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

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.