Advertisement

Journal of comparative physiology

, Volume 145, Issue 1, pp 29–35 | Cite as

Adrenergic regulation of chloride secretion across the opercular epithelium: The role of cyclic AMP

  • Susan A. Mendelsohn
  • Bruce D. Cherksey
  • Kevin J. Degnan
Article

Summary

Activation of the β-adrenergic receptors of the opercular epithelium ofFundulus heteroclitus stimulates Cl secretion, while activation of the α-adrenergic receptors inhibits Cl secretion (Degnan and Zadunaisky, 1979). The possible involvement of adenosine 3′, 5′-monophosphate (cAMP) in these adrenergic responses was investigated. Isolated opercular epithelia incubated in Ringer, containing 10 mM theophylline, had cAMP levels ranging between 5.3 and 19.3 pmoles·mg protein−1 (mean=9.5±1.0 pmoles·mg protein−1). Activation of the β-receptors by 10−5 M isoproterenol increased the mean cAMP level 430% (P<0.001). Blockage of the β-receptors with propranolol greatly reduced the increase in cAMP in response to isoproterenol. Activation of the α-receptors by 10−5 M arterenol stimulated the mean cAMP level 270% (P<0.01). However, when the β-receptors were blocked with propranolol, arterenol had no effect on the cAMP level. The possible involvement of Ca++ in these adrenergic responses was investigated. Neither the stimulatory effect of isoproterenol, nor the inhibitory effect of arterenol on the Cl secretion were diminished in the absence of extracellular Ca++. The Ca++ ionophore, A23187, and the calmodulin inhibitor, trifluoperazine, had no effects on the Cl secretion. The Ca++-channel blocker, D600, had a significant inhibitory effect (P<0.005). Guanosine 3′,5′-monophosphate (cGMP) had no effect on the Cl secretion.

The results indicate that β-adrenergic stimulation of Cl secretion across the opercular epithelium is accompanied by an elevation in tissue cAMP levels. α-adrenergic inhibition of Cl secretion does not involve changes in the tissue cAMP. Neither of these responses appear to require Ca++.

