Skip to main content

The Biosynthesis and Actions of Prostaglandins in the Renal Collecting Tubule and Thick Ascending Limb

  • Chapter

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 259))

Abstract

The intent of this review is to describe our current perceptions of the biosynthesis and function of prostaglandins in the renal collecting tubule and thick ascending limb of Henle’s loop. Although the presentation will have a biochemical bias, we have attempted to couch our discussion in the context of the regulation of water reabsorption by the kidney. Specifically, our goal will be to summarize the data that support the model depicted in Fig. 1.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. M.J. Dunn, J.F. Liard, F. Dray, Basal and stimulated rates of renal secretion and excretion of prostaglandins E2, Fα, and 13, 14- dihy-dro-15-keto Fα in the dog, Kidney Int. 13:136–143 (1978).

    Article  CAS  Google Scholar 

  2. S.H. Ferreira and J.R. Vane, Prostaglandins: their disappearance from and release into the circulation, Nature 216:868–873 (1967).

    Article  PubMed  CAS  Google Scholar 

  3. W.L. Smith, Cellular and subcellular compartmentalization of prostaglandin and thromboxane synthesis, in: “Biochemistry of Arachidonic Acid Metabolism,” W.E.M. Lands, ed., Martinus Nijhoff, Boston, pp. 79–93 (1985).

    Google Scholar 

  4. J.B. Lee, K. Crowshaw, B.H. Takman, K.A. Attrep, The identification of prostaglandins E2, F and A2 from rabbit kidney medulla, Biochem. J. 105:1251–1260 (1967).

    PubMed  CAS  Google Scholar 

  5. E.G. Daniels, J.W. Hinman, B.E. Leach and E.E. Muirhead, Identification of prostaglandin E2 as the principal vasodepressor lipid of rabbit renal medulla, Nature 215:1298–1299 (1967).

    Article  PubMed  CAS  Google Scholar 

  6. M. Hamberg, Biosynthesis of prostaglandins in the renal medulla of rabbit, FEBS Lett. 5:127–130 (1969).

    Article  PubMed  CAS  Google Scholar 

  7. K. Crowshaw, Prostaglandin biosynthesis from endogenous precursors in rabbit kidney, Nature New Biol. 231:240–242 (1971).

    PubMed  CAS  Google Scholar 

  8. J.B. Lee, Renal homeostasis and the hypertensive state: a unifying hypothesis, in: “The Prostaglandins,” Vol. I, P.W. Ramwell, ed., Plenum Press, New York, pp. 133–187 (1973).

    Chapter  Google Scholar 

  9. M.J. Dunn and V.L. Hood, Prostaglandins and the kidney, Am. J. Physiol. 233:F169–F184 (1977).

    CAS  Google Scholar 

  10. E.E. Muirhead, G.B. Brown, G.S. Germain, B.E. Leach, The renal medulla as an antihypertensive organ, J. Lab. Clin. Invest. 76:641–649 (1970).

    CAS  Google Scholar 

  11. A.R. Whorton, M. Smigel, J.A. Oates, J.C. Frohlich, Regional differences in prostaglandin formation by the kidney: prostacyclin is a major prostaglandin of the renal cortex, Biochem. Biophys. Acta 529:176–180 (1978).

    Article  PubMed  CAS  Google Scholar 

  12. W.L. Smith, D.L. DeWitt, M.L. Allen, Bimodal distribution of the prostaglandin I2 synthase antigen in smooth muscle cells, J. Biol. Chem. 258:5922–5926 (1983).

    PubMed  CAS  Google Scholar 

  13. J.C. McGiff, Interactions of renal prostaglandins with the renin-angiotensin and kallekrein-kinin systems, in: “Prostaglandins in Cardiovascular and Renal Function,” A. Scriabine, A.M. Lefer, and F.A. Kuehl, Jr., eds., Spectrum Publications, New York, pp. 387–398 (1980).

