Home LiteratureArticle Details
PMID: 23091036 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Conformation of receptor-bound visual arrestin.

Kim M, Vishnivetskiy SA, Van Eps N, Alexander NS, Cleghorn WM, Zhan X, Hanson SM, Morizumi T, Ernst OP, Meiler J, Gurevich VV, Hubbell WL

Abstract

Arrestin-1 (visual arrestin) binds to light-activated phosphorylated rhodopsin (P-Rh*) to terminate G-protein signaling. To map conformational changes upon binding to the receptor, pairs of spin labels were introduced in arrestin-1 and double electron-electron resonance was used to monitor interspin distance changes upon P-Rh* binding. The results indicate that the relative position of the N and C domains remains largely unchanged, contrary to expectations of a "clam-shell" model. A loop implicated in P-Rh* binding that connects β-strands V and VI (the "finger loop," residues 67-79) moves toward the expected location of P-Rh* in the complex, but does not assume a fully extended conformation. A striking and unexpected movement of a loop containing residue 139 away from the adjacent finger loop is observed, which appears to facilitate P-Rh* binding. This change is accompanied by smaller movements of distal loops containing residues 157 and 344 at the tips of the N and C domains, which correspond to "plastic" regions of arrestin-1 that have distinct conformations in monomers of the crystal tetramer. Remarkably, the loops containing residues 139, 157, and 344 appear to have high flexibility in both free arrestin-1 and the P-Rh*complex.

MeSH Terms
Arrestin/chemistry,metabolism Crystallography, X-Ray Electrons Models, Molecular Mutant Proteins/chemistry,metabolism Phosphorylation Protein Binding Protein Multimerization Protein Stability Protein Structure, Secondary Rhodopsin/metabolism Sequence Deletion Solutions Staining and Labeling Temperature
Chemicals
Arrestin Mutant Proteins Solutions Rhodopsin
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Kim Miyeon
Jules Stein Eye Institute, Department of Ophthalmology, University of California, Los Angeles, CA 90095, USA.
Vishnivetskiy Sergey A
Van Eps Ned
Alexander Nathan S
Cleghorn Whitney M
Zhan Xuanzhi
Hanson Susan M
Morizumi Takefumi
Ernst Oliver P
Meiler Jens
Gurevich Vsevolod V
Hubbell Wayne L
References (62)
62 references, click to expand
  1. Structural properties of arrestin studied by chemical modification and circular dichroism.
    Biochemistry. 1992 Apr 28;31(16):3902-6 PMID: 1567843
  2. Silent scaffolds: inhibition OF c-Jun N-terminal kinase 3 activity in cell by dominant-negative arrestin-3 mutant.
    J Biol Chem. 2012 Jun 1;287(23):19653-64 PMID: 22523077
  3. Crystal structure of cone arrestin at 2.3A: evolution of receptor specificity.
    J Mol Biol. 2005 Dec 16;354(5):1069-80 PMID: 16289201
  4. Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes.
    J Biol Chem. 2003 Jun 13;278(24):21655-21662 PMID: 12663652
  5. beta-Arrestin: a protein that regulates beta-adrenergic receptor function.
    Science. 1990 Jun 22;248(4962):1547-50 PMID: 2163110
  6. Conservation of the phosphate-sensitive elements in the arrestin family of proteins.
    J Biol Chem. 2002 Mar 15;277(11):9043-8 PMID: 11782458
  7. Activation of G protein-coupled receptor kinase 1 involves interactions between its N-terminal region and its kinase domain.
    Biochemistry. 2011 Mar 22;50(11):1940-9 PMID: 21265573
  8. De novo high-resolution protein structure determination from sparse spin-labeling EPR data.
    Structure. 2008 Feb;16(2):181-95 PMID: 18275810
  9. Structure of bovine rhodopsin in a trigonal crystal form.
    J Mol Biol. 2004 Nov 5;343(5):1409-38 PMID: 15491621
  10. Transition of arrestin into the active receptor-binding state requires an extended interdomain hinge.
    J Biol Chem. 2002 Nov 15;277(46):43961-7 PMID: 12215448
  11. Mapping molecular flexibility of proteins with site-directed spin labeling: a case study of myoglobin.
    Biochemistry. 2012 Aug 21;51(33):6568-83 PMID: 22809279
  12. Arrestin: mutagenesis, expression, purification, and functional characterization.
    Methods Enzymol. 2000;315:422-37 PMID: 10736718
  13. Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist.
