Disrupted eye and head development in rainbow trout with reduced ultraviolet (<i>sws1</i>) opsin expression

Flamarique, Inĩgo Novales; Fujihara, Ryo; Yazawa, Ryosuke; Bolstad, Kennedy; Gowen, Brent; Yoshizaki, Goro

doi:10.1002/cne.25144

Cited by 8 publications

(9 citation statements)

References 34 publications

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“…Simultaneous incubation with two antibodies for the purpose of detecting two different opsins was only possible with AHblue and AB5407. Antibody AB5407 is known to label SWS2, RH2, and RH1 opsins with varying affinity in rainbow trout, Oncorhynchus mykiss (Novales Flamarique et al., 2021), and 4D2 labels RH2 and RH1 opsins in multiple fishes (Novales Flamarique, 2011). Antibody 1D4 against bovine RH1 opsin (Molday & MacKenzie, 1983) and AB5405 (Chemicon) against human MWS/LWS opsin were also attempted.…”

Section: Methodsmentioning

confidence: 99%

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Chromatic organization of retinal photoreceptors during eye migration of Atlantic halibut (Hippoglossus hippoglossus)

Bolstad

Flamarique

2022

J of Comparative Neurology

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The retinas of fishes often have single and double cone photoreceptors that are organized in lattice‐like mosaics. In flatfishes experiencing eye migration (i.e., the metamorphic process whereby one eye migrates to the other side of the head), the hexagonal lattice of single cones present in the larva undergoes major restructuring resulting in a dominant square mosaic postmetamorphosis consisting of four double cones surrounding each single cone. The expression of different opsin types during eye migration has not been examined despite its importance in understanding photoreceptor plasticity and whether cell fate (in terms of spectral phenotype) could influence square mosaic formation. Here, we probed the retina of Atlantic halibut undergoing eye migration for opsin expression using two antibodies, AHblue and AB5407, that labeled short wavelength sensitive 2 (SWS2) opsin and longer wavelength (predominantly middle wavelength sensitive, RH2) opsins, respectively. Throughout the retina, double and triple cones labeled with AB5407 exclusively, whereas the vast majority of single cones labeled with AHblue. A minority (<5%) of single cones in the square mosaic of the centroventral retina labeled with AB5407. In regions of mosaic transition and near peripheral growth zones, some single cones co‐expressed at least two opsins as they labeled with both antibodies. Short wavelength (SWS2 expressing, or S) cones formed a nonrandom mosaic gradient from central to dorsal retina in a region dominated by the larval single cone mosaic. Our results demonstrate the expression of at least two opsins throughout the postmetamorphic retina and suggest opsin switching as a mechanism to create new cone spectral phenotypes. In addition, the S cone gradient at the onset of eye migration may underlie a plastic, cell induction mechanism by which a cone's phenotype determines that of its neighbors and the formation of the square mosaic.

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Section: Methodsmentioning

confidence: 99%

“…Novales Flamarique et al, 2021), and 4D2 labels RH2 and RH1 opsins in multiple fishes(Novales Flamarique, 2011). Antibody 1D4 against bovine RH1 opsin(Molday & MacKenzie, 1983) and AB5405 (Chemicon) against human MWS/LWS opsin were also attempted.…”

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confidence: 99%

Chromatic organization of retinal photoreceptors during eye migration of Atlantic halibut (Hippoglossus hippoglossus)

Bolstad

Flamarique

2022

J of Comparative Neurology

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“…The lack of sws1 does not cause retinal degeneration in mouse, 52 , 53 but causes serious retinal developmental defects in rainbow trout. 54 Sws1 deficiency did not lead to retinal degeneration in medaka. The reason why the loss of sws1 did not induce serious effects as trout is unclear, but the sequence of opsin genesis may explain it.…”

Section: Discussionmentioning

confidence: 79%

“…Although a lack of sws1 in mouse does not cause retinal degeneration, 52 , 53 a recent study of CRISPR/Cas-driven sws1 -mutant trout reports serious effects on the retina, including retinal degeneration. 54 Thus, we investigated the effect of sws1 deficiency on retinal structure and arrestin expression using medaka. To this end, we established two medaka lines, a transgenic sws1 -reporter and an sws1 -deficient line, and produced a monoclonal antibody specifically recognizing SWS1.…”

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confidence: 99%

Retinal Cone Mosaic in sws1-Mutant Medaka (Oryzias latipes), A Teleost

Matsuo

Matsuyama

Kobayashi

et al. 2022

Invest. Ophthalmol. Vis. Sci.

