Molecular mechanism of phosphorylation-dependent arrestin activation

Current Opinion in Structural Biology

Volumn 29, Issue , 2014, Pages 143-151

  Ostermaier, Martin K ^a   Schertler, Gebhard FX ^a,b   Standfuss, Joerg ^a  

^a PAUL SCHERRER INSTITUTE   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PHOSPHATE; RETINA S ANTIGEN; PHOSPHOPEPTIDE; PROTEIN BINDING;

ANTIGEN STRUCTURE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; MOLECULAR DYNAMICS; MUTAGENESIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RECEPTOR BINDING; REVIEW; SPECTROSCOPY; AMINO ACID SEQUENCE; CHEMISTRY; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; ARRESTINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84916601178     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2014.07.006     Document Type: Review

References (68)

1. Venkatakrishnan A.J., Deupi X., Lebon G., Tate C.G., Schertler G.F., Babu M.M. Molecular signatures of G-protein-coupled receptors. Nature 2013, 494:185-194.
2. Gurevich E.V., Tesmer J.J.G., Mushegian A., Gurevich V.V. G protein-coupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol Therap 2012, 133:40-69.
3. Lohse M.J., Hoffmann C. Arrestin interactions with G protein-coupled receptors. Handbook of Experimental Pharmacology 2013, Springer, Berlin Heidelberg, pp. 15-56.
4. Gurevich V.V., Gurevich E.V. Structural determinants of arrestin functions. Prog Mol Biol Transl Sci 2013, 118:57-92.
5. Kuehn H. Light-regulated binding of rhodopsin kinase and other proteins to cattle photoreceptor membranes. Biochemistry 1978, 17:4389-4395.
6. Kühn H., Hall S.W., Wilden U. Light-induced binding of 48-kDa protein to photoreceptor membranes is highly enhanced by phosphorylation of rhodopsin. FEBS Lett 1984, 176:473-478.
7. Gurevich V.V., Benovic J.L. Visual arrestin interaction with rhodopsin. Sequential multisite binding ensures strict selectivity toward light-activated phosphorylated rhodopsin. J Biol Chem 1993, 268:11628-11638.
8. Gurevich V.V., Hanson S.M., Song X., Vishnivetskiy S.A., Gurevich E.V. The functional cycle of visual arrestins in photoreceptor cells. Prog Retin Eye Res 2011, 30:405-430.
9. Shukla A.K., Manglik A., Kruse A.C., Xiao K., Reis R.I., Tseng W.-C., Staus D.P., Hilger D., Uysal S., Huang L.Y., et al. Structure of active β-arrestin-1 bound to a G-protein-coupled receptor phosphopeptide. Nature 2013, doi: 10.1038/nature12120.
10. Hanson S.M., Francis D.J., Vishnivetskiy S.A., Kolobova E.A., Hubbell W.L., Klug C.S., Gurevich V.V. Differential interaction of spin-labeled arrestin with inactive and active phosphorhodopsin. Proc Natl Acad Sci USA 2006, 103:4900-4905.
11. Zhuang T., Chen Q., Cho M.-K., Vishnivetskiy S.A., Iverson T.M., Gurevich V.V., Sanders C.R. Involvement of distinct arrestin-1 elements in binding to different functional forms of rhodopsin. Proc Natl Acad Sci USA 2013, 110:942-947.
12. Vishnivetskiy S.A., Francis D., Van Eps N., Kim M., Hanson S.M., Klug C.S., Hubbell W.L., Gurevich V.V. The role of arrestin α-helix i in receptor binding. J Mol Biol 2010, 395:42-54.
13. Palczewski K., Pulvermüller A., Buczyłko J., Hofmann K.P. Phosphorylated rhodopsin and heparin induce similar conformational changes in arrestin. J Biol Chem 1991, 266:18649-18654.
14. Hirsch J.A., Schubert C., Gurevich V.V., Sigler P.B. The 2.8 A crystal structure of visual arrestin: a model for arrestin's regulation. Cell 1999, 97:257-269.
15. Han M., Gurevich V.V., Vishnivetskiy S.A., Sigler P.B., Schubert C. Crystal structure of beta-arrestin at 1.9 A: possible mechanism of receptor binding and membrane translocation. Structure/Fold Design 2001, 9:869-880.
