UV-Sensitive Photoreceptor Protein OPN5 in Humans and Mice

Yoshitaka Fukada,Rika Morishita,Daisuke Kojima,Suguru Mori,Akimori Wada,Masaki Torii,Shin Yamazaki

doi:10.1371/journal.pone.0026388

Abstract

A variety of animal species utilize the ultraviolet (UV) component of sunlight as their environmental cues, whereas physiological roles of UV photoreception in mammals, especially in human beings, remain open questions. Here we report that mouse neuropsin (OPN5) encoded by the Opn5 gene exhibited an absorption maximum (λmax) at 380 nm when reconstituted with 11-cis-retinal. Upon UV-light illumination, OPN5 was converted to a blue-absorbing photoproduct (λmax 470 nm), which was stable in the dark and reverted to the UV-absorbing state by the subsequent orange light illumination, indicating its bistable nature. Human OPN5 also had an absorption maximum at 380 nm with spectral properties similar to mouse OPN5, revealing that OPN5 is the first and hitherto unknown human opsin with peak sensitivity in the UV region. OPN5 was capable of activating heterotrimeric G protein Gi in a UV-dependent manner. Immuno-blotting analyses of mouse tissue extracts identified the retina, the brain and, unexpectedly, the outer ears as the major sites of OPN5 expression. In the tissue sections of mice, OPN5 immuno-reactivities were detected in a subset of non-rod/non-cone retinal neurons as well as in the epidermal and muscle cells of the outer ears. Most of these OPN5-immuno-reactivities in mice were co-localized with positive signals for the alpha-subunit of Gi. These results demonstrate the first example of UV photoreceptor in human beings and strongly suggest that OPN5 triggers a UV-sensitive Gi-mediated signaling pathway in the mammalian tissues.

Highlights

The ultraviolet (UV) component of sunlight is utilized in a variety of animal species for their environmental cues, e.g., for flower discrimination and orientation/navigation in insects [1,2] and for mate choice and parent-offspring communication in birds [3,4]
The Opn5 gene was first identified in the mouse and human genomes, and its mRNA expression was detected in various neural tissues such as the brain, the spinal cord and the retina [8], though detailed expression pattern within these mammalian tissues has not been reported to date
Spectral properties of mouse and human OPN5 For functional analysis, we first attempted overexpression of mouse OPN5 in HEK293T cells by transient transfection without supply of retinals, which yielded no detectable amount of OPN5 protein

Summary

Introduction

The ultraviolet (UV) component of sunlight is utilized in a variety of animal species for their environmental cues, e.g., for flower discrimination and orientation/navigation in insects [1,2] and for mate choice and parent-offspring communication in birds [3,4] These animals have UV-sensitive photoreceptors in their eyes [5]. Avian homologues of OPN5 have been reported to function as a violet(quail) or UV- (chicken) sensitive photopigment and to activate G protein signaling [10,11] These studies suggest spectral divergence of OPN5 among species, leaving a question as to whether mammalian OPN5 has the maximal sensitivity in the visible region like many other opsins, or in the UV region. We present several lines of evidence suggesting that OPN5 activates a Gi-mediated phototransduction pathway in the mammalian cells

Methods

Results

Conclusion