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PMID: 17069872 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Arrestin can act as a regulator of rhodopsin photochemistry.

Vision research ·Vol. 46 ·No. 27 ·2006-12-00 ·Pages 4532-46

Sommer ME, Farrens DL

Abstract

We report that visual arrestin can regulate retinal release and late photoproduct formation in rhodopsin. Our experiments, which employ a fluorescently labeled arrestin and rhodopsin solubilized in detergent/phospholipid micelles, indicate that arrestin can trap a population of retinal in the binding pocket with an absorbance characteristic of Meta II with the retinal Schiff-base intact. Furthermore, arrestin can convert Metarhodopsin III (formed either by thermal decay or blue-light irradiation) to a Meta II-like absorbing species. Together, our results suggest arrestin may be able to play a more complex role in the rod cell besides simply quenching transducin activity. This possibility may help explain why arrestin deficiency leads to problems like stationary night blindness (Oguchi disease) and retinal degeneration.

MeSH Terms
Animals Arrestin/analysis,physiology Dark Adaptation Micelles Night Blindness/metabolism Protein Binding Recombinant Proteins/analysis,metabolism Retinal Rod Photoreceptor Cells/metabolism Retinaldehyde/metabolism Rhodopsin/metabolism Schiff Bases/metabolism Spectrophotometry, Ultraviolet Transducin/metabolism Vision, Ocular
Chemicals
Arrestin Micelles Recombinant Proteins Schiff Bases metarhodopsins Rhodopsin Transducin Retinaldehyde
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Sommer Martha E
Department of Biochemistry and Molecular Biology, Oregon Health and Science University, Portland, OR 97239-3098, USA.
Farrens David L
References (81)
81 references, click to expand
  1. A2-rhodopsin: a new fluorophore isolated from photoreceptor outer segments.
    Org Biomol Chem. 2003 Apr 7;1(7):1101-5 PMID: 12926382
  2. Metarhodopsin III formation and decay kinetics: comparison of bovine and human rhodopsin.
    Vision Res. 1997 Jan;37(1):1-8 PMID: 9068826
  3. Interaction with transducin depletes metarhodopsin III: a regulated retinal storage in visual signal transduction?
    J Biol Chem. 2004 Nov 12;279(46):48112-9 PMID: 15322130
  4. Modulation of arrestin release in the light-driven regeneration of Rh1 Drosophila rhodopsin.
    Biochemistry. 1996 Feb 13;35(6):1848-55 PMID: 8639666
  5. 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 U S A. 1986 Mar;83(5):1174-8 PMID: 3006038
  6. Phototransduction: crystal clear.
    Trends Biochem Sci. 2003 Sep;28(9):479-87 PMID: 13678959
  7. Dynamics of arrestin-rhodopsin interactions: acidic phospholipids enable binding of arrestin to purified rhodopsin in detergent.
