Limulus ventral photoreceptors contain two functionally dissimilar inositol triphosphate-induced calcium release...

Injections of inositol 1,4,5 triphosphate (InsP3) into Limulus ventral photoreceptors give rise to a rapid depolarization and an elevation of intracellular calcium concentration (Cai). This response to InsP3 is followed by a period of desensitization that persists as long as Cai remains elevated (feedback inhibition). Limulus ventral photoreceptors have two types of lobe: a light-sensitive rhabdomeric lobe (R lobe), and a light-insensitive arhabdomeric lobe (A lobe). Evidence showing the presence of feedback inhibition has been so far demonstrated only in the R lobe. In this study, simultaneous measurements of Cai were made using aequorin and double-barreled calcium-sensitive electrodes in each type of lobe. We carefully checked the location of the R lobe and A lobe by scanning a microspot of light across the whole photoreceptor. We then inserted a double-barreled calcium-sensitive microelectrode with InsP3 in either type of lobe. In the R lobe, injections of InsP3 led to a large Cai increase, a rapid depolarization and feedback inhibition; a brief flash of light induced a rapid depolarization and a Cai increase measured by both aequorin and the calcium-sensitive electrode. In the A lobe, injection of InsP3 led to an increase in Cai measured by the calcium-sensitive electrode but to no depolarization or aequorin luminescence. Further there was no evidence of feedback inhibition in the A lobe; the elevation of Cai caused by the first injection did not desensitize the photoreceptor to a second injection of InsP3 3 s later. To verify that the aequorin and the cell membrane respond to an increase in Cai, we presented a brief flash of light. Following a uniform illumination, there is indeed a typical large luminescence increase and a receptor potential. The calcium-sensitive electrode measures a small and slow Cai increase because its tip is located in the A lobe and it is measuring Ca2+ diffusing from the R lobe. Our observation that the InsP3-induced Cai increase in the A lobe is not apparently accompanied by a subsequent desensitization to InsP3 may suggest that there are more than one type of InsP3 receptor in the same cell. Alternatively, the InsP3 receptor could be the same but some additional factor, which confers feedback inhibition, could be missing in the A lobe.