Biophysical processes in invertebrate photoreceptors: recent progress and a critical overview based on Limulus photoreceptors

Abstract

Limulus ventral nerve photoreceptor, a classical preparation for the study the phototransduction in invertebrate eyes, seems to have a very complex mechanism to transform light energy into a physiological signal. Although the main function of the photoreceptor is to change the membrane conductance according to the illumination, the cell has voltage-activated conductances as well. The voltage-gated conductances are matched to the light-activated ones in the sense that they make the function of the cell more efficient. The complex mechanism of phototransduction and the presence of four different voltage-gated conductance in Limulus ventral nerve photoreceptors indicate that these cells are far less differentiated than the photoreceptor cells of vertebrates. Indications accumulated in recent years support the view that the ventral photoreceptor of Limulus has different light-activated macroscopic current components, ion channels and terminal transmitters. After conclusions from macroscopic current measurements (Payne, 1986; Payne et al. 1986 a, b), direct evidence was presented by single-channel (Nagy & Stieve, 1990 a, b; Nagy, 1990 a, b) and macroscopic current measurements (Deckert et al. 1991 a, b) for three different light-activated conductances. It has been shown that two of these conductances are stimulated by two different excitation mechanisms. The two mechanisms, having different kinetics, release probably two different transmitters. One of them might be the cGMP (Johnson et al. 1986), the other one the calcium ion (Payne et al. 1986 a, b). However, the biochemical processes which link the rhodopsin molecules and the ion channels are not known. The unknown chemical details of the phototransduction result in a delay for the mathematical description of the biophysical mechanisms. More biochemical details are known about the adaptation mechanism. It was found that inositol 1,4,5-trisphosphate is a messenger for the release of calcium ions from the intracellular stores and that calcium ions are the messengers for adaptation (Payne et al. 1986 b; Payne & Fein, 1987). Concerning the mechanism of calcium release, it was revealed that a negative feedback acts on the enzyme cascade to regulate the internal calcium level and to protect the stores against complete emptying (Payne et al. 1988, 1990). Calcium ions also play an important role in the excitation mechanism. (a) In [Ca2+]i-depleted cells the light-induced current was increased after intracellular Ca2+ injection, suggesting that calcium is necessary for the transduction mechanism (Bolsover & Brown, 1985).(ABSTRACT TRUNCATED AT 400 WORDS)

Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors.

“…Recent advances in our understanding of invertebrate phototransduction (Fein, Payne, Corson, Berridge and Irvine, 1984;Brown et al, 1984;Fein and Payne, 1989;Hardie, 1991;Hardie and Minke, 1992;Nagy, 1991;Minke and Selinger, 1988) point to an Ins(1-4-5)P3-mediated molecular mechanism being responsible for excitation in photoreceptors. According to this scheme, the excited rhodopsin molecules in microvillar membranes trigger Ca2+-release from internal stores close to the base of the microvilli.…”

Capacitative calcium entry

“…20 ms. Unitary Ca2+ signalling events with kinetics very similar to these bumps in Drosophila photoreceptors have been recorded in other cells (Figure 4c). Examples include the quantum emission domains (QED) in presynaptic terminals [121,122], the spontaneous miniature outward current (SMOC) in sympathetic neurons [123], the sparks in cardiac cells [124], bumps in Limulus photoreceptors [125] and the puffs in Xenopus oocytes [126]. All these events depend upon the brief opening of either a single or a small localized group of Ca2+ channels located either in the plasma membrane or on the stores (Figure 4b) to produce a localized cloud of calcium that builds up quickly and then decays away exponentially by passive diffusion as soon as the channel closes (Figure 4c).…”

“…Note that the bumps observed in invertebrate photoreceptors have different origins. In Limulus they represent Ca2+ release from internal stores [125], whereas in Drosophila they seem to result from the conformational-coupling complexes responsible for calcium entry.…”

Evidence for the Involvement of Inositol Trisphosphate but Not Cyclic Nucleotides in Visual Transduction in HermissendaEye

“…Assay of PIP 2 Breakdown and PLC Activity-Isolated Hermissenda eyes were incubated in 10 l of ASW containing 10 Ci of [ standard was added as a carrier and to aid in the identification of the lipids. Phospholipids were extracted and separated by thin layer chromatography as described previously (9).…”

“…There is abundant evidence that the phosphoinositide cascade is involved in invertebrate phototransduction; however, the specific roles of inositol trisphosphate (IP 3 ) 1 and/or Ca 2ϩ in visual excitation have not yet been established (1)(2)(3). The involvement of phosphatidylinositol 4,5-bisphosphate (PIP 2 ) hydrolysis by phospholipase C (PLC) in the generation of IP 3 in photoreceptors of Limulus (4,5), squid (6 -8), Drosophila (9 -12), and Hermissenda (13) is supported by several lines of biochemical and biophysical evidence.…”