Q344ter mutation causes mislocalization of rhodopsin molecules that are catalytically active: A mouse model of Q344ter-induced retinal degeneration

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Concepcion, Francis ^a   Chen, Jeannie ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; RHODOPSIN; TRANSDUCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL DEATH; CELL VACUOLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE ACTIVATION; GENE EXPRESSION; GENE LOCATION; GENETIC CROSS; IN VIVO STUDY; KNOCKOUT MOUSE; LIGHT EXPOSURE; MICROSCOPY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN DOMAIN; RETINA DEGENERATION; RETINA ROD; RETINA ROD OUTER SEGMENT; SIGNAL TRANSDUCTION; TRANSGENE; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; BLOTTING, WESTERN; CATALYSIS; CELL DEATH; DISEASE MODELS, ANIMAL; MICE; MICE, TRANSGENIC; MUTATION; PHOTORECEPTOR CELLS, VERTEBRATE; RETINAL DEGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHODOPSIN;

MUS; MUS MUSCULUS;

EID: 77955199065     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010904     Document Type: Article

References (69)

1. Rivolta C, Sharon D, DeAngelis MM, Dryja TP (2002) Retinitis pigmentosa and allied diseases: numerous diseases, genes, and inheritance patterns. Hum Mol Genet 11: 1219-1227.
2. Hamel C (2006) Retinitis pigmentosa. Orphanet J Rare Dis 1: 40.
3. Sohocki MM, Daiger SP, Bowne SJ, Rodriquez JA, Northrup H, et al. (2001) Prevalence of mutations causing retinitis pigmentosa and other inherited retinopathies. Hum Mutat 17: 42-51.
4. Wang DY, Chan WM, Tam PO, Baum L, Lam DS, et al. (2005) Gene mutations in retinitis pigmentosa and their clinical implications. Clin Chim Acta 351: 5-16.
5. Gregory-Evans K, Bhattacharya SS (1998) Genetic blindness: current concepts in the pathogenesis of human outer retinal dystrophies. Trends Genet 14: 103-108.
6. Sung CH, Schneider BG, Agarwal N, Papermaster DS, Nathans J (1991) Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci U S A 88: 8840-8844.
7. Kaushal S, Khorana HG (1994) Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33: 6121-6128.
8. Mendes HF, van der Spuy J, Chapple JP, Cheetham ME (2005) Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy. Trends Mol Med 11: 177-185.
9. Sung CH, Davenport CM, Nathans J (1993) Rhodopsin mutations responsible for autosomal dominant retinitis pigmentosa. Clustering of functional classes along the polypeptide chain. J Biol Chem 268: 26645-26649.
10. Deretic D, Schmerl S, Hargrave PA, Arendt A, McDowell JH (1998) Regulation of sorting and post-Golgi trafficking of rhodopsin by its C-terminal sequence QVS(A)PA. Proc Natl Acad Sci U S A 95: 10620-10625.
11. Deretic D, Puleo-Scheppke B, Trippe C (1996) Cytoplasmic domain of rhodopsin is essential for post-Golgi vesicle formation in a retinal cell-free system. J Biol Chem 271: 2279-2286.
12. 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.
13. Olsson JE, Gordon JW, Pawlyk BS, Roof D, Hayes A, et al. (1992) Transgenic mice with a rhodopsin mutation (Pro23His): a mouse model of autosomal dominant retinitis pigmentosa. Neuron 9: 815-830.
14. Tan E, Wang Q, Quiambao AB, Xu X, Qtaishat NM, et al. (2001) The relationship between opsin overexpression and photoreceptor degeneration. Invest Ophthalmol Vis Sci 42: 589-600.
15. Concepcion F, Mendez A, Chen J (2002) The carboxyl-terminal domain is essential for rhodopsin transport in rod photoreceptors. Vision Res 42: 417-426.
16. Zack DJ, Bennett J, Wang Y, Davenport C, Klaunberg B, et al. (1991) Unusual topography of bovine rhodopsin promoter-lacZ fusion gene expression in transgenic mouse retinas. Neuron 6: 187-199.
17. Palczewski K, Buczylko J, Kaplan MW, Polans AS, Crabb JW (1991) Mechanism of rhodopsin kinase activation. J Biol Chem 266: 12949-12955.
18. Lem J, Krasnoperova NV, Calvert PD, Kosaras B, Cameron DA, et al. (1999) Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc Natl Acad Sci U S A 96: 736-741.
19. Adamus G, Zam ZS, Arendt A, Palczewski K, McDowell JH, et al. (1991) Anti-rhodopsin monoclonal antibodies of defined specificity: characterization and application. Vision Res 31: 17-31.
