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Trafficking of Membrane-Associated Proteins to Cone Photoreceptor Outer Segments Requires the Chromophore 11-Cis-Retinal

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Trafficking of Membrane-Associated Proteins to Cone Photoreceptor Outer Segments Requires the Chromophore 11-Cis-Retinal 4008 • The Journal of Neuroscience, April 9, 2008 • 28(15):4008–4014 Neurobiology of Disease Trafficking of Membrane-Associated Proteins to Cone Photoreceptor Outer Segments Requires the Chromophore 11-cis-Retinal Houbin Zhang,1 Jie Fan,3 Sha Li,1 Sukanya Karan,5 Baerbel Rohrer,3 Krzysztof Palczewski,4 Jeanne M. Frederick,1 Rosalie K. Crouch,3 and Wolfgang Baehr1,2,5 Departments of 1Ophthalmology and 2Neurobiology and Anatomy, University of Utah Health Science Center, Salt Lake City, Utah 84132, 3Department of Ophthalmology, Medical University of South Carolina, Charleston, South Carolina 29425, 4Department of Pharmacology, Case Western Reserve University, Cleveland, Ohio 44106, and 5Department of Biology, University of Utah, Salt Lake City, Utah 84112 Lecithin retinol acyl transferase (LRAT) and retinal pigment epithelium protein 65 (RPE65) are key enzymes of the retinoid cycle. In Lrat Ϫ/Ϫ and Rpe65 Ϫ/Ϫ mice, models of human Leber congenital amaurosis, the retinoid cycle is disrupted and 11-cis-retinal, the chromophore of visual pigments, is not produced. The Lrat Ϫ/Ϫ and Rpe65 Ϫ/Ϫ retina phenotype presents with rapid sectorial cone degeneration, and the visual pigments, S-opsin and M/L-opsin, fail to traffic to cone outer segments appropriately. In contrast, rod opsin trafficsnormallyinmutantrods.Concomitantly,guanylatecyclase1,coneT␣-subunit,conephosphodiesterase6␣Ј(PDE6␣Ј),andGRK1 (G-protein-coupled receptor kinase 1; opsin kinase) are not transported to Lrat Ϫ/Ϫ and Rpe65 Ϫ/Ϫ cone outer segments. Aberrant localization of these membrane-associated proteins was evident at postnatal day 15, before the onset of ventral and central cone degen- eration. Protein levels of cone T␣ and cone PDE6␣Ј were reduced, whereas their transcript levels were unchanged, suggesting posttrans- lational degradation. In an Rpe65 Ϫ/ϪRho Ϫ/Ϫ double knock-out model, trafficking of cone pigments and membrane-associated cone phototransduction polypeptides to the outer segments proceeded normally after 11-cis-retinal administration. These results suggest that ventral and central cone opsins must be regenerated with 11-cis-retinal to permit transport to the outer segments. Furthermore, the presence of 11-cis-retinal is essential for proper transport of several membrane-associated cone phototransduction polypeptides in these cones. Key words: cone visual pigments; LRAT (lecithin retinol acyl transferase); RPE65; retinoid isomerase; membrane protein trafficking; Leber congenital amaurosis Introduction 11-cis-retinal in the retinoid cycle is essential for maintaining Photon absorption by photosensitive visual pigments in rod normal visual function (Wald, 1968). After photobleaching, and cone photoreceptors initiates signal transduction and vi- all-trans-retinal separates from rhodopsin and cone opsins sion (Palczewski, 2006). Visual pigments are G-protein- and is reduced to all-trans-retinol (Maeda et al., 2007). All- coupled receptors using as their ligand 11-cis-retinal, which trans-retinol, in turn, is exported to the retinal pigment epi- isomerizes to the all-trans form with light. Regeneration of thelium (RPE), where it is converted into retinyl esters by lecithin retinol acyltransferase (LRAT). All-trans retinyl esters are the substrate for RPE protein 65 (RPE65), recently identi- Received Jan. 23, 2008; revised March 7, 2008; accepted March 12, 2008. fied as the retinoid isomerase that generates 11-cis-retinol (Jin ThisworkwassupportedbyNationalInstitutesofHealth(NIH)GrantsEY04939(R.K.C.),EY13520(B.R.),EY09339 et al., 2005; Moiseyev et al., 2005; Redmond et al., 2005). After (K.P.),EY14793(MedicalUniversityofSouthCarolinavisioncore),EY08123(W.B.),EY014800-039003(NationalEye oxidation to 11-cis-retinal, the chromophore is exported back Institute core grant), by a grant from the Foundation Fighting Blindness (K.P.), a Foundation Fighting Blindness center grant to the University of Utah, and unrestricted grants to the Departments of Ophthalmology at the Medical to the photoreceptors for the regeneration of functional University of South Carolina and the University of Utah from Research to Prevent Blindness (RPB) (New York, NY). pigments. R.K.C. is an RPB Senior Scientific Investigator, and B.R. is an RPB Olga Keith Weiss Scholar. The animal studies were LRAT and RPE65 knock-out mice have been shown to lack conductedinafacilityconstructedwithsupportfromtheResearchFacilitiesProgramandGrantCO6RR015455from 11-cis-retinal for visual pigment regeneration. In the Lrat Ϫ/Ϫ the NIH National Center for Research Resources. We thank Drs. Ching-Kang Chen (Virginia Commonwealth Univer- sity,Richmond,VA)foranti-rodtransducin-␣antibody,CherylCraft(UniversityofSouthernCalifornia,LosAngeles, mouse, only trace amounts of all-trans-retinyl esters were de- CA) for anti-mouse cone arrestin antibody, Tiansen Li (Harvard University, Cambridge, MA) for anti-cone PDE6␣Ј tected, consistent with blockage of the retinoid