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. 1985 Sep;76(3):978–984. doi: 10.1172/JCI112098

Bradykinin-induced changes in phosphatidyl inositol turnover in cultured rabbit papillary collecting tubule cells.

J A Shayman, A R Morrison
PMCID: PMC423962  PMID: 2995453

Abstract

Rabbit renal papillary collecting tubule cells were isolated as a homogeneous population and grown in primary culture. These cells were maintained in fully defined medium to inhibit fibroblast overgrowth and to facilitate labeling of endogenous inositol phospholipids with myo-[2-3H]inositol with high specific activity. These cells demonstrated the morphology, cyclic AMP responsiveness, and prostaglandin E2 (PGE2) elaboration, consistent with previous published characterizations. When cells labeled with myo-[2-3H]inositol were stimulated by bradykinin at 10(-7) M, time-dependent and reversible changes in the distribution of inositol polyphosphates were observed. Inositol 1,4,5-triphosphate and inositol 1,4-diphosphate showed time-dependent and dose-dependent increases to maximal levels of 225 and 223% of control, respectively. These data indicate that the elaboration of inositol polyphosphates is a biochemical correlate to bradykinin stimulation and may play a role in PGE2 release in renal papillary collecting tubule cells.

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Selected References

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  1. Agranoff B. W., Murthy P., Seguin E. B. Thrombin-induced phosphodiesteratic cleavage of phosphatidylinositol bisphosphate in human platelets. J Biol Chem. 1983 Feb 25;258(4):2076–2078. [PubMed] [Google Scholar]
  2. Bell R. L., Baenziger N. L., Majerus P. W. Bradykinin-stimulated release of arachidonate from phosphatidyl inositol in mouse fibrosarcoma cells. Prostaglandins. 1980 Aug;20(2):269–274. doi: 10.1016/s0090-6980(80)80045-1. [DOI] [PubMed] [Google Scholar]
  3. Benabe J. E., Spry L. A., Morrison A. R. Effects of angiotensin II on phosphatidylinositol and polyphosphoinositide turnover in rat kidney. Mechanism of prostaglandin release. J Biol Chem. 1982 Jul 10;257(13):7430–7434. [PubMed] [Google Scholar]
  4. Berridge M. J. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem J. 1983 Jun 15;212(3):849–858. doi: 10.1042/bj2120849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burn P., Rotman A., Meyer R. K., Burger M. M. Diacylglycerol in large alpha-actinin/actin complexes and in the cytoskeleton of activated platelets. Nature. 1985 Apr 4;314(6010):469–472. doi: 10.1038/314469a0. [DOI] [PubMed] [Google Scholar]
  6. Craven P. A., DeRubertis F. R. Effects of vasopressin and urea on Ca2+-calmodulin-dependent renal prostaglandin E. Am J Physiol. 1981 Dec;241(6):F649–F658. doi: 10.1152/ajprenal.1981.241.6.F649. [DOI] [PubMed] [Google Scholar]
  7. Edwards R. M., Jackson B. A., Dousa T. P. ADH-sensitive cAMP system in papillary collecting duct: effect of osmolality and PGE2. Am J Physiol. 1981 Apr;240(4):F311–F318. doi: 10.1152/ajprenal.1981.240.4.F311. [DOI] [PubMed] [Google Scholar]
  8. Emilsson A., Sundler R. Differential activation of phosphatidylinositol deacylation and a pathway via diphosphoinositide in macrophages responding to zymosan and ionophore A23187. J Biol Chem. 1984 Mar 10;259(5):3111–3116. [PubMed] [Google Scholar]
  9. Fahey J. V., Ciosek C. P., Jr, Newcombe D. S. Human synovial fibroblasts: the relationships between cyclic AMP, bradykinin, and prostaglandins. Agents Actions. 1977 Jul;7(2):255–264. doi: 10.1007/BF01969984. [DOI] [PubMed] [Google Scholar]
