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In the heart, the rapid propagation and synchronization of action potentials necessary for a normal heart rhythm and an effective cardiac output are mediated by specialized ionic channels that link adjacent cells and are known collectively as gap junctions. Cardiac gap junctions are gated by various physiological and pharmacological agents, but the role of voltage in their gating is unclear. Whereas embryonic or neonatal ventricular cells have voltage-gated gap junctions, adult cells are reported to have only voltage-independent gap junctions. We studied the voltage dependence of adult rat atrial gap junctions by individually voltage clamping each cell of a connected cell pair and controlling the transjunctional voltage (Vj), measuring transjunctional current (Ij), and calculating junctional conductance (gj). Two distinct populations of cell pairs were observed: highly coupled pairs with the peak gjs ranging from 3.4 to 40 nS and weakly coupled pairs with the peak gjs ranging from 0.3 to 2.0 nS. gj was dependent on Vj, and Ij decayed exponentially, with the time constants being voltage dependent. Voltage dependence was most apparent when cells were poorly coupled. The gj did not decrease to zero. The normalized conductance--Vj plot was fit with a two-state Boltzmann model as a first approximation, resulting in a half-inactivation potential and gating charge of 42.5 mV and 1.14 eV, respectively, for the weakly coupled cell pairs. For highly coupled cell pairs, the half-inactivation potential shifted to 53.3 mV. Single gap junctional channels had a gj of 36.2 +/- 7.6 pS (range, 27-49 pS), which was Vj independent.(ABSTRACT TRUNCATED AT 250 WORDS)

Voltage-dependent gating and single-channel conductance of adult mammalian atrial gap junctions.