A novel, quantitative model for study of endothelial cell migration and sprout formation within three-dimensional collagen matrices
Abstract
Interactions between migratory endothelial cells (ECs) and surrounding extracellular matrix (ECM) are of central importance to vascular growth. Here, we present a new model of EC migration and morphogenesis within three-dimensional ECM termed "radial invasion of matrix by aggregated cells" (RIMAC). In the RIMAC model, single aggregates of defined numbers of bovine aortic ECs were embedded within small, lenticular gels of type I collagen supported by annuli of nylon mesh. Culture of the gels in nutrient media resulted in quantifiable, reproducible, radial migration of ECs into the collagen. The angiogenic proteins basic fibroblast growth factor (bFGF) and vascular endothelial growth factor (VEGF) each stimulated migration of ECs in a concentration-dependent manner. In combination, bFGF and VEGF stimulated migration synergistically. In contrast, transforming growth factor-beta1 inhibited migration of ECs. Low concentrations (0.1-0.5 ng/ml) of VEGF induced ECs to form multicellular sprouts, some of which possessed lumen-like spaces. Mitomycin C, an inhibitor of cell proliferation, did not affect the migration of ECs into collagen induced by 0.5 ng/ml VEGF but moderately inhibited migration induced by 5 ng/ml VEGF. Increasing the density (concentration) of the collagen gel inhibited the migration of single ECs and increased the branching and anastomosis of multicellular sprouts. We conclude that the RIMAC model is a highly efficacious assay for the screening of potentially angiogenic and angiostatic compounds and, moreover, is advantageous for mechanistic studies of vascular morphogenesis.
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The grid method has been used in a previous study to quantify migration of sprouts in a 3D matrix.
“This grid has been used in a previous study to quantify the migration of sprouts in a 3D matrix [29].”
From Macrophage functional polarization (M1/M2) in response to varying fiber and pore dimensions of electrospun scaffolds (2013) · cites this paper as [29]
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- Authors
- Vernon, R. B., & Sage, E. H.
- Affiliations
- University of Washington (US)
- Venue
- Microvascular Research
- Publisher
- Elsevier BV
- Published
- 1999-03
- Volume
- 57
- Issue
- 2
- Pages
- 118-133
- ISSN
- 0026-2862 (ISSN-L)
- OpenAlex
- W1984914037
- Cited by
- 185
- References
- 50
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 3 · 2021: 6 · 2020: 3 · 2019: 6 · 2018: 3 · 2017: 3 · 2016: 6 · 2015: 5 · 2014: 11 · 2013: 6 · 2012: 5
- FWCI
- 3.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Microvascular Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL-18645, P01HL018645)
- National Institute of General Medical Sciences (GM40711, R01GM040711)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
- Keywords
- endothelial cell migration, angiogenesis, sprout formation, 3D collagen matrix, type I collagen gel, basic fibroblast growth factor, vascular endothelial growth factor, TGF-β1, lumen formation, vascular morphogenesis, cell aggregates
- MeSH terms
- Animals, Cattle, Cell Movement, Clone Cells, Collagen, Endothelium, Vascular, Extracellular Matrix, Gels, Lymphokines, Models, Cardiovascular, Fibroblast Growth Factor 2, Endothelial Growth Factors, Mitomycin, Neovascularization, Physiologic, Vascular Endothelial Growth Factors, Vascular Endothelial Growth Factor A
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