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. 1975 Jul;56(1):208–217. doi: 10.1172/JCI108069

Effects of acute unilateral renal denervation in the rat.

E Bello-Reuss, R E Colindres, E Pastoriza-Muñoz, R A Mueller, C W Gottschalk
PMCID: PMC436571  PMID: 1141432

Abstract

Studies were undertaken to characterize the renal responses to acute unilateral renal denervation and the mechanisms involved in these responses. Denervation was produced in anesthetized nondiuretic rats by application of phenol to the left renal artery. Studies were also performed in sham-denervated nondiuretic rats. Whole kidney and individual nephron studies were performed before and after denervation or sham denervation. Denervation increased urine volume from the left kidney to about twice its control value (P less than 0.001) and increased urinary sodium excretion from 332 neq min minus -1 to 1,887 neq min minus -1 (P less than 0.001). Glomerular filtration rate (GFR) and renal plasma flow (RPF) remained unchanged in both kidneys after the procedure. The innervated right kidney showed no changes in urine volume or in sodium excretion. After denervation, late proximal ratio of tubular fluid inulin concentration to that of plasma [(F/P)In] decreased from 2.23 to 1.50 (P less than 0.001) while single nephron GFR remained unchanged. Absolute reabsorption decreased from 16.5 to 9.9 n. min minus -1 (P less than 0.001). (F/P)In ratios were also decreased in early distal (from 6.21 to 3.18, P less 0.001) and late distal convolutions (from 16.41 to 8.33, P less than 0.001) during the experimental period. (F/P)Na ratios remained unchanged in the early distal convolutions, but increased from 0.18 to 0.38 (P less than 0.01) in late distal convolutions after denervation. Absolute Na reabsorption after denervation increased in the loop of Henle, distal convolution, and collecting ducts. Any changes in intrarenal hydrostatic pressures after denervation were always small. There were no changes in GFR, RPF, urine volume, urinary sodium excretion, or late proximal (F/P)In after sham denervation. We conclude that the diuresis and natriuresis seen after acute renal denervation were caused by a marked depression of sodium and water reabsorption in the proximal tubule with partial compensation in more distal nephron segments. These responses appeared to be unrelated to systemic or intrarenal hemodynamic changes. The results demonstrate an effect of the renal nerves on proximal tubular function.

