Abstract
Brown trout were fitted with indwelling, intraperitoneal catheters and injected with 4–6 μmol · kg-1 of the α-receptor agonist phenylephrine or the β-receptor agonist isoproterenol. The intracellular concentrations of sodium, chlorine, potassium and phosphorus in the pavement epithelial cells and the mitochondria-rich cells of the branchial epithelium were measured by X-ray microanalysis 1 h after the injection of the adrenoreceptor agonists. Injection with phenylephrine resulted in a significant increase in intracellular chlorine and potassium in mitochondria-rich cells and a significant but relatively smaller increase in chlorine in pavement epithelial cells. Injection with isoproterenol resulted in a significant increase in sodium and chlorine concentration in pavement epithelial cells and a significant decrease in potassium concentration. The only significant effect of isoproterenol injection on mitochondria-rich cells was a decrease in intracellular chlorine concentration. The results suggest that these adrenoreceptor agonists have a direct effect on the influx of Na+ and Cl- across the branchial epithelium. These effects may be a mechanism for acid-base regulation during the severe stress conditions that elicit catecholamine release in vivo. These results corroborate previous studies using X-ray microanalysis which suggested that pavement epithelial cells are the sites of Na+ uptake in freshwater fish whilst Cl- uptake occurs via mitochondria-rich cells.
Similar content being viewed by others
Abbreviations
- LTSEM :
-
low-temperature scanning electron microscope
- MR cells :
-
mitochondria-rich cells
- PE cells :
-
pavement epithelial cells
- XRMA :
-
X-ray microanalysis
References
Aota S, Holmgren KD, Gallaugher P, Randall DJ (1990) A possible role for catecholamines in the ventilatory responses associated with internal acidosis or external hypoxia in the rainbow trout Oncorhynchus mykiss. J Exp Biol 151:57–70
Avella M, Masoni A, Bornancin M, Mayer-Gostan N (1987) Gill morphology and sodium influx in the rainbow trout (Salmo gairneri) acclimated to artificial freshwater environments. J Exp Biol 241:159–169
Boutilier RG, Dobson GP, Hoeger U, Randall DJ (1988) Acute exposure to graded levels of hypoxia in rainbow trout (Salmo gairdneri): metabolic and respiratory adaptations. Respir Physiol 71:69–82
Farrell AP, Sobin SS, Randall DJ, Crosby S (1980) Intralamellar blood flow patterns in fish gills. Am J Physiol 239: R429-R436
Goss GG, Laurent P, Perry SP (1992) Evidence for a morphological component in acid-base regulation during environmental hypercapnia in the brown bullhead (Ictalurus nebulosus). Cell Tissue Res 268:539–552
Harvey BJ (1992) Energization of sodium absorption by the H+-ATPase pump in mitochondria-rich cells of frog skin. J Exp Biol 172:289–230
Laurent P, Hobe H, Dunel-Erb S (1985) The role of environmental sodium chloride relative to calcium in gill morphology of fresh-water salmonid fish. Cell Tissue Res 240:675–692
Laurent P, Goss GG, Perry SF (1994) Proton pumps in fish gill pavement cells? Arch Int Physiol Biochim Biophys 102:77–79
Lin H, Pfeiffer DC, Vogl AW, Pan J, Randall DJ (1994) Immunolocalization of H+-ATPase in the gill epithelia of rainbow trout. J Exp Biol 195:169–183
McDonald DG, Rogano MS (1986) Ion regulation by the rainbow trout (Salmo gairdneri) in ion-poor water. Physiol Zool 59: 318–331
McDonald DG, Tang Y, Boutilier RG (1989a) The role of β-adrenoreceptors in the recovery from exhaustive exercise of freshwater-adapted rainbow trout. J Exp Biol 147:471–491
McDonald DG, Tang Y, Boutilier RG (1989b) Acid and ion transfer across the gills of fish: mechanisms and regulation. Can J Zool 67:3046–3054
Morgan IJ, Potts WTW (1995) The effects of thiocyanate on the intracellular ion concentrations in branchial epithelial cells of brown trout. J Exp Biol 198:1129–1232
Morgan IJ, Potts WTW, Oates K (1994) Intracellular ion concentrations in branchial epithelial cells of brown trout (Salmo trutta L.) determined by X-ray microanalysis. J Exp Biol 194:139–151
Motais R, Scheuring F, Borgese F, Garcia-Romeu F (1990) Characteristics of β-adrenergic-activated Na-proton transport in red blood cells. In: Ritchie JH et al. (eds) Progress in cell research, vol 1. Elsevier, Amsterdam, pp 179–193
Nikinmaa M (1990) Vertebrate red blood cells. Zoophysiology, vol. 28. Springer, Heidelberg
Nilsson S (1984) Innervation and pharmacology of the gills. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol. XA. Academic Press, New York, pp 185–227
Oates K, Potts WTW (1985) Electron beam penetration and X-ray excitation depth in ice. Micron Microsc Acta 16:1–4
Perry SF, Laurent P (1989) Adaptational responses of rainbow trout to lowered external NaCl concentration: contribution of the branchial chloride cell. J Exp Biol 147:147–168
Perry SF, Payan P, Girard JP (1984a) Adrenergic control of branchial chloride transport in the isolated perfused head of the freshwater rainbow trout (Salmo gairdneri). J Comp Physiol B 154:269–274
Perry SF, Daxboeck C, Ellis AG, Smith DJ (1984b) Perfusion methods for the study of gill physiology. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol. XB. Academic Press, New York
Perry SF, Malone S, Ewing D (1987) Hypercapnic acidosis in the rainbow trout (Salmo gairdneri). I. Branchial ionic fluxes and blood acid-base status. Can J Zool 65:888–895
Perry SF, Kinkead R, Fritsche R (1992) Are circulating catecholamines involved in the control of breathing by fishes? Rev Fish Biol Fish 2:65–83
Randall DJ, Daxboeck C (1984) Oxygen and carbon dioxide transfer across fish gills. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol. XA. Academic Press, London, pp 263–314
Randall DJ, Perry SF (1992) Catecholamines. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol. XIIB. Academic Press, London, pp 255–300
Randall DJ, Taylor EW (1992) Control of breathing in fish. Evidence of a role for catecholamines. Rev Fish Biol Fish 1: 139–157
Tang Y, Boutilier RG (1988) Correlation between catecholamine release and degree of acidototic stress in rainbow trout, Salmo gairdneri. Am J Physiol 255:R395-R399
Vermette MG, Perry SF (1987) The effects of prolonged epinephrine infusion on the physiology of the rainbow trout, Salmo gairdneri. II. Branchial solute fluxes. J Exp Biol 128:255–267
Vermette MG, Perry SF (1988) Effects of prolonged epinephrine infusion on blood respiratory and acid-base states in the rainbow trout: alpha and beta effects. Fish Physiol Biochem 4:189–202
Wood CM (1988) Acid-base and ionic exchanges at gills and kidney after exhaustive exercise in the rainbow trout. J Exp Biol 136: 461–481
Author information
Authors and Affiliations
Additional information
Communicated by H. Huddart
Rights and permissions
About this article
Cite this article
Morgan, I.J., Potts, W.T.W. The effects of the adrenoreceptor agonists phenylephrine and isoproterenol on the intracellular ion concentrations of branchial epithelial cells of brown trout (Salmo trutta L.). J Comp Physiol B 165, 458–463 (1995). https://doi.org/10.1007/BF00261300
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00261300