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Am J Physiol Cell Physiol (October 27, 2004). doi:10.1152/ajpcell.00211.2004
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Submitted on April 28, 2004
Accepted on October 26, 2004

Mitogen-activated protein kinase signaling regulates endothelial cell assembly into networks and the expression of MT1-MMP and MMP-2

Pamela J Boyd1, Jennifer Doyle1, Eric Gee1, Shelley Pallan1, and Tara L Haas1*

1 Kinesiology and Health Sciences, York University, Toronto, ON, Canada

* To whom correspondence should be addressed. E-mail: thaas{at}yorku.ca.

Microvascular endothelial cells embedded within three-dimensional (3D) type I collagen matrices assemble into cellular networks, a process that requires the upregulation of membrane-type-1 (MT1) matrix-metalloproteinase (MMP) and MMP-2. The purpose of this study was to identify the signaling pathways responsible for the transcriptional activation of MT1-MMP and MMP-2 in endothelial cells in 3D collagen lattices. We hypothesized that the 3D type I collagen induction of MT1-MMP and MMP-2 is mediated by the mitogen-activated protein kinase family of enzymes. Here, we show that 3D type I collagen elicits a persistent increase in ERK1/2 and JNK activation and a decrease in p38 activation. Inhibition of ERK1/2 or JNK disrupted endothelial network formation in 3D type I collagen lattices, whereas inhibition of p38 promoted network formation. mRNA levels of both MT1-MMP and MMP-2 were attenuated by ERK1/2 inhibition, but unaffected by either JNK or p38 inhibition. By contrast, expression of constitutively active MEK was sufficient to stimulate MMP-2 and MT1-MMP production in a monolayer of endothelial cells cultured on type I collagen. These results provide evidence that signaling through both ERK1/2 and JNK regulate endothelial assembly into cellular networks, but that the ERK1/2 signaling cascade specifically regulates network formation and the production of both MT1-MMP and MMP-2 genes in response to 3D type I collagen.




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