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2 Chain, Matrix Metalloproteinase-2, and Membrane Type-1-Matrix/Metalloproteinase Are Required for Mimicry of Embryonic Vasculogenesis by Aggressive Melanoma1
Department of Anatomy and Cell Biology [R. E. B. S., E. A. S., L. M. G. G., M. J. C. H.] and The Holden Comprehensive Cancer Center [R. E. B. S., E. A. S., M. J. C. H.] at The University of Iowa, Iowa City, Iowa 52242; Department of Cell Biology, The Scripps Research Institute, La Jolla, California 92037 [N. K., M. B., V. Q.]; Cancer Genetics Branch, National Human Genome Research Institute [P. S. M.] and Extracellular Matrix Pathology, Laboratory Pathology [W. G. S-S.], National Cancer Institute, NIH, Bethesda, Maryland 20892
Vasculogenic mimicry describes a process where aggressive tumor cells in
three-dimensionalmatrices mimic embryonic vasculogenesis by forming extracellular matrix
(ECM)-rich, patterned tubular networks. Microarray gene chip analyses
revealed significant increases in the expression of laminin 5 (Ln-5,
2 chain) and matrix metalloproteinases (MMP)-1, -2, -9, and MT1-MMP
(MMP-14) in aggressive compared with poorly aggressive melanoma cells.
These components colocalized with developing patterned networks and
antisense oligonucleotides to the Ln-5 2 chain (but not sense
oligonucleotides), and antibodies to MMP-2 or MT1-MMP (but not MMP-9)
inhibited the formation of these networks. Cultures which did not
receive antibodies to either MMPs-2 or -14 contained the Ln-5 2
chain promigratory cleavage fragments. Poorly aggressive melanoma cells
seeded on collagen I matrices preconditioned by the aggressive cells
formed tubular networks along the Ln-5 2 chain-enriched tracks
deposited by the aggressive cells. These results suggest that increased
expression of MMP-2 and MT1-MMP, along with matrix deposition of the
Ln-5 2 chain and/or its cleavage fragments, are required for
vasculogenic mimicry by aggressive melanoma cells. Furthermore, the
apparent recapitulation of laminin-rich, patterned networks observed in
aggressive melanoma patients’ tissue sections by aggressive melanoma
tumor cells in three-dimensional culture may also serve as a model to
help identify specific molecular targets which could function as
templates for the coordinated migration of aggressive tumor cells and
their proteolytic remodeling of the ECM and may have profound
implications for the development of novel therapies directed at the ECM
to alter tumor progression.
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