    Google Scholar 

  14. F.H.A. Janszen and A.H. Nugteren, A histochemical study of the prostaglandin biosynthesis in the urinary system of rabbit, guinea pig, goldhamster and rat, in: “Advances in the Biosciences,” S. Bergstrom, ed., Pergamon, New York, pp. 287–292 (1973).

    Google Scholar 

  15. W.L. Smith and G.P. Wilkin, Immunochemistry of prostaglandin endoperoxide-forming cyclooxygenase: the detection of the cycloooxygenase in rat, rabbit and guinea pig kidneys by immunofluorescence, Prostaglandins 13:873–892 (1977).

    PubMed  CAS  Google Scholar 

  16. W.L. Smith and T.G. Bell, Immunohistochemical localization of the prostaglandin- forming cyclooxygenase in renal cortex, Am. J. Physiol. 235: F451–F457 (1978).

    PubMed  CAS  Google Scholar 

  17. W.L. Smith, F.C. Grenier, T.G. Bell, G.P. Wilkin, Cellular distribution of enzymes involved in prostaglandin metabolism in the mammalian kidney, in: “Prostaglandins in Cardiovascular and Renal Function,” A. Scriabine, A.M. Lefer and F.A. Kuehl, Jr., eds., Spectrum Publications, New York, pp. 71–91 (1980).

    Google Scholar 

  18. W.L. Smith, F.C. Grenier, D.L. DeWitt, A. Garcia-Perez, T.G. Bell, Cellular compartmentalization of the biosynthesis and function of PGE2 and PGI2 in the renal medulla, in: “Prostaglandins and the Kidney,” M.J. Dunn and C. Patrono, eds., Plenum Publishing Co., New York, pp. 27–39 (1983).

    Chapter  Google Scholar 

  19. M. Hemler, W.E.M. Lands, W.L. Smith, Purification of the cyclooxygenase that forms prostaglandins. Demonstration of two forms of iron in the holoenzyme, J. Biol. Chem. 251:5575–5579 (1976).

    PubMed  CAS  Google Scholar 

  20. M.G. Currie and P. Needleman, Renal arachidonic acid metabolism, Ann. Rev. Physiol. 46:327–341 (1984).

    Article  CAS  Google Scholar 

  21. N. Farman, P. Pradelles, J.P. Bonvalet, Determination of prostaglandin E2 synthesis along rabbit nephron by enzyme immunoassay, Am. J. Physiol. 251:F238–F244 (1986).

    PubMed  CAS  Google Scholar 

  22. M.A. Kirschenbaum, A.G. Lowe, W. Trizna, L.G. Fine, Regulation of vasopressin action by prostaglandins, J. Clin. Invest. 70:1193–1204 (1982).

    Article  PubMed  CAS  Google Scholar 

  23. D. Schlondorff, J.A. Satriano, V.W. Folkert, J. Eveloff, Prostaglandin synthesis by isolated collecting tubules from adult and neonatal rabbits, Am. J. Physiol. 248:F134–F144 (1985).

    PubMed  CAS  Google Scholar 

  24. F.C. Grenier and W.L. Smith, Formation of 6-keto-PGF by collecting tubule cells isolated from rabbit renal papillae, Prostaglandins 16: 759–772 (1978).

    CAS  Google Scholar 

  25. D. Schlondorff, R. Zanger, J.A. Satriano, V.W. Folkert, J. Eveloff, Prostaglandin synthesis by isolated cells from the outer medulla and from the thick ascending loop of Henle of rabbit kidney, J. Pharmacol. Exp. Therap. 223:120–124 (1982).

    CAS  Google Scholar 

  26. J. Sraer, J. Foidart, D. Chansel, P. Mahieu, B. Kourznetzova, R. Ardaillou, Prostaglandin synthesis by mesangial and epithelial glomerular cultured cells, FEBS Lett. 104:420–424 (1979).

