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Molecular and Cellular Biology, April 1999, p. 3205-3215, Vol. 19, No. 4
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Regulation of Early Events in Integrin Signaling by Protein Tyrosine Phosphatase SHP-2

Eok-Soo Oh,1 Haihua Gu,1 Tracy M. Saxton,2 John F. Timms,1 Sharon Hausdorff,1,dagger Ernst U. Frevert,3 Barbara B. Kahn,3 Tony Pawson,2 Benjamin G. Neel,1,* and Sheila M. Thomas1,*

Cancer Biology Program, Division of Hematology-Oncology,1 and Diabetes Unit,3 Department of Medicine, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts 02215, and Samuel Lunenfeld Research Institute, Mt. Sinai Hospital, Toronto, Ontario M5G 1X5, Canada2

Received 29 May 1998/Returned for modification 16 July 1998/Accepted 14 January 1999

The nontransmembrane protein tyrosine phosphatase SHP-2 plays a critical role in growth factor and cytokine signaling pathways. Previous studies revealed that a fraction of SHP-2 moves to focal contacts upon integrin engagement and that SHP-2 binds to SHP substrate 1 (SHPS-1)/SIRP-1alpha , a transmembrane glycoprotein with adhesion molecule characteristics (Y. Fujioka et al., Mol. Cell. Biol. 16:6887-6899, 1996; M. Tsuda et al., J. Biol. Chem. 273:13223-13229). Therefore, we asked whether SHP2-SHPS-1 complexes participate in integrin signaling. SHPS-1 tyrosyl phosphorylation increased upon plating of murine fibroblasts onto specific extracellular matrices. Both in vitro and in vivo studies indicate that SHPS-1 tyrosyl phosphorylation is catalyzed by Src family protein tyrosine kinases (PTKs). Overexpression of SHPS-1 in 293 cells potentiated integrin-induced mitogen-activated protein kinase (MAPK) activation, and potentiation required functional SHP-2. To further explore the role of SHP-2 in integrin signaling, we analyzed the responses of SHP-2 exon 3-/- and wild-type cell lines to being plated on fibronectin. Integrin-induced activation of Src family PTKs, tyrosyl phosphorylation of several focal adhesion proteins, MAPK activation, and the ability to spread on fibronectin were defective in SHP-2 mutant fibroblasts but were restored upon SHP-2 expression. Our data suggest a positive-feedback model in which, upon integrin engagement, basal levels of c-Src activity catalyze the tyrosyl phosphorylation of SHPS-1, thereby recruiting SHP-2 to the plasma membrane, where, perhaps by further activating Src PTKs, SHP-2 transduces positive signals for downstream events such as MAPK activation and cell shape changes.

* Corresponding author. Mailing address: Cancer Biology Program, Division of Hematology-Oncology, Beth Israel Deaconess Hospital and Harvard Medical School, Boston, MA 02215. Phone: (617) 667-4174. Fax: (617) 667-0610. E-mail for B.G.N.: bneel{at}bidmc.harvard.edu. E-mail for S.M.T.: sthomas{at}bidmc.harvard.edu.

dagger Present address: Ariad Pharmaceuticals, Cambridge, MA 02139.

Molecular and Cellular Biology, April 1999, p. 3205-3215, Vol. 19, No. 4
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


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