α-arrestin 1 (ARRDC1) and β-arrestins cooperate to mediate Notch degradation in mammals

Journal of Cell Science

Volumn 126, Issue 19, 2013, Pages 4457-4468

  Puca, Loredana ^a,b   Chastagner, Patricia ^a   Meas Yedid, Vannary ^a   Israël, Alain ^a   Brou, Christel ^a  

^a INSTITUT PASTEUR   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Arrestin; Endocytosis; Itch; Notch; Ubiquitin

Indexed keywords

ALPHA ARRESTIN 1 PROTEIN; BETA ARRESTIN; NOTCH RECEPTOR; RETINA S ANTIGEN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION;

ARRESTIN; ENDOCYTOSIS; ITCH; NOTCH; UBIQUITIN;

ANIMALS; ARRESTINS; CELL LINE, TUMOR; ENDOCYTOSIS; FIBROBLASTS; HEK293 CELLS; HUMANS; MICE; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSFECTION; UBIQUITINATION;

EID: 84885457871     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.130500     Document Type: Article

References (46)

1. Alvarez, C. E. (2008). On the origins of arrestin and rhodopsin. BMC Evol. Biol. 8, 222.
2. Angers, A., Ramjaun, A. R. and McPherson, P. S. (2004). The HECT domain ligase itch ubiquitinates endophilin and localizes to the trans-Golgi network and endosomal system. J. Biol. Chem. 279, 11471-11479.
3. Becuwe, M., Herrador, A., Haguenauer-Tsapis, R., Vincent, O., and Léon, S. (2012a). Ubiquitin-mediated regulation of endocytosis by proteins of the arrestin family. Biochem. Res. Int. 2012, 242764.
4. Becuwe, M., Vieira, N., Lara, D., Gomes-Rezende, J., Soares-Cunha, C., Casal, M., Haguenauer-Tsapis, R., Vincent, O., Paiva, S., and Léon, S. (2012b). A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J. Cell Biol. 196, 247-259.
5. Bhandari, D., Trejo, J., Benovic, J. L., and Marchese, A. (2007). Arrestin-2 interacts with the ubiquitin-protein isopeptide ligase atrophin-interacting protein 4, and mediates endosomal sorting of the chemokine receptor CXCR4. J. Biol. Chem. 282, 36971-36979.
6. Boularan, C., Scott, M. G. H., Bourougaa, K., Bellal, M., Esteve, E., Thuret, A., Benmerah, A., Tramier, M., Coppey-Moisan, M., Labbé-Jullié, C. et al. (2007). beta-arrestin 2 oligomerization controls the Mdm2-dependent inhibition of p53. Proc. Natl. Acad. Sci. USA 104, 18061-18066.
7. Bray, S. J. (2006). Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689.
8. Brou, C. (2009). Intracellular trafficking of Notch receptors, and ligands. Exp. Cell Res. 315, 1549-1555.
9. Chastagner, P., Israël, A., and Brou, C. (2006). Itch/AIP4 mediates Deltex degradation through the formation of K29-linked polyubiquitin chains. EMBO Rep. 7, 1147-1153.
10. Chastagner, P., Israël, A., and Brou, C. (2008). AIP4/Itch regulates Notch receptor degradation in the absence of ligand. PLoS ONE 3, e2735.
11. Coureuil, M., Lécuyer, H., Scott, M. G. H., Boularan, C., Enslen, H., Soyer, M., Mikaty, G., Bourdoulous, S., Nassif, X., and Marullo, S. (2010). Meningococcus Hijacks a b2-adrenoceptor/b-Arrestin pathway to cross brain microvasculature endothelium. Cell 143, 1149-1160.
12. de Chaumont, F., Dallongeville, S., Chenouard, N., Hervé, N., Pop, S., Provoost, T., Meas-Yedid, V., Pankajakshan, P., Lecomte, T., Le Montagner, Y., et al. (2012). Icy: an open bioimage informatics platform for extended reproducible research. Nat. Methods 9, 690-696.
13. Han, S. O., Kommaddi, R. P., and Shenoy, S. K. (2012). Distinct roles for b-arrestin2, and arrestin-domain-containing proteins in b2 adrenergic receptor trafficking. EMBO Rep. 14, 164-171.
