Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1991 May;436:421–429. doi: 10.1113/jphysiol.1991.sp018558

Regional heterogeneity of endothelium-dependent vasodilatation in the rabbit kidney.

H S Cairns 1, M E Rogerson 1, J Westwick 1, G H Neild 1
PMCID: PMC1181513  PMID: 1712038

Abstract

1. Regional heterogeneity of endothelial function exists but its role in the local regulation of vascular tone is uncertain. This heterogeneity may be very important in the control of the glomerular filtration rate (GFR) in which the differential tone in the afferent and efferent arterioles is crucial. 2. When an endothelium-independent vasodilator, prostacyclin (PGI2) or nitroprusside, was infused into anaesthetized rabbits there were dose-dependent falls in both mean arterial pressure (MAP) and GFR; PGI2 (0.4 nmol kg-1 min-1) altered MAP and GFR by -18.5 +/- 3.6% (mean +/- S.E.M.) and -37.7 +/- 13.3% respectively and nitroprusside (30 nmol kg-1 min-1) by -29.7 +/- 3.1% and -67.0 +/- 2.4%. In contrast infusion of an endothelium-dependent vasodilator, acetylcholine (ACh) or substance P, produced dose-dependent decreases in MAP but dose-dependent increases in GFR; ACh (10 nmol kg-1 min-1) -15.1 +/- 2.0% and +43.8 +/- 16.5% and substance P (30 nmol kg-1 min-1) -18.7 +/- 1.9% and +45.3 +/- 23.1% respectively. The effects of endothelium-dependent and independent vasodilators on GFR was significantly different (p less than 0.005). 3. Simultaneous administration of indomethacin, Methylene Blue or NG-monomethyl-L-arginine (L-NMMA), inhibitors of cyclo-oxygenase and endothelium-derived relaxing factor (EDRF) respectively, attenuated or reversed the effect of ACh (10 nmol kg-1 min-1) on MAP and GFR. 4. These data suggest that endothelium-dependent vasodilatation in the kidney has a heterogeneous effect on the renal microvasculature, exerting a preferential effect on afferent glomerular arterioles and thereby preserving GFR despite the fall in MAP.(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF
425

