Journal of Comparative Physiology B

, Volume 165, Issue 8, pp 665–676 | Cite as

Modulation of catecholamine storage and release by the pituitary-interrenal axis in the rainbow trout, Oncorhynchus mykiss

  • S. G. Reid
  • M. M. Vijayan
  • S. F. Perry
Original Paper

Abstract

This study examined the effects of pituitary-interrenal hormones on catecholamine storage and release in the rainbow trout Oncorhynchus mykiss. An extract of trout pituitary elicited the release of adrenaline, but not noradrenaline, using an in situ perfusion preparation. A variety of doses of adrenocorticotropic hormone (2–2000 mU) caused the release of both catecholamines in situ which was unaffected by pre-treatment with the ganglion blocker, hexamethonium, or the serotonergic receptor antagonist, methysergide, but was abolished in calcium-free media. Intra-arterial injections of adrenocorticotrophic hormone in vivo caused an elevation of plasma adrenaline but not noradrenaline levels. Injections of cortisol in situ did not elicit catecholamine release. Trout given an intraperitoneal implant of cortisol (50 mg·kg-1 body weight) had significantly higher plasma cortisol concentrations when compared to controls after 7 days of implantation. Increases in the levels of stored catecholamines were observed in various regions of the kidney and posterior cardinal vein following 3 and 7 days of cortisol treatment. The ability of the chromaffin cells to release catecholamines in response to cholinergic stimulation was assessed in situ after 7 days of treatment. Basal (non-stimulated) adrenaline outflowing perfusate levels were greater in the cortisol-treated fish. Cortisol treatment increased the responsiveness of the catecholamine release process to low doses of the cholinoceptor agonist carbachol. Three or 7 days of cortisol treatment did not alter the in vitro activity of the enzyme phenylethanolamine-N-methyl-transferase. The results of this study demonstrate that interactions within the pituitary-adrenal axis can influence both catecholamine storage and release in the rainbow trout.

Key words

Catecholamines Cortisol Chromaffin cells Adrenocorticotropic hormone Rainbow trout, Oncorhynchus mykiss 

Abbreviations

ACTH

adrenocorticotropic hormone

AK

anterior third of the kidney

APCV

anterior third of the PCV

HPLC

high performance liquid chromatography

MK

middle third of the kidney

M1

maximum value

MPCV

middle third of the PCV

MS222

ethyl-aminobenzoate

P1

pre value

PCA

perchloric acid

PCV

posterior cardinal vein

PK

posterior third of the kidney

PNMT

phenylethanolamine-N-methyltransferase

PPCV

posterior third of the PCV

rbc

red blood cells

SEM

standard error of the mean

TK

total kidney (i.e. the sum of the AK, MK, and PK)

TPCV

total PCV (i.e. the sum of the APCV, MPCV and PPCV)

