Light-dependent translocation of arrestin in the absence of rhodopsin phosphorylation and transducin signaling

Journal of Neuroscience

Volumn 23, Issue 8, 2003, Pages 3124-3129

  Mendez, Ana ^a   Lem, Janis ^b   Simon, Melvin ^c   Chen, Jeannie ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Arrestin; Retina; Rhodopsin phosphorylation; Rod photoreceptor; RPE65; Transducin

Indexed keywords

RETINA S ANTIGEN; RHODOPSIN; TRANSDUCIN;

ACTIVE TRANSPORT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIFFUSION; MOUSE; NONHUMAN; PHOTOLYSIS; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RETINA ROD; SIGNAL TRANSDUCTION; VERTEBRATE;

EID: 0037847499     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-08-03124.2003     Document Type: Article

References (43)

1. Ablonczy Z, Crouch RK, Goletz PW, Redmond TM, Knapp DR, Ma JX, Rohrer B (2002) 11-cis-retinal reduces constitutive opsin phosphorylation and improves quantum catch in retinoid-deficient mouse rod photoreceptors. J Biol Chem 277:40491-40498.
2. Arshavsky VY, Lamb TD, Pugh Jr EN (2002) G Proteins and phototransduction. Annu Rev Physiol 64:153-187.
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 EFJ, Janssen APM, Winkens HJ (1985) Light induced shift and binding of S-antigen in retinal rods. Curr Eye Res 4:613-618.
5. Broekhuyse RM, Janssen APM, Tolhuizen EFJ (1987) Effect of light adaptation on the binding of 48-kDa protein (S-antigen) to photoreceptor cell membranes. Curr Eye Res 6:607-610.
6. Buczylko J, Saari JC, Crouch RK, Palczewski K (1996) Mechanisms of opsin activation. J Biol Chem 271:20621-20630.
7. Burns ME, Baylor DA (2001) Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu Rev Neurosci 24:779-805.
8. Calvert PD, Krasnoperova NV, Lyubarsky AL, Isayama T, Nicolo M, Kosaras B, Wong G, Gannon KS, Margolskee RF, Sidman RL, Pugh Jr EN, Makino CL, Lem J (2000) Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proc Natl Acad Sci USA 97:13913-13918.
9. Chen J, Makino CL, Peachey NS, Baylor DA, Simon MI (1995) Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science 267:374-377.
10. Chen CK, Burns ME, Spencer M, Niemi GA, Chen J, Hurley JB, Baylor DA, Simon MI (1999a) Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc Natl Acad Sci USA 96:3718-3722.
11. Chen J, Simon MI, Matthes MT, Yasumura D, LaVail MM (1999b) Increased susceptibility to light damage in an arrestin knockout mouse model of Oguchi disease (stationary night blindness). Invest Ophthalmol Vis Sci 40:2978-2982.
12. Cornwall MC, Fain GL (1994) Bleached pigment activates transduction in isolated rods of the salamander retina. J Physiol (Lond) 480:261-279.
13. Eckmiller MS, Toman A (1998) Association of kinesin with microtubules in diverse cytoskeletal systems in the outer segments of rods and cones. Acta Anat 162:133-141.
14. Fain GL, Matthews HR, Cornwall MC, Koutalos Y (2001) Adaptation in vertebrate photoreceptors. Physiol Rev 81:117-151.
15. 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.
16. Hamm HE, Bownds MD (1986) Protein complement of rod outer segments of frog retina. Biochemistry 25:4512-4523.
17. Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065-1070.
18. 11-mediated signaling pathway for photic entrainment of the chicken pineal circadian clock. J Neurosci 22:7321-7325.
19. Koutalos Y, Yau KW (1996) Regulation of sensitivity invertebrate rod photoreceptors by calcium. Trends Neurosci 19:73-81.
20. Mangini NJ, Pepperberg DR (1988) Immunolocalization of 48K in rod photoreceptors. Light and ATP increase OS labeling. Invest Ophthalmol Vis Sci 29:1221-1234.