Keywords

Propranolol Theophylline Monophosphate Guanosine Isoproterenol 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abdel-Latif AA, Owen MP, Matheny JL (1976) Adrenergic and cholinergic stimulation of32P-labeling of phospholipids in rabbit iris muscle. Biochem. Pharmacol 25:461–469Google Scholar
  2. Bolton JE, Field M (1977) Ca ionophore-stimulated ion secretion in rabbit ileal mucosa: relation to actions of cyclic 3′,5′-AMP and carbamylcholine. J Membr Biol 35:159–173Google Scholar
  3. Brown BL, Albano JDM, Ekins RP, Sgherzi AM (1971) A simple and sensitive assay method for the measurement of adenosine 3′:5′-cyclic monophosphate. Biochem J 121:561–562Google Scholar
  4. Candia OA, Montoreano R, Podos SM (1977) Effect of ionophore A23187 on chloride tranpsort across isolated frog cornea. Am J Physiol 233:F94-F101Google Scholar
  5. Cuthbert AW, Pic P (1973) Adrenoceptors and adenyl cyclase in gills. Br J Pharmacol 49:134–137Google Scholar
  6. Degnan KJ, Zadunaisky JA (1979) Open-circuit sodium and chloride fluxes across isolated opercular epithelia from the teleostFundulus heteroclitus. J Physiol (Lond) 294:484–495Google Scholar
  7. Degnan KJ, Zadunaisky JA (1980) Ionic contributions to the potential and current across the opercular epithelium. Am J Physiol 238:R231-R239Google Scholar
  8. Degnan KJ, Zadunaisky JA (1981) The sodium and chloride dependence of active Cl secretion across the opercular epithelium. Fed Proc 40:370Google Scholar
  9. Degnan KJ, Karnaky Jr, KJ, Zadunaisky JA (1977) Active Cl transport in thein vitro opercular skin of a teleost (Fundulus heteroclitus), a gill-like epithelium rich in chloride cells. J Physiol (Lond) 271:155–191Google Scholar
  10. Ernst SA, Dodson WC, Karnaky Jr, KJ (1980) Structural diversity of occluding junctions in the low-resistance chloride-secreting opercular epithelium of seawater-adapted killifish (Fundulus heteroclitus). J Cell Biol 87:488–497Google Scholar
  11. Exton JH (1980) Mechanisms involved in α-adrenergic phenomena: Role of calcium ions in actions of catecholamines in liver and other tissues. Am J Physiol 238:E3-E12Google Scholar
  12. Fairhurst AS, Whittaker ML, Ehlert FJ (1980) Interactions of D600 (methoxyverapamil) and local anesthetics with rat brain α-adrenergic and muscarinic receptors. Biochem Pharmacol 29:155–162Google Scholar
  13. Ferrendelli JA, Kinscherf DA, Chang MM (1975) Comparison of the effects of biogenic amines on cyclic GMP and cyclic AMP levels in mouse cerebellumin vitro. Brain Res 84: 63–73Google Scholar
  14. Frizzell RA (1977) Active chloride secretion by rabbit colon: Calcium-dependent stimulation by ionophore A23187. J Membr Biol 35:175–187Google Scholar
  15. Frizzell RA, Field M, Schultz SG (1979) Sodium-coupled chloride transport by epithelial tissues. Am J Physiol 236:F1-F8Google Scholar
  16. Garrison JC, Borland MK, Florio VA, Twible DA (1979) The role of calcium ion as a mediator of the effects of angiotensin II, catecholamines and vasopressin on the phosphorylation and activity of enzymes in isolated hepatocytes. J Biol Chem 254:7147–7156Google Scholar
  17. Girard J-P (1976) Salt excretion by the perfused head of trout adapted to sea water and its inhibition by adrenaline. J Comp Physiol 111:77–91Google Scholar
  18. Girard J-P, Thomson AJ, Sargent JR (1977) Adrenaline induced turnover of phosphatidic acid and phosphatidyl inositol in chloride cells from the gills ofAnguilla anguilla. FEBS Lett 73:267–270Google Scholar
  19. Greengard P (1979) Cyclic nucleotides, phosphorylated proteins, and the nervous system. Fed Proc 38:2208–2217Google Scholar
  20. Haywood GP, Isaia J, Maetz J (1977) Epinephrine effects on branchial water and urea flux in rainbow trout. Am J Physiol 232:R110-R115Google Scholar
  21. Jones LM, Michell RH (1975) The relationship of calcium to receptor-controlled stimulation of phosphatidylinositol turnover. Biochem J 148:479–485Google Scholar
  22. Karnaky Jr KJ, Kinter WB (1977) Killifish opercular skin: a flat epithelium with a high density of chloride cells. J Exp Zool 199:355–364Google Scholar
  23. Karnaky Jr KJ, Degnan KJ, Zadunaisky JA (1977) Chloride transport across isolated opercular epithelium of killifish: a membrane rich in chloride cells. Science 195:203–205Google Scholar
  24. Karnaky Jr KJ, Degnan KJ, Zadunaisky JA (1979) Correlation of chloride cell number and short-circuit current in chloridesecreting epithelia ofFundulus heteroclitus. Bull Mt Desert Isl Biol Lab 19:109–111Google Scholar
  25. Kass RS, Tsien RW (1975) Multiple effects of calcium antagonists on plateau currents in cardiac purkinje fibers. J Gen Physiol 66:169–192Google Scholar
