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

Journal of Neuroscience

Volumn 24, Issue 11, 2004, Pages 2623-2632

  Luo, Wenqin ^a   Marsh Armstrong, Nicholas ^a   Rattner, Amir ^a   Nathans, Jeremy ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Inner segment; Outer segment; Palmitoylation; Photoreceptor; Protein sorting; Retinol dehydrogenase; Transgenic Xenopus

Indexed keywords

CYSTEINE; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; OPSIN; RETINOL DEHYDROGENASE; RHODOPSIN;

ACYLATION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; ENDOSOME; ENZYME LOCALIZATION; ENZYME MODIFICATION; ENZYME RELEASE; ENZYME SPECIFICITY; ENZYME STRUCTURE; GENETIC CONSERVATION; HUMAN; HUMAN CELL; HYDROLYSIS; MEMBRANE BINDING; NONHUMAN; PALMITOYLATION; PEROXISOME; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN TARGETING; RETINA CONE; RETINA ROD; TRANSGENE; XENOPUS;

ALCOHOL OXIDOREDUCTASES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CATTLE; CELL LINE; CONSERVED SEQUENCE; GREEN FLUORESCENT PROTEINS; HUMANS; LARVA; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; PALMITIC ACID; PHOTORECEPTORS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; ROD OUTER SEGMENTS; TRANSFECTION; XENOPUS LAEVIS; ZEBRAFISH;

EID: 1642377058     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5302-03.2004     Document Type: Article

References (56)