20. Hodges RS, Heaton RJ, Parker JM, Molday L, Molday RS (1988) Antigen-antibody interaction. Synthetic peptides define linear antigenic determinants recognized by monoclonal antibodies directed to the cytoplasmic carboxyl terminus of rhodopsin. J Biol Chem 263: 11768-11775.
21. 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 U S A 93: 14176-14181.
22. Humphries MM, Rancourt D, Farrar GJ, Kenna P, Hazel M, et al. (1997) Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat Genet 15: 216-219.
23. Lee ES, Burnside B, Flannery JG (2006) Characterization of peripherin/rds and rom-1 transport in rod photoreceptors of transgenic and knockout animals. Invest Ophthalmol Vis Sci 47: 2150-2160.
24. Danciger M, Matthes MT, Yasamura D, Akhmedov NB, Rickabaugh T, et al. (2000) A QTL on distal chromosome 3 that influences the severity of light-induced damage to mouse photoreceptors. Mamm Genome 11: 422-427.
25. Vaughan DK, Coulibaly SF, Darrow RM, Organisciak DT (2003) A morphometric study of light-induced damage in transgenic rat models of retinitis pigmentosa. Invest Ophthalmol Vis Sci 44: 848-855.
26. Roca A, Shin KJ, Liu X, Simon MI, Chen J (2004) Comparative analysis of transcriptional profiles between two apoptotic pathways of light-induced retinal degeneration. Neuroscience 129: 779-790.
27. Grimm C, Wenzel A, Hafezi F, Yu S, Redmond TM, et al. (2000) Protection of Rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat Genet 25: 63-66.
28. Alfinito PD, Townes-Anderson E (2002) Activation of mislocalized opsin kills rod cells: a novel mechanism for rod cell death in retinal disease. Proc Natl Acad Sci U S A 99: 5655-5660.
29. Kuhn H, Wilden U (1987) Deactivation of photoactivated rhodopsin by rhodopsin-kinase and arrestin. J Recept Res 7: 283-298.
30. Metaye T, Gibelin H, Perdrisot R, Kraimps JL (2005) Pathophysiological roles of G-protein-coupled receptor kinases. Cell Signal 17: 917-928.
31. Laird DW, Molday RS (1988) Evidence against the role of rhodopsin in rod outer segment binding to RPE cells. Invest Ophthalmol Vis Sci 29: 419-428.
32. Alloway PG, Howard L, Dolph PJ (2000) The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 28: 129-138.
33. Kiselev A, Socolich M, Vinos J, Hardy RW, Zuker CS, et al. (2000) A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron 28: 139-152.
34. Chen J, Shi G, Concepcion FA, Xie G, Oprian D, et al. (2006) Stable Rhodopsin/Arrestin Complex Leads to Retinal Degeneration in a Transgenic Mouse Model of Autosomal Dominant Retinitis Pigmentosa. J Neurosci 26: 11929-11937.
35. Hao W, Wenzel A, Obin MS, Chen CK, Brill E, et al. (2002) Evidence for two apoptotic pathways in light-induced retinal degeneration. Nat Genet 32: 254-260.
36. Chen J, Simon MI, Matthes MT, Yasumura D, LaVail MM (1999) Increased susceptibility to light damage in an arrestin knockout mouse model of Oguchi disease (stationary night blindness). Invest Ophthalmol Vis Sci 40: 2978-2982.
37. Chen CK, Burns ME, Spencer M, Niemi GA, Chen J, et al. (1999) Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc Natl Acad Sci U S A 96: 3718-3722.
38. Gurevich VV, Benovic JL (1993) Visual arrestin interaction with rhodopsin. Sequential multisite binding ensures strict selectivity toward light-activated phosphorylated rhodopsin. J Biol Chem 268: 11628-11638.
39. Gurevich VV, Gurevich EV (2004) The molecular acrobatics of arrestin activation. Trends Pharmacol Sci 25: 105-111.
40. Mendez A, Burns ME, Roca A, Lem J, Wu LW, et al. (2000) Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 28: 153-164.
41. Zanazzi G, Matthews G (2009) The molecular architecture of ribbon presynaptic terminals. Mol Neurobiol 39: 130-148.
42. Deretic D, Williams AH, Ransom N, Morel V, Hargrave PA, et al. (2005) Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proc Natl Acad Sci U S A 102: 3301-3306.
43. Mazelova J, Astuto-Gribble L, Inoue H, Tam BM, Schonteich E, et al. (2009) Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. Embo J 28: 183-192.
44. Shi G, Concepcion FA, Chen J (2004) Targeting of visual pigments to rod outer segment in rhodopsin knockout mice. In: Williams DS, editor. Photoreceptor Cell Biology and Inherited Retinal Degenerations. Singapore: World Scientific. pp. 93-107.
