Early opsin expression in Xenopus embryos precedes photoreceptor differentiation

doi:10.1016/0169-328X(93)90016-I

Molecular Brain Research

Volume 17, Issues 3–4, March 1993, Pages 307-318

https://doi.org/10.1016/0169-328X(93)90016-I Get rights and content

Abstract

The visual pigment which serves as the first step in the phototransduction cycle in vertebrate rod cells consists of a retinal chromophore which is linked to the transmembrane protein, opsin. Opsin genes have been isolated from a number of different organisms and studies have shown opsin to be developmentally regulated with both mRNA and protein expression associated with the morphological differentiation of photoreceptor cells. Due to its potential utility as a marker for rod photoreceptor determination in studies of retinal tissue interactions, and because no amphibian opsin genes have as yet been cloned, we isolated cDNA clones of the Xenopus laevis opsin gene. Sequence analysis shows that within the coding region Xenopus opsin shares a high degree of identity with other rod opsin genes, except at the C-terminal where it more closely resembles the mammalian color opsins. A developmental analysis, on the other hand, reveals that Xenopus opsin transcripts are detectable in a retina-specific fashion early in retinal development. Using in situ hybridization we find that Xenopus opsin mRNA is initially restricted to a few isolated cells in the presumptive photoreceptor layer which express the gene at relatively high levels. This suggests that rod photoreceptor determination occurs in single cells, and that the mechanisms controlling opsin expression in Xenopus are initiated well before any evidence of morphological differentiation.

