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Blood, 1 March 2001, Vol. 97, No. 5, pp. 1321-1329
HEMOSTASIS, THROMBOSIS, AND VASCULAR BIOLOGY
A permissive role for tumor necrosis factor in vascular
endothelial growth factor-induced vascular permeability
Matthias Clauss,
Cord Sunderkötter,
Baldur Sveinbjörnsson,
Stefan Hippenstiel,
Antje Willuweit,
Michael Marino,
Elvira Haas,
Rolf Seljelid,
Peter Scheurich,
Norbert Suttorp,
Matthias Grell, and
Werner Risau
From the Department of Molecular Cell Biology,
Max-Planck-Institute, Bad Nauheim, Germany; Institute of Experimental
Dermatology and Department of Dermatology, Wilhelms-University of
Münster, Münster, Germany; Department of Experimental
Pathology, University of Tromsø, Tromsø, Norway; Department of
Internal Medicine, Charité, Humboldt-University, Berlin, Germany;
Ludwig Institute for Cancer Research, New York, NY; Institute of Cell
Biology and Immunology, University of Stuttgart, Stuttgart, Germany;
and Merck KGaA, Biomed Fo/ONC, Darmstadt, Germany.
Vascular endothelial growth factor (VEGF) induces both
angiogenesis and an increase in vascular permeability, 2 processes that
are considered to be important for both tumor growth and the delivery
of drugs to the site of tumors. This study demonstrates that
transmembrane expression of tumor necrosis factor (tmTNF) is
up-regulated in the endothelium of a murine methylcholanthrene (meth
A)-induced sarcoma in comparison to the adjacent normal dermal
vasculature and is also present on cultivated human endothelial cells.
It is further shown that tmTNF is required for VEGF-mediated endothelial hyperpermeability in vitro and in vivo. This permissive activity of TNF appears to be selective, because anti-TNF antibodies ablated the VEGF-induced permeability but not proliferation of cultivated human endothelial cells. Furthermore, tnf
gene-deficient mice show no obvious defects in vascularization
and develop normally but failed to respond to administration of VEGF
with an increase in vascular permeability. Subsequent studies indicated
that the tmTNF and VEGF signaling pathways converge at the level of a
secondary messenger, the "stress-activated protein kinase-2"
(SAPK-2)/p38: (1) up-regulated endothelial expression of tmTNF resulted
in the continuous activation of SAPK-2/p38 in vitro, and (2) an
inhibitor of SAPK-2/p38 activation abolished the vascular permeability
activity of VEGF in vivo. In conclusion, the study's finding that
continuous autocrine signaling by tmTNF sensitizes endothelial cells to
respond to VEGF by increasing their vascular permeability provides new therapeutic concepts for manipulating vascular hyperpermeability.
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