Massive Light-Driven Translocation of Transducin between the Two Major Compartments of Rod Cells

Abstract

We report a new cellular mechanism of rod photoreceptor adaptation in vivo, which is triggered by daylight levels of illumination. The mechanism involves a massive light-dependent translocation of the photoreceptor-specific G protein, transducin, between the functional compartments of rods. To characterize the mechanism, we developed a novel technique that combines serial tangential cryodissection of the rat retina with Western blot analysis of protein distribution in the sections. Up to 90% of transducin translocates from rod outer segments to other cellular compartments on the time scale of tens of minutes. The reduction in the transducin content of the rod outer segments is accompanied by a corresponding reduction in the amplification of the rod photoresponse, allowing rods to operate in illumination up to 10-fold higher than would otherwise be possible.

Light-Dependent Translocation of Arrestin in the Absence of Rhodopsin Phosphorylation and Transducin Signaling

“…Immunoreactivity of the transducin ␣ and ␤ subunits shifts in the opposite direction in response to light (Philp et al, 1987;Whelan and McGinnis, 1988;McGinnis et al, 1992). Recently, Sokolov et al (2002) confirmed the physiological movement of transducin by combining serial tangential cryosectioning of the retina with Western blot analysis and demonstrated that this movement extends the range of light intensities in which the rods can operate. The light-driven redistribution of arrestin was recently reexamined by Peterson et al (2003), who expressed an arrestin-green fluorescent protein (GFP) fusion protein in transgenic Xenopus and observed light-dependent translocation of GFP fluorescence to rod outer segments.…”

“…One mechanism that may contribute to regulation of the performance of the rod cell is the light-driven redistribution of certain signal-transducing proteins within the compartments of the rod cell (Sokolov et al, 2002). Both transducin and arrestin immunoreactivity redistribute in rods in response to light (Broekhuyse et al, 1985(Broekhuyse et al, , 1987Philp et al, 1987;Mangini and Pepperberg, 1988;Whelan and McGinnis, 1988).…”

Function of phosducin-like proteins in G protein signaling and chaperone-assisted protein folding

“…This idea is based on the observations that in vivo phosphorylation of S54 blocks the binding of Pdc to G t βγ and that the rate of S54 phosphorylation and the rate of translocation to the outer segment are similar, with half-lives in the 90 min. range [49,56]. Moreover, it has been recently reported that S54 phosphorylation is localized in the ellipsoid region of the inner segment near the thin cilium that connects the inner and outer segments, while S73 phosphorylation is found throughout the rod cell [57].…”

Why photoreceptors die (and why they don't)

“…Transducin in the dark is mostly concentrated in the outer segment of the rod and moves in the light to the inner segment. (76)(77)(78)(79)(80) Arrestin in the dark is mostly in the inner segment and moves to the outer segment. (77,78,80 -82) These translocations are usually asserted to contribute to the change in sensitivity during adaptation (but see Ref.…”

“…83). It is now clear, however, that the movements only occur after exposure to background illumination so bright that it exceeds the normal range of vision in a rod, (79) and their contribution to adaptation is small, causing at most a modest delay in the recovery of sensitivity after bright light exposure.…”