Catalytic activation of β-Arrestin by GPCRs

Nature

Volumn 557, Issue 7705, 2018, Pages 381-386

  Eichel, Kelsie ^a   Jullié, Damien ^a   Barsi Rhyne, Benjamin ^a   Latorraca, Naomi R ^b,c,d   Masureel, Matthieu ^d   Sibarita, Jean Baptiste ^e,f   Dror, Ron O ^b,c,d   Von Zastrow, Mark ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c Stanford University   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e CNRS   (France)

^f UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN; CLATHRIN; G PROTEIN COUPLED RECEPTOR; PHOSPHATIDYLINOSITIDE; SCAFFOLD PROTEIN; PHOSPHATIDYLINOSITOL;

CATALYSIS; CELL COMPONENT; MEMBRANE; PROTEIN; STOICHIOMETRY;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL MEMBRANE; CELL MIGRATION; CHEMICAL STRUCTURE; CLATHRIN COATED ENDOCYTIC STRUCTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISSOCIATION; ENDOSOME; ENZYME REGULATION; HEK293 CELL LINE; HUMAN; LIVE CELL IMAGING; MAPK SIGNALING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; ANIMAL; BIOCATALYSIS; CHEMISTRY; CHLOROCEBUS AETHIOPS; CV-1 CELL LINE; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; BETA-ARRESTINS; BIOCATALYSIS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; HEK293 CELLS; HUMANS; PHOSPHATIDYLINOSITOLS; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED;

EID: 85046902824     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/s41586-018-0079-1     Document Type: Article

References (41)

