Segmental differences in upregulated apical potassium channels in mammalian colon during potassium adaptation

Abstract

Rat proximal and distal colon are net K+secretory and net K+absorptive epithelia, respectively. Chronic dietary K+loading increases net K+secretion in the proximal colon and transforms net K+absorption to net K+secretion in the distal colon, but changes in apical K+channel expression are unclear. We evaluated expression/activity of apical K+(BK) channels in surface colonocytes in proximal and distal colon of control and K+-loaded animals using patch-clamp recording, immunohistochemistry, and Western blot analyses. In controls, BK channels were more abundant in surface colonocytes from K+secretory proximal colon (39% of patches) than in those from K+-absorptive distal colon (12% of patches). Immunostaining demonstrated more pronounced BK channel α-subunit protein expression in surface cells and cells in the upper 25% of crypts in proximal colon, compared with distal colon. Dietary K+loading had no clear-cut effects on the abundance, immunolocalization, or expression of BK channels in proximal colon. By contrast, in distal colon, K+loading 1) increased BK channel abundance in patches from 12 to 41%; 2) increased density of immunostaining in surface cells, which extended along the upper 50% of crypts; and 3) increased expression of BK channel α-subunit protein when assessed by Western blotting ( P < 0.001). Thus apical BK channels are normally more abundant in K+secretory proximal colon than in K+absorptive distal colon, and apical BK channel expression in distal (but not proximal) colon is greatly stimulated as part of the enhanced K+secretory response to dietary K+loading.