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Background  The physiological function of the ubiquitous cellular prion protein, PrP c , is still under debate. It was essentially studied in nervous system, but poorly investigated in epithelial cells. We previously reported that PrP c  is targeted to cell–cell junctions of polarized epithelial cells, where it interacts with c-Src.    Methodology/Findings  We show here that, in cultured human enterocytes and in intestine  in vivo , the mature PrP c  is differentially targeted either to the nucleus in dividing cells or to cell–cell contacts in polarized/differentiated cells. By proteomic analysis, we demonstrate that the junctional PrP c  interacts with cytoskeleton-associated proteins, such as gamma- and beta-actin, alpha-spectrin, annexin A2, and with the desmosome-associated proteins desmoglein, plakoglobin and desmoplakin. In addition, co-immunoprecipitation experiments revealed complexes associating PrP c , desmoglein and c-Src in raft domains. Through siRNA strategy, we show that PrP c  is necessary to complete the process of epithelial cell proliferation and for the sub-cellular distribution of proteins involved in cell architecture and junctions. Moreover, analysis of the architecture of the intestinal epithelium of PrP c  knock-out mice revealed a net decrease in the size of desmosomal junctions and, without change in the amount of BrdU incorporation, a shortening of the length of intestinal villi.    Conclusions/Significance  From these results, PrP c  could be considered as a new partner involved in the balance between proliferation and polarization/differentiation in epithelial cells.

The Cellular Prion Protein PrPc Is Involved in the Proliferation of Epithelial Cells and in the Distribution of Junction-Associated Proteins