cycle at the ester- Ϫ Ϫ antibody, Stefan Heller (Stanford University, Palo Alto, CA) for anti-R9AP antibody, and Nils Brose (Max Planck ification step (Batten et al., 2004). In the Rpe65 / mouse, retinyl Institute for Experimental Medicine, Goettingen, Germany) for anti-complexin III antibody. esters accumulate, and 11-cis-retinal cannot be produced (Red- Correspondence should be addressed to Wolfgang Baehr, John A. Moran Eye Center, University of Utah Health mond et al., 1998b). Administration of exogenous 9- or 11-cis- Science Center, Salt Lake City, UT 84132. E-mail: [email protected]. Ϫ/Ϫ DOI:10.1523/JNEUROSCI.0317-08.2008 retinal can significantly improve rod function in Rpe65 mice, Copyright © 2008 Society for Neuroscience 0270-6474/08/284008-07$15.00/0 even as old as 18 months (Van Hooser et al., 2002; Rohrer et al., Zhang et al. • 11-cis-Retinal and Membrane Protein Trafficking in Cones J. Neurosci., April 9, 2008 • 28(15):4008–4014 • 4009 2003). Cones and rods are supported by the retinoid cycle in a ware version 4.5; Diagnostic Instruments, Sterling Heights, MI). Cones similar, but not identical, manner. In primates, RPE65 and its were counted from five fields (far dorsal, dorsal, central, ventral, and far substrate all-trans-retinyl esters are localized at highest concen- ventral) per flat-mounted retina and averaged for six mice of each geno- 2 Ϯ trations in the RPE cells that cover the foveal region of the retina type. Data are expressed as the mean number of cones/mm SEM. For (Jacobson et al., 2007). The possibility has been raised that addi- overall changes in cell numbers between the two retinoid cycle mutants and wild-type (WT) retinas, data were analyzed by repeated-measures tional processes may exist that generate 11-cis-retinal for cones ANOVA followed by Dunnett’s post hoc test ( p Ͻ 0.05); for analysis of supplementing the major RPE65-dependent pathway (Mata et regional differences in cone cell counts, one-way ANOVA followed by al., 2005; Muniz et al., 2007; Schonthaler et al., 2007). Residual pairwise Tukey’s post hoc test was used ( p Ͻ 0.05). function of RPE65-Leber congenital amaurosis (LCA) cones and Immunolocalization by confocal microscopy. Age-matched mouse eyes prolonged cone photoreceptor survival in human patients sup- were immersion fixed for 2 h using freshly prepared 4% paraformalde- port this speculation (Jacobson et al., 2007). hyde in 0.1 M phosphate buffer, pH 7.4, and cryoprotected. Eyes were Unlike rods, cone photoreceptors degenerate rapidly (Znoiko coembedded, frozen, and sectioned at 12 ␮m thickness before incuba- et al., 2005), and notably, cone opsins (both S-opsin and M/L- tions for immunocytochemistry as described by Bhosale et al. (2004) and ␮ opsin) (Ebrey and Koutalos, 2001) were found to mislocalize in Baehr et al. (2007). Affinity-purified primary antibodies (15–25 l) were the Rpe65 Ϫ/Ϫ cones and unable to traffic to the cone outer seg- applied to each group of two to four sections in a humidified, rotating chamber overnight at 4°C. Propidium iodide (1:3000 dilution; Invitro- ments (COSs) properly (Rohrer et al., 2005). Administration of gen) was added to the solution containing FITC-conjugated secondary 11-cis-retinal before onset of degeneration [postnatal day 10 antibody. The sections were viewed using a Zeiss LSM 510 inverted laser- (P10)] prevented cone opsin mistrafficking and slowed the rate of scanning confocal microscope with a 40ϫ 1.3 numerical aperture oil degeneration (Rohrer et al., 2005). Here, we explored the conse- objective lens and optical slit setting of Ͻ0.9 ␮m. Antibodies and dilu- Ϫ/Ϫ Ϫ/Ϫ quences of 11-cis-retinal absence in Rpe65 and Lrat mice tions used in this study were described previously (Baehr et al., 2007). on trafficking of integral and peripheral membrane-associated Immunoblotting. Wild-type and Lrat Ϫ/Ϫ retinas (one each) at age of proteins (PMPs) to cone outer segments. We show that cone P15–P16 were homogenized by sonication. Equal amounts (1/15 of total opsins mislocalized to the inner segment and synaptic pedicle at amount) of the proteins from each retina were loaded on a 12.5% SDS- P15, and polypeptides of the cone phototransduction cascade PAGE gel. After separation, the proteins were transferred to a nitrocellu- [including guanylate cyclase 1 (GC1) and G-protein-coupled re- lose filter and probed with primary antibodies as described previously ceptor kinase 1 (GRK1)] failed to transport to the cone outer (Zhang et al., 2007). The signals were visualized by ECL (NEN/Perkin- Elmer, Waltham MA). segments in both models. Early and repeated administration of Ϫ/Ϫ Ϫ/Ϫ Quantitative reverse transcription-PCR. Semiquantitative real-time re- exogenous 11-cis-retinal to Rpe65 Rho double knock-out verse transcription (RT)-PCR was performed using total RNA from WT, pups prevented these mislocalizations. These results are consis- Lrat Ϫ/Ϫ, and Rpe65 Ϫ/Ϫ retinas. Total RNAs were extracted from P15 tent with a key role of 11-cis-retinal bound to cone opsins for retina, and real-time RT-PCR was performed with 25 ng of RNA as retinal protein sorting, transport, and targeting and, ultimately, described previously (Baehr et al., 2007). Primers [Gnat2 forward, 5Ј- cell survival.
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