Active sodium transport and the electrophysiology of rabbit colon

Abstract

The electrophysiologic properties of rabbit colonic epithelial cells were investigated employing microelectrode techniques. Under open-circuit conditions, the transepithelial electrical potential difference (PD) averaged 20 mV, serosa positive, and the intracellular electrical potential (psimc) averaged -32 mV, cell interior negative with respect to the mucosal solution; under short-circuit conditions, psimc averaged -46 mV. The addition of amiloride to the mucosal solution abolishes the transepithelial PD and active Na transport, and psimc is hyperpolarized to an average value of -53 mV. These results indicate that Na entry into the mucosal cell is a conductive process which, normally, depolarized psimc. The data obtained were interpreted using a double-membrane equivalent electrical circuit model of the "active Na transport pathway" involving two voltage-independent electromotive forces (emf's) and two voltage-independent resistances arrayed in series. Our observations are consistent with the notions that: (a) The emf's and resistances across the mucosal and baso-lateral membranes are determined predominantly by the emf (64 mV) and resistance of the Na entry process and the emf (53 mV) and resistance of the process responsible for active Na extrusion across the baso-lateral membranes: that is, the electrophysiological properties of the cell appear to be determined solely by the properties and processes responsible for transcellular active Na transport. The emf of the Na entry process is consistent with the notion that the Na activity in the intracellular transport pool is approximately one-tenth that in the mucosal solution or about 14 mM. (b) In the presence of amiloride, the transcellular conductance is essentially abolished and the total tissue conductance is the result of ionic diffusion through paracellular pathways. (c) The negative intracellular potential (with respect to the mucosal solution) is due primarily to the presence of a low resistance paracellular "shunt" pathway which permits electrical coupling between the emf at the baso-lateral membrane and the potential difference across the mucosal membrane; in the absence of this shunt, the "well-type" electrical potential profile characteristic of rabbit colonic cells would be 'converted' into a "staircase-type" profile similar to those reported for frog skin and toad urinary bladder by some investigators.

Electrophysiology of pig distal colon measured during early post‐natal development.

“…The situation in the basolateral membrane of the 4-day-old pig colon closely resembles that found in adult rabbits (R. of 92 0 cm' in the pig compared with 95-100 C1 cm2 in the rabbit; E. of 66 mV in the pig compared with 53-55 mV in the rabbit: values of R. and E. for rabbit colons taken from the papers of Schultz et al (1977) and Wills et al (1979)). It is concluded from this that the major changes in cellular function seen to take place in the distal colon during early neonatal development arise from alterations in the properties of brush border membranes only.…”

“…These changes, which were statistically significant (P < 0.05 and < 0.01 respectively), are predicted from the known action of amiloride in blocking Na+ entry across the brush border membrane. The most important fact to emerge from these experiments, however, was the finding that Em was cell-interior negative and not positive as reported by Schultz et al (1977) for the adult rabbit colon. It is concluded from this that some other ion besides Na+ is contributing to the brush border membrane electromotive force in the distal colons of neonatal pigs.…”

“…It is concluded from this that the major changes in cellular function seen to take place in the distal colon during early neonatal development arise from alterations in the properties of brush border membranes only. The shunt resistance of the 4-day-old pig colon was much lower than that found in the descending colon of the adult rabbit (RSh of 127 n cm2 for the pig compared with 345-730 0 cm2 for the rabbit: values for rabbit taken from the papers of Schultz et al (1977) and Wills et al (1979)). The percentage conductance of the paracellular pathway was, however, similar for the two different tissues; this is because the brush border membrane resistance of the pig distal colon is significantly lower than that ofthe rabbit.…”

Volume-regulatory responses of Amphiuma red cells in anisotonic media. The effect of amiloride.

“…Despite the many similarities between amiloride-sensitive Na transport in Amphiuma red cells and conductive Na transport in "tight" epithelia, such as toad urinary bladder (Sudou and Hoshi, 1977), frog skin (Fuchs et al, 1977 ;Helman and Fisher, 1977), and rabbit colon (Schultz et al, 1977), we have noted that the Amphiuma red cell transporter acts as a Na/H antiport (or a Na/OH or Na/ HCO3 symport) (Cala, 1980 ;Siebens and Kregenow, 1980 ;Kregenow et al, 1985). This mechanism appears to be similar to that in various cells including many "leaky" epithelia, such as gallbladder (Weinman and Reuss, 1982) and proximal renal tubule (Kinsella and Aronson, 1981 ;Boron and Boulpaep, 1983).…”

Conversion of sodium channels to a form sensitive to cyclic AMP by component(s) from red cells

“…In the rabbit the situation is somewhat different in that amiloride-sensitive sodium transport is present normally (Schultz, Frizzell & Nellans, 1977) but nevertheless, can be increased by mineralocorticoids . The avian coprodaeum behaves rather as the rat in that amiloride-sensitive sodium transport appears only after salt deprivation (Choshniak, Munck & Skadhauge, 1977;Bindslev, Cuthbert, Edwardson & Skadhauge, 1982).…”