21. Mangini NJ, Garner GL, Okajima TI, Donoso LA, Pepperberg DR (1994) Effect of hydroxylamine on the subcellular distribution of arrestin (S-antigen) in rod photoreceptors. Vis Neurosci 11:561-568.
22. Marszalek JR, Liu X, Roberts EA, Chui D, Marth JD, Williams DS, Goldstein LSB (2000) Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102:175-187.
23. McGinnis JF, Whelan JP, Donoso LA (1992) Transient, cyclic changes in mouse visual cell gene products during the light-dark cycle. J Neurosci Res 31:584-590.
24. 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.
25. Mendez A, Burns ME, Roca A, Lem J, Wu LW, Simon MI, Baylor DA, Chen J (2000) Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 28:153-164.
26. Offermanns S (2001) In vivo functions of heterotrimeric G-proteins: studies in Gα-deficient mice. Oncogene 20:1635-1642.
27. Organisciak DT, Xie A, Wang HM, Jiang YL, Darrow RM, Donoso LA (1991) Adaptive changes in visual cell transduction protein levels: effect of light. Exp Eye Res 53:773-779.
28. Peng Y-W, Rhee SG, Yu W-P, Ho Y-K, Schoen T, Chader GJ, Yau K-W (1997) Identification of components of a phosphoinositide signaling pathway in retinal rod outer segments. Proc Natl Acad Sci USA 94:1995-2000.
29. 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, in press.
30. Philp NJ, Chang W, Long K (1987) Light-stimulated protein movement in rod photoreceptor cells of the rat retina. FEBS Lett 225:127-132.
31. Pugh Jr EN, Lamb TD (1990) Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Res 30:1923-1948.
32. Pugh Jr EN, Nikonov S, Lamb TD (1999) Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9:410-418.
33. Pulvermuller A, Maretzki D, Rudnicka-Nawrot M, Smith WC, Palczewski K, Hofmann KP (1997) Functional differences in the interaction of arrestin and its splice variant, p44, with rhodopsin. Biochemistry 36:9253-9260.
34. Raport CJ, Lem J, Makino C, Chen CK, Fitch CL, Hobson A, Baylor D, Simon MI, Hurley JB (1994) Downregulation of cGMP phosphodiesterase induced by expression of GTPase-deficient cone transducin in mouse rod photoreceptors. Invest Ophthalmol Vis Sci 35:2932-2947.
35. Redmond TM, Yu S, Lee E, Bok D, Hamasaki D, Chen N, Goletz P, Ma JX, Crouch RK, Pfeifer K (1998) Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat Genet 20:344-351.
36. Robinson PR, Cohen GB, Zhukovsky EA, Oprian DD (1992) Constitutively active mutants of rhodopsin. Neuron 9:719-725.
37. 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.
38. Surya A, Foster KW, Knox BE (1995) Transducin activation by the bovine opsin apoprotein. J Biol Chem 270:5024-5031.
39. Van Hooser JP, Liang Y, Maeda T, Kuksa V, Jang G-F, He Y-G, Rieke F, Fong HKW, Detwiler PB, Palczewski K (2002) Recovery of visual functions in a mouse model of Leber congenital amaurosis. J Biol Chem 277:19173-19182.
40. Whelan JP, McGinnis JF (1988) Light-dependent subcellular movement of photoreceptor proteins. J Neurosci Res 20:263-270.
41. Wilden U (1995) Duration and amplitude of the light-induced cGMP hydrolysis in vertebrate photoreceptors are regulated by multiple phosphorylation of rhodopsin and by arrestin binding. Biochemistry 34:1446-1454.
42. Wilden U, Hall SW, Kühn H (1986) Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48-kDa protein of rod outer segments. Proc Natl Acad Sci USA 83:1174-1178.
43. Xu J, Dodd RL, Makino CL, Simon MI, Baylor DA, Chen J (1997) Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389:505-509.