Crystal structure of pre-activated arrestin p44

Nature

Volumn 497, Issue 7447, 2013, Pages 142-146

  Kim, Yong Ju ^a   Hofmann, Klaus Peter ^a,b   Ernst, Oliver P ^c   Scheerer, Patrick ^a   Choe, Hui Woog ^a,d   Sommer, Martha E ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY OF TORONTO   (Canada)

^d Chonbuk National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARRESTIN 1; RETINA S ANTIGEN; UNCLASSIFIED DRUG;

CHEMICAL BONDING; CRYSTAL STRUCTURE; HYDROGEN; PHOSPHATE; PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVATION; ESCHERICHIA COLI; FLUORESCENCE SPECTROSCOPY; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RECEPTOR BINDING; VISUAL SYSTEM;

ALTERNATIVE SPLICING; ANIMALS; ARRESTINS; CATTLE; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR WEIGHT; PROTEIN CONFORMATION; PROTEIN ISOFORMS; ROTATION; SEQUENCE DELETION; STATIC ELECTRICITY;

BOVINAE;

EID: 84877581910     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12133     Document Type: Article

References (47)

1. 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. USA 83, 1174-1178 (1986).
2. Lohse, M. J., Benovic, J. L., Codina, J., Caron, M. G. & Lefkowitz, R. J. b-Arrestin: a protein that regulates b-adrenergic receptor function. Science 248, 1547-1550 (1990).
3. Shukla, A. K., Xiao, K. & Lefkowitz, R. J. Emerging paradigms of b-arrestindependent seven transmembrane receptor signaling. Trends Biochem. Sci. 36, 457-469 (2011).
4. 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).
5. Granzin, J. et al. X-ray crystal structure of arrestin frombovine rod outer segments. Nature 391, 918-921 (1998).
6. Hirsch, J. A., Schubert, C., Gurevich, V. V.& Sigler, P. B. The 2.8A? crystal structure of visual arrestin: a model for arrestin's regulation. Cell 97, 257-269 (1999).
7. Feuerstein, S. E. et al. Helix formation in arrestin accompanies recognition of photoactivated rhodopsin. Biochemistry 48, 10733-10742 (2009).
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. 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).
10. Kim, M. et al. Conformation of receptor-bound visual arrestin. Proc. Natl Acad. Sci. USA 109, 18407-18412 (2012).
11. 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. http://dx.doi.org/10.1074/jbc.M113.450031 jbcM113.450031 (2013).
12. 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).
13. Schroer, K., Pulvermuller, 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).
14. Kirchberg, K. et al. Conformational dynamics of helix 8 in the GPCR rhodopsin controls arrestin activation in the desensitization process. Proc. Natl Acad. Sci. USA 108, 18690-18695 (2011).
15. Schleicher, A., Kun, H.& Hofmann, K. P. Kinetics, binding constant, and activation energy of the 48-kDa protein-rhodopsin complex by extra-metarhodopsin II. Biochemistry 28, 1770-1775 (1989).
16. Smith, W. C. et al. A splice variant of arrestin. Molecular cloning and localization in bovine retina. J. Biol. Chem. 269, 15407-15410 (1994).
17. Pulvermu?ller, A. et al. Functional differences in the interaction of arrestin and its splice variant, p44, with rhodopsin. Biochemistry 36, 9253-9260 (1997).
18. Scheerer, P. et al. Crystal structure of opsin in its G-protein-interacting conformation. Nature 455, 497-502 (2008).
19. Choe, H. W. et al. Crystal structure of metarhodopsin II. Nature 471, 651-655 (2011).
20. Gurevich, V. V. & Benovic, J. L. Visual arrestin binding to rhodopsin. Diverse functional roles of positively charged residues within the phosphorylationrecognition region of arrestin. J. Biol. Chem. 270, 6010-6016 (1995).
21. Vishnivetskiy, S. A. et al. An additional phosphate-binding element in arrestin molecule. Implications for themechanismof arrestin activation. J. Biol. Chem. 275, 41049-41057 (2000).
22. 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).
23. Granzin, J. et al. Crystal structure of p44, a constitutively active splice variant of visual arrestin. J. Mol. Biol. 416, 611-618 (2012).
24. Mansoor, S. E., Dewitt, M. A. & Farrens, D. L. Distance mapping in proteins using fluorescence spectroscopy: the tryptophan-induced quenching (TrIQ) method. Biochemistry 49, 9722-9731 (2010).
25. Sommer, M. E., Hofmann, K. P. & Heck, M. Distinct loops in arrestin differentially regulate ligand binding within the GPCR opsin. Nature Commun. 3, 995 (2012).
26. 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. 286, 7359-7369 (2011).
27. 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 (2012).
28. Gurevich, V. V. et al. Arrestin interactions with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, b2-adrenergic, and m2 muscarinic cholinergic receptors. J. Biol. Chem. 270, 720-731 (1995).
29. Azarian, S. M., King, A. J., Hallett, M. A. & Williams, D. S. Selective proteolysis of arrestin by calpain. Molecular characteristics and its effect on rhodopsin dephosphorylation. J. Biol. Chem. 270, 24375-24384 (1995).
30. 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).
31. Kabsch, W. Xds. Acta Crystallogr. D 66, 125-132 (2010).
32. Evans,P.Scaling andassessment of dataquality. Acta Crystallogr.D62,72- 82(2006).
33. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
34. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658-674 (2007).
35. Vagin, A. A. et al. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D 60, 2184-2195 (2004).
36. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
37. Winn, M. D., Isupov, M. N. & Murshudov, G. N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D 57, 122-133 (2001).
38. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
39. Vaguine, A. A., Richelle, J. & Wodak, S. J. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr. D 55, 191-205 (1999).
40. Laskowski, R. A., Moss, D. S. & Thornton, J. M. Procheck: a program to check the stereo chemical quality of protein structures. J. Appl. Cryst. 26, 283-291 (1993).
41. Hooft, R. W., Vriend, G., Sander, C. & Abola, E. E. Errors in protein structures. Nature 381, 272 (1996).
42. McDonald, I. K.&Thornton, J. M.Satisfyinghydrogenbonding potential in proteins. J. Mol. Biol. 238, 777-793 (1994).
43. Wallace, A. C., Laskowski, R. A. & Thornton, J. M. LIGPLOT: a program to generate schematic diagramsof protein-ligandinteractions. ProteinEng. 8,127-134(1995).
44. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98, 10037-10041 (2001).
45. Poornam, G. P.,Matsumoto, A., Ishida, H. & Hayward, S. Amethod for the analysis of domainmovements in large biomolecular complexes. Proteins 76, 201-212 (2009).
46. DeLano, W. L. The PyMOL Molecular Graphics System (DeLano Scientific, 2002).
47. 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).