Potassium channels in primary cultures of seawater fish gill cells. II. Channel activation by hypotonic shock

Abstract

Previous studies performed on apical membranes of seawater fish gills in primary culture have demonstrated the existence of stretch-activated K(+) channels with a conductance of 122 pS. The present report examines the involvement of K(+) channels in ion transport mechanisms and cell swelling. In the whole cell patch-clamp configuration, K(+) currents were produced by exposing cells to a hypotonic solution or to 1 microM ionomycin. These K(+) currents were inhibited by the addition of quinidine and charybdotoxin to the bath solution. Isotopic efflux measurements were performed on cells grown on permeable supports using (86)Rb(+) as a tracer to indicate potassium movements. Apical and basolateral membrane (86)Rb effluxes were stimulated by the exposure of cells to a hypotonic medium. During the hypotonic shock, the stimulation of (86)Rb efflux on the apical side of the monolayer was inhibited by 500 microM quinidine or 100 microM gadolinium but was insensitive to scorpion venom [Leirus quinquestriatus hebraeus (LQH)]. An increased (86)Rb efflux across the basolateral membrane was also reduced by the addition of quinidine and LQH venom but was not modified by gadolinium. Moreover, basolateral and apical membrane (86)Rb effluxes were not modified by bumetanide or thapsigargin. There is convincing evidence for two different populations of K(+) channels activated by hypotonic shock. These populations can be separated according to their cellular localization (apical or basolateral membrane) and as a function of their kinetic behavior and pharmacology.

Swelling-activated transport of taurine in cultured gill cells of sea bass: physiological adaptation and pavement cell plasticity

“…RVD occurs through an efflux of K ϩ , Cl Ϫ , and organic osmolytes accompanied by osmotically obligate water loss (20,28). We have previously demonstrated the presence of stretch-activated K ϩ channels in sea bass gill cells and discussed their mechanosensitivity during hypotonic-induced cell swelling (12,13). This study focuses taurine permeability in response to hypoosmotic shock.…”

“…When asymmetrical osmotic shocks were applied, we observed higher permeability and sensitivity of the basolateral membrane compared with the apical membrane. In a previous study, we described the relative impermeability of the apical side of sea bass gill epithelium in culture toward Cl Ϫ when measuring 125 I flux (reflecting chloride flux) during asymmetrical hypoosmotic shock (13). Moreover, Gilmour et al (15) found a reduction of the transcellular permeability and an increase in transepithelial resistance when the apical membrane of gill cells in culture was exposed to hypotonicity (freshwater).…”

“…Moreover, we found that gill pavement cells in culture were important for ionic transport and more specifically Cl Ϫ transport (3). We also described the relative impermeability of the apical membrane of sea bass gill epithelium during hypotonic shock as a possible adaptation of this tissue to limit cell invasion by water (13). Hence, gill cells (and more specifically pavement cells), which have been proven to be involved in osmotic regulation, can represent a very good model for investigating RVD mechanism and molecular adaptations to salinity changes.…”

Regulatory volume decrease and P receptor signaling in fish cells: mechanisms, physiology, and modeling approaches

“…Thus, the presence of voltage‐sensitive K + efflux, inhibited e.g. by BaCl 2 , was reported in goldfish renal proximal tubules (Terreros et al, '90), sea bass ( Dicentrarchus labrax ) gill cells (Duranton et al, 2000b), trout red cells (Egée et al, 2000), Gobius niger enterocytes (Trischitta et al, 2004), turbot hepatocytes (Ollivier et al, 2006c), and Gilthead sea bream hepatocytes (Faggio et al, 2011). In contrast, BaCl 2 was without effect on swelling‐induced K + fluxes in rainbow trout hepatocytes (Bianchini et al, '88) and brown trout ( Salmo trutta ) proximal renal tubules (Kanli and Norderhus, '98), indicating not only cell‐specific, but also species‐specific differences in the expression of the transporter.…”

Effects of carbon monoxide on trout and lamprey vessels

“…Although one study has suggested that CO activates K ATP channels (20), most (54 -56, 60) have focused more on CO binding and activation of large-conductance Ca 2ϩ -activated K ϩ (BK Ca ) channels. Previous studies have demonstrated the apparent presence of K Ca channels in isolated retinal ganglion cells from trout (26,27), and even charybdotoxin-sensitive gill epithelial cells from sea bass, Dicentrarchus labrax (16). However, these channels have yet to be characterized in trout vascular smooth muscle.…”