Functional competence of a partially engaged GPCR-β-arrestin complex

Nature Communications

Volumn 7, Issue , 2016, Pages

  Kumari, Punita ^a   Srivastava, Ashish ^a   Banerjee, Ramanuj ^a   Ghosh, Eshan ^a   Gupta, Pragya ^a   Ranjan, Ravi ^a   Chen, Xin ^b   Gupta, Bhagyashri ^a   Gupta, Charu ^a   Jaiman, Deepika ^a   Shukla, Arun K ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY KANPUR   (India)

^b CHANGZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN 1; BETA ARRESTIN 2; CARVEDILOL; G PROTEIN COUPLED RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; BETA ARRESTIN; CARBAZOLE DERIVATIVE; PROPANOLAMINE DERIVATIVE; PROTEIN BINDING;

CELLS AND CELL COMPONENTS; DRUG; ENZYME; ENZYME ACTIVITY; LIGAND; PROTEIN;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME BINDING; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE SPECTROSCOPY; IN VITRO STUDY; PROTEIN EXPRESSION; CHEMISTRY; DRUG EFFECT; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR DOCKING; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

BETA-ARRESTINS; CARBAZOLES; ENDOCYTOSIS; HEK293 CELLS; HUMANS; MOLECULAR DOCKING SIMULATION; PHOSPHORYLATION; PROPANOLAMINES; PROTEIN BINDING; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84994890792     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13416     Document Type: Article

References (69)

