Engineering visual arrestin-1 with special functional characteristics

Journal of Biological Chemistry

Volumn 288, Issue 5, 2013, Pages 3394-3405

  Vishnivetskiy, Sergey A ^a   Chen, Qiuyan ^a   Palazzo, Maria C ^a   Brooks, Evan K ^b   Altenbach, Christian ^b   Iverson, Tina M ^a   Hubbell, Wayne L ^b   Gurevich, Vsevolod V ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SURFACE; FUNCTIONAL CHARACTERISTICS; THERAPEUTIC POTENTIALS;

OLIGOMERS;

RHODIUM;

BETA ARRESTIN 1; BINDING PROTEIN; RHODOPSIN;

ARTICLE; GENE MUTATION; IN VIVO STUDY; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROPENSITY SCORE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; RECEPTOR BINDING; WILD TYPE;

ANIMALS; ARRESTINS; EYE; HEK293 CELLS; HUMANS; MICE; MODELS, MOLECULAR; MUTANT PROTEINS; MUTATION; PHOSPHATES; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; RHODOPSIN; STATIC ELECTRICITY; TEMPERATURE;

EID: 84873323643     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.445437     Document Type: Article

References (70)

1. Baylor, D. A., Lamb, T. D., and Yau, K. W. (1979) Responses of retinal rods to single photons. J. Physiol. 288, 613-634
2. Rieke, F., and Baylor, D. A. (1998) Origin of reproducibility in the responses of retinal rods to single photons. Biophys. J. 75, 1836-1857
3. Caruso, G., Bisegna, P., Lenoci, L., Andreucci, D., Gurevich, V. V., Hamm, H. E., and Di Benedetto, E. (2010) Kinetics of rhodopsin deactivation and its role in regulating recovery and reproducibility of rod photoresponse. PLoS Comput. Biol. 6, e1001031
4. Caruso, G., Bisegna, P., Andreucci, D., Lenoci, L., Gurevich, V. V., Hamm, H. E., and Di Benedetto, E. (2011) Identification of key factors that reduce the variability of the single photon response. Proc. Natl. Acad. Sci. U. S. A. 108, 7804-7807
5. Burns, M. E., and Baylor, D. A. (2001) Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu. Rev. Neurosci. 24, 779-805
6. Krispel, C. M., Chen, D., Melling, N., Chen, Y. J., Martemyanov, K. A., Quillinan, N., Arshavsky, V. Y., Wensel, T. G., Chen, C. K., and Burns, M. E. (2006) RGS expression rate-limits recovery of rod photoresponses. Neuron 51, 409-416
7. Gross, O. P., and Burns, M. E. (2010) Control of rhodopsin active lifetime by arrestin-1 expression in mammalian rods. J. Neurosci. 30, 3450-3457
8. Fuchs, S., Nakazawa, M., Maw, M., Tamai, M., Oguchi, Y., and Gal, A. (1995) A homozygous 1-base pair deletion in the arrestin gene is a frequent cause of Oguchi disease in Japanese. Nat. Genet. 10, 360-362
9. Yamamoto, S., Sippel, K. C., Berson, E. L., and Dryja, T. P. (1997) Defects in the rhodopsin kinase gene in the Oguchi form of stationary night blindness. Nat. Genet. 15, 175-178
10. Apfelstedt-Sylla, E., Kunisch, M., Horn, M., Ruther, K., Gerding, H., Gal, A., and Zrenner, E. (1993) Ocular findings in a family with autosomal dominant retinitis pigmentosa and a frameshift mutation altering the carboxyl terminal sequence of rhodopsin. Br. J. Ophthalmol. 77, 495-501
11. Song, X., Vishnivetskiy, S. A., Gross, O. P., Emelianoff, K., Mendez, A., Chen, J., Gurevich, E. V., Burns, M. E., and Gurevich, V. V. (2009) Enhanced arrestin facilitates recovery and protects rods lacking rhodopsin phosphorylation. Curr. Biol. 19, 700-705
12. Gurevich, V. V., and Gurevich, E. V. (2010) Custom-designed proteins as novel therapeutic tools? The case of arrestins. Expert. Rev. Mol. Med. 12, e13
13. Hanson, S. M., Gurevich, E. V., Vishnivetskiy, S. A., Ahmed, M. R., Song, X., and Gurevich, V. V. (2007) Each rhodopsin molecule binds its own arrestin. Proc. Natl. Acad. Sci. U. S. A. 104, 3125-3128
14. Song, X., Vishnivetskiy, S. A., Seo, J., Chen, J., Gurevich, E. V., and Gurevich, V. V. (2011) Arrestin-1 expression level in rods. Balancing functional performance and photoreceptor health. Neuroscience 174, 37-49
15. Strissel, K. J., Sokolov, M., Trieu, L. H., and Arshavsky, V. Y. (2006) Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. J. Neurosci. 26, 1146-1153
