Functional map of arrestin binding to phosphorylated opsin, with and without agonist

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Peterhans, Christian ^a   Lally, Ciara C M ^b   Ostermaier, Martin K ^b   Sommer, Martha E ^b   Standfuss, Jörg ^a  

^a PAUL SCHERRER INSTITUTE   (Switzerland)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

OPSIN; PROTEIN BINDING; RETINA S ANTIGEN;

ANIMAL; BOVINE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN DOMAIN;

ANIMALS; ARRESTIN; CATTLE; MODELS, MOLECULAR; MUTATION; OPSINS; PROTEIN BINDING; PROTEIN DOMAINS;

EID: 84976535182     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28686     Document Type: Article

References (58)

1. Fredriksson, R., Lagerström, M. C., Lundin, L.-G. & Schiöth, H. B. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 63, 1256-1272 (2003).
2. Lefkowitz, R. J. Seven transmembrane receptors: something old, something new. Acta Physiol (Oxf) 190, 9-19 (2007).
3. Schöneberg, T. T. et al. Mutant G-protein-coupled receptors as a cause of human diseases. Pharmacol. Ther. 104, 173-206 (2004).
4. Gurevich, E. V. & Gurevich, V. V. Arrestins: ubiquitous regulators of cellular signaling pathways. Genome Biol. 7, 236 (2006).
5. Nobles, K. N. et al. Distinct phosphorylation sites on the β (2)-Adrenergic receptor establish a barcode that encodes differential functions of β-Arrestin. Sci Signal 4, ra51 (2011).
6. Yang, F. et al. Phospho-selective mechanisms of arrestin conformations and functions revealed by unnatural amino acid incorporation and (19)F-NMR. Nat Commun 6, 8202 (2015).
7. Violin, J. D. & Lefkowitz, R. J. Beta-Arrestin-biased ligands at seven-Transmembrane receptors. Trends Pharmacol. Sci. 28, 416-422 (2007).
8. Ostermaier, M. K., Schertler, G. F. & Standfuss, J. Molecular mechanism of phosphorylation-dependent arrestin activation. Curr. Opin. Struct. Biol. 29C, 143-151 (2014).
9. 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 111, 1825-1830 (2014).
10. Schröder, K., Pulvermöller, 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, 43987-43996 (2002).
11. 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 30, 405-430 (2011).
12. Shukla, A. K. et al. Structure of active β-Arrestin-1 bound to a G-protein-coupled receptor phosphopeptide. Nature 497, 137-141 (2013).
13. Kim, Y. J. et al. Crystal structure of pre-Activated arrestin p44. Nature 497, 142-146 (2013).
14. Kang, Y. et al. Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523, 561-567 (2015).
15. Arshavsky, V. Y. et al. Regulation of transducin GTPase activity in bovine rod outer segments. J. Biol. Chem. 269, 19882-19887 (1994).
16. Köhn, H. Light-regulated binding of rhodopsin kinase and other proteins to cattle photoreceptor membranes. Biochemistry 17, 4389-4395 (1978).
17. Mendez, A. et al. Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 28, 153-164 (2000).
18. Vishnivetskiy, S. A. et al. Regulation of arrestin binding by rhodopsin phosphorylation level. J. Biol. Chem. 282, 32075-32083 (2007).
19. Hofmann, K. P., Pulvermöller, A., Buczylko, J., Van Hooser, P. & Palczewski, K. The role of arrestin and retinoids in the regeneration pathway of rhodopsin. J. Biol. Chem. 267, 15701-15706 (1992).
20. Zhuang, T. et al. Involvement of distinct arrestin-1 elements in binding to different functional forms of rhodopsin. Proc. Natl. Acad. Sci. USA 110, 942-947 (2013).
21. Lee, K. A., Nawrot, M., Garwin, G. G., Saari, J. C. & Hurley, J. B. Relationships among visual cycle retinoids, rhodopsin phosphorylation, and phototransduction in mouse eyes during light and dark adaptation. Biochemistry 49, 2454-2463 (2010).
22. Sommer, M. E., Hofmann, K. P. & Heck, M. Distinct loops in arrestin differentially regulate ligand binding within the GPCR opsin. Nat Commun 3, 995 (2012).
23. Sommer, M. E. & Farrens, D. L. Arrestin can act as a regulator of rhodopsin photochemistry. Vision Res 46, 4532-4546 (2006).
24. Sommer, M. E. et al. Structure-based biophysical analysis of the interaction of rhodopsin with G protein and arrestin. Methods in Enzymology 556, 563-608 (2015).
25. Chatterjee, D. et al. Influence of Arrestin on the Photodecay of Bovine Rhodopsin. Angew Chem Int Ed Engl 54, 13555-13560 (2015).
26. Fuchs, S. S. et al. A homozygous 1-base pair deletion in the arrestin gene is a frequent cause of Oguchi disease in Japanese. Nat. Genet. 10, 360-362 (1995).
