Skip to main content
PMC home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1980 May;65(5):1192–1201. doi: 10.1172/JCI109774

Importance of Efferent Arteriolar Vascular Tone in Regulation of Proximal Tubule Fluid Reabsorption and Glomerulotubular Balance in the Rat

Iekuni Ichikawa 1,2, Barry M Brenner 1,2
PMCID: PMC371453  PMID: 7364945

Abstract

Micropuncture study was performed in 21 mildly volume-expanded Munich-Wistar rats before and during partial aortic constriction to examine the effects of endogenous prostaglandins (PG) and angiotensin II (AII) on single nephron glomerular filtration rate (SNGFR) and absolute proximal reabsorption rate (APR). Animals received either vehicle (group 1), indomethacin (group 2), or indomethacin plus saralasin (group 3). Before aortic constriction, these inhibitors were without effect on values of SNGFR and APR. In group 1 rats, reduction in mean renal arterial perfusion pressure (R̄ĀP̄) to ∼65 mm Hg resulted in marked and proportional declines in SNGFR and APR. With equivalent reduction in R̄ĀP̄ in group 2 rats, however, SNGFR fell to a lesser extent and APR tended to increase slightly above preconstriction values. Indomethacin administration was therefore associated with disruption of glomerulotubular balance. In view of the roughly equivalent declines in afferent arteriolar resistance measured in groups 1 and 2, the magnitude of increase in efferent arteriolar resistance (RE) appeared to be of major importance in determining the observed presence or absence of glomerulotubular balance. Thus, the lesser fall in SNGFR in group 2 than in group 1 was a result of the higher value for glomerular capillary hydraulic pressure in group 2, a consequence of the higher value of RE. The higher average value for APR during reduced R̄ĀP̄ in group 2 than in group 1 is also attributable to this pronounced rise in RE, the effect of which was to augment the net reabsorptive pressure both by favoring higher postglomerular oncotic pressure and lower downstream (peritubular capillary) hydraulic pressure. Since intrarenal release of AII is enhanced when R̄ĀP̄ declines, and because AII is known to raise RE selectively, it is likely that endogenous AII brought about the marked increase in RE in group 2, which was readily demonstrable only in indomethacin-treated rats, presumably because endogenous PG synthesis was suppressed.

In keeping with this conclusion, when the action of endogenous AII was inhibited by saralasin in group 3 rats, reduction in R̄ĀP̄ failed to induce a rise in RE, so that net filtration and reabsorption pressures again declined proportionally, as did SNGFR and APR. The present evidence therefore suggests that glomerulotubular balance is influenced to an important extent by the prevailing vasomotor tone of the efferent arteriole.

