.1981.241.4.F443. [DOI] [PubMed] [Google Scholar]
  27. Higashihara E., Stokes J. B., Kokko J. P., Campbell W. B., DuBose T. D., Jr Cortical and papillary micropuncture examination of chloride transport in segments of the rat kidney during inhibition of prostaglandin production. Possible role for prostaglandins in the chloruresis of acute volume expansion. J Clin Invest. 1979 Nov;64(5):1277–1287. doi: 10.1172/JCI109583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Holt W. F., Lechene C. ADH-PGE2 interactions in cortical collecting tubule. I. Depression of sodium transport. Am J Physiol. 1981 Oct;241(4):F452–F460. doi: 10.1152/ajprenal.1981.241.4.F452. [DOI] [PubMed] [Google Scholar]
  29. Iino Y., Imai M. Effects of prostaglandins on Na transport in isolated collecting tubules. Pflugers Arch. 1978 Feb 22;373(2):125–132. doi: 10.1007/BF00584850. [DOI] [PubMed] [Google Scholar]
  30. Johnston H. H., Herzog J. P., Lauler D. P. Effect of prostaglandin E1 on renal hemodynamics, sodium and water excretion. Am J Physiol. 1967 Oct;213(4):939–946. doi: 10.1152/ajplegacy.1967.213.4.939. [DOI] [PubMed] [Google Scholar]
  31. Kauker M. L. Prostaglandin E2 effect from the luminal side on renal tubular 22Na efflux: tracer microinjection studies. Proc Soc Exp Biol Med. 1977 Feb;154(2):274–277. doi: 10.3181/00379727-154-39653. [DOI] [PubMed] [Google Scholar]
  32. Kokko J. P., Rector F. C., Jr Countercurrent multiplication system without active transport in inner medulla. Kidney Int. 1972 Oct;2(4):214–223. doi: 10.1038/ki.1972.97. [DOI] [PubMed] [Google Scholar]
  33. Morel F., Imbert-Teboul M., Chabardès D. Cyclic nucleotides and tubule function. Adv Cyclic Nucleotide Res. 1980;12:301–313. [PubMed] [Google Scholar]
  34. ORLOFF J., HANDLER J. S., BERGSTROM S. EFFECT OF PROSTAGLANDIN (PGE-1) ON THE PERMEABILITY RESPONSE OF TOAD BLADDER TO VASOPRESSIN, THEOPHYLLINE AND ADENOSINE 3',5'-MONOPHOSPHATE. Nature. 1965 Jan 23;205:397–398. doi: 10.1038/205397a0. [DOI] [PubMed] [Google Scholar]
  35. Posternak T., Weimann G. The preparation of acylated derivatives of cyclic nucleotides. Methods Enzymol. 1974;38:399–409. doi: 10.1016/0076-6879(74)38057-3. [DOI] [PubMed] [Google Scholar]
  36. Rocha A. S., Kokko J. P. Sodium chloride and water transport in the medullary thick ascending limb of Henle. Evidence for active chloride transport. J Clin Invest. 1973 Mar;52(3):612–623. doi: 10.1172/JCI107223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sasaki S., Imai M. Effects of vasopressin on water and NaCl transport across the in vitro perfused medullary thick ascending limb of Henle's loop of mouse, rat, and rabbit kidneys. Pflugers Arch. 1980 Feb;383(3):215–221. doi: 10.1007/BF00587521. [DOI] [PubMed] [Google Scholar]
  38. Schafer J. A., Andreoli T. E. Cellular constraints to diffusion. The effect of antidiuretic hormone on water flows in isolated mammalian collecting tubules. J Clin Invest. 1972 May;51(5):1264–1278. doi: 10.1172/JCI106921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Schlondorff D., Carvounis C. P., Jacoby M., Satriano J. A., Levine S. D. Multiple sites for interaction of prostaglandin and vasopressin in toad urinary bladder. Am J Physiol. 1981 Dec;241(6):F625–F631. doi: 10.1152/ajprenal.1981.241.6.F625. [DOI] [PubMed] [Google Scholar]
  40. Stokes J. B. Effect of prostaglandin E2 on chloride transport across the rabbit thick ascending limb of Henle. Selective inhibitions of the medullary portion. J Clin Invest. 1979 Aug;64(2):495–502. doi: 10.1172/JCI109487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stokes J. B., Kokko J. P. Inhibition of sodium transport by prostaglandin E2 across the isolated, perfused rabbit collecting tubule. J Clin Invest. 1977 Jun;59(6):1099–1104. doi: 10.1172/JCI108733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Strickland S., Loeb J. N. Obligatory separation of hormone binding and biological response curves in systems dependent upon secondary mediators of hormone action. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1366–1370. doi: 10.1073/pnas.78.3.1366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. WIRZ H. Der osmotische Druck in den corticalen Tubuli der Rattenniere. Helv Physiol Pharmacol Acta. 1956;14(3):353–362. [PubMed] [Google Scholar]
  44. Wallin J. D., Barratt L. J., Rector F. C., Jr, Seldin D. W. The influence of flow rate and chloride delivery on TcH2O formation in the rat. Kidney Int. 1973 May;3(5):282–290. doi: 10.1038/ki.1973.46. [DOI] [PubMed] [Google Scholar]
  45. Zook T. E., Strandhoy J. W. Inhibition of ADH-enhanced transepithelial urea and water movement by prostaglandins. Prostaglandins. 1980 Jul;20(1):1–13. doi: 10.1016/0090-6980(80)90002-7. [DOI] [PubMed] [Google Scholar]
  46. Zusman R. M., Keiser H. R., Handler J. S. Vasopressin-stimulated prostaglandin E biosynthesis in the toad urinary bladder. Effect of water flow. J Clin Invest. 1977 Dec;60(6):1339–1347. doi: 10.1172/JCI108893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Zusman R. M., Keiser H. R. Prostaglandin biosynthesis by rabbit renomedullary interstitial cells in tissue culture. Stimulation by angiotensin II, bradykinin, and arginine vasopressin. J Clin Invest. 1977 Jul;60(1):215–223. doi: 10.1172/JCI108758. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES