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Prepublished online as a Blood First Edition Paper on September 19, 2002; DOI 10.1182/blood-2002-05-1593.
Submitted June 7, 2002
Accepted September 12, 2002
Membrane-type matrix metalloproteinase mediated angiogenesis in a fibrin-collagen matrix
Annemie Collen, Roeland Hanemaaijer, Florea Lupu, Paul H Quax, Natascha van Lent, Jos Grimbergen, Erna Peters, Pieter Koolwijk, and Victor W van Hinsbergh*
Gaubius Laboratory, TNO-PG, Leiden, The Netherlands; Department of Dermatology, Leiden University Medical Center, Leiden, The Netherlands
Department of Dermatology, Leiden University Medical Center, Leiden, The Netherlands
Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, USA
Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands
Gaubius Laboratory, TNO-PG, Leiden, The Netherlands
Gaubius Laboratory, TNO-PG, Leiden, The Netherlands; Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands
* Corresponding author; email: vwm.vanhinsbergh{at}pg.tno.nl.
Adult angiogenesis, associated with pathological 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 (hMVEC) seeded on top of a fibrin-10% collagen matrix form capillary-like tubular structures after stimulation with bFGF/TNF or VEGF/TNF. In the fibrin-collagen matrix the metalloproteinase inhibitor BB94 inhibited tubule formation by 70-80%. Simultaneous inhibition of plasmin and metalloproteinases by aprotinin and BB94 caused a nearly complete inhibition of tubule formation. Adenoviral transduction of TIMP-1 and TIMP-3 into endothelial cells revealed that TIMP-3 markedly inhibited angiogenesis, while TIMP-1 had only a minor effect. Immunohistochemical analysis showed the presence of MMP-1, MMP-2 and MT1-MMP, while MMP-9 was absent. The endothelial production of these MMPs was confirmed by antigen assays and real-time 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 capillary-like 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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