Full text

PDF
1194

Selected References

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

  1. Arendshorst W. J., Beierwaltes W. H. Renal and nephron hemodynamics in spontaneously hypertensive rats. Am J Physiol. 1979 Mar;236(3):F246–F251. doi: 10.1152/ajprenal.1979.236.3.F246. [DOI] [PubMed] [Google Scholar]
  2. Bank N., Aynedjian H. S., Wada T. Effect of peritubular capillary perfusion rate on proximal sodium reabsorption. Kidney Int. 1972 Jun;1(6):397–405. doi: 10.1038/ki.1972.52. [DOI] [PubMed] [Google Scholar]
  3. Baylis C., Brenner B. M. Modulation by prostaglandin synthesis inhibitors of the action of exogenous angiotensin II on glomerular ultrafiltration in the rat. Circ Res. 1978 Dec;43(6):889–898. doi: 10.1161/01.res.43.6.889. [DOI] [PubMed] [Google Scholar]
  4. Baylis C., Deen W. M., Myers B. D., Brenner B. M. Effects of some vasodilator drugs on transcapillary fluid exchange in renal cortex. Am J Physiol. 1976 Apr;230(4):1148–1158. doi: 10.1152/ajplegacy.1976.230.4.1148. [DOI] [PubMed] [Google Scholar]
  5. Bell R. D., Parry W. L., Grundy W. G. Renal lymph sodium and potassium concentrations following renal vasodilation. Proc Soc Exp Biol Med. 1973 Jun;143(2):499–501. doi: 10.3181/00379727-143-37352. [DOI] [PubMed] [Google Scholar]
  6. Berl T., Henrich W. L., Erickson A. L., Schrier R. W. Prostaglandins in the beta-adrenergic and baroreceptor-mediated secretion of renin. Am J Physiol. 1979 May;236(5):F472–F477. doi: 10.1152/ajprenal.1979.236.5.F472. [DOI] [PubMed] [Google Scholar]
  7. Blackshear J. L., Spielman W. S., Knox F. G., Romero J. C. Dissociation of renin release and renal vasodilation by prostaglandin synthesis inhibitors. Am J Physiol. 1979 Jul;237(1):F20–F24. doi: 10.1152/ajprenal.1979.237.1.F20. [DOI] [PubMed] [Google Scholar]
  8. Blantz R. C., Konnen K. S., Tucker B. J. Angiotensin II effects upon the glomerular microcirculation and ultrafiltration coefficient of the rat. J Clin Invest. 1976 Feb;57(2):419–434. doi: 10.1172/JCI108293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Blantz R. C., Tucker B. J. Determinants of peritubular capillary fluid uptake in hydropenia and saline and plasma expansion. Am J Physiol. 1975 Jun;228(6):1927–1935. doi: 10.1152/ajplegacy.1975.228.6.1927. [DOI] [PubMed] [Google Scholar]
  10. Brenner B. M., Troy J. L., Daugharty T. M., MacInnes R. M. Quantitative importance of changes in postglomerular colloid osmotic pressure in mediating glomerulotubular balance in the rat. J Clin Invest. 1973 Jan;52(1):190–197. doi: 10.1172/JCI107164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brenner B. M., Troy J. L. Postglomerular vascular protein concentration: evidence for a causal role in governing fluid reabsorption and glomerulotublar balance by the renal proximal tubule. J Clin Invest. 1971 Feb;50(2):336–349. doi: 10.1172/JCI106501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Davis J. O., Freeman R. H. Mechanisms regulating renin release. Physiol Rev. 1976 Jan;56(1):1–56. doi: 10.1152/physrev.1976.56.1.1. [DOI] [PubMed] [Google Scholar]
  13. Deen W. M., Robertson C. R., Brenner B. M. A model of peritubular capillary control of isotonic fluid reabsorption by the renal proximal tubule. Biophys J. 1973 Apr;13(4):340–358. doi: 10.1016/S0006-3495(73)85989-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Deen W. M., Troy J. L., Robertson C. R., Brenner B. M. Dynamics of glomerular ultrafiltration in the rat. IV. Determination of the ultrafiltration coefficient. J Clin Invest. 1973 Jun;52(6):1500–1508. doi: 10.1172/JCI107324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Earley L. E., Friedler R. M. The effects of combined renal vasodilatation and pressor agents on renal hemodynamics and the tubular reabsorption of sodium. J Clin Invest. 1966 Apr;45(4):542–551. doi: 10.1172/JCI105368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Falchuk K. H., Brenner B. M., Tadokoro M., Berliner R. W. Oncotic and hydrostatic pressures in peritubular capillaries and fluid reabsorption by proximal tubule. Am J Physiol. 1971 May;220(5):1427–1433. doi: 10.1152/ajplegacy.1971.220.5.1427. [DOI] [PubMed] [Google Scholar]
  17. Gotshall R. W., Davis J. O., Blaine E. H., Musacchia X. J., Braverman B., Freeman R., Johnson J. A. Increased renin release during renal arteriolar dilatation in dogs. Am J Physiol. 1974 Aug;227(2):251–255. doi: 10.1152/ajplegacy.1974.227.2.251. [DOI] [PubMed] [Google Scholar]
  18. Hall J. E., Guyton A. C., Jackson T. E., Coleman T. G., Lohmeier T. E., Trippodo N. C. Control of glomerular filtration rate by renin-angiotensin system. Am J Physiol. 1977 Nov;233(5):F366–F372. doi: 10.1152/ajprenal.1977.233.5.F366. [DOI] [PubMed] [Google Scholar]
  19. Ichikawa I., Brenner B. M. Local intrarenal vasoconstrictor-vasodilator interactions in mild partial ureteral obstruction. Am J Physiol. 1979 Feb;236(2):F131–F140. doi: 10.1152/ajprenal.1979.236.2.F131. [DOI] [PubMed] [Google Scholar]