27. Vishnivetskiy, S. A. et al. Constitutively active rhodopsin mutants causing night blindness are effectively phosphorylated by GRKs but differ in arrestin-1 binding. Cell Signal 25, 2155-2162 (2013).
28. Singhal, A. et al. Insights into congenital stationary night blindness based on the structure of G90D rhodopsin. EMBO Reports 14, 520-526 (2013).
29. Chuang, J.-Z., Vega, C., Jun, W. & Sung, C.-H. Structural and functional impairment of endocytic pathways by retinitis pigmentosa mutant rhodopsin-Arrestin complexes. J. Clin. Invest. 114, 131-140 (2004).
30. Ostermaier, M. K. et al. AAscan, PCRdesign and MutantChecker: A Suite of Programs for Primer Design and Sequence Analysis for High-Throughput Scanning Mutagenesis. PLoS ONE 8, e78878 (2013).
31. 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. 268, 11628-11638 (1993).
32. Hirsch, J. A., Schubert, C., Gurevich, V. V. & Sigler, P. B. The 2.8 A crystal structure of visual arrestin: A model for arrestins regulation. Cell 97, 257-269 (1999).
33. Krupnick, J. G. J., Gurevich, V. V. V., Schepers, T. T., Hamm, H. E. H. & Benovic, J. L. J. Arrestin-rhodopsin interaction. Multi-site binding delineated by peptide inhibition. J. Biol. Chem. 269, 3226-3232 (1994).
34. Vishnivetskiy, S. A. et al. An additional phosphate-binding element in arrestin molecule. Implications for the mechanism of arrestin activation. J. Biol. Chem. 275, 41049-41057 (2000).
35. Szczepek, M. et al. Crystal structure of a common GPCR-binding interface for G protein and arrestin. Nat Commun 5, 4801 (2014).
36. Hanson, S. M. et al. Differential interaction of spin-labeled arrestin with inactive and active phosphorhodopsin. Proc. Natl. Acad. Sci. USA 103, 4900-4905 (2006).
37. Sommer, M. E., Smith, W. C. & Farrens, D. L. Dynamics of arrestin-rhodopsin interactions: Acidic phospholipids enable binding of arrestin to purified rhodopsin in detergent. J. Biol. Chem. 281, 9407-9417 (2006).
38. 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. 282, 25560-25568 (2007).
39. Feuerstein, S. E. et al. Helix formation in arrestin accompanies recognition of photoactivated rhodopsin. Biochemistry 48, 10733-10742 (2009).
40. Sommer, M. E., Hofmann, K. P. & Heck, M. M. Arrestin-rhodopsin binding stoichiometry in isolated rod outer segment membranes depends on the percentage of activated receptors. J. Biol. Chem. 286, 7359-7369 (2011).
41. 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, 3458-3462 (2006).
42. Duarte, J. M., Srebniak, A., Schärer, M. A. & Capitani, G. Protein interface classification by evolutionary analysis. BMC Bioinformatics 13, 334 (2012).
43. Vogel, R. & Siebert, F. Conformations of the active and inactive states of opsin. J. Biol. Chem. 276, 38487-38493 (2001).
44. Park, J. H., Scheerer, P., Hofmann, K. P., Choe, H.-W. & Ernst, O. P. Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454, 183-187 (2008).
45. Deupi, X. et al. Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II. Proc. Natl. Acad. Sci. USA 109, 119-124 (2012).
46. Choe, H.-W. et al. Crystal structure of metarhodopsin II. Nature 471, 651-655 (2011).
47. Standfuss, J. et al. The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471, 656-660 (2011).
48. Gibson, S., Parkes, J. & Liebman, P. Phosphorylation stabilizes the active conformation of rhodopsin. Biochemistry 37, 13910 (1998).
49. 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, 6010-6016 (1995).
50. Palczewski, K., Buczylko, 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. 266, 15334-15339 (1991).
51. Granzin, J. et al. Crystal structure of p44, a constitutively active splice variant of visual arrestin. J. Mol. Biol. 416, 611-618 (2012).
52. 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, 15808 (2015).
53. Pulvermöller, A. et al. Functional differences in the interaction of arrestin and its splice variant, p44, with rhodopsin. Biochemistry 36, 9253-9260 (1997).
54. Granzin, J. et al. X-ray crystal structure of arrestin from bovine rod outer segments. nature 391, 918-921 (1998).
55. 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, 869-880 (2001).
56. Sutton, R. B. et al. Crystal structure of cone arrestin at 2.3A: evolution of receptor specificity. J. Mol. Biol. 354, 1069-1080 (2005).
57. Kim, M. et al. Conformation of receptor-bound visual arrestin. Proc. Natl. Acad. Sci. USA 109, 18407-18412 (2012).
58. 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, 6861-6871 (2005).