Rhodopsin kinase and arrestin binding control the decay of photoactivated rhodopsin and dark adaptation of mouse rods

Abstract

G-protein receptor kinase and arrestin 1 are required for inactivation of photoactivated vertebrate rhodopsin. Frederiksen et al. show that they additionally regulate the subsequent decay of inactive rhodopsin into opsin and all-trans retinal and therefore dark adaptation.

Convergent selection pressures drive the evolution of rhodopsin kinetics at high altitudes via nonparallel mechanisms

“…), where corresponding kinetic rates are strongly associated in vivo with the recovery rate of dark adaptation (Frederiksen et al. ), as well as overall rod photosensitivity (Imai et al. ; Yue et al.…”

“…Visual performance in organisms is reliant not only on wavelength detection, but also on the neural signaling of rod photoreceptors, which is initiated by rhodopsin-mediated phototransduction. This proceeds through a complex series of inactive-and active-state rhodopsin conformations that exist in temperature-and pH-dependent photochemical equilibria (Schafer et al 2016;Van Eps et al 2017), where corresponding kinetic rates are strongly associated in vivo with the recovery rate of dark adaptation (Frederiksen et al 2016), as well as overall rod photosensitivity (Imai et al 2007;Yue et al 2017). In particular, the spontaneous thermal decay rate of the inactive dark-state conformation and the decay rate of the light-activated MII conformation are two distinct nonspectral functional properties considered evolutionary innovations to dim light (Aho et al 1988;Imai et al 1997;Lamb et al 2016;Yue et al 2017).…”

“…It is precisely the conformational stability of the rhodopsin dark and active states, which directly governs the photochemistry and kinetic rates of these physiologically important rod equilibria described above (Schafer et al 2016;Van Eps et al 2017). It is therefore highly likely that the conformational stability of rhodopsin indirectly modulates these properties of rod photoreceptors strongly associated with animal visual performance (Aho et al 1988;Kefalov et al 2003;Imai et al 2007;Frederiksen et al 2016;Yue et al 2017). As ectotherms restricted to cold high altitude environments Ma et al 2016), Andean and Himalayan catfish specialists are likely to experience slowed biochemical processes relative to closely related taxa at lowland temperatures (Siddiqui and Cavicchioli 2006;Fields et al 2015;Åqvist 2017).…”

“…Rhodopsin detects photons through isomerization of its chromophore causing conformational changes that result in a series of equilibria among active-state rhodopsin intermediates, of which the metarhodopsin II (MII) form is thought to activate the second messenger G protein transducin, ultimately resulting in a neural signal (Ebrey and Koutalos 2001). Recently, it was demonstrated that the conformational stability of rhodopsin directly governs the kinetic rates of these rod equilibria (Schafer et al 2016;Van Eps et al 2017), which are temperature-sensitive and set a physiological limit on visual performance, as demonstrated in vivo (Aho et al 1988;Kefalov et al 2003;Imai et al 2007;Frederiksen et al 2016;Yue et al 2017). The temperature dependence and physiological importance of these rod equilibria suggests that natural selection may alter rhodopsin stability as a means to modulate visual performance in response to natural temperature variation.…”

Phosphorylation at Serine 21 in G protein‐coupled receptor kinase 1 (GRK1) is required for normal kinetics of dark adaption in rod but not cone photoreceptors

“…Dark adaptation is typically defined as the ability to regain photosensitivity after bright light stimulation, which, in the case of rods, is very slow, requiring 1‐3 hours . In both rods and cones, dark adaptation requires regeneration of the bleached visual pigment, a process that involves the dephosphorylation of the opsins, the release of all ‐trans ‐retinal from the pigment, and the binding of fresh 11‐ cis ‐retinal following its recycling . Recently, it has been shown that both rhodopsin and the M‐cone pigment are dephosphorylated by protein phosphatase 2A (PP2A), allowing them to reset to their ground state in a timely fashion and respond to another photon …”