Selected References

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

  1. Ausiello D. A., Kreisberg J. I., Roy C., Karnovsky M. J. Contraction of cultured rat glomerular cells of apparent mesangial origin after stimulation with angiotensin II and arginine vasopressin. J Clin Invest. 1980 Mar;65(3):754–760. doi: 10.1172/JCI109723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baer P. G., Navar L. G., Guyton A. C. Renal autoregulation, filtration rate, and electrolyte excretion during vasodilatation. Am J Physiol. 1970 Sep;219(3):619–625. doi: 10.1152/ajplegacy.1970.219.3.619. [DOI] [PubMed] [Google Scholar]
  3. Banks R. O., Fondacaro J. D., Schwaiger M. M., Jacobson E. D. Renal histamine H1 and H2 receptors: characterization and functional significance. Am J Physiol. 1978 Dec;235(6):F570–F575. doi: 10.1152/ajprenal.1978.235.6.F570. [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. Bhardwaj R., Moore P. K. Endothelium-derived relaxing factor and the effects of acetylcholine and histamine on resistance blood vessels. Br J Pharmacol. 1988 Nov;95(3):835–843. doi: 10.1111/j.1476-5381.1988.tb11712.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Caldwell P. R., Seegal B. C., Hsu K. C., Das M., Soffer R. L. Angiotensin-converting enzyme: vascular endothelial localization. Science. 1976 Mar 12;191(4231):1050–1051. doi: 10.1126/science.175444. [DOI] [PubMed] [Google Scholar]
  7. Ciabattoni G., Cinotti G. A., Pierucci A., Simonetti B. M., Manzi M., Pugliese F., Barsotti P., Pecci G., Taggi F., Patrono C. Effects of sulindac and ibuprofen in patients with chronic glomerular disease. Evidence for the dependence of renal function on prostacyclin. N Engl J Med. 1984 Feb 2;310(5):279–283. doi: 10.1056/NEJM198402023100502. [DOI] [PubMed] [Google Scholar]
  8. Curtis J. J., Luke R. G., Whelchel J. D., Diethelm A. G., Jones P., Dustan H. P. Inhibition of angiotensin-converting enzyme in renal-transplant recipients with hypertension. N Engl J Med. 1983 Feb 17;308(7):377–381. doi: 10.1056/NEJM198302173080707. [DOI] [PubMed] [Google Scholar]
  9. Donker A. J., Brentjens J. R., van der Hem G. K., Arisz L. Treatment of the nephrotic syndrome with indomethacin. Nephron. 1978;22(4-6):374–381. doi: 10.1159/000181478. [DOI] [PubMed] [Google Scholar]
  10. Edwards R. M. Segmental effects of norepinephrine and angiotensin II on isolated renal microvessels. Am J Physiol. 1983 May;244(5):F526–F534. doi: 10.1152/ajprenal.1983.244.5.F526. [DOI] [PubMed] [Google Scholar]
  11. Flower R. J. Drugs which inhibit prostaglandin biosynthesis. Pharmacol Rev. 1974 Mar;26(1):33–67. [PubMed] [Google Scholar]
  12. Furchgott R. F., Zawadzki J. V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980 Nov 27;288(5789):373–376. doi: 10.1038/288373a0. [DOI] [PubMed] [Google Scholar]
  13. Gerritsen M. E., Cheli C. D. Arachidonic acid and prostaglandin endoperoxide metabolism in isolated rabbit and coronary microvessels and isolated and cultivated coronary microvessel endothelial cells. J Clin Invest. 1983 Nov;72(5):1658–1671. doi: 10.1172/JCI111125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gerritsen M. E., Printz M. P. Sites of prostaglandin synthesis in the bovine heart and isolated bovine coronary microvessels. Circ Res. 1981 Nov;49(5):1152–1163. doi: 10.1161/01.res.49.5.1152. [DOI] [PubMed] [Google Scholar]
  15. Goldsmith J. C., Kisker C. T. Thrombin - endothelial cell interactions: critical importance of endothelial cell vessel of origin. Thromb Res. 1982 Jan 1;25(1-2):131–136. doi: 10.1016/0049-3848(82)90222-5. [DOI] [PubMed] [Google Scholar]
  16. Griffith T. M., Edwards D. H., Davies R. L., Harrison T. J., Evans K. T. EDRF coordinates the behaviour of vascular resistance vessels. Nature. 1987 Oct 1;329(6138):442–445. doi: 10.1038/329442a0. [DOI] [PubMed] [Google Scholar]
  17. Griffith T. M., Edwards D. H., Lewis M. J., Newby A. C., Henderson A. H. The nature of endothelium-derived vascular relaxant factor. Nature. 1984 Apr 12;308(5960):645–647. doi: 10.1038/308645a0. [DOI] [PubMed] [Google Scholar]
  18. Hogan J. C., Lewis M. J., Henderson A. H. In vivo EDRF activity influences platelet function. Br J Pharmacol. 1988 Aug;94(4):1020–1022. doi: 10.1111/j.1476-5381.1988.tb11616.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hricik D. E., Browning P. J., Kopelman R., Goorno W. E., Madias N. E., Dzau V. J. Captopril-induced functional renal insufficiency in patients with bilateral renal-artery stenoses or renal-artery stenosis in a solitary kidney. N Engl J Med. 1983 Feb 17;308(7):373–376. doi: 10.1056/NEJM198302173080706. [DOI] [PubMed] [Google Scholar]
