Progressive reduction of its expression in rods reveals two pools of Arrestin-1 in the outer segment with different roles in photoresponse recovery

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Cleghorn, Whitney M ^a   Tsakem, Elviche L ^a   Song, Xiufeng ^a   Vishnivetskiy, Sergey A ^a   Seo, Jungwon ^a,c   Chen, Jeannie ^b   Gurevich, Eugenia V ^a   Gurevich, Vsevolod V ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c Wonkwang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARRESTIN 1; RETINA S ANTIGEN; RHODOPSIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAM; LIGHT INTENSITY; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RETINA ROD OUTER SEGMENT; WILD TYPE; ANIMAL; LIGHT; METABOLISM; PHOTOTRANSDUCTION; RADIATION EXPOSURE; TIME;

MUS;

ANIMALS; ARRESTIN; LIGHT; LIGHT SIGNAL TRANSDUCTION; MICE; ROD CELL OUTER SEGMENT; TIME FACTORS;

EID: 79960817781     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022797     Document Type: Article

References (71)

1. Luo DG, Xue T, Yau KW, (2008) How vision begins: an odyssey. Proc Natl Acad Sci U S A 105: 9855-9862.
2. Vishnivetskiy SA, Raman D, Wei J, Kennedy MJ, Hurley JB, et al. (2007) Regulation of arrestin binding by rhodopsin phosphorylation level. J Biol Chem 282: 32075-32083.
3. 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.
4. Makino CL, Wen XH, Lem J, (2003) Piecing together the timetable for visual transduction with transgenic animals. Curr Opin Neurobiol 13: 404-412.
5. Calvert PD, Govardovskii VI, Krasnoperova N, Anderson RE, Lem J, et al. (2001) Membrane protein diffusion sets the speed of rod phototransduction. Nature 411: 90-94.
6. Wen XH, Shen L, Brush RS, Michaud N, Al-Ubaidi MR, et al. (2009) Overexpression of rhodopsin alters the structure and photoresponse of rod photoreceptors. Biophys J 96: 939-950.
7. Krispel CM, Chen D, Melling N, Chen YJ, Martemyanov KA, et al. (2006) RGS expression rate-limits recovery of rod photoresponses. Neuron 51: 409-416.
8. Gross OP, Burns ME, (2010) Control of rhodopsin's active lifetime by arrestin-1 expression in mammalian cells. J Neurosci 30: 3450-3457.
9. Doan T, Azevedo AW, Hurley JB, Rieke F, (2009) Arrestin competition influences the kinetics and variability of the single-photon responses of mammalian rod photoreceptors. J Neurosci 29: 11867-11879.
10. Song X, Vishnivetskiy SA, Seo J, Chen J, Gurevich EV, et al. (2011) Arrestin-1 expression level in rods: Balancing functional performance and photoreceptor health. Neuroscience 174: 37-49.
11. Strissel KJ, Sokolov M, Trieu LH, Arshavsky VY, (2006) Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. J Neurosci 26: 1146-1153.
12. Hanson SM, Gurevich EV, Vishnivetskiy SA, Ahmed MR, Song X, et al. (2007) Each rhodopsin molecule binds its own arrestin. Proc Natl Acad Sci 104: 3125-3128.
13. Burns ME, Pugh EN Jr, (2009) RGS9 concentration matters in rod phototransduction. Biophys J 97: 1538-1547.
14. 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 Nat Acad Sci USA 96: 3718-3722.
15. 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.
16. Xu J, Dodd RL, Makino CL, Simon MI, Baylor DA, et al. (1997) Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389: 505-509.
17. Nikonov SS, Brown BM, Davis JA, Zuniga FI, Bragin A, et al. (2008) Mouse cones require an arrestin for normal inactivation of phototransduction. Neuron 59: 462-474.
18. 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.
19. Krupnick JG, Gurevich VV, Benovic JL, (1997) Mechanism of quenching of phototransduction: binding competition between arrestin and transducin for phosphorhodopsin. J Biol Chem 272: 18125-18131.
20. 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.
21. 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.
22. Philp NJ, Chang W, Long K, (1987) Light-stimulated protein movement in rod photoreceptor cells of the rat retina. FEBS Lett 225: 127-132.
23. Pugh EN Jr, Lamb TD, (2000) Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation. In: Stavenga DG, editors. Handbook of biological physics Molecular mechanisms in visual transduction Amsterdam Elsevier pp. 183-255.
24. Lyubarsky AL, Pugh EN Jr, (1996) Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. Journal of Neuroscience 16: 563-571.
25. Hetling JR, Pepperberg DR, (1999) Sensitivity and kinetics of mouse rod flash responses determined in vivo from paired-flash electroretinograms. J Physiol 516: 593-609.
