Site-specific ubiquitination determines lysosomal sorting and signal attenuation of the granulocyte colony-stimulating factor receptor

Traffic

Volumn 10, Issue 8, 2009, Pages 1168-1179

  Wölfler, Albert ^a,b   Irandoust, Mahban ^a   Meenhuis, Annemarie ^a   Gits, Judith ^a   Roovers, Onno ^a   Touw, Ivo P ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Congenital neutropenia; G CSF receptor; Leukemia; Lysosomal routing; Suppressor of cytokine signaling; Ubiquitination

Indexed keywords

BETA CYCLODEXTRIN; GRANULOCYTE COLONY STIMULATING FACTOR RECEPTOR; LYSINE; MUTANT PROTEIN; SUCROSE; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ARTICLE; CANCER RISK; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; INTERNALIZATION; LEUKEMIA; LYSOSOME; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NEUTROPENIA; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; DNA MUTATIONAL ANALYSIS; ENDOCYTOSIS; HELA CELLS; HUMANS; LYSINE; LYSOSOMES; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; RECEPTORS, GRANULOCYTE COLONY-STIMULATING FACTOR; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; UBIQUITINATION;

EID: 67649888820     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00928.x     Document Type: Article

References (46)

1. Akbarzadeh S, Layton JE. Granulocyte colony-stimulating factor receptor: structure and function. Vitam Horm 2001;63:159-194.
2. Avalos BR, Gasson JC, Hedvat C, Quan SG, Baldwin GC, Weisbart RH, Williams RE, Golde DW, DiPersio JF. Human granulocyte colony-stimulating factor: Biologic activities and receptor characterization on hematopoietic cells and small cell lung cancer cell lines. Blood 1990;75:851-857.
3. Touw IP, van de Geijn GJ. Granulocyte colony-stimulating factor and its receptor in normal myeloid cell development, leukemia and related blood cell disorders. Front Biosci 2007;12:800-815.
4. Germeshausen M, Ballmaier M, Welte K. Incidence of CSF3R mutations in severe congenital neutropenia and relevance for leukemogenesis: Results of a long-term survey. Blood 2007;109:93-99.
5. Hunter MG, Avalos BR. Deletion of a critical internalization domain in the G-CSFR in acute myelogenous leukemia preceded by severe congenital neutropenia. Blood 1999;93:440-446.
6. Ward AC, van Aesch YM, Schelen AM, Touw IP. Defective internalization and sustained activation of truncated granulocyte colony-stimulating factor receptor found in severe congenital neutropenia/acute myeloid leukemia. Blood 1999;93:447-458.
7. Hermans MH, van de Geijn GJ, Antonissen C, Gits J, van Leeuwen D, Ward AC, Touw IP. Signaling mechanisms coupled to tyrosines in the granulocyte colony-stimulating factor receptor orchestrate G-CSF-induced expansion of myeloid progenitor cells. Blood 2003;101:2584-2590.
8. Hortner M, Nielsch U, Mayr LM, Johnston JA, Heinrich PC, Haan S. Suppressor of cytokine signaling-3 is recruited to the activated granulocyte-colony stimulating factor receptor and modulates its signal transduction. J Immunol 2002;169:1219-1227.
9. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007;315:201-205.
10. Marmor MD, Yarden Y. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 2004;23:2057-2070.
11. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 2006;21:737-748.
12. Huang F, Goh LK, Sorkin A. EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci U S A 2007;104:16904-16909.
13. Belouzard S, Rouille Y. Ubiquitylation of leptin receptor OB-Ra regulates its clathrin-mediated endocytosis. EMBO J 2006;25:932-942.
14. Kumar KG, Barriere H, Carbone CJ, Liu J, Swaminathan G, Xu P, Li Y, Baker DP, Peng J, Lukacs GL, Fuchs SY. Site-specific ubiquitination exposes a linear motif to promote interferon-alpha receptor endocytosis. J Cell Biol 2007;179:935-950.
15. Irandoust MI, Aarts LH, Roovers O, Gits J, Erkeland SJ, Touw IP. Suppressor of cytokine signaling 3 controls lysosomal routing of G-CSF receptor. EMBO J 2007;26:1782-1793.
16. Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 2007;7:454-465.
17. Kamura T, Maenaka K, Kotoshiba S, Matsumoto M, Kohda D, Conaway RC, Conaway JW, Nakayama KI. VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes Dev 2004;18:3055-3065.
18. Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, Dikic I. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 2003;5:461-466.
19. Hicke L, Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 2003;19:141-172.
20. Raiborg C, Rusten TE, Stenmark H. Protein sorting into multivesicular endosomes. Curr Opin Cell Biol 2003;15:446-455.
21. Sigismund S, Polo S, Di Fiore PP. Signaling through monoubiquitination. Curr Top Microbiol Immunol 2004;286:149-185.
22. Hunter T. The age of crosstalk: Phosphorylation, ubiquitination, and beyond. Mol Cell 2007;28:730-738.
