Transducin activation state controls its light-dependent translocation in rod photoreceptors

Light-dependent redistribution of transducin between the rod outer segments ( OS) and other photoreceptor compartments including the inner segments (IS) and synaptic terminals (ST) is recognized as a critical contributing factor to light and dark adaptation. The mechanisms of light-induced transducin translocation to the IS/ST and its return to the OS during dark adaptation are not well understood. We have probed these mechanisms by examining light-dependent localizations of the transducin-alpha subunit (Gt alpha) in mice lacking the photoreceptor GAP-protein RGS9, or expressing the GTPase-deficient mutant Gt alpha Q200L. An illumination threshold for the Gt alpha movement out of the OS is lower in the RGS9 knockout mice, indicating that the fast inactivation of transducin in the wild-type mice limits its translocation to the IS/ST. Transgenic Gt alpha Q200L mice have significantly diminished levels of proteins involved in cGMP metabolism in rods, most notably the PDE6 catalytic subunits, and severely reduced sensitivity to light. Similarly to the native Gt alpha, the Gt alpha Q200L mutant is localized to the IS/ST compartment in light-adapted transgenic mice. However, the return of Gt alpha Q200L to the OS during dark adaptation is markedly slower than normal. Thus, the light-dependent translocations of transducin are controlled by the GTP-hydrolysis on Gt alpha, and apparently, do not require Gt alpha interaction with RGS9 and PDE6.