Dark rearing rescues P23H rhodopsin-induced retinal degeneration in a transgenic Xenopus laevis model of retinitis pigmentosa: A chromophore-dependent mechanism characterized by production of N-terminally truncated mutant rhodopsin

Journal of Neuroscience

Volumn 27, Issue 34, 2007, Pages 9043-9053

  Tam, Beatrice M ^a   Moritz, Orson L ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

ER stress; Neuronal death; Photoreceptor; Protein misfolding; Rhodopsin; Signal transduction

Indexed keywords

RHODOPSIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATOPHORE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN FOLDING; RETINA DEGENERATION; XENOPUS LAEVIS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CATTLE; CELL LINE, TRANSFORMED; DARKNESS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HISTIDINE; HUMANS; MICE; MICROSCOPY, ELECTRON, SCANNING; MUTATION; PEPTIDE FRAGMENTS; PROLINE; RETINALDEHYDE; RETINITIS PIGMENTOSA; RHODOPSIN; RODS (RETINA); TRANSFECTION; XENOPUS LAEVIS;

EID: 34548169402     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2245-07.2007     Document Type: Article

References (36)

1. Adamus G, Zam ZS, Arendt A, Palczewski K, McDowell JH, Hargrave PA (1991) Anti-rhodopsin monoclonal antibodies of defined specificity: characterization and application. Vision Res 31:17-31.
2. Bass J, Turck C, Rouard M, Steiner DF (2000) Furin-mediated processing in the early secretory pathway: sequential cleavage and degradation of misfolded insulin receptors. Proc Natl Acad Sci USA 97:11905-11909.
3. Berson EL (1971) Light deprivation for early retinitis pigmentosa. A hypothesis. Arch Ophthalmol 85:521-529.
4. Berson EL (2000) Nutrition and retinal degenerations. Int Ophthalmol Clin 40:93-111.
5. Berson EL, Rosner B, Sandberg MA, Hayes KC, Nicholson BW, Weigel-DiFranco C, Willett W (1993a) A randomized trial of vitamin A and vitamin E supplementation for retinitis pigmentosa. Arch Ophthalmol 111:761-772.
6. Berson EL, Rosner B, Sandberg MA, Hayes KC, Nicholson BW, Weigel-DiFrano C, Willett W (1993b) Vitamin A supplementation for retinitis pigmentosa. Arch Ophthalmol 111:1456-1459.
7. Besharse JC, Hollyfield JG, Rayborn ME (1977) Turnover of rod photoreceptor outer segments. II. Membrane addition and loss in relationship to light. J Cell Biol 75:507-527.
8. Cideciyan AV, Hood DC, Huang Y, Banin E, Li ZY, Stone EM, Milam AH, Jacobson SG (1998) Disease sequence from mutant rhodopsin allele to rod and cone photoreceptor degeneration in man. Proc Natl Acad Sci USA 95:7103-7108.
9. Cideciyan AV, Jacobson SG, Aleman TS, Gu D, Pearce-Kelling SE, Sumaroka A, Acland GM, Aguirre GD (2005) In vivo dynamics of retinal injury and repair in the rhodopsin mutant dog model of human retinitis pigmentosa. Proc Natl Acad Sci USA 102:5233-5238.
10. Cohen GB, Yang T, Robinson PR, Oprian DD (1993) Constitutive activation of opsin: influence of charge at position 134 and size at position 296. Biochemistry 32:6111-6115.
11. Dryja TP, McGee TL, Reichel E, Hahn LB, Cowley GS, Yandell DW, Sandberg MA, Berson EL (1990) A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature 343:364-366.
12. Franke RR, Sakmar TP, Oprian DD, Khorana HG (1988) A single amino acid substitution in rhodopsin (lysine 248-leucine) prevents activation of transducin. J Biol Chem 263:2119-2122.
13. Galy A, Roux MJ, Sahel JA, Leveillard T, Giangrande A (2005) Rhodopsin maturation defects induce photoreceptor death by apoptosis: a fly model for Rhodopsin Pro23 His human retinitis pigmentosa. Hum Mol Genet 14:2547-2557.