1. Anant JS, Ong OC, Xie H, Clarke S, O'Brien PJ, Fung BK-K (1992) In vivo differential prenylation of retinal cyclic GMP phosphodiesterase catalytic subunits. J Biol Chem 267:687-690.
2. Blaner WS, Churchich JE (1980) The membrane bound retinol dehydrogenase from bovine rod outer segments. Biochem Biophys Res Commun 94:820-826.
3. Brann MR, Cohen LV (1987) Diurnal expression of transducin mRNA and translocation of transducin in rods of rat retina. Science 235:585-587.
4. Broekhuyse RM, Tolhuizen EF, Janssen AP, Winkens HJ (1985) Light induced shift and binding of S-antigen in retinal rods. Curr Eye Res 4:613-618.
5. Concepcion F, Mendez A, Chen J (2002) The carboxyl-terminal domain is essential for rhodopsin transport in rod photoreceptors. Vis Res 42:417-426.
6. Dryja TP, McGee TL, Hahn LB, Cowley GS, Olsson JE, Reichel E, Sandberg MA, Berson EL (1990) Mutations within the rhodopsin gene in patients with autosomal dominant retinitis pigmentosa. N Engl J Med 323:1302-1307.
7. Dryja TP, Hahn LB, Cowley GS, McGee TL, Berson EL (1991) Mutation spectrum of the rhodopsin gene among patients with autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci USA 88:9370-9374.
8. El-Husseini Ael-D, Craven SE, Brock SC, Bredt DS (2001) Polarized targeting of peripheral membrane proteins in neurons. J Biol Chem 276:44984-44992.
9. El-Husseini Ael-D, Bredt DS (2002) Protein palmitoylation: a regulator of neuronal development and function. Nat Rev Neurosci 3:791-802.
10. Gao J, Cheon K, Nusinowitz S, Liu Q, Bei D, Atkins K, Azimi A, Daiger SP, Farber DB, Heckenlively JR, Pierce EA, Sullivan LS, Zuo J (2002) Progressive photoreceptor degeneration, outer segment dysplasia, and rhodopsin mislocalization in mice with targeted disruption of the retinitis pigmentosa-1 (Rp1) gene. Proc Natl Acad Sci USA 99:5698-5703.
11. Gonzalo S, Linder ME (1998) SNAP-25 palmitoylation and plasma membrane targeting require a functional secretory pathway. Mol Biol Cell 9:585-597.
12. Heilker R, Spiess M, Crottet P (1999) Recognition of sorting signals by clathrin adaptors. BioEssays 21:558-567.
13. Ishiguro S, Suzuki Y, Tamai M, Mizuno K (1991) Purification of retinol dehydrogenase from bovine retinal rod outer segments. J Biol Chem 266:15520-15524.
14. Jackson CS, Magee AI (2002) Analysis of protein acylation. In: Current protocols in protein science, Vol 2 (Coligan JE, Dunn BM, Ploegh HL, Speicher DW, Wingfield PT, eds), pp 14.2.1-14.2.9. New York: Wiley.
15. Knowles A, Dartnall HJA (1977) The photobiology of vision. New York: Academic.
16. Knox BE, Schlueter C, Sanger BM, Green CB, Besharse JC (1998) Transgene expression in Xenopus rods. FEBS Lett 423:117-121.
17. Kroll KK, Amaya E (1996) Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 122:3173-3183.
18. Li T, Snyder WK, Olsson JE, Dryja TP (1996) Transgenic mice carrying the dominant rhodopsin mutation P347S: evidence for defective vectorial transport of rhodopsin to the outer segments. Proc Natl Acad Sci USA 93:14176-14181.
19. Linder ME, Kleuss C, Mumby SM (1995) Palmitoylation of G-protein α subunits. Methods Enzymol 250:314-330.
20. Lingappa VR, Blobel G (1980) Early events in the biosynthesis of secretory and membrane proteins: the signal hypothesis. Recent Prog Horm Res 36:451-475.
21. Lion F, Rotmans JP, Daemen FJM, Bonting SL (1975) Stereospecificity of ocular retinol dehydrogenases and the visual cycle. Biochim Biophys Acta 384:283-292.
22. Liu Q, Zhou J, Daiger SP, Farber DB, Heckenlively JR, Smith JE, Sullivan LS, Zuo J, Milam AH, Pierce EA (2002) Identification and subcellular localization of the RP1 protein in human and mouse photoreceptors. Invest Ophthalmol Vis Sci 43:22-32.
23. Liu Q, Lyubarsky A, Skalet JH, Pugh Jr EN, Pierce EA (2003) RP1 is required for the correct stacking of outer segment discs. Invest Ophthalmol Vis Sci 44:4171-4183.
24. Macke JP, Hennessey JC, Nathans J (1995) Rhodopsin mutation proline347-to-alanine in a family with autosomal dominant retinitis pigmentosa indicates an important role for proline at position 347. Hum Mol Genet 4:775-776.
25. McGinnis JF, Matsumoto B, Whelan JP, Cao W (2002) Cytoskeleton participation in subcellular trafficking of signal transduction proteins in rod photoreceptor cells. J Neurosci Res 67:290-297.
26. Mendez A, Lem J, Simon M, Chen J (2003) Light-dependent translocation of arrestin in the absence of rhodopsin phosphorylation and transducin signaling. J Neurosci 23:3124-3129.
27. Molday RS (1998) Photoreceptor membrane proteins, phototransduction, and retinal degenerative diseases. Invest Ophthalmol Vis Sci 39:2491-2513.
28. Moritz OL, Tam BM, Knox BE, Papermaster DS (1999) Fluorescent photoreceptors of transgenic Xenopus laevis imaged in vivo by two microscopy techniques. Invest Ophthalmol Vis Sci 40:3276-3280.
