Lysine 63-linked polyubiquitination is required for EGF receptor degradation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 39, 2013, Pages 15722-15727

  Huang, Fangtian ^a   Zeng, Xuemei ^b   Kim, Woong ^c   Balasubramani, Manimalha ^b   Fortian, Arola ^a   Gygi, Steven P ^c   Yates, Nathan A ^a,b   Sorkin, Alexander ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; POLYUBIQUITIN; PROTEIN SH3;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; STOICHIOMETRY; UBIQUITINATION; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOTHELIAL CELLS; HUMANS; KINETICS; LYSINE; LYSOSOMES; MOLECULAR SEQUENCE DATA; POLYUBIQUITIN; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SUS SCROFA; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 84884613817     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1308014110     Document Type: Article

References (48)

1. Acconcia F, Sigismund S, Polo S (2009) Ubiquitin in trafficking: The network at work. Exp Cell Res 315(9):1610-1618.
2. Hurley JH, Stenmark H (2011) Molecular mechanisms of ubiquitin-dependent membrane traffic. Annu Rev Biophys 40:119-142.
3. Clague MJ, Liu H, Urbé S (2012) Governance of endocytic trafficking and signaling by reversible ubiquitylation. Dev Cell 23(3):457-467.
4. Pickart CM (2001) Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533.
5. Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78:363-397.
6. Walczak H, Iwai K, Dikic I (2012) Generation and physiological roles of linear ubiquitin chains. BMC Biol 10:23.
7. Rahighi S, Dikic I (2012) Selectivity of the ubiquitin-binding modules. FEBS Lett 586(17):2705-2710.
8. Varadan R, et al. (2004) Solution conformation of Lys63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling. J Biol Chem 279(8): 7055-7063.
9. Sekiyama N, et al. (2012) NMR analysis of Lys63-linked polyubiquitin recognition by the tandem ubiquitin-interacting motifs of Rap80. J Biomol NMR 52(4):339-350.
10. Kulathu Y, Akutsu M, Bremm A, Hofmann K, Komander D (2009) Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain. Nat Struct Mol Biol 16(12): 1328-1330.
11. Komander D, Rape M (2012) The ubiquitin code. Annu Rev Biochem 81:203-229.
12. Ye Y, et al. (2012) Ubiquitin chain conformation regulates recognition and activity of interacting proteins. Nature 492(7428):266-270.
13. Galcheva-Gargova Z, Theroux SJ, Davis RJ (1995) The epidermal growth factor receptor is covalently linked to ubiquitin. Oncogene 11(12):2649-2655.
14. Sibilia M, et al. (2007) The epidermal growth factor receptor: From development to tumorigenesis. Differentiation 75(9):770-787.
15. Levkowitz G, et al. (1998) c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 12(23):3663-3674.
16. Stang E, Johannessen LE, Knardal SL, Madshus IH (2000) Polyubiquitination of the epidermal growth factor receptor occurs at the plasma membrane upon ligandinduced activation. J Biol Chem 275(18):13940-13947.
17. Umebayashi K, Stenmark H, Yoshimori T (2008) Ubc4/5 and c-Cbl continue to ubiquitinate EGF receptor after internalization to facilitate polyubiquitination and degradation. Mol Biol Cell 19(8):3454-3462.
18. Goh LK, Huang F, Kim W, Gygi S, Sorkin A (2010) Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J Cell Biol 189(5):871-883.
19. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A (2006) Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 21(6):737-748.
20. Haglund K, et al. (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 5(5):461-466.
21. Argenzio E, et al. (2011) Proteomic snapshot of the EGF-induced ubiquitin network. Mol Syst Biol 7:462.
22. Meijer IM, van Rotterdam W, van Zoelen EJ, van Leeuwen JE (2012) Recycling of EGFR and ErbB2 is associated with impaired Hrs tyrosine phosphorylation and decreased deubiquitination by AMSH. Cell Signal 24(11):1981-1988.
