Arrestin-3 binds c-Jun N-terminal kinase 1 (JNK1) and JNK2 and facilitates the activation of these ubiquitous JNK isoforms in cells via scaffolding

Journal of Biological Chemistry

Volumn 288, Issue 52, 2013, Pages 37332-37342

  Kook, Seunghyi ^a   Zhan, Xuanzhi ^a   Kaoud, Tamer S ^b,c   Dalby, Kevin N ^c   Gurevich, Vsevolod V ^a   Gurevich, Eugenia V ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Minia University   (Egypt)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-JUN N-TERMINAL KINASE; IN-VITRO; INTACT CELLS; ISOFORMS;

BIOCHEMISTRY; BIOLOGY;

SCAFFOLDS (BIOLOGY);

APOPTOSIS SIGNAL REGULATING KINASE 1; ARRESTIN 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE P38; RETINA S ANTIGEN; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; STRESS ACTIVATED PROTEIN KINASE 1ALPHA1; STRESS ACTIVATED PROTEIN KINASE 2ALPHA2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL TYPE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION;

EID: 84891403318     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.510412     Document Type: Article

References (70)

1. Gurevich, V. V., and Gurevich, E. V. (2004) The molecular acrobatics of arrestin activation. Trends Pharmacol. Sci. 25, 105-111
2. Carman, C. V., and Benovic, J. L. (1998) G-protein-coupled receptors. Turn-ons and turn-offs. Curr. Opin. Neurobiol. 8, 335-344
3. Gurevich, E. V., and Gurevich, V. V. (2006) Arrestins are ubiquitous regulators of cellular signaling pathways. Genome Biology 7, 236
4. DeWire, S. M., Ahn, S., Lefkowitz, R. J., and Shenoy, S. K. (2007) β-Arrestins and cell signaling. Annu. Rev. Physiol. 69, 483-510
5. Gurevich, V. V., and Gurevich, E. V. (2006) The structural basis of arrestin-mediated regulation of Gprotein-coupled receptors. Pharmacol. Ther. 110, 465-502
6. McDonald, P. H., Chow, C. W., Miller, W. E., Laporte, S. A., Field, M. E., Lin, F. T., Davis, R. J., and Lefkowitz, R. J. (2000) β-arrestin 2. A receptorregulated MAPK scaffold for the activation of JNK3. Science 290, 1574-1577
7. Miller, W. E., McDonald, P. H., Cai, S. F., Field, M. E., Davis, R. J., and Lefkowitz, R. J. (2001) Identification of a motif in the carboxyl terminus of β-arrestin2 responsible for activation of JNK3. J. Biol. Chem. 276, 27770-27777
8. Song, X., Coffa, S., Fu, H., and Gurevich, V. V. (2009) How does arrestin assemble MAPKs into a signaling complex? J. Biol. Chem. 284, 685-695
9. Seo, J., Tsakem, E. L., Breitman, M., and Gurevich, V. V. (2011) Identification of arrestin-3-specific residues necessary for JNK3 activation. J. Biol. Chem. 286, 27894-27901
10. Zhan, X., Kaoud, T. S., Dalby, K. N., and Gurevich, V. V. (2011) Non-visual arrestins function as simple scaffolds assembling MKK4-JNK3α2 signaling complex. Biochemistry 50, 10520-10529
11. 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 the cell by a dominant-negative arrestin-3 mutant. J. Biol. Chem. 287, 19653-19664
12. Zhan, X., Kaoud, T. S., Kook, S., Dalby, K. N., and Gurevich, V. V. (2013) JNK3 enzyme binding to arrestin-3 differentially affects the recruitment of upstream mitogen-activated protein (MAP) kinase kinases. J. Biol. Chem. 288, 28535-28547
13. Yang, D. D., Kuan, C. Y., Whitmarsh, A. J., Rincón, M., Zheng, T. S., Davis, R. J., Rakic, P., and Flavell, R. A. (1997) Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389, 865-870
