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

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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^, 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 focalcontacts upon integrin engagement and that SHP-2 binds to SHPsubstrate 1 (SHPS-1)/SIRP-1 $alpha$ , a transmembrane glycoprotein withadhesion 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 participatein integrin signaling. SHPS-1 tyrosyl phosphorylation increasedupon plating of murine fibroblasts onto specific extracellularmatrices. Both in vitro and in vivo studies indicate that SHPS-1tyrosyl phosphorylation is catalyzed by Src family protein tyrosinekinases (PTKs). Overexpression of SHPS-1 in 293 cells potentiatedintegrin-induced mitogen-activated protein kinase (MAPK) activation,and potentiation required functional SHP-2. To further explorethe role of SHP-2 in integrin signaling, we analyzed the responsesof SHP-2 exon 3^/ and wild-type cell lines to being plated on fibronectin. Integrin-inducedactivation of Src family PTKs, tyrosyl phosphorylation of severalfocal adhesion proteins, MAPK activation, and the ability to spreadon fibronectin were defective in SHP-2 mutant fibroblasts butwere restored upon SHP-2 expression. Our data suggest a positive-feedbackmodel in which, upon integrin engagement, basal levels of c-Srcactivity catalyze the tyrosyl phosphorylation of SHPS-1, therebyrecruiting SHP-2 to the plasma membrane, where, perhaps by furtheractivating Src PTKs, SHP-2 transduces positive signals for downstreamevents such as MAPK activation and cell shapechanges.

^* Corresponding author. Mailing address: Cancer Biology Program, Division of Hematology-Oncology, Beth Israel Deaconess Hospitaland 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.

Present address: Ariad Pharmaceuticals, Cambridge, MA02139.

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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