    J Biol Chem. 2006 Apr 7;281(14):9407-17 PMID: 16428804
  8. Phosphorylation of non-bleached rhodopsin in intact retinas and living frogs.
    J Biol Chem. 1996 Aug 16;271(33):19826-30 PMID: 8702691
  9. Schiff bases formed from retinal and phosphatidylethanolamine, phosphatidylserine, ethanolamine or serine.
    Biochem J. 1969 Dec;115(5):927-34 PMID: 5360725
  10. Constitutive activation of opsin: interaction of mutants with rhodopsin kinase and arrestin.
    Biochemistry. 1995 Sep 19;34(37):11938-45 PMID: 7547930
  11. Functional differences in the interaction of arrestin and its splice variant, p44, with rhodopsin.
    Biochemistry. 1997 Jul 29;36(30):9253-60 PMID: 9230059
  12. Constitutive activation of phototransduction by K296E opsin is not a cause of photoreceptor degeneration.
    Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3551-5 PMID: 7724596
  13. Rotational diffusion of rhodopsin in the visual receptor membrane.
    Nat New Biol. 1972 Mar 15;236(63):39-43 PMID: 4537062
  14. Light-dependent redistribution of visual arrestins and transducin subunits in mice with defective phototransduction.
    Mol Vis. 2003 Jun 9;9:231-7 PMID: 12802257
  15. THE ACTION OF LIGHT ON RHODOPSIN.
    Proc Natl Acad Sci U S A. 1958 Feb;44(2):130-9 PMID: 16590155
  16. Arrestin and its splice variant Arr1-370A (p44). Mechanism and biological role of their interaction with rhodopsin.
    J Biol Chem. 2002 Nov 15;277(46):43987-96 PMID: 12194979
  17. Temporal kinetics of the light/dark translocation and compartmentation of arrestin and alpha-transducin in mouse photoreceptor cells.
    Mol Vis. 2004 Sep 15;10:672-81 PMID: 15467522
  18. Responses of the phototransduction cascade to dim light.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4677-82 PMID: 8643463
  19. Photoregeneration of bovine rhodopsin from its signaling state.
    Biochemistry. 1995 Jul 25;34(29):9333-40 PMID: 7626602
  20. Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by protein-protein interactions.
    Neuron. 2005 May 19;46(4):555-67 PMID: 15944125
  21. Adaptive changes in visual cell transduction protein levels: effect of light.
    Exp Eye Res. 1991 Dec;53(6):773-9 PMID: 1783015
  22. Visual arrestin binding to microtubules involves a distinct conformational change.
    J Biol Chem. 2006 Apr 7;281(14):9765-72 PMID: 16461350
  23. How activated receptors couple to G proteins.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):4819-21 PMID: 11320227
  24. Rhodopsin self-associates in asolectin liposomes.
    Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3060-5 PMID: 16492772
  25. Concentration-dependent tetramerization of bovine visual arrestin.
    Biophys J. 2003 Aug;85(2):1186-95 PMID: 12885662
  26. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration.
    Prog Retin Eye Res. 2005 Mar;24(2):275-306 PMID: 15610977
  27. Characterization of a truncated form of arrestin isolated from bovine rod outer segments.
    Protein Sci. 1994 Feb;3(2):314-24 PMID: 8003967
  28. Molecular basis of visual excitation.
    Science. 1968 Oct 11;162(3850):230-9 PMID: 4877437
  29. Lateral diffusion of visual pigment in photorecptor disk membranes.
    Science. 1974 Aug 2;185(4149):457-9 PMID: 4546260
  30. Dark adaptation and the retinoid cycle of vision.
    Prog Retin Eye Res. 2004 May;23(3):307-80 PMID: 15177205
  31. Increased susceptibility to light damage in an arrestin knockout mouse model of Oguchi disease (stationary night blindness)
    Invest Ophthalmol Vis Sci. 1999 Nov;40(12):2978-82 PMID: 10549660
  32. Signaling states of rhodopsin: absorption of light in active metarhodopsin II generates an all-trans-retinal bound inactive state.
    J Biol Chem. 2001 Aug 10;276(32):30161-6 PMID: 11384968
  33. Physiological activity of isorhodopsin in rat rods.
    Vision Res. 1977;17(6):711-4 PMID: 602031
  34. 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. 2003 May;76(5):553-63 PMID: 12697419
  35. The role of arrestin and retinoids in the regeneration pathway of rhodopsin.
    J Biol Chem. 1992 Aug 5;267(22):15701-6 PMID: 1386362
  36. Kinetics, binding constant, and activation energy of the 48-kDa protein-rhodopsin complex by extra-metarhodopsin II.
    Biochemistry. 1989 Feb 21;28(4):1770-5 PMID: 2719933
  37. Deactivation of rhodopsin in the transition from the signaling state meta II to meta III involves a thermal isomerization of the retinal chromophore C[double bond]D.
    Biochemistry. 2003 Aug 26;42(33):9863-74 PMID: 12924935
  38. Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin.
    J Neurosci. 2006 Jan 25;26(4):1146-53 PMID: 16436601
  39. Secondary binding sites of retinoids in opsin: characterization and role in regeneration.
    Vision Res. 2003 Dec;43(28):3003-10 PMID: 14611936
  40. Structure and function in rhodopsin: asymmetric reconstitution of rhodopsin in liposomes.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13409-12 PMID: 12370420
  41. The orientation of the chromophore of vertebrate rhodopsin in the "meta" intermediate states and the reversibility of the meta II-meta III transition.
