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Mol Cell Biol, July 1998, p. 3838-3850, Vol. 18, No. 7
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Identification of Major Binding Proteins and
Substrates for the SH2-Containing Protein Tyrosine Phosphatase SHP-1
in Macrophages
John F.
Timms,1 *
Kristen
Carlberg,2
Haihua
Gu,1
Haiyan
Chen,1
Shubhangi
Kamatkar,1
Monica J. S.
Nadler,1
Larry R.
Rohrschneider,2 and
Benjamin G.
Neel1
Cancer Biology Program, Division of
Hematology-Oncology, Department of Medicine, Beth Israel Deaconess
Medical Center and Harvard Medical School, Boston, Massachusetts
02215,1 and
Division of Basic
Sciences, Fred Hutchinson Cancer Research Center, Seattle,
Washington 981092
Received 20 January 1998/Returned for modification 2 March
1998/Accepted 9 April 1998
The protein tyrosine phosphatase SHP-1 is a critical regulator of
macrophage biology, but its detailed mechanism of action remains
largely undefined. SHP-1 associates with a 130-kDa
tyrosyl-phosphorylated species (P130) in macrophages, suggesting that
P130 might be an SHP-1 regulator and/or substrate. Here we show that
P130 consists of two transmembrane glycoproteins, which we identify as
PIR-B/p91A and the signal-regulatory protein (SIRP) family member BIT.
These proteins also form separate complexes with SHP-2. BIT, but not PIR-B, is in a complex with the colony-stimulating factor 1 receptor (CSF-1R), suggesting that BIT may direct SHP-1 to the CSF-1R. BIT and
PIR-B bind preferentially to substrate-trapping mutants of SHP-1 and
are hyperphosphorylated in macrophages from motheaten viable mice, which express catalytically impaired forms of SHP-1, indicating that these proteins are SHP-1 substrates. However, BIT and
PIR-B are hypophosphorylated in motheaten macrophages, which completely lack SHP-1 expression. These data suggest a model in
which SHP-1 dephosphorylates specific sites on BIT and PIR-B while
protecting other sites from dephosphorylation via its SH2 domains.
Finally, BIT and PIR-B associate with two tyrosyl phosphoproteins and a
tyrosine kinase activity. Tyrosyl phosphorylation of these proteins and
the level of the associated kinase activity are increased in the
absence of SHP-1. Our data suggest that BIT and PIR-B recruit multiple
signaling molecules to receptor complexes, where they are regulated by
SHP-1 and/or SHP-2.
*
Corresponding author. Mailing address: HIM 1043, Beth
Israel Deaconess Medical Center, 330 Brookline Ave., Boston, MA 02215. Phone: (617) 667-2901. Fax: (617) 667-0610. E-mail:
jtimms{at}bidmc.harvard.edu.
Mol Cell Biol, July 1998, p. 3838-3850, Vol. 18, No. 7
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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