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The Journal of Neuroscience, March 17, 2004, 24(11):2623-2632; doi:10.1523/JNEUROSCI.5302-03.2004

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Cellular/Molecular
An Outer Segment Localization Signal at the C Terminus of the Photoreceptor-Specific Retinol Dehydrogenase

Wenqin Luo,¹ Nicholas Marsh-Armstrong,^1,2 Amir Rattner,³ and Jeremy Nathans^1,3,4

¹Department of Neuroscience, ²Kennedy Krieger Institute, ³Department of Molecular Biology and Genetics, and ⁴Department of Ophthalmology, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205

Photoreceptor retinol dehydrogenase (prRDH) is a membrane-associated cytosolic protein that localizes to the outer segments (OS) of rods and cones. Here, we demonstrate that the C-terminal 16 amino acids of prRDH confer membrane association as well as cone and rod OS targeting on a linked green fluorescent protein. Membrane association in transfected 293 cells and in transgenic Xenopus photoreceptors is mediated by fatty acylation at one or more evolutionarily conserved cysteines within the prRDH C-terminal tail. In bovine OS, native prRDH is similarly acylated, and hydrolysis of this linkage releases the protein from the membrane. Efficient OS localization requires both membrane association and the prRDH sequence... (V/I)XPX at the extreme C terminus, which closely resembles the C-terminal sequence that targets opsin/rhodopsin to the OS. Taken together, these data imply that the C-terminal... (V/I)XPX sequence is a general OS localization signal that can function in the context of both integral and peripheral membrane proteins. This strategy for OS localization resembles those used for protein localization to mitochondria, peroxisomes, endosomes, and endoplasmic reticulum; in each case, a short N- or C-terminal sequence is shared among structurally diverse proteins that are targeted to the same subcellular destination.

Key words: outer segment; protein sorting; photoreceptor; palmitoylation; retinol dehydrogenase; inner segment; transgenic Xenopus

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Received Dec 1, 2003; revised January 23, 2004; accepted January 27, 2004.

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