Recent evidences suggest that SUMOylation, a post-translational modification able to modulate the stability and subcellular localization of target proteins, critically modifies members of the TGF signaling pathway. TGF treatment. These data indicate that SUMOylation is a novel regulatory mechanism that modulates p27Kip1 function in response to TGF stimulation. Given the involvement of TGF signaling in cancer cell proliferation and invasion, our data may shed light on an important aspect of this pathway during tumor progression. and models (Belletti et al., 2005). TGF A-395 induces cell cycle arrest by both increasing p27 protein levels and favoring its nuclear accumulation (Lecanda et al., 2007, 2009). Despite extensive evidences supporting that p27 is a key downstream molecule determining the fate of TGF-responsive cells, the precise molecular mechanisms whereby TGF regulates both p27 stability and nuclear accumulation are only poorly understood. It has been described that TGF blocks p27 ubiquitin-dependent nuclear degradation through the Smad2/3-mediated downregulation of two key members of the SCFSkp2 E3 ligase complex, Csk1 and Skp2. However, this mechanism seems to be necessary for the maintenance rather than the induction of p27 nuclear accumulation since the decrease of Csk1 and Skp2 follows, rather than precedes, p27 accumulation (Lecanda et al., 2009). It is clear that p27 is differently localized and phosphorylated in TGF-resistant compared with TGF-sensitive breast epithelial cells, and these modifications are associated with the failure of TGF to induce the inhibition of CDKs and the cell cycle arrest (Ciarallo et al., 2002), but it is much less clear whether and how TGF directly modifies p27 phosphorylation and/or localization. Recent evidences suggest A-395 that SUMOylation regulates the TGF signaling pathway. SUMO modification significantly impacts on TGF type I receptor (Kang et al., 2008), and Smad proteins function (Imoto et al., 2003; Lee et al., 2003; Lin et al., 2003; Liang et al., 2004). Moreover, TGF directly impinge on Smad4 SUMOylation, through the stabilization of its E3 SUMO-ligase PIASx (Ohshima and Shimotohno, 2003). SUMOylation is a reversible post-translational modification that consists in the covalent attachment of a SUMO molecule to one or more lysines of A-395 the target substrate. Four small ubiquitin-like modifier (SUMO) proteins are known in vertebrates. SUMOylation occurs in a stepwise manner and involves a cascade of SUMO-specific enzymes. These include an E1-activating enzyme (the Aos1/Uba2 heterodimer), the unique E2-conjugating enzyme Ubc9, and several E3 ligases, which contribute to substrate selectivity and increase the SUMOylation efficiency (Kerscher et al., 2006; Geiss-Friedlander and Melchior, 2007). The functional consequences of SUMOylation may vary and include modulation of function, subcellular localization, complex formation, and/or stability of the target proteins RNU2AF1 (Wilkinson and Henley, 2010). Here, we test the hypothesis that SUMOylation could be involved in the regulation of p27 by TGF and demonstrate that TGF induces p27 SUMOylation on lysine 134, eventually increasing p27 stability and contributing to its nuclear accumulation and cell cycle exit. Results p27 is SUMOylated in vitro and in vivo and lysine 134 is the modified residue To evaluate whether p27 could be targeted by SUMOylation, we first performed analyses using SUMOplot? (Abgent) and SUMOsp (Ren et al., 2009) prediction analysis programs (Supplementary Figure S1). These analyses revealed that several lysines (K) present in p27 protein, although non-consensus, are potential sites for SUMO attachment, and indicated K134 as the residue predicted to be SUMOylated with the highest score (Supplementary Figure S1B and C). We also observed that p27 co-immunoprecipitated with Ubc9, the sole E2 SUMO-conjugating enzyme and thus essential for SUMOylation (Supplementary Figure S1D and E), A-395 supporting the possibility that p27 was SUMOylated SUMOylation assay, using the recombinant histidine (His)-tagged p27WT as substrate, confirmed the appearance of higher molecular-weight.
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