Retinal photoreceptors – cones and rods – are able to undergo light adaptation over a wide range of illumination levels due to a complex of regulatory mechanisms. Among these, the best studied are calcium feedback circuits, which can explain about 50% of the actual regulation of light sensitivity. There are other regulatory mechanisms also able to adjust photoreceptor light responses depending on the illumination level, in particular regulation of the phototransduction cascade through the diurnal rhythm. During the dark phase of the diurnal cycle, cAMP levels in photoreceptors increase and rod sensitivity increases, which can be regarded as an adaptive action. In the case of cones, which operate at high illumination levels and make virtually no contribution to vision in twilight conditions, the increase in sensitivity in the dark phase may not have adaptive value. We report here our studies of how changes in [cAMP]in affect the operation of the phototransduction cascade in carp cones. Increases in [cAMP]in were obtained by incubating cells with the adenylate cyclase activator forskolin. Forskolin was found to slow both phases – the rise phase and the descending phase – of the light response in cones. As a result, cones, in contrast to rods, did not respond to forskolin with increases in light sensitivity but showed an almost two-fold reduction in the dark current. Thus, the reaction of the cone phototransduction cascade to increases in [cAMP]in was significantly different from the reaction in rods. This effect of [cAMP]in in cones may also have adaptive value – not in the form of increased sensitivity but as a reduction in the metabolic load on cells not functioning in the dark phase.
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R. S. Molday and O. L. Moritz, “Photoreceptors at a glance,” J. Cell Sci., 128, No. 22, 4039–4045 (2015).
C. K. Chen, “The vertebrate phototransduction cascade: amplification and termination mechanisms,” Rev. Physiol. Biochem. Pharmacol., 154, 101–121 (2005).
E. N. Pugh, Jr. and T. D. Lamb, “Phototransduction in vertebrate rods and cones: Molecular mechanisms of amplification, recovery and adaptation,” in: Handbook of Biological Physics (2000), Vol. 3, Chap. 5, pp. 183–255.
V. Y. Arshavsky and M. E. Burns, “Photoreceptor signaling: Supporting vision across a wide range of light intensities,” J. Biol. Chem., 287, No. 3, 1620–1626 (2012).
F. Vinberg and V. J. Kefalov, “Investigating the Ca2+-dependent and Ca2+-independent mechanisms for mammalian cone light adaptation,” Sci. Rep., 8, No. 1, 15864 (2018).
T. D. Lamb and D. M. Hunt, “Evolution of the calcium feedback steps of vertebrate phototransduction,” Open Biol., 8, No. 9, 180119 (2018).
P. P. Schnetkamp, A. H. Jalloul, G. Liu, and R. T. Szerencsei, “The SLC24 family of K+-dependent Na+–Ca2+ exchangers: structure-function relationships,” Curr. Top. Membr., 73, 263–287 (2014).
L. A. Astakhova, M. L. Firsov, and V. I. Govardovskii, “Kinetics of turn-offs of frog rod phototransduction cascade,” J. Gen. Physiol., 132, No. 5, 587–604 (2008).
M. Sokolov, A. L. Lyubarsky, K. J. Strissel, et al., “Massive lightdriven translocation of transducin between the two major compartments of rod cells: a novel mechanism of light adaptation,” Neuron, 34, No. 1, 95–106 (2002).
J. J. Peterson, B. M. Tam, O. L. Moritz, et al., “Arrestin migrates in photoreceptors in response to light: a study of arrestin localization using an arrestin-GFP fusion protein in transgenic frogs,” Exp. Eye Res., 76, No. 5, 553–563 (2003).
I. Nir, R. Haque, and P. M. Iuvone, “Regulation of cAMP by light and dopamine receptors is dysfunctional in photoreceptors of dystro phic retinal degeneration slow(rds) mice,” Exp. Eye Res., 73, No. 2, 265–272 (2001).
