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Blood, Vol. 93 No. 8 (April 15), 1999:
pp. 2707-2720
A Novel SH2-Containing Phosphatidylinositol 3,4,5-Trisphosphate
5-Phosphatase (SHIP2) Is Constitutively Tyrosine Phosphorylated and
Associated With src Homologous and Collagen Gene (SHC)
in Chronic Myelogenous Leukemia Progenitor Cells
David Wisniewski,
Annabel Strife,
Steve Swendeman,
Hediye Erdjument-Bromage,
Scott Geromanos,
W. Michael Kavanaugh,
Paul Tempst, and
Bayard Clarkson
From the Sloan-Kettering Institute for Cancer Research, Molecular
Pharmacology and Therapeutics Program and Molecular Biology Program,
and Memorial Hospital for Cancer and Allied Diseases, Department of
Medicine, Division of Hematologic Oncology, Leukemia Service, Memorial
Sloan-Kettering Cancer Center (MSKCC), New York, NY; the Chiron Corp,
Emeryville, CA; and Cornell University Medical College, New York,
NY.
Because of the probable causal relationship between constitutive
p210bcr/abl protein tyrosine kinase activity and
manifestations of chronic-phase chronic myelogenous leukemia (CML;
myeloid expansion), a key goal is to identify relevant p210 substrates
in primary chronic-phase CML hematopoietic progenitor cells. We
describe here the purification and mass spectrometric identification of
a 155-kD tyrosine phosphorylated protein associated with src homologous
and collagen gene (SHC) from
p210bcr/abl-expressing hematopoietic cells as
SHIP2, a recently reported, unique SH2-domain-containing protein
closely related to phosphatidylinositol polyphosphate 5-phosphatase
SHIP. In addition to an N-terminal SH2 domain and a central
catalytic region, SHIP2 (like SHIP1) possesses both potential PTB(NPXY)
and SH3 domain (PXXP) binding motifs. Thus, two unique 5-ptases with
striking structural homology are coexpressed in hematopoietic
progenitor cells. Stimulation of human hematopoietic growth factor
responsive cell lines with stem cell factor (SCF), interleukin-3
(IL-3), and granulocyte-macrophage colony-stimulating factor (GM-CSF)
demonstrate the rapid tyrosine phosphorylation of SHIP2 and its
resulting association with SHC. This finding suggests that SHIP2, like
that reported for SHIP1 previously, is linked to downstream signaling
events after activation of hematopoietic growth factor receptors.
However, using antibodies specific to these two proteins, we
demonstrate that, whereas SHIP1 and SHIP2 selectively hydrolyze
PtdIns(3,4,5)P3 in vitro, only SHIP1 hydrolyzes soluble
Ins(1,3,4,5)P4. Such an enzymatic difference raises the
possibility that SHIP1 and SHIP2 may serve different functions.
Preliminary binding studies using lysates from
p210bcr/abl-expressing cells indicate that both
Ptyr SHIP2 and Ptyr SHIP1 bind to the PTB domain of SHC but not to its
SH2 domain. Interestingly, SHIP2 was found to selectively bind to the
SH3 domain of ABL, whereas SHIP1 selectively binds to the SH3 domain of
Src. Furthermore, in contrast to SHIP1, SHIP2 did not bind to
either the N-terminal or C-terminal SH3 domains of GRB2.
These observations suggest (1) that SHIP1 and SHIP2 may have a
different hierarchy of binding SH3 containing proteins and therefore
may modulate different signaling pathways and/or localize to different
cellular compartments and (2) that they may be substrates for tyrosine
phosphorylation by different tyrosine kinases. Because recent evidence
has clearly implicated both PI(3,4,5)P3 and
PI(3,4)P2 in growth factor-mediated signaling, our finding
that both SHIP1 and SHIP2 are constitutively tyrosine phosphorylated in
CML primary hematopoietic progenitor cells may thus have important
implications in p210bcr/abl-mediated myeloid expansion.
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