Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1989 Jan;83(1):84–89. doi: 10.1172/JCI113888

Vasopressin V1 receptors on the principal cells of the rabbit cortical collecting tubule. Stimulation of cytosolic free calcium and inositol phosphate production via coupling to a pertussis toxin substrate.

M A Burnatowska-Hledin 1, W S Spielman 1
PMCID: PMC303646  PMID: 2536047

Abstract

The effects of arginine vasopressin (AVP) on the cytosolic free calcium concentration ([Ca2+]f) were examined in freshly immunodissected rabbit cortical collecting tubule cells using fluorescent Ca2+ indicators fura-2 and indo-1. The addition of AVP to a cell suspension resulted in a rapid and transient increase in the [Ca2+]f. The 1-deamino-8-D-AVP (dDVP), a V2 receptor agonist of AVP that stimulated adenosine 3',5' cAMP production in these cells, had no effect on [Ca2+]f and did not affect AVP-induced increase in [Ca2+]f. The AVP-induced increase in [Ca2+]f but not cAMP production was blocked by the V1 receptor antagonist, [1-(beta-mercapto-beta-beta-cyclopentamethylene propionic acid), 2-(O-methyl)tyrosine] Arg8-vasopressin. The AVP-stimulated increase in [Ca2+]f appeared to be largely due to Ca2+ release from intracellular stores as reduction of extracellular Ca2+ with EGTA had little if any effect on the AVP-induced increase in [Ca2+]f. This AVP-induced increase in [Ca2+]f was associated with an increase in inositol-1,4,5-trisphosphate production and appeared to involve a guanine nucleotide-binding protein (G), since the pretreatment of cells with pertussis toxin for 4-6 h inhibited this effect. Finally, measurements of [Ca2+]f in single cells suggest that only the principal cells of the collecting tubules respond to AVP with an increase in [Ca2+]f. In summary, these results demonstrate that the principal cells of the cortical collecting tubule possess two distinct receptor systems for vasopressin, the well-known V2 receptor coupled to adenylate cyclase, and a V1 receptor system that leads to the mobilization of cytosolic calcium, coupled through a pertussis toxin substrate (G protein) to a production of inositol phosphates.