1. Bjarnadottir, T. K., et al. Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse. Genomics 88, 263-273 (2006
2. Bockaert, J., & Pin, J. P. Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J. 18, 1723-1729 (1999
3. DeWire, S. M., Ahn, S., Lefkowitz, R. J., & Shenoy, S. K. Beta-arrestins and cell signaling. Annu. Rev. Physiol. 69, 483-510 (2007
4. Ghosh, E., Kumari, P., Jaiman, D., & Shukla, A. K. Methodological advances: the unsung heroes of the GPCR structural revolution. Nat. Rev. Mol. Cell Biol. 16, 69-81 (2015
5. 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
6. 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
7. Kim, M., et al. Conformation of receptor-bound visual arrestin. Proc. Natl Acad. Sci. USA 109, 18407-18412 (2012
8. 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
9. Szczepek, M., et al. Crystal structure of a common GPCR-binding interface for G protein and arrestin. Nat. Commun. 5, 4801 (2014
10. Kang, Y., et al. Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523, 561-567 (2015
11. Shukla, A. K., et al. Visualization of arrestin recruitment by a G-protein-coupled receptor. Nature 512, 218-222 (2014
12. Xiao, K., et al. Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc. Natl Acad. Sci. USA 107, 15299-15304 (2010
13. Xiao, K., et al. Functional specialization of beta-arrestin interactions revealed by proteomic analysis. Proc. Natl Acad. Sci. USA 104, 12011-12016 (2007
14. Srivastava, A., Gupta, B., Gupta, C., & Shukla, A. K. Emerging functional divergence of beta-arrestin isoforms in GPCR function. Trends Endocrinol. Metab. 26, 628-642 (2015
15. Gurevich, V. V., & Gurevich, E. V. Structural determinants of arrestin functions. Prog. Mol. Biol. Transl. Sci. 118, 57-92 (2013
16. Ostermaier, M. K., Schertler, G. F., & Standfuss, J. Molecular mechanism of phosphorylation-dependent arrestin activation. Curr. Opin. Struct. Biol. 29, 143-151 (2014
17. Gurevich, V. V., & Gurevich, E. V. The molecular acrobatics of arrestin activation. Trends Pharmacol. Sci. 25, 105-111 (2004
18. Oakley, R. H., Laporte, S. A., Holt, J. A., Caron, M. G., & Barak, L. S. Differential affinities of visual arrestin, beta arrestin1, and beta arrestin2 for G proteincoupled receptors delineate two major classes of receptors. J. Biol. Chem. 275, 17201-17210 (2000
19. 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
20. 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
21. Feuerstein, S. E., et al. Helix formation in arrestin accompanies recognition of photoactivated rhodopsin. Biochemistry 48, 10733-10742 (2009
22. Sinha, A., Jones Brunette, A. M., Fay, J. F., Schafer, C. T., & Farrens, D. L. Rhodopsin TM6 can interact with two separate and distinct sites on arrestin: evidence for structural plasticity and multiple docking modes in arrestin-rhodopsin binding. Biochemistry 53, 3294-3307 (2014
23. Azzi, M., et al. Beta-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors. Proc. Natl Acad. Sci. USA 100, 11406-11411 (2003
24. Ahn, S., Shenoy, S. K., Wei, H., & Lefkowitz, R. J. Differential kinetic and spatial patterns of beta-arrestin and G protein-mediated ERK activation by the angiotensin II receptor. J. Biol. Chem. 279, 35518-35525 (2004
25. Shenoy, S. K., et al. beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor. J. Biol. Chem. 281, 1261-1273 (2006
26. Wei, H., et al. Independent beta-arrestin 2 and G protein-mediated pathways for angiotensin II activation of extracellular signal-regulated kinases 1 and 2. Proc. Natl Acad. Sci. USA 100, 10782-10787 (2003
27. Coffa, S., et al. The effect of arrestin conformation on the recruitment of c-Raf1, MEK1, and ERK1/2 activation. PLoS ONE 6, e28723 (2011
28. Luttrell, L. M., et al. Activation and targeting of extracellular signal-regulated kinases by beta-arrestin scaffolds. Proc. Natl Acad. Sci. USA 98, 2449-2454 (2001
29. Luttrell, L. M., & Lefkowitz, R. J. The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals. J. Cell Sci. 115, 455-465 (2002
30. Lefkowitz, R. J., & Shenoy, S. K. Transduction of receptor signals by beta-arrestins. Science 308, 512-517 (2005
31. Shukla, A. K., et al. Structure of active beta-arrestin-1 bound to a G-protein-coupled receptor phosphopeptide. Nature 497, 137-141 (2013
32. Xiao, K., Shenoy, S. K., Nobles, K., & Lefkowitz, R. J. Activation-dependent conformational changes in {beta}-arrestin 2. J. Biol. Chem. 279, 55744-55753 (2004
33. 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. 282, 21370-21381 (2007
34. Ring, A. M., et al. Adrenaline-activated structure of beta2-adrenoceptor stabilized by an engineered nanobody. Nature 502, 575-579 (2013
35. Goodman, Jr O. B., et al. Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature 383, 447-450 (1996
36. Goodman, Jr O. B., Krupnick, J. G., Gurevich, V. V., Benovic, J. L., & Keen, J. H. Arrestin/clathrin interaction. Localization of the arrestin binding locus to the clathrin terminal domain. J. Biol. Chem. 272, 15017-15022 (1997
