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Angiotensin II directly increases rabbit renal brush-border membrane sodium transport: Presence of local signal transduction system

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Summary

In the present study, we have examined the direct actions of angiotensin II (AII) in rabbit renal brush border membrane (BBM) where binding sites for AII exist. Addition of AII (10−11–10−7 m) was found to stimulate22Na uptake by the isolated BBM vesicles directly. AII did not affect the Na+-dependent BBM glucose uptake, and the effect of AII on BBM22Na+ uptake was inhibited by amiloride, suggesting the involvement of Na+/H+ exchange mechanism. BBM proton permeability as assessed by acridine orange quenching was not affected by AII, indicating the direct effect of AII on Na+/H+ antiport system.

In search of the signal transduction mechanism, it was found that AII activated BBM phospholipase A2 (PLA) and that BBM contains a 42-kDa guanine nucleotide-binding regulatory protein (G-protein) that underwent pertussis toxin (PTX)-catalyzed ADP-ribosylation. Addition of GTP potentiated, while GDP-ßS or PTX abolished, the effects of AII on BBM PLA and22Na+ uptake, suggesting the involvement of G-protein in AII's actions. On the other hand, inhibition of PLA by mepacrine prevented AII's effect on BBM22Na+ uptake, and activation of PLA by mellitin or addition of arachidonic acid similarly enhanced BBM22Na+ uptake, suggesting the role of PLA activation in mediating AII's effect on BBM22Na+ uptake.

In summary, results of the present study show a direct stimulatory effect of AII on BBM Na+/H+ antiport system, and suggest the presence of a local signal transduction system involving G-protein mediated PLA activation.

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References

  1. Aronson, P.S., Sacktor, B. 1975. The Na gradient-dependent transport ofd-glucose in renal brush border membrane vesicles.J. Biol. Chem. 250:6032–6039

    Google Scholar 

  2. Berridge, M.J., Downes, C.P., Hanley, M.R. 1982. Lithium amplifies agonist-dependent phosphatidyl inositol responses in brain and salivary glands.Biochem. J. 206:587–595

    Google Scholar 

  3. Biber, J., Stieger, B., Haase, W., Murer, H. 1981. A high yield preparation for rat kidney brush border membranes. Different behavior of lysosomal markers.Biochim. Biophys. Acta 772:140–148

    Google Scholar 

  4. Brown, G.P., Douglas, J.G. 1982. Angiotensin II binding sites on isolated rat renal brush border membranes.Endocrinology 111:1830–1836

    Google Scholar 

  5. Brown, G.P., Douglas, J.G. 1987. Influence of transmembrane potential differences of renal tubular cell on ANG II binding.Am. J. Physiol. 252:F209-F214

    Google Scholar 

  6. Dominquez, J.H., Snowdowne, K.W., Freudenrich, C.C., Brown, T., Borle, A.B. 1987. Intracellular messenger for action of angiotensin II on fluid transport in rabbit proximal tubule.Am. J. Physiol. 252:F423-F309

    Google Scholar 

  7. Douglas, J.G. 1987. Angiotensin receptor subtypes of the kidney cortex.Am. J. Physiol. 253:F1-F7

    Google Scholar 

  8. Felder, C.C., Blecher, M., Jose, P.A. 1989. Dopamine-1-mediated stimulation of phospholipase C activity in rat renal cortical membranes.J. Biol. Chem. 264:8739–8745

    Google Scholar 

  9. Folch, J., Lees, M., Stanley, G.H. 1957. A simple method for the isolation and purification of total lipids from animal tissues.J. Biol. Chem. 226:497–509

    Google Scholar 

  10. Gesek, F.A., Schoolwerth, A.C. 1990. Hormonal interactions with the proximal Na−H+ exchanger.Am. J. Physiol. 258:F514-F521

    Google Scholar 

  11. Harris, P.J. 1979. Stimulation of proximal tubular sodium reabsorption by ile5 angiotensin II in the rat kidney.Pfluegers Arch. 381:83–85

    Google Scholar 

  12. Harris, P.J., Navar, L.G. 1985. Tubular transport response to angiotensin.Am. J. Physiol. 248:F621-F630

    Google Scholar 

  13. Harris, P.J., Young, J.A. 1977. Dose-dependent stimulation and inhibition of proximal tubular sodium reabsorption by angiotensin II in the rat kidney.Pfluegers Arch. 367:295–297

    Google Scholar 

  14. Hubscher, G., West, G.R. 1965. Specific assays of some phosphotase in subcellular fractions of small intestinal mucosa.Nature (London) 205:799–800

    Google Scholar 

  15. Ingelfinger, J.R., Zuo, W.M., Fon, E.A., Ellison, K.E., Dzau, V.J. 1990. In situ hybridization evidence for angiotensinogen messenger RNA in the rat proximal tubule.J. Clin. Invest. 85:417–423

    Google Scholar 

  16. Jacquez, J.A. 1978. Tracers in the study of membrane processes.In: Membrane Physiology. T.E. Andreoli, J.F. Hoffman, and D.D. Fanestil, editors. pp. 157–159. Plenum, New York

    Google Scholar 

  17. Lansing, A.K., Belkhode, M.L., Lynch, W.E., Lieberman, I. 1967. Enzymes of plasma membranes of liver.J. Biol. chem. 242:1772–1775

    Google Scholar 

  18. Liu, F.Y., Cogan, M.G. 1987. A potent regulator of acidification in the rat early proximal convoluted tubule.J. Clin. Invest. 80:272–275

