Endocrine control of Na+,K+-ATPase and chloride cell development in brown trout (Salmo trutta): Interaction of insulin-like growth factor-I with prolactin and growth hormone

Abstract

A 2-factorial (3 x 3) injection experiment was used to investigate the effect and interaction between different hormones on the initial phase of seawater (SW) acclimation in brown trout (Salmo trutta). Each fish was given 4 injections on alternate days in freshwater (FW). Factor 1 was either saline, 2 μg ovine prolactin (oPRL)/g, or 2 μg ovine growth hormone (oGH)/g. Factor 2 was either 0, 0.01, or 0.1 μg recombinant human insulin- like growth factor-I (rhIGF-I)/g. In each of the 9 treatment groups, half of the fish were subjected to a 48-h SW-challenge test, and the remaining fish were sham-transferred to FW one day after the last injection. Hypo- osmoregulatory performance was increased by GH and impaired by PRL treatment as judged by changes in plasma osmolality, [Na+], [Cl-], total [Mg] and muscle water content (MWC) after SW transfer. IGF-I reduced plasma osmolality after transfer to SW but had no effect on plasma total [Mg] or MWC. The effects of the two factors on plasma osmolality, [Na+], [Cl-], and MWC were additive. In sham-transferred fish, GH and IGF-I, alone and in combination, stimulated Na+,K+-ATPase α-subunit mRNA (α-mRNA) content in the gill. This was paralleled by an overall increase in gill Na+,K+-ATPase activity in fish treated with 0.01 μg IGF-I/g. Simultaneous administration of PILL completely inhibited the increase in gill α-mRNA observed in the IGF-I- injected groups. Combination of GH and IGF-I did not further affect the α- mRNA level relative to the single hormone-injected groups. There was an overall decrease in Na+,K+-ATPase activity in pyloric caeca and middle intestine by the low dose and both doses of IGF-I respectively. No effect was observed in the posterior intestine. PRL and GH treatments did not affect enzyme activity in any intestinal segment. Both doses of IGF-I increased Na+,K+-ATPase-immunoreactive (NKIR) cell density in gill primary filaments. PRL and GH had no effect on primary filament NKIR cell density. GH and both doses of IGF-I reduced secondary lamellar NKIR cell density, whereas PRL had no effect. The main conclusion is that IGF-I and GH induce an overall redistribution of NKIR cells away from the secondary lamella onto the primary filament of FW-acclimated trout. This is associated with an overall increased α-mRNA level in the gill, which may reflect an increased expression within individual NKIR cells in the primary filament. PILL completely abolished the IGF-I stimulation of α-mRNA levels, suggesting a desensitisation of the gill tissue to IGF-I, which may explain the overall anti-SW adaptive effect of PRL.