    Vision Res. 1979;19(9):1005-18 PMID: 43624
  42. Direct binding of visual arrestin to microtubules determines the differential subcellular localization of its splice variants in rod photoreceptors.
    J Biol Chem. 2004 Sep 24;279(39):41240-8 PMID: 15272005
  43. Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin.
    Science. 1996 Nov 1;274(5288):768-70 PMID: 8864113
  44. The kinetics of multiphosphorylation of rhodopsin.
    Arch Biochem Biophys. 1993 Aug 1;304(2):443-7 PMID: 8346919
  45. Molecular genetics of Oguchi disease, fundus albipunctatus, and other forms of stationary night blindness: LVII Edward Jackson Memorial Lecture.
    Am J Ophthalmol. 2000 Nov;130(5):547-63 PMID: 11078833
  46. Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes.
    J Biol Chem. 2003 Jun 13;278(24):21655-62 PMID: 12663652
  47. Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt's macular degeneration.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):5928-33 PMID: 15067110
  48. Ligand channeling within a G-protein-coupled receptor. The entry and exit of retinals in native opsin.
    J Biol Chem. 2003 Jul 4;278(27):24896-903 PMID: 12707280
  49. Rhodopsin phosphorylation and its role in photoreceptor function.
    Vision Res. 1998 May;38(10):1341-52 PMID: 9667002
  50. Signaling states of rhodopsin. Formation of the storage form, metarhodopsin III, from active metarhodopsin II.
    J Biol Chem. 2003 Jan 31;278(5):3162-9 PMID: 12427735
  51. Rhodopsin-phospholipid interactions: dependence of rate of the meta I to meta II transition on the level of associated disk phospholipid.
    Biochemistry. 1981 Feb 3;20(3):631-4 PMID: 7213599
  52. Formation of Meta III during the decay of activated rhodopsin proceeds via Meta I and not via Meta II.
    Biochemistry. 2004 Jul 27;43(29):9457-66 PMID: 15260488
  53. Photoreactions of metarhodopsin III.
    Biochemistry. 2004 Aug 10;43(31):10255-64 PMID: 15287753
  54. Dynamics of arrestin-rhodopsin interactions: arrestin and retinal release are directly linked events.
    J Biol Chem. 2005 Feb 25;280(8):6861-71 PMID: 15591052
  55. Early receptor potential: photoreversible charge displacement in rhodopsin.
    Science. 1967 Mar 3;155(3766):1128-31 PMID: 6021913
  56. Structure and function in rhodopsin. Measurement of the rate of metarhodopsin II decay by fluorescence spectroscopy.
    J Biol Chem. 1995 Mar 10;270(10):5073-6 PMID: 7890614
  57. A splice variant of arrestin. Molecular cloning and localization in bovine retina.
    J Biol Chem. 1994 Jun 3;269(22):15407-10 PMID: 7515057
  58. Site of attachment of retinal in rhodopsin.
    Nature. 1967 Dec 23;216(5121):1178-81 PMID: 4294735
  59. The identity of metarhodopsin III.
    Vis Neurosci. 2003 May-Jun;20(3):249-65 PMID: 14570247
  60. Rhodopsin structure, dynamics, and activation: a perspective from crystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking.
    Adv Protein Chem. 2003;63:243-90 PMID: 12629973
  61. Studies of Rh1 metarhodopsin stabilization in wild-type Drosophila and in mutants lacking one or both arrestins.
    Biochemistry. 1997 Feb 25;36(8):2188-96 PMID: 9047319
  62. Structural and functional impairment of endocytic pathways by retinitis pigmentosa mutant rhodopsin-arrestin complexes.
    J Clin Invest. 2004 Jul;114(1):131-40 PMID: 15232620
  63. Crystal structure of rhodopsin: A G protein-coupled receptor.
    Science. 2000 Aug 4;289(5480):739-45 PMID: 10926528
  64. Activation, deactivation, and adaptation in vertebrate photoreceptor cells.
    Annu Rev Neurosci. 2001;24:779-805 PMID: 11520918
  65. Isolation and identification of the phosphorylated species of rhodopsin.
    Biochemistry. 1984 Apr 10;23(8):1737-41 PMID: 6722121
  66. Blue light's effects on rhodopsin: photoreversal of bleaching in living rat eyes.
    Invest Ophthalmol Vis Sci. 2000 Nov;41(12):3984-90 PMID: 11053303
  67. REACTION OF THE RHODOPSIN CHROMOPHORE WITH SODIUM BOROHYDRIDE.
    Nature. 1965 Jan 16;205:254-7 PMID: 14270706
  68. Reduction of all-trans-retinal limits regeneration of visual pigment in mice.
    Vision Res. 1998 May;38(10):1325-33 PMID: 9667000
  69. Transition of rhodopsin into the active metarhodopsin II state opens a new light-induced pathway linked to Schiff base isomerization.
    J Biol Chem. 2004 Nov 12;279(46):48102-11 PMID: 15322129
  70. Determination of protein secondary structure and solvent accessibility using site-directed fluorescence labeling. Studies of T4 lysozyme using the fluorescent probe monobromobimane.
    Biochemistry. 1999 Dec 7;38(49):16383-93 PMID: 10587464
  71. Light-dependent translocation of arrestin in the absence of rhodopsin phosphorylation and transducin signaling.
    J Neurosci. 2003 Apr 15;23(8):3124-9 PMID: 12716919
  72. Structure of rhodopsin and the metarhodopsin I photointermediate.
    Curr Opin Struct Biol. 2005 Aug;15(4):408-15 PMID: 16043340
  73. Kinetics of visual pigment regeneration in excised mouse eyes and in mice with a targeted disruption of the gene encoding interphotoreceptor retinoid-binding protein or arrestin.
    Biochemistry. 1999 Sep 14;38(37):12012-9 PMID: 10508404
  74. Temperature and pH dependence of the metarhodopsin I-metarhodopsin II equilibrium and the binding of metarhodopsin II to G protein in rod disk membranes
    Biochemistry. 1999 Jun 29;38(26):8598 PMID: 10387108
  75. Reduction of all-trans retinal to all-trans retinol in the outer segments of frog and mouse rod photoreceptors.
    Biophys J. 2005 Mar;88(3):2278-87 PMID: 15626704
  76. Photoactivation of rhodopsin and interaction with transducin in detergent micelles. Effect of 'doping' with steroid molecules.
    FEBS Lett. 1989 Oct 23;257(1):163-6 PMID: 2806558
  77. A role for cytoskeletal elements in the light-driven translocation of proteins in rod photoreceptors.
    Invest Ophthalmol Vis Sci. 2005 Nov;46(11):3988-98 PMID: 16249472
  78. Evidence for two apoptotic pathways in light-induced retinal degeneration.
    Nat Genet. 2002 Oct;32(2):254-60 PMID: 12219089
  79. Light-induced binding of 48-kDa protein to photoreceptor membranes is highly enhanced by phosphorylation of rhodopsin.
    FEBS Lett. 1984 Oct 29;176(2):473-8 PMID: 6436059
  80. The dark side of light: rhodopsin and the silent death of vision the proctor lecture.
    Invest Ophthalmol Vis Sci. 2005 Aug;46(8):2671-82 PMID: 16043837
  81. A2E, a byproduct of the visual cycle.
    Vision Res. 2003 Dec;43(28):2983-90 PMID: 14611934
Article Info
Journal
Vision research
Abbr.
Vision Res
ISSN
0042-6989
Published
2006-12-00
Epub
2006-00-27
Pages
4532-46
Language
English
Region
England
NLM ID
0417402
PMCID
PMC2877124
Subset
IM
Grants
NIDA NIH HHS · R01 DA018169 · United States
NEI NIH HHS · R01 EY015436 · United States
NIDA NIH HHS · DA018169 · United States
NEI NIH HHS · EY015436 · United States
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