Carotenoid and retinoid — two pigments in a gecko eye lens

https://doi.org/10.1016/S1095-6433(99)00165-8Get rights and content

Abstract

The eye lenses of the Moroccan day gecko Quedenfeldtia trachyblepharus contain two different pigments: a retinoid (minor pigment) and a carotenoid (major pigment). The retinoid, all-trans 3,4-didehydroretinol, is bound to ι-crystallin, which comprises only 2% of the total amount of crystallins. The carotenoid is associated to γs-crystallin – comprising about 10% of total amount of crystallins – and causes the dark yellow colour of the lens. The absorption spectrum of the isolated carotenoid shows a major, triple-peaked band at 372, 392, and 416 nm and two minor peaks at 284 and 294 nm. This spectrum reminds of that of galloxanthin, a carotenoid found in oil droplets of some avian retinae. The absorption spectrum of the carotenoid-γs-crystallin complex is shifted 6–8 nm bathochromically. In the lens, this complex absorbs ultraviolet and shortwave blue radiation, supposedly improving the optical quality of the dioptric apparatus and protecting the retina against photodamage. Both the retinoid and the carotenoid are present in eye cups. The lenticular carotenoid of Quedenfeldtia is the first example of a carotenoid in the lens of a terrestrial vertebrate with a sufficiently high concentration to be physiologically effective as a UV-filter. Additionally, it is unique in being the first example of a carotenoid associated with γs-crystallin.

Introduction

The vertebrate eye lens is an avascular, transparent organ focusing the incoming light onto the retina. Its optical properties are defined by densely packed, highly stable structural proteins called crystallins. These can be divided into three main classes. The first class comprises the α- and β/γ-crystallins, which are ubiquitous in vertebrate lenses. These crystallins are more or less closely related to stress response proteins (Wistow and Piatigorsky, 1988, de Jong et al., 1994). The second class of crystallins involves ten taxon-specific crystallins which are found only in scattered groups of vertebrates and which are related to or even identical with enzymes, mostly pyridine nucleotide binding oxidoreductases (Wistow, 1995, Röll et al., 1995, Röll and de Jong, 1996).

The third class of crystallins so far comprises only the recently described ι-crystallin, which is not an enzyme (Röll et al., 1996, Röll and Schwemer, 1999). ι-Crystallin is identical with the cellular retinol-binding protein type I (CRBP I) which belongs to the family of small, intracellular lipid-binding proteins (Werten et al., 1998). It occurs exclusively in lenses of several diurnal geckos, absorbs shortwave radiation and may promote visual quality by reducing glare and chromatic aberration and by enhancing contrast (Röll et al., 1996, Röll and Schwemer, 1999).

The endogenous ligand of ι-crystallin turned out to be 3,4-didehydroretinol (vitamin A2). Dependent on its concentration, the ι-crystallin/3,4-didehydroretinol complex accounts for the characteristic pale or dark yellow colouration of lenses. In lenses of the Morrocan day gecko Quedenfeldtia trachyblepharis, ι-crystallin reaches only up to 2% of the total amount of crystallins. The colour of the lenses, however, is dark yellow, similar to lenses of Pristurus, which contain up to 9–12% ι-crystallin (Röll and Schwemer, 1999). Thus, the deep yellow colour of the lens of Quedenfeldtia should be due to another pigment.

The present paper reports the presence of a second pigment, a carotenoid, in the lens of Quedenfeldtia. This is the first example of a carotenoid in the lens of a terrestrial vertebrate reaching a sufficiently high concentration to be physiologically effective as a UV-filter. Additionally, it is the first example of a carotenoid associated with γs-crystallin.

Section snippets

Preparation of lens extracts

Geckos used in this study were adult specimens with a snout to vent length of 35–40 mm and a hatchling 1-week-old. Geckos were chilled, killed by decapitation, and enucleated. The eyes were carefully incised at their posterior segments so that the lenses could be removed. Freshly isolated or frozen lenses were homogenized in distilled water or buffer solution, depending on the different experiments. Insoluble fractions were removed by centrifugation at 4°C for 15 min at 15 000×g. Protein

Lens pigments

In order to identify lipid-soluble pigments of the lenses, extracts of them were analysed by HPLC. The chromatograms reveal two main peaks. One peak (Fig. 1A, peak 5) contains all-trans 3,4-didehydroretinol, the endogenous ligand of ι-crystallin. In contrast, the other peak (Fig. 1A, peak 4) does not contain a retinoid, but a substance with a conspicuous absorption spectrum (Fig. 2, solid line). Its major peak has a definite fine structure with an absorption maximum at 392 nm, two secondary

Discussion

The Moroccan day gecko Q. trachyblepharus inhabits predominantly rocky areas of the Atlas Mountains, where it is exposed to high ambient light intensities. Its eyelids are fused to a transparent spectacle and its pupil diameter is virtually constant, as in other diurnal geckos. Thus, the only alternative to reduce radiation of potentially harmful wavelengths before reaching the retina is to absorb it in the lens. In the lens of Quedenfeldtia, this is achieved by the presence of two different

Acknowledgements

I am grateful to Professor Dr J. Schwemer, Bochum, for generous help with the samples for HPLC analysis.

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