  20. Ignarro L. J., Harbison R. G., Wood K. S., Kadowitz P. J. Activation of purified soluble guanylate cyclase by endothelium-derived relaxing factor from intrapulmonary artery and vein: stimulation by acetylcholine, bradykinin and arachidonic acid. J Pharmacol Exp Ther. 1986 Jun;237(3):893–900. [PubMed] [Google Scholar]
  21. Kon V., Ichikawa I. Effector loci for renal nerve control of cortical microcirculation. Am J Physiol. 1983 Nov;245(5 Pt 1):F545–F553. doi: 10.1152/ajprenal.1983.245.5.F545. [DOI] [PubMed] [Google Scholar]
  22. Kreisberg J. I., Venkatachalam M., Troyer D. Contractile properties of cultured glomerular mesangial cells. Am J Physiol. 1985 Oct;249(4 Pt 2):F457–F463. doi: 10.1152/ajprenal.1985.249.4.F457. [DOI] [PubMed] [Google Scholar]
  23. Kuehl F. A., Jr Prostaglandins, cyclic nucleotides and cell function. Prostaglandins. 1974 Feb 25;5(4):325–340. doi: 10.1016/s0090-6980(74)80116-4. [DOI] [PubMed] [Google Scholar]
  24. MacIntyre D. E., Pearson J. D., Gordon J. L. Localisation and stimulation of prostacyclin production in vascular cells. Nature. 1978 Feb 9;271(5645):549–551. doi: 10.1038/271549a0. [DOI] [PubMed] [Google Scholar]
  25. Mené P., Dunn M. J. Modulation of mesangial cell contraction by arachidonate metabolites. Trans Assoc Am Physicians. 1986;99:125–131. [PubMed] [Google Scholar]
  26. 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]
  27. Oken D. E. Does the ultrafiltration coefficient play a key role in regulating glomerular filtration in the rat. Am J Physiol. 1989 Apr;256(4 Pt 2):F505–F515. doi: 10.1152/ajprenal.1989.256.4.F505. [DOI] [PubMed] [Google Scholar]
  28. Olesen S. P., Clapham D. E., Davies P. F. Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature. 1988 Jan 14;331(6152):168–170. doi: 10.1038/331168a0. [DOI] [PubMed] [Google Scholar]
  29. Palmer R. M., Ashton D. S., Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature. 1988 Jun 16;333(6174):664–666. doi: 10.1038/333664a0. [DOI] [PubMed] [Google Scholar]
  30. Palmer R. M., Ferrige A. G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987 Jun 11;327(6122):524–526. doi: 10.1038/327524a0. [DOI] [PubMed] [Google Scholar]
  31. Palmer R. M., Moncada S. A novel citrulline-forming enzyme implicated in the formation of nitric oxide by vascular endothelial cells. Biochem Biophys Res Commun. 1989 Jan 16;158(1):348–352. doi: 10.1016/s0006-291x(89)80219-0. [DOI] [PubMed] [Google Scholar]
  32. Rees D. D., Palmer R. M., Moncada S. Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proc Natl Acad Sci U S A. 1989 May;86(9):3375–3378. doi: 10.1073/pnas.86.9.3375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schmidt H. H., Klein M. M., Niroomand F., Böhme E. Is arginine a physiological precursor of endothelium-derived nitric oxide? Eur J Pharmacol. 1988 Mar 29;148(2):293–295. doi: 10.1016/0014-2999(88)90578-x. [DOI] [PubMed] [Google Scholar]
  34. Schnermann J., Briggs J. P., Weber P. C. Tubuloglomerular feedback, prostaglandins, and angiotensin in the autoregulation of glomerular filtration rate. Kidney Int. 1984 Jan;25(1):53–64. doi: 10.1038/ki.1984.8. [DOI] [PubMed] [Google Scholar]
  35. Schor N., Ichikawa I., Brenner B. M. Mechanisms of action of various hormones and vasoactive substances on glomerular ultrafiltration in the rat. Kidney Int. 1981 Oct;20(4):442–451. doi: 10.1038/ki.1981.160. [DOI] [PubMed] [Google Scholar]
  36. Takeda K., Meyer-Lehnert H., Kim J. K., Schrier R. W. Effect of angiotensin II on Ca2+ kinetics and contraction in cultured rat glomerular mesangial cells. Am J Physiol. 1988 Feb;254(2 Pt 2):F254–F266. doi: 10.1152/ajprenal.1988.254.2.F254. [DOI] [PubMed] [Google Scholar]
  37. Vanhoutte P. M. The endothelium--modulator of vascular smooth-muscle tone. N Engl J Med. 1988 Aug 25;319(8):512–513. doi: 10.1056/NEJM198808253190809. [DOI] [PubMed] [Google Scholar]
  38. Walshe J. J., Venuto R. C. Acute oliguric renal failure induced by indomethacin: possible mechanism. Ann Intern Med. 1979 Jul;91(1):47–49. doi: 10.7326/0003-4819-91-1-47. [DOI] [PubMed] [Google Scholar]
  39. Yanagisawa M., Kurihara H., Kimura S., Tomobe Y., Kobayashi M., Mitsui Y., Yazaki Y., Goto K., Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988 Mar 31;332(6163):411–415. doi: 10.1038/332411a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES