Davies, W.I., Zheng, L., Hughes, S., Tamai, T.K., Turton, M., Halford, S., Foster, R.G., Whitmore, D., and Hankins, M.W. (2011) Functional diversity of melanopsins and their global expression in the teleost retina. Cellular and molecular life sciences : CMLS. 68(24):4115-32.
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.