16. Schubert, C., Hirsch, J. A., Gurevich, V. V., Engelman, D. M., Sigler, P. B., and Fleming, K. G. (1999) Visual arrestin activity may be regulated by self-association. J. Biol. Chem. 274, 21186-21190
17. Imamoto, Y., Tamura, C., Kamikubo, H., and Kataoka, M. (2003) Concentrationdependent tetramerization of bovine visual arrestin. Biophys. J. 85, 1186-1195
18. Hanson, S. M., Van Eps, N., Francis, D. J., Altenbach, C., Vishnivetskiy, S. A., Arshavsky, V. Y., Klug, C. S., Hubbell, W. L., and Gurevich, V. V. (2007) Structure and function of the visual arrestin oligomer. EMBO J. 26, 1726-1736
19. Hanson, S. M., Dawson, E. S., Francis, D. J., Van Eps, N., Klug, C. S., Hubbell, W. L., Meiler, J., and Gurevich, V. V. (2008) A model for the solution structure of the rod arrestin tetramer. Structure 16, 924-934
20. Gurevich, V. V., Hanson, S. M., Song, X., Vishnivetskiy, S. A., and Gurevich, E. V. (2011) The functional cycle of visual arrestins in photoreceptor cells. Prog. Retin. Eye Res. 30, 405-430
21. Gurevich, V. V. (1996) Use of bacteriophage RNA polymerase in RNA synthesis. Methods Enzymol. 275, 382-397
22. Elowitz, M., and Lim, W. A. (2010) Build life to understand it. Nature 468, 889-890
23. Gimenez, L. E., Kook, S., Vishnivetskiy, S. A., Ahmed, M. R., Gurevich, E. V., and Gurevich, V. V. (2012) Role of receptor-attached phosphates in binding of visual and non-visual arrestins to G protein-coupled receptors. J. Biol. Chem. 287, 9028-9040
24. Song, X., Raman, D., Gurevich, E. V., Vishnivetskiy, S. A., and Gurevich, V. V. (2006) Visual and both non-visual arrestins in their "inactive" conformation bind JNK3 and Mdm2 and relocalize them from the nucleus to the cytoplasm. J. Biol. Chem. 281, 21491-21499
25. Song, X., Gurevich, E. V., and Gurevich, V. V. (2007) Cone arrestin binding to JNK3 and Mdm2. Conformational preference and localization of interaction sites. J. Neurochem. 103, 1053-1062
26. Vishnivetskiy, S. A., Raman, D., Wei, J., Kennedy, M. J., Hurley, J. B., and Gurevich, V. V. (2007) Regulation of arrestin binding by rhodopsin phosphorylation level. J. Biol. Chem. 282, 32075-32083
27. Vishnivetskiy, S. A., Gimenez, L. E., Francis, D. J., Hanson, S. M., Hubbell, W. L., Klug, C. S., and Gurevich, V. V. (2011) Few residues within an extensive binding interface drive receptor interaction and determine the specificity of arrestin proteins. J. Biol. Chem. 286, 24288-24299
28. Breitman, M., Kook, S., Gimenez, L. E., Lizama, B. N., Palazzo, M. C., Gurevich, E. V., and Gurevich, V. V. (2012) Silent scaffolds. Inhibition of c-Jun. N-terminal kinase 3 activity in cell by dominant-negative arrestin-3 mutant. J. Biol. Chem. 287, 19653-19664
29. Gurevich, V. V., and Benovic, J. L. (2000) Arrestin. Mutagenesis, expression, purification, and functional characterization. Methods Enzymol. 315, 422-437
30. Hanson, S. M., Vishnivetskiy, S. A., Hubbell, W. L., and Gurevich, V. V. (2008) Opposing effects of inositol hexakisphosphate on rod arrestin and arrestin2 self-association. Biochemistry 47, 1070-1075
31. Gurevich, V. V. (1998) The selectivity of visual arrestin for light-activated phosphorhodopsin is controlled by multiple nonredundant mechanisms. J. Biol. Chem. 273, 15501-15506
32. Vishnivetskiy, S. A., Schubert, C., Climaco, G. C., Gurevich, Y. V., Velez, M.-G., and Gurevich, V. V. (2000) An additional phosphate-binding element in arrestin molecule. Implications for the mechanism of arrestin activation. J. Biol. Chem. 275, 41049-41057
33. Sutton, R. B., Vishnivetskiy, S. A., Robert, J., Hanson, S. M., Raman, D., Knox, B. E., Kono, M., Navarro, J., and Gurevich, V. V. (2005) Crystal structure of cone arrestin at 2.3 Å. Evolution of receptor specificity. J. Mol. Biol. 354, 1069-1080
34. Gurevich, V. V., and Benovic, J. L. (1995) 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