    Article  PubMed  CAS  Google Scholar 

  27. M.L. Allen, W.K. Sonnenburg, M. Bumatowska-Hieden, W.S. Spielman, W.L. Smith, Immunodissection of cortical and medullary thick ascending limb cells from rabbit kidney, Am. J. Physiol, submitted.

    Google Scholar 

  28. A. Hassid, M. Konieczkowski, M. Dunn, Prostaglandin synthesis in isolated glomeruli, Proc. Nat. Acad. Sci. U.S.A. 76:1155–1159 (1979).

    Article  CAS  Google Scholar 

  29. F.C. Grenier and W.L. Smith, Formation of 6-keto-PGF by collecting tubule cells isolated from rabbit renal papillae, Prostaglandins 16:759–772 (1978).

    CAS  Google Scholar 

  30. F.C. Grenier, T.E. Rollins, W.L. Smith, Kinin-induced prostaglandin synthesis by renal papillary collecting tubule cells in culture, Am. J. Physiol. 241:F94–F104 (1981).

    PubMed  CAS  Google Scholar 

  31. Y. Tanaka, S.L. Ward, W.L. Smith, Immunochemical and kinetic evidence for two different prostaglandin H-prostaglandin E isomerases in sheep vesicular gland microsomes, J. Biol. Chem. 262:1374–1381 (1987).

    PubMed  CAS  Google Scholar 

  32. A.J. Marcus, B.B. Weksler, E.A. Jaffe, M.J. Broekman, Synthesis of prostacyclin from platelet-derived endoperoxide by cultured human endothelial cells, J. Clin. Invest. 66:979–983 (1980).

    Article  PubMed  CAS  Google Scholar 

  33. J.B. Stokes, Integrated actions of renal medullary prostaglandins in the control of water excretion, Am. J. Physiol. 240:F471–F480 (1981).

    PubMed  CAS  Google Scholar 

  34. V.L. Schuster, J.P. Kokko, H.R. Jacobson, Interactions of lysyl-bradykinin and anti-diuretic hormone in the rabbit cortical collecting tubule, J. Clin. Invest. 73:1659–1669 (1984).

    Article  PubMed  CAS  Google Scholar 

  35. A. Garcia-Perez and W.L. Smith, Use of monoclonal antibodies to isolate cortical collecting tubule cells: AVP induces PGE release, Am. J. Physiol. 244:C211–C220 (1983).

    PubMed  CAS  Google Scholar 

  36. A. Garcia-Perez and W.L. Smith, Apical-basolateral membrane asymmetry in canine cortical collecting tubule cells: bradykinin, arginine vasopressin, prostaglandin E2 interrelationships, J. Clin. Invest. 74: 63–74 (1984).

    Article  PubMed  CAS  Google Scholar 

  37. M. Sato and M.J. Dunn, Interactions of vasopressin, prostaglandins, and cAMP in rat renal papillary collecting tubule cells in culture, Am. J. Physiol. 247:F423–F433 (1984).

    PubMed  CAS  Google Scholar 

  38. W.S. Spielman, W.K. Sonnenburg, M.L. Allen, L.J. Arend, K. Gerozissis, W.L. Smith, Immunodissection and culture of rabbit cortical collecting tubule cells, Am. J. Physiol. 251:F348–F357 (1986).

    PubMed  CAS  Google Scholar 

  39. J.L. Stokes, Modulation of vasopressin-induced water permeability of the cortical collecting tubule by endogenous and exogenous prostaglandins, Mineral Electrolyte Metab. 11:240–248 (1985).

    CAS  Google Scholar 

  40. A.W. Cuthbert, P.V. Halushka, H.S. Margolius, J.A. Spayne, Mediators of the secretory response to kinins, Br. J. Pharmacol. 82:597–607 (1984).

    Article  PubMed  CAS  Google Scholar 

  41. W.L. Smith, Prostaglandin biosynthesis and its compartmentalization in vascular smooth muscle and endothelial cells, Ann. Rev. Physiol. 48: 251–262 (1986).