    Nature. 2012 Jan 25;482(7386):547-51 PMID: 22278061
  14. G-protein-coupled receptors: turn-ons and turn-offs.
    Curr Opin Neurobiol. 1998 Jun;8(3):335-44 PMID: 9687355
  15. Arrestin interaction with rhodopsin: conceptual models.
    Cell Biochem Biophys. 2006;46(1):1-15 PMID: 16943619
  16. Robust self-association is a common feature of mammalian visual arrestin-1.
    Biochemistry. 2011 Mar 29;50(12):2235-42 PMID: 21288033
  17. The new face of active receptor bound arrestin attracts new partners.
    Structure. 2003 Sep;11(9):1037-42 PMID: 12962621
  18. Targeted construction of phosphorylation-independent beta-arrestin mutants with constitutive activity in cells.
    J Biol Chem. 1999 Mar 12;274(11):6831-4 PMID: 10066734
  19. RosettaEPR: an integrated tool for protein structure determination from sparse EPR data.
    J Struct Biol. 2011 Mar;173(3):506-14 PMID: 21029778
  20. Structure and function of the visual arrestin oligomer.
    EMBO J. 2007 Mar 21;26(6):1726-36 PMID: 17332750
  21. Dynamics of arrestin-rhodopsin interactions: loop movement is involved in arrestin activation and receptor binding.
    J Biol Chem. 2007 Aug 31;282(35):25560-8 PMID: 17606620
  22. Molecular basis for activation of G protein-coupled receptor kinases.
    EMBO J. 2010 Oct 6;29(19):3249-59 PMID: 20729810
  23. N-terminal and C-terminal domains of arrestin both contribute in binding to rhodopsin.
    Photochem Photobiol. 2007 Mar-Apr;83(2):385-92 PMID: 17132044
  24. Helix formation in arrestin accompanies recognition of photoactivated rhodopsin.
    Biochemistry. 2009 Nov 17;48(45):10733-42 PMID: 19835414
  25. Topographic study of arrestin using differential chemical modifications and hydrogen/deuterium exchange.
    Protein Sci. 1994 Dec;3(12):2428-34 PMID: 7756996
  26. Few residues within an extensive binding interface drive receptor interaction and determine the specificity of arrestin proteins.
    J Biol Chem. 2011 Jul 8;286(27):24288-99 PMID: 21471193
  27. Crystal structure of the human beta2 adrenergic G-protein-coupled receptor.
    Nature. 2007 Nov 15;450(7168):383-7 PMID: 17952055
  28. Each rhodopsin molecule binds its own arrestin.
    Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3125-8 PMID: 17360618
  29. Arrestins: ubiquitous regulators of cellular signaling pathways.
    Genome Biol. 2006;7(9):236 PMID: 17020596
  30. The role of arrestin alpha-helix I in receptor binding.
    J Mol Biol. 2010 Jan 8;395(1):42-54 PMID: 19883657
  31. Custom-designed proteins as novel therapeutic tools? The case of arrestins.
    Expert Rev Mol Med. 2010 Apr 23;12:e13 PMID: 20412604
  32. Mapping the arrestin-receptor interface. Structural elements responsible for receptor specificity of arrestin proteins.
    J Biol Chem. 2004 Jan 9;279(2):1262-8 PMID: 14530255
  33. Distance measurements in the nanometer range by pulse EPR.
    Chemphyschem. 2002 Nov 15;3(11):927-32 PMID: 12503132
  34. Distinct loops in arrestin differentially regulate ligand binding within the GPCR opsin.
    Nat Commun. 2012;3:995 PMID: 22871814
  35. Crystal structure of the β2 adrenergic receptor-Gs protein complex.
    Nature. 2011 Jul 19;477(7366):549-55 PMID: 21772288
  36. Arrestin-1 expression level in rods: balancing functional performance and photoreceptor health.
    Neuroscience. 2011 Feb 3;174:37-49 PMID: 21075174
  37. Elucidation of inositol hexaphosphate and heparin interaction sites and conformational changes in arrestin-1 by solution nuclear magnetic resonance.