Full text

PDF
84

Selected References

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

  1. Ausiello D. A., Skorecki K. L., Verkman A. S., Bonventre J. V. Vasopressin signaling in kidney cells. Kidney Int. 1987 Feb;31(2):521–529. doi: 10.1038/ki.1987.31. [DOI] [PubMed] [Google Scholar]
  2. Balla T., Baukal A. J., Guillemette G., Catt K. J. Multiple pathways of inositol polyphosphate metabolism in angiotensin-stimulated adrenal glomerulosa cells. J Biol Chem. 1988 Mar 25;263(9):4083–4091. [PubMed] [Google Scholar]
  3. Berridge M. J., Dawson R. M., Downes C. P., Heslop J. P., Irvine R. F. Changes in the levels of inositol phosphates after agonist-dependent hydrolysis of membrane phosphoinositides. Biochem J. 1983 May 15;212(2):473–482. doi: 10.1042/bj2120473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berridge M. J. The molecular basis of communication within the cell. Sci Am. 1985 Oct;253(4):142–152. doi: 10.1038/scientificamerican1085-142. [DOI] [PubMed] [Google Scholar]
  5. Bonventre J. V., Skorecki K. L., Kreisberg J. I., Cheung J. Y. Vasopressin increases cytosolic free calcium concentration in glomerular mesangial cells. Am J Physiol. 1986 Jul;251(1 Pt 2):F94–102. doi: 10.1152/ajprenal.1986.251.1.F94. [DOI] [PubMed] [Google Scholar]
  6. Burnatowska-Hledin M. A., Spielman W. S. Vasopressin increases cytosolic free calcium in LLC-PK1 cells through a V1-receptor. Am J Physiol. 1987 Aug;253(2 Pt 2):F328–F332. doi: 10.1152/ajprenal.1987.253.2.F328. [DOI] [PubMed] [Google Scholar]
  7. Garcia-Perez A., Smith W. L. Use of monoclonal antibodies to isolate cortical collecting tubule cells: AVP induces PGE release. Am J Physiol. 1983 Mar;244(3):C211–C220. doi: 10.1152/ajpcell.1983.244.3.C211. [DOI] [PubMed] [Google Scholar]
  8. Grantham J. J., Burg M. B. Effect of vasopressin and cyclic AMP on permeability of isolated collecting tubules. Am J Physiol. 1966 Jul;211(1):255–259. doi: 10.1152/ajplegacy.1966.211.1.255. [DOI] [PubMed] [Google Scholar]
  9. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  10. Handler J. S., Orloff J. Antidiuretic hormone. Annu Rev Physiol. 1981;43:611–624. doi: 10.1146/annurev.ph.43.030181.003143. [DOI] [PubMed] [Google Scholar]
  11. Morel F. Sites of hormone action in the mammalian nephron. Am J Physiol. 1981 Mar;240(3):F159–F164. doi: 10.1152/ajprenal.1981.240.3.F159. [DOI] [PubMed] [Google Scholar]
  12. Nabika T., Velletri P. A., Lovenberg W., Beaven M. A. Increase in cytosolic calcium and phosphoinositide metabolism induced by angiotensin II and [Arg]vasopressin in vascular smooth muscle cells. J Biol Chem. 1985 Apr 25;260(8):4661–4670. [PubMed] [Google Scholar]
  13. Nakamura T., Ui M. Simultaneous inhibitions of inositol phospholipid breakdown, arachidonic acid release, and histamine secretion in mast cells by islet-activating protein, pertussis toxin. A possible involvement of the toxin-specific substrate in the Ca2+-mobilizing receptor-mediated biosignaling system. J Biol Chem. 1985 Mar 25;260(6):3584–3593. [PubMed] [Google Scholar]
  14. Roy C., Ausiello D. A. Characterization of (8-lysine) vasopressin binding sites on a pig kidney cell line (LLC-PK1). Evidence for hormone-induced receptor transition. J Biol Chem. 1981 Apr 10;256(7):3415–3422. [PubMed] [Google Scholar]
  15. Scharschmidt L. A., Dunn M. J. Prostaglandin synthesis by rat glomerular mesangial cells in culture. Effects of angiotensin II and arginine vasopressin. J Clin Invest. 1983 Jun;71(6):1756–1764. doi: 10.1172/JCI110931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Smith W. L., Garcia-Perez A. Immunodissection: use of monoclonal antibodies to isolate specific types of renal cells. Am J Physiol. 1985 Jan;248(1 Pt 2):F1–F7. doi: 10.1152/ajprenal.1985.248.1.F1. [DOI] [PubMed] [Google Scholar]
  17. Spielman W. S., Sonnenburg W. K., Allen M. L., Arend L. J., Gerozissis K., Smith W. L. Immunodissection and culture of rabbit cortical collecting tubule cells. Am J Physiol. 1986 Aug;251(2 Pt 2):F348–F357. doi: 10.1152/ajprenal.1986.251.2.F348. [DOI] [PubMed] [Google Scholar]
  18. Tang M. J., Weinberg J. M. Vasopressin-induced increases of cytosolic calcium in LLC-PK1 cells. Am J Physiol. 1986 Dec;251(6 Pt 2):F1090–F1095. doi: 10.1152/ajprenal.1986.251.6.F1090. [DOI] [PubMed] [Google Scholar]
  19. Troyer D. A., Kreisberg J. I., Schwertz D. W., Venkatachalam M. A. Effects of vasopressin on phosphoinositides and prostaglandin production in cultured mesangial cells. Am J Physiol. 1985 Jul;249(1 Pt 2):F139–F147. doi: 10.1152/ajprenal.1985.249.1.F139. [DOI] [PubMed] [Google Scholar]
  20. Wakelam M. J., Murphy G. J., Hruby V. J., Houslay M. D. Activation of two signal-transduction systems in hepatocytes by glucagon. Nature. 1986 Sep 4;323(6083):68–71. doi: 10.1038/323068a0. [DOI] [PubMed] [Google Scholar]
  21. Williamson J. R., Cooper R. H., Joseph S. K., Thomas A. P. Inositol trisphosphate and diacylglycerol as intracellular second messengers in liver. Am J Physiol. 1985 Mar;248(3 Pt 1):C203–C216. doi: 10.1152/ajpcell.1985.248.3.C203. [DOI] [PubMed] [Google Scholar]
  22. Wuthrich R. P., Vallotton M. B. Prostaglandin E2 and cyclic AMP response to vasopressin in renal medullary tubular cells. Am J Physiol. 1986 Sep;251(3 Pt 2):F499–F505. doi: 10.1152/ajprenal.1986.251.3.F499. [DOI] [PubMed] [Google Scholar]

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

RESOURCES