Interrelationships between gill chloride cell morphology and calcium uptake in freshwater teleosts

Abstract

The involvement of the freshwater fish gill chloride cells (CCs) in trans-branchial calcium uptake (JinCa(2+)) was investigated. This was accomplished by assessing the interspecific relationships between the apical surface area of CCs exposed to the external environment and JinCa(2+). Three species of freshwater teleosts, the rainbow trout (Oncorhynchus mykiss), the American eel (Anguilla rostrata) and the brown bullhead catfish (Ictalurus nebulosus), were used. Chronic (ten-day) treatment with cortisol in each species was used as a tool to evoke variations in both JinCa(2+) and gill CC morphology in order to assess intraspecific relationships between CC surface area and JinCa(2+). The results of quantitative morphometry, based on analysis of scanning electron micrographs, demonstrated that catfish possessed the lowest fractional area of exposed CC (CCFA) on the gill filament epithelium (12,744 ± 2248 μm(2)/mm(2)) and was followed, in increasing order, by American eel (21,355 ± 981 μm(2)/mm(2)) and rainbow trout (149,928 ± 26,545 μm(2)/mm(2)). With the exception of catfish, chronic treatment with cortisol caused significant increases in CCFA owing to proliferation of CCs and/or enlargement of individual CCs (eel only). The rates of JinCa(2+) closely reflected the CC fractional area in each species. The results of correlation analysis revealed significant correlations between CC fractional area and JinCa(2+) in trout and eel. Owing to the absence of an effect of cortisol treatment, there was no significant correlation in catfish because of insufficient variation in CC fractional area in this species. CC fractional area was significantly correlated with JinCa(2+) among the three species examined. These results suggest that CC is involved in calcium uptake in freshwater teleosts and that both intra- and interspecific differences in the rates of calcium uptake can be accounted for by variability in the surface area of exposed CCs on the gill epithelia.

Short-term transformation and long-term replacement of branchial chloride cells in killifish transferred from seawater to freshwater, revealed by morphofunctional observations and a newly established `time-differential double fluorescent staining' technique

“…In killifish gills, seawater-type chloride cells have an apical pit and interdigitate with neighboring accessory cells to form multicellular complexes, whereas the apical membrane is flat or protrusive with developed microvilli on it in freshwater-type cells (Katoh et al, 2001). A similar apical membrane structure has been observed in several species adapted to freshwater (Hossler et al, 1985;Laurent and Hebibi, 1988;Perry et al, 1992;Shawn et al, 1993;Greco et al, 1996;Perry, 1997Perry, , 1998Kelly et al, 1999). …”

The effects of thermally induced gill remodeling on ionocyte distribution and branchial chloride fluxes in goldfish (Carassius auratus)

“…It is puzzling that the changes in ionocyte SA were not accompanied by similar changes in NKA activities, and clearly this result begs the question as to which metric is a better indicator of branchial ion transport capacity. Given the tight correlation between ionocyte SA and ionic uptake in freshwater teleosts (Perry et al, 1992a;Perry et al, 1992b) and the reports of a lack of correspondence between NKA activities and ionocyte abundance (McCormick, 1995;Sloman et al, 2001), the more reliable indicator would seem to be ionocyte SA. The fact that Cl -uptake did not significantly increase with increasing ionocyte SA in the present study suggests that one or more other factors (including NKA activity) are regulating this process in the fish experiencing gill remodeling.…”

Hormonal and environmental regulation of epithelial calcium channel in gill of rainbow trout (Oncorhynchus mykiss)

“…On the basis of these and other indirect or correlative studies (18,26,28,32), a model was constructed (27) in which the MRC was implicated as the principal (potentially exclusive) cell type responsible for Ca 2ϩ uptake. In the present study, however, immunocytochemical analysis of gill cross sections in fish exposed to soft water failed to demonstrate strong colocalization of Na ϩ /K ϩ -ATPase (representative of MRCs) and ECaC-positive cells (Fig.…”

“…It has been suggested that fish ECaC and TRPV subfamilies diverged prior to a possible gene duplication giving rise to TRPV5 and TRPV6 (35). Although the site of Ca 2ϩ uptake in freshwater fish is believed to be the chloride cell (also termed mitochondria-rich cell, MRC) (18,23,24,27,28,32), ECaC appears to be ubiquitously expressed in all of the gill epithelial cell types, including pavement cells (PVCs) and chloride cells (35).…”