The role of retinal photoisomerase in the visual cycle of the honeybee.

Abstract

The compound eye of the honeybee has previously been shown to contain a soluble retinal photoisomerase which, in vitro, is able to catalyze stereospecifically the photoconversion of all-trans retinal to 11-cis retinal. In this study we combine in vivo and in vitro techniques to demonstrate how the retinal photoisomerase is involved in the visual cycle, creating 11-cis retinal for the generation of visual pigment. Honeybees have approximately 2.5 pmol/eye of retinal associated with visual pigments, but larger amounts (4-12 pmol/eye) of both retinal and retinol bound to soluble proteins. When bees are dark adapted for 24 h or longer, greater than 80% of the endogenous retinal, mostly in the all-trans configuration, is associated with the retinal photoisomerase. On exposure to blue light the retinal is isomerized to 11-cis, which makes it available to an alcohol dehydrogenase. Most of it is then reduced to 11-cis retinol. The retinol is not esterified and remains associated with a soluble protein, serving as a reservoir of 11-cis retinoid available for renewal of visual pigment. Alternatively, 11-cis retinal can be transferred directly to opsin to regenerate rhodopsin, as shown by synthesis of rhodopsin in bleached frog rod outer segments. This retinaldehyde cycle from the honeybee is the third to be described. It appears very similar to the system in another group of arthropods, flies, and differs from the isomerization processes in vertebrates and cephalopod mollusks.

Visual pigment, dark adaptation and rhodopsin renewal in the eye of Pontoporeia affinis (Crustacea, Amphipoda)

“…6), suggesting that during this period no change in the amount of rhodopsin in the rhabdoms occurs. In arthropod eyes it is well established that rhodopsin regeneration is closely linked to membrane turnover and occurs in the retinular cell before incorporation in the microvillar membrane (Schwemer 1983(Schwemer , 1984(Schwemer , 1986(Schwemer , 1989Stowe et al 1990;Smith and Goldsmith 1991). 7, that measure the rhodopsin/metarhodopsin ratio, show that this ratio undergoes only slight changes during the first 24 h after the exposure.…”

Regeneration of 11-cis-Retinal in Visual Systems with Monostable and Bistable Visual Pigments

“…(Constructed, in part, using the pathway proposed by Wang et al 2012) (Schwemer et al 1984), and characterized in squid (see foregoing discussion). Their role in the regeneration cycle of bistable visual pigments has been clarified by studies of the visual system of the honey bee (Apis mellifera) (Smith and Goldsmith 1991;Cugnoli et al 1989). A remarkable property of the honeybee retina is that 80 % of its retinal was extracted into an aqueous buffer where it was demonstrated to be bound to a photoisomerase (RalPI440) (Smith and Goldsmith 1991).…”

“…Their role in the regeneration cycle of bistable visual pigments has been clarified by studies of the visual system of the honey bee (Apis mellifera) (Smith and Goldsmith 1991;Cugnoli et al 1989). A remarkable property of the honeybee retina is that 80 % of its retinal was extracted into an aqueous buffer where it was demonstrated to be bound to a photoisomerase (RalPI440) (Smith and Goldsmith 1991). Following illumination, the 11-cis-retinal formed could be either reduced to 11-cis-retinol by an uncharacterized dehydrogenase or delivered to opsin to regenerate rhodopsin.…”

“…Honeybee photoisomerase has been proposed to supply 11-cisretinal for rhodopsin biosynthesis in a slow renewal process involving membrane turnover (Pepe and Cugnoli 1992). However, given the large amount of photoisomerase (and perhaps other retinoid-binding proteins) (soluble retinal + retinol~4-12 pmol/eye; visual pigment-associated retinal~2.5 pmol/ eye), it is conceivable that photoisomerase could serve as a reservoir of 11-cisretinoid, which could fill up during daylight hours and deliver 11-cis-retinal to photolysed opsin in the dark (Smith and Goldsmith 1991), a role proposed for retinochrome in squid retina (see earlier). Drosophila has been reported to have "photoisomerase" activity (Pepe and Cugnoli 1992), but there is insufficient information available to determine whether it could function in a manner similar to that of the honey bee.…”

Retinoids in the lateral eye of Limulus: Evidence for a retinal photoisomerase

“…For insertion into the membrane as visual pigment, a supply of 1 \-cis retinal is also required. In contrast, the photoisomerase of honeybees is soluble in aqueous buffers (Pepe & Cugnoli, 1980;Schwemer et al, 1984;Smith & Goldsmith, 1991a). In squid and other cephalopods, this photoisomerase is an intrinsic membrane protein, retinochrome (Hara & Hara, 1972).…”