Advertisement

Pflügers Archiv

, Volume 427, Issue 1–2, pp 1–8 | Cite as

Hormone-mediated Ca2+ transients in isolated renal cortical thick ascending limb cells

  • Long -Jun Dai
  • Gary A. Quamme
Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands

Abstract

Peptide hormones control salt reabsorption in cortical thick ascending limb (cTAL) cells of the loop of Henle. These agonists act, in part, through alterations on intracellular Ca2+ ([Ca2+]i). Primary cell cultures were prepared from porcine kidneys using a double antibody technique (goat antihuman Tamm-Horsfall and rabbit antigoat IgG antibodies). [Ca2+]i was determined in single cells with fluorescent techniques using fura-2. Parathyroid hormone (PTH) and arginine vasopressin (AVP) transiently increased [Ca2+]i in a dose-dependent manner. [Ca2+]i maximally increased from 85±5 nmol/l to 608±99 nmol/l with PTH, 10−6M, and to 766±162 nmol/l with AVP, 10−7 M. The increment in [Ca2+]i by both hormones was by intracellular Ca2+ release and entry through plasma membrane Ca2+ channels. 8-Bromoadenosine-3′, 5′-cyclic monophosphate (8-BrcAMP), 10−4M, increased [Ca2+]i(basal 83±3 to 427±121 nmol/l) but only from internal sources as nifedipine (10 μmol), ([Ca2+]i changes: 86±4 to 390±29 nmol/l) and removal of bath Ca o 2+ , ([Ca2+]ichanges: 84±6 to 517±142 nmol/l), were without effect on agonist-induced [Ca2+]i. Thapsigargin, 1.5 μmol, completely abolished the AVP- and cyclic adenosine monophosphate-(cAMP)-induced Ca2+ transients, and partially inhibited PTH-mediated Ca2+ transients by about 50%. Pretreatment with 8-BrcAMP inhibited the PTH and AVP responses likely through depletion of cAMP-sensitive Ca2+ stores. Activation of protein kinase C (PKC) with phorbol esters inhibited PTH and AVP responses and 8-BrcAMP-induced [Ca2+]i transients. The responses partially returned following down-regulation of PKC with prolonged exposure to phorbol esters. These data suggest that PKC activation modulates agonist-induced Ca2+ release and entry, possibly through actions on intracellular release mechanisms. In summary, PTH and AVP stimulate Ca2+ signals by similar pathways involving cAMP and inositol 1,3,4-trisphosphate activity at similar sites on the endoplasmic reticulum and plasma membrane. These results suggest that peptide hormones may act through Ca2+ and be modulated by different pathways which may have diverse effects on cTAL function.

