Voltage sensitive, high-conductance chloride channels in the luminal membrane of cultured pulmonary alveolar (type II) cells

Abstract

The properties of ion channels in patches from the luminal membrane of cultured monolayers of type II alveolar epithelial cells from adult rat lung have been studied. In excised patches, prepared as described to yield the "outside-out" configuration (with cesium ions in the bathing solutions to suppress currents arising from potassium channels), we observed anion-selective channels with a conductance of 350-400 pS, and burst lengths lasting seconds. When patches were bathed in solutions with equal chloride concentrations, channels opened and closed spontaneously at membrane voltages close to zero, but tended to close when the potential was shifted by +/- 10 mV, particularly in the negative direction. Other anions could pass through these channels with a permeability sequence of I(1.5) greater than Br(1.02) = greater than Cl(1.00) greater than NO3(0.9) greater than gluconate(0.6) but there was a very low permeability for sodium (PNa/PCl = 0.015 +/- 0.006). Calcium ions reduced channel conductance. The channels probably have a role to play in salt absorption by this epithelium, but insufficient information is available about how sodium crosses it for the role of the anion channels in transport to be defined with confidence.

The maxi-anion channel: a classical channel playing novel roles through an unidentified molecular entity

“…These channels were similar to those observed in cultured cortical astrocytes from rats [4,49,50] and mice [5][6][7]51] as well as in a rat astrocytic RGCN cell line [52]. In epithelia, the urinary bladder [53], gastric [54], pancreatic [55][56][57], colonic [58][59][60], airway [61][62][63], choroid plexus [64], bile duct [65,66], ciliary [67][68][69], renal [9,19,[70][71][72][73][74][75][76][77][78], vestibular [79], placental [80][81][82][83][84][85][86], ruminal [87] and ovarian [84] epithelial cells were also found to express the maxianion channel with properties similar to those of excitable cells. Resembling maxi-anion channels were also found in fibroblasts [14,…”

“…Thus, the channel was deemed to provide a rout for solute transport and/or bicarbonate secretion in pancreatic duct cells [55], in alveolar epithelium [63], in syncytiotrophoblasts of placenta [83,129], in sheep ruminal epithelium [87] and in glomus cells of the rat carotid body [109]. The channel is thought to participate in the Cl -efflux during cell volume regulation in cortical collecting duct epithelium [9,75], pigmented ciliary epithelial cells [68], lymphocytes [102,104], myoblasts [23], placenta [80], neuronal cells [3] and astrocytes [4].…”

Single-channel recordings from cultured human retinal pigment epithelial cells.

“…Similar voltage dependence has been reported for large-conductance anionic or nonselective channels in many tissues (Blatz and Magleby, 1983;Schwarze and Kolb, 1984;Sather et al, 1985;Nelson et al, 1984;Gray et al, 1984;Hanrahan et al, 1985;Kolb et al, 1985;Schneider et al, 1985;Krouse et al, 1986), but the voltage at which the decline in Po begins to be most pronounced differs somewhat from preparation to preparation. Krouse et al (1986) report that the large anion channel in rat lung alveolar epithelium begins to inactivate as the potential is changed from 0 mV.…”

“…However, a detailed understanding of the properties of epithelial cell channels has become possible only with the advent of patch-clamp recording methods (Hamili et al, 1981). Recent patch-clamp studies have shown that some channels in epithelial cells closely resemble those previously described in excitable cells, e.g., calciumactivated potassium channels (Petersen and Maruyama, 1984) and large anion channels (Nelson et al, 1984;Hanrahan et al, 1985;Kolb et al, 1985;Schneider et al, 1985;Krouse et al, 1986). In addition, many channel types not previously seen in nerve and muscle have recently been observed (van Driessche and Zeiske, 1985), particularly in ocular epithelia (Rae and Levis, 1984b;Rae, 1985).…”

“…According to Gray et al (1984), Schwarze and Kolb (1984), and Kolb et al (1985), these channels are approximately one-fifth as permeable to sodium as to chloride, with potassium being less permeable than sodium. The anion channels described by Nelson et al (1984), Hanrahan et al (1985), and Schneider et al (1985) are also, though to a lesser extent, permeable to cations. These channels resemble, in many respects, the voltage-dependent anion channel (Schein et al, 1976) and bovine lens gap junction channel (Zampighi et al, 1985) observed in artificial membranes.…”