generation of novel cytoplasmic forms of protein tyrosine phosphatase epsilon by proteolytic...

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Generation of novel cytoplasmic forms of protein tyrosine phosphatase epsilon by proteolytic processing and translational control Hava Gil-Henn 1 , Gloria Volohonsky 1 , Hila Toledano-Katchalski 1 , Shilpa Gandre 1 and Ari Elson* ,1 1 Department of Molecular Genetics, The Weizmann Institute of Science, Rehovot 76100, Israel Two protein forms of tyrosine phosphatase epsilon (PTPe) are known ± receptor-like (tm-PTPe) and non receptor-like (cyt-PTPe), with each form possessing unique tissue-speci®c expression patterns, subcellular localization, and physiological functions. We describe two additional forms of PTPe protein ± p67 and p65. p67 is produced by initiation of translation at an internal initiation codon of PTPe mRNA molecules, while p65 is produced by speci®c proteolytic cleavage of larger PTPe proteins. Cleavage is inhibited by MG132, but is proteasome-independent. In contrast with full-length tm-PTPe and cyt-PTPe, p67 and p65 are exclusively cytoplasmic, are not phosphorylated by Neu, and do not associate with Grb2 in unstimulated cells. p67 and p65 are catalytically active and can reduce Src-mediated phosphorylation of the Kv2.1 voltage-gated potassium channel, albeit with reduced eciency which most likely results from their cytoplasmic localization. We also show that full-length cyt-PTPe protein can be found at the cell membrane and in the nucleus and that it is the ®rst 27 residues of cyt-PTPe which determine this localization. p67 and p65 provide mechanisms for removing PTPe activity from the cell membrane, possibly serving to down-regulate PTPe activity there. PTPe emerges as a family of four related proteins whose expression, subcellular localization and most likely physiological roles are subject to complex regulation at the transcrip- tional, translational and post-translational levels. Onco- gene (2000) 19, 4375 ± 4384. Keywords: phosphatase; tyrosine; proteolysis; MG132; translational regulation; cleavage Introduction Accurate phosphorylation of tyrosine residues in proteins is vital for the well-being of cells and organisms, and is a process closely regulated by opposing activities of protein tyrosine kinases and tyrosine phosphatases (Hunter, 1995). Because they are genetically, structurally, and functionally distinct from tyrosine kinases, tyrosine phosphatases (PTPases) oer a unique vantage point from which to study regulation of biological processes by tyrosine phosphorylation. In recent years it has become evident that subcellular localization of non-membranal PTPases is an impor- tant factor in determining their physiological roles (reviewed in Mauro and Dixon, 1994; Fischer, 1999). Along these lines, SHP1 and SHP2 can be recruited, via their SH2 domains, to activated growth factor receptors (Stein-Gerlach et al., 1998), while several other non-membranal PTPases possess protein motifs which allow them to associate with cytoskeletal or membranal proteins. Several cytoplasmic phosphatases, such as PTP1B, PTP-PEST, and STEP, can undergo proteolytic cleavage, which alters their subcellular localization and can result in their activation (Frangio- ni et al., 1993; Gu and Majerus, 1996; Gurd et al., 1999; Nguyen et al., 1999). In general, subcellular localization of a PTPase can in¯uence its physiological function by determining the repertoire of potential substrates and interactors available to the enzyme. PTPe, which is at the focus of this study, was originally cloned as a transmembranal, receptor-type PTPase (tm-PTPe; Krueger et al., 1990). A second form of PTPe, one which is not an integral membrane protein, was subsequently identi®ed (cyt-PTPe; Elson and Leder, 1995a; Nakamura et al., 1996). cyt-PTPe and tm-PTPe are identical throughout most of their sequence, including their two catalytic domains; their N-termini are, however, entirely distinct from one another, a fact which determines their unique sub- cellular localizations. tm-PTPe and cyt-PTPe are products of distinct mRNA species transcribed from the single PTPe gene by use of alternative promoters; the two proteins have virtually non-overlapping expression patterns in cells and among tissues, suggesting that they play distinct physiological roles (Elson and Leder, 1995a; Elson et al., 1996; Tanuma et al., 1999). As the catalytic domains of tm-PTPe and cyt-PTPe are identical, their distinct roles are believed to result from their dierent expression patterns. Along these lines, we have shown that tm-PTPe, but not cyt-PTPe, is expressed in mouse mammary tumors initiated speci®cally by ras or neu, but not by myc, int- 2, TGF-a, or heregulin (Elson and Leder, 1995b). This ®nding suggests that tm-PTPe may participate in molecular processes by which ras or neu speci®cally transform mammary epithelium. In agreement with this interpretation, overexpression of tm-PTPe in mouse mammary epithelium promotes mammary hyperplasia and associated neoplasia (Elson, 1999). tm-PTPe can down-regulate insulin receptor signaling in certain types of cultured cells (Moller et al., 1995), a function which is not shared with cyt-PTPe due to the predominantly non-membrane localization of the latter (JN Andersen, A Elson, R Lammers, J Romer, JT Clausen, KB Moller and NPH Moller, manuscript submitted for publication). We have recently shown that cyt-PTPe is a regulator of myelination of Oncogene (2000) 19, 4375 ± 4384 ã 2000 Macmillan Publishers Ltd All rights reserved 0950 ± 9232/00 $15.00 www.nature.com/onc *Correspondence: A Elson Received 27 March 2000; revised 29 June 2000; accepted 7 July 2000

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