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Blood, 15 April 2001, Vol. 97, No. 8, pp. 2323-2332
HEMOSTASIS, THROMBOSIS, AND VASCULAR BIOLOGY
Growth factor-induced angiogenesis in vivo requires specific
cleavage of fibrillar type I collagen
Marco Seandel,
Katharina Noack-Kunnmann,
Dan Zhu,
Ronald T. Aimes, and
James P. Quigley
From the Department of Pathology, State University of
New York at Stony Brook, Stony Brook, NY, and the Department of
Vascular Biology, The Scripps Research Institute, La Jolla, CA.
The contribution of specific type I collagen remodeling in
angiogenesis was studied in vivo using a quantitative chick embryo assay that measures new blood vessel growth into well-defined fibrillar
collagen implants. In response to a combination of basic fibroblast
growth factor (bFGF) and vascular endothelial growth factor (VEGF), a
strong angiogenic response was observed, coincident with invasion into
the collagen implants of activated fibroblasts, monocytes, heterophils,
and endothelial cells. The angiogenic effect was highly dependent on
matrix metalloproteinase (MMP) activity, because new vessel
growth was inhibited by both a synthetic MMP inhibitor, BB3103, and a
natural MMP inhibitor, TIMP-1. Multiple MMPs were detected in the
angiogenic tissue including MMP-2, MMP-13, MMP-16, and a recently
cloned MMP-9-like gelatinase. Using this assay system, wild-type
collagen was compared to a unique collagenase-resistant collagen (r/r),
with regard to the ability of the respective collagen implants to
support cell invasion and angiogenesis. It was found that
collagenase-resistant collagen constitutes a defective substratum for
angiogenesis. In implants made with r/r collagen there was a
substantial reduction in the number of endothelial cells and newly
formed vessels. The presence of the r/r collagen, however, did not
reduce the entry into the implants of other cell types, that is,
activated fibroblasts and leukocytes. These results indicate that
fibrillar collagen cleavage at collagenase-specific sites is a
rate-limiting event in growth factor-stimulated angiogenesis in vivo.
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