Journal
JOURNAL OF BIOLOGICAL CHEMISTRY
Volume 292, Issue 31, Pages 12971-12980Publisher
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DOI: 10.1074/jbc.M117.793539
Keywords
brain; G protein-coupled receptor (GPCR); molecular evolution; photobiology; rhodopsin; ultraviolet-visible spectroscopy (UV-Vis spectroscopy)
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Funding
- JSPS KAKENHI Grants [25840122, 17K15109, 26708002]
- Uehara Memorial Foundation
- Center for the Promotion of Integrated Sciences of SOKENDAI
- Cooperative Study Program of the National Institute for Physiological Sciences
- Grants-in-Aid for Scientific Research [26708002, 17K15109] Funding Source: KAKEN
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Ciliary opsins were classically thought to function only in vertebrates for vision, but they have also been identified recently in invertebrates for non-visual photoreception. Larvae of the annelid Platynereis dumerilii are used as a zooplankton model, and this zooplankton species possesses a vertebrate-type ciliary opsin (named c-opsin) in the brain. Platynereis c-opsin is suggested to relay light signals for melatonin production and circadian behaviors. Thus, the spectral and biochemical characteristics of this c-opsin would be directly related to non-visual photoreception in this zooplankton model. Here we demonstrate that the c-opsin can sense UV to activate intracellular signaling cascades and that it can directly bind exogenous all-trans-retinal. These results suggest that this c-opsin regulates circadian signaling in a UV-dependent manner and that it does not require a supply of 11-cis-retinal for photoreception. Avoidance of damaging UV irradiation is a major cause of large-scale daily zooplankton movement, and the observed capability of the c-opsin to transmit UV signals and bind all-trans-retinal is ideally suited for sensing UV radiation in the brain, which presumably lacks enzymes producing 11-cis-retinal. Mutagenesis analyses indicated that a unique amino acid residue (Lys-94) is responsible for c-opsin-mediated UV sensing in the Platynereis brain. We therefore propose that acquisition of the lysine residue in the c-opsin would be a critical event in the evolution of Platynereis to enable detection of ambient UV light. In summary, our findings indicate that the c-opsin possesses spectral and biochemical properties suitable for UV sensing by the zooplankton model.
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