    Google Scholar 

  19. Liu, F.Y., Cogan, M.G. 1988. Angiotensin II stimulation of hydrogen ion secretion in the rat early proximal tubule.J. Clin. Invest. 82:601–607

    Google Scholar 

  20. Liu, F.Y., Cogan, M.G. 1989. Angiotensin II stimulates early proximal bicarbonate absorption in the rat by decreasing cyclic adenosine monophosphate.J. Clin. Invest. 84:83–91

    Google Scholar 

  21. Marinetti, G.V. 1962. Chromatographic separation, identification and analysis of phospholipids.J. Lipid Res. 3:1–20

    Google Scholar 

  22. Mujais, S.K., Kauffman, S., Katz, A.I. 1986. Angiotensin II binding sites in individual segments of the rat nephron.J. Clin. Invest. 77:315–318

    Google Scholar 

  23. Nijssen, J.G., Roosenboom, C.F.P., Van den Bosch, H. 1986. Identification of a calcium-independent phospholipase A2 in rat lung cytosol and differentiation from acetylhydrolase for PAF-acether.Biochim. Biophys. Acta 876:611–618

    Google Scholar 

  24. Norman, J., Dezfooly, B.B., Nord, E.P., Kurtz, I., Schlosser, J., Chaudhari, A., Fine, L.G. 1987. EGF-induced mitogenesis in proximal tubular cells: Potentiation by angiotensin II.Am. J. Physiol. 253:F299-F309

    Google Scholar 

  25. Peterson, D.R., Charbaszcz, G., Peterson, W.R., Oparil, S. 1979. Mechanism for renal tubular handling of angiotensin.Am. J. Physiol. 236:F365-F372

    Google Scholar 

  26. Pind, S., Kuksis, A. 1987. Isolation of purified brush border membranes from rat jejunum containing a Ca-independent phospholipase A2 activity.Biochim. Biophys. Acta 901:78–87

    Google Scholar 

  27. Quingley, J.P., Gotterer, G.S. 1969. Distribution of (Na+K)-stimulated ATPase activity in rat intestinal mucosa.Biochim. Biophys. Acta 173:456–468

    Google Scholar 

  28. Rabon, E., Chang, H., Sachs, G. 1978. Quantitation of hydrogen ion and potential gradients in gastric plasma membrane vesicles.Biochemistry 17:3345–3353

    Google Scholar 

  29. Rajaraman, S., Graves, K., Kunapuli, S. 1988. Identification of the sites of synthesis of angiotensin and renin in the kidney.Kidney Int. 33:169A

    Google Scholar 

  30. Saccomani, G., Mitchell, K.D., Navar, L.G. 1990. Angiotensin II stimulation of Na+−H+ exchange in proximal tubule cells.Am. J. Physiol. 258:F1188-F1195

    Google Scholar 

  31. Schlondorff, D., DeCandido, S., Satriano, J.A. 1987. Angiotensin II stimulates phospholipase C and A2 in cultured rat messangial cells.Am. J. Physiol. 253:C113-C120

    Google Scholar 

  32. Schuster, V.L., Kokko, J.P., Jacobson, H.R. 1984. Angiotensin II directly stimulates sodium transport in rabbit proximal convoluted tubules.J. Clin. Invest. 73:507–515

    Google Scholar 

  33. Sedmak, J.J., Grossberg, S.E. 1977. A rapid, sensitive and versatile assay for protein using Coomassie Brilliant blue G250.Anal. Biochem. 79:544–552

    Google Scholar 

  34. Seikaly, M.G., Arant, B.S., Seney, F.D. 1990. Endogenous angiotensin concentrations in specific intrarenal fluid compartments of the rat.J. Clin. Invest. 86:1352–1357

    Google Scholar 

  35. Welsh, C., Dubyak, J.G., Douglas, J.G. 1988. Relationship between phospholipase C activation and prostaglandin E2 and cyclic adenosine monophosphate production in rabbit tubular epithelial cells. Effects of angiotensin, bradykinin, and arginine vasopressin.J. Clin. Invest. 81:710–719

    Google Scholar 

  36. Wharton, D.C., Tzgoloff, A. 1967. Cytochrome oxidase from beef heart mitochondria.Methods Enzymol. 10:245–250

    Google Scholar 

  37. Wolf, R.A., Gross, R.W. 1985. Identification of neutral active phospholipase C which hydrolyzes choline glycerophospholipids and plasmalogen selective phospholipase A2 in canine myocardium.J. Biol. Chem. 260:7295–7303

    Google Scholar 

  38. Woodcock, E.A., Johnston, C.I. 1982. Inhibition of adenylate cyclase by angiotensin II in rat renal cortex.Endocrinology 111:1687–1691

    Google Scholar 

  39. Yanagawa, N., Capparelli, A.W., Jo, O.D., Friedal, A., Barrett, J.D., Eggena, P. 1991. Production of angiotensinogen and renin-like activity by rabbit proximal tubular cells in culture.Kidney Int. (in press)

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Morduchowicz, G.A., Sheikh-Hamad, D., Dwyer, B.E. et al. Angiotensin II directly increases rabbit renal brush-border membrane sodium transport: Presence of local signal transduction system. J. Membrain Biol. 122, 43–53 (1991). https://doi.org/10.1007/BF01872738

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  • DOI: https://doi.org/10.1007/BF01872738

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