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References

  1. Abrahamson T (1979) Phenylethanolamine-N-methyltransferase (PNMT) activity and catecholamine storage and release from chromaffin tissue of the spiny dogfish, Squalus acanthias. Comp Biochem Physiol 64C: 169–172Google Scholar
  2. Abrahamson T (1980) The effect of SK & F 64139, an inhibitor of phenylethanolamine-N-methyltransferase (PNMT), on adrenaline and noradrenaline content in sympathetic neurons of the cod, Gadus morhua. Comp Biochem Physiol 67C: 49–54Google Scholar
  3. Abrahamson T, Nilsson S (1976) Thenylethanolamine-N-methyl-transferase (PNMT) activity and catecholamine content in chromaffin tissue and sympathetic neurons in the cod, Gadus morhua. Acta Physiol Scand 96: 94–99Google Scholar
  4. Anderson DE, Reid SD, Moon TW, Perry SF (1991) Metabolic effects associated with chronically elevated cortisol in rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 48: 1811–1817Google Scholar
  5. Augustinsson KB, Fänge R, Johnels A, Östlund E (1956) Histological, physiological and biochemical studies on the heart of two cyclostomes, hagfish (Myxine) and lamprey (Lampetra). J Physiol (London). 131: 257–276Google Scholar
  6. Axelrod J, Reisine TD (1984) Stress hormones: their interaction and regulation. Science 224: 452–459Google Scholar
  7. Betito K, Diorio J, Boska P (1993) Brief cortisol exposure elevates adrenal phenylethanolamine-N-methyltransferase after a necessary lag period. Eur J Pharmacol 238: 273–282Google Scholar
  8. Ciaranello RD, Wooten GF, Axelrod L (1975) Regulation of dopamine-β-hydroxylase in rat adrenal glands. J Biol Chem 250: 3204–3211Google Scholar
  9. Donaldson EM (1981) The pituitary-interrenal axis as an indicator of stress in fish. In: AD Pickering (ed) Stress and fish. Academic Press, London New York Toronto Sydney San Francisco, pp 11–48Google Scholar
  10. Evinger MJ, Towle AC, Park DH, Lee P, Joh TH (1992) Glucocorticoids stimulate transcription of the rat phenylethanolamine-N-methyltransferase (PNMT) gene in vivo and in vitro. Cell Mol Neurobiol 12: 193–215Google Scholar
  11. Fritsche R, Reid SG, Thomas S, Perry SF (1993) Serotonin-mediated release of catecholamines in the rainbow trout Oncorhynchus mykiss. J Exp Biol 178: 191–204Google Scholar
  12. Gamperl AK, Vijayan MM, Boutilier RG (1994) Experimental control of stress hormone levels in fishes: techniques and applications. Rev Fish Biol Fisheries 4: 215–255Google Scholar
  13. Hathaway CB, Epple A (1989) The sources of plasma catecholamines in the American eel. Anguilla rostrata. Gen Comp Endocrinol 74: 418–430Google Scholar
  14. Jiang W, Uht R, Bohn MC (1989) Regulation of phenylethanolamine-N-methyltransferase (PNMT) mRNA in the rat adrenal medulla by corticosterone. Int J Dev Neurosci 7: 513–520Google Scholar
  15. Jönsson A-C (1983) Catecholamine formation in vitro in the systemic and portal hearts of the Atlantic hagfish, Myxine glutinosa. Mol Physiol 3: 297–304Google Scholar
  16. Jönsson A-C, Wahlqvish I, Hansson T (1983) Effects of hypophysectomy and cortisol on the catecholamine biosynthesis and catecholamine content in chromaffin tissue from rainbow trout, Salmo gairdner. Gen Comp Endocrinol 51: 278–285Google Scholar
  17. Livett BG, Marley PD (1993) Noncholinergic control of adrenal catecholamine secretion. J Anat 183: 277–289Google Scholar
  18. Mazeaud MM (1972) Epinephrine biosynthesis in Petromyzon (Cyclostoma) and Salmo gairdneri (teleost). Comp Gen Pharmacol 3: 457–468Google Scholar
  19. Nakano T, Tomlinson N (1967) Catecholamine and carbohydrate concentrations in the rainbow trout (Salmo gairdneri) in relation to physical disturbances. J Fish Res Board Can 24: 1701–1715Google Scholar
  20. Nandi J (1961) New arrangement of interrenal and chromaffin tissues of teleost fish. Science 134: 389–390Google Scholar
  21. Nilsson S (1983) Autonomic nerve function in the vertebrates. Zoophysiology, vol 13. Springer, BerlinGoogle Scholar
  22. Nilsson GE (1989) Effects of anoxia on catecholamine levels in brain and kidney of the crucian carp. Am J Physiol 257: R10-R14Google Scholar
  23. Nilsson GE (1990) Long-term anoxia in the crucian carp: changes in the levels of amino acid and monoamine neurotransmitters in the brain, catecholamines in the chromaffin tissue, and liver glycogen. J Exp Biol 150: 295–320Google Scholar
  24. Nilsson GE, Block M (1991) Decreased norepinephrine and epinephrine contents in the chromaffin tissue of the rainbow trout (Oncorhynchus mykiss) exposed to diethyldithiocarbamate and amylxanthate. Comp Biochem Physiol 98C: 391–394Google Scholar
  25. Ottaviani E, Caselgrandi E, Petraglia F, Franceschi C (1992) Stress response in the freshwater snail Planorbarius coreneus (L.) (Gastropoda, Pulmonata)-interaction between CRF, ACTH and biogenic amines. Gen Comp Endocrinol 87: 354–360Google Scholar
  26. Perry SF, Kinkead R, Gallaugher P, Randall DJ (1989) Evidence that hypoxemia promotes catecholamine release during hypercapnic acidosis in rainbow trout (Salmo gairdneri). Respir Physiol 77: 351–364Google Scholar
  27. Perry SF, Fritsche R, Kinkead R, Nilsson S (1991) Control of catecholamine release in vivo and in situ in the Atlantic cod (Gadus morhua) during hypoxia. J Exp Biol 155: 549–566Google Scholar