  10. Garcia-Perez A., Smith W. L. Apical-basolateral membrane asymmetry in canine cortical collecting tubule cells. Bradykinin, arginine vasopressin, prostaglandin E2 interrelationships. J Clin Invest. 1984 Jul;74(1):63–74. doi: 10.1172/JCI111419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grenier F. C., Rollins T. E., Smith W. L. Kinin-induced prostaglandin synthesis by renal papillary collecting tubule cells in culture. Am J Physiol. 1981 Jul;241(1):F94–104. doi: 10.1152/ajprenal.1981.241.1.F94. [DOI] [PubMed] [Google Scholar]
  12. Hong S. L., Deykin D. The activation of phosphatidylinositol-hydrolyzing phospholipase A2 during prostaglandin synthesis in transformed mouse BALB/3T3 cells. J Biol Chem. 1981 May 25;256(10):5215–5219. [PubMed] [Google Scholar]
  13. Hong S. L., Levine L. Stimulation of prostaglandin synthesis by bradykinin and thrombin and their mechanisms of action on MC5-5 fibroblasts. J Biol Chem. 1976 Sep 25;251(18):5814–5816. [PubMed] [Google Scholar]
  14. Jefferson D. M., Cobb M. H., Gennaro J. F., Jr, Scott W. N. Transporting renal epithelium: culture in hormonally defined serum-free medium. Science. 1980 Nov 21;210(4472):912–914. doi: 10.1126/science.7434005. [DOI] [PubMed] [Google Scholar]
  15. Joseph S. K., Thomas A. P., Williams R. J., Irvine R. F., Williamson J. R. myo-Inositol 1,4,5-trisphosphate. A second messenger for the hormonal mobilization of intracellular Ca2+ in liver. J Biol Chem. 1984 Mar 10;259(5):3077–3081. [PubMed] [Google Scholar]
  16. Kolesnick R. N., Gershengorn M. C. Ca2+ ionophores affect phosphoinositide metabolism differently than thyrotropin-releasing hormone in GH3 pituitary cells. J Biol Chem. 1984 Aug 10;259(15):9514–9519. [PubMed] [Google Scholar]
  17. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  18. Lum G. M., Aisenbrey G. A., Dunn M. J., Berl T., Schrier R. W., McDonald K. M. In vivo effect of indomethacin to potentiate the renal medullary cyclic AMP response to vasopressin. J Clin Invest. 1977 Jan;59(1):8–13. doi: 10.1172/JCI108624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Manning D. C., Snyder S. H., Kachur J. F., Miller R. J., Field M. Bradykinin receptor-mediated chloride secretion in intestinal function. Nature. 1982 Sep 16;299(5880):256–259. doi: 10.1038/299256a0. [DOI] [PubMed] [Google Scholar]
  20. McGiff J. C., Itskovitz H. D., Terragno A., Wong P. Y. Modulation and mediation of the action of the renal kallikrein-kinin system by prostaglandins. Fed Proc. 1976 Feb;35(2):175–180. [PubMed] [Google Scholar]
  21. Meltzer V., Weinreb S., Bellorin-Font E., Hruska K. A. Parathyroid hormone stimulation of renal phosphoinositide metabolism is a cyclic nucleotide-independent effect. Biochim Biophys Acta. 1982 Aug 18;712(2):258–267. doi: 10.1016/0005-2760(82)90342-3. [DOI] [PubMed] [Google Scholar]
  22. Muirhead E. E., Germain G., Leach B. E., Pitcock J. A., Stephenson P., Brooks B., Brosius W. L., Daniels E. G., Hinman J. W. Production of renomedullary prostaglandins by renomedullary interstitial cells grown in tissue culture. Circ Res. 1972 Sep;31(9 Suppl):161–172. [PubMed] [Google Scholar]
  23. Omachi R. S., Robbie D. E., Handler J. S., Orloff J. Effects of ADH and other agents on cyclic AMP accumulation in toad bladder epithelium. Am J Physiol. 1974 May;226(5):1152–1157. doi: 10.1152/ajplegacy.1974.226.5.1152. [DOI] [PubMed] [Google Scholar]
  24. Pugliese F., Sato M., Williams S., Aikawa M., Hassid A., Dunn M. Rabbit and rat renal papillary collecting tubule cells in culture: the interactions of arginine vasopressin, prostaglandins, and cyclic AMP. Adv Prostaglandin Thromboxane Leukot Res. 1983;11:517–523. [PubMed] [Google Scholar]