23. Laney JD, Hochstrasser M. Substrate targeting in the ubiquitin system. Cell 1999;97:427-430.
24. Fuchs SY, Spiegelman VS, Kumar KG. The many faces of beta-TrCP E3 ubiquitin ligases: Reflections in the magic mirror of cancer. Oncogene 2004;23:2028-2036.
25. Kumar KG, Tang W, Ravindranath AK, Clark WA, Croze E, Fuchs SY. SCF(HOS) ubiquitin ligase mediates the ligand-induced down-regulation of the interferon-alpha receptor. EMBO J 2003;22:5480-5490.
26. Aarts LH, Roovers O, Ward AC, Touw IP. Receptor activation and 2 distinct COOH-terminal motifs control G-CSF receptor distribution and internalization kinetics. Blood 2004;103:571-579.
27. Meyer L, Deau B, Forejtnikova H, Dumenil D, Margottin-Goguet F, Lacombe C, Mayeux P, Verdier F. Beta-Trcp mediates ubiquitination and degradation of the erythropoietin receptor and controls cell proliferation. Blood 2007;109:5215-5222.
28. Alam SL, Langelier C, Whitby FG, Koirala S, Robinson H, Hill CP, Sundquist WI. Structural basis for ubiquitin recognition by the human ESCRT-II EAP45 GLUE domain. Nat Struct Mol Biol 2006;13:1029-1030.
29. Tanaka Y, Hamano S, Gotoh K, Murata Y, Kunisaki Y, Nishikimi A, Takii R, Kawaguchi M, Inayoshi A, Masuko S, Himeno K, Sasazuki T, Fukui Y. T helper type 2 differentiation and intracellular trafficking of the interleukin 4 receptor-alpha subunit controlled by the Rac activator Dock2. Nat Immunol 2007;8:1067-1075.
30. Traub LM, Lukacs GL. Decoding ubiquitin sorting signals for clathrin-dependent endocytosis by CLASPs. J Cell Sci 2007;120:543-553.
31. Umebayashi K, Stenmark H, Yoshimori T. Ubc4/5 and c-Cbl continue to ubiquitinate EGF receptor after internalization to facilitate polyubiquitination and degradation. Mol Biol Cell 2008;19:3454-3462.
32. King RW, Deshaies RJ, Peters JM, Kirschner MW. How proteolysis drives the cell cycle. Science 1996;274:1652-1659.
33. Mosesson Y, Shtiegman K, Katz M, Zwang Y, Vereb G, Szollosi J, Yarden Y. Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem 2003;278:21323-21326.
34. Slagsvold T, Pattni K, Malerod L, Stenmark H. Endosomal and non-endosomal functions of ESCRT proteins. Trends Cell Biol 2006;16:317-326.
35. Slagsvold T, Aasland R, Hirano S, Bache KG, Raiborg C, Trambaiolo D, Wakatsuki S, Stenmark H. Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J Biol Chem 2005;280:19600-19606.
36. Teo H, Gill DJ, Sun J, Perisic O, Veprintsev DB, Vallis Y, Emr SD, Williams RL. ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 2006;125:99-111.
37. Dong F, Brynes RK, Tidow N, Welte K, Lowenberg B, Touw IP. Mutations in the gene for the granulocyte colony-stimulating-factor receptor in patients with acute myeloid leukemia preceded by severe congenital neutropenia. N Engl J Med 1995;333:487-493.
38. Kindwall-Keller TL, Druhan LJ, Ai J, Hunter MG, Massullo P, Loveland M, Avalos BR. Role of the proteasome in modulating native G-CSFR expression. Cytokine 2008;43:114-123.
39. Govers R, ten Broeke T, van Kerkhof P, Schwartz AL, Strous GJ. Identification of a novel ubiquitin conjugation motif, required for ligand-induced internalization of the growth hormone receptor. EMBO J 1999;18:28-36.
40. Duncan LM, Piper S, Dodd RB, Saville MK, Sanderson CM, Luzio JP, Lehner PJ. Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J 2006;25:1635-1645.
41. Walter RB, Hausermann P, Raden BW, Teckchandani AM, Kamikura DM, Bernstein ID, Cooper JA. Phosphorylated ITIMs enable ubiquitylation of an inhibitory cell surface receptor. Traffic 2008;9:267-279.
42. Liu F, Kunter G, Krem MM, Eades WC, Cain JA, Tomasson MH, Hennighausen L, Link DC. Csf3r mutations in mice confer a strong clonal HSC advantage via activation of Stat5. J Clin Invest 2008;118:946-955.
43. van de Geijn GJ, Gits J, Aarts LH, Heijmans-Antonissen C, Touw IP. G-CSF receptor truncations found in SCN/AML relieve SOCS3-controlled inhibition of STAT5 but leave suppression of STAT3 intact. Blood 2004;104:667-674.
44. de Koning JP, Soede-Bobok AA, Schelen AM, Smith L, van Leeuwen D, Santini V, Burgering BM, Bos JL, Lowenberg B, Touw IP. Proliferation signaling and activation of Shc, p21Ras, and Myc via tyrosine 764 of human granulocyte colony-stimulating factor receptor. Blood 1998;91:1924-1933.
45. Hermans MH, Antonissen C, Ward AC, Mayen AE, Ploemacher RE, Touw IP. Sustained receptor activation and hyperproliferation in response to granulocyte colony-stimulating factor (G-CSF) in mice with a severe congenital neutropenia/acute myeloid leukemia-derived mutation in the G-CSF receptor gene. J Exp Med 1999;189:683-692.
46. Raiborg C, Bache KG, Gillooly DJ, Madshus IH, Stang E, Stenmark H. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 2002;4:394-398.