35. Nair, K. S., Hanson, S. M., Mendez, A., Gurevich, E. V., Kennedy, M. J., Shestopalov, V. I., Vishnivetskiy, S. A., Chen, J., Hurley, J. B., Gurevich, V. V., and Slepak, V. Z. (2005) Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by proteinprotein interactions. Neuron 46, 555-567
36. Hanson, S. M., and Gurevich, V. V. (2006) The differential engagement of arrestin surface charges by the various functional forms of the receptor. J. Biol. Chem. 281, 3458-3462
37. Hirsch, J. A., Schubert, C., Gurevich, V. V., and Sigler, P. B. (1999) The 2.8 Åcrystal structure of visual arrestin. Amodel for arrestin's regulation. Cell 97, 257-269
38. Vishnivetskiy, S. A., Paz, C. L., Schubert, C., Hirsch, J. A., Sigler, P. B., and Gurevich, V. V. (1999) How does arrestin respond to the phosphorylated state of rhodopsin? J. Biol. Chem. 274, 11451-11454
39. Vishnivetskiy, S. A., Hirsch, J. A., Velez, M.-G., Gurevich, Y. V., and Gurevich, V. V. (2002) Transition of arrestin into the active receptor-binding state requires an extended interdomain hinge. J. Biol. Chem. 277, 43961-43968
40. Gurevich, V. V., and Benovic, J. L. (1992) Cell-free expression of visual arrestin. Truncation mutagenesis identifies multiple domains involved in rhodopsin interaction. J. Biol. Chem. 267, 21919-21923
41. Gurevich, V. V., and Benovic, J. L. (1993) Visual arrestin interaction with rhodopsin. Sequential multisite binding ensures strict selectivity toward light-activated phosphorylated rhodopsin. J. Biol. Chem. 268, 11628-11638
42. Gurevich, V. V., and Benovic, J. L. (1997) Mechanism of phosphorylationrecognition by visual arrestin and the transition of arrestin into a high affinity binding state. Mol. Pharmacol. 51, 161-169
43. Gurevich, V. V., Dion, S. B., Onorato, J. J., Ptasienski, J., Kim, C. M., Sterne-Marr, R., Hosey, M. M., and Benovic, J. L. (1995) Arrestin interactions with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, β2-adrenergic, and m2 muscarinic cholinergic receptors. J. Biol. Chem. 270, s731
44. Gurevich, V. V., and Gurevich, E. V. (2006) The structural basis of arrestinmediated regulation of G-protein-coupled receptors. Pharmacol. Ther. 110, 465-502
45. Gurevich, E. V., and Gurevich, V. V. (2006) Arrestins. Ubiquitous regulators of cellular signaling pathways. Genome Biology 7, 236
46. Gurevich, V. V., and Gurevich, E. V. (2012) Synthetic biology with surgical precision: targeted reengineering of signaling proteins. Cell. Signal. 24, 1899-1908
47. Pan, L., Gurevich, E. V., and Gurevich, V. V. (2003) The nature of the arrestin x receptor complex determines the ultimate fate of the internalized receptor. J. Biol. Chem. 278, 11623-11632
48. Seo, J., Tsakem, E. L., Breitman, M., and Gurevich, V. V. (2011) Identification of arrestin-3-specific residues necessary for JNK3 kinase activation. J. Biol. Chem. 286, 27894-27901
49. Coffa, S., Breitman, M., Spiller, B. W., and Gurevich, V. V. (2011) A single mutation in arrestin-2 prevents ERK1/2 activation by reducing c-Raf1 binding. Biochemistry 50, 6951-6958
50. Kristiansen, K. (2004) Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors. Molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacol. Ther. 103, 21-80
51. Gurevich, V. V., and Gurevich, E. V. (2008) Rich tapestry of G proteincoupled receptor signaling and regulatory mechanisms. Mol. Pharmacol. 74, 312-316
52. Schöneberg, T., Schulz, A., Biebermann, H., Hermsdorf, T., Römpler, H., and Sangkuhl, K. (2004) Mutant G-protein-coupled receptors as a cause of human diseases. Pharmacol. Ther. 104, 173-206
53. Barak, L. S., Oakley, R. H., Laporte, S. A., and Caron, M. G. (2001) Constitutive arrestin-mediated desensitization of a human vasopressin receptor mutant associated with nephrogenic diabetes insipidus. Proc. Natl. Acad. Sci. U. S. A. 98, 93-98
54. Rim, J., and Oprian, D. D. (1995) Constitutive activation of opsin: interaction of mutants with rhodopsin kinase and arrestin. Biochemistry 34, 11938-11945
