11-cis retinal restores visual function in vitamin A-deficient Manduca

Abstract

Larvae of the tobacco hornworm moth Manduca sexta were reared on either a carotenoid-supplemented or a carotenoid-deficient diet. The former yields fortified adults with normal visual function, whereas visual sensitivity and rhodopsin content are reduced by 2−4 log units in the compound eyes of the deprived moths reared on the latter. We characterized the retinoids of fortified retinas and investigated the recovery of visual function in deprived moths that were provided with retinaldehyde as a source of photopigment chromophore. Retinoids were identified and measured by high-performance liquid chromatography (HPLC). Fortified retinas contained mainly 3-hydroxyretinaldehyde (R3); 11-cis R3 predominated in dark-adaptation, all-trans in light-adaptation, indicating that R3 is the photopigment chromophore. No retinoids could be measured in deprived eyes. Retinaldehyde (R1) was delivered to the retinas of deprived moths by “painting” solutions of 11-cis or all-trans R1 in dimethylsulfoxide (DMSO) on the corneal surfaces of the compound eyes or on the head capsule between the eyes. 11-cis R1 induced rapid recovery: during 3 days, sensitivity rose to within a log unit of that measured from fortified animals. By 7 days, sensitivity was close to normal. Although rhodopsin and P-face particle densities of photoreceptor membranes increased, neither rose to the levels found in fortified animals. All-trans R1 induced only a slight increase in sensitivity that could have resulted from some nonspecific isomerization of the all-trans to the 11-cis isomer; we found no evidence for a retinal isomerase that functions in darkness. Small amounts of R3 were measured in recovering retinas, indicating some conversion of R1 to R3. However, the chromophore of most of the rhodopsin that was synthesized must have been R1. It is possible that rhodopsin did not reach normal levels in the retina even after a week of recovery because the normal chromophore R3 was not provided. Although the rhodopsin that initially formed in recovering moths may have resulted from the association of the chromophore with pre-existing opsin, the extent of eventual recovery indicates that opsin synthesis was stimulated by 11-cis R1.

Carotenoid replacement inDrosophila: freeze-fracture electron microscopy

“…In Drosophila, opsin is reduced to 1% of normal levels (Ozaki et al, 1993). Visual pigment is restored in mature insect photoreceptors when they are provided with chromophore Bennett & White, 1991;Sapp et al, 1991a;Chen & Stark, 1992). Although the conditions of chromophore depletion and recovery are certainly non-physiological, they provide opportunities for experiments on the possible roles played by the chromophore in regulating synthesis, turnover, maturation and deployment of visual pigment.…”

“…Although the conditions of chromophore depletion and recovery are certainly non-physiological, they provide opportunities for experiments on the possible roles played by the chromophore in regulating synthesis, turnover, maturation and deployment of visual pigment. To focus this discussion and avoid the possible complication of species differences, we will consider mainly experiments with Drosophila, but data from the blowfly Calliphora (Paulsen & Schwemer, 1983;Schwemer & Spengler, 1992;Shukolyukov & Denisova, 1992;Huber et at., 1994) and the moth Manduca Bennett & White, 1991) are also relevant.…”

“…Other studies suggest that insects recover visual function as levels of opsin and rhodopsin rise (e.g. Paulsen & Schwemer, 1983;Bennett & White, 1991;Sapp et al, 1991a). Results from experiments with Drosophila (Sun et al, 1993) and Calliphora (Schwemer & Spengler, 1992) have led to the tantalizing suggestion that retinoids may control opsin gene transcription in insects.…”

Electrophysiological sensitivity of carotenoid deficient and replaced Drosophila

“…Some more obviously relevant precursors, especially 1 \-cis retinal, have had limited utility to date because of limited availability. Likewise, ll-cis retinal was applied directly to the head of the moth (Manduca) and led to a small visual recovery (Bennett & White, 1991). Also, many forms of vitamin A do not work well in the diet (Stark, 1977).…”

Light-dependent metabolic pathway of 3-hydroxyretinoids in the eye of a butterfly, Papilio xuthus

“…It has been reported that eyes of lepidopteran insects are unable to synthesize 3-hydroxyretinoids from retinal or retinol (Vogt 1984;Bennett and White 1991). In order to verify the oxidation of all-trans 3-hydroxyretinol to all-trans 3-hydroxyretinal in the distal layer of the eyes, all-trans retinol was used as a tracer.…”