14. Hicks D, Molday RS (1986) Differential immunogold-dextran labeling of bovine and frog rod and cone cells using monoclonal antibodies against bovine rhodopsin. Exp Eye Res 42:55-71.
15. Illing ME, Rajan RS, Bence NF, Kopito RR (2002) A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J Biol Chem 28:28.
16. Kaushal S, Khorana HG (1994) Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33:6121-6128.
17. Kroll KL, Amaya E (1996) Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 122:3173-3183.
18. Levitan A, Trebitsh T, Kiss V, Pereg Y, Dangoor I, Danon A (2005) Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum. Proc Natl Acad Sci USA 102:6225-6230.
19. Li QB, Guy CL (2001) Evidence for non-circadian light/dark-regulated expression of Hsp70s in spinach leaves. Plant Physiol 125:1633-1642.
20. Li ZY, Jacobson SG, Milam AH (1994) Autosomal dominant retinitis pigmentosa caused by the threonine-17-methionine rhodopsin mutation: retinal histopathology and immunocytochemistry. Exp Eye Res 58:397-408.
21. Loo TW, Clarke DM (1998) Quality control by proteases in the endoplasmic reticulum. Removal of a protease-sensitive site enhances expression of human P-glycoprotein. J Biol Chem 273:32373-32376.
22. Luo W, Marsh-Armstrong N, Rattner A, Nathans J (2004) An outer segment localization signal at the C terminus of the photoreceptor-specific retinol dehydrogenase. J Neurosci 24:2623-2632.
23. MacKenzie D, Arendt A, Hargrave P, McDowell JH, Molday RS (1984) Localization of binding sites for carboxyl terminal specific anti- rhodopsin monoclonal antibodies using synthetic peptides. Biochemistry 23:6544-6549.
24. 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.
25. 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 timedependent pattern. J Biol Chem 276:28242-28251.
26. Moritz OL, Biddle KE, Tam BM (2002) Selection of transgenic Xenopus laevis using antibiotic resistance. Transgenic Res 11:315-319.
27. Naash ML, Peachey NS, Li ZY, Gryczan CC, Goto Y, Blanks J, Milam AH, Ripps H (1996) Light-induced acceleration of photoreceptor degeneration in transgenic mice expressing mutant rhodopsin. Invest Ophthalmol Vis Sci 37:775-782.
28. Nelson RM, Long GL (1989) A general method of site-specific mutagenesis using a modification of the Thermus aquaticus polymerase chain reaction. Anal Biochem 180:147-151.
29. Noorwez SM, Malhotra R, McDowell JH, Smith KA, Krebs MP, Kaushal S (2004) Retinoids assist the cellular folding of the autosomal dominant retinitis pigmentosa opsin mutant P23H. J Biol Chem 279:16278-16284.
30. Organisciak DT, Darrow RM, Barsalou L, Kutty RK, Wiggert B (2003) Susceptibility to retinal light damage in transgenic rats with rhodopsin mutations. Invest Ophthalmol Vis Sci 44:486-492.
31. Paskowitz DM, Lavail MM, Duncan JL (2006) Light and inherited retinal degeneration. Br J Ophthalmol 90:1060-1066.
32. Rao RV, Bredesen DE (2004) Misfolded proteins, endoplasmic reticulum stress and neurodegeneration. Curr Opin Cell Biol 16:653-662.
33. Samardzija M, Wenzel A, Naash M, Reme CE, Grimm C (2006) Rpe65 as a modifier gene for inherited retinal degeneration. Eur J Neurosci 23:1028-1034.
34. Tam BM, Moritz OL (2006) Characterization of rhodopsin P23H-induced retinal degeneration in a Xenopus laevis model of retinitis pigmentosa. Invest Ophthalmol Vis Sci 47:3234-3241.
35. Tam BM, Xie G, Oprian DD, Moritz OL (2006) Mislocalized rhodopsin does not require activation to cause retinal degeneration and neurite out-growth in Xenopus laevis. J Neurosci 26:203-209.
36. Wu X, Sakata N, Lele KM, Zhou M, Jiang H, Ginsberg HN (1997) A two-site model for ApoB degradation in HepG2 cells. J Biol Chem 272:11575-11580.