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Studies in birds have confirmed that light can pass through the eggshell, stimulate the eyes and affect the performance of bird embryos (Mascetti and Vallortigara, 2001; Archer, 2018). In amphibians, early opsin expression occurred in Xenopus laevis embryos before the morphological differentiation of rod photoreceptors (Saha and Grainger, 1993). These findings could indicate that the visual systems in these species are functional.
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This assumption, which has created considerable confusion in the field, would only be warranted if the entire process of photoreceptor differentiation were controlled cell autonomously by intrinsic mechanisms set in motion in early photoreceptor progenitors; but it is not. Although cell-autonomous mechanisms do control some initial aspects of photoreceptor differentiation, including the expression of a small group of photoreceptor-specific genes (Adler, 2000; Bradford et al., 2005; Bruhn and Cepko, 1996; Johnson et al., 2001; Saha and Grainger, 1993; Stenkamp et al., 1997), most aspects of the photoreceptor differentiation occur much later in development and appear to be regulated by microenvironmental factors rather than by cell-autonomous mechanisms. These late differentiation events include outer segment formation, synaptogenesis and the expression of most photoreceptor-specific genes (Bradford et al., 2005; Bruhn and Cepko, 1996; Bumsted et al., 1997; Cepko, 1996; Johnson et al., 2001).
How does a retinal progenitor choose to differentiate as a rod or a cone and, if it becomes a cone, which one of their different subtypes? The mechanisms of photoreceptor cell fate specification and differentiation have been extensively investigated in a variety of animal model systems, including human and non-human primates, rodents (mice and rats), chickens, frogs (Xenopus) and fish. It appears timely to discuss whether it is possible to synthesize the resulting information into a unified model applicable to all vertebrates. In this review we focus on several widely used experimental animal model systems to highlight differences in photoreceptor properties among species, the diversity of developmental strategies and solutions that vertebrates use to create retinas with photoreceptors that are adapted to the visual needs of their species, and the limitations of the methods currently available for the investigation of photoreceptor cell fate specification. Based on these considerations, we conclude that we are not yet ready to construct a unified model of photoreceptor cell fate specification in the developing vertebrate retina.
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Early genes are first expressed at, or shortly after the time of photoreceptor birth, preceding outer segment formation by many days, or even weeks. Examples, analyzed by in situ hybridization and/or immunocytochemistry, include IRPB and visinin in the chick (this report; see also Bruhn and Cepko, 1996), IRPB in the goldfish (Stenkamp et al., 1997), arrestin, rhodopsin, and recoverin in the ferret (Johnson et al., 2001), and rhodopsin in Xenopus (Saha and Grainger, 1993). Several lines of evidence suggest that this early phase of photoreceptor differentiation is regulated by cell-intrinsic mechanisms.
Photoreceptor differentiation requires the coordinated expression of numerous genes. It is unknown whether those genes share common regulatory mechanisms or are independently regulated by distinct mechanisms. To distinguish between these scenarios, we have used in situ hybridization, RT-PCR, and real-time PCR to analyze the expression of visual pigments and other photoreceptor-specific genes during chick embryo retinal development in ovo, as well as in retinal cell cultures treated with molecules that regulate the expression of particular visual pigments. In ovo, onset of gene expression was asynchronous, becoming detectable at the time of photoreceptor generation (ED 5–8) for some photoreceptor genes, but only around the time of outer segment formation (ED 14–16) for others. Treatment of retinal cell cultures with activin, staurosporine, or CNTF selectively induced or down-regulated specific visual pigment genes, but many cognate rod- or cone-specific genes were not affected by the treatments. These results indicate that many photoreceptor genes are independently regulated during development, are consistent with the existence of at least two distinct stages of gene expression during photoreceptor differentiation, suggest that intrinsic, coordinated regulation of a cascade of gene expression triggered by a commitment to the photoreceptor fate is not a general mechanism of photoreceptor differentiation, and imply that using a single photoreceptor-specific “marker” as a proxy to identify photoreceptor cell fate is problematic.
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The role of thyroid hormone in Xenopus metamorphosis is particularly well understood as it plays an essential role in that process. However, recent evidence suggests that thyroid hormone may play an earlier role in amphibian embryogenesis. We demonstrate that Xenopus thyroid hormone receptor β (XTRβ) is expressed shortly after neural fold closure, and that its expression is localized to the developing retina. Retinoid X receptor γ (RXRγ), a potential dimerization partner for XTRβ, was also found to be expressed in the retina at early stages, and at later stages RXRγ was also expressed in the liver diverticulum. Addition of either thyroid hormone or 9-cis retinoic acid, the ligands for XTRβ and RXRγ, respectively, did not alter the expression of their receptors. However, the addition of thyroid hormone and 9-cis retinoic acid did alter rhodopsin mRNA expression. Addition of thyroid hormone generates a small expansion of the rhodopsin expression domain. When 9-cis retinoic acid or a combination of thyroid hormone and 9-cis retinoic acid was administered, there was a decrease in the expression domain of rhodopsin in the developing retina. These results provide evidence for an early role for XTRβ and RXRγ in the developing Xenopus retina.
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Others have a similar time of onset, but are found throughout the cell (e.g. γ-transducin, PDEγ, and phosducin), implying that distinct protein-trafficking mechanisms are at work (Fariss et al., 1997). The onset of expression of each of these proteins appears to be synchronized amongst both old and young photoreceptors, whereas the rod opsin and recoverin protein-expression patterns emerge gradually in cells in accord with their neurogenetic gradients, occurring first in a few cells in the central retina, spreading to cells at increasingly peripheral locations, and continuing to be expressed in more and more cells at all retinal loci as these cells are generated (Johnson et al., 2001b; see also Bowes et al., 1988; Treisman et al., 1988; Saha and Grainger, 1993). Because rod opsin and recoverin protein expression follow such different spatio-temporal gradients from those other outer segment-associated proteins, and since in some other species, rod opsin is reported to be expressed at the same time as these other proteins (Timmers et al., 1993; van Ginkel and Hauswirth, 1994), one might question whether the early immunodetection of rod opsin and recoverin was spurious or artifactual.
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Research reportEarly opsin expression in Xenopus embryos precedes photoreceptor differentiation

Abstract

J. Biol. Chem.

Vision Res.

Vision Res.

FEBS Lett.

Exp. Eye Res.

Dev. Biol.

J. Biol. Chem.

Cell

Methods Cell Biol.

Dev. Biol.

Biochem. Biophys. Res. Commun.

Neuron

TIG

Dev. Biol.

J. Mol. Biol.

Cell

Prog. Brain Res.

Int. J. Biol. Macromol.

Dev. Biol.

Curr. Opin. Genet. Dev.

Vision Res.

Neuron

A temporally regulated, diffusible activity is required for rod photoreceptor development in vitro

Development

Characterization of bovine rhodopsin mRNA and cDNA

Biophys. J.

A molecular view of vertebrate retinal development

Mol. Neurobiol.

The structural and functional development of the retina in larval Xenopus

J. Embryol. Exp. Morphol.

S-antigen in the developing retina and pineal gland: a monoclonal antibody study

Invest. Opthamol. Vis. Sci.

The molecular genetics of photoreceptor cells

Prog. Ret. Res.

The pineal eye in Xenopus laevis, embryos and larvae: a photoreceptor with a direct excitatory effect on behavior

J. Comp. Physiol.

Research report
Early opsin expression in Xenopus embryos precedes photoreceptor differentiation