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Selected References

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  1. ANTON A. H., SAYRE D. F. A study of the factors affecting the aluminum oxide-trihydroxyindole procedure for the analysis of catecholamines. J Pharmacol Exp Ther. 1962 Dec;138:360–375. [PubMed] [Google Scholar]
  2. Allison M. E., Lipham E. M., Gottschalk C. W. Hydrostatic pressure in the rat kidney. Am J Physiol. 1972 Oct;223(4):975–983. doi: 10.1152/ajplegacy.1972.223.4.975. [DOI] [PubMed] [Google Scholar]
  3. BERNE R. M. Hemodynamics and sodium excretion of denervated kidney in anesthetized and unanesthetized dog. Am J Physiol. 1952 Oct;171(1):148–158. doi: 10.1152/ajplegacy.1952.171.1.148. [DOI] [PubMed] [Google Scholar]
  4. BRICKER N. S., STRAFFON R. A., MAHONEY E. P., MERRILL J. P. The functional capacity of the kidney denervated by autotransplantation in the dog. J Clin Invest. 1958 Feb;37(2):185–193. doi: 10.1172/JCI103597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barajas L., Müller J. The innervation of the juxtaglomerular apparatus and surrounding tubules: a quantitative analysis by serial section electron microscopy. J Ultrastruct Res. 1973 Apr;43(1):107–132. doi: 10.1016/s0022-5320(73)90073-7. [DOI] [PubMed] [Google Scholar]
  6. Bastide F., Jard S. Actions de la noradrénaline et de l'oxytocine sur le transport actif de sodium et la permeabilité à l'eau de la peau de grenouille. Rôle du 3',5'-AMP cyclique. Biochim Biophys Acta. 1968 Jan 3;150(1):113–123. doi: 10.1016/0005-2736(68)90014-x. [DOI] [PubMed] [Google Scholar]
  7. Blake W. D., Jurf A. N. Renal sodium reabsorption after acute renal denervation in the rabbit. J Physiol. 1968 May;196(1):65–73. doi: 10.1113/jphysiol.1968.sp008494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bonjour J. P., Churchill P. C., Malvin R. L. Change of tubular reabsorption of sodium and water after renal denervation in the dog. J Physiol. 1969 Oct;204(3):571–582. doi: 10.1113/jphysiol.1969.sp008932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brenner B. M., Falchuk K. H., Keimowitz R. I., Berliner R. W. The relationship between peritubular capillary protein concentration and fluid reabsorption by the renal proximal tubule. J Clin Invest. 1969 Aug;48(8):1519–1531. doi: 10.1172/JCI106118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cole W. R., Witte M. H., Kash S. L., Rodger M., Bleisch W. R., Muelheims G. H. Thoracic duct-to-pulmonary vein shunt in the treatment of experimental right heart failure. Circulation. 1967 Oct;36(4):539–543. doi: 10.1161/01.cir.36.4.539. [DOI] [PubMed] [Google Scholar]
  11. Colindres R. E., Lechene C. Technical problems associated with collection of distal tubular fluid in the rat. Yale J Biol Med. 1972 Jun-Aug;45(3-4):233–239. [PMC free article] [PubMed] [Google Scholar]
  12. Cortney M. A. Renal tubular transfer of water and electrolytes in adrenalectomized rats. Am J Physiol. 1969 Mar;216(3):589–598. doi: 10.1152/ajplegacy.1969.216.3.589. [DOI] [PubMed] [Google Scholar]
  13. Davidman M., Alexander E., Lalone R., Levinsky N. Nephron function during volume expansion in the rat. Am J Physiol. 1972 Jul;223(1):188–193. doi: 10.1152/ajplegacy.1972.223.1.188. [DOI] [PubMed] [Google Scholar]
  14. FUHR J., KACZMARCZYK J., KRUTTGEN C. D. Eine einfache colorimetrische Methode zur Inulinbestimmung für Nieren-Clearance-Untersuchungen bei Stoffwechselgesunden und Diabetikern. Klin Wochenschr. 1955 Aug 1;33(29-30):729–730. doi: 10.1007/BF01473295. [DOI] [PubMed] [Google Scholar]
  15. Field M., McColl I. Ion transport in rabbit ileal mucosa. 3. Effects of catecholamines. Am J Physiol. 1973 Oct;225(4):852–857. doi: 10.1152/ajplegacy.1973.225.4.852. [DOI] [PubMed] [Google Scholar]
  16. GOTTSCHALK C. W., MOREL F., MYLLE M. TRACER MICROINJECTION STUDIES OF RENAL TUBULAR PERMEABILITY. Am J Physiol. 1965 Jul;209:173–178. doi: 10.1152/ajplegacy.1965.209.1.173. [DOI] [PubMed] [Google Scholar]
  17. GOTTSCHALK C. W., MYLLE M. Micropuncture study of pressures in proximal tubules and peritubular capillaries of the rat kidney and their relation to ureteral and renal venous pressures. Am J Physiol. 1956 May;185(2):430–439. doi: 10.1152/ajplegacy.1956.185.2.430. [DOI] [PubMed] [Google Scholar]
  18. Gill J. R., Jr, Carr A. A., Fleischmann L. E., Casper A. G., Bartter F. C. Effects of pentolinium on sodium excretion in dogs with constriction of the vena cava. Am J Physiol. 1967 Jan;212(1):191–196. doi: 10.1152/ajplegacy.1967.212.1.191. [DOI] [PubMed] [Google Scholar]
  19. Gill J. R., Jr, Casper A. G. Depression of proximal tubular sodium reabsorption in the dog in response to renal beta adrenergic stimulation by isoproterenol. J Clin Invest. 1971 Jan;50(1):112–118. doi: 10.1172/JCI106464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gill J. R., Jr, Casper A. G. Effect of renal alpha-adrenergic stimulation on proximal tubular sodium reabsorption. Am J Physiol. 1972 Nov;223(5):1201–1205. doi: 10.1152/ajplegacy.1972.223.5.1201. [DOI] [PubMed] [Google Scholar]
  21. Handler J. S., Bensinger R., Orloff J. Effect of adrenergic agents on toad bladder response to ADH, 3',5'-AMP, and theophylline. Am J Physiol. 1968 Nov;215(5):1024–1031. doi: 10.1152/ajplegacy.1968.215.5.1024. [DOI] [PubMed] [Google Scholar]
  22. Howards S. S., Davis B. B., Knox F. G., Wright F. S., Berliner R. W. Depression of fractional sodium reabsorption by the proximal tubule of the dog without sodium diuresis. J Clin Invest. 1968 Jul;47(7):1561–1572. doi: 10.1172/JCI105848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. KAMM D. E., LEVINSKY N. G. THE MECHANISM OF DENERVATION NATRIURESIS. J Clin Invest. 1965 Jan;44:93–102. doi: 10.1172/JCI105131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. MITCHELL G. A. G. The nerve supply of the kidneys. Acta Anat (Basel) 1950;10(1-2):1–37. doi: 10.1159/000140455. [DOI] [PubMed] [Google Scholar]
  25. McKenna O. C., Angelakos E. T. Adrenergic innervation of the canine kidney. Circ Res. 1968 Mar;22(3):345–354. doi: 10.1161/01.res.22.3.345. [DOI] [PubMed] [Google Scholar]
  26. Morgan T., Berliner R. W. A study by continuous microperfusion of water and electrolyte movements in the loop of Henle and distal tubule of the rat. Nephron. 1969;6(3):388–405. doi: 10.1159/000179741. [DOI] [PubMed] [Google Scholar]
  27. Müller J., Barajas L. Electron microscopic and histochemical evidence for a tubular innervation in the renal cortex of the monkey. J Ultrastruct Res. 1972 Dec;41(5):533–549. doi: 10.1016/s0022-5320(72)90054-8. [DOI] [PubMed] [Google Scholar]
  28. NATHAN P. W., SEARS T. A. Effects of phenol on nervous conduction. J Physiol. 1960 Mar;150:565–580. doi: 10.1113/jphysiol.1960.sp006405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pomeranz B. H., Birtch A. G., Barger A. C. Neural contrfl of intrarenal blood flow. Am J Physiol. 1968 Nov;215(5):1067–1081. doi: 10.1152/ajplegacy.1968.215.5.1067. [DOI] [PubMed] [Google Scholar]
  30. SURTSHIN A., MUELLER C. B., WHITE H. L. Effect of acute changes in glomerular filtration rate on water and electrolyte excretion; mechanism of denervation diuresis. Am J Physiol. 1952 Apr;169(1):159–173. doi: 10.1152/ajplegacy.1952.169.1.159. [DOI] [PubMed] [Google Scholar]
  31. Stein J. H., Osgood R. W., Boonjarern S., Ferris T. F. A comparison of the segmental analysis of sodium reabsorption during Ringer's and hyperoncotic albumin infusion in the rat. J Clin Invest. 1973 Sep;52(9):2313–2323. doi: 10.1172/JCI107420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Takács L., Bencsáth P., Demeczky L. Renal sodium and water excretion after unilateral splanchnicotomy in the dog. Acta Physiol Acad Sci Hung. 1971;39(4):283–291. [PubMed] [Google Scholar]

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