The surface epithelium of teleostean fish gills. Cellular and junctional adaptations of the chloride cell in relation to salt adaptation.

Abstract

Various species of teleostean fishes were adapted to fresh or salt water and their gill surface epithelium was examined using several techniques of electron microscopy.In both fresh and salt water the branchial epithelium is mostly covered by flat respiratory cells. They are characterized by unusual outer membrane fracture faces containing intramembranous particles and pits in various stages of ordered aggregation. Freeze fracture studies showed that the tight junctions between respiratory cells are made of several interconnecting strands, probably representing high resistance junctions. The organization of intramembranous elements and the morphological characteristics of the junctions do not vary in relation to the external salinity. Towards the base of the secondary gill lamellae, the layer of respiratory cells is interrupted by mitochondria-rich cells ("chloride cells"), also linked to respiratory cells by multistranded junctions.There is a fundamental reorganization of the chloride cells associated with salt water adaptation. In salt water young adjacent chloride cells send interdigitations into preexisting chloride cells. The apex of the seawater chloride cell is therefore part of a mosaic of sister cells linked to surrounding respiratory cells by multistranded junctions. The chloride cells are linked to each other by shallow junctions made of only one strand and permeable to lanthanum. It is therefore suggested that salt water adaptation triggers a cellular reorganization of the epithelium in such a way that leaky junctions (a low resistance pathway) appear at the apex of the chloride cells.Chloride cells are characterized by an extensive tubular reticulum which is an extension of the basolateral plasma membrane. It is made of repeating units and is the site of numerous ion pumps. The presence of shallow junctions in sea wateradapted fish makes it possible for the reticulum to contact the external milieu. In contrast in the freshwater-adapted fish the chloride cell's tubular reticulum is separated by deep apical junctions from the external environment.Based on these observations we discuss how solutes could transfer across the epithelium.t Deceased 16 August I977. 96J. CELL BIOLOGY 9 The Rockefeller University Press 9

Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus

“…Permeability of the paracellular pathway in transporting epithelia is an important aspect of controlling ion homeostasis. The freshwater gill of F. heteroclitus actively accumulates Na + , but not Cl − , and relies on the regulation of epithelial tight junction proteins, such as claudins and occludins, to regulate the efflux of ions across the gill (Ernst et al, 1980;Patrick et al, 1997;Sardet et al, 1979). Claudins and occludins are involved in tight junction formation and play a role in paracellular ion transport (Furuse et al, 1993;Van Itallie and Anderson, 2006).…”

Non‐electrolyte permeability of trout gills: effect of temperature and adrenaline

“…Gill permeability to non-electrolytes during adaptation to sea water Salt adaptation is accompanied by ultrastructural changes affecting chiefly the chloride cells and their junctions (Sardet et al 1978). The essential feature of this process is the opening of trans-and paracellular channels, the junctions between chloride cells consisting of a single strand in sea water (leaky junctions) as compared with six strands in fresh water (tight junctions).…”

“…The essential feature of this process is the opening of trans-and paracellular channels, the junctions between chloride cells consisting of a single strand in sea water (leaky junctions) as compared with six strands in fresh water (tight junctions). While the functional unit in sea water is two 'mother-daughter' chloride cells, these are isolated and surrounded by epithelial cells in fresh water (Sardet et al 1978).…”

“…Small liposoluble and water-soluble molecules (butanol, water and urea) are assumed to take a cellular pathway involving most of the gill epithelium and sensitive to the action of adrenaline, which acts in addition by selectively * (Shirai & Utida, 1970; Thomson & Sargent, 1977), salt adaptation involves the development of young chloride cells which send arms into those already existing (Sardet, Pisam & Maetz, 1978 (Haywood, Isaia & Matetz, 1977;Girard & Payan, 1976).…”

Mantle and gill fine structure in the freshwater Asiatic clam,Corbicula fluminea(Müller)

“…The mucocyte structure is completely different from the secretory cell structure. Moreover, the secretory cells display the same structure as the chloride cells described in fish gills (Sardet et al, 1979, WendelaarBonga et al 1990). Therefore they could be cells involved in active exchanges between water and haemolymph, particularly ionic exchanges.…”