Skip to main content
SpringerLink
Log in

Atrial natriuretic peptide and angiotensin II binding sites in cerebral capillaries of spontaneously hypertensive rats

  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Summary

  1. 1.

    We carried out investigations on specific atrial natriuretic peptide (ANP) and angiotensin II (ANG) binding sites in capillaries isolated from the cerebral cortex of spontaneously hypertensive rats (SHR), an animal model of human essential hypertension, and also from Wistar Kyoto rats (WKY).

  2. 2.

    In an equilibrium binding study done in the presence of increasing concentrations of the radiolabeled ligands, the binding of125I-ratα-ANP (1–28) [ANF-(99–126)] (125I-rANP) and125I-ANG (5-l-isoleucine) (125I-ANG) to the cerebral capillaries was single and of a high affinity.

  3. 3.

    The maximum binding capacity (B max) and dissociation constant (K d) in the125I-rANP binding of 20-week-old, hypertensive SHR was significantly lower than in age-matched, normotensive WKY. Conversely, a significant increase in theB max of125I-ANG binding of adult SHR was observed, with a significant decrease in theK d.

  4. 4.

    There was no differences in theB max of125I-rANP and125I-ANG binding between 4-week-old, prehypertensive SHR and age-matched WKY. However, there was a significant decrease in theK d of125I-rANP binding of SHR.

  5. 5.

    As a dramatic change in the binding kinetics of125I-rANP and125I-ANG was noted in the cerebral capillaries of adult sustained-hypertensive SHR, the possibility that ANP and ANG play a role in the etiology of dysfunction of the blood-brain barrier complicated with hypertension, by interacting with specific receptors, would have to be considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aguilera, G., and Catt, K. (1981). Regulation of vascular angiotensin II receptors in the rat during altered sodium intake.Circ. Res. 49751–758.

    Google Scholar 

  • Berk, B. C., Aronow, M. S., Brock, T. A., Cragoe, E., Jr., Gimbrone, M. A., Jr., and Alexander, R. W. (1987). Angiotensin II-stimulated Na+/H+ exchange in cultured vascular smooth muscle cells. Evidence for protein kinase C-dependent and -independent pathways.J. Biol. Chem. 2625057–5064.

    Google Scholar 

  • Betz, A. L. (1986). Transport of ions across the blood-brain barrier.Fed. Proc. 452050–2054.

    Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Anal. Biochem. 72248–254.

    Google Scholar 

  • Brendel, K., Meezan, E., and Carlson, E. C. (1974). Isolated brain microvessels: A purified, metabolically active preparation from bovine cerebral cortex.Science 185953–955.

    Google Scholar 

  • Cantiello, H. F., and Ausiello, D. A. (1986). Atrial natriuretic factor and cGMP inhibit amiloride-sensitive Na+ transport in the cultured renal epithelial cell line, LLC-PK1.Biochem. Biophys. Res. Commun. 134852–860.

    Google Scholar 

  • Chabrier, P. E., Roubert, P., and Braquet, P. (1987). Specific binding of atrial natriuretic factor in brain microvessels.Proc. Natl. Acad. Sci. USA 842078–2081.

    Google Scholar 

  • De Léan, A. (1986). Amiloride potentiates atrial natriuretic factor inhibitory action by increasing receptor binding in bovine adrenal zona glomerulosa.Life Sci. 391109–1116.

    Google Scholar 

  • Feig, P. U., D'Occhio, M. A., and Boylan, J. W. (1987). Lymphocyte membrane sodium-proton exchange in spontaneously hypertensive rats.Hypertension 9282–288.

    Google Scholar 

  • Grubb, R. L., Jr., and Raichle, M. E. (1981). Intraventricular angiotensin II increases brain vascular permeability.Brain Res. 210426–430.

    Google Scholar 

  • Gutkind, J. S., Kurihara, M., Castrén, E., and Saavedra, J. M. (1987). Atrial natriuretic peptide receptors in sympathetic ganglia: Biochemical response and alterations in genetically hypertensive rats.Biochem. Biophys. Res. Commun. 14965–72.

    Google Scholar 

  • Gutkowska, J., Horky, K., Lachance, C., Racz, K., Garcia, R., Thibault, G., Kuchel, O., Genest, J., and Cantin M. (1986). Atrial natriuretic factor in spontaneously hypertensive rats.Hypertension 8 (Suppl. I):I-137–I-140.

    Google Scholar 

  • Harik, S. I., Sharma, V. K., Wetherbee, J. R., Warren, R. H., and Banerjee, S. P. (1981). Adrenergic and cholinergic receptors of cerebral microvessels.J. Cereb. Blood Flow Metabol. 1329–338.

    Google Scholar 

  • Harik, S. I., Doull, G. H., and Dick, A. P. K. (1985). Specific ouabain binding to brain microvessels and choroid plexus.J. Cereb. Blood Flow Metabol. 5156–160.