14. Attramadal, H., Arriza, J. L., Aoki, C., Dawson, T. M., Codina, J., Kwatra, M. M., Snyder, S. H., Caron, M. G., and Lefkowitz, R. J. (1992)β-Arrestin2, a novel member of the arrestin/β-arrestin gene family. J. Biol. Chem. 267, 17882-17890
15. Sterne-Marr, R., Gurevich, V. V., Goldsmith, P., Bodine, R. C., Sanders, C., Donoso, L. A., and Benovic, J. L. (1993) Polypeptide variants of β-arrestin and arrestin3. J. Biol. Chem. 268, 15640-15648
16. Davis, R. J. (2000) Signal transduction by the JNK group of MAP kinases. Cell 103, 239-252
17. Gupta, S., Barrett, T., Whitmarsh, A. J., Cavanagh, J., Sluss, H. K., Dérijard, B., and Davis, R. J. (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15, 2760-2770
18. Johnson, G. L. (2011) Defining MAPK interactomes. ACS Chem. Biol. 6, 18-20
19. Madsen, J. A., Kaoud, T. S., Dalby, K. N., and Brodbelt, J. S. (2011) 193-nm photodissociation of singly and multiply charged peptide anions for acidic proteome characterization. Proteomics 11, 1329-1334
20. Yan, C., Kaoud, T., Lee, S., Dalby, K. N., and Ren, P. (2011) Understanding the specificity of a docking interaction between JNK1 and the scaffolding protein JIP1. J. Phys. Chem. B 115, 1491-1502
21. Kaoud, T. S., Park, H., Mitra, S., Yan, C., Tseng, C. C., Shi, Y., Jose, J., Taliaferro, J. M., Lee, K., Ren, P., Hong, J., and Dalby, K. N. (2012) Manipulating JNK signaling with (-)-zuonin A. ACS Chem. Biol. 7, 1873-1883
22. Donoso, L. A., Gregerson, D. S., Smith, L., Robertson, S., Knospe, V., Vrabec, T., and Kalsow, C. M. (1990) S-antigen. Preparation and characterization of site-specific monoclonal antibodies. Curr. Eye. Res. 9, 343-355
23. Song, X., Vishnivetskiy, S. A., Seo, J., Chen, J., Gurevich, E. V., and Gurevich, V. V. (2011) Arrestin-1 expression in rods. Balancing functional performance and photoreceptor health. Neuroscience 174, 37-49
24. 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
25. Gurevich, E. V., Benovic, J. L., and Gurevich, V. V. (2004) Arrestin2 expression selectively increases during neural differentiation. J. Neurochem. 91, 1404-1416
26. 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
27. Scott, M. G., Le Rouzic, E., Périanin, A., Pierotti, V., Enslen, H., Benichou, S., Marullo, S., and Benmerah, A. (2002) Differential nucleocytoplasmic shuttling of β-arrestins. Characterization of a leucine-rich nuclear export signal in β-arrestin2. J. Biol. Chem. 277, 37693-37701
28. Wacker, W. B., Donoso, L. A., Kalsow, C. M., Yankeelov, J. A., Jr., and Organisciak, D. T. (1977) Experimental allergic uveitis. Isolation, characterization, and localization of a soluble uveitopathogenic antigen from bovine retina. J. Immunol. 119, 1949-1958
29. Kohout, T. A., Lin, F. S., Perry, S. J., Conner, D. A., and Lefkowitz, R. J. (2001) β-Arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking. Proc. Natl. Acad. Sci. U.S.A. 98, 1601-1606
30. Lawler, S., Fleming, Y., Goedert, M., and Cohen, P. (1998) Synergistic activation of SAPK1/JNK1 by two MAP kinase kinases in vitro. Curr. Biol. 8, 1387-1390
31. Haeusgen, W., Herdegen, T., and Waetzig, V. (2011) The bottleneck of JNK signaling. Molecular and functional characteristics of MKK4 and MKK7. Eur. J. Cell Biol. 90, 536-544
32. Keshet, Y., and Seger, R. (2010) The MAP kinase signaling cascades. A system of hundreds of components regulates a diverse array of physiological functions. Methods Mol. Biol. 661, 3-38
