Potassium currents in rat colonic smooth muscle cells and changes during development and aging

Abstract

In a previous study on freshly isolated single smooth muscle cells from the circular layer of the rat distal colon, we reported that the L-type Ca²⁺ current density increased during development and gradually declined with further aging [ZI Xiong, N Sperelakis, N Noffsinger, C Fenoglio-Preiser (1993) Am J Physiol 265: C617–C625]. Since K⁺ current plays a key role in controlling excitability of the cells and hence the motility of the colon, in the present study the voltage-gated K⁺ channel currents, (I _K) were investigated using the whole-cell voltage-clamp technique in colonic myocytes from rats of different ages. A Ca²⁺-sensitive K⁺ current [I _K(Ca)] and two kinds of Ca²⁺-insensitive outward K⁺ currents were identified and characterized. I _K(Ca) was recorded at potentials more positive than −40 mV in Ca²⁺-containing bath solution, and was blocked by Ca²⁺ channel antagonists and tetraethylammonium ion (TEA⁺). After removing Ca²⁺ from the bath solution and using a high ethylenebis(oxonitrilo)tetraacetate (EGTA, 4 mM) concentration in the pipette, two types of Ca²⁺-insensitive I _K were recorded. The first and faster component was usually activated at potentials more positive than −50 mV, and was more sensitive to 4-aminopyridine (4-AP). In contrast, the second and slower (delayed) component was activated at potentials more positive than −30 mV, and was more sensitive to TEA. The total density of the Ca²⁺-insensitive I _K component decreased dramatically during the neonatal period: from 32.2±3.2 pA/pF in 3-day-old rats to 17.8±2.6 pA/pF in 40-day-old rats; there was no further decline during aging (up to 480 days). This total I _K decline was due primarily to a decline in the 4-AP-sensitive component; the TEA-sensitive component remained unchanged at all ages. The possible physiological implications of the decline in density of the 4-AP-sensitive I _K component during neonatal development are discussed.