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Prepublished online as a Blood First Edition Paper on September 19, 2002; DOI 10.1182/blood-2002-05-1593.
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Blood, 1 March 2003, Vol. 101, No. 5, pp. 1810-1817
HEMOSTASIS, THROMBOSIS, AND VASCULAR BIOLOGY
Membrane-type matrix metalloproteinase-mediated angiogenesis
in a fibrin-collagen matrix
Annemie Collen,
Roeland Hanemaaijer,
Florea Lupu,
Paul H. A. Quax,
Natascha van Lent,
Jos Grimbergen,
Erna Peters,
Pieter Koolwijk, and
Victor W. M. van
Hinsbergh
From the Gaubius Laboratory TNO-PG, Leiden, The
Netherlands; Department of Dermatology, Leiden University
Medical Center, Leiden, The Netherlands; Cardiovascular
Biology Research Program, Oklahoma Medical Research Foundation,
Oklahoma City; Department of Physiology, Institute for Cardiovascular
Research, VU University Medical Center, Amsterdam, The
Netherlands.
Adult angiogenesis, associated with pathologic conditions, is often
accompanied by the formation of a fibrinous exudate. This temporary
matrix consists mainly of fibrin but is intermingled with plasma
proteins and collagen fibers. The formation of capillary structures in
a fibrinous matrix in vivo was mimicked by an in vitro model, in which
human microvascular endothelial cells (hMVECs) seeded on top of a
fibrin-10% collagen matrix form capillarylike tubular structures after
stimulation with basic fibroblast growth factor/tumor necrosis factor
 (bFGF/TNF-) or vascular endothelial growth factor
(VEGF)/TNF-. In the fibrin-collagen matrix the metalloproteinase
inhibitor BB94 inhibited tubule formation by 70% to 80%. Simultaneous
inhibition of plasmin and metalloproteinases by aprotinin and BB94
caused a nearly complete inhibition of tubule formation. Adenoviral
transduction of tissue inhibitor of metalloproteinases 1 (TIMP-1) and TIMP-3 into endothelial cells revealed that TIMP-3 markedly inhibited angiogenesis, whereas TIMP-1 had only a minor effect. Immunohistochemical analysis showed the presence of matrix metalloproteinase 1 (MMP-1), MMP-2, and membrane-type 1 (MT1)-MMP, whereas MMP-9 was absent. The endothelial production of
these MMPs was confirmed by antigen assays and real-time polymerase chain reaction (PCR). MT1-MMP mRNA was markedly increased in
endothelial cells under conditions that induced tubular structures. The
presence of MMP-1, MMP-2, and MT1-MMP was also demonstrated in vivo in the newly formed vessels of a recanalized arterial mural thrombus. These data suggest that MMPs, in particular MT-MMPs, play a pivotal role in the formation of capillarylike tubular structures in a collagen-containing fibrin matrix in vitro and may be involved in
angiogenesis in a fibrinous exudate in vivo.
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