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.