1.05 - Phototransduction in Microvillar Photoreceptors of Drosophila and Other Invertebrates

Abstract

Invertebrate microvillar photoreceptors depolarize in response to light by opening nonselective cation channels. Often the same cells can respond sensitively and rapidly to single photons, and yet light adapt to encode fluctuations of intensity under full sunlight. The underlying molecular mechanisms have been most extensively studied in the fruitfly Drosophila. Incident light is absorbed in the rhabdomere, a 1- to 2-μm diameter, 100-μm-long waveguide composed of ∼40 000 tightly packed microvilli, which contain the visual pigment rhodopsin and all the major components of the cascade. The extreme compartmentalization provided by this microvillar design is key to understanding the combination of sensitivity, rapid kinetics, and large dynamic range. Excitation is mediated by activation of G q protein and phospholipase C (PLC) resulting in activation of two classes of Ca 2+-permeable channel. These are encoded by the transient receptor potential ( trp) and trp-like ( trpl) genes, the founding members of the large and diverse TRP (light-activated nonspecific cation channel encoded by trp gene) superfamily of nonvoltage-gated cation channels. Several components of the cascade, including TRP, PLC, and protein kinase C (PKC) are assembled into a multimolecular signaling complex by the scaffolding protein INAD. Recent evidence suggests that the primary activator of the channels is likely to be a lipid messenger derived from the hydrolysis of phosphatidylinositol 4,5-bisphosphate (PIP 2) by PLC. Candidates include diacylglycerol (DAG), polyunsaturated acids (PUFAs), or the reduction in PIP 2. Ca 2+ influx via TRP channels is essential for rapid kinetics, amplification, and light adaptation, and mediates both positive and negative feedback via multiple downstream targets, including calmodulin (CaM), both TRP and TRPL (light-activated nonspecific cation channel encoded by trpl gene) channels, PKC, and PLC. Ca 2+ influx is also required for proper functioning of the visual pigment cycle, which involves CaMKII-dependent phosphorylation of arrestin and Ca 2+ CaM-dependent dephosphorylation of rhodopsin.