The non-visual opsins expressed in deep brain neurons projecting to the retina in lampreys

• Published in: Scientific reports Vol. 10; no. 1; p. 9669
• Main Authors: Kawano-Yamashita, Emi, Koyanagi, Mitsumasa, Wada, Seiji, Saito, Tomoka, Sugihara, Tomohiro, Tamotsu, Satoshi, Terakita, Akihisa
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 15.06.2020; Nature Publishing Group
• Subjects: 631/378/2613; 631/443/376; 631/45/612/194; Animals; Cell culture; Cephalaspidomorphi; Cilia; Cloning, Molecular; Fish Proteins - genetics; Fish Proteins - metabolism; Gene Expression Regulation; GTP-Binding Protein alpha Subunits - metabolism; Humanities and Social Sciences; Lampetra ayresii; Lampreys - genetics; Lampreys - metabolism; Mesencephalon; Mesencephalon - metabolism; multidisciplinary; Opsins; Opsins - genetics; Opsins - metabolism; Photoreception; Phylogeny; Pineal gland; Retina; Retina - metabolism; Rivers; Science; Science (multidisciplinary); Spectroscopy; Tissue Distribution; Vertebrates; Visual discrimination
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-020-66679-2

In lower vertebrates, brain photoreceptor cells express vertebrate-specific non-visual opsins. We previously revealed that a pineal-related organ-specific opsin, parapinopsin, is UV-sensitive and allows pineal wavelength discrimination in lampreys and teleost. The Australian pouched lamprey was recently reported as having two parapinopsin-related genes. We demonstrate that a parapinopsin-like opsin from the Japanese river lamprey exhibits different molecular properties and distribution than parapinopsin. This opsin activates Gi-type G protein in a mammalian cell culture assay in a light-dependent manner. Heterologous action spectroscopy revealed that the opsin forms a violet to blue-sensitive pigment. Interestingly, the opsin is co-localised with green-sensitive P-opsin in the cells of the M5 nucleus of Schober (M5NS) in the mesencephalon of the river and brook lamprey. Some opsins-containing cells of the river lamprey have cilia and others an axon projecting to the retina. The opsins of the brook lamprey are co-localised in the cilia of centrifugal neurons projecting to the retina, suggesting that cells expressing the parapinopsin-like opsin and P-opsin are sensitive to violet to green light. Moreover, we found neural connections between M5NS cells expressing the opsins and the retina. These findings suggest that the retinal activity might be modulated by brain photoreception.