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The Journal of Neuroscience, July 15, 2000, 20(14):5254-5263
Light Transduction in Invertebrate Hyperpolarizing
Photoreceptors: Possible Involvement of a Go-Regulated
Guanylate Cyclase
Maria del Pilar
Gomez and
Enrico
Nasi
Department of Physiology, Boston University School of Medicine,
Boston, Massachusetts 02118, and Marine Biological Laboratory, Woods
Hole, Massachusetts 02543
The hyperpolarizing receptor potential of scallop ciliary
photoreceptors is attributable to light-induced opening of
K+-selective channels. Having previously
demonstrated the activation of this K+ current by
cGMP, we examined upstream events in the transduction cascade.
GTP- -S produced persistent excitation after a flash, accompanied by
decreased sensitivity and acceleration of the photocurrent, whereas
GDP- -S only inhibited responsiveness, consistent with the
involvement of a G-protein. Because Go (but not
Gt nor Gq) recently has been
detected in the ciliary retinal layer of a related species, we tested
the effects of activators of Go; mastoparan peptides
induced an outward current suppressible by blockers of the
light-sensitive conductance such as
L-cis-diltiazem. In addition, intracellular
dialysis with the A-protomer of pertussis toxin (PTX) depressed the
photocurrent. The mechanisms that couple G-protein stimulation to
changes in cGMP were investigated. Intracellular IBMX enhanced the
photoresponse with little effect on the baseline current, a result that
argues against regulation by light of phosphodiesterase activity.
LY83583, an inhibitor of guanylate cyclase (GC), exerted a reversible,
dose-dependent suppression of the photocurrent. By contrast, ODQ, an
antagonist of NO-sensitive GC, and YC-1, an activator of NO-sensitive
GC, failed to alter the light response or the holding current;
furthermore, the NO synthase inhibitor N-methyl-
L-arginine was inert, indicating that the NO signaling pathway is not implicated. Taken together, these results suggest a
novel type of phototransduction cascade in which stimulation of a
PTX-sensitive Go may activate a membrane GC to induce an increase in cGMP and the consequent opening of light-dependent channels.
Key words:
invertebrate photoreceptors; light-dependent channels; phototransduction; cGMP; guanylate cyclase; PDE; PTX; G-protein
Copyright © 2000 Society for Neuroscience 0270-6474/00/20145254-10$05.00/0
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