33. Yasuda, J., Whitmarsh, A. J., Cavanagh, J., Sharma, M., and Davis, R. J. (1999) The JIP group of mitogen-activated protein kinase scaffold proteins. Mol. Cell. Biol. 19, 7245-7254
34. Engström, W., Ward, A., and Moorwood, K. (2010) The role of scaffold proteins in JNK signalling. Cell Prolif. 43, 56-66
35. Matsuura, H., Nishitoh, H., Takeda, K., Matsuzawa, A., Amagasa, T., Ito, M., Yoshioka, K., and Ichijo, H. (2002) Phosphorylation-dependent scaffolding role of JSAP1/JIP3 in the ASK1-JNK signaling pathway. A new mode of regulation of the MAP kinase cascade. J. Biol. Chem. 277, 40703-40709
36. Kelkar, N., Gupta, S., Dickens, M., and Davis, R. J. (2000) Interaction of a mitogen-activated protein kinase signaling module with the neuronal protein JIP3. Mol. Cell. Biol. 20, 1030-1043
37. Dhanasekaran, D. N., Kashef, K., Lee, C. M., Xu, H., and Reddy, E. P. (2007) Scaffold proteins of MAP-kinase modules. Oncogene 26, 3185-3202
38. Levchenko, A., Bruck, J., and Sternberg, P. W. (2000) Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc. Natl. Acad. Sci. U.S.A. 97, 5818-5823
39. Levchenko, A., Bruck, J., and Sternberg, P. W. (2004) Regulatory modules that generate biphasic signal response in biological systems. Syst. Biol. (Stevenage) 1, 139-148
40. Kyriakis, J. M., and Avruch, J. (2001) Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81, 807-869
41. Widmann, C., Gibson, S., Jarpe, M. B., and Johnson, G. L. (1999) Mitogenactivated protein kinase. Conservation of a three-kinase module from yeast to human. Physiol. Rev. 79, 143-180
42. Burack, W. R., and Shaw, A. S. (2000) Signal transduction. Hanging on a scaffold. Curr. Opin. Cell Biol. 12, 211-216
43. 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
44. 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
45. Carter, J. M., Gurevich, V. V., Prossnitz, E. R., and Engen, J. R. (2005) Conformational differences between arrestin2 and pre-activated mutants as revealed by hydrogen exchange mass spectrometry. J. Mol. Biol. 351, 865-878
46. 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
47. Kovoor, A., Celver, J., Abdryashitov, R. I., Chavkin, C., and Gurevich, V. V. (1999) Targeted construction of phosphorylation-independent b-arrestin mutants with constitutive activity in cells. J. Biol. Chem. 274, 6831-6834
48. Vishnivetskiy, S. A., Hirsch, J. A., Velez, M.-G., Gurevich, Y. V., and Gurevich, V. V. (2002) Transition of arrestin in the active receptor-binding state requires an extended interdomain hinge. J. Biol. Chem. 277, 43961-43967
49. Hanson, S. M., Cleghorn, W. M., Francis, D. J., Vishnivetskiy, S. A., Raman, D., Song, X., Nair, K. S., Slepak, V. Z., Klug, C. S., and Gurevich, V. V. (2007) Arrestin mobilizes signaling proteins to the cytoskeleton and redirects their activity. J. Mol. Biol. 368, 375-387
50. Tournier, C., Hess, P., Yang, D. D., Xu, J., Turner, T. K., Nimnual, A., Bar-Sagi, D., Jones, S. N., Flavell, R. A., and Davis, R. J. (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288, 870-874
51. Gao, Y., Signore, A. P., Yin, W., Cao, G., Yin, X. M., Sun, F., Luo, Y., Graham, S. H., and Chen, J. (2005) Neuroprotection against focal ischemic brain injury by inhibition of c-Jun N-terminal kinase and attenuation of the mitochondrial apoptosis-signaling pathway. J. Cereb. Blood Flow Metab. 25, 694-712
52. Namgung, U., and Xia, Z. (2000) Arsenite-induced apoptosis in cortical neurons is mediated by c-Jun N-terminal protein kinase 3 and p38 mitogen-activated protein kinase. J. Neurosci. 20, 6442-6451