14. Hara, M. R., Kovacs, J. J., Whalen, E. J., Rajagopal, S., Strachan, R. T., Grant, W., Towers, A. J., Williams, B., Lam, C. M., Xiao, K., et al. (2011). A stress response pathway regulates DNA damage through b2-adrenoreceptors, and b-arrestin-1. Nature 477, 349-353.
15. Havugimana, P. C., Hart, G. T., Nepusz, T., Yang, H., Turinsky, A. L., Li, Z., Wang, P. I., Boutz, D. R., Fong, V., Phanse, S., et al. (2012). A census of human soluble protein complexes. Cell 150, 1068-1081.
16. Hori, K., Sen, A., Kirchhausen, T., and Artavanis-Tsakonas, S. (2011). Synergy between the ESCRT-III complex, and Deltex defines a ligand-independent Notch signal. J. Cell Biol. 195, 1005-1015.
17. Ingham, R. J., Gish, G., and Pawson, T. (2004). The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture. Oncogene 23, 1972-1984.
18. Kovacs, J. J., Hara, M. R., Davenport, C. L., Kim, J., and Lefkowitz, R. J. (2009). Arrestin development: emerging roles for beta-arrestins in developmental signaling pathways. Dev. Cell 17, 443-458.
19. Lin, C. H., MacGurn, J. A., Chu, T., Stefan, C. J., and Emr, S. D. (2008). Arrestinrelated ubiquitin-ligase adaptors regulate endocytosis, and protein turnover at the cell surface. Cell 135, 714-725.
20. Logeat, F., Bessia, C., Brou, C., LeBail, O., Jarriault, S., Seidah, N. G., and Israël, A. (1998). The Notch1 receptor is cleaved constitutively by a furin-like convertase. Proc. Natl. Acad. Sci. USA 95, 8108-8112.
21. Malik, R., and Marchese, A. (2010). Arrestin-2 interacts with the endosomal sorting complex required for transport machinery to modulate endosomal sorting of CXCR4. Mol. Biol. Cell 21, 2529-2541.
22. Masutani, H., Yoshihara, E., Masaki, S., Chen, Z., and Yodoi, J. (2012). Thioredoxin binding protein (TBP)-2/Txnip, and a-arrestin proteins in cancer, and diabetes mellitus. J. Clin. Biochem. Nutr. 50, 23-34.
23. Minoguchi, S., Taniguchi, Y., Kato, H., Okazaki, T., Strobl, L. J., Zimber-Strobl, U., Bornkamm, G. W., and Honjo, T. (1997). RBP-L, a transcription factor related to RBP-Jkappa. Mol. Cell. Biol. 17, 2679-2687.
24. Moretti, J., Chastagner, P., Liang, C.-C., Cohn, M. A., Israël, A., and Brou, C. (2012). The ubiquitin-specific protease 12 (USP12) is a negative regulator of notch signaling acting on notch receptor trafficking toward degradation. J. Biol. Chem. 287, 29429-29441.
25. Mukherjee, A., Veraksa, A., Bauer, A., Rosse, C., Camonis, J., and Artavanis-Tsakonas, S. (2005). Regulation of Notch signalling by non-visual beta-arrestin. Nat. Cell Biol. 7, 1191-1201.
26. Nabhan, J. F., Pan, H., and Lu, Q. (2010). Arrestin domain-containing protein 3 recruits the NEDD4 E3 ligase to mediate ubiquitination of the beta2-adrenergic receptor. EMBO Rep. 11, 605-611.
27. Nabhan, J. F., Hu, R., Oh, R. S., Cohen, S. N., and Lu, Q. (2012). Formation, and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc. Natl. Acad. Sci. USA 109, 4146-4151.
28. O'Donnell, A. F., Apffel, A., Gardner, R. G., and Cyert, M. S. (2010). Alpha-arrestins Aly1, and Aly2 regulate intracellular trafficking in response to nutrient signaling. Mol. Biol. Cell 21, 3552-3566.
29. Patwari, P., Chutkow, W. A., Cummings, K., Verstraeten, V. L. R. M., Lammerding, J., Schreiter, E. R., and Lee, R. T. (2009). Thioredoxin-independent regulation of metabolism by the alpha-arrestin proteins. J. Biol. Chem. 284, 24996-25003.
30. Polo, S., and Di Fiore, P. P. (2008). Finding the right partner: science or ART? Cell 135, 590-592.
31. Rand, M. D., Grimm, L. M., Artavanis-Tsakonas, S., Patriub, V., Blacklow, S. C., Sklar, J., and Aster, J. C. (2000). Calcium depletion dissociates, and activates heterodimeric notch receptors. Mol. Cell. Biol. 20, 1825-1835.
