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Other ubiquitylated endocytic proteins

In addition to ubiquitylation of UIM-containing endocytic proteins, a number of other proteins of the endocytic machinery were described to undergo ubiquitylation. The list of examples of substrates/E3 pairs is extending, but clear ideas about the corresponding functions of this modification is often lacking. Examples include once more proteins invi-olved in the internalization step or in later endocytic steps. We already described the link between Rsp5p and endocytic proteins important for the organization of the actin cytoskeleton, and the function still undefined of Rvs167/amphiphysin ubiquitylation [107]. Amphiphysin displays domains (SH3, BAR domain) and properties similar to that of endophilin. A specific endophilin isoform, endophilin A1, was described to undergo ubiquitylation by the Nedd4-like protein Itch, probably at endosomes [184].
Agonist-dependent internalization of G protein-coupled receptors via clathrin-coated pits is dependent on the adaptor protein b-arrestin, which interacts with elements of the endocytic machinery such as AP2 and clathrin. For the b2-adrenergic receptor (b2-AR) this requires ubiquitylation of b-arrestin by monomeric RING E3, Mdm2. Although the receptor is ubiquitylated, it is b-arrestin ubiquitylation which is critical for its internalization. Two distinct patterns of b-arrestin trafficking within the cell have been observed for different classes of GPCRs. For class A (Ex : b2AR), b-arrestin interacts transiently with the receptor at the cell surface, and for class B (Ex : vasopressin receptor V2R), b-arrestin displays simultaneous trafficking with the receptors from the cell membrane to endocytic vesicles. This differential behavior was shown to rely on different ubiquitylation/deubiquitylation patterns of b-arrestin during trafficking of these two class of receptors. b2AR stimulation leads to only transient b-arrestin ubiquiitylation, whereas V2R stimulation leads to stable b-arrestin ubiquitylation Expression of arrestin-ubiquitin chimera transforms a class A receptor to class B with respect to intracellular trafficking. One possible interpretation could be that persistently ubiquitylated b-arrestin in complex with internalized receptors somehow leads to their MVB sorting, instead of recycling [185]. Mechanisms underlying regulation of b-arrestin deubiquitylation have still to be defined.
Similar features prevail in the case of EGFR internalization. In the CIN85-endophilin-Cbl complex required for EGFR endocytosis, CIN85 itself is massively monoubiquitylated by Cbl after EGF treatment [186]. Both Cbl and CIN85 are then targeted to MVBs and degraded together with EGFR. Strikingly, Cbl-directed CIN85 monoubiquitylation is not specific of a particular Lys residue. Dominant negative forms of CIN85 which delay EGFR degradation display impaired monoubiquitylation, indicating that this modification plays a critical role in EGFR endocytic pathway, likely for both internalization, and MVB sorting. These data are rather similar to that reported for b2-AR and b-arrestin, since in both case there is a ligand stimulated ubiquitylation simultaneously for the endocytic cargoes, and for a corresponding adaptor. In addition,

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