On visual pigment templates and the spectral shape

Authors: Doekele G Stavenga

Publish Date: 2010/08/20

Volume: 196, Issue: 11, Pages: 869-878

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Abstract

The absorbance spectra of visual pigments can be approximated with mathematical expressions using as single parameter the absorbance peak wavelength A comparison of the formulae of Stavenga et al in Vision Res 331011–1017 1993 and Govardovskii et al in Vis Neurosci 17509–528 2000 applied to a number of invertebrate rhodopsins reveals that both templates well describe the normalized αband of rhodopsins with peak wavelength  400 nm the template spectra are virtually indistinguishable in an absorbance range of about three log units The template formulae of Govardovskii et al in Vis Neurosci 17509–528 2000 describe the rhodopsin spectra better for absorbances below 10−3 The template predicted spectra deviate in the ultraviolet wavelength range from each other as well as from measured spectra preventing a definite conclusion about the spectral shape in the wavelength range 400 nm The metarhodopsin spectra of blowfly and fruitfly R16 photoreceptors derived from measured data appear to be virtually identical The established templates describe the spectral shape of fly metarhodopsin reasonably well However the best fitting template spectrum slightly deviates from the experimental spectra near the peak and in the longwavelength tail Improved formulae for fitting the fly metarhodopsin spectra are proposedVision starts with the absorption of photons by the visual pigment rhodopsin molecules This causes conversion of the rhodopsin molecules into the socalled active metarhodopsin state which then by coupling to a Gprotein triggers the phototransduction process The metarhodopsin is inactivated by binding to an arrestin molecule which stops the phototransduction machinery In the photoreceptors of vertebrates the metarhodopsins rapidly thermally decay into a separate opsin protein and chromophore and hence the possible photoreconversion of metarhodopsin into the native rhodopsin is in normal light conditions negligible the visual pigment content of vertebrate photoreceptors therefore is maintained by a highly involved enzymatic renewal process Saari 2000 In contrast with this the metarhodopsins of invertebrate photoreceptors are thermostable Hamdorf 1979 The metarhodopsin—both the active and inactive state—can also absorb a photon which then results in regeneration of the rhodopsin eventually after release of the bound arrestin and dephosphorylation of rhodopsin Photoreconversion of metarhodopsin is therefore considered to be a prominent pathway for visual pigment maintenance in invertebrates Nevertheless invertebrates renew their visual pigment molecules also Schwemer 1984 Goldsmith and Bernard 1985 but like in vertebrates this process is slow taking several minutes to hours Schwemer 1989Intense and prolonged illumination of invertebrate photoreceptors results in a photoequilibrium of their visual pigments where the rhodopsin to metarhodopsin concentration ratio is determined by the absorbance spectra and quantum efficiencies of the two visual pigment states and the spectral composition of the illuminant Consequently in studies of invertebrate phototransduction not only the spectral properties of the rhodopsin but also those of the metarhodopsin have to be known specifically when concerning the interaction of arrestin with metarhodopsin Belušič et al 2010 Satoh et al 2010 The aim of the present paper was to update the current knowledge of invertebrate visual pigment spectraThe absorbance spectra of vertebrate rhodopsins known half a century ago inspired Dartnall 1953 to devise a nomogram from which the spectral shape of any rhodopsin could be derived using only one parameter the peak wavelength λ max This lead was followed by several other investigators notably Mansfield and MacNichol MacNichol 1986 who demonstrated that the spectra of vertebrate visual pigments have the same shape when plotted on an inverse wavelength scale The two classes of visual pigments based on vitamin A1 and vitamin A2 each appeared to have a specific invariant shapeFor both the vitamin A1 and A2based visual pigments Stavenga et al 1993 developed modified lognormal formulae with free parameter λ max that well described the shape of experimental absorbance spectra plotted on a linear ordinate scale Absorbance measurements can usually be accurately measured over about two log units of magnitude but photoreceptor spectral sensitivities can often be conveniently measured over several log units Lamb 1995 therefore devised a new template that covered a large sensitivity range Govardovskii et al 2000 elaborated this approach further by fitting the spectra of several vertebrate visual pigments thus achieving a now widely used set of formulaeConcerning the visual pigments of invertebrates Lipetz and Cronin 1988 found that experimentally measured spectra of crustacean rhodopsins were well described by the vitamin A1 template of vertebrate visual pigments but not by the template of vitamin A2 visual pigments and thus they suggested that retinal is the chromophore of crustacean rhodopsins Vertebrate and invertebrate visual pigments apparently follow very similar spectral rules and the templates initially developed for vertebrate rhodopsins thus are now used by both researchers of vertebrate and invertebrate visionAssuming that the rhodopsin template also holds for metarhodopsins metarhodopsin spectra have been derived from absorbance difference measurements on isolated invertebrate eyes eg moth Langer et al 1979 crayfish Cronin and Goldsmith 1982 fruitfly Salcedo et al 1999 Kiselev et al 2000 firefly Cronin et al 2000 Here we reconsider the rhodopsin and metarhodopsin absorbance spectra of a number of invertebrate species and specifically investigate whether the R16 photoreceptors of the blowfly Calliphora and Drosophila have metarhodopsins with the same invariant spectral shape as that of the rhodopsins It appears that the fly metarhodopsin absorbance spectra slightly deviate from the spectrum predicted by the rhodopsin template

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