Nedd4-1 binds and ubiquitylates activated FGFR1 to control its endocytosis and function

EMBO Journal

Volumn 30, Issue 16, 2011, Pages 3259-3273

  Persaud, Avinash ^a,b   Alberts, Philipp ^a,b   Hayes, Madeline ^a,b   Guettler, Sebastian ^b,c   Clarke, Ian ^a,b   Sicheri, Frank ^b,c   Dirks, Peter ^a,b   Ciruna, Brian ^a,b   Rotin, Daniela ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

Author keywords

E3 ubiquitin ligase; endocytosis; FGF receptor; Nedd4; WW domain

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUTANT PROTEIN; PHOSPHOLIPASE C GAMMA; PROTEIN; PROTEIN FRS2ALPHA; PROTEIN KINASE B; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; ESCRT PROTEIN; FGFR1 PROTEIN, HUMAN; HYBRID PROTEIN; NEDD4 UBIQUITIN PROTEIN LIGASES; PEPTIDE FRAGMENT; UBIQUITIN PROTEIN LIGASE;

ARTICLE; DOWNSTREAM PROCESSING; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENDOCYTOSIS; GENE SILENCING; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UBIQUITINATION; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CHEMISTRY; CYTOLOGY; ENZYME SPECIFICITY; GENETICS; METABOLISM; MOLECULAR GENETICS; MORPHOGENESIS; NERVE CELL; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN TRANSPORT; RAT; SPECIES DIFFERENCE; STEM CELL;

ANIMALIA; DANIO RERIO;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BODY PATTERNING; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE KNOCKDOWN TECHNIQUES; HUMANS; MOLECULAR SEQUENCE DATA; NEURONS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RATS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; STEM CELLS; SUBSTRATE SPECIFICITY; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; ZEBRAFISH;

EID: 80155192453     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.234     Document Type: Article

References (54)