    Google Scholar 

  • Hirata, Y., Tomita, M., Takada, S., and Yoshimi, H. (1985). Vascular receptor binding activities and cyclic GMP responses by synthetic human and rat atrial natriuretic peptides (ANP) and receptor down-regulation by ANP.Biochem. Biophys. Res. Commun. 128538–546.

    Google Scholar 

  • Imada, T., Takayanagi, R., and Inagami, T. (1985). Changes in the content of atrial natriuretic factor with the progression of hypertension in spontaneously hypertensive rats.Biochem. Biophys. Res. Commun. 133759–765.

    Google Scholar 

  • Johansson, B. B., and Martinsson, L. (1980). The blood-brain barrier in adrenaline-induced hypertension. Circadian variations and modification by beta-adrenoreceptor antagonists.Acta Neurol. Scand. 6296–102.

    Google Scholar 

  • Kobayashi, H., Memo, M., Spano, P. F., and Trabucchi, M. (1981). Identification ofβ-adrenergic receptor binding sites in rat brain microvessels, using [125I]iodohydroxybenzylpindolol.J. Neurochem. 361383–1388.

    Google Scholar 

  • Kobayashi, H., Take, K., Wada, A., Izumi, F., and Magnoni, M. S. (1984). Angiotensin-converting enzyme activity is reduced in brain microvessels of spontaneously hypertensive rats.J. Neurochem. 421655–1658.

    Google Scholar 

  • Kobayashi, H., Wada, A., Izumi, F., Take, K., and Magnoni, M. S. (1985a). Low activity of angiotensin-converting enzyme in cerebral microvessels of young spontaneously hypertensive rats.J. Neurochem. 441318–1320.

    Google Scholar 

  • Kobayashi, H., Wada, A., Izumi, F., Magnoni, M. S., and Trabucchi, M. (1985b).α-Adrenergic receptors in cerebral microvessels of normotensive and spontaneously hypertensive rats.Circ. Res. 56402–409.

    Google Scholar 

  • Kurihara, M. Castrén, E., Gutkind, J. S., and Saavedra J. M. (1987). Lower number of atrial natriuretic peptide receptors in thymocytes and spleen cells of spontaneously hypertensive rats.Biochem. Biophys. Res. Commun. 1491132–1140.

    Google Scholar 

  • Leitman, D. C., Andresen, J. W., Kuno, T., Kamisaki, Y., Chang, J., and Murad, F. (1986). Identification of multiple binding sites for atrial natriuretic factor by affinity cross-linking in cultured endothelial cells.J. Biol. Chem. 26111650–11655.

    Google Scholar 

  • Lynch, D. R., Braas, K. M., and Snyder, S. H. (1986). Atrial natriuretic factor receptors in rat kidney, adrenal gland, and brain: Autoradiographic localization and fluid balance dependent changes.Proc. Natl. Acad. Sci. USA 833357–3361.

    Google Scholar 

  • Magnoni, M. S., Kobayashi, H., Cazzaniga, A., Izumi, F., Spano, P. F., and Trabucchi, M. (1983). Hypertension reduces the number of beta-adrenergic receptors in rat brain microvessels.Circulation 67610–613.

    Google Scholar 

  • Majack, R. A., and Bhalla R. C. (1981). Ultrastructural characteristics of endothelial permeability pathways in chronic hypertension.Hypertension 3586–595.

    Google Scholar 

  • Meloche, S., Ong, H., and De Léan, A. (1987). Functional heterogeneity of atrial natriuretic factor receptor in bovine adrenal zona glomerulosa is explained by an amiloride-sensitive high affinity molecular complex.J. Biol. Chem. 26210252–10258.

    Google Scholar 

  • Mueller, S. M., and Heistad, D. D. (1980). Effect of chronic hypertension on the blood-brain barrier.Hypertension 2809–812.

    Google Scholar 

  • Munson, P. J., and Rodbard, D. (1980). LIGAND: A versatile computerized approach for characterization of ligand-binding systems.Anal. Biochem. 107220–239.

    Google Scholar 

  • Naftalin, L., Child, V. J., and Morley, D. A. (1969). Observations on the site of origin of serum gamma-glutamyl transpeptidase.Clin. Chim. Acta 26293–296.

    Google Scholar 

  • Nag, S. (1984). Cerebral endothelial surface charge in hypertension.Acta Neuropathol. 63276–281.

    Google Scholar 

  • Niwa, M., Ibaragi, M., Tsutsumi, K., Kurihara, M., Himeno, A., Mori, K., and Ozaki, M. (1988). Specific atrial natriuretic peptide binding sites in rat cerebral capillaries.Neurosci. Lett. 9189–94.

    Google Scholar 

  • Ogura, T., Mitsui, T., Yamamoto, I., Katayama, E., Ota, Z., and Ogawa, N. (1987). Differential changes in atrial natriuretic peptide and vasopressin receptor binding in kidney of spontaneously hypertensive rat.Life Sci. 40233–238.

    Google Scholar 

  • Okamoto, K. (1972).Spontaneous Hypertension. Its Pathogenesis and Complications, Igaku Shoin, Tokyo, pp. 1–126.

