Properties of spontaneously active cells distributed in the submucosal layer of mouse proximal colon

Abstract

Intracellular electrical activity was recorded from smooth muscle tissues of the mouse proximal colon, and the impaled cells were visualized by injection of neurobiotin. Slow potentials with initial fast and subsequent plateau components (plateau potentials), generated at a frequency of 14.8 min⁻¹, were recorded from oval-shaped cells with bipolar processes. Periodic bursts of spike potentials (4.6 min⁻¹) and bursts of oscillatory potentials (4.3 min⁻¹) were recorded in circular and longitudinal smooth muscle cells, respectively. Nifedipine (0.1 μm) abolished the bursts of spike and oscillatory potentials and reduced the duration of plateau potentials. The plateau potentials were abolished by 1 μm nifedipine. The plateau potentials were also abolished by cyclopiazonic acid (an inhibitor of Ca²⁺ uptake into internal stores) or 2-aminoethoxydiphenyl borate (an inhibitor of inositol 1,4,5-trisphosphate receptor-mediated Ca²⁺ release), and were inhibited by bis-(aminophenoxy) ethane-N,N,N′,N′-tetraacetic acid acetoxymethyl ester (a chelator of intracellular Ca²⁺). Carbonyl cyanide m-chlorophenylhydrazone (a mitochondrial protonophore) abolished plateau potentials, and its action was not mimicked by oligomycin (an inhibitor of mitochondrial ATPase). It is concluded that in mouse proximal colon, submucosal c-kit-positive bipolar cells spontaneously generate plateau potentials with rhythms different from those generated by smooth muscle cells. The plateau potentials are generated through activation of voltage-gated Ca²⁺ channels, which are coupled to the release of Ca²⁺ from the internal stores and the handling of Ca²⁺ in mitochondria.