Topography of Extracellular Matrix Mediates Vascular Morphogenesis and Migration Speeds in Angiogenesis

Bauer, Amy L.; Jackson, Trachette L.; Jiang, Yi

doi:10.1371/journal.pcbi.1000445

Title: Topography of Extracellular Matrix Mediates Vascular Morphogenesis and Migration Speeds in Angiogenesis

Journal Article · 23 July 2009 · PLoS Computational Biology (Online)

DOI: https://doi.org/10.1371/journal.pcbi.1000445 · OSTI ID:1627193

Bauer, Amy L. ^[1]; Jackson, Trachette L. ^[2]; Jiang, Yi ^[3]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Division; DOE/OSTI
Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Mathematics
Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Division

The extracellular matrix plays a critical role in orchestrating the events necessary for wound healing, muscle repair, morphogenesis, new blood vessel growth, and cancer invasion. In this study, we investigate the influence of extracellular matrix topography on the coordination of multi-cellular interactions in the context of angiogenesis. To do this, we validate our spatio-temporal mathematical model of angiogenesis against empirical data, and within this framework, we vary the density of the matrix fibers to simulate different tissue environments and to explore the possibility of manipulating the extracellular matrix to achieve pro- and anti-angiogenic effects. The model predicts specific ranges of matrix fiber densities that maximize sprout extension speed, induce branching, or interrupt normal angiogenesis, which are independently confirmed by experiment. We then explore matrix fiber alignment as a key factor contributing to peak sprout velocities and in mediating cell shape and orientation. We also quantify the effects of proteolytic matrix degradation by the tip cell on sprout velocity and demonstrate that degradation promotes sprout growth at high matrix densities, but has an inhibitory effect at lower densities. Our results are discussed in the context of ECM targeted pro- and anti-angiogenic therapies that can be tested empirically.

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Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1627193

Journal Information:: PLoS Computational Biology (Online), Journal Name: PLoS Computational Biology (Online) Journal Issue: 7 Vol. 5; ISSN 1553-7358

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Rheology and Confocal Reflectance Microscopy as Probes of Mechanical Properties and Structure during Collagen and Collagen/Hyaluronan Self-Assembly Yang, Ya-li; Kaufman, Laura J. Biophysical Journal, Vol. 96, Issue 4 https://doi.org/10.1016/j.bpj.2008.10.063	journal	February 2009
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Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis Zaman, M. H.; Trapani, L. M.; Sieminski, A. L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 29 https://doi.org/10.1073/pnas.0604460103	journal	July 2006
Cadherin interaction probed by atomic force microscopy Baumgartner, W.; Hinterdorfer, P.; Ness, W. Proceedings of the National Academy of Sciences, Vol. 97, Issue 8 https://doi.org/10.1073/pnas.070052697	journal	April 2000
Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo Lobov, I. B.; Brooks, P. C.; Lang, R. A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 17 https://doi.org/10.1073/pnas.172161899	journal	August 2002
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Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. Ingber, D. E.; Folkman, J. Journal of Cell Biology, Vol. 109, Issue 1 https://doi.org/10.1083/jcb.109.1.317	journal	July 1989
VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia Gerhardt, Holger; Golding, Matthew; Fruttiger, Marcus The Journal of Cell Biology, Vol. 161, Issue 6 https://doi.org/10.1083/jcb.200302047	journal	June 2003
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