S. S. Chaurasia, R. Haque, N. Pozdeyev, et al., “Temporal coupling of cyclic AMP and Ca/calmodulin-stimulated adenylyl cyclase to the circadian clock in chick retinal photoreceptor cells,” J. Neurochem., 99, No. 4, 1142–1150 (2006).
Tosini, G., N. Pozdeyev, K. Sakamoto, and P. M. Iuvone, “The circadian clock system in the mammalian retina,” Bioessays, 30, No. 7, 624–633 (2008).
L. A. Astakhova, E. V. Samoiliuk, V. I. Govardovskii, and M. L. Firsov, “cAMP controls rod photoreceptor sensitivity via multiple targets in the phototransduction cascade,” J. Gen. Physiol., 140, No. 4, 421–433 (2012).
L. A. Astakhova, S. V. Kapitskii, V. I. Govardovskii, and M. L. Firsov, “cAMP as a phototransduction cascade regulator,” Ros. Fiziol. Zh., 98, No. 11, 1273–1285 (2012)
L. A. Astakhova, D. A. Nikolaeva, T. V. Fedotkina, et al., “Elevated cAMP improves signal-to-noise ratio in amphibian rod photoreceptors,” J. Gen. Physiol., 149, No. 7, 689–701 (2017).
D. A. Baylor, G. Matthews, and K. W. Yau, “Two components of electrical dark noise in toad retinal rod outer segments,” J. Physiol., 309, 591–621 (1980).
F. Rieke and D. A. Baylor, “Molecular origin of continuous dark noise in rod photoreceptors,” Biophys. J., 71, No. 5, 2553–2572 (1996).
P. Witkovsky, “Dopamine and retinal function,” Doc. Ophthalmol., 108, No. 1, 17–40 (2004).
E. Popova, “Role of dopamine in distal retina,” J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol., 200, No. 5, 333–358 (2014).
D. A. Nikolaeva, L. A. Astakhova, and M. L. Firsov, “The effects of dopamine and dopamine receptor agonists on the phototransduction cascade of frog rods,” Mol. Vis., 25, 400–414 (2019).
N. T. Ingram, A. P. Sampath, and G. L. Fain, “Why are rods more sensitive than cones?” J. Physiol., 594, No. 19, 5415–5426 (2016).
X. M. Abalo, D. Lagman, G. Heras, et al., “Circadian regulation of phosphodiesterase 6 genes in zebrafish differs between cones and rods: Implications for photopic and scotopic vision,” Vision Res., 166, 43–51 (2020).
D. A. Baylor, T. D. Lamb, and K. W. Yau, “The membrane current of single rod outer segments,” J. Physiol., 288, 589–611 (1979).
T. D. Lamb and E. N. Pugh, Jr., “A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors,” J. Physiol., 449, 719–758 (1992).
L. Astakhova, M. Firsov, and V. Govardovskii, “Activation and quenching of the phototransduction cascade in retinal cones as inferred from electrophysiology and mathematical modeling,” Mol. Vis., 21, 244–263 (2015).
J. Z. Nowak, B. Sek, and E. Zurawska, “Activation of D2 dopamine receptors in hen retina decreases forskolin-stimulated cyclic AMP accumulation and serotonin N-acetyltransferase (NAT) activity,” Neurochem. Int., 16, No. 1, 73–80 (1990).
K. W. Koch and L. Stryer, “Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions,” Nature, 334, 64–66 (1988).
A. M. Dizhoor, D. G. Lowe, E. V. Olshevskaya, et al., “The human photoreceptor membrane guanylyl cyclase, RetGC, is present in outer segments and is regulated by calcium and a soluble activator,” Neuron, 12, No. 6, 1345–1352 (1994).
Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 106, No. 4, pp. 448–461, April, 2020.
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Sitnikova, V.S., Astakhova, L.A. & Firsov, M.L. cAMP-Dependent Regulation of the Phototransduction Cascade in Cones. Neurosci Behav Physi 51, 108–115 (2021). https://doi.org/10.1007/s11055-020-01045-3
- circadian rhythm