Bertolesi GE et al. (2021), Type II Opsins in the Eye, the Pineal Complex a...

XB-ART-58863

Front Neuroanat 2021 Jan 01;15:784478. doi: 10.3389/fnana.2021.784478.

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Type II Opsins in the Eye, the Pineal Complex and the Skin of Xenopus laevis: Using Changes in Skin Pigmentation as a Readout of Visual and Circadian Activity.

Bertolesi GE , Debnath N , Malik HR , Man LLH , McFarlane S .

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The eye, the pineal complex and the skin are important photosensitive organs. The African clawed frog, Xenopus laevis, senses light from the environment and adjusts skin color accordingly. For example, light reflected from the surface induces camouflage through background adaptation while light from above produces circadian variation in skin pigmentation. During embryogenesis, background adaptation, and circadian skin variation are segregated responses regulated by the secretion of α-melanocyte-stimulating hormone (α-MSH) and melatonin through the photosensitivity of the eye and pineal complex, respectively. Changes in the color of skin pigmentation have been used as a readout of biochemical and physiological processes since the initial purification of pineal melatonin from pigs, and more recently have been employed to better understand the neuroendocrine circuit that regulates background adaptation. The identification of 37 type II opsin genes in the genome of the allotetraploid X. laevis, combined with analysis of their expression in the eye, pineal complex and skin, is contributing to the elucidation of the role of opsins in the different photosensitive organs, but also brings new questions and challenges. In this review, we analyze new findings regarding the anatomical localization and functions of type II opsins in sensing light. The contribution of X. laevis in revealing the neuroendocrine circuits that regulate background adaptation and circadian light variation through changes in skin pigmentation is discussed. Finally, the presence of opsins in X. laevis skin melanophores is presented and compared with the secretory melanocytes of birds and mammals.

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Species referenced: Xenopus laevis
Genes referenced: opn3 opn4 opn5 opn6a opn7a opn7b opn8 opnpl rgr rho rpe rrh tmtopn tmtopn2 zswim7
GO keywords: circadian rhythm [+]

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	Figure 1. Pigmentation response induced by reflected light from the substrate (background adaptation) or environmental light (dark/light) over Xenopus laevis development. (A) Pigmentation levels at different developmental times represented approximately (50%; day 5/6) from embryos raised on a white background (WB) (yellow column). The light shines from above in cycles of 12 h ON/12 h OFF and the pigmentation is measured at the middle of the light cycle. The timeline in days (X-axis) of embryos maintained at 16°C until stage 43/44 is assigned to the approximate developmental stage. Tadpoles raised on a white substrate (WB) are switched either to a black background for 4 h (BB; red columns) or dark for 30 min (D; green columns) (see schematic). The pigmentation response is measured in the dorsal head (see pictures). (B) Pigmentation response of stage 43/44 embryos compared to enucleation (No eye), pinealectomy (No P.C) or both (No eye, No P.C.). The surgery is performed 24 h before pigmentation measurement. (C) Morphological pigmentation of embryos induced by raising tadpoles on a black background from early stages. Note the difference in the “morphological” pigmentation (increase in melanophore number mainly around the eye) when tadpoles are raised on a BB vs. the quick “physiological” responses seen in tadpoles raised on a WB. See text for additional details.
	Figure 2. Expression of opsins in the Xenopus larval eye, pineal complex, and skin. (A) RT-PCR analysis showing mRNA expression of the indicated opsins at stage 43/44 in the whole embryo and isolated tails, and in a melanophore cell line (MEX) obtained from stage 30–35 X. laevis tadpoles (Kashina et al., 2004). RT-PCR conditions are similar to those published previously (Bertolesi et al., 2020, 2021). (B) Opsins identified in the X. laevis genome and their expression in the pineal complex, eye and tails. The putative amino acid sequences were compared, and a molecular phylogenetic analysis performed by the maximum-likelihood method is shown (not to scale). Type II opsins are grouped according to what was initially considered as their tissue localization: visual opsins (red); pineal opsins (green); non-visual opsins (blue); neuropsins (orange); photoisomerases (pink) and melanopsins (purple). Groups are also approximately reflected in the phylogenetic tree. Brackets denote genes duplicated and maintained on the long (L) and short (S) chromosomes, with single copy genes indicated with an asterisk. The table show the summary of expression of opsins in the eye (Bertolesi et al., 2021), the pineal complex (Bertolesi et al., 2020), and the tails and MEX cells as determined by RT-PCR as in A. (C) A comparative expression analysis determined by RNAseq of opn4 in different organs from both genes (L and S) is reproduced from Xenbase (http://www.xenbase.org/, RRID:SCR_003280). Darker color reflects higher mRNA expression.
	Figure 3. Localization and developmental expression of opsins in the eye. (A) Schematic of the central retina showing the expression of opsins in photoreceptors in the outer nuclear layer (ONL) in rods (Rh1; green and Sws2; white) and cones (Lws; orange and Sws1, blue). Pinopsin (light blue) is always co-expressed dorsally with a few sws1 positive cells. Melanopsin (yellow) is expressed both by intrinsically photosensitive horizontal cells (ipHC) located dorsally in the retina in the inner nuclear layer (INL), and a minor population of retinal ganglion cells in the ganglion cell layer (GCL) (RGCs; 2% of total), called the intrinsically photosensitive RGCs (ipRGC). opn5 mRNA (magenta) is expressed by cells in the outer portion of the INL and in the GCL, while opn8 mRNA (pink) is present in cells in the inner part of the INL, likely amacrine cells. opn6 (purple) expressing cells sit at the boundary of the proliferative CMZ and the ONL. rgr and rrh mRNAs (pink) are expressed by the RPE but excluded from the CMZ. A developmental timeline is schematized with an arrow at the bottom, with the emergence of opsin expression or specific behavioral responses indicated. (B) Opsins expressed in the eye, the pineal complex, and the skin (tails or MEX cells) of Xenopus laevis are shown at the approximate absorbance peak of their spectral sensitivity, and compared to the spectral sensitivity of human visual opsins. See text for additional details.

References [+] :

Allen, Form vision from melanopsin in humans. 2019, Pubmed