  20. Ichikawa I., Brenner B. M. Mechanism of inhibition of proximal tubule fluid reabsorption after exposure of the rat kidney to the physical effects of expansion of extracellular fluid volume. J Clin Invest. 1979 Nov;64(5):1466–1474. doi: 10.1172/JCI109605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ichikawa I., Miele J. F., Brenner B. M. Reversal of renal cortical actions of angiotensin II by verapamil and manganese. Kidney Int. 1979 Aug;16(2):137–147. doi: 10.1038/ki.1979.115. [DOI] [PubMed] [Google Scholar]
  22. Kaloyanides G. J., Ahrens R. E., Shepherd J. A., DiBona G. F. Inhibition of prostaglandin E2 secretion. Failure to abolish autoregulation in the isolated dog kidney. Circ Res. 1976 Feb;38(2):67–73. doi: 10.1161/01.res.38.2.67. [DOI] [PubMed] [Google Scholar]
  23. Lewy J. E., Windhager E. E. Peritubular control of proximal tubular fluid reabsorption in the rat kidney. Am J Physiol. 1968 May;214(5):943–954. doi: 10.1152/ajplegacy.1968.214.5.943. [DOI] [PubMed] [Google Scholar]
  24. McGiff J. C., Crowshaw K., Terragno N. A., Lonigro A. J., Strand J. C., Williaon M. A., Lee J. B., Ng K. K. Prostaglandin-like substances appearing in canine renal venous blood during renal ischemia. Their patial characterization by pharmacologic and chromatographic procedures. Circ Res. 1970 Nov;27(5):765–782. doi: 10.1161/01.res.27.5.765. [DOI] [PubMed] [Google Scholar]
  25. Myers B. D., Deen W. M., Brenner B. M. Effects of norepinephrine and angiotensin II on the determinants of glomerular ultrafiltration and proximal tubule fluid reabsorption in the rat. Circ Res. 1975 Jul;37(1):101–110. doi: 10.1161/01.res.37.1.101. [DOI] [PubMed] [Google Scholar]
  26. Nizet A. Quantitative influence of non-hormonal blood factors on the control of sodium excretion by the isolated dog kidney. Kidney Int. 1972;1(1):27–37. doi: 10.1038/ki.1972.5. [DOI] [PubMed] [Google Scholar]
  27. O'morchoe C. C., Omorchoe P. J., Donati E. J. Comparison of hilar and capsular renal lymph. Am J Physiol. 1975 Aug;229(2):416–421. doi: 10.1152/ajplegacy.1975.229.2.416. [DOI] [PubMed] [Google Scholar]
  28. Ott C. E., Haas J. A., Cuche J. L., Knox F. G. Effect of increased peritubule protein concentration on proximal tubule reabsorption in the presence and absence of extracellular volume expansion. J Clin Invest. 1975 Mar;55(3):612–620. doi: 10.1172/JCI107969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Quinn M. D., Marsh D. J. Peritubular capillary control of proximal tubule reabsorption in the rat. Am J Physiol. 1979 May;236(5):F478–F487. doi: 10.1152/ajprenal.1979.236.5.F478. [DOI] [PubMed] [Google Scholar]
  30. Robertson C. R., Deen W. M., Troy J. L., Brenner B. M. Dynamics of glomerular ultrafiltration in the rat. 3. Hemodynamics and autoregulation. Am J Physiol. 1972 Nov;223(5):1191–1200. doi: 10.1152/ajplegacy.1972.223.5.1191. [DOI] [PubMed] [Google Scholar]
  31. Seymour A. A., Zehr J. E. Influence of renal prostaglandin synthesis on renin control mechanisms in the dog. Circ Res. 1979 Jul;45(1):13–25. doi: 10.1161/01.res.45.1.13. [DOI] [PubMed] [Google Scholar]
  32. Spitzer A., Windhager E. E. Effect of peritubular oncotic pressure changes on proximal tubular fluid reabsorption. Am J Physiol. 1970 Apr;218(4):1188–1193. doi: 10.1152/ajplegacy.1970.218.4.1188. [DOI] [PubMed] [Google Scholar]
  33. Starling E. H. The glomerular functions of the kidney. J Physiol. 1899 Jun 13;24(3-4):317–330. doi: 10.1113/jphysiol.1899.sp000760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Steiner R. W., Tucker B. J., Blantz R. C. Glomerular hemodynamics in rats with chronic sodium depletion. Effect of saralasin. J Clin Invest. 1979 Aug;64(2):503–512. doi: 10.1172/JCI109488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Strandhoy J. W., Ott C. E., Schneider E. G., Willis L. R., Beck N. P., Davis B. B., Knox F. G. Effects of prostaglandins E1 and E2 on renal sodium reabsorption and Starling forces. Am J Physiol. 1974 May;226(5):1015–1021. doi: 10.1152/ajplegacy.1974.226.5.1015. [DOI] [PubMed] [Google Scholar]
  36. Swain J. A., Heyndrickx G. R., Boettcher D. H., Vatner S. F. Prostaglandin control of renal circulation in the unanesthetized dog and baboon. Am J Physiol. 1975 Sep;229(3):826–830. doi: 10.1152/ajplegacy.1975.229.3.826. [DOI] [PubMed] [Google Scholar]
  37. Tucker B. J., Blantz R. C. Determinants of proximal tubular reabsorption as mechanisms of glomerulotubular balance. Am J Physiol. 1978 Aug;235(2):F142–F150. doi: 10.1152/ajprenal.1978.235.2.F142. [DOI] [PubMed] [Google Scholar]
  38. Weinman E. J., Kashgarian M., Hayslett J. P. Role of peritubular protein concentration in sodium reabsorption. Am J Physiol. 1971 Nov;221(5):1521–1528. doi: 10.1152/ajplegacy.1971.221.5.1521. [DOI] [PubMed] [Google Scholar]
  39. Wolgast M., Persson E., Schnermann J., Ulfendahl H., Wunderlich P. Colloid osmotic pressure of the subcapsular interstitial fluid of rat kidneys during hydropenia and volume expansion. Pflugers Arch. 1973 May 18;340(2):123–131. doi: 10.1007/BF00588171. [DOI] [PubMed] [Google Scholar]

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

RESOURCES