The ubiquitin code and its decoding machinery in the endocytic pathway

Journal of Biochemistry

Volumn 153, Issue 6, 2013, Pages 497-504

  Tanno, Hidetaka ^a   Komada, Masayuki ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

endocytosis; endosome; lysosome; multivesicular body; ubiquitin

Indexed keywords

ACID HYDROLASE; ANKRD13 PROTEIN; CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPSIN; MEMBRANE PROTEIN; UBIQUITIN; UBIQUITIN BINDING PROTEIN; UNCLASSIFIED DRUG; URACIL;

AMINO ACID SEQUENCE; DNA REPAIR; ENDOCYTOSIS; ENDOSOME; LYSOSOME; MULTIVESICULAR BODY; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ENDOCYTOSIS; ENDOSOME; LYSOSOME; MULTIVESICULAR BODY; UBIQUITIN;

ANIMALS; CELL MEMBRANE; ENDOCYTOSIS; ENDOSOMES; HUMANS; LYSOSOMES; MEMBRANE PROTEINS; TRANSPORT VESICLES; UBIQUITIN;

EID: 84878586878     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvt028     Document Type: Review

References (57)

1. Gao, T., Liu, Z., Wang, Y., Cheng, H., Yang, Q., Guo, A., Ren, J., and Xue, Y. (2012) UUCD: A family-based database of ubiquitin and ubiquitin-like conjugation. Nucleic Acids Res. 41, D445-D451
2. Meierhofer, D., Wang, X., Huang, L., and Kaiser, P. (2008) Quantitative analysis of global ubiquitination in HeLa cells by mass spectrometry. J. Proteome Res. 7, 4566-4576
3. Kulathu, Y. and Komander, D. (2012) Atypical ubiquitylation - The unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 13, 508-523
4. Iwai, K. (2012) Diverse ubiquitin signaling in NF-kB activation. Trends Cell Biol. 22, 355-364
5. Husnjak, K. and Dikic, I. (2012) Ubiquitin-binding proteins: Decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81, 291-322
6. McMahon, H.T. and Boucrot, E. (2011) Molecular mechanism and physiological functions of clathrinmediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533
7. Grant, B.D. and Donaldson, J.G. (2009) Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597-608
8. Henne, W.M., Buchkovich, N.J., and Emr, S.D. (2011) The ESCRT pathway. Dev. Cell 21, 77-91
9. Wollert, T. and Hurley, J.H. (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864-869
10. Kölling, R. and Hollenberg, C.P. (1994) The ABC-Transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13, 3261-3271
11. Hicke, L. and Riezman, H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277-287
12. Galan, J.M. and Haguenauer-Tsapis, R. (1997) Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J. 16, 5847-5854
13. Springael, J.Y., Galan, J.M., Haguenauer-Tsapis, R., and André, B. (1999) NH4 -induced down-regulation of the Saccharomyces cerevisiae Gap1p permease involves its ubiquitination with lysine-63-linked chains. J. Cell Sci. 112, 1375-1383
14. Terrell, J., Shih, S., Dunn, R., and Hicke, L. (1998) A function for monoubiquitination in the internalization of a G protein-coupled receptor. Mol. Cell 1, 193-202
15. Shih, S.C., Sloper-Mould, K.E., and Hicke, L. (2000) Monoubiquitin carries a novel internalization signal that is appended to activated receptors. EMBO J. 19, 187-198
16. Lauwers, E., Jacob, C., and André, B. (2009) K63-linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway. J. Cell Biol. 185, 493-502
17. Kim, Y., Deng, Y., and Philpott, C.C. (2007) GGA2-And ubiquitin-dependent trafficking of Arn1, the ferrichrome transporter of Saccharomyces cerevisiae. Mol. Biol. Cell 18, 1790-1802
18. Erpapazoglou, Z., Froissard, M., Nondier, I., Lesuisse, E., Haguenauer-Tsapis, R., and Belgareh-Touzé, N. (2008) Substrate- And ubiquitin-dependent trafficking of the yeast siderophore transporter Sit1. Traffic 9, 1372-1391
19. Strous, G.J., van Kerkhof, P., Govers, R., Ciechanover, A., and Schwartz, A.L. (1996) The ubiquitin conjugation system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO J. 15, 3806-3812
