Light-transduction in melanopsin-expressing photoreceptors of Amphioxus
- 2 June 2009
- journal article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences
- Vol. 106 (22), 9081-9086
- https://doi.org/10.1073/pnas.0900708106
Abstract
Spatial vision in different organisms is mediated by 2 classes of photoreceptors: microvillar and ciliary. Recently, additional photosensitive cells implicated in nonvisual light-dependent functions have been identified in the mammalian retina. A previously undescribed photopigment, melanopsin, underlies these photoresponses, and it has been proposed that its transduction mechanisms may be akin to the lipid-signaling scheme of invertebrate microvillar receptors, rather than the cyclic-nucleotide cascade of vertebrates. Melanopsin has an ancient origin in deuterostomia, and expresses in 2 morphologically distinct classes of cells in the neural tube of Amphioxus, the most basal extant chordate: pigmented ocelli, and Joseph cells. However, to our knowledge, their physiology and alleged photosensitivity had never been investigated. We dissociated both types of cells, and conclusively demonstrated by patch-electrode recoding that they are primary photoreceptors; their receptor potential is depolarizing, accompanied by an increase in membrane conductance. The action spectrum peaks in the blue region, approximately 470 nm, similar to the absorption of melanopsin in vitro. The light-dependent conductance rectifies inwardly; Na and Ca are differentially implicated in the 2 cell types. Fluorescence Ca imaging reveals that photostimulation rapidly mobilizes calcium from internal stores. Intracellular 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetate severely impairs the photoresponse, indicating that light-evoked Ca elevation is an important event in photoexcitation. These observations support the notion that the lineage of microvillar photoreceptors and its associated light-signaling pathway also evolved in the chordates. Thus, Joseph cells and pigmented ocelli of the Amphioxus may represent a link between ancestral rhabdomeric-like light sensors present in prebilaterians and the circadian photoreceptors of higher vertebrates.Keywords
This publication has 44 references indexed in Scilit:
- Photon capture and signalling by melanopsin retinal ganglion cellsNature, 2008
- The outer segment serves as a default destination for the trafficking of membrane proteins in photoreceptorsThe Journal of general physiology, 2008
- Gq‐coupled Rhodopsin Subfamily Composed of Invertebrate Visual Pigment and Melanopsin†Photochemistry and Photobiology, 2008
- The amphioxus genome and the evolution of the chordate karyotypeNature, 2008
- Melanopsin-Containing Retinal Ganglion Cells: Architecture, Projections, and Intrinsic PhotosensitivityScience, 2002
- New perspectives on the evolution of protochordate sensory and locomotory systems, and the origin of brains and headsPhilosophical Transactions Of The Royal Society B-Biological Sciences, 2001
- Ion permeation through light-activated channels in rhabdomeric photoreceptors. Role of divalent cations.The Journal of general physiology, 1996
- Pupillary light reflexCurrent Opinion in Opthalmology, 1995
- On the Fine Structure of the Amphioxus PhotoreceptorThe Tohoku Journal of Experimental Medicine, 1964
- Fine structure of photoreceptors in amphioxusJournal of Ultrastructure Research, 1962