Internal Balance of K+
The kidney is primarily responsible for maintaining total body K+ content by matching K+ intake with K+ excretion. Adjustments in renal K+ excretion occur over several hours; therefore, changes in extracellular K+ concentration are initially buffered by movement of K+ into or out of skeletal muscle. The regulation of K+ distribution between the intracellular and extracellular space is referred to as internal K+ balance. The most important factors regulating this movement under normal conditions are insulin and catecholamines (1).
After a meal, the postprandial release of insulin functions to not only regulate the serum glucose concentration but also shift dietary K+ into cells until the kidney excretes the K+ load re-establishing K+ homeostasis. These effects are mediated through insulin binding to cell surface receptors, which stimulates glucose uptake in insulin-responsive tissues through the insertion of the glucose transporter protein GLUT4 (2,3). An increase in the activity of the Na+-K+-ATPase mediates K+ uptake (Figure 1). In patients with the metabolic syndrome or CKD, insulin-mediated glucose uptake is impaired, but cellular K+ uptake remains normal (4,5), demonstrating differential regulation of insulin-mediated glucose and K+ uptake.
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Catecholamines regulate internal K+ distribution, with α-adrenergic receptors impairing and β-adrenergic receptors promoting cellular entry of K+. β2-Receptor-induced stimulation of K+ uptake is mediated by activation of the Na+-K+-ATPase pump. These effects play a role in regulating the cellular release of K+ during exercise (6).
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Under normal circumstances, exercise is associated with movement of intracellular K+ into the interstitial space in skeletal muscle. Increases in interstitial K+ can be as high as 10-12 mM with severe exercise. Accumulation of K+ is a factor limiting the excitability and contractile force of muscle accounting for the development of fatigue (7,8). Additionally, increases in interstitial K+ play a role in eliciting rapid vasodilation, allowing for blood flow to increase in exercising muscle (9). During exercise, release of catecholamines through β2 stimulation limits the rise in extracellular K+ concentration that otherwise occurs as a result of normal K+ release by contracting muscle. Although the mechanism is likely to be multifactorial, total body K+ depletion may blunt the accumulation of K+ into the interstitial space, limiting blood flow to skeletal muscle and accounting for the association of hypokalemia with rhabdomyolysis.
Changes in plasma tonicity and acid-base disorders also influence internal K+ balance. Hyperglycemia leads to water movement from the intracellular to extracellular compartment. This water movement favors K+ efflux from the cell through the process of solvent drag. In addition, cell shrinkage causes intracellular K+ concentration to increase, creating a more favorable concentration gradient for K+ efflux. Mineral acidosis, but not organic acidosis, can be a cause of cell shift in K+. As recently reviewed, the general effect of acidemia to cause K+ loss from cells is not because of a direct K+-H+ exchange, but, rather, is because of an apparent coupling resulting from effects of acidosis on transporters that normally regulate cell pH in skeletal muscle (10) (Figure 2).
Intracellular K+ serves as a reservoir to limit the fall in extracellular K+ concentrations occurring under pathologic conditions where there is loss of K+ from the body. The efficiency of this effect was shown by military recruits undergoing training in the summer (11). These subjects were able to maintain a near-normal serum K+ concentration despite daily sweat K+ loses of >40 mmol and an 11-day cumulative total body K+ deficit of approximately 400 mmol.
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Studies in rats using a K+ clamp technique afforded insight into the role of skeletal muscle in regulating extracellular K+ concentration (12). With this technique, insulin is administered at a constant rate, and K+ is simultaneously infused at a rate designed to prevent any drop in plasma K+ concentration. The amount of K+ administered is presumed to be equal to the amount of K+ entering the intracellular space of skeletal muscle.
In rats deprived of K+ for 10 days, the plasma K+ concentration decreased from 4.2 to 2.9 mmol/L. Insulin-mediated K+ disappearance declined by more than 90% compared with control values. This decrease in K+ uptake was accompanied by a >50% reduction in both the activity and expression of muscle Na+-K+-ATPase, suggesting that decreased pump activity might account for the decrease in insulin effect. This decrease in muscle K+ uptake, under conditions of K+ depletion, may limit excessive falls in extracellular K+ concentration that occur under conditions of insulin stimulation. Concurrently, reductions in pump expression and activity facilitate the ability of skeletal muscle to buffer declines in extracellular K+ concentrations by donating some component of its intracellular stores.
There are differences between skeletal and cardiac muscle in the response to chronic K+ depletion. Although skeletal muscle readily relinquishes K+ to minimize the drop in plasma K+ concentration, cardiac tissue K+ content remains relatively well preserved. In contrast to the decline in activity and expression of skeletal muscle Na+-K+-ATPase, cardiac Na+-K+-ATPase pool size increases in K+-deficient animals. This difference explains the greater total K+ clearance capacity after the acute administration of intravenous KCl to rats fed a K+-free diet for 2 weeks compared with K+-replete controls (13,14). Cardiac muscle accumulates a considerable amount of K+ in the setting of an acute load. When expressed on a weight basis, the cardiac capacity for K+ uptake is comparable with that of skeletal muscle under conditions of K+ depletion and may actually exceed skeletal muscle under control conditions.
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