26. Robson JG, Frishman LJ, (1995) Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Visual Neuroscience 12: 837-850.
27. Robson JG, Frishman LJ, (1996) Photoreceptor and bipolar cell contributions to the cat electroretinogram: a kinetic model for the early part of the flash response. Journal of the Optical Society of America, A, Optics, Image Science, & Vision 13: 613-622.
28. Pepperberg DR, Birch DG, Hood DC, (1997) Photoresponses of human rods in vivo derived from paired-flash electroretinograms. Vis Neurosci 14: 73-82.
29. Bayburt TH, Vishnivetskiy SA, McLean M, Morizumi T, Huang CC, et al. (2011) Rhodopsin monomer is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding. J Biol Chem 286: 1420-1428.
30. Lyubarsky AL, Daniele LL, Pugh EN Jr, (2004) From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG. Vision Res 44: 3235-3251.
31. Shen L, Caruso G, Bisegna P, Andreucci D, Gurevich VV, et al. (2010) Dynamics of mouse rod phototransduction and its sensitivity to variation of key parameters. IET Syst Biol 4: 12-32.
32. Burns ME, Pugh EN Jr, (2010) Lessons from photoreceptors: turning off g-protein signaling in living cells. Physiology (Bethesda) 25: 72-84.
33. Caruso G, Bisena P, Lenoci L, Andreucci D, Gurevich VV, et al. (2010) Kinetics of rhodopsin inactivation and its role in regulating recovery and reproducibility of rod photoresponse. PLoS Computational Biology 6: e1001031.
34. Kim M, Hanson SM, Vishnivetskiy SA, Song X, Cleghorn WM, et al. (2011) Robust self-association is a common feature of mammalian visual arrestin-1. Biochemistry 50: 2235-2242.
35. Schubert C, Hirsch JA, Gurevich VV, Engelman DM, Sigler PB, et al. (1999) Visual arrestin activity may be regulated by self-association. J Biol Chem 274: 21186-21190.
36. Imamoto Y, Tamura C, Kamikubo H, Kataoka M, (2003) Concentration-dependent tetramerization of bovine visual arrestin. Biophys J 85: 1186-1195.
37. Hanson SM, Van Eps N, Francis DJ, Altenbach C, Vishnivetskiy SA, et al. (2007) Structure and function of the visual arrestin oligomer. EMBO J 26: 1726-1736.
38. Hanson SM, Dawson ES, Francis DJ, Van Eps N, Klug CS, et al. (2008) A model for the solution structure of the rod arrestin tetramer. Structure 16: 924-934.
39. Kim M, Hanson SM, Vishnivetskiy SA, Song X, Cleghorn WM, et al. (2011) Robust self-association is a common feature of mammalian visual arrestin-1. Biochemistry 50 in press.
40. Gurevich VV, Benovic JL, (1993) Visual arrestin interaction with rhodopsin: Sequential multisite binding ensures strict selectivity towards light-activated phosphorylated rhodopsin. J Biol Chem 268: 11628-11638.
41. Gurevich VV, Benovic JL, (1995) Visual arrestin binding to rhodopsin: diverse functional roles of positively charged residues within the phosphorylation-recignition region of arrestin. J Biol Chem 270: 6010-6016.
42. Gurevich VV, Dion SB, Onorato JJ, Ptasienski J, Kim CM, et al. (1995) Arrestin interaction with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, b2-adrenergic, and m2 muscarinic cholinergic receptors. J Biol Chem 270: 720-731.
43. Vishnivetskiy SA, Hosey MM, Benovic JL, Gurevich VV, (2004) Mapping the arrestin-receptor interface: structural elements responsible for receptor specificity of arrestin proteins. J Biol Chem 279: 1262-1268.
44. Vishnivetskiy SA, Francis DJ, Van Eps N, Kim M, Hanson SM, et al. (2010) The role of arrestin alpha-helix I in receptor binding. J Mol Biol 395: 42-54.
45. Vishnivetskiy SA, Gimenez LE, Francis DJ, Hanson SM, Hubbell WL, et al. (2011) Few residues within an extensive binding interface drive receptor interaction and determine the specificity of arrestin proteins. J Biol Chem 286 in press.
46. Hanson SM, Francis DJ, Vishnivetskiy SA, Kolobova EA, Hubbell WL, et al. (2006) Differential interaction of spin-labeled arrestin with inactive and active phosphorhodopsin. Proc Natl Acad Sci U S A 103: 4900-4905.
47. Hanson SM, Gurevich VV, (2006) The differential engagement of arrestin surface charges by the various functional forms of the receptor. J Biol Chem 281: 3458-3462.
48. Gurevich VV, Hanson SM, Gurevich EV, Vishnivetskiy SA, (2007) How rod arrestin achieved perfection: regulation of its availability and binding selectivity. In: Kisselev O, Fliesler SJ, editors. Methods in signal transduction series Boca Raton, FL CRC Press pp. 55-88.
