Transduction mechanisms of vertebrate and invertebrate photoreceptors.

Vertebrate and invertebrate visual photoreceptors detect light with exquisite sensitivity and rapid kinetics. They can detect single photons and by adapting to background light respond to changes in illumination over broad ranges of intensity. This review outlines the quite different biochemical mechanisms by which vertebrate and invertebrate photoreceptors respond to light (Fig. 1). Photoreceptor Structure and Function Both vertebrate and invertebrate photoreceptors contain highly specialized structures dedicated to phototransduction. Disk membranes of vertebrate rod outer segments and microvilli of invertebrate rhabdomeres provide large membrane substrata on which the molecular interactions of phototransduction occur. Vertebrates-A rod outer segment is a stack of flattened membrane vesicles, or disks, within a plasma membrane. Cone outer segments consist of highly invaginated plasma membrane. In darkness , a " dark current " leaves inner segments as K+ and enters outer segments as Na' and Ca2+ (1, 2). Light blocks Na' and Ca2+ entry into the outer segments. The resulting hyperpolarization slows glutamate release at synapses with bipolar cells (3). Znuertebrates-The rhabdomere, a crystalline array of microvilli, is the photosensitive structure of invertebrate photoreceptors (4). Rhabdomeres are underlaid by vesicular structures called sub-rhabdomeric cisternae. Illumination depolarizes invertebrate pho-toreceptors by stimulating Na' influx across the plasma membrane (5). The neurotransmitter released by Drosophila and Limulus pho-toreceptors appears to be histamine (6, 7). Excitation Mechanisms Primary Photoeuent: Absorption of Light by Rhodopsin Rhodopsins and related visual pigments are the primary light sensors of retinal photoreceptors. The protein components of visual pigments, opsins, belong to the seven-transmembrane a-helix receptor superfamily (8). The chromophore of most eukaryotic rho-dopsins is ll-cis-retinal linked to lysine as a protonated Schiff base, but chromophores can also be ll-cis-isomers of other retinoids (9). Light isomerizes ll-cis-retinal to all-trans, inducing conforma-tional changes in the protein that initiate rapid transitions between short lived spectral intermediates. Multichromatic visual systems are based on photoreceptors with visual pigments tuned to distinct spectral sensitivities (10, 11). Vertebrates-Light isomerizes ll-cis-retinal in rhodopsin in <200 fs (12), but subsequent production of active metarhodopsin I1 takes milliseconds (13). Metarhodopsin 11, a relatively stable intermediate with a deprotonated Schiff base, initiates the phototransduc-tion cascade. Models of rhodopsin structure place the glycosylated N terminus in the intradiscal space and the C terminus in the cytoplasm (13-16). A low resolution projection map of rhodopsin is consistent with a seven-a-helical structure (17). The absorption spectrum of rhodopsin depends on chromophorelamino acid side chain interactions in the retinal binding …