16. Zhan X., Gimenez L.E., Gurevich V.V., Spiller B.W. Crystal structure of arrestin-3 reveals the basis of the difference in receptor binding between two non-visual subtypes. J Mol Biol 2011, 406:467-478.
17. Sutton R.B., Vishnivetskiy S.A., Robert J., Hanson S.M., Raman D., Knox B.E., Kono M., Navarro J., Gurevich V.V. Crystal structure of cone arrestin at 2.3Å: evolution of receptor specificity. J Mol Biol 2005, 354:1069-1080.
18. Kim Y.J., Hofmann K.P., Ernst O.P., Scheerer P., Choe H.-W., Sommer M.E. Crystal structure of pre-activated arrestin p44. Nature 2013, 497:142-146.
19. Kim M., Vishnivetskiy S.A., Van Eps N., Alexander N.S., Cleghorn W.M., Zhan X., Hanson S.M., Morizumi T., Ernst O.P., Meiler J., et al. Conformation of receptor-bound visual arrestin. Proc Natl Acad Sci USA 2012, 109:18407-18412.
20. Sinha A., Brunette A.M.J., Fay J.F., Schafer C.T., Farrens D.L. Rhodopsin TM6 can contact two separate and distinct sites on arrestin: evidence for structural plasticity and multiple docking modes in arrestin-rhodopsin binding. Biochemistry 2014, doi: 10.1021/bi401534y.
21. Sun D., Ostermaier M.K., Heydenreich F.M., Mayer D., Jaussi R., Standfuss J., Veprintsev D.B. AAscan, PCRdesign and MutantChecker: a suite of programs for primer design and sequence analysis for high-throughput scanning mutagenesis. PLoS One 2013, 8:e78878.
22. Ostermaier M.K., Peterhans C., Jaussi R., Deupi X., Standfuss J. Functional map of arrestin-1 at single amino acid resolution. Proc Natl Acad Sci USA 2014, 111:1825-1830.
23. Vishnivetskiy S.A., Schubert C., Climaco G.C., Gurevich Y.V., Velez M.G., Gurevich VV: An additional phosphate-binding element in arrestin molecule. Implications for the mechanism of arrestin activation. J Biol Chem 2000, 275:41049-41057.
24. Gurevich V.V., Benovic J.L. Cell-free expression of visual arrestin. Truncation mutagenesis identifies multiple domains involved in rhodopsin interaction. J Biol Chem 1992, 267:21919-21923.
25. Palczewski K., Buczyłko J., Imami N.R., McDowell J.H., Hargrave P.A. Role of the carboxyl-terminal region of arrestin in binding to phosphorylated rhodopsin. J Biol Chem 1991, 266:15334-15339.
26. Nobles K.N., Guan Z., Xiao K., Oas T.G., Lefkowitz R.J. The active conformation of beta-arrestin1: direct evidence for the phosphate sensor in the N-domain and conformational differences in the active states of beta-arrestins1 and -2. J Biol Chem 2007, 282:21370-21381.
27. Granzin J., Cousin A., Weirauch M., Schlesinger R., Büldt G., Batra-Safferling R. Crystal structure of p44, a constitutively active splice variant of visual arrestin. J Mol Biol 2012, 416:611-618.
28. Palczewski K., Buczylko J., Ohguro H., Annan R.S., Carr S.A., Crabb J.W., Kaplan M.W., Johnson R.S., Walsh K.A. Characterization of a truncated form of arrestin isolated from bovine rod outer segments. Protein Sci 1994, 3:314-324.
29. Feuerstein S.E., Pulvermüller A., Hartmann R., Granzin J., Stoldt M., Henklein P., Ernst O.P., Heck M., Willbold D., Koenig B.W. Helix formation in arrestin accompanies recognition of photoactivated rhodopsin. Biochemistry 2009, 48:10733-10742.
30. Sommer M.E., Farrens D.L., McDowell J.H., Weber L.A., Smith W.C. Dynamics of arrestin-rhodopsin interactions: loop movement is involved in arrestin activation and receptor binding. J Biol Chem 2007, 282:25560-25568.
31. Vishnivetskiy S.A., Hosey M.M., Benovic J.L., Gurevich V.V. Mapping the arrestin-receptor interface. Structural elements responsible for receptor specificity of arrestin proteins. J Biol Chem 2004, 279:1262-1268.
32. Puig J., Arendt A., Tomson F.L., Abdulaeva G., Miller R., Hargrave P.A., McDowell J.H. Synthetic phosphopeptide from rhodopsin sequence induces retinal arrestin binding to photoactivated unphosphorylated rhodopsin. FEBS Lett 1995, 362:185-188.
33. McDowell J.H., Robinson P.R., Miller R.L., Brannock M.T., Arendt A., Smith W.C., Hargrave P.A. Activation of arrestin: requirement of phosphorylation as the negative charge on residues in synthetic peptides from the carboxyl-terminal region of rhodopsin. Invest Ophthalmol Vis Sci 2001, 42:1439-1443.
34. Hanson S.M., Gurevich V.V. The differential engagement of arrestin surface charges by the various functional forms of the receptor. J Biol Chem 2006, 281:3458-3462.
35. Ascano M., Robinson P.R. Differential phosphorylation of the rhodopsin cytoplasmic tail mediates the binding of arrestin and its splice variant, p44 †. Biochemistry 2006, 45:2398-2407.
36. Vishnivetskiy S.A., Raman D., Wei J., Kennedy M.J., Hurley J.B., Gurevich V.V. Regulation of arrestin binding by rhodopsin phosphorylation level. J Biol Chem 2007, 282:32075-32083.
37. Mendez A., Burns M.E., Roca A., Lem J., Wu L.W., Simon M.I., Baylor D.A., Chen J. Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 2000, 28:153-164.
38. Wisler J.W., Xiao K., Thomsen A.R., Lefkowitz R.J. Recent developments in biased agonism. Curr Opin Cell Biol 2014, 27:18-24.
39. Shukla A.K., Xiao K., Lefkowitz R.J. Emerging paradigms of β-arrestin-dependent seven transmembrane receptor signaling. Trends Biochem Sci 2011, 36:457-469.
40. Reiter E., Ahn S., Shukla A.K., Lefkowitz R.J. Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors. Annu Rev Pharmacol Toxicol 2012, 52:179-197.
41. Shukla A.K., Violin J.D., Whalen E.J., Gesty-Palmer D., Shenoy S.K., Lefkowitz R.J. Distinct conformational changes in beta-arrestin report biased agonism at seven-transmembrane receptors. Proc Natl Acad Sci USA 2008, 105:9988-9993.
42. Oakley R.H., Laporte S.A., Holt J.A., Barak L.S., Caron M.G. Association of beta-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J Biol Chem 1999, 274:32248-32257.
43. Liu J.J., Horst R., Katritch V., Stevens R.C., Wuthrich K. Biased signaling pathways in beta2-adrenergic receptor characterized by 19F-NMR. Science 2012, 335:1106-1110.
44. Vishnivetskiy S.A., Ostermaier M.K., Singhal A., Panneels V., Homan K.T., Glukhova A., Sligar S.G., Tesmer J.J.G., Schertler G.F.X., Standfuss J., et al. Constitutively active rhodopsin mutants causing night blindness are effectively phosphorylated by GRKs but differ in arrestin-1 binding. Cell Signal 2013, 25:2155-2162.
45. Ren X.-R., Reiter E., Ahn S., Kim J., Chen W., Lefkowitz R.J. Different G protein-coupled receptor kinases govern G protein and beta-arrestin-mediated signaling of V2 vasopressin receptor. Proc Natl Acad Sci USA 2005, 102:1448-1453.
46. Oakley R.H., Laporte S.A., Holt J.A., Barak L.S., Caron M.G. Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-beta-arrestin complexes after receptor endocytosis*. J Biol Chem 2001, 276:19452-19460.
47. Kirchberg K., Kim T.-Y., Möller M., Skegro D., Dasara Raju G., Granzin J., Büldt G., Schlesinger R., Alexiev U. Conformational dynamics of helix 8 in the GPCR rhodopsin controls arrestin activation in the desensitization process. Proc Natl Acad Sci USA 2011, 108:18690-18695.
48. Zhuang T., Vishnivetskiy S.A., Gurevich V.V., Sanders C.R. Elucidation of inositol hexaphosphate and heparin interaction sites and conformational changes in arrestin-1 by solution nuclear magnetic resonance. Biochemistry 2010, 49:10473-10485.
49. Kruse A.C., Ring A.M., Manglik A., Hu J., Hu K., Eitel K., Hübner H., Pardon E., Valant C., Sexton P.M., et al. Activation and allosteric modulation of a muscarinic acetylcholine receptor. Nature 2014, 504:101-106.
50. Singhal A., Ostermaier M.K., Vishnivetskiy S.A., Panneels V., Homan K.T., Tesmer J.J.G., Veprintsev D., Deupi X., Gurevich V.V., Schertler G.F.X., et al. Insights into congenital stationary night blindness based on the structure of G90D rhodopsin. EMBO Rep 2013, 14:520-526.
51. Rasmussen S.G.F., Choi H.-J., Fung J.J., Pardon E., Casarosa P., Chae P.S., DeVree B.T., Rosenbaum D.M., Thian F.S., Kobilka T.S., et al. Structure of a nanobody-stabilized active state of the beta2 adrenoceptor. Nature 2012, 469:175-180.
52. Deupi X., Edwards P., Singhal A., Nickle B., Oprian D., Schertler G., Standfuss J. Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II. Proc Natl Acad Sci USA 2012, 109:119-124.
53. Rasmussen S.G.F., DeVree B.T., Zou Y., Kruse A.C., Chung K.Y., Kobilka T.S., Thian F.S., Chae P.S., Pardon E., Calinski D., et al. Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 2011, 477:549-555.
54. Choe H.-W., Kim Y.J., Park J.H., Morizumi T., Pai E.F., Krauß N., Hofmann K.P., Scheerer P., Ernst O.P. Crystal structure of metarhodopsin II. Nature 2011, 471:651-655.
55. Standfuss J., Edwards P.C., D'Antona A., Fransen M., Xie G., Oprian D.D., Schertler G.F.X. The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 2011, 471:656-660.
56. Rao V.R., Cohen G.B., Oprian D.D. Rhodopsin mutation G90D and a molecular mechanism for congenital night blindness. Nature 1994, 367:639-642.
57. Hopkins A.L., Groom C.R. The druggable genome. Nat Rev Drug Discov 2002, 1:727-730.
58. Schubert C., Hirsch J.A., Gurevich V.V., Engelman D.M., Sigler P.B., Fleming K.G. Visual arrestin activity may be regulated by self-association. J Biol Chem 1999, 274:21186-21190.
59. Imamoto Y., Tamura C., Kamikubo H., Kataoka M. Concentration-dependent tetramerization of bovine visual arrestin. Biophys J 2003, 85:1186-1195.
60. Hanson S.M., Dawson E.S., Francis D.J., Van Eps N., Klug C.S., Hubbell W.L., Meiler J., Gurevich V.V. A model for the solution structure of the rod arrestin tetramer. Structure 2008, 16:924-934.
61. Sommer M.E., Hofmann K.P., Heck M. Distinct loops in arrestin differentially regulate ligand binding within the GPCR opsin. Nat Commun 2012, 3:995.
62. Sommer M.E., Hofmann K.P., Heck M. Arrestin-rhodopsin binding stoichiometry in isolated rod outer segment membranes depends on the percentage of activated receptors. J Biol Chem 2011, 286:7359-7369.
63. Kang D.S., Kern R.C., Puthenveedu M.A., Zastrow von M., Williams J.C., Benovic J.L. Structure of an arrestin2-clathrin complex reveals a novel clathrin binding domain that modulates receptor trafficking. J Biol Chem 2009, 284:29860-29872.
64. Milano S.K., Kim Y.M., Stefano F.P., Benovic J.L., Brenner C. Nonvisual arrestin oligomerization and cellular localization are regulated by inositol hexakisphosphate binding. J Biol Chem 2006, 281:9812-9823.
65. Milano S.K., Pace H.C., Kim Y.-M., Brenner C., Benovic J.L. Scaffolding functions of arrestin-2 revealed by crystal structure and mutagenesis †. Biochemistry 2002, 41:3321-3328.
66. Granzin J., Wilden U., Choe H.W., Labahn J., Krafft B., Büldt G. X-ray crystal structure of arrestin from bovine rod outer segments. Nature 1998, 391:918-921.
67. Szczepek M., Beyrière F., Hofmann K.P., Elgeti M., Kazmin R., Rose A., Bartl F.J., Stetten von D., Heck M., Sommer M.E., et al. Crystal structure of a common GPCR-binding interface for G protein and arrestin. Nat Commun 2014, 5:4801.
68. Shukla A.K., Westfield G.H., Xiao K., Reis R.I., Huang L.-Y., Tripathi-Shukla P., Qian J., Li S., Blanc A., Oleskie A.N., et al. Visualization of arrestin recruitment by a G-protein-coupled receptor. Nature 2014, 512:218-222.