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Purpose Ablation of short single cones (SSCs) expressing short-wavelength-sensitive opsin (SWS1) is well analyzed in the field of regenerative retinal cells. In contrast with ablation studies, the phenomena caused by the complete deletion of SWS1 are less well-understood. To assess the effects of SWS1 deficiency on retinal structure, we established and analyzed sws1 -mutant medaka. Methods To visualize SWS1, a monoclonal anti-SWS1 antibody and transgenic reporter fish ( Tg ( sws1:mem-egfp )) were generated. We also developed a CRISPR/Cas-driven sws1 -mutant line. Retinal structure of sws1 mutant was visualized using anti-SWS1, 1D4, and ZPR1 antibodies and coumarin derivatives and compared with wild type, Tg ( sws1:mem-egfp ) , and another opsin ( lws ) mutant. Results Our rat monoclonal antibody specifically recognized medaka SWS1. S ws1 mutant retained regularly arranged cone mosaic as lws mutant and its SSCs had neither SWS1 nor long wavelength sensitive opsin. Depletion of sws1 did not affect the expression of long wavelength sensitive opsin, and vice versa. ZPR1 antibody recognized arrestin spread throughout double cones and long single cones in wild-type, transgenic, and sws1 -mutant lines. Conclusions Comparative observation of sws1 -mutant and wild-type retinas revealed that ZPR1 negativity is not a marker for SSCs with SWS1, but SSCs themselves. Loss of functional sws1 did not cause retinal degeneration, indicating that sws1 is not essential for cone mosaic development in medaka. Our two fish lines, one with visualized SWS1 and the other lacking functional SWS1, offer an opportunity to study neural network synapsing with SSCs and to clarify the role of SWS1 in vision.

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“…Ontogenetic changes in cone opsin expression levels as a response to change in habitat have been reported in other reef fishes, for example, spotted unicornfish ( Naso brevirostris ) ( Tettamanti et al 2019 ) and dusky dottyback ( Pseudochromis fuscus ) ( Cortesi et al 2016 ). Alternatively, the SWS1α opsin may be expressed in other tissues and/or organs, where animal opsins have been demonstrated to serve other sensory modalities, for example, nonimage forming vision, thermosensation, hearing (see review by Leung and Montell [2017] ), taste ( Leung et al 2020 ), or potentially a nonsensory related function such as early eye and cranial development (see Novales Flamarique et al 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Molecular Evolution of Ultraviolet Visual Opsins and Spectral Tuning of Photoreceptors in Anemonefishes (Amphiprioninae)

Mitchell

Cheney

Lührmann

et al. 2021

Genome Biology and Evolution

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Many animals including birds, reptiles, insects, and teleost fishes can see ultraviolet (UV) light (shorter than 400 nm), which has functional importance for foraging and communication. For coral reef fishes, shallow reef environments transmit a broad spectrum of light, rich in UV, driving the evolution of diverse spectral sensitivities. However, the identities and sites of the specific visual genes that underly vision in reef fishes remain elusive and are useful in determining how evolution has tuned vision to suit life on the reef. We investigated the visual systems of 11 anemonefish (Amphiprioninae) species, specifically probing for the molecular pathways that facilitate UV-sensitivity. Searching the genomes of anemonefishes, we identified a total of eight functional opsin genes from all five vertebrate visual opsin subfamilies. We found rare instances of teleost UV-sensitive SWS1 opsin gene duplications, that produced two functionally-coding paralogs (SWS1α and SWS1β) and a pseudogene. We also found separate green sensitive RH2A opsin gene duplicates not yet reported in the family Pomacentridae. Transcriptome analysis revealed false clown anemonefish (Amphiprion ocellaris) expressed one rod opsin (RH1) and six cone opsins (SWS1β, SWS2B, RH2B, RH2A-1, RH2A-2, LWS) in the retina. Fluorescent in-situ hybridisation highlighted the (co-)expression of SWS1β with SWS2B in single cones, and either RH2B, RH2A, or RH2A together with LWS in different members of double cone photoreceptors (two single cones fused together). Our study provides the first in-depth characterisation of visual opsin genes found in anemonefishes and provides a useful basis for the further study of UV-vision in reef fishes.

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Disrupted eye and head development in rainbow trout with reduced ultraviolet (sws1) opsin expression

Cited by 8 publications

References 34 publications

Chromatic organization of retinal photoreceptors during eye migration of Atlantic halibut (Hippoglossus hippoglossus)

Chromatic organization of retinal photoreceptors during eye migration of Atlantic halibut (Hippoglossus hippoglossus)

Retinal Cone Mosaic in sws1-Mutant Medaka (Oryzias latipes), A Teleost

Molecular Evolution of Ultraviolet Visual Opsins and Spectral Tuning of Photoreceptors in Anemonefishes (Amphiprioninae)

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