  25. Rhodes D., Prpić V., Exton J. H., Blackmore P. F. Stimulation of phosphatidylinositol 4,5-bisphosphate hydrolysis in hepatocytes by vasopressin. J Biol Chem. 1983 Mar 10;258(5):2770–2773. [PubMed] [Google Scholar]
  26. Roscher A. A., Manganiello V. C., Jelsema C. L., Moss J. Autoregulation of bradykinin receptors and bradykinin-induced prostacyclin formation in human fibroblasts. J Clin Invest. 1984 Aug;74(2):552–558. doi: 10.1172/JCI111452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Roscher A. A., Manganiello V. C., Jelsema C. L., Moss J. Autoregulation of bradykinin receptors and bradykinin-induced prostacyclin formation in human fibroblasts. J Clin Invest. 1984 Aug;74(2):552–558. doi: 10.1172/JCI111452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schacht J. Extraction and purification of polyphosphoinositides. Methods Enzymol. 1981;72:626–631. doi: 10.1016/s0076-6879(81)72054-8. [DOI] [PubMed] [Google Scholar]
  29. Schuster V. L., Kokko J. P., Jacobson H. R. Interactions of lysyl-bradykinin and antidiuretic hormone in the rabbit cortical collecting tubule. J Clin Invest. 1984 Jun;73(6):1659–1667. doi: 10.1172/JCI111372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sheetz M. P., Febbroriello P., Koppel D. E. Triphosphoinositide increases glycoprotein lateral mobility in erythrocyte membranes. Nature. 1982 Mar 4;296(5852):91–93. doi: 10.1038/296091a0. [DOI] [PubMed] [Google Scholar]
  31. Steiner A. L., Pagliara A. S., Chase L. R., Kipnis D. M. Radioimmunoassay for cyclic nucleotides. II. Adenosine 3',5'-monophosphate and guanosine 3',5'-monophosphate in mammalian tissues and body fluids. J Biol Chem. 1972 Feb 25;247(4):1114–1120. [PubMed] [Google Scholar]
  32. Streb H., Irvine R. F., Berridge M. J., Schulz I. Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature. 1983 Nov 3;306(5938):67–69. doi: 10.1038/306067a0. [DOI] [PubMed] [Google Scholar]
  33. Tamayo J., Bellorin-Font E., Sicard G., Anderson C., Martin K. J. Desensitization to parathyroid hormone in the isolated perfused canine kidney: reversal of altered receptor-adenylate cyclase system by guanosine triphosphate in vitro. Endocrinology. 1982 Oct;111(4):1311–1317. doi: 10.1210/endo-111-4-1311. [DOI] [PubMed] [Google Scholar]
  34. Taub M., Chuman L., Saier M. H., Jr, Sato G. Growth of Madin-Darby canine kidney epithelial cell (MDCK) line in hormone-supplemented, serum-free medium. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3338–3342. doi: 10.1073/pnas.76.7.3338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Torikai S., Kurokawa K. Effect of PGE2 on vasopressin-dependent cell cAMP in isolated single nephron segments. Am J Physiol. 1983 Jul;245(1):F58–F66. doi: 10.1152/ajprenal.1983.245.1.F58. [DOI] [PubMed] [Google Scholar]
  36. Vallee R. B., DiBartolomeis M. J., Theurkauf W. E. A protein kinase bound to the projection portion of MAP 2 (microtubule-associated protein 2). J Cell Biol. 1981 Sep;90(3):568–576. doi: 10.1083/jcb.90.3.568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yandrasitz J. R., Berry G., Segal S. High-performance liquid chromatography of phospholipids with UV detection: optimization of separations on silica. J Chromatogr. 1981 Oct 9;225(2):319–328. doi: 10.1016/s0378-4347(00)80280-7. [DOI] [PubMed] [Google Scholar]
  38. Zusman R. M., Keiser H. R. Prostaglandin biosynthesis by rabbit renomedullary interstitial cells in tissue culture. Stimulation by angiotensin II, bradykinin, and arginine vasopressin. J Clin Invest. 1977 Jul;60(1):215–223. doi: 10.1172/JCI108758. [DOI] [PMC free article] [PubMed] [Google Scholar]

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