55. Bainbridge, J. W., Smith, A. J., Barker, S. S., Robbie, S., Henderson, R., Balaggan, K., Viswanathan, A., Holder, G. E., Stockman, A., Tyler, N., Petersen-Jones, S., Bhattacharya, S. S., Thrasher, A. J., Fitzke, F. W., Carter, B. J., Rubin, G. S., Moore, A. T., and Ali, R. R. (2008) Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Engl. J. Med. 358, 2231-2239
56. Cideciyan, A. V., Aleman, T. S., Boye, S. L., Schwartz, S. B., Kaushal, S., Roman, A. J., Pang, J. J., Sumaroka, A., Windsor, E. A., Wilson, J. M., Flotte, T. R., Fishman, G. A., Heon, E., Stone, E. M., Byrne, B. J., Jacobson, S. G., and Hauswirth, W. W. (2008) Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proc. Natl. Acad. Sci. U. S. A. 105, 15112-15117
57. Hauswirth, W. W., Aleman, T. S., Kaushal, S., Cideciyan, A. V., Schwartz, S. B., Wang, L., Conlon, T. J., Boye, S. L., Flotte, T. R., Byrne, B. J., and Jacobson, S. G. (2008) Treatment of leber congenital amaurosis due to RPE65 mutations by ocular subretinal injection of adeno-associated virus gene vector. Short-term results of a phase I trial. Hum. Gene Ther. 19, 979-990
58. Maguire, A. M., Simonelli, F., Pierce, E. A., Pugh, E. N., Jr., Mingozzi, F., Bennicelli, J., Banfi, S., Marshall, K. A., Testa, F., Surace, E. M., Rossi, S., Lyubarsky, A., Arruda, V. R., Konkle, B., Stone, E., Sun, J., Jacobs, J., Dell'Osso, L., Hertle, R., Ma, J. X., Redmond, T. M., Zhu, X., Hauck, B., Zelenaia, O., Shindler, K. S., Maguire, M. G., Wright, J. F., Volpe, N. J., McDonnell, J. W., Auricchio, A., High, K. A., and Bennett, J. (2008) Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358, 2240-2248
59. Chen, J., Makino, C. L., Peachey, N. S., Baylor, D. A., and Simon, M. I. (1995) Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science 267, 374-377
60. Kovoor, A., Celver, J., Abdryashitov, R. I., Chavkin, C., and Gurevich, V. V. (1999) Targeted construction of phosphorylation-independent β-arrestin mutants with constitutive activity in cells. J. Biol. Chem. 274, 6831-6834
61. Celver, J., Vishnivetskiy, S. A., Chavkin, C., and Gurevich, V. V. (2002) Conservation of the phosphate-sensitive elements in the arrestin family of proteins. J. Biol. Chem. 277, 9043-9048
62. 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., Gurevich, V. V., and Hubbell, W. L. (2012) Conformation of receptorbound visual arrestin. Proc. Natl. Acad. Sci. U. S. A. 109, 18407-18412
63. Gurevich, E. V., Benovic, J. L., and Gurevich, V. V. (2002) Arrestin2 and arrestin3 are differentially expressed in the rat brain during postnatal development. Neuroscience 109, 421-436
64. Gurevich, E. V., Benovic, J. L., and Gurevich, V. V. (2004) Arrestin2 expression selectively increases during neural differentiation. J. Neurochem. 91, 1404-1416
65. Han, M., Gurevich, V. V., Vishnivetskiy, S. A., Sigler, P. B., and Schubert, C. (2001) Crystal structure of β-arrestin at 1.9 Å, Possible mechanism of receptor binding and membrane Translocation. Structure 9, 869-880
66. Zhan, X., Gimenez, L. E., Gurevich, V. V., and Spiller, B. W. (2011) Crystal structure of arrestin-3 reveals the basis of the difference in receptor binding between two non-visual subtypes. J. Mol. Biol. 406, 467-478
67. Celver, J. P., Lowe, J., Kovoor, A., Gurevich, V. V., and Chavkin, C. (2001) Threonine 180 is required for G-protein-coupled receptor kinase 3-and β-arrestin 2-mediated desensitization of the μ-opioid receptor in Xenopus oocytes. J. Biol. Chem. 276, 4894-4900
68. Gimenez, L. E., Vishnivetskiy, S. A., Baameur, F., and Gurevich, V. V. (2012) Manipulation of very few receptor discriminator residues greatly enhances receptor specificity of non-visual arrestins. J. Biol. Chem. 287, 29495-29505
69. Lim, W. A., and Pawson, T. (2010) Phosphotyrosine signaling. Evolving a new cellular communication system. Cell 142, 661-667
70. Kim, M., Hanson, S. M., Vishnivetskiy, S. A., Song, X., Cleghorn, W. M., Hubbell, W. L., and Gurevich, V. V. (2011) Robust self-association is a common feature of mammalian visual arrestin-1. Biochemistry 50, 2235-2242