Opsin-G11-Mediated Signaling Pathway for Photic Entrainment of the Chicken Pineal Circadian Clock

Aug 28, 2002The Journal of neuroscience : the official journal of the Society for Neuroscience

Light-sensitive signaling pathway that helps the chicken’s pineal gland keep daily time

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Abstract

G11alpha, a subunit of a specific signaling protein, is expressed in both the chicken pineal gland and retina.

G11alpha was identified in chicken pineal cells and retinal photoreceptor cells through various molecular techniques.
Colocalization of G11alpha with pinopsin and rhodopsin suggests it may functionally interact with these light-sensitive molecules.
Evidence indicates that G11alpha interacts with rhodopsin in a manner that depends on light and a specific signaling molecule (GTP).
Activation of G11alpha through a specific receptor in cultured pineal cells led to phase-dependent shifts in melatonin rhythm, similar to light exposure effects.
No effect was observed on the rhythm in control cells or those expressing a different receptor type, indicating the selectivity of G11 protein activation.

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Light is a major environmental signal for entrainment of the circadian clock, but little is known about the intracellular phototransduction pathway triggered by light activation of the photoreceptive molecule(s) responsible for the phase shift of the clock in vertebrates. The chicken pineal gland and retina contain the autonomous circadian oscillators together with the photic entrainment pathway, and hence they represent useful experimental models for the clock system. Here we show the expression of G11alpha, an alpha subunit of heterotrimeric G-protein, in both tissues by cDNA cloning, Northern blot, and Western blot analyses. G11alpha immunoreactivity was colocalized with pinopsin in the chicken pineal cells and also with rhodopsin in the outer segments of retinal photoreceptor cells, suggesting functional coupling of G11alpha with opsins in the clock-containing photosensitive tissues. The physical interaction was examined by coimmunoprecipitation experiments, the results of which provided evidence for light- and GTP-dependent coupling between rhodopsin and G11alpha. To examine whether activation of endogenous G11 leads to a phase shift of the oscillator, Gq/11-coupled m1-type muscarinic acetylcholine receptor (mAChR) was ectopically expressed in the cultured pineal cells. Subsequent treatment of the cells with carbamylcholine (CCh), an agonist of mAChR, induced phase-dependent phase shifts of the melatonin rhythm in a manner very similar to the effect of light. In contrast, CCh treatment induced no measurable effect on the rhythm of nontransfected (control) cells or cells expressing G(i/o)-coupled m2-type mAChR, indicating selectivity of the G-protein activation. Together, our results demonstrate the existence of a G11-mediated opsin-signaling pathway contributing to the photic entrainment of the circadian clock.

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Opsin-G11-Mediated Signaling Pathway for Photic Entrainment of the Chicken Pineal Circadian Clock

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