RNF11 is a GGA protein cargo and acts as a molecular adaptor for GGA3 ubiquitination mediated by Itch

Oncogene

Volumn 34, Issue 26, 2015, Pages 3377-3390

  Santonico, E ^a   Mattioni, A ^a   Panni, S ^b   Belleudi, F ^c   Mattei, M ^a   Torrisi, M R ^c,d   Cesareni, G ^a,e   Castagnoli, L ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF CALABRIA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADP RIBOSYLATION FACTOR BINDING PROTEIN; ADP RIBOSYLATION FACTOR BINDING PROTEIN 1; ADP RIBOSYLATION FACTOR BINDING PROTEIN 2; ADP RIBOSYLATION FACTOR BINDING PROTEIN 3; GAMMA ADAPTIN; RING FINGER PROTEIN; RING FINGER PROTEIN 11; UNCLASSIFIED DRUG; CARRIER PROTEIN; CHAPERONE; GGA ADAPTOR PROTEINS; ITCH PROTEIN, HUMAN; PROTEIN BINDING; REPRESSOR PROTEIN; RNF11 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN TARGETING; RING FINGER MOTIF; TRANS GOLGI NETWORK; UBIQUITINATION; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; BINDING SITES; CARRIER PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; REPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84933278156     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.256     Document Type: Article

References (50)

