Neurohypophysial hormone regulation of Cl- secretion: physiological evidence for V1-type receptors in sea bass gill respiratory cells in culture

Abstract

Neurohypophysial hormone receptors were studied in primary cultures of sea bass (Dicentrarchus labrax) gill respiratory-like cells grown on permeable supports. This preparation was previously shown to provide a functional model for investigating the hormonal regulation of Cl secretion.Under control conditions, the cultured monolayered epithelium had a short-circuit current (I SC ) of 3·5 1·1 µA cm 2 . This current had previously been identified as an active Cl secretion. The addition of increasing concentrations of the fish neurohypophysial hormones, arginine vasotocin (AVT) or isotocin (IT), elicited a concentration-dependent stimulation of the I SC . Maximal increases of 60·9 12·1% and 117·7 28·0% above the basal I SC value were obtained for 10 7 M AVT and IT respectively. Half-maximal effects were obtained for 3·1 10 9 M AVT and for 1·4 10 9 M IT. Mucosal application of 1·0 mM diphenylalamine-2-carboxylic acid (a specific blocker of Cl channels) after serosal addition of 5 10 8 M AVT or IT inhibited not only the basal but also the stimulated current, revealing a correlation with a hormone-dependent Cl transport.Specific V1 or V2 receptor analogues of vasopressin (mammalian hormone) were used to characterize the type of neurohypophysial hormone receptors pharmaco- ]-vasopressin used at the same concentration had no significant effect. In contrast, similar experiments carried out in the presence of 10 8 M IT showed that both antagonists significantly reduced the IT-stimulated Cl secretion, with the efficiency of the V1 receptor antagonist being significantly greater than that of the V2.This study provides evidence for neurohypophysial hormone control of Cl secretion in fish cultured gill respiratory cells. It suggests that on a physiological basis the hormonal effect is shared by the two peptides present in fish neurohypophysis (AVT and IT), acting by means of two distinct, although pharmacologically similar, V1-type receptors (according to the mammalian classification). These specific receptors are expected to play an important role in controlling ion homeostasis in seawater fish.

Cortisol modulates vasotocinergic and isotocinergic pathways in the gilthead sea bream (Sparus aurata, Linnaeus 1758)

“…The pattern of changes in plasma AVT and IT levels (see above), as well as expression of the AVT and IT receptors within the gill (Fig. 7), suggests that stimulation of the vasotocinergic and isotocinergic systems could be important for increasing sodium and chloride secretion during the initial stress period, which has previously been described in Carassius auratus (Maetz et al, 1964) and following hormonal administration to gill respiratory cell culture in Dicentrarchus labrax (Guibbolini and Avella, 2003).…”

New insights into neuropeptide modulation of aggression: field studies of arginine vasotocin in a territorial tropical damselfish

“…The V1a receptor is the dominant one expressed in the brain (Strand 1999) and, while the V2 receptor mainly has a peripheral distribution, the V1b receptor is also distributed in the brain (Strand 1999) making it a candidate also to mediate behavioural modulation by AVT. While only V1-type receptors have so far been identified in teleosts (Mahlmann et al 1994;Warne 2001;Guibbolini & Avella 2003), the presence of multiple AVT receptor subtypes in other taxa at least suggests their presence and possible co-modulation of behaviour among teleosts.…”

“…However, Manning compound, an AVP antagonist specific to the V1a receptor (see Barberis et al 1999) that is commonly used as an AVT V1 receptor antagonist in teleosts (e.g. Mahlmann et al 1994;Goodson & Bass 2000a;Guibbolini & Avella 2003), does not show the reciprocal effect. Manning compound decreases T-TP aggression towards IP males, but has no influence on T-TP aggression towards T-TP males (Semsar et al 2001).…”

Molecular cloning, sequencing and phylogeny of vasotocin receptor genes in the air-breathing catfish Heteropneustes fossilis with sex dimorphic and seasonal variations in tissue expression

“…VT administration caused an increase in urine volume, osmolarity and sodium levels in hypophysectomized catfish (Parwez and Goswami 1985). Studies in other fishes have also shown that VT secretion is sensitive to changes in environmental salinity, which regulates water and ionic exchanges through the cognate receptors (Mahlmann et al 1994;Kulczykowska 2001;Warne 2001;Warne et al 2002;Guibbolini and Avella 2003;Balment et al 2006). In the catfish, the three VT receptor subtype genes are expressed in the gill and kidney in both sexes, implying a VT regulation of their functions.…”

“…In the trout Oncorhynchus mykiss, Conklin et al (1999) characterized pharmacologically the V1A-type receptor that mediated the VT-induced vascular smooth muscle contraction. In cultured gill epithelium of European sea bass (Dicentrarchus labrax), VT and the V1-type receptor agonist [Phe2, Orn8]-oxytocin were found to stimulate Cl -secretion while the V2-type receptor agonist failed to produce any effect (Guibbolini and Avella 2003). A V2-type receptor, or at least one that acted by altering the intracellular cAMP level, was reported in isolated renal tubules from the rainbow trout by Perrott et al (1993).…”