37. Krupnick, J. G., Goodman, O. B. Jr, Keen, J. H., & Benovic, J. L. Arrestin/clathrin interaction. Localization of the clathrin binding domain of nonvisual arrestins to the carboxy terminus. J. Biol. Chem. 272, 15011-15016 (1997
38. Kim, K. M., & Caron, M. G. Complementary roles of the DRY motif and C-terminus tail of GPCRS for G protein coupling and beta-arrestin interaction. Biochem. Biophys. Res. Commun. 366, 42-47 (2008
39. Marion, S., Oakley, R. H., Kim, K. M., Caron, M. G., & Barak, L. S. A betaarrestin binding determinant common to the second intracellular loops of rhodopsin family G protein-coupled receptors. J. Biol. Chem. 281, 2932-2938 (2006
40. Shukla, A. K., Xiao, K., & Lefkowitz, R. J. Emerging paradigms of beta-arrestindependent seven transmembrane receptor signaling. Trends Biochem. Sci. 36, 457-469 (2011
41. Violin, J. D., & Lefkowitz, R. J. Beta-arrestin-biased ligands at seventransmembrane receptors. Trends Pharmacol. Sci. 28, 416-422 (2007
42. Whalen, E. J., Rajagopal, S., & Lefkowitz, R. J. Therapeutic potential of beta-arrestin-and G protein-biased agonists. Trends Mol. Med. 17, 126-139 (2011
43. Wisler, J. W., et al. A unique mechanism of beta-blocker action: carvedilol stimulates beta-arrestin signaling. Proc. Natl Acad. Sci. USA 104, 16657-16662 (2007
44. Pierce, K. L., & Lefkowitz, R. J. Classical and new roles of beta-arrestins in the regulation of G-protein-coupled receptors. Nat. Rev. Neurosci. 2, 727-733 (2001
45. Pierce, K. L., Premont, R. T., & Lefkowitz, R. J. Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 3, 639-650 (2002
46. Rasmussen, S. G., et al. Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 477, 549-555 (2011
47. Scheerer, P., et al. Crystal structure of opsin in its G-protein-interacting conformation. Nature 455, 497-502 (2008
48. Kim, Y. J., et al. Crystal structure of pre-activated arrestin p44. Nature 497, 142-146 (2013
49. Nuber, S., et al. beta-Arrestin biosensors reveal a rapid, receptor-dependent activation/deactivation cycle. Nature 531, 661-664 (2016
50. Lee, M. H., et al. The conformational signature of beta-arrestin2 predicts its trafficking and signalling functions. Nature 531, 665-668 (2016
51. Ranjan, R., Gupta, P., & Shukla, A. K. GPCR Signaling: beta-arrestins Kiss and Remember. Curr. Biol. 26, R285-R288 (2016
52. Eichel, K., Jullie, D., & von Zastrow, M. beta-Arrestin drives MAP kinase signalling from clathrin-coated structures after GPCR dissociation. Nat. Cell Biol. 18, 303-310 (2016
53. Goodman, O. B. Jr, et al. Role of arrestins in G-protein-coupled receptor endocytosis. Adv. Pharmacol. 42, 429-433 (1998
54. Zhan, X., Kook, S., Gurevich, E. V., & Gurevich, V. V. Arrestin-dependent activation of JNK family kinases. Handb. Exp. Pharmacol. 219, 259-280 (2014
55. McDonald, P. H., et al. Beta-arrestin 2: a receptor-regulated MAPK scaffold for the activation of JNK3. Science 290, 1574-1577 (2000
56. Luttrell, L. M., et al. Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes. Science 283, 655-661 (1999
57. Beaulieu, J. M., et al. An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122, 261-273 (2005
58. Shenoy, S. K., & Lefkowitz, R. J. beta-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol. Sci. 32, 521-533 (2011
59. Shukla, A. K., et al. Arresting a transient receptor potential (TRP) channel: beta-arrestin 1 mediates ubiquitination and functional down-regulation of TRPV4. J. Biol. Chem. 285, 30115-30125 (2010
60. Marchese, A., & Trejo, J. Ubiquitin-dependent regulation of G protein-coupled receptor trafficking and signaling. Cell. Signal. 25, 707-716 (2013
61. Kenakin, T., & Christopoulos, A. Signalling bias in new drug discovery: detection, quantification and therapeutic impact. Nat. Rev. Drug Discov. 12, 205-216 (2013
62. Onaran, H. O., Rajagopal, S., & Costa, T. What is biased efficacy? defining the relationship between intrinsic efficacy and free energy coupling. Trends Pharmacol. Sci. 35, 639-647 (2014
63. Shukla, A. K., Singh, G., & Ghosh, E. Emerging structural insights into biased GPCR signaling. Trends Biochem. Sci. 39, 594-602 (2014
64. Rajagopal, S., Rajagopal, K., & Lefkowitz, R. J. Teaching old receptors new tricks: biasing seven-transmembrane receptors. Nat. Rev. Drug Discov. 9, 373-386 (2010
65. Shukla, A. K., et al. Distinct conformational changes in beta-arrestin report biased agonism at seven-transmembrane receptors. Proc. Natl Acad. Sci. USA 105, 9988-9993 (2008
66. 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
67. Liu, J. J., Horst, R., Katritch, V., Stevens, R. C., & Wuthrich, K. Biased signaling pathways in beta2-adrenergic receptor characterized by 19F-NMR. Science 335, 1106-1110 (2012
68. Kahsai, A. W., et al. Multiple ligand-specific conformations of the beta2-adrenergic receptor. Nat. Chem. Biol. 7, 692-700 (2011
69. Paduch, M., et al. Generating conformation-specific synthetic antibodies to trap proteins in selected functional states. Methods 60, 3-14 (2013