29. Moritz OL, Tam BM, Papermaster DS, Nakayama T (2001) A functional rhodopsin-green fluorescent protein fusion protein localizes correctly in transgenic Xenopus laevis retinal rods and is expressed in a time-dependent pattern. J Biol Chem 276:28242-28251.
30. Nicotra C, Livrea MA (1982) Retinol dehydrogenase from bovine retinal rod outer segments. Kinetic mechanism of the solubilized enzyme. J Biol Chem 257:11836-11841.
31. Palczewski K, Jager S, Buczylko J, Crouch RK, Bredberg DL, Hofmann KP, Asson-Batres MA, Saari JC (1994) Rod outer segment retinol dehydrogenase: substrate specificity and role in phototransduction. Biochemistry 33:13741-13750.
32. Papermaster DS (1982) Preparation of retinal rod outer segments. Methods Enzymol 81:48-52.
33. Pazour GJ, Baker SA, Deane JA, Cole DG, Dickert BL, Rosenbaum JL, Witman GB, Besharse JC (2002) The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J Cell Biol 157:103-113.
34. Peterson JJ, Tam BM, Moritz OL, Shelamer CL, Dugger DR, McDowell JH, Hargrave PA, Papermaster DS, Smith WC (2003) Arrestin migrates in photoreceptors in response to light: a study of arrestin localization using an arrestin-GFP fusion protein in transgenic frogs. Exp Eye Res 76:553-563.
35. Philp NJ, Chang W, Long K (1987) Light-stimulated protein movement in rod photoreceptor cells of the rat retina. FEBS Lett 225:127-132.
36. Pugh Jr EN, Lamb TD (1993) Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta 1141:111-149.
37. Qin N, Pittler SJ, Baehr W (1992) In vitro isoprenylation and membrane association of mouse rod photoreceptor cGMP phosphodiesterase alpha and beta subunits expressed in bacteria. J Biol Chem 267:8458-8463.
38. Rattner A, Smallwood PM, Nathans J (2000) Identification and characterization of all-trans-retinol dehydrogenase from photoreceptor outer segments, the visual cycle enzyme that reduces all-trans-retinal to all-transretinol. J Biol Chem 275:11034-11043.
39. Reiss Y, Goldstein JL, Seabra MC, Casey PJ, Brown MS (1990) Inhibition of purified p21ras farnesyl:protein transferase by Cys-AAX tetrapeptides. Cell 62:81-88.
40. Resh MD (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1451:1-16.
41. Rosas DJ, Roman AJ, Weissbrod P, Macke JP, Nathans J (1994) Autosomal dominant retinitis pigmentosa in a large family: a clinical and molecular genetic study. Invest Ophthalmol Vis Sci 35:3134-3144.
42. Sacksteder KA, Gould SJ (2000) The genetics of peroxisome biogenesis. Annu Rev Genet 34:623-652.
43. Sawicki MW, Erman M, Puranen T, Vihko P, Ghosh zens(1999) Structure of the ternary complex of human 17beta-hydroxysteroid dehydrogenase type 1 with 3-hydroxyestra-1,3,5,7-tetraen-17-one (equilin) and NADP+. Proc Natl Acad Sci USA 96:840-845.
44. Slimane TA, Hoekstra D (2002) Sphingolipid trafficking and protein sorting in epithelial cells. FEBS Lett 529:54-59.
45. Sokolov M, Lyubarsky AL, Strissel KJ, Savchenko AB, Govardovskii VI, Pugh Jr EN, Arshavsky VY (2002) Massive light-driven translocation of transducin between the two major compartments of rod cells: a novel mechanism of light adaptation. Neuron 34:95-106.
46. Srinivasa SP, Bernstein LS, Blumer KJ, Linder ME (1998) Plasma membrane localization is required for RGS4 function in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 95:5584-5589.
47. Sung CH, Davenport CM, Hennessey JC, Maumenee IH, Jacobson SG, Heckenlively JR, Nowakowski R, Fishman G, Gouras P, Nathans J (1991) Rhodopsin mutations in autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci USA 88:6481-6485.
48. Sung CH, Makino C, Baylor D, Nathans J (1994) A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment. J Neurosci 14:5818-5833.
49. Tai AW, Chuang JZ, Bode C, Wolfrum U, Sung CH (1999) Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1. Cell 97:877-887.
50. Tam BM, Moritz OL, Hurd LB, Papermaster DS (2000) Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis. J Cell Biol 151:1369-1380.
51. Voos W, Martin H, Krimmer T, Pfanner N (1999) Mechanisms of protein translocation into mitochondria. Biochim Biophys Acta 1422:235-254.
52. Wald G, Hubbard R (1949) The reduction of retinene-1 to vitamin A-1 in vitro. J Gen Physiol 32:367-389.
53. Whelan JP, McGinnis JF (1988) Light-dependent subcellular movement of photoreceptor proteins. J Neurosci Res 20:263-270.
54. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385-419.
55. Young RW (1967) The renewal of photoreceptor cell outer segments. J Cell Biol 33:61-72.
56. Zhao Y, Hong DH, Pawlyk B, Yue G, Adamian M, Grynberg M, Godzik A, Li T (2003) The retinitis pigmentosa GTPase regulator (RPGR)-interacting protein: subserving RPGR function and participating in disk morphogenesis. Proc Natl Acad Sci USA 100:3965-3970.