Myoendothelial coupling is unidirectional in guinea pig spiral modiolar arteries

Abstract

Gap junctions (GJs) facilitate communication and promote transfer of signaling molecules or current between adjacent cells in various organs to coordinate cellular activity. In arteries, homocellular GJs are present between adjacent smooth muscle cells (SMCs) and between adjacent endothelial cells (ECs), whilst many arteries also exhibit heterocellular GJs between SMCs and ECs. To test the hypothesis that there is differential cell coupling in guinea pig spiral modiolar arteries (SMA), we used intracellular recording technique to record cellular activities simultaneously in ECs or SMCs in acutely isolated guinea pig SMA preparations. Cell types were identified by injection of a fluorescent dye, propidium iodide (PI), through recording microelectrodes. Stable intracellular recordings were made in 120 cells among which 61 were identified as SMCs and 28 as ECs. Dual intracellular recordings were conducted to detect the coexistence of the two distinct levels of resting potential (RP) and to estimate the intensity of electrical coupling between two cells by a current pulse of up to 0.5-1.5 nA. The electrotonic potential was detected not only in the current-injected cell, but also in the majority of non-injected cells. The electrical coupling ratios (ECRs) of homocellular cells were not significant (P>0.05) (0.084±0.032 (n=6) and 0.069±0.031 (n=7) for EC-EC and SMC-SMC pairs, respectively). By contrast, the ECRs of heterocellular cells were significantly different when a current pulse (1.5 nA, 2s) was injected into EC and SMC respectively (0.072±0.025 for EC; 0.003±0.001 for SMC, n=5, P<0.01). The putative gap junction blocker 18β-glycyrrhetinic acid significantly attenuated electrical coupling in both homocellular and heterocellular forms. The results suggest that homocellular GJs within SMCs or ECs are well coordinated but myoendothelial couplings between ECs and SMCs are unidirectional.