    Article  CAS  Google Scholar 

  42. L.A. Bito and R.A. Baroody, Impermeability of rabbit erythrocytes to prostaglandins, Am. J. Physiol. 229:1580–1584 (1975).

    PubMed  CAS  Google Scholar 

  43. J.J. Irish, Secretion of prostaglandin E2 by rabbit proximal tubules, Am. J. Physiol. 237:F268–F273 (1979).

    PubMed  CAS  Google Scholar 

  44. S. Moneada, R. Korbut, S. Bunting, J.R. Vane, Prostacyclin is not a circulating hormone, Nature 273:767–769 (1978).

    Article  Google Scholar 

  45. J.J. Grantham and J. Orloff, Effect of prostaglandin E1 on the permeability response of the isolated collecting tubule to vasopressin, adenosine 3′,5′-monophosphate, and theophylline, J. Clin. Invest. 47: 1154–1161 (1968).

    Article  PubMed  CAS  Google Scholar 

  46. J.S. Handler and J. Orloff, Antidiuretic hormone, Ann. Rev. Physiol. 43: 611–624 (1981).

    Article  CAS  Google Scholar 

  47. T.R. Beck and M.J. Dunn, The relationship of antidiuretic hormone and renal prostaglandins, Mineral Electrolyte Metab. 6:46–59 (1981).

    CAS  Google Scholar 

  48. D. Steinberg, M. Vaughan, P.J. Nestel, O. Strand, S. Bergstrom, Effects of prostaglandins on hormone-induced mobilization of free fatty acids, J. Clin. Invest. 43:1533–1540 (1963).

    Article  Google Scholar 

  49. R.W. Butcher and C.E. Baird, Effects of prostaglandins on adenosine 3′,5′-monophosphate levels in fat and other tissues, J. Biol. Chem. 243:1713–1717 (1968).

    PubMed  CAS  Google Scholar 

  50. R.M. Edwards, B.A. Jackson, T.P. Dousa, ADH-sensitive cAMP system in papillary collecting duct: effect of osmolality and PGE2, Am. J. Physiol. 240:F311–F318 (1981).

    PubMed  CAS  Google Scholar 

  51. S. Torikai and K. Kurokawa, Effect of PGE2 on vasopressin-dependent cell cAMP in isolated single nephron segments, Am. J. Physiol. 245: F58–F66 (1983).

    PubMed  CAS  Google Scholar 

  52. K. Yatsunami, A. Ichikawa, K. Tomita, Accumulation of adenosine 3′,5′-monophosphate induced by prostaglandin E2 binding to mastocytoma P-815 cells, Biochem. Pharmacol. 11:1325–1332 (1981).

    Article  Google Scholar 

  53. P. Menè, G.R. Dubyak, A. Scarpa, M.J. Dunn, Stimulation of cytosolic free calcium and inositol phosphates by prostaglandins in cultured rat mesangial cells, Biochem. Biophys. Res. Comm. 142(2): 579–586 (1987).

    Article  PubMed  Google Scholar 

  54. R.A. Coleman and I. Kennedy, Characterization of the prostanoid receptors mediating contraction of guinea pig isolated trachea, Prostaglandins 29:363–375 (1985).

    PubMed  CAS  Google Scholar 

  55. R.A. Coleman, P.P.A. Humphrey, I. Kennedy, Prostanoid receptors in smooth muscle: further evidence for a proposed classification, in: “Trends in Autonomic Pharmacology,” Vol. 3, Kalsner, S., ed., Taylor and Francis Publishing, London, pp. 35–49 (1985).

    Google Scholar 

  56. D.A. Ausiello and J.V. Bonventre, Calcium and calmodulin as mediators of hormone action and transport events, Sem. in Nephrol. 4:134–143 (1984).

    CAS  Google Scholar 

  57. V.C. Manganiello, T. Yamamoto, M. Lin, M.L. Elks, M. Vaughan, Regulation of specific forms of cyclic nucleotide phosphodiesterases in cultured cells, Adv. Cyclic Nucleotide Res. 16:291–301 (1984).

