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Distal Colonic K⁺ Secretion Occurs via BK Channels

Matthias Sausbier^*, Joana E. Matos, Ulrike Sausbier^*, Golo Beranek^*, Claudia Arntz^*, Winfried Neuhuber, Peter Ruth^* and Jens Leipziger

^* Pharmakologie und Toxikologie, Pharmazeutisches Institut, Universität Tübingen, Tübingen, Germany; Institute of Physiology and Biophysics, The Water and Salt Research Center, University of Aarhus, Aarhus C, Denmark; and Anatomisches Institut, Universität Erlangen-Nürnberg, Erlangen, Germany

Address correspondence to: Dr. Jens Leipziger, Ole Worms Alle 160, 8000 Aarhus C, Denmark. Phone: +45-89-42-2826; Fax: +45-86-12-9065; E-mail: leip{at}fi.au.dk

Received for publication October 24, 2005. Accepted for publication February 6, 2006.

K⁺ secretion in the kidney and distal colon is a main determinant of K⁺ homeostasis. This study investigated the identity of the relevant luminal secretory K⁺ ion channel in distal colon. An Ussing chamber was used to measure ion transport in the recently generated BK channel–deficient (BK^–/–) mice. BK^–/– mice display a significant colonic epithelial phenotype with (1) lack of Ba²⁺-sensitive resting K⁺ secretion, (2) absence of K⁺ secretion stimulated by luminal P2Y₂ and P2Y₄ receptors, (3) absence of luminal Ca²⁺ ionophore (A23187)-stimulated K⁺ secretion, (4) reduced K⁺ and increased Na⁺ contents in feces, and (5) an increased colonic Na⁺ absorption. In contrast, resting and uridine triphosphate (UTP)-stimulated K⁺ secretion was not altered in mice that were deficient for the intermediate conductance Ca²⁺-activated K⁺ channel SK4. BK channels localize to the luminal membrane of crypt, and reverse transcription–PCR results confirm the expression of the BK channel -subunit in isolated distal colonic crypts. It is concluded that BK channels are the responsible K⁺ channels for resting and stimulated Ca²⁺-activated K⁺ secretion in mouse distal colon.

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