49. Nair KS, Hanson SM, Mendez A, Gurevich EV, Kennedy MJ, et al. (2005) Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by protein-protein interactions. Neuron 46: 555-567.
50. Elias RV, Sezate SS, Cao W, McGinnis JF, (2004) Temporal kinetics of the light/dark translocation and compartmentation of arrestin and alpha-transducin in mose photoreceptor cells. Mol Vis 10.
51. Orisme W, Li J, Goldmann T, Bolch S, Wolfrum U, et al. (2010) Light-dependent translocation of arrestin in rod photoreceptors is signaled through a phospholipase C cascade and requires ATP. Cell Signal 22: 447-456.
52. Peet JA, Bragin A, Calvert PD, Nikonov SS, Mani S, et al. (2004) Quantification of the cytoplasmic spaces of living cells with EGFP reveals arrestin-EGFP to be in disequilibrium in dark adapted rod photoreceptors. J Cell Sci 117: 3049-3059.
53. Slepak VZ, Hurley JB, (2008) Mechanism of light-induced translocation of arrestin and transducin in photoreceptors: interaction-restricted diffusion. IUBMB Life 60: 2-9.
54. Bayburt TH, Vishnivetskiy SA, McLean M, Morizumi T, Huang CC, et al. (2011) Rhodopsin monomer is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding. J Biol Chem 286: 1420-1428.
55. Tsukamoto H, Sinha A, Dewitt M, Farrens DL, (2010) Monomeric Rhodopsin Is the Minimal Functional Unit Required for Arrestin Binding. J Mol Biol 399: 501-511.
56. Nair KS, Hanson SM, Kennedy MJ, Hurley JB, Gurevich VV, et al. (2004) Direct binding of visual arrestin to microtubules determines the differential subcellular localization of its splice variants in rod photoreceptors. J Biol Chem 279: 41240-41248.
57. Hanson SM, Francis DJ, Vishnivetskiy SA, Klug CS, Gurevich VV, (2006) Visual arrestin binding to microtubules involves a distinct conformational change. J Biol Chem 281: 9765-9772.
58. Song X, Raman D, Gurevich EV, Vishnivetskiy SA, Gurevich VV, (2006) Visual and both non-visual arrestins in their "inactive" conformation bind JNK3 and Mdm2 and relocalize them from the nucleus to the cytoplasm. J Biol Chem 281: 21491-21499.
59. Ahmed MR, Zhan X, Song X, Gurevich VV, Gurevich EV, (2011) Ubiquitin ligase parkin promotes Mdm2-arrestin interaction but inhibits arrestin ubiquitination. Biochemistry 50: 3749-3763.
60. Wu N, Hanson SM, Francis DJ, Vishnivetskiy SA, Thibonnier M, et al. (2006) Arrestin binding to calmodulin: a direct interaction between two ubiquitous signaling proteins. J Mol Biol 364: 955-963.
61. Huang SP, Brown BM, Craft CM, (2010) Visual Arrestin 1 acts as a modulator for N-ethylmaleimide-sensitive factor in the photoreceptor synapse. J Neurosci 30: 9381-9391.
62. Smith WC, Bolch SN, Dugger DR, Li J, Esquenazi I, et al. (2011) Interaction of arrestin with enolase1 in photoreceptors. Invest Ophthalmol Vis Sci 52: 1832-1840.
63. Eckmiller MS, (2000) Microtubules in a rod-specific cytoskeleton associated with outer segment incisures. Vis Neurosci 17: 711-722.
64. Nir I, Ransom N, (1992) S-antigen in rods and cones of the primate retina: different labeling patterns are revealed with antibodies directed against specific domains in the molecule. J Histochem Cytochem 40: 343-352.
65. Nir I, Ransom N, (1993) Ultrastructural analysis of arrestin distribution in mouse photoreceptors during dark/light cycle. Exp Eye Res 57: 307-318.
66. Hanson SM, Cleghorn WM, Francis DJ, Vishnivetskiy SA, Raman D, et al. (2007) Arrestin mobilizes signaling proteins to the cytoskeleton and reidrects their activity. J Mol Biol 368: 375-387.
67. Chen CK, Woodruff ML, Chen FS, Chen D, Fain GL, (2010) Background light produces a recoverin-dependent modulation of activated-rhodopsin lifetime in mouse rods. J Neurosci 30: 1213-1220.
68. Song X, Vishnivetskiy SA, Gross OP, Emelianoff K, Mendez A, et al. (2009) Enhanced Arrestin Facilitates Recovery and Protects Rods Lacking Rhodopsin Phosphorylation. Current Biology 19: 700-705.
69. Lyubarsky AL, Lem J, Chen J, Falsini B, Iannaccone A, et al. (2002) Functionally rodless mice: transgenic models for the investigation of cone function in retinal disease and therapy. Vision Res 42: 401-415.
70. Pepperberg DR, Cornwall MC, Kahlert M, Hofmann KP, Jin J, et al. (1992) Light-dependent delay in the falling phase of the retinal rod photoresponse. Vis Neurosci 8: 9-18.
71. Birch DG, Hood DC, Nusinowitz S, Pepperberg DR, (1995) Abnormal activation and inactivation mechanisms of rod transduction in patients with autosomal dominant retinitis pigmentosa and the pro-23-his mutation. Invest Ophthalmol Vis Sci 36: 1603-1614.