    CAS  Google Scholar 

  58. I.L.O. Buxton and L.L. Brunton, Action of the cardiac α1-adrenergic receptor. Activation of cAMP degradation, J. Biol. Chem. 260:6733–6737 (1985).

    PubMed  CAS  Google Scholar 

  59. W.L. Smith, W.K. Sonnenburg, T. Watanabe, K. Umegaki, Mechanism of action of prostaglandin E2 and prostaglandin F2 : PGE and PGE receptors, in: “Eicosanoids in the Cardiovascular and Renal Systems,” P.V. Halushka, ed., MTP Press, Lancaster, in press.

    Google Scholar 

  60. W.L. Smith and A. Garcia-Perez, A two receptor model for the mechanism of action of prostaglandins in the renal collecting tubule, in: “Prostaglandins, Leukotrienes and Lipoxins,” J.M. Bailey, ed., Plenum Publishing, New York, pp. 35–45 (1985).

    Chapter  Google Scholar 

  61. B.B. Clark and R.W. Butcher, Desensitization of adenylate cyclase in cultured fibroblasts with prostaglandin E1 and epinephrine, J. Biol. Chem. 254:9373–9378 (1979).

    PubMed  CAS  Google Scholar 

  62. S. Kassis and P.H. Fishman, Different mechanism of desensitization of adenylate cyclase by isoproterenol and prostaglandin E1 in human fibroblasts: role of regulatory components in desensitization, J. Biol. Chem. 257:5312–5318 (1982).

    PubMed  CAS  Google Scholar 

  63. D.R. Sibley and R.J. Lefkowitz, Molecular mechanism of receptor desensitization using the β-adrenergic receptor-coupled adenylate cyclase system as a model, Nature 317:124–129 (1985).

    Article  PubMed  CAS  Google Scholar 

  64. T. Watanabe, K. Umegaki, W.L. Smith, Association of a solubilized prostaglandin E2 receptor from renal medulla with a pertussis toxin-reactive guanine nucleotide regulatory protein, J. Biol. Chem. 261:13430–13439 (1986).

    PubMed  CAS  Google Scholar 

  65. R. Grandt, K. Aktories, K.H. Jakobs, Guanine nucleotides and monovalent cations increase agonist affinity of prostaglandin E2 receptors in hamster adipocytes, Mol. Pharmacol. 22:320–326 (1982).

    PubMed  CAS  Google Scholar 

  66. J.A. Garcia-Sainz, Decreased sensitivity to α2 adrenergic amines, adenosine and prostaglandins in white fat cells from hamsters treated with pertussis toxin, FEBS Lett. 126:306–308 (1981).

    Article  PubMed  CAS  Google Scholar 

  67. R.J. Anderson, P.D. Wilson, M.A. Dillingham, R. Breckon, U. Schwertschlaf, J.A. Garcia-Sainz, Pertussis toxin reverses prostaglandin E2 inhibition of arginine vasopressin (AVP) and forskolin in rabbit collecting tubular epithelium, (Abstract), Am. Soc. Nephrol. Mtg. 154, (1984).

    Google Scholar 

  68. J.W. Regan, H. Nakata, R.M. DeMarinis, M.G. Caron, R.J. Lefkowitz, Purification and characterization of the human platelet α2-adrenergic receptor, J. Biol. Chem. 261:3894–3900 (1986).

    PubMed  CAS  Google Scholar 

  69. R.A. Cerione, J.W. Regan, H. Nakata, J. Codina, J.L. Benovic, P. Gierschik, R.L. Somers, A.M. Spiegel, L. Birnbaumer, R.J. Lefkowitz, M.G. Caron, Functional reconstitution of the α2-adrenergic receptor with guanine nucleotide regulatory proteins in phospholipid vesicles, J. Biol. Chem. 261:3901–3909 (1986).