1. Bonifacino JS, Lippincott-Schwartz J. Coat proteins: shaping membrane transport. Nat Rev Mol Cell Biol 2003; 4: 409-414.
2. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003; 72: 395-447.
3. Boman AL, Zhang CJ, Zhu X, Kahn RA. A family of ADP-ribosylation factor effectors that can alter membrane transport through the trans-Golgi. Mol Biol Cell 2000; 11: 1241-1255.
4. Dell'Angelica EC, Puertollano R, Mullins C, Aguilar RC, Vargas JD, Hartnell LM. GGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J Cell Biol 2000; 149: 81-94.
5. Hirst J, Lui WW, Bright NA, Totty N, Seaman MN, Robinson MS. A family of proteins with gamma-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J Cell Biol 2000; 149: 67-80.
6. Takatsu H, Yoshino K, Nakayama K. Adaptor gamma ear homology domain conserved in gamma-adaptin and GGA proteins that interact with gammasynergin. Biochem Biophys Res Commun 2000; 271: 719-725.
7. Jacobsen L, Madsen P, Nielsen MS, Geraerts WPM, Gliemann J, Smit AB. The sorLA cytoplasmic domain interacts with GGA1 and-2 and defines minimum requirements for GGA binding. FEBS Lett 2002; 511: 155-158.
8. Misra S, Puertollano R, Kato Y, Bonifacino JS, Hurley JH. Structural basis for acidic-cluster-dileucine sorting-signal recognition by VHS domains. Nature 2002; 415: 933-937.
9. Ghosh P, Kornfeld S. The GGA proteins: key players in protein sorting at the trans-Golgi network. Eur J Cell Biol 2004; 83: 257-262.
10. Bonifacino JS. The GGA proteins: adaptors on the move. Nat Rev Mol Cell Biol 2004; 5: 23-32.
11. Doray B, Misra S, Qian Y, Brett TJ, Kornfeld S. Do GGA adaptors bind internal DXXLL motifs? Traffic 2012; 13: 1315-1325.
12. Shiba Y, Katoh Y, Shiba T, Yoshino K, Takatsu H, Kobayashi H. GAT (GGA and Tom1) domain responsible for ubiquitin binding and ubiquitination. J Biol Chem 2004; 279: 7105-7111.
13. Scott PM, Bilodeau PS, Zhdankina O, Winistorfer SC, Hauglund MJ, Allaman MM. GGA proteins bind ubiquitin to facilitate sorting at the trans-Golgi network. Nat Cell Biol 2004; 6: 252-259.
14. Puertollano R, Bonifacino JS. Interactions of GGA3 with the ubiquitin sorting machinery. Nat Cell Biol 2004; 6: 244-251.
15. Puertollano R, Randazzo PA, Presley JF, Hartnell LM, Bonifacino JS. The GGAs promote ARF-dependent recruitment of clathrin to the TGN. Cell 2001; 105: 93-102.
16. Puertollano R, Aguilar RC, Gorshkova I, Crouch RJ, Bonifacino JS. Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 2001; 292: 1712-1716.
17. Zhu Y, Doray B, Poussu A, Lehto VP, Kornfeld S. Binding of GGA2 to the lysosomal enzyme sorting motif of the mannose 6-phosphate receptor. Science 2001; 292: 1716-1718.
18. Takatsu H, Katoh Y, Shiba Y, Nakayama K. Golgi-localizing, gamma-adaptin ear homology domain, ADP-ribosylation factor-binding (GGA) proteins interact with acidic dileucine sequences within the cytoplasmic domains of sorting receptors through their Vps27p/Hrs/STAM (VHS) domains. J Biol Chem 2001; 276: 28541-28545.
19. Nielsen MS, Madsen P, Christensen EI, Nykjaer A, Gliemann J, Kasper D. The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J 2001; 20: 2180-2190.
20. He X, Chang W-P, Koelsch G, Tang J. Memapsin 2 (beta-secretase) cytosolic domain binds to the VHS domains of GGA1 and GGA2: implications on the endocytosis mechanism of memapsin 2. FEBS Lett 2002; 524: 183-187.
21. Boucher R, Larkin H, Brodeur J, Gagnon H, Thériault C, Lavoie C. Intracellular trafficking of LRP9 is dependent on two acidic cluster/dileucine motifs. Histochem Cell Biol 2008; 130: 315-327.
22. Santonico E, Belleudi F, Panni S, Torrisi MR, Cesareni G, Castagnoli L. Multiple modification and protein interaction signals drive the Ring finger protein 11 (RNF11) E3 ligase to the endosomal compartment. Oncogene 2010; 29: 5604-5618.
23. Burger AM, Zhang X, Li H, Ostrowski JL, Beatty B, Venanzoni M. Down-regulation of T1A12/mac25, a novel insulin-like growth factor binding protein related gene, is associated with disease progression in breast carcinomas. Oncogene 1998; 16: 2459-2467.
24. Seki N, Hattori A, Hayashi A, Kozuma S, Sasaki M, Suzuki Y. Cloning and expression profile of mouse and human genes, Rnf11/RNF11, encoding a novel RING-H2 finger protein. Biochim Biophys Acta 1999; 1489: 421-427.
25. Sudol M, Hunter T. NeW wrinkles for an old domain. Cell 2000; 103: 1001-1004.
26. Kitching R, Wong MJ, Koehler D, Burger AM, Landberg G, Gish G. The RING-H2 protein RNF11 is differentially expressed in breast tumours and interacts with HECT-type E3 ligases. Biochim Biophys Acta 2003; 1639: 104-112.
27. Bernassola F, Karin M, Ciechanover A, Melino G. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 2008; 14: 10-21.
28. van Wijk SJL, Timmers HTM. The family of ubiquitin-conjugating enzymes (E2s): deciding between life and death of proteins. FASEB J 2010; 24: 981-993.
29. Li H, Seth A. An RNF11: Smurf2 complex mediates ubiquitination of the AMSH protein. Oncogene 2004; 23: 1801-1808.
30. Azmi P, Seth A. RNF11 is a multifunctional modulator of growth factor receptor signalling and transcriptional regulation. Eur J Cancer 2005; 41: 2549-2560.
31. Shembade N, Parvatiyar K, Harhaj NS, Harhaj EW. The ubiquitin-editing enzyme A20 requires RNF11 to downregulate NF-kappaB signalling. EMBO J 2009; 28: 513-522.
32. Kostaras E, Sflomos G, Pedersen NM, Stenmark H, Fotsis T, Murphy C. SARA and RNF11 interact with each other and ESCRT-0 core proteins and regulate degradative EGFR trafficking. Oncogene 2013; 32: 5220-5232.
33. Frank R. The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports-principles and applications. J Immunol Methods 2002; 267: 13-26.
34. Pastorino L, Ikin AF, Nairn AC, Pursnani A, Buxbaum JD. The carboxyl-terminus of BACE contains a sorting signal that regulates BACE trafficking but not the formation of total A(beta). Mol Cell Neurosci 2002; 19: 175-185.
35. Huse JT, Pijak DS, Leslie GJ, Lee VM, Doms RW. Maturation and endosomal targeting of beta-site amyloid precursor protein-cleaving enzyme. The Alzheimer's disease beta-secretase. J Biol Chem 2000; 275: 33729-33737.
36. Simons K, Zerial M. Rab proteins and the road maps for intracellular transport. Neuron 1993; 11: 789-799.
37. Mattera R, Boehm M, Chaudhuri R, Prabhu Y, Bonifacino JS. Conservation and diversification of dileucine signal recognition by adaptor protein (AP) complex variants. J Biol Chem 2011; 286: 2022-2030.
38. Söderberg O, Gullberg M, Jarvius M, Ridderstråle K, Leuchowius K-J, Jarvius J. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 2006; 3: 995-1000.
39. Söderberg O, Leuchowius K-J, Gullberg M, Jarvius M, Weibrecht I, Larsson L-G. Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 2008; 45: 227-232.
40. Weibrecht I, Leuchowius K-J, Clausson C-M, Conze T, Jarvius M, Howell WM. Proximity ligation assays: a recent addition to the proteomics toolbox. Expert Rev Proteomics 2010; 7: 401-409.
41. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994; 127: 915-934.
42. Hicke L. Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2001; 2: 195-201.
43. Hoppe T. Multiubiquitylation by E4 enzymes: 'one size' doesn't fit all. Trends Biochem Sci 2005; 30: 183-187.
44. Pak Y, Glowacka WK, Bruce MC, Pham N, Rotin D. Transport of LAPTM5 to lysosomes requires association with the ubiquitin ligase Nedd4, but not LAPTM5 ubiquitination. J Cell Biol 2006; 175: 631-645.
45. Oberst A, Malatesta M, Aqeilan RI, Rossi M, Salomoni P, Murillas R. The Nedd4-binding partner 1 (N4BP1) protein is an inhibitor of the E3 ligase Itch. Proc Natl Acad Sci USA 2007; 104: 11280-11285.
46. Parachoniak CA, Luo Y, Abella JV, Keen JH, Park M. GGA3 functions as a switch to promote Met receptor recycling, essential for sustained ERK and cell migration. Dev Cell 2011; 20: 751-763.
47. Clague MJ. Met receptor: a moving target. Sci Signal 2011; 4: pe40.
48. Chen C, Zhou Z, Liu R, Li Y, Azmi PB, Seth AK. The WW domain containing E3 ubiquitin protein ligase 1 upregulates ErbB2 and EGFR through RING finger protein 11. Oncogene 2008; 27: 6845-6855.
49. Burger A, Amemiya Y, Kitching R, Seth AK. Novel RING E3 ubiquitin ligases in breast cancer. Neoplasia 2006; 8: 689-695.
50. Santonico E, Panni S, Falconi M, Castagnoli L, Cesareni G. Binding to DPF-motif by the POB1 EH domain is responsible for POB1-Eps15 interaction. BMC Biochem 2007; 8: 29.