Calcium-Independent, cGMP-Mediated Light Adaptation in Invertebrate Ciliary Photoreceptors

Abstract

Calcium is thought to be essential for adaptation of sensory receptor cells. However, the transduction cascade of hyperpolarizing, ciliary photoreceptors of the scallop does not use IP 3 -mediated Ca release, and the light-sensitive conductance is not measurably permeable to Ca 2ϩ . Therefore, two typical mechanisms that couple the light response to [Ca] i changes seem to be lacking in these photoreceptors. Using fluorescent indicators, we determined that, unlike in their microvillar counterparts, photostimulation of ciliary cells under voltage clamp indeed evokes no detectable change in cytosolic Ca. Notwithstanding, these cells exhibit all of the hallmarks of light adaptation, including response range compression, sensitivity shift, and photoresponse acceleration. A possible mediator of Ca-independent sensory adaptation is cGMP, the second messenger that regulates the light-sensitive conductance; cGMP and 8-bromo cGMP not only activate lightdependent K channels but also reduce the amplitude of the light response to an extent greatly in excess of that expected from simple occlusion between light and chemical stimulation. In addition, these substances accelerate the time course of the photocurrent. Tests with pharmacological antagonists suggest that protein kinase G may be a downstream effector that controls, in part, the cGMP-triggered changes in photoresponse properties during light adaptation. However, additional messengers are likely to be implicated, especially in the regulation of response kinetics. These observations suggest a novel feedback inhibition pathway for signaling sensory adaptation.

Cyclic GMP and Cilia Motility

“…C-type natriuretic peptide (CNP) significantly elevates cGMP levels in ocular nonpigmented ciliary epithelial cells [ 22 ]. Even though non-microvillar photoreceptor cilia have distinctly different regulatory features than those of microvillar photoreceptors, invertebrate ciliary photoreceptors also regulate light adaptation through cGMP and PKG [ 23 ]. The elevation of cGMP levels decreases light sensitivity, as cGMP analogs are capable of potentiating light-induced desensitization.…”

Regulation of metabolism in estivating land snails: role of reversible protein phosphorylation

“…PKG has diverse functioning across the mollusc phylum. This kinase (and/or the cGMP second messenger that activates it) has been well characterized in the context of neural regulation in such models as Pectin irradians, sea hares of the genus Aplysia, and H. aspersa (Sung et al, 2004;Gomez and Nasi, 2005). There is also substantial evidence linking cGMP/PKG to key regulatory roles in hypometabolism in many mollusc models.…”

“…PKG seems to be central to cellular regulation across the Phylum Mollusca. In particular, PKG has been established in mediating neural functioning in several mollusc models such as Pectin irradians, sea hares of the genus Aplysia, and Helix aspersa (Sung et al, 2004;Gomez and Nasi, 2005). PKG has higher activity than protein kinase A (PKA) in bivalve myocardium (Higgins and Greenberg, 1974) and mediates gill muscle potentiation in the clam Mercenaria mercenaria (Gainey and Greenberg, 2003).…”

“…Recall that PKG stimulation in vitro mimicked the changes in recoverable Na+K+-ATPase and G6PDH activities that were observed in vivo in dormant snails and PKG stimulation was also linked with the activation of both AMPK and PKB. PKG has been implicated in regulating several aspects of mollusc biochemistry, from neural regulation to muscle potentiation (Gainey and Greenberg, 2003;Sung et al, 2004;Gomez and Nasi, 2005); in particular, it has been linked with metabolic reorganization during anoxia, another hypometabolic state (Larade and Storey, 2004). Thus, there is precedence for this kinase for having diverse and profound regulatory capacity in mollusc systems.…”

“…PKG is activated by cyclic 3'5'-guanosine monophosphate (cGMP) and seems to play a central role in cellular metabolic regulation across the Phylum Mollusca. Elevated cGMP and/or PKG is known to be involved in mollusc nerve regulation (Sung et al, 2004;Gomez and Nasi, 2005), as well as in other mollusc tissues (Higgins and Greenberg, 1974;Gainey and Greenberg, 2003). In vitro studies have linked PKG with the regulation of several enzymes of carbohydrate metabolism in estivating O. lactea (Brooks and Storey, 1997).…”