  28. Perry SF, Reid SD (1993) β-adrenergic signal transduction in fish: interactive effects of catecholamines and cortisol. Fish Physiol Biochem 11: 195–203Google Scholar
  29. Perry SF, Fritsche R, Thomas S (1993) Storage and release of catecholamines from the chromaffin tissue of the Atlantic hagfish. J Exp Biol 183: 165–184Google Scholar
  30. Perry SF, Reid SG (1994a) Injection techniques. In: Hochachka P, Mommsen T (eds) Biochemistry and molecular biology of fishes, vol 3. Elsevier Science, pp 85–92Google Scholar
  31. Perry SF, Reid SG (1994b) The effects of acclimation temperature on the dynamics of catecholamine release during acute hypoxia in the rainbow trout, Oncorhynchus mykiss. J Exp Biol 186: 289–307Google Scholar
  32. Pickering AD, Pottinger TG, Sumpter JP, Carragher JF, Le Bail PY (1991) Effects of acute and chronic stress on the levels of circulating growth hormone in the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 83: 86–93Google Scholar
  33. Randall DJ, Perry SF (1992) Catecholamines. In: Randall DJ et al (eds) Fish physiology, vol 12B. Academic Press, New York, pp 255–300Google Scholar
  34. Reid SD, Perry SF (1991) The effects and physiological consequences of raised levels of cortisol on rainbow trout (Oncorhynchus mykiss) erythrocyte β-adrenoceptors. J Exp Biol 158: 217–240Google Scholar
  35. Reid SD, Moon TW, Perry SF (1991) Characterization of β-adrenoceptors of rainbow trout (Oncorhynchus mykiss) erythrocytes. J Exp Biol 158: 199–216Google Scholar
  36. Reid SD, Moon TW, Perry SF (1992) Rainbow trout (Oncorhynchus mykiss) hepatocyte β-adrenoceptors, catecholamine responsiveness and the effects of cortisol. Am J Physiol 262: R794-R799Google Scholar
  37. Reid SD, Lebras Y, Perry SF (1993) The in vitro effect of hypoxia on the trout erythrocyte β-adrenergic signal transduction system. J Exp Biol 176: 103–116Google Scholar
  38. Reid SG, Perry SF (1994) Storage and differential release of catecholamines in rainbow trout (Oncorhynchus mykiss) and American eel (Anguilla rostrata). Physiol Zool 67: 216–237Google Scholar
  39. Reid SG, Furimsky M, Perry SF (1994) The effects of repeated physical stress or fasting on catecholamine storage and release in the rainbow trout, Oncorhynchus mykiss. J fish Biol 45: 365–378Google Scholar
  40. Reid SG, Fritsche R, Jönsson A-C (1995) Immunohistochemical localization of bioactive peptides and amines associated with the chromaffin tissue of five species of fish. Cell Tissue Res 280: 499–512Google Scholar
  41. Ross ME, Evinger MJ, Hyman SE, Carroll JM, Mucke L, Comb M, Reis DJ, Joh TH, Goodman HM (1990) Identification of a functional glucocorticoid response element in the phenylethanolamine-N-methyltransferase promoter using fusion genes introduced into chromaffin cells in primary culture. J Neurosci 10: 520–530Google Scholar
  42. Vijayan MM, Leatherland JF (1989) Cortisol-induced changes in plasma glucose, protein, and thyroid hormone levels and liver glycogen content of coho salmon (Oncorhynchus kisutch Walbaum). Can J Zool 67: 2746–2750Google Scholar
  43. Vijayan MM, Leatherland JF (1990) High stocking density affects cortisol secretion and tissue distribution in brook charr, Salvelinus fontinalis. J Endocrinol 124: 311–318Google Scholar
  44. Vijayan MM, Ballantyne JS, Leatherland JF (1991) Cortisol-induced changes in some aspects of the intermediary metabolism of Salvelinus fontinalis. Gen Comp Endocrinol 82: 476–486Google Scholar
  45. Vijayan MM, Moon TW (1992) Acute handling stress alters hepatic glycogen metabolism in food deprived rainbow trout (Oncorhynchus mykiss). Can J Fish Aqu Sci 49: 2260–2266Google Scholar
  46. Wan DC-C, Livett BG (1989) Induction of phenylethanolamine-N-methyltransferase mRNA expression by glucocorticoids in cultured bovine adrenal chromaffin cells. Eur J Pharmacol 172: 107–115Google Scholar
  47. Wolf K (1963) Physiological salines for freshwater teleosts. Progr Fish Cult 25: 135–140Google Scholar
  48. Wong DL, Bildstien CL, Siddall B, Lesage A, Young Sook Yoo (1993) Neural regulation of phenylethanolamine-N-methyltransferase in vivo: transcriptional and translational changes. Mol Brain Res 18: 107–114Google Scholar
  49. Woodward JJ (1982) Plasma catecholamines in resting rainbow trout, Salmo gairdneri Richardson, by high-pressure liquid chromatography. J Fish Biol 21: 429–432Google Scholar
  50. Wurtman RJ, Axelrod J (1966) Control of enzymatic synthesis of adrenaline in the adrenal medulla by adrenal cortical steroids. J Biol Chem 241: 2301–2305Google Scholar
  51. Wurtman RJ, Noble EP, Axelrod J (1967) Inhibition of enzymatic synthesis of epinephrine by low doses of glucocorticoids. Endocrinology 80: 825–828Google Scholar
  52. Wurtman RJ, Axelrod J, Veseli ES, Ross GT (1968) Species differences in inducibility of phenylethanolamine-N-methyltransferase. Endocrinology 82: 584–590Google Scholar
  53. Yamamoto KR (1985) Steroid receptor regulated transcription of specific genes and gene networks. Anuu Rev Genet 19: 209–252Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • S. G. Reid
    • 1
  • M. M. Vijayan
    • 1
  • S. F. Perry
    • 1
  1. 1.Department of BiologyUniversity of OttawaOttawaCanada

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