Key words

Receptors Parathyroid hormone Calcitonin Glucagon Antidiuretic hormone cAMP [Ca2+]i Phorbol ester Porcine thick ascending limb cells 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Ansah T-A, Dho S, Case RM (1986) Calcium concentration and amylase secretion in guinea pig pancreatic acini: interactions between carbachol, cholecystokinin, octapeptide, and the phorbol ester, 12-0-tetradecanoylphorbol 13-acetate. Biochim Biophys Acta 889:326–333Google Scholar
  2. 2.
    Bailly C, Roinel N, Amiel C (1984) PTH-like glucagon stimulation of Ca and Mg reabsorption in Henle's loop of the rat. Am J Physiol 246:F205-F212Google Scholar
  3. 3.
    Berridge MJ (1993) Inositol triphosphate and calcium signalling. Nature 361:315–325Google Scholar
  4. 4.
    Bird G St J, Rossier MF, Obie JF, Putney JW Jr (1993) Sinusoidal oscillations in intracellular calcium requiring negative feedback by protein kinase C. J Biol Chem 268:8425–8428Google Scholar
  5. 5.
    Bourdeau JE, Eby BK, Hu J (1990) cAMP-stimulated rise of [Ca2+]i in rabbit connecting tubules: role of peritubular calcium. Am J Physiol 258:F751-F755Google Scholar
  6. 6.
    Bruzzone R, Regazzi R, Wollheim C (1988) Caerulin causes translocation of protein kinase C in rat acini without increasing cytosolic free Ca2+. Am J Physiol 255:G33-G39Google Scholar
  7. 7.
    Chabardès D, Imbert M, Clique A, Montégut M, Morel F (1975) PTH sensitive adenyl cyclase activity in different segments of the rabbit nephron. Pflügers Arch 354:229–239Google Scholar
  8. 8.
    Dai L-j, Quamme GA (1991) Intracellular Mg2+ and magnesium depletion in isolated renal thick ascending limb cells. J Clin Invest 88:1255–1264Google Scholar
  9. 9.
    Di Stefano A, Wittner M, Nitschke R, Braitsch R, Greger R, Bailly C, Amiel C, Roinel N, de Rouffignac C (1990) Effects of parathyroid hormone and calcitonin on Na+, Cl, K+, Mg2+ and Ca2+ transport in cortical and medullary thick ascending limbs of mouse kidney. Pflügers Arch 417:161–167Google Scholar
  10. 10.
    Dublineau I, Elalouf J-M, Pradelles P, de Rouffignac C (1989) Independent desensitization of rat renal thick ascending limbs and collecting ducts to ADH. Am J Physiol 256:F656-F663Google Scholar
  11. 11.
    Elalouf JM, Chabanne-Sari S, de Rouffignac C (1986) Additivity of the effects of glucagon and vasopressin on renal Mg reabsorption and urinary concentration ability in the rat. Pflügers Arch 407:566–571Google Scholar
  12. 12.
    Elalouf JM, Di Stefano A, de Rouffignac C (1986) Sensitivities of rat kidney thick ascending limbs and collecting ducts to vasopressin (in vivo). Proc Natl Acad Sci USA 83:2276–2280Google Scholar
  13. 13.
    Elalouf JM, Chabane-Sari S, Roinel N, de Rouffignac C (1988) Desensitization of rat renal thick ascending limb to vasopressin. Proc Nat Acad Sci USA 85:2407–2416Google Scholar
  14. 14.
    Glennon MC, Bird GSJ, Kwan C-y, Putney J Jr (1992) Actions of vasopressin and the Ca2+-ATPase inhibitor, thapsigargin, on Ca2+ signalling in hepatocytes. J Biol Chem 267:8230–8233Google Scholar
  15. 15.
    Greger R (1985) Ion transport mechanisms in thick ascending limb of Henle's loop of mammalian nephron. Physiol Rev 65:760–797Google Scholar
  16. 16.
    Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indications with greatly improved fluorescence properties. J Biol Chem 260:3440–3450Google Scholar
  17. 17.
    Hallam TJ, Rink TJ (1989) Receptor-mediated Ca2+ entry in diversity of function and mechanism. Trends Pharmacol Sci 10:8–10Google Scholar
  18. 18.
    Herbert SC, Andreoli TE (1984) Control of NaCl transport in the thick ascending limb. Am J Physiol 246:F745-F756Google Scholar
  19. 19.
    Horn VJ, Baum BJ, Ambudkar IS (1988)β-Adrenergic receptor stimulation induces inositol trisphosphate production and Ca2+ mobilization in rat acinar cells. J Biol Chem 263: 12454–12460Google Scholar
  20. 20.
    Kikkawa U, Nishizuka Y (1986) The role of protein kinase C in transmembrane signalling. Annu Rev Cell Biol 2:149–178Google Scholar
  21. 21.
    Kuno M, Gardner P (1987) Ion channels activated by inositol 1,4,5-trisphosphate in plasma membrane of human T-lymphocytes. Nature 326:301–304Google Scholar