  26. Keys AB, Bateman JB (1932) Branchial responses to adrenaline and to pitressin in the eel. Biol Bull Mar Biol Lab (Woods Hole, Mass) 63:327–336Google Scholar
  27. Kimberg DV, Shlatz LJ, Cattieu KA (1979) Cyclic nucleotidedependent protein kinases in membranes from rat small intestine. In: Binder HJ (ed) Mechanisms of intestinal secretion. Liss, New York, pp 131–146Google Scholar
  28. Klyce SD, Wong RKS (1977) Site and mode of adrenaline action on chloride transport across the rabbit corneal epithelium. J Physiol (Lond) 266:777–799Google Scholar
  29. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  30. Marshall WS, Nishioka RS (1980) Relation of mitochondria-rich chloride cells to active chloride transport in the skin of a marine teleost. J Exp Zool 214:147–156Google Scholar
  31. Michell RH (1975) Inositol phospholipids and cell surface receptor function. Biochim Biophys Acta 415:81–147Google Scholar
  32. Michell RH, Jones LM (1974) Enhanced phosphatidylinositol labelling in rat parotid fragments exposed to α-adrenergic stimulation. Biochem J 138:47–52Google Scholar
  33. Montoreano R, Candia OA, Cook P (1976) α- and β-adrenergic receptors in regulation of ionic transport in frog cornea. Am J Physiol 230:1487–1493Google Scholar
  34. Nagel W, Reinach P (1980) Mechanism of stimulation by epinephrine of active transepithelial Cl transport in isolated frog cornea. J Membr Biol 56:73–79Google Scholar
  35. O'Dea RF, Zatz M (1976) Catecholamine stimulated cyclic GMP accumulation in the rat pineal: apparent presynaptic site of action. Proc Natl Acad Sci USA 73:3398–3402Google Scholar
  36. Orom Y, Lowe M, Selinger Z (1975) Incorporation of inorganic (32P) phosphate into rat parotid phosphatidylinositol. Induction through activation of alpha adrenergic and cholinergic receptors and relation to K+ release. Mol Pharmacol 11:79–86Google Scholar
  37. Pic P, Djabali M (1979) Effets de la theophylline sur la concentration branchiale en AMP cyclique et sur les transferts branchiaux d'eau chezMugil capito en cau de mer. CR Acad Sci [D] (Paris) 289:417–420Google Scholar
  38. Pic P, Mayer-Gostan N, Maetz J (1974) Branchial effects of epinephrine in the seawater-adapted mullet. I. Water permeability. Am J Physiol 226:698–702Google Scholar
  39. Pic P, Mayer-Gostan N, Maetz J (1975) Branchial effects of epinephrine in the seawater-adapted mullet. II. Na+ and Cl extrusion. Am J Physiol 228:441–447Google Scholar
  40. Putney JW jr (1977) Muscarinic alpha-adrenergic and peptide receptors regulate the same calcium influx sites in the parotid gland. J Physiol (Lond) 268:139–149Google Scholar
  41. Putney JW Jr (1979) Stimulus-permeability coupling: role of calcium in the receptor regulation of membrane permeability. Pharmacol Rev 30:209–245Google Scholar
  42. Robinson GA, Butcher RW, Sutherland EW (1971) Cyclic AMP. Academic Press, New YorkGoogle Scholar
  43. Rosenberger L, Triggle DJ (1978) Calcium-calcium translocation and specific calcium antagonists. In: Weiss GB (ed) Calcium in drug action. Plenum Press, New York, pp 3–32Google Scholar
  44. Rowing GM, Zadunaisky JA (1978) Inhibition of chloride transport by acetylcholine in the isolated opercular epithelia ofFundulus heteroclitus. Presence of a muscarinic receptor. Bull Mt Desert Isl Biol Lab 18:101–104Google Scholar
  45. Schulman H, Greengard P (1978a) Stimulation of brain membrane phosphorylation by calcium and an endogenous heat-stable protein. Nature 271:478–479Google Scholar
  46. Schulman H, Greengard P (1978b) Ca2+-dependent protein phosphorylation system in membranes from various tissues, and its activation by ‘calcium-dependent regulator’. Proc Natl Acad Sci USA 75:5432–5436Google Scholar
  47. Silva P, Stoff J, Field M, Fine L, Forrest JN, Epstein FH (1977) Mechanism of active chloride secretion by shark rectal gland: Role of Na-K-ATPase in chloride transport. Am J Physiol 233:F298-F306Google Scholar
  48. Wolff DJ, Brostrom CO (1979) Properties and functions of the calcium-dependent regulator protein. In: Greengard P, Robinson GA (eds) Advances in cyclic nucleotide research. Raven Press, New York, pp 27–88Google Scholar
  49. Zadunaisky JA, Lande MA, Chalfie M, Neufeld AH (1973) Ion pumps in the cornea and their stimulation by epinephrine and cyclic-AMP. Exp Eye Res 15:577–584Google Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • Susan A. Mendelsohn
    • 1
    • 2
  • Bruce D. Cherksey
    • 1
    • 2
  • Kevin J. Degnan
    • 1
    • 2
  1. 1.Department of Physiology and BiophysicsNew York University Medical CenterNew YorkUSA
  2. 2.Mt. Desert Island Biological LaboratorySalsbury CoveUSA

Personalised recommendations