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Am J Physiol Cell Physiol 278: C303-C314, 2000;
0363-6143/00 $5.00
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Vol. 278, Issue 2, C303-C314, February 2000

Role of K+ channel expression in polyamine-dependent intestinal epithelial cell migration

Jian-Ying Wang1,2, Jian Wang3, Vera A. Golovina4, Li Li1,2, Oleksandr Platoshyn3, and Jason Xiao-Jian Yuan3

Departments of 1 Surgery and 4 Physiology, University of Maryland School of Medicine and 2 Baltimore Veterans Affairs Medical Center, Baltimore, Maryland 21201; and 3 Department of Medicine, School of Medicine, University of California, San Diego, California 92103

Polyamines are essential for cell migration during early mucosal restitution after wounding in the gastrointestinal tract. Activity of voltage-gated K+ channels (Kv) controls membrane potential (Em) that regulates cytoplasmic free Ca2+ concentration ([Ca2+]cyt) by governing the driving force for Ca2+ influx. This study determined whether polyamines are required for the stimulation of cell migration by altering K+ channel gene expression, Em, and [Ca2+]cyt in intestinal epithelial cells (IEC-6). The specific inhibitor of polyamine synthesis, alpha -difluoromethylornithine (DFMO, 5 mM), depleted cellular polyamines (putrescine, spermidine, and spermine), selectively inhibited Kv1.1 channel (a delayed-rectifier Kv channel) expression, and resulted in membrane depolarization. Because IEC-6 cells did not express voltage-gated Ca2+ channels, the depolarized Em in DFMO-treated cells decreased [Ca2+]cyt as a result of reduced driving force for Ca2+ influx through capacitative Ca2+ entry. Migration was reduced by 80% in the polyamine-deficient cells. Exogenous spermidine not only reversed the effects of DFMO on Kv1.1 channel expression, Em, and [Ca2+]cyt but also restored cell migration to normal. Removal of extracellular Ca2+ or blockade of Kv channels (by 4-aminopyridine, 1-5 mM) significantly inhibited normal cell migration and prevented the restoration of cell migration by exogenous spermidine in polyamine-deficient cells. These results suggest that polyamine-dependent intestinal epithelial cell migration may be due partially to an increase of Kv1.1 channel expression. The subsequent membrane hyperpolarization raises [Ca2+]cyt by increasing the driving force (the electrochemical gradient) for Ca2+ influx and thus stimulates cell migration.

polyamines; voltage-gated potassium channels; intracellular calcium; membrane potential; intestinal epithelial cells


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