    Google Scholar 

  • Pandey, K. N., Inagami, T., and Misono, K. S. (1987). Three distinct forms of atrial natriuretic factor receptors: Kidney tubular epithelium cells and vascular smooth muscle cells contain different types of receptors.Biochem. Biophys. Res. Commun. 1471146–1152.

    Google Scholar 

  • Saavedra, J. M. (1987a). Regulation of atrial natriuretic peptide receptors in the rat brain.Cell. Mol. Neurobiol. 7151–173.

    Google Scholar 

  • Saavedra, J. M., Correa, F. M. A., Plunkett, L. M., Israel, A., Kurihara, M., and Shigematsu, K. (1986a). Binding of angiotensin and atrial natriuretic peptide in brain of hypertensive rats.Nature 320758–760.

    Google Scholar 

  • Saavedra, J. M., Kurihara, M., and Israel, A. (1986b). Alterations in angiotensin and atrial natriuretic peptide receptors in brain nuclei of spontaneously hypertensive rats.J. Hypertens. 4 (Suppl. 6):395–397.

    Google Scholar 

  • Saavedra, J. M., Israel, A., Kurihara, M., and Fuchs, E. (1986c). Decreased number and affinity of rat atrial natriuretic peptide (6-33) binding sites in the subfornical organ of spontaneously hypertensive rats.Circ. Res. 58389–392.

    Google Scholar 

  • Saavedra, J. M., Israel, A., and Kurihara, M. (1987b). Increased atrial natriuretic peptide binding sites in the rat subfornical organ after water deprivation.Endocrinology 120426–428.

    Google Scholar 

  • Saito, H., Inui, K., Matsukawa, Y., Okano, T., Maegawa, H., Nakao, K., Morii, N., Imura, H., Makino, S., and Hori, R. (1986). Specific binding of atrial natriuretic polypeptide to renal basolateral membranes in spontaneously hypertensive rats (SHR) and stroke-prone SHR.Biochem. Biophys. Res. Commun. 1371079–1085.

    Google Scholar 

  • Saitta, M. N., Hannaert, P. A., Rosati, C., Meyer. P., and Garay, R. P. (1987). A kinetic analysis of inward Na+, K+ cotransport in erythrocytes from spontaneously hypertensive rats.J. Hypertens. 5 (Suppl. 5): 285–286.

    Google Scholar 

  • Schiffrin, E. L., and St-Louis, J. (1987). Decreased density of vascular receptors for atrial natriuretic peptide in DOCA-salt hypertensive rats.Hypertension 9504–512.

    Google Scholar 

  • Schiffrin, E. L., Poissant, L., Cantin, M., and Thibault, G. (1986). Receptors for atrial natriuretic factor in cultured vascular smooth muscle cells.Life Sci. 38817–826.

    Google Scholar 

  • Speth, R. C., and Harik, S. I. (1985). Angiotensin II receptor binding sites in brain microvessels.Proc. Natl. Acad. Sci. USA 826340–6343.

    Google Scholar 

  • Speth, R. C., Singh, R., Smeby, R. R. Ferrario, C. M., and Husain, A. (1984). Restricted dietary sodium intake alters peripheral but not central angiotensin II receptors.Neuroendorcrinology 38387–392.

    Google Scholar 

  • Steardo, L., and Nathanson, J. A. (1987). Brain barrier tissues: End organs for atriopeptins.Science 235470–473.

    Google Scholar 

  • Swithers, S. E., Stewart, R. E., and McCarty, R. (1987). Binding sites for atrial natriuretic factor (ANF) in kidneys and adrenal glands of spontaneously hypertensive (SHR) rats.Life Sci. 401673–1681.

    Google Scholar 

  • Takayanagi, R., Imada, T., Grammer, R. T., Misono, K. S., Naruse, M., and Inagami, T. (1986a). Atrial natriuretic factor in spontaneously hypertensive rats: Concentration changes with the progression of hypertension and elevated formation of cyclic GMP.J. Hypertens. 4 (Suppl. 3):303–307.

    Google Scholar 

  • Takayanagi, R., Grammer, R. T., and Inagami, T. (1986b). Regional increase of cyclic GMP by atrial natriuretic factor in rat brain: Markedly elevated response in spontaneously hypertensive rats.Lief Sci. 39573–580.

    Google Scholar 

  • Tokushige, A., Kino, M., Tamura, H., Hopp, L., Searle, B. W., and Aviv, A. (1986). Bumetanide-sensitive sodium-22 transport in vascular smooth muscle cell of the spontaneously hypertensive rat.Hypertension 8379–385.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology 2, Nagasaki University School of Medicine, 852, Nagasaki, Japan

    Masa-aki Ibaragi & Masami Niwa

Authors
  1. Masa-aki Ibaragi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masami Niwa
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ibaragi, Ma., Niwa, M. Atrial natriuretic peptide and angiotensin II binding sites in cerebral capillaries of spontaneously hypertensive rats. Cell Mol Neurobiol 9, 221–231 (1989). https://doi.org/10.1007/BF00713030

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00713030

Key words

Search

Navigation