    Biochemistry. 2010 Dec 14;49(49):10473-85 PMID: 21050017
  38. Crystal structure of beta-arrestin at 1.9 A: possible mechanism of receptor binding and membrane Translocation.
    Structure. 2001 Sep;9(9):869-80 PMID: 11566136
  39. 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
  40. High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation.
    Proc Natl Acad Sci U S A. 2008 May 27;105(21):7439-44 PMID: 18490656
  41. The surface of visual arrestin that binds to rhodopsin.
    Mol Vis. 2004 Jun 15;10:392-8 PMID: 15215746
  42. Phosphorylated rhodopsin and heparin induce similar conformational changes in arrestin.
    J Biol Chem. 1991 Oct 5;266(28):18649-54 PMID: 1917988
  43. Biochemistry. An ensemble view of allostery.
    Science. 2010 Feb 5;327(5966):653-4 PMID: 20133562
  44. The structural basis of arrestin-mediated regulation of G-protein-coupled receptors.
    Pharmacol Ther. 2006 Jun;110(3):465-502 PMID: 16460808
  45. 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
  46. Monomeric rhodopsin is the minimal functional unit required for arrestin binding.
    J Mol Biol. 2010 Jun 11;399(3):501-11 PMID: 20417217
  47. Arrestin-rhodopsin binding stoichiometry in isolated rod outer segment membranes depends on the percentage of activated receptors.
    J Biol Chem. 2011 Mar 4;286(9):7359-69 PMID: 21169358
  48. The molecular acrobatics of arrestin activation.
    Trends Pharmacol Sci. 2004 Feb;25(2):105-11 PMID: 15102497
  49. The 2.8 A crystal structure of visual arrestin: a model for arrestin's regulation.
    Cell. 1999 Apr 16;97(2):257-69 PMID: 10219246
  50. Crystal structure of arrestin-3 reveals the basis of the difference in receptor binding between two non-visual subtypes.
    J Mol Biol. 2011 Feb 25;406(3):467-78 PMID: 21215759
  51. Flexible nets. The roles of intrinsic disorder in protein interaction networks.
    FEBS J. 2005 Oct;272(20):5129-48 PMID: 16218947
  52. Beta-arrestins and cell signaling.
    Annu Rev Physiol. 2007;69:483-510 PMID: 17305471
  53. Long-range distance determinations in biomacromolecules by EPR spectroscopy.
    Q Rev Biophys. 2007 Feb;40(1):1-53 PMID: 17565764
  54. Arrestins as multi-functional signaling adaptors.
    Handb Exp Pharmacol. 2008;(186):15-37 PMID: 18491047
  55. Arrestin mobilizes signaling proteins to the cytoskeleton and redirects their activity.
    J Mol Biol. 2007 Apr 27;368(2):375-87 PMID: 17359998
  56. Differential interaction of spin-labeled arrestin with inactive and active phosphorhodopsin.
    Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):4900-5 PMID: 16547131
  57. Role of the amino terminus of G protein-coupled receptor kinase 2 in receptor phosphorylation.
    Biochemistry. 2009 Aug 4;48(30):7325-33 PMID: 19715378
  58. Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding.
    J Biol Chem. 2011 Jan 14;286(2):1420-8 PMID: 20966068
  59. Crystal structure of opsin in its G-protein-interacting conformation.
    Nature. 2008 Sep 25;455(7212):497-502 PMID: 18818650
  60. A model for the solution structure of the rod arrestin tetramer.
    Structure. 2008 Jun;16(6):924-34 PMID: 18547524
  61. Visual arrestin binding to rhodopsin. Diverse functional roles of positively charged residues within the phosphorylation-recognition region of arrestin.
    J Biol Chem. 1995 Mar 17;270(11):6010-6 PMID: 7890732
  62. An additional phosphate-binding element in arrestin molecule. Implications for the mechanism of arrestin activation.
    J Biol Chem. 2000 Dec 29;275(52):41049-57 PMID: 11024026
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2012-11-06
Epub
2012-00-22
Pages
18407-12
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3494953
Subset
IM
Grants
NIGMS NIH HHS · T32 GM008320 · United States
NIMH NIH HHS · F31 MH086222 · United States
NIGMS NIH HHS · R01 GM081756 · United States
NEI NIH HHS · P30 EY000331 · United States
NEI NIH HHS · EY011500 · United States
NEI NIH HHS · EY00331 · United States
NEI NIH HHS · R01 EY005216 · United States
NIMH NIH HHS · R01 MH090192 · United States
NIGMS NIH HHS · GM080403 · United States
NIGMS NIH HHS · GM077561 · United States
NEI NIH HHS · R01 EY011500 · United States
NEI NIH HHS · R37 EY005216 · United States
NIGMS NIH HHS · GM081756 · United States
NIGMS NIH HHS · R01 GM080403 · United States
NIMH NIH HHS · MH086222 · United States
NIGMS NIH HHS · R01 GM077561 · United States
NIMH NIH HHS · MH090192 · United States
NEI NIH HHS · EY005216 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com