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Functional diversity of melanopsins and their global expression in the teleost retina

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Abstract

Melanopsin (OPN4) is an opsin photopigment that, in mammals, confers photosensitivity to retinal ganglion cells and regulates circadian entrainment and pupil constriction. In non-mammalian species, two forms of opn4 exist, and are classified into mammalian-like (m) and non-mammalian-like (x) clades. However, far less is understood of the function of this photopigment family. Here we identify in zebrafish five melanopsins (opn4m-1, opn4m-2, opn4m-3, opn4x-1 and opn4x-2), each encoding a full-length opsin G protein. All five genes are expressed in the adult retina in a largely non-overlapping pattern, as revealed by RNA in situ hybridisation and immunocytochemistry, with at least one melanopsin form present in all neuronal cell types, including cone photoreceptors. This raises the possibility that the teleost retina is globally light sensitive. Electrophysiological and spectrophotometric studies demonstrate that all five zebrafish melanopsins encode a functional photopigment with peak spectral sensitivities that range from 470 to 484 nm, with opn4m-1 and opn4m-3 displaying invertebrate-like bistability, where the retinal chromophore interchanges between cis- and trans-isomers in a light-dependent manner and remains within the opsin binding pocket. In contrast, opn4m-2, opn4x-1 and opn4x-2 are monostable and function more like classical vertebrate-like photopigments, where the chromophore is converted from 11-cis to all-trans retinal upon absorption of a photon, hydrolysed and exits from the binding pocket of the opsin. It is thought that all melanopsins exhibit an invertebrate-like bistability biochemistry. Our novel findings, however, reveal the presence of both invertebrate-like and vertebrate-like forms of melanopsin in the teleost retina, and indicate that photopigment bistability is not a universal property of the melanopsin family. The functional diversity of these teleost melanopsins, together with their widespread expression pattern within the retina, suggests that melanopsins confer global photosensitivity to the teleost retina and might allow for direct “fine-tuning” of retinal circuitry and physiology in the dynamic light environments found in aquatic habitats.

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Acknowledgments

We thank Dr. Rosalie Crouch and Dr. Jill Cowing for the generous provision of 11-cis retinal and 1D4 antibody; Dr. Stephen Price and Dr. Sofia Godinho for help with RNA in situ hybridisation experiments; Dr. Kara Cerveny for microscopy and photography advice; Dr. Stuart Peirson for his assistance on UV-vis template fitting and useful discussions; and University College London Fish Facility for adult zebrafish. We thank Prof. Shaun Collin for his advice on photoreceptor morphology. This work was supported by a grant awarded by the UK Biotechnology and Biological Research Council (BBSRC) to MWH.

Conflict of interest

The authors declare no competing financial interests.

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Authors and Affiliations

  1. Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neurosciences, Levels 5-6 West Wing, John Radcliffe Hospital, University of Oxford, Headley Way, Oxford, OX3 9DU, UK

    Wayne I. L. Davies, Lei Zheng, Steven Hughes, Michael Turton, Stephanie Halford, Russell G. Foster & Mark W. Hankins

  2. Department of Cell and Developmental Biology, Centre for Cell and Molecular Dynamics, University College London, 21 University Street, London, WC1E 6DE, UK

    T. Katherine Tamai & David Whitmore

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  1. Wayne I. L. Davies
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  2. Lei Zheng
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Correspondence to Mark W. Hankins.

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W. I. L. Davies and L. Zheng contributed equally to this research.

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Davies, W.I.L., Zheng, L., Hughes, S. et al. Functional diversity of melanopsins and their global expression in the teleost retina. Cell. Mol. Life Sci. 68, 4115–4132 (2011). https://doi.org/10.1007/s00018-011-0785-4

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