Mitochondrial potassium transport: the K(+) cycle.

Potassium transport plays three distinct roles in mitochondria. Volume homeostasis to prevent excess matrix swelling is a housekeeping function that is essential for maintaining the structural integrity of the organelle. This function is mediated by the K(+)/H(+) antiporter and was first proposed by Peter Mitchell. Volume homeostasis to prevent excess matrix contraction is a recently discovered function that maintains a fully expanded matrix when diffusive K(+) influx declines due to membrane depolarization caused by high rates of electron transport. Maintaining matrix volume under these conditions is important because matrix contraction inhibits electron transport and also perturbs the structure-function of the intermembrane space (IMS). This volume regulation is mediated by the mitochondrial ATP-sensitive K(+) channel (mitoK(ATP)). Cell signaling functions to protect the cell from ischemia-reperfusion injury and also to trigger transcription of genes required for cell growth. This function depends on the ability of mitoK(ATP) opening to trigger increased mitochondrial production of reactive oxygen species (ROS). This review discusses the properties of the mitochondrial K(+) cycle that help to understand the basis of these diverse effects.