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Blood, Vol. 95 No. 11 (June 1), 2000:
pp. 3403-3411
Endostatin-induced tyrosine kinase signaling through the Shb
adaptor protein regulates endothelial cell apoptosis
Johan Dixelius,
Helena Larsson,
Takako Sasaki,
Kristina Holmqvist,
Lingge Lu,
Åke Engström,
Rupert Timpl,
Michael Welsh, and
Lena Claesson-Welsh
From the Department of Genetics and Pathology, Rudbeck Laboratory,
Uppsala, Sweden; Max-Planck-Institut für Biochemie, Martinsried,
Germany; and Department of Medical Cell Biology and Department of
Medical Biochemistry and Microbiology, Biomedical Center, Uppsala,
Sweden.
Endostatin, which corresponds to the C-terminal fragment of collagen
XVIII, is a potent inhibitor of angiogenesis. Fibroblast growth
factor-2 (FGF-2)-induced angiogenesis in the chicken chorioallantoic membrane was inhibited by endostatin, but not by an endostatin mutant
R158/270A, lacking heparin-binding ability. Endostatin was internalized
by endothelial cells, but not by mouse fibroblasts. Treatment of murine
brain endothelial (IBE) cells with endostatin reduced the proportion of
cells in S phase, whereas growth-arrested IBE cells in collagen gels
treated with endostatin displayed enhanced tubular morphogenesis. IBE
cells overexpressing Shb, an adaptor protein implicated in
angiostatin-induced apoptosis, displayed elevated apoptosis and
decreased tubular morphogenesis in collagen gels in response to
endostatin when added together with FGF-2. Induction of apoptosis was
dependent on the heparin-binding ability of endostatin and the
expression of Shb with a functional Src homology 2 (SH2)-domain.
Endostatin treatment for 10 minutes or 24 hours induced tyrosine
phosphorylation of Shb and formation of multiprotein complexes. An Shb
SH2 domain fusion protein precipitated a 125-kd phosphotyrosyl protein
in endostatin-treated cells. The 125-kd component either contained
intrinsic tyrosine kinase activity or occurred in complex with a
tyrosine kinase. In conclusion, our data show that endostatin induces
tyrosine kinase activity and enhanced apoptosis in FGF-treated
endothelial cells.
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