53. Okuno, S., Saito, A., Hayashi, T., and Chan, P. H. (2004) The c-Jun N-terminal protein kinase signaling pathway mediates Bax activation and subsequent neuronal apoptosis through interaction with Bim after transient focal cerebral ischemia. J. Neurosci. 24, 7879-7887
54. 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
55. Zanke, B. W., Boudreau, K., Rubie, E., Winnett, E., Tibbles, L. A., Zon, L., Kyriakis, J., Liu, F. F., and Woodgett, J. R. (1996) The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation, or heat. Curr. Biol. 6, 606-613
56. Chang, L., Kamata, H., Solinas, G., Luo, J. L., Maeda, S., Venuprasad, K., Liu, Y. C., and Karin, M. (2006) The E3 ubiquitin ligase itch couples JNK activation to TNFα-induced cell death by inducing c-FLIP(L) turnover. Cell 124, 601-613
57. De Smaele, E., Zazzeroni, F., Papa, S., Nguyen, D. U., Jin, R., Jones, J., Cong, R., and Franzoso, G. (2001) Induction of gadd45β by NF-κB down-regulates pro-apoptotic JNK signalling. Nature 414, 308-313
58. Deng, Y., Ren, X., Yang, L., Lin, Y., and Wu, X. (2003) A JNK-dependent pathway is required for TNFα-induced apoptosis. Cell 115, 61-70
59. Dhanasekaran, D. N., and Reddy, E. P. (2008) JNK signaling in apoptosis. Oncogene 27, 6245-6251
60. Fogarty, M. P., Downer, E. J., and Campbell, V. (2003) A role for c-Jun N-terminal kinase 1 (JNK1), but not JNK2, in the β-amyloid-mediated stabilization of protein p53 and induction of the apoptotic cascade in cultured cortical neurons. Biochem. J. 371, 789-798
61. Kamata, H., Honda, S., Maeda, S., Chang, L., Hirata, H., and Karin, M. (2005) Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120, 649-661
62. Oleinik, N. V., Krupenko, N. I., and Krupenko, S. A. (2007) Cooperation between JNK1 and JNK2 in activation of p53 apoptotic pathway. Oncogene 26, 7222-7230
63. Tang, G., Minemoto, Y., Dibling, B., Purcell, N. H., Li, Z.-W., Karin, M., and Lin, A. (2001) Inhibition of JNK activation through NF-κB target genes. Nature 414, 313-317
64. Good, M., Tang, G., Singleton, J., Reményi, A., and Lim, W. A. (2009) The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136, 1085-1097
65. Bhattacharyya, R. P., Reményi, A., Good, M. C., Bashor, C. J., Falick, A. M., and Lim, W. A. (2006) The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311, 822-826
66. Pullikuth, A., McKinnon, E., Schaeffer, H. J., and Catling, A. D. (2005) The MEK1 scaffolding protein MP1 regulates cell spreading by integrating PAK1 and Rho signals. Mol. Cell. Biol. 25, 5119-5133
67. Willoughby, E. A., Perkins, G. R., Collins, M. K., and Whitmarsh, A. J. (2003) The JNK-interacting protein-1 scaffold protein targets MAPK phosphatase-7 to dephosphorylate JNK. J. Biol. Chem. 278, 10731-10736
68. Kortum, R. L., and Lewis, R. E. (2004) The molecular scaffold KSR1 regulates the proliferative and oncogenic potential of cells.. Mol. Cell. Biol. 24, 4407-4416
69. Milano, S. K., Kim, Y. M., Stefano, F. P., Benovic, J. L., and Brenner, C. (2006) Nonvisual arrestin oligomerization and cellular localization are regulated by inositol hexakisphosphate binding. J. Biol. Chem. 281, 9812-9823
70. Storez, H., Scott, M. G., Issafras, H., Burtey, A., Benmerah, A., Muntaner, O., Piolot, T., Tramier, M., Coppey-Moisan, M., Bouvier, M., Labbé-Jullié, C., and Marullo, S. (2005) Homo- and hetero-oligomerization of β-arrestins in living cells. J. Biol. Chem. 280, 40210-40215