  22. 22.
    Luini A, Lewis D, Guild S, Corda D, Axelrod J (1985) Hormone secretagogues increase cytosolic calcium by increasing cAMP in corticotropin-secreting cells. Proc Natl Acad Sci USA 82:8034–8038Google Scholar
  23. 23.
    Mauger J-P, Claret M (1986) Mobilization of intracellular calcium by glucagon and cyclic AMP analogues in isolated rat hepatocytes. FEBS Let 195:106–110Google Scholar
  24. 24.
    Morel F (1981) Sites of hormone action in the mammalian nephron. Am J. Physiol 240:F159-F164Google Scholar
  25. 25.
    Morel F, Chabardès D, Imbert-Teboul M, Le Bouffant F, HusCitharel A, Montégut M (1982) Multiple hormonal control of adenylate-cyclase in distal segments of the rat kidney. Kidney Int 21:S55-S62Google Scholar
  26. 26.
    Nitschke R, Fröbe U, Greger R (1991) Antidiuretic hormone acts via V1 receptors on intracellular calcium in the isolated perfused rabbit cortical thick ascending limb. Pflügers Arch 417:622–632Google Scholar
  27. 27.
    Rosenthal W, Hescheler J, Trautwein W, Schultz G (1988) Control of voltage-dependent Ca2+ channels by G proteincoupled receptors. FASEB J 2:1784–1790Google Scholar
  28. 28.
    Rouffignac C de, Elalouf JM, Roinel N, Bailly C, Amiel C (1984) Similarity of the effects of antidiuretic hormone, parathyroid hormone, calcitonin, and glucagon or rat kidney. In: Robinson RR (ed) Nephrology. Springer, Berlin Heidelberg New York, pp 340–357Google Scholar
  29. 29.
    Rouffignac C de, Di Stefano A, Wittner M, Roinel N, Elalouf JM (1991) Consequences of differential effects of ADH and other peptide hormones on thick ascending limbs of mammalian kidney. Am J Physiol 260:R1023-R1035Google Scholar
  30. 30.
    Schiebinger RJ, Braley LM, Menachery A, Williams GH (1985) Calcium, a “third messenger” of cAMP-stimulated adrenal steroid secretion. Am J Physiol 248:E89-E94Google Scholar
  31. 31.
    Takemura H, Hughes AR, Thastrup O, Putney JW Jr (1989) Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells: evidence that an intracellular calcium pool, and not an inositol phosphate, regulates calcium fluxes at the plasma membrane. J Biol Chem 264:12266–12271Google Scholar
  32. 32.
    Tan YP, Marty A (1991) Protein kinase C-mediated desensitization of the muscarinic response in rat lacrimal gland cells. J Physiol (Lond) 433:357–371Google Scholar
  33. 33.
    Taniguchi S, Marchetti J, Morel F (1989) Cytosolic free calcium in single microdissected rat cortical collecting tubules. Pflügers Arch 414:125–133Google Scholar
  34. 34.
    Thastrup O, Cullen PJ, Drobak B, Hanley MR, Dawson AP (1990) Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2+-ATPase. Proc Natl Acad Sci USA 87:2466–2470Google Scholar
  35. 35.
    Uneyama H, Uneyama C, Akaike N (1933) Intracellular mechanisms of cytoplasmic Ca2+ oscillation in rat megakaryocyte. J Biol Chem 268:168–174Google Scholar
  36. 36.
    Willems PHGM, Van Den Brock BAM, Van Os CH, De Pont JJHHM (1989) Inhibition of inositol 1,4,5-triphosphate-induced Ca2+ release in permeabilized pancreatic acinar cells hy hormonal and phorbol ester pretreatment. J Biol Chem 264:9762–9767Google Scholar
  37. 37.
    Wittner M, Di Stefano A, Wangemann P, Nitschke R, Greger R, Bailly C, Amiel C, Roinel N, de Rouffignac C (1988) Different effects of ADH on sodium, chloride, potassium, calcium, and magnesium transport in cortical and medullary thick ascending limbs of mouse nephron. Pflügers Arch 412: 516–523Google Scholar
  38. 38.
    Wittner M, Di Stefano A, Mandon B, Roinel N, de Rouffignac C (1991) Stimulation of NaCl reabsorption by antidiuretic hormone in the cortical thick ascending limb of Henle's loop of the mouse. Pflügers Arch 419:212–214Google Scholar
  39. 39.
    Woods NM, Cuthbertson KSR, Cobbold PTS (1987) Phorbolester-induced alterations of free calcium ion transients in single rat hepatocytes. Biochem J 246:619–623Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Long -Jun Dai
    • 1
  • Gary A. Quamme
    • 1
  1. 1.Department of Medicine, University Hospital - UBC SiteUniversity of British ColumbiaVancouverCanada

Personalised recommendations