Ion movements and oxygen consumption in kidney cortex slices

Abstract

It is generally recognized that the oxygen consumption of cells is related to the amount of free energy being utilized by such processes as secretion, contraction, and the synthesis of complex molecules. Two questions arise concerning the nature of the coupling between energy release from metabolism and its utilization. First, what fraction of the cell's total metabolism is devoted to a particular energy-requiring process; and secondly, how is an increase in oxygen consumption elicited in order to ensure a supply of the requisite energy? This paper deals with these problems in connexion with the active movements of ions in kidney cortex slices.In slices of kidney cortex from adult rabbits and guinea-pigs the establishment and maintenance of concentration gradients of sodium and potassium ions between intracellular and extracellular fluid depends on energy from respiration (Mudge, 1951 a, b;Whittam & Davies, 1953). The evidence for this is chiefly the fact that active transport is stopped when the energy supply is decreased by the inhibition of respiration. Such studies have not revealed the fraction of the total respiratory energy expended on these ion movements or whether the latter in turn influence the rate of respiration. Kidney cortex is a particularly suitable tissue for studying the interdependence of ion transport and metabolism, because both its rate of respiration and the turnover rate of its potassium are high, so that a reduction in oxygen uptake which might result from stopping transport could easily be measured. The coupling between respiration and potassium transport in slices of kidney cortex has been investigated in the present study by comparing the effects of ouabain, sodium ion, oc-oxoglutarate, and temperature on tissue potassium concentration and respiration during incubation at 25 and 380 C. A preliminary account of this work has been reported previously (Whittam & Willis, 1962).

Sodium Extrusion and Potassium Uptake in Guinea Pig Kidney Cortex Slices

“…The entry of choline (52,11) would make the membrane potential less negative and, secondarily, would lower the cell K concentration. However, this type of pump could not explain the findings of Whittam and Willis (38), where it was noticed that K influx stops in Na-depleted cells. Therefore, some coupling between Na extrusion and K uptake, however loose it may be, is required.…”

“…This work shows that Na extrusion requires and depends on the presence of K in the bathing fluid. Evidence that cell Na is necessary for K influx arises from experiments by Whittam and Willis (38). They found that the net influx of K stopped in Na-depleted cells and reappeared when Na was added to the immersion medium.…”

The metabolic response of brain slices to agents affecting the sodium pump

“…It is not easy to explain this result in terms of the simple hypothesis described above, inasmuch as a decrease in the rate of metabolism would be expected when the sodium pump is inhibited. As the effect is not found with liver and kidney (Whittam & Willis, 1963;Elshove & Van Rossum, 1963), it may be connected with the excitable nature of neuronal membranes. Further study is needed with a system more amenable to precise work than is possible with tissue slices.…”

“…There was no decrease in the rate of lactate production when oligomycin was present. Gascoyne & Yoshida, 1963), and the influence of active transport on metabolism (see Whittam & Willis, 1963) (Ashford & Dixon, 1934;Dickens & Greville, 1935;Dixon, 1949). The salient features are an increase in oxygen consumption and in the aerobic utilization of glucose to lactic acid.…”

EFFECT OF HYPO‐ AND HYPERTONIC SALINE AND RAFFINOSE ON CELL CONTENT OF Na, Cl and K IN RESPIRING RAT KIDNEY CORTEX AT 37°

“…This tendency to restore original cell volume is referred to as volume regulation and is incomplete in renal epithelial cells but nearly complete in red cells (Kregenow, 1971a;Schmidt and McManus, 1977). The mechanism for this partial return to original cell volume in kidney cells has been variously attributed to a cation pump, either sensitive to inhibition of the Na"*"-, K+-ATPase by cardiac glycosides (Whittam and Willis, 1963) or not (Kleinzeller and Knotkova, 1964;Hughes and MacKnight, 1976), in which case a second cardiac glycoside-insensitive pump has been postulated (Schmidt and McManus, 1977). It has also been attributed to physical elastic 'recoil' forces of the cell (Kleinzeller and Knotkova, 1964) or its basement membrane (Linshav/ et al, 1977).…”