45. Tam BM, Xie G, Oprian DD, Moritz OL (2006) Mislocalized rhodopsin does not require activation to cause retinal degeneration and neurite outgrowth in Xenopus laevis. J Neurosci 26: 203-209.
46. Hagstrom SA, Adamian M, Scimeca M, Pawlyk BS, Yue G, et al. (2001) A role for the Tubby-like protein 1 in rhodopsin transport. Invest Ophthalmol Vis Sci 42: 1955-1962.
47. Hagstrom SA, Duyao M, North MA, Li T (1999) Retinal degeneration in tulp1-/- mice: vesicular accumulation in the interphotoreceptor matrix. Invest Ophthalmol Vis Sci 40: 2795-2802.
48. Heckenlively JR, Chang B, Erway LC, Peng C, Hawes NL, et al. (1995) Mouse model for Usher syndrome: linkage mapping suggests homology to Usher type I reported at human chromosome 11p15. Proc Natl Acad Sci U S A 92: 11100-11104.
49. Blanks JC, Spee C (1992) Retinal degeneration in the pcd/pcd mutant mouse: accumulation of spherules in the interphotoreceptor space. Exp Eye Res 54: 637-644.
50. Lee ES, Flannery JG (2007) Transport of truncated rhodopsin and its effects on rod function and degeneration. Invest Ophthalmol Vis Sci 48: 2868-2876.
51. Hu G, Wensel TG (2002) R9AP, a membrane anchor for the photoreceptor GTPase accelerating protein, RGS9-1. Proc Natl Acad Sci U S A 99: 9755-9760.
52. Zhang X, Wensel TG, Kraft TW (2003) GTPase regulators and photoresponses in cones of the eastern chipmunk. J Neurosci 23: 1287-1297.
53. Kanaho Y, Tsai SC, Adamik R, Hewlett EL, Moss J, et al. (1984) Rhodopsin-enhanced GTPase activity of the inhibitory GTP-binding protein of adenylate cyclase. J Biol Chem 259: 7378-7381.
54. Terakita A, Yamashita T, Nimbari N, Kojima D, Shichida Y (2002) Functional interaction between bovine rhodopsin and G protein transducin. J Biol Chem 277: 40-46.
55. Oguni M, Shinohara H, Asano T, Kato K, Setogawa T (1996) Ontogeny of GTP-binding proteins, Gi and G(o), in rat retina. Histochem Cell Biol 106: 235-240.
56. Robinson PR, Cohen GB, Zhukovsky EA, Oprian DD (1992) Constitutively active mutants of rhodopsin. Neuron 9: 719-725.
57. Brill E, Malanson KM, Radu RA, Boukharov NV, Wang Z, et al. (2007) A novel form of transducin-dependent retinal degeneration: accelerated retinal degeneration in the absence of rod transducin. Invest Ophthalmol Vis Sci 48: 5445-5453.
58. Jozwick C, Valter K, Stone J (2006) Reversal of functional loss in the P23H-3 rat retina by management of ambient light. Exp Eye Res 83: 1074-1080.
59. Naash MI, Ripps H, Li S, Goto Y, Peachey NS (1996) Polygenic disease and retinitis pigmentosa: albinism exacerbates photoreceptor degeneration induced by the expression of a mutant opsin in transgenic mice. J Neurosci 16: 7853-7858.
60. 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.
61. White DA, Fritz JJ, Hauswirth WW, Kaushal S, Lewin AS (2007) Increased sensitivity to light-induced damage in a mouse model of autosomal dominant retinal disease. Invest Ophthalmol Vis Sci 48: 1942-1951.
62. Berson EL, Rosner B, Weigel-DiFranco C, Dryja TP, Sandberg MA (2002) Disease progression in patients with dominant retinitis pigmentosa and rhodopsin mutations. Invest Ophthalmol Vis Sci 43: 3027-3036.
63. Oh KT, Longmuir R, Oh DM, Stone EM, Kopp K, et al. (2003) Comparison of the clinical expression of retinitis pigmentosa associated with rhodopsin mutations at codon 347 and codon 23. Am J Ophthalmol 136: 306-313.
64. Noell WK, Walker VS, Kang BS, Berman S (1966) Retinal damage by light in rats. Invest Ophthalmol 5: 450-473.
65. Noell WK (1980) Possible mechanisms of photoreceptor damage by light in mammalian eyes. Vision Res 20: 1163-1171.
66. Wenzel A, Grimm C, Samardzija M, Reme CE (2005) Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res 24: 275-306.
67. Mendez A, Krasnoperova NV, Lem J, Chen J (2000) Functional study of rhodopsin phosphorylation in vivo. Methods Enzymol 316: 167-185.
68. Sim-Selley LJ, Childers SR (2002) Neuroanatomical localization of receptor-activated G proteins in brain. Methods Enzymol 344: 42-58.
69. Taylor MR, Van Epps HA, Kennedy MJ, Saari JC, Hurley JB, et al. (2000) Biochemical analysis of phototransduction and visual cycle in zebrafish larvae. Methods Enzymol 316: 536-557.