32. Rauch, S., and Martin-Serrano, J. (2011). Multiple interactions between the ESCRT machinery, and arrestin-related proteins: implications for PPXY-dependent budding. J. Virol. 85, 3546-3556.
33. Sakata, T., Sakaguchi, H., Tsuda, L., Higashitani, A., Aigaki, T., Matsuno, K., and Hayashi, S. (2004). Drosophila Nedd4 regulates endocytosis of notch, and suppresses its ligand-independent activation. Curr. Biol. 14, 2228-2236.
34. Schroeter, E. H., Kisslinger, J. A., and Kopan, R. (1998). Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393, 382-386.
35. Scott, M. G. H., Le Rouzic, E., Périanin, A., Pierotti, V., Enslen, H., Benichou, S., Marullo, S., and Benmerah, A. (2002). Differential nucleocytoplasmic shuttling of beta-arrestins. Characterization of a leucine-rich nuclear export signal in betaarrestin2. J. Biol. Chem. 277, 37693-37701.
36. Shea, F. F., Rowell, J. L., Li, Y., Chang, T.-H., and Alvarez, C. E. (2012). Mammalian a arrestins link activated seven transmembrane receptors to Nedd4 family e3 ubiquitin ligases, and interact with b arrestins. PLoS ONE 7, e50557.
37. Shenoy, S. K., McDonald, P. H., Kohout, T. A., and Lefkowitz, R. J. (2001). Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor, and beta-arrestin. Science 294, 1307-1313.
38. Shenoy, S. K., Xiao, K., Venkataramanan, V., Snyder, P. M., Freedman, N. J., and Weissman, A. M. (2008). Nedd4 mediates agonist-dependent ubiquitination, lysosomal targeting,, and degradation of the beta2-adrenergic receptor. J. Biol. Chem. 283, 22166-22176.
39. Six, E. M., Ndiaye, D., Sauer, G., Laâbi, Y., Athman, R., Cumano, A., Brou, C., Israël, A., and Logeat, F. (2004). The notch ligand Delta1 recruits Dlg1 at cell-cell contacts, and regulates cell migration. J. Biol. Chem. 279, 55818-55826.
40. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K.-J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L.-G., et al. (2006). Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000.
41. Storez, H., Scott, M. G. H., Issafras, H., Burtey, A., Benmerah, A., Muntaner, O., Piolot, T., Tramier, M., Coppey-Moisan, M., Bouvier, M., et al. (2005). Homo-, and hetero-oligomerization of beta-arrestins in living cells. J. Biol. Chem. 280, 40210-40215.
42. Vaccari, T., Lu, H., Kanwar, R., Fortini, M. E., and Bilder, D. (2008). Endosomal entry regulates Notch receptor activation in Drosophila melanogaster. J. Cell Biol. 180, 755-762.
43. Wilkin, M. B., Carbery, A.-M., Fostier, M., Aslam, H., Mazaleyrat, S. L., Higgs, J., Myat, A., Evans, D. A. P., Cornell, M., and Baron, M. (2004). Regulation of notch endosomal sorting, and signaling by Drosophila Nedd4 family proteins. Curr. Biol. 14, 2237-2244.
44. Wilkin, M., Tongngok, P., Gensch, N., Clemence, S., Motoki, M., Yamada, K., Hori, K., Taniguchi-Kanai, M., Franklin, E., Matsuno, K., et al. (2008). Drosophila HOPS, and AP-3 complex genes are required for a Deltex-regulated activation of notch in the endosomal trafficking pathway. Dev. Cell 15, 762-772.
45. Xiao, K., McClatchy, D. B., Shukla, A. K., Zhao, Y., Chen, M., Shenoy, S. K., Yates, J. R., 3rd, and Lefkowitz, R. J. (2007). Functional specialization of beta-arrestin interactions revealed by proteomic analysis. Proc. Natl. Acad. Sci. USA 104, 12011-12016.
46. Yamada, K., Fuwa, T. J., Ayukawa, T., Tanaka, T., Nakamura, A., Wilkin, M. B., Baron, M., and Matsuno, K. (2011). Roles of Drosophila deltex in Notch receptor endocytic trafficking, and activation. Genes Cells 16, 261-272.