20. Govers, R., ten Broeke, T., van Kerkhof, P., Schwartz, A.L., and Strous, G.J. (1999) Identification of a novel ubiquitin conjugation motif, required for ligand-induced internalization of the growth hormone receptor. EMBO J. 18, 28-36
21. Staub, O., Gautschi, I., Ishikawa, T., Breitschopf, K., Ciechanover, A., Schild, L., and Rotin, D. (1997) Regulation of stability and function of the epithelial Na channel (ENaC) by ubiquitination. EMBO J. 16, 6325-6336
22. Levkowitz, G., Waterman, H., Zamir, E., Kam, Z., Oved, S., Langdon, W.Y., Beguinot, L., Geiger, B., and Yarden, Y. (1998) c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12, 3663-3674
23. Levkowitz, G., Waterman, H., Ettenberg, S.A., Katz, M., Tsygankov, A.Y., Alroy, I., Lavi, S., Iwai, K., Reiss, Y., Ciechanover, A., Lipkowitz, S., and Yarden, Y. (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4, 1029-1040
24. Huang, F., Goh, L.K., and Sorkin, A. (2007) EGF receptor ubiquitination is not necessary for its internalization. Proc. Natl Acad. Sci. U.S.A. 104, 16904-16909
25. Haglund, K., Sigismund, S., Polo, S., Szymkiewicz, I., Di Fiore, P.P., and Dikic, I. (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466
26. Mosesson, Y., Shtiegman, K., Katz, M., Zwang, Y., Vereb, G., Szollosi, J., and Yarden, Y. (2003) Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J. Biol. Chem. 278, 21323-21326
27. Raiborg, C., Bache, K.G., Gillooly, D.J., Madshus, I.H., Stang, E., and Stenmark, H. (2002) Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4, 394-398
28. Nakatsu, F., Sakuma, M., Matsuo, Y., Arase, H., Yamasaki, S., Nakamura, N., Saito, T., and Ohno, H. (2000) A di-leucine signal in the ubiquitin moiety. Possible involvement in ubiquitination-mediated endocytosis. J. Biol. Chem. 275, 26213-26219
29. Huang, F., Kirkpatrick, D., Jiang, X., Gygi, S., and Sorkin, A. (2006) Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 21, 737-748
30. Geetha, T., Jiang, J., and Wooten, M.W. (2005) Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Mol. Cell 20, 301-312
31. Duncan, L.M., Piper, S., Dodd, R.B., Saville, M.K., Sanderson, C.M., Luzio, J.P., and Lehner, P.J. (2006) Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J. 25, 1635-1645
32. Varghese, B., Barriere, H., Carbone, C.J., Banerjee, A., Swaminathan, G., Plotnikov, A., Xu, P., Peng, J., Goffin, V., Lukacs, G.L., and Fuchs, S.Y. (2008) Polyubiquitination of prolactin receptor stimulates its internalization, postinternalization sorting, and degradation via the lysosomal pathway. Mol. Cell. Biol. 28, 5275-5287
33. Barriere, H., Nemes, C., Lechardeur, D., Khan-Mohammad, M., Fruh, K., and Lukacs, G.L. (2006) Molecular basis of oligoubiquitin-dependent internalization of membrane proteins in mammalian cells. Traffic 7, 282-297
34. Barriere, H., Nemes, C., Du, K., and Lukacs, G.L. (2007) Plasticity of polyubiquitin recognition as lysosomal targeting signals by the endosomal sorting machinery. Mol. Biol. Cell 18, 3952-3965
35. Boname, J.M., Thomas, M., Stagg, H.R., Xu, P., Peng, J., and Lehner, P.J. (2010) Efficient internalization of MHC I requires lysine-11 and lysine-63 mixed linkage polyubiquitin chains. Traffic 11, 210-220
36. Goto, E., Yamanaka, Y., Ishikawa, A., Aoki-Kawasumi, M., Mito-Yoshida, M., Ohmura-Hoshino, M., Matsuki, Y., Kajikawa, M., Hirano, H., and Ishido, S. (2010) Contribution of lysine 11-linked ubiquitination to MIR2-mediated major histocompatibility complex class I internalization. J. Biol. Chem. 285, 35311-35319
37. Hofmann, K. and Falquet, L. (2001) A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26, 347-350
38. Sigismund, S., Woelk, T., Puri, C., Maspero, E., Tacchetti, C., Transidico, P., Di Fiore, P.P., and Polo, S. (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl Acad. Sci. U.S.A. 102, 2760-2765
39. Dores, M.R., Schnell, J.D., Maldonado-Baez, L., Wendland, B., and Hicke, L. (2010) The function of yeast epsin and Ede1 ubiquitin-binding domains during receptor internalization. Traffic 11, 151-160
