The effects of valinomycin on ion movements across the sarcoplasmic reticulum in frog muscle.

The effects of valinomycin on the elemental composition and the fractional volume of the terminal cisternae (t.c.) of the sarcoplasmic reticulum (s.r.) were determined in rapidly frozen frog semitendinosus muscles. The concentrations of valinomycin used for the electron probe studies (5 microM) had no effect on tetanus tension or t.c. volume (2.% of fibre volume). Mitochondria were markedly swollen and their K content was significantly increased in both the resting and the tetanized valinomycin-treated muscles. Valinomycin had no effect on the concentration of Na, Mg, P, Cl, K and Ca in the t.c. of resting muscles. In untreated, tetanized muscles, Ca2+ release was accompanied by the uptake of K and Mg into the t.c. in an amount that was significantly less than the positive charge removed through Ca2+ release, confirming previous observations showing an apparent charge deficit (Somlyo, Gonzalez-Serratos, Shuman, McClellan & Somlyo, 1981). Valinomycin abolished the apparent charge deficit: in tetanized, valinomycin-treated muscles, the uptake of K into the t.c. was significantly (P less than 0.001) greater than in the untreated muscles and Mg uptake also remained highly significant. It is suggested that Ca2+ release from activated muscle is an electrogenic process and that the K+ conductance of the s.r. in untreated frog muscles is insufficient to allow charge neutralization of the Ca2+ current during release. The increase in K+ permeability caused by valinomycin permits the greater counter movement of K+ under the combined influence of the electrical potential generated by outward Ca2+ movement and the acidic cation binding proteins in the lumen of the s.r. The results are consistent with the proposal (Somlyo et al. 1981) that in normal frog muscles not treated with valinomycin, the apparent positive charge deficit observed after a tetanus reflects the movement of protons and, possibly, organic cations.