1. Rosenbaum, D. M., Rasmussen, S. G. F. & Kobilka, B. K. The structure and function of G-protein-coupled receptors. Nature 459, 356-363 (2009).
2. Lohse, M. J., Benovic, J. L., Codina, J., Caron, M. G. & Lefkowitz, R. J. beta- Arrestin: A protein that regulates beta-Adrenergic receptor function. Science 248, 1547-1550 (1990).
3. Kang, D. S., Tian, X. & Benovic, J. L. Role of β-Arrestins and arrestin domaincontaining proteins in G protein-coupled receptor trafficking. Curr. Opin. Cell Biol. 27, 63-71 (2014).
4. Pierce, K. L., Premont, R. T. & Lefkowitz, R. J. Seven-Transmembrane receptors. Nat. Rev. Mol. Cell Biol. 3, 639-650 (2002).
5. Gurevich, E. V. & Gurevich, V. V. Arrestins: ubiquitous regulators of cellular signaling pathways. Genome Biol. 7, 236 (2006).
6. Lohse, M. J. & Hoffmann, C. Arrestins-Pharmacology and Therapeutic Potential (Springer, Berlin, Heidelberg, 2014).
7. Shukla, A. K., Xiao, K. & Lefkowitz, R. J. Emerging paradigms of β-Arrestindependent seven transmembrane receptor signaling. Trends Biochem. Sci. 36, 457-469 (2011).
8. Gurevich, V. V. & Gurevich, E. V. The structural basis of arrestin-mediated regulation of G-protein-coupled receptors. Pharmacol. Ther. 110, 465-502 (2006).
9. Nuber, S. et al. β-Arrestin biosensors reveal a rapid, receptor-dependent activation/deactivation cycle. Nature 531, 661-664 (2016).
10. Cahill, T. J. III et al. Distinct conformations of GPCR-β-Arrestin complexes mediate desensitization, signaling, and endocytosis. Proc. Natl Acad. Sci. USA 114, 2562-2567 (2017).
11. Lee, M.-H. et al. The conformational signature of β-Arrestin2 predicts its trafficking and signalling functions. Nature 531, 665-668 (2016).
12. Kumari, P. et al. Functional competence of a partially engaged GPCR-β-Arrestin complex. Nat. Commun. 7, 13416 (2016).
13. Kumari, P. et al. Core engagement with β-Arrestin is dispensable for agonistinduced vasopressin receptor endocytosis and ERK activation. Mol. Biol. Cell 28, 1003-1010 (2017).
14. Branco, A. F. et al. Isoproterenol cytotoxicity is dependent on the differentiation state of the cardiomyoblast H9c2 cell line. Cardiovasc. Toxicol. 11, 191-203 (2011).
15. Puthenveedu, M. A. & von Zastrow, M. Cargo regulates clathrin-coated pit dynamics. Cell 127, 113-124 (2006).
16. Santini, F., Gaidarov, I. & Keen, J. H. G protein-coupled receptor/arrestin3 modulation of the endocytic machinery. J. Cell Biol. 156, 665-676 (2002).
17. Barak, L. S., Ferguson, S. S., Zhang, J. & Caron, M. G. A β-Arrestin/green fluorescent protein biosensor for detecting G protein-coupled receptor activation. J. Biol. Chem. 272, 27497-27500 (1997).
18. Eichel, K., Jullié, D. & von Zastrow, M. β-Arrestin drives MAP kinase signalling from clathrin-coated structures after GPCR dissociation. Nat. Cell Biol. 18, 303-310 (2016).
19. Mondin, M. et al. Neurexin-neuroligin adhesions capture surface-diffusing AMPA receptors through PSD-95 scaffolds. J. Neurosci. 31, 13500-13515 (2011).
20. Shukla, A. K. et al. Structure of active β-Arrestin-1 bound to a G-protein-coupled receptor phosphopeptide. Nature 497, 137-141 (2013).
21. Shukla, A. K. et al. Visualization of arrestin recruitment by a G-protein-coupled receptor. Nature 512, 218-222 (2014).
22. Xiao, K., Shenoy, S. K., Nobles, K. & Lefkowitz, R. J. Activation-dependent conformational changes in β-Arrestin 2. J. Biol. Chem. 279, 55744-55753 (2004).
23. Nobles, K. N., Guan, Z., Xiao, K., Oas, T. G. & Lefkowitz, R. J. The active conformation of β-Arrestin1: direct evidence for the phosphate sensor in the N-domain and conformational differences in the active states of β-Arrestins1 and -2. J. Biol. Chem. 282, 21370-21381 (2007).
24. McCorvy, J. D. et al. Structure-inspired design of β-Arrestin-biased ligands for aminergic GPCRs. Nat. Chem. Biol. 14, 126-134 (2018).
25. Gimenez, L. E., Babilon, S., Wanka, L., Beck-Sickinger, A. G. & Gurevich, V. V. Mutations in arrestin-3 differentially affect binding to neuropeptide Y receptor subtypes. Cell. Signal. 26, 1523-1531 (2014).
26. Violin, J. D., Ren, X.-R. & Lefkowitz, R. J. G-protein-coupled receptor kinase specificity for β-Arrestin recruitment to the β2-Adrenergic receptor revealed by fluorescence resonance energy transfer. J. Biol. Chem. 281, 20577-20588 (2006).
27. Peterson, S. M. et al. Elucidation of G-protein and β-Arrestin functional selectivity at the dopamine D2 receptor. Proc. Natl Acad. Sci. USA 112, 7097-7102 (2015).
28. Gurevich, V. V. The selectivity of visual arrestin for light-Activated phosphorhodopsin is controlled by multiple nonredundant mechanisms. J. Biol. Chem. 273, 15501-15506 (1998).
29. Scheerer, P. & Sommer, M. E. Structural mechanism of arrestin activation. Curr. Opin. Struct. Biol. 45, 160-169 (2017).
30. Chen, Q. et al. Structural basis of arrestin-3 activation and signaling. Nat. Commun. 8, 1427 (2017).
31. Gaidarov, I., Krupnick, J. G., Falck, J. R., Benovic, J. L. & Keen, J. H. Arrestin function in G protein-coupled receptor endocytosis requires phosphoinositide binding. EMBO J. 18, 871-881 (1999).
32. Lally, C. C. M., Bauer, B., Selent, J. & Sommer, M. E. C-edge loops of arrestin function as a membrane anchor. Nat. Commun. 8, 14258 (2017).
33. Goodman, O. B. Jr et al. β-Arrestin acts as a clathrin adaptor in endocytosis of the β2-Adrenergic receptor. Nature 383, 447-450 (1996).
34. Laporte, S. A., Oakley, R. H., Holt, J. A., Barak, L. S. & Caron, M. G. The interaction of β-Arrestin with the AP-2 adaptor is required for the clustering of β 2-Adrenergic receptor into clathrin-coated pits. J. Biol. Chem. 275, 23120- 23126 (2000).
35. Oakley, R. H., Laporte, S. A., Holt, J. A., Barak, L. S. & Caron, M. G. Association of β-Arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J. Biol. Chem. 274, 32248-32257 (1999).
36. Santos, M. de S., Naal, R. M. Z. G., Baird, B. & Holowka, D. Inhibitors of PI(4, 5)P2 synthesis reveal dynamic regulation of IgE receptor signaling by phosphoinositides in RBL mast cells. Mol. Pharmacol. 83, 793-804 (2013).
37. Manley, S. et al. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5, 155-157 (2008).
38. Hammond, G. R. V., Sim, Y., Lagnado, L. & Irvine, R. F. Reversible binding and rapid diffusion of proteins in complex with inositol lipids serves to coordinate free movement with spatial information. J. Cell Biol. 184, 297-308 (2009).
39. Liu, A. P., Loerke, D., Schmid, S. L. & Danuser, G. Global and local regulation of clathrin-coated pit dynamics detected on patterned substrates. Biophys. J. 97, 1038-1047 (2009).
40. Latorraca, N. R. et al. Molecular mechanism of GPCR-mediated arrestin activation. Nature https://doi.org/10.1038/s41586-018-0077-3 (2018).
41. O'Hayre, M. et al. Genetic evidence that β-Arrestins are dispensable for the initiation of β2-Adrenergic receptor signaling to ERK. Sci. Signal. 10, eaal3395 (2017).