Structure and cellular physiology of Ca2+ stores in invertebrate photoreceptors

Abstract

Invertebrate microvillar photoreceptors contain an extensive, morphologically continuous endoplasmic reticulum (ER) that comprises several distinct subregions. Most prominent is the smooth submicrovillar ER, a sponge-like cisternal network underneath the photoreceptive microvillar membrane. The submicrovillar ER spatially separates the microvilli and a narrow space of submicrovillar cytoplasm from the remaining cell body, and, thus, defines a transduction compartment. In bee and locust photoreceptors, the shape and position of these submicrovillar ER cisternae is maintained by interaction with actin filaments. The structural layout of the ER is either rather static, or, in some invertebrate species, the ER undergoes dramatic rearrangements during illumination. The submicrovillar ER has a high Ca content in dark-adapted cells (47.5 mmol/kg dry weight in bee photoreceptors), and acts as a source and sink for Ca2+ mobilized by illumination. About 50% of the Ca content is released by a 3 s, non-saturating light stimulus, and an almost equimolar amount of Mg is taken up to maintain electroneutrality within the ER. Ca2+ release is initiated by Ins(1,4,5)P3. In addition, the submicrovillar ER contains a heparin-insensitive, caffeine- and ryanodine-sensitive Ca2+ release pathway in bee photoreceptors. Both the Ins(1,4,5)P3-dependent and the ryanodine-sensitive Ca2+ release mechanism are modulated by cytosolic Ca2+, but at different Ca2+ concentrations. The presence of two release pathways with different Ca2+ sensitivities may be a prerequisite for highly localized, exceptionally fast and large Ca2+ elevations during the illumination of invertebrate photoreceptors.