Endothelial-Cell-Mediated Displacement of Extracellular Matrix during Angiogenesis
Mechanical interaction between endothelial cells (ECs) and the extracellular matrix (or collagen gel) is known to influence the sprouting response of endothelial cells during angiogenesis. This influence is believed to impact on the capability of endothelial cells to sense soluble chemical cues. Quantitative analysis of endothelial-cell-mediated displacement of the collagen gel provides a means to explore this mechanical interaction. Existing analysis in this context is generally limited to 2D settings. In this paper, we investigate the mechanical interaction between endothelial cells and the extracellular matrix in terms of the endothelial-cellmediated displacement of the collagen gel in both 2D and 3D. Digital image correlation and Digital volume correlation are applied on confocal reflectance image stacks to analyze cell-mediated displacement of the gel. The skeleton of the sprout is extracted from phase contrast images and superimposed on the displacement field to further investigate the link between the development of the sprout and the displacement of the gel.
[1] P. Carmeliet, "Angiogenesis in health and disease," Nat. Med., vol. 9,
No. 6, pp.653-660, Jun 2003.
[2] D. E. Ingber, "Can cancer be reversed by engineering the tumor
microenvironment?" Semin. Cancer Biol., vol. 18, pp. 356-364, Apr
2008.
[3] N. C. Rivron, E. J. Vrij, J. Rouwkema, G. S. Le, van den Berg A, R. K.
Truckenm├╝ller and C. A. van Blitterswijk, "Tissue deformation spatially
modulates VEGF signaling and angiogenesis," Proc. Natl. Acad. Sci. U
S A, vol. 109, no. 18, pp. 6886-6891, May 2012.
[4] A. Shay-salit, M. Shushy, E. Wolfovitz, H. Yahav, F. Breviario, E.
Dejana and N. Resnick, "VEGF receptor 2 and the adherens junction as
a mechanical transducer in vascular endothelial cells," Proc. Natl. Acad.
Sci. U S A, vol. 99, pp. 9462-9467, Jul. 2002.
[5] D. L. Christiansen, E. K. Huang and F. H. Silver, "Assembly of type I
collagen: fusion of fibril subunits and the influence of fibril diameter on
mechanical properties," Matrix Biol., vol. 19, pp. 409-420, Sep. 2000.
[6] S. Kanzawa, H. Endo and N. Shioya, "Improved in vitro angiogenesis
model by collagen density reduction and the use of type III collagen,"
Ann. Plast. Surg., vol. 30, no. 3, pp. 244-251, Mar. 1993.
[7] A. L. Sieminski, R. P. Hebbel and K. J. Gooch, "The relative magnitude
of endothelial force generation and matrix stiffness modulate capillary
morphogenesis," Exp. Cell Res., vol. 297, no. 2, pp. 574-584, Jul 2004.
[8] A. Stéphanou, G. Meskaoui, B. Vailhé and P. Tracqui, "The rigidity in
fibrin gels as a contributing factor to the dynamics of in vitro vascular
cord formation," Microvasc. Res.,vol. 73, no. 3, pp. 182-190, Dec 2007.
[9] C. Y. Chen Peter, S. C. Herath, Dong-An Wang, K. Su, K. Liao and H.
Asada, "Active manipulation of uniaxial ECM stiffness by magnetic
anchoring of bio-conjugated beads," in Proc. ASME Summer Bioengin.
Conf., Pennsylvania, 2011, pp. 1-14.
[10] M. C. Kim, C. Kim, L. Wood, D. Neal, R. D. Kamm and H. H. Asada,
"Integrating focal adhesion dynamics, cytoskeleton remodeling, and
actin motor activity for predicting cell migration on 3D curved surfaces
of the extracellular matrix," Integr. Biol., vol. 4, pp. 1386-1397, Oct
2012.
[11] C. Franck, S. A. Masharinec, D. A. Tirrell and G. Ravichandran "Three-
Dimensional Traction Force Microscopy: A New Tool for Quantifying
Cell-Matrix Interactions," PLoS One, vol. 6, pp. e17833, Mar 2011.
[12] W. A. Farahat, L. B. Wood, I. K. Zervantonakis, A. Schor, S. Ong, D.
Neal, R. D. Kamm and H. H. Asada, "Ensemble Analysis of Angiogenic
Growth in Three-Dimensional Microfluidic Cell Cultures," PLoS One
vol.7, pp. e37333, May 2012.
[13] Adrian RJ, "Twenty years of particle image velocimetry," Exp. Fluids,
vol. 39, pp. 159-169, 2005.
[14] M. Raffel, C. Willert, S. Wereley and J. Kompenhans, Particle Image
Velocimetry: A PracticleGuide. New York: Springer-Verlag, 2007, ch.
3.
[15] S. A. Maskarinec, C. Frank, D. A. Tirrell and G. Ravichandran,
"Quantifying cellular traction forces in three dimensions," Proc. Natl.
Acad. Sci. U S A, vol. 106, no.52, pp. 22108-22113, Dec 2009..
[16] N. D. Kirkpatrick, S. Andreou, J. B. Hoying and U. Utzinger, "Live
imaging of collagen remodeling during angiogenesis," Am. J. Physiol.
Heart Circ. Physiol., vol. 292, pp. H3198-H3206, Jun 2007.
[17] L. B. Wood, R. Ge, R. D. Kamn and H. H. Asada, "Nascent vessel
elongation rate is inversely related to diameter in in vitro angiogenesis"
Integr. Biol., vol. 4, pp. 1081-1089, Sep 2012.
[18] A. N. Stratman, W. B. Saunders, A. Sacharidou, W. Koh, K. E. Fisher,
D. C. Zawieja, M. J. Davis and G. E. Davis, " Endothelial cell lumen
and vascular guidance tunnel ormation requires MT1-MMP-dependent
proteolysis in 3-dimensional collagen matrices," Blood, vol. 114, pp.
237-247, Apr 2009.
[19] T. H. Chun, F. Sabeh, I. Ota, H. Murphy, K. T. McDonagh, K.
Holmbeck, H. Birkedal-Hansen, E. D. Allen and S. J. Weiss, "MT1-
MMP-dependent neovessel formation within the confines of the threedimensional
extracellular matrix," J. Cell Biol., vol. 167, pp. 757-767,
Nov 2004.
[1] P. Carmeliet, "Angiogenesis in health and disease," Nat. Med., vol. 9,
No. 6, pp.653-660, Jun 2003.
[2] D. E. Ingber, "Can cancer be reversed by engineering the tumor
microenvironment?" Semin. Cancer Biol., vol. 18, pp. 356-364, Apr
2008.
[3] N. C. Rivron, E. J. Vrij, J. Rouwkema, G. S. Le, van den Berg A, R. K.
Truckenm├╝ller and C. A. van