40. Hurley, J.H., Lee, S., and Prag, G. (2006) Ubiquitinbinding domains. Biochem. J. 399, 361-372
41. Hawryluk, M.J., Keyel, P.A., Mishra, S.K., Watkins, S.C., Heuser, J.E., and Traub, L.M. (2006) Epsin 1 is a polyubiquitin-selective clathrin-Associated sorting protein. Traffic 7, 262-281
42. Sato, Y., Yoshikawa, A., Mimura, H., Yamashita, M., Yamagata, A., and Fukai, S. (2009) Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by tandem UIMs of RAP80. EMBO J. 28, 2461-2468
43. Tanno, H., Yamaguchi, T., Goto, E., Ishido, S., and Komada, M. (2012) The Ankrd 13 family of UIM-bearing proteins regulates EGF receptor endocytosis from the plasma membrane. Mol. Biol. Cell 23, 1343-1353
44. Ren, X. and Hurley, J.H. (2010) VHS domains of ESCRT-0 cooperate in high-Avidity binding to polyubiquitinated cargo. EMBO J. 29, 1045-1054
45. Lange, A., Castañeda, C., Hoeller, D., Lancelin, J.M., Fushman, D., and Walker, O. (2012) Evidence for cooperative and domain-specific binding of the signal transducing adaptor molecule 2 (STAM2) to Lys63-linked diubiquitin. J. Biol. Chem. 287, 18687-18699
46. Roxrud, I., Raiborg, C., Pedersen, N.M., Stang, E., and Stenmark, H. (2008) An endosomally localized isoform of Eps15 interacts with Hrs to mediate degradation of epidermal growth factor receptor. J. Cell Biol. 180, 1205-1218
47. Sundquist, W.I., Schubert, H.L., Kelly, B.N., Hill, G.C., Holton, J.M., and Hill, C.P. (2004) Ubiquitin recognition by the human TSG101 protein. Mol. Cell 13, 783-789
48. Agromayor, M., Soler, N., Caballe, A., Kueck, T., Freund, S.M., Allen, M.D., Bycroft, M., Perisic, O., Ye, Y., McDonald, B., Scheel, H., Hofmann, K., Neil, S.J., Martin-Serrano, J., and Williams, R.L. (2012) The UBAP1 subunit of ESCRT-I interacts with ubiquitin via a SOUBA domain. Structure 20, 414-428
49. Slagsvold, T., Aasland, R., Hirano, S., Bache, K.G., Raiborg, C., Trambaiolo, D., Wakatsuki, S., and Stenmark, H. (2005) Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem. 280, 19600-19606
50. Kulathu, Y., Akutsu, M., Bremm, A., Hofmann, K., and Komander, D. (2009) Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain. Nat. Struct. Mol. Biol. 16, 1328-1330
51. Dowlatshahi, D.P., Sandrin, V., Vivona, S., Shaler, T.A., Kaiser, S.E., Melandri, F., Sundquist, W.I., and Kopito, R.R. (2012) ALIX is a Lys63-specific polyubiquitin binding protein that functions in retrovirus budding. Dev. Cell 23, 1247-1254
52. Keren-Kaplan, T., Attali, I., Estrin, M., Kuo, L.S., Farkash, E., Jerabek-Willemsen, M., Blutraich, N., Artzi, S., Peri, A., Freed, E.O., Wolfson, H.J., and Prag, G. (2013) Structure-based in silico identification of ubiquitin-binding domains provides insights into the ALIX-V: Ubiquitin complex and retrovirus budding. EMBO J. 32, 538-551
53. Mizuno, E., Kawahata, K., Kato, M., Kitamura, N., and Komada, M. (2003) STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif. Mol. Biol. Cell 14, 3675-3689
54. Alam, S.L., Sun, J., Payne, M., Welch, B.D., Blake, B.K., Davis, D.R., Meyer, H.H., Emr, S.D., and Sundquist, W.I. (2004) Ubiquitin interactions of NZF zinc fingers. EMBO J. 23, 1411-1421
55. Hirano, S., Kawasaki, M., Ura, H., Kato, R., Raiborg, C., Stenmark, H., and Wakatsuki, S. (2006) Doublesided ubiquitin binding of Hrs-UIM in endosomal protein sorting. Nat. Struct. Mol. Biol. 13, 272-277
56. Stefani, F., Zhang, L., Taylor, S., Donovan, J., Rollinson, S., Doyotte, A., Brownhill, K., Bennion, J., Pickering-Brown, S., and Woodman, P. (2011) UBAP1 is a component of an endosome-specific ESCRT-I complex that is essential for MVB sorting. Curr. Biol. 21, 1245-1250
57. Ren, X. and Hurley, J.H. (2011) Proline-rich regions and motifs in trafficking: From ESCRT interaction to viral exploitation. Traffic 12, 1282-1290