[Beta adrenergic receptors on the branchial epithelial cells of trout (Salmo gairdneri) adapted to seawater].
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Biomedical subjects
Publications and source records attributed to P Payan.
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The present study discusses the respective roles of the chloride and respiratory cells in branchial ion exchange in freshwater- and seawater-adapted teleosts. In the gill, two distinct epithelia are defined according to their blood irrigation and cellular characteristics: the primary lamellar epithelium containing mostly chloride cells is functionally connected to the venous compartment; the secondary lamellar epithelium consisting of respiratory cells is irrigated by the arterioarterial circulation. The fundamental reorganization occurring in the chloride cells during adaptation to seawater consists of the appearance of leaky ultrastructure related to an increase in the ionic and nonelectrolyte permeabilities of the primary lamellar epithelium. The physiological functions of respiration, excretion, and the maintenance of acid-base balance occur through the secondary lamellar epithelium both in freshwater and seawater fish. The increase of the exchange diffusion across the secondary lamellar epithelium on seawater adaptation is directly related to the increase in the external salinity. The study of adrenergic control in the teleost gill emphasizes the functional advantage to the fish during adaptation to seawater of the anatomic separation of the osmoregulatory primary lamellar epithelium.
A Na+/NH4+ exchange similar to that characterizing the fish gill in fresh water was shown to function in the trout adapted to sea water with the help of the head perfusion technique. This exchange stimulated by adrenaline through beta adrenoreceptors and inhibited by amiloride added to the external medium.
The effects of adrenaline on the Na+ and Cl- influxes in the seawater adapted trout were studied with the perfused isolated head technique. With 10(-5) M adrenaline in the perfusion fluid, the lamellar influx of Na+ is increased by 60%, while the Cl- influx is inhibited by 90%. This catecholamine does not modify the extra-lamellar entry of NaCl which passes into the filamental sinus.
In the perfused head of Trout the gills are the site of ammonia clearance which corresponds exactly to the appearance rate of ammonia in the external medium. Thus metabolic production of ammonia by the gill apparently does not participate to its excretion. Under ammonia-free Ringer perfusion however, endogenous production is observed and ammonia is excreted in both external and internal media.
1. Sodium and chloride influxes across the gills of sea water adapted trout were studied with the perfused isolated head technique. 2. The haemodynamic scheme describing anastomoses between efferent gill arteries and the filamentous sinus was confirmed and utilized to determine partitioning of sodium and chloride influxes. 3. Two routes of sodium and chloride entry were demonstrated, one lamellar and the other sinusal. The lamellar sodium and chloride fluxes are respectively 133+/-21-8 and 271+/-43-7 micronequiv/hr. 100 g. The sinus sodium and chloride fluxes are: 50+/-18-3 and 50+/-11-3 micronequiv/hr. 100 g. 4. The relative permeabilities of the apical and basal barriers of the lamellar epithelium were determined with influx experiments coupled to radioactive unloading experiments. The basal membrane is 30 times less permeable than the apical to sodium, while this ratio is 45 for chloride. Thus, the basal membrane represents the limiting factor in salt movement across the branchial epithelium. 5. The intracellular pools of the lamellar compartment were calculated for sodium: 1-1+/-0-17 micronequiv/100 g of fish weight; and for chloride: 5-1+/-0-83 micronequiv/100 g of fish weight.
1. Na and Cl intake through the gill of the perfused head of trout were studied in fresh water with (10(-5)M) or without adrenaline in the perfusing solution. 2. Ionic influxes occur exclusively across the lamellae in fresh water while in the sea-water adapted trout part of salt entry is extralamellar. 3. In absence of adrenaline, Na and Cl enter the gills at the same rate (respectively 6.9 +/- 1.30 and 6.6 +/- 1.55 muequiv/hr. 100 g). Adrenaline (10(-5)M) increased the Na influx to 47.8 +/- 4.12 muequiv/hr. 100 g, a value similar to that observed in vivo. The Cl influx remains unchanged however (6.3 +/- 2.40 muequiv/hr. 100 g), a value much smaller than that found in vivo. 4. Radioactive loading experiments coupled with unloading experiments allowed the determination of the relative permeabilities of the serosal and mucosal barrier for Na+ and Cl-. For both ions, the basal membrane is less permeable. Adrenaline by increasing the Na permeability across the apical barrier enhances the active Na pumping through the basal membrane. 5. Intracellular Na and Cl exchangeable pools were calculated. They represent less than 1% of the total ionic content of the epithelium. Adrenaline increased by sixfold the Na pool without modifying the Cl pool.
A technique of perfusing the isolated head of trout with a constant-fluid flow was used to study adrenergic factors controlling the vasomotricity of the gill. The use of adrenergic blockers (phentolamine 10(-4) M and propranolol 10(-4) M) enabled the vascular effect of epinephrine to be split into two components: an alpha-vasoconstrictor effect superimposed upon the dominant beta-vasodilator effect. Effect alpha appears more rapidly than effect beta and causes an initial vasoconstriction. Under constant-flow perfusion the effect of epinephrine on the efferent arterial and venous flows is a diminution of the venous flow and an increase of the arterial. This is the result of closure of the anastomoses between the efferent artery and the central compartment of the filament. It was shown that only alpha-vasoconstrictor adrenoreceptors occur in this region.
The filling of the gills and head vascular space of a teleost fish was measured in vitro by perfusing an isolated head of a trout with a Ringer solution containing 131I-labeled human serum albumin. The presence of epinephrine in the Ringer solution significantly increased afferent (ventral aortic) flow rate and efferent (dorsal aorta) flow rate, whereas branchial venous system circulation was reduced. When perfused with an epinephrine-free Ringer, the branchial vascular space appears 5-6 times greater than the head vascular space (per 100 g of tissue). Epinephrine, 10(-5) M, in the Ringer solution significantly decreased the branchial vascular space without modifying that of the head. The increase in perfusion rate and decrease in branchial vascular space due to the epinephrine can only be interpreted by taking into account a branchial nonlamellar compartment of a considerable volume.
The gills of the dogfish Scyliorhinus canicula are more permeable to Cl than to Na. In sea water, influx of Na and Cl exceeded the efflux of these ions. Under these conditions the fish were slightly electronegative, by about 2 mV, to the external solution. The net accumulation of Cl could be accounted for by diffusion along the observed electrochemical gradient byt the movement of Na into the fish was more consistent with an electrically neutral active Na transport mechanism (using the Ussing flux ratio criterion). When the external pH was was changed from 7-8 to 6-9,, influxes of Na and Cl were depressed, while the effluxes were unaffected, and the fish became slightly less electronegative. In artificial solutions, in which the concentrations of Na and Cl were lowered and replaced with urea to maintain the total osmotic concentration, Na influx displayed saturation kinetics, while Na efflux increased with decreasing Na concentrations. Cl influx decreased linearly, while Cl efflux remained constant. The efflux of Cl could not be reconciled with a process of passive diffusion along any of the observed electrochemical gradients and thus could reflect the presence of an active transport mechanism.
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