1. Abriel H, Loffing J, Rebhun JF, Pratt JH, Schild L, Horisberger JD, Rotin D, Staub O (1999) Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle's syndrome. J Clin Invest 103: 667-673
2. Arevalo JC, Waite J, Rajagopal R, Beyna M, Chen ZY, Lee FS, Chao MV (2006) Cell survival through Trk neurotrophin receptors is differentially regulated by ubiquitination. Neuron 50: 549-559
3. Bache KG, Slagsvold T, Stenmark H (2004) Defective downregulation of receptor tyrosine kinases in cancer. EMBO J 23: 2707-2712
4. Cao XR, Lill NL, Boase N, Shi PP, Croucher DR, Shan H, Qu J, Sweezer EM, Place T, Kirby PA, Daly RJ, Kumar S, Yang B (2008) Nedd4 controls animal growth by regulating IGF-1 signaling. Sci Signal 1: ra5
5. Chi CL, Martinez S, Wurst W, Martin GR (2003) The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130: 2633-2644
6. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A (2005) Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3: e283
7. Eswarakumar VP, Lax I, Schlessinger J (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16: 139-149
8. Fouladkou F, Lu C, Jiang C, Zhou L, She Y,Walls JR, Kawabe H, Brose N, Henkelman RM, Huang A, Bruneau BG, Rotin D (2010) The ubiquitin ligase Nedd4-1 is required for heart development and is a suppressor of thrombospondin-1. J Biol Chem 285: 6770-6780
9. Furthauer M, Thisse C, Thisse B (1997) A role for FGF-8 in the dorsoventral patterning of the zebrafish gastrula. Development 124: 4253-4264
10. 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: 871-883
11. Griffin K, Patient R, Holder N (1995) Analysis of FGF function in normal and no tail zebrafish embryos reveals separate mechanisms for formation of the trunk and the tail. Development 121: 2983-2994
12. Haugsten EM, Malecki J, Bjorklund SM, Olsnes S, Wesche J (2008) Ubiquitination of fibroblast growth factor receptor 1 is required for its intracellular sorting but not for its endocytosis. Mol Biol Cell 19: 3390-3403
13. Kamynina E, Debonneville C, Bens M, Vandewalle A, Staub O (2001) A novel mouse Nedd4 protein suppresses the activity of the epithelial Na+ channel. FASEB J 15: 204-214
14. Kanelis V, Bruce MC, Skrynnikov NR, Rotin D, Forman-Kay JD (2006) Structural determinants for high-affinity binding in a Nedd4 WW3* domain-Comm PY motif complex. Structure 14: 543-553
15. Kanelis V, Rotin D, Forman-Kay JD (2001) Solution structure of a Nedd4 WW domain-ENaC peptide complex. Nat Struct Biol 8: 407-412
16. Kawabe H, Neeb A, Dimova K, Young Jr SM, Takeda M, Katsurabayashi S, Mitkovski M, Malakhova OA, Zhang DE, Umikawa M, Kariya K, Goebbels S, Nave KA, Rosenmund C, Jahn O, Rhee J, Brose N (2010) Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development. Neuron 65: 358-372
17. Kimura T, Kawabe H, Jiang C, Zhang W, Xiang YY, Lu C, Salter MW, Brose N, Lu WY, Rotin D (2011) Deletion of the ubiquitin ligase Nedd4L in lung epithelia causes cystic fibrosis-like disease. Proc Natl Acad Sci USA 108: 3216-3221
18. Krauss S, Johansen T, Korzh V, Fjose A (1991) Expression pattern of zebrafish pax genes suggests a role in early brain regionalization. Nature 353: 267-270
19. Lamb TM, Harland RM (1995) Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anteriorposterior neural pattern. Development 121: 3627-3636
20. Lee PL, Johnson DE, Cousens LS, Fried VA, Williams LT (1989) Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science 245: 57-60
21. Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141: 1117-1134
22. Liu A, Losos K, Joyner AL (1999) FGF8 can activate Gbx2 and transform regions of the rostral mouse brain into a hindbrain fate. Development 126: 4827-4838
23. Liu Y, Oppenheim RW, Sugiura Y, Lin W (2009) Abnormal development of the neuromuscular junction in Nedd4-deficient mice. Dev Biol 330: 153-166
24. Marmor MD, Yarden Y (2004) Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23: 2057-2070
25. Martinez S, Crossley PH, Cobos I, Rubenstein JL, Martin GR (1999) FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression. Development 126: 1189-1200
26. Mohammadi M, Honegger AM, Rotin D, Fischer R, Bellot F, Li W, Dionne CA, Jaye M, Rubinstein M, Schlessinger J (1991) A tyrosine-phosphorylated carboxy-terminal peptide of the fibroblast growth factor receptor (Flg) is a binding site for the SH2 domain of phospholipase C-gamma 1. Mol Cell Biol 11: 5068-5078
27. Mohammadi M, Schlessinger J, Hubbard SR (1996) Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86: 577-587
28. Morita T, Nitta H, Kiyama Y, Mori H, Mishina M (1995) Differential expression of two zebrafish emx homeoprotein mRNAs in the developing brain. Neurosci Lett 198: 131-134
29. Nowak M, Machate A, Yu SR, Gupta M, Brand M (2011) Interpretation of the FGF8 morphogen gradient is regulated by endocytic trafficking. Nat Cell Biol 13: 153-158