    PubMed  CAS  Google Scholar 

  70. T. Katada, G.M. Bokoch, J.K. Northup, M. Ui, A.G. Gilman, The inhibitory guanine nucleotide-binding regulatory component of adenylate cyclase: properties and function of the purified protein, J. Biol. Chem. 259:3568–3577 (1984).

    PubMed  CAS  Google Scholar 

  71. T. Katada, G.M. Bokoch, M.D. Smigel, M. Ui, A.G. Gilman, The inhibitory guanine nucleotide-binding regulatory component of adenylate cyclase: Subunit dissociation and the inhibition of adenylate cyclase in S49 cyc and wild type membranes, J. Biol. Chem. 260:3477–3483 (1985).

    Google Scholar 

  72. M.L. Elks, M. Jackson, V.C. Manganiello, M. Vaughan, Effect of N6-(L-2-phenylisopropyl)adenosine and insulin on cAMP metabolism in 3T3-L1 adipocytes, Am. J. Physiol. 252:C342–C348 (1987).

    PubMed  CAS  Google Scholar 

  73. R.M. Culpepper and T.E. Andreoli, Interactions among prostaglandin E2, antidiuretic hormone, and cyclic adenosine monophosphate in modulating Cl- absorption in single mouse medullary thick ascending limbs of Henle, J. Clin. Invest. 71:1588–1601 (1983).

    Article  PubMed  CAS  Google Scholar 

  74. S. Hebert and T.E. Andreoli, Control of NaCl transport in the thick ascending limb, Am. J. Physiol. 246:F745–F756 (1984).

    PubMed  CAS  Google Scholar 

  75. R.M. Culpepper, Pertussis toxin blunts PGE2 inhibition of ADH-stimulated Ve in mouse mTALH, Kidney Int. 27:255 (1985).

    Google Scholar 

  76. J.L. Stokes, Personal communication.

    Google Scholar 

  77. S. Torikai and K. Kurokawa, Distribution of prostaglandin E2-sensitive adenylate cyclase along the rat nephron, Prostaglandins 21:427–438 (1981).

    PubMed  CAS  Google Scholar 

  78. R.J. Lefkowitz, D. Mullikin, C.L. Wood, T.B. Gore, C. Mukherjee, Regulation of prostaglandin receptors by prostaglandins and guanine nucleotides in frog erythrocytes, J. Biol. Chem. 252:5295–5303 (1977).

    PubMed  CAS  Google Scholar 

  79. H.A. Lester, M.L. Steer, A. Levitzki, Prostaglandin-stimulated GTP hydrolysis associated with activation of adenylate cyclase in human platelet membranes, Proc. Nat. Acad. Sci. U.S.A. 79:719–723 (1982).

    Article  CAS  Google Scholar 

  80. I. Teitelbaum, J.N. Mansour, T. Berl, Effect of cAMP on prostaglandin E2 production in cultured rat inner medullary collecting tubule cells, Am. J. Physiol. 251:F671–F677 (1986).

    PubMed  CAS  Google Scholar 

  81. W.G. Tarpley, N.K. Hopkins, R.R. Gorman, Reduced hormone-stimulated adenylate cyclase activity in NIH-3T3 cells expressing the EJ human bladder ras oncogene, Proc. Nat. Acad. Sci. U.S.A. 83:3703–3707 (1986).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1989 Plenum Press, New York

About this chapter

Cite this chapter

Smith, W.L., Sonnenburg, W.K., Allen, M.L., Watanabe, T., Zhu, J., El-Harith, E.A. (1989). The Biosynthesis and Actions of Prostaglandins in the Renal Collecting Tubule and Thick Ascending Limb. In: Dunn, M.J., Patrono, C., Cinotti, G.A. (eds) Renal Eicosanoids. Advances in Experimental Medicine and Biology, vol 259. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5700-1_6

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-5700-1_6

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-5702-5

  • Online ISBN: 978-1-4684-5700-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics