Structural mechanism of arrestin activation

Current Opinion in Structural Biology

Volumn 45, Issue , 2017, Pages 160-169

  Scheerer, Patrick ^a,b   Sommer, Martha E ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Group Protein X ray Crystallography Signal Transduction   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; RETINA S ANTIGEN;

ANTIGEN FUNCTION; ANTIGEN STRUCTURE; C EDGE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; FINGER LOOP; HYDROGEN BOND; INTERDOMAIN ROTATION; POLAR CORE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; STRUCTURE ANALYSIS; ANIMAL; CHEMISTRY; HUMAN; METABOLISM; PROTEIN DOMAIN; ROTATION;

ANIMALS; ARRESTIN; HUMANS; PROTEIN DOMAINS; ROTATION;

EID: 85020299127     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2017.05.001     Document Type: Review

References (48)

1. Scheerer, P., Park, J.H., Hildebrand, P.W., Kim, Y.J., Krauss, N., Choe, H.W., Hofmann, K.P., Ernst, O.P., Crystal structure of opsin in its G-protein-interacting conformation. Nature 455 (2008), 497–502.
2. 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 471 (2011), 651–655.
3. Manglik, A., Kim, T.H., Masureel, M., Altenbach, C., Yang, Z., Hilger, D., Lerch, M.T., Kobilka, T.S., Thian, F.S., Hubbell, W.L., et al. Structural insights into the dynamic process of beta2-adrenergic receptor signaling. Cell 161 (2015), 1101–1111.
4. Rasmussen, S.G., 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 beta2 adrenergic receptor-Gs protein complex. Nature 477 (2011), 549–555.
5. Carpenter, B., Nehme, R., Warne, T., Leslie, A.G., Tate, C.G., Structure of the adenosine A(2A) receptor bound to an engineered G protein. Nature 536 (2016), 104–107.
6. Wilden, U., Hall, S.W., Kuhn, H., 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. 83 (1986), 1174–1178.
7. Lohse, M.J., Hoffmann, C., Arrestin interactions with G protein-coupled receptors. Handb. Exp. Pharmacol. 219 (2014), 15–56.
8. Gurevich, V.V., Gurevich, E., Extensive shape shifting underlies functional versatility of arrestins. Curr. Opin. Cell Biol. 27 (2014), 1–9.
9. Shukla, A.K., Xiao, K., Lefkowitz, R.J., Emerging paradigms of beta-arrestin-dependent seven transmembrane receptor signaling. Trends Biochem. Sci. 36 (2011), 457–469.
10. Shenoy, S.K., Lefkowitz, R.J., beta-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol. Sci. 32 (2011), 521–533.
11. Yang, F., Yu, X., Liu, C., Qu, C.X., Gong, Z., Liu, H.D., Li, F.H., Wang, H.M., He, D.F., Yi, F., et al. Phospho-selective mechanisms of arrestin conformations and functions revealed by unnatural amino acid incorporation and (19)F-NMR. Nat. Commun., 6, 2015, 8202 Groundbreaking biophysical study directly showing how distinct conformational changes in arrestin-2 are elicited by phosphopetides with different phosphorylation patterns.
12. Nuber, S., Zabel, U., Lorenz, K., Nuber, A., Milligan, G., Tobin, A.B., Lohse, M.J., Hoffmann, C., beta-Arrestin biosensors reveal a rapid, receptor-dependent activation/deactivation cycle. Nature 531 (2016), 661–664.
13. Lee, M.H., Appleton, K.M., Strungs, E.G., Kwon, J.Y., Morinelli, T.A., Peterson, Y.K., Laporte, S.A., Luttrell, L.M., The conformational signature of beta-arrestin2 predicts its trafficking and signalling functions. Nature 531 (2016), 665–668.
14. Reiter, E., Ahn, S., Shukla, A.K., Lefkowitz, R.J., Molecular mechanism of beta-arrestin-biased agonism at seven-transmembrane receptors. Annu. Rev. Pharmacol. Toxicol. 52 (2012), 179–197.
15. Smith, J.S., Rajagopal, S., The beta-arrestins: multifunctional regulators of G protein-coupled receptors. J. Biol. Chem. 291 (2016), 8969–8977.
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. 406 (2011), 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 2.3 A: evolution of receptor specificity. J. Mol. Biol. 354 (2005), 1069–1080.
18. 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 9 (2001), 869–880.
19. 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 97 (1999), 257–269.
20. Granzin, J., Wilden, U., Choe, H.W., Labahn, J., Krafft, B., Buldt, G., X-ray crystal structure of arrestin from bovine rod outer segments. Nature 391 (1998), 918–921.
21. Feuerstein, S.E., Pulvermuller, 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 48 (2009), 10733–10742.
22. Sommer, M.E., Smith, W.C., Farrens, D.L., Dynamics of arrestin–rhodopsin interactions: arrestin and retinal release are directly linked events. J. Biol. Chem. 280 (2005), 6861–6871.
23. 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. U. S. A. 103 (2006), 4900–4905.
24. Szczepek, M., Beyriere, F., Hofmann, K.P., Elgeti, M., Kazmin, R., Rose, A., Bartl, F.J., von Stetten, D., Heck, M., Sommer, M.E., et al. Crystal structure of a common GPCR-binding interface for G protein and arrestin. Nat. Commun., 5, 2014, 4801 Landmark crystal structure showing a peptide analogue of the arrestin finger loop bound within the cytoplasmic crevice of an active GPCR. The paper shows how arrestin and G protein share this binding binding site.
25. Vishnivetskiy, S.A., Baameur, F., Findley, K.R., Gurevich, V.V., Critical role of central 139-loop in stability and binding selectivity of arrestin-1. J. Biol. Chem. 288 (2013), 11741–11750.
26. Hanson, S.M., Gurevich, V.V., The differential engagement of arrestin surface charges by the various functional forms of the receptor. J. Biol. Chem. 281 (2006), 3458–3462.
27. Vishnivetskiy, S.A., Paz, C.L., Schubert, C., Hirsch, J.A., Sigler, P.B., Gurevich, V.V., How does arrestin respond to the phosphorylated state of rhodopsin?. J. Biol. Chem. 274 (1999), 11451–11454.
28. Vishnivetskiy, S.A., Schubert, C., Climaco, G.C., Gurevich, Y.V., Velez, M.G., Gurevich, V.V., An additional phosphate-binding element in arrestin molecule: implications for the mechanism of arrestin activation. J. Biol. Chem. 275 (2000), 41049–41057.
29. Kuhn, 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. 176 (1984), 473–478.
30. Schröder, K., Pulvermüller, A., Hofmann, K.P., Arrestin and its splice variant Arr1-370A (p44). Mechanism and biological role of their interaction with rhodopsin. J. Biol. Chem. 277 (2002), 43987–43996.
31. Kirchberg, K., Kim, T.Y., Moller, M., Skegro, D., Dasara Raju, G., Granzin, J., Buldt, 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. U. S. A. 108 (2011), 18690–18695.
32. Kumari, P., Srivastava, A., Banerjee, R., Ghosh, E., Gupta, P., Ranjan, R., Chen, X., Gupta, B., Gupta, C., Jaiman, D., et al. Functional competence of a partially engaged GPCR-beta-arrestin complex. Nat. Commun., 7, 2016, 13416.
33. Palczewski, K., Pulvermüller, A., Buczylko, J., Hofmann, K.P., Phosphorylated rhodopsin and heparin induce similar conformational changes in arrestin. J. Biol. Chem. 266 (1991), 18649–18654.
34. Gurevich, V.V., Benovic, J.L., Visual arrestin binding to rhodopsin. Diverse functional roles of positively charged residues within the phosphorylation-recognition region of arrestin. J. Biol. Chem. 270 (1995), 6010–6016.
35. 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 497 (2013), 142–146 Crystal structure of C-terminally truncated, pre-active arrestin. The structure displays hallmarks of arrestin activation.
36. 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. 416 (2012), 611–618.
37. 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 beta-arrestin-1 bound to a G-protein-coupled receptor phosphopeptide. Nature 497 (2013), 137–141 Crystal structure of arrestin-2 bound to a phosphopeptide analogue of a phosphorylated receptor C-terminus. The structure displays hallmarks of arrestin activation and how receptor-attached phosphates engage specific residues within the arrestin N-domain.
38. Borshchevskiy, V., Buldt, G., Structural biology: active arrestin proteins crystallized. Nature 497 (2013), 45–46.
39. Granzin, J., Stadler, A., Cousin, A., Schlesinger, R., Batra-Safferling, R., Structural evidence for the role of polar core residue Arg175 in arrestin activation. Sci. Rep., 5, 2015, 15808.
40. Kang, Y., Zhou, X.E., Gao, X., He, Y., Liu, W., Ishchenko, A., Barty, A., White, T.A., Yefanov, O., Han, G.W., et al. Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523 (2015), 561–567 Landmark crystal structure of an arrestin-GPCR complex that gives a first indication of how conformational changes associated with arrestin activation facilitate binding of the active receptor.
41. Lally, C.C., Bauer, B., Selent, J., Sommer, M.E., C-edge loops of arrestin function as a membrane anchor. Nat. Commun., 8, 2017, 14258 This study combined molecular dynamics simulations and site-directed fluorescence experiments to show how the arrestin C-edge engages the membrane when arrestin interacts with a phosphorylated GPCR.
42. Nobles, K.N., Xiao, K., Ahn, S., Shukla, A.K., Lam, C.M., Rajagopal, S., Strachan, R.T., Huang, T.Y., Bressler, E.A., Hara, M.R., et al. Distinct phosphorylation sites on the beta(2)-adrenergic receptor establish a barcode that encodes differential functions of beta-arrestin. Sci. Signal., 4, 2011, ra51.
43. Shenoy, S.K., Modi, A.S., Shukla, A.K., Xiao, K., Berthouze, M., Ahn, S., Wilkinson, K.D., Miller, W.E., Lefkowitz, R.J., Beta-arrestin-dependent signaling and trafficking of 7-transmembrane receptors is reciprocally regulated by the deubiquitinase USP33 and the E3 ligase Mdm2. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 6650–6655.
44. Peterhans, C., Lally, C.C., Ostermaier, M.K., Sommer, M.E., Standfuss, J., Functional map of arrestin binding to phosphorylated opsin with and without agonist. Sci. Rep., 6, 2016, 28686.
45. 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. U. S. A. 109 (2012), 18407–18412.
46. 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 512 (2014), 218–222 This negative stain-electron microsopy study identifies different modes of arrestin binding to a phosphorylated GPCR.
47. Thomsen, A.R., Plouffe, B., Cahill, T.J. 3rd, Shukla, A.K., Tarrasch, J.T., Dosey, A.M., Kahsai, A.W., Strachan, R.T., Pani, B., Mahoney, J.P., et al. GPCR-G protein-beta-arrestin super-complex mediates sustained G protein signaling. Cell 166 (2016), 907–919 This negative stain-electron microsopy study gives evidence that G protein and arrestin could simultaneously engage an active GPCR.
48. Kang, D.S., Kern, R.C., Puthenveedu, M.A., von Zastrow, 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. 284 (2009), 29860–29872.