30. Ota S, Tonou-Fujimori N, Nakayama Y, Ito Y, Kawamura A, Yamasu K (2010) FGF receptor gene expression and its regulation by FGF signaling during early zebrafish development. Genesis 48: 707-716
31. Ota S, Tonou-Fujimori N, Yamasu K (2009) The roles of the FGF signal in zebrafish embryos analyzed using constitutive activation and dominant-negative suppression of different FGF receptors. Mech Dev 126: 1-17
32. Oxtoby E, Jowett T (1993) Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res 21: 1087-1095
33. Pak Y, Glowacka WK, Bruce MC, Pham N, Rotin D (2006) Transport of LAPTM5 to lysosomes requires association with the ubiquitin ligase Nedd4, but not LAPTM5 ubiquitination. J Cell Biol 175: 631-645
34. Persaud A, Alberts P, Amsen EM, Xiong X, Wasmuth J, Saadon Z, Fladd C, Parkinson J, Rotin D (2009) Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Mol Syst Biol 5: 333
35. Peschard P, Fournier TM, Lamorte L, Naujokas MA, Band H, Langdon WY, Park M (2001) Mutation of the c-Cbl TKB domain binding site on the Met receptor tyrosine kinase converts it into a transforming protein. Mol Cell 8: 995-1004
36. Pham N, Rotin D (2001) Nedd4 regulates ubiquitination and stability of the guanine-nucleotide exchange factor CNrasGEF. J Biol Chem 276: 46995-47003
37. Plant PJ, Yeger H, Staub O, Howard P, Rotin D (1997) The C2 domain of the ubiquitin protein ligase Nedd4 mediates Ca2+-dependent plasma membrane localization. J Biol Chem 272: 32329-32336
38. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, Bayani J, Head R, Lee M, Bernstein M, Squire JA, Smith A, Dirks P (2009) Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 4: 568-580
39. Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, Bossi G, Chen H, De Camilli P, Di Fiore PP (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416: 451-455
40. Rathinam C, Thien CB, Flavell RA, Langdon WY (2010) Myeloid leukemia development in c-Cbl RING finger mutant mice is dependent on FLT3 signaling. Cancer Cell 18: 341-352
41. Rotin D, Kumar S (2009) Physiological functions of the HECT family of ubiquitin ligases. Nat Rev Mol Cell Biol 10: 398-409
42. Sargin B, Choudhary C, Crosetto N, Schmidt MH, Grundler R, Rensinghoff M, Thiessen C, Tickenbrock L, Schwable J, Brandts C, August B, Koschmieder S, Bandi SR, Duyster J, Berdel WE, Muller-Tidow C, Dikic I, Serve H (2007) Flt3-dependent transformation by inactivating c-Cbl mutations in AML. Blood 110: 1004-1012
43. Scholpp S, Groth C, Lohs C, Lardelli M, Brand M (2004) Zebrafish fgfr1 is a member of the fgf8 synexpression group and is required for fgf8 signalling at the midbrain-hindbrain boundary. Dev Genes Evol 214: 285-295
44. Shi PP, Cao XR, Sweezer EM, Kinney TS, Williams NR, Husted RF, Nair R, Weiss RM, Williamson RA, Sigmund CD, Snyder PM, Staub O, Stokes JB, Yang B (2008) Salt-sensitive hypertension and cardiac hypertrophy in mice deficient in the ubiquitin ligase Nedd4-2. Am J Physiol Renal Physiol 295: F462-F470
45. Snyder PM, Olson DR, McDonald FJ, Bucher DB (2001) Multiple WW domains, but not the C2 domain, are required for inhibition of the epithelial Na+ channel by human Nedd4. J Biol Chem 276: 28321-28326
46. Sorokin A, Mohammadi M, Huang J, Schlessinger J (1994) Internalization of fibroblast growth factor receptor is inhibited by a point mutation at tyrosine 766. J Biol Chem 269: 17056-17061
47. Soubeyran P, Kowanetz K, Szymkiewicz I, Langdon WY, Dikic I (2002) Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416: 183-187
48. Staub O, Dho S, Henry P, Correa J, Ishikawa T, McGlade J, Rotin D (1996) WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome. EMBO J 15: 2371-2380
49. Trokovic R, Trokovic N, Hernesniemi S, Pirvola U, Vogt Weisenhorn DM, Rossant J, McMahon AP, Wurst W, Partanen J (2003) FGFR1 is independently required in both developing mid-and hindbrain for sustained response to isthmic signals. EMBO J 22: 1811-1823
50. Turner N, Grose R (2010) Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 10: 116-129
51. Vecchione A, Marchese A, Henry P, Rotin D, Morrione A (2003) The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Mol Cell Biol 23: 3363-3372
52. Waterman H, Levkowitz G, Alroy I, Yarden Y (1999) The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor. J Biol Chem 274: 22151-22154
53. Wong A, Lamothe B, Lee A, Schlessinger J, Lax I (2002) FRS2 alpha attenuates FGF receptor signaling by Grb2-mediated recruitment of the ubiquitin ligase Cbl. Proc Natl Acad Sci USA 99: 6684-6689
54. Yang B, Gay DL, MacLeod MK, Cao X, Hala T, Sweezer EM, Kappler J, Marrack P, Oliver PM (2008) Nedd4 augments the adaptive immune response by promoting ubiquitin-mediated degradation of Cbl-b in activated T cells. Nat Immunol 9: 1356-1363