Abstract
Scallop retinas contain ciliary photoreceptor cells that respond to light by hyperpolarization like vertebrate rods and cones, but the response is generated by a different phototransduction cascade from those of rods and cones. To elucidate the cascade, we investigated a visual pigment and a G-protein functioning in the hyperpolarizing cell. Sequencing of cDNAs and in situ hybridization experiments showed that the hyperpolarizing cells express a novel subtype of visual pigment, which showed significant differences in amino acid sequence from other visual pigments. Cloning cDNA genes of G-protein and immunohistochemical analysis revealed the presence of an alpha subunit of a Go type G-protein, 83% identical in amino acid sequence to mammalian Go(alpha) in the nervous system, in the photoreceptive region of the cells. The results demonstrate that a novel, Go-mediated, phototransduction cascade is present in the hyperpolarizing cells. The phototransduction cascade in the scallop hyperpolarizing cell provides an alternative system to investigate Go-mediated transduction pathways in the nervous system. Molecular phylogenetic analysis strongly suggests that the Go-mediated phototransduction system emerged before the divergence of animals into vertebrate and invertebrate in the course of evolution.
Highlights
The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EBI Data Bank with accession number(s) AB006454, AB006455, AB006456, and AB006457
One is the Gt1-mediated system of vertebrate hyperpolarizing photoreceptor cells in which the visual pigment activates a cGMP-specific phosphodiesterase via a heterotrimeric G-protein, transducin (Gt) [1,2,3]
After the first electrophysiological recordings of Hartline [10], the mechanism of the hyperpolarizing response as well as its evolution have been discussed in comparison with vertebrate hyperpolarizing ciliary photoreceptor cells, rods and cones [11,12,13,14]
Summary
Daisuke Kojima‡§¶, Akihisa Terakita‡, Toru Ishikawa‡, Yasuo Tsukaharaʈ, Akio Maeda‡, and Yoshinori Shichida‡**. Scallop retinas contain ciliary photoreceptor cells that respond to light by hyperpolarization like vertebrate rods and cones, but the response is generated by a different phototransduction cascade from those of rods and cones. In the photoreceptor cells of animals’ eyes, visual pigments trigger a G-protein-mediated phototransduction cascade, which eventually generates an electrical response of the cells. After the first electrophysiological recordings of Hartline [10], the mechanism of the hyperpolarizing response as well as its evolution have been discussed in comparison with vertebrate hyperpolarizing ciliary photoreceptor cells, rods and cones [11,12,13,14] It has been reported, that the hyperpolarizing response in the scallop cell is due to opening of a cGMPsensitive potassium channel [11,12,13,14], which is different from that of the vertebrate cells (closing of a cGMP-sensitive cationic channel) [15]. We show evidence that the phototransduction system in the invertebrate hyperpolarizing photoreceptor cells is not mediated by Gt or Gq, but rather uses a novel, Go-mediated cascade
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