23. Galan JM, Haguenauer-Tsapis R (1997) Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J 16(19):5847-5854.
24. Paiva S, et al. (2009) Glucose-induced ubiquitylation and endocytosis of the yeast Jen1 transporter: Role of lysine 63-linked ubiquitin chains. J Biol Chem 284(29): 19228-19236.
25. Erpapazoglou Z, et al. (2012) A dual role for K63-linked ubiquitin chains in multivesicular body biogenesis and cargo sorting. Mol Biol Cell 23(11):2170-2183.
26. Lauwers E, Jacob C, André B (2009) K63-linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway. J Cell Biol 185(3):493-502.
27. Lauwers E, Erpapazoglou Z, Haguenauer-Tsapis R, André B (2010) The ubiquitin code of yeast permease trafficking. Trends Cell Biol 20(4):196-204.
28. Stringer DK, Piper RC (2011) A single ubiquitin is sufficient for cargo protein entry into MVBs in the absence of ESCRT ubiquitination. J Cell Biol 192(2):229-242.
29. Geetha T, Jiang J, Wooten MW (2005) Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Mol Cell 20(2): 301-312.
30. Vina-Vilaseca A, Sorkin A (2010) Lysine 63-linked polyubiquitination of the dopamine transporter requires WW3 and WW4 domains of Nedd4-2 and UBE2D ubiquitinconjugating enzymes. J Biol Chem 285(10):7645-7656.
31. Duncan LM, et al. (2006) Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J 25(8):1635-1645.
32. Zhang L, Xu M, Scotti E, Chen ZJ, Tontonoz P (2013) Both K63 and K48 ubiquitin linkages signal lysosomal degradation of the LDL receptor. J Lipid Res 54(5): 1410-1420.
33. Kumar KG, et al. (2007) Site-specific ubiquitination exposes a linear motif to promote interferon-alpha receptor endocytosis. J Cell Biol 179(5):935-950.
34. Mao Y, et al. (2011) Polyubiquitination of insulin-like growth factor I receptor (IGF-IR) activation loop promotes antibody-induced receptor internalization and down-regulation. J Biol Chem 286(48):41852-41861.
35. Marx C, Held JM, Gibson BW, Benz CC (2010) ErbB2 trafficking and degradation associated with K48 and K63 polyubiquitination. Cancer Res 70(9):3709-3717.
36. Kirkpatrick DS, et al. (2006) Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat Cell Biol 8(7):700-710.
37. Barriere H, Nemes C, Du K, Lukacs GL (2007) Plasticity of polyubiquitin recognition as lysosomal targeting signals by the endosomal sorting machinery. Mol Biol Cell 18(10): 3952-3965.
38. Hawryluk MJ, et al. (2006) Epsin 1 is a polyubiquitin-selective clathrin-associated sorting protein. Traffic 7(3):262-281.
39. Ren X, Hurley JH (2010) VHS domains of ESCRT-0 cooperate in high-avidity binding to polyubiquitinated cargo. EMBO J 29(6):1045-1054.
40. Sato Y, et al. (2008) Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains. Nature 455(7211):358-362.
41. Davies CW, Paul LN, Kim MI, Das C (2011) Structural and thermodynamic comparison of the catalytic domain of AMSH and AMSH-LP: Nearly identical fold but different stability. J Mol Biol 413(2):416-429.
42. Polo S, et al. (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416(6879):451-455.
43. Urbé S, et al. (2003) The UIM domain of Hrs couples receptor sorting to vesicle formation. J Cell Sci 116(Pt 20):4169-4179.
44. Caunt CJ, Keyse SM (2013) Dual-specificity MAP kinase phosphatases (MKPs): Shaping the outcome of MAP kinase signalling. FEBS J 280(2):489-504.
45. Mosesson Y, et al. (2003) Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem 278(24):21323-21326.
46. Carter RE, Sorkin A (1998) Endocytosis of functional epidermal growth factor receptor-green fluorescent protein chimera. J Biol Chem 273(52):35000-35007.
47. Zeng X, et al. (2011) Lung cancer serum biomarker discovery using label-free liquid chromatography-tandem mass spectrometry. J Thorac Oncol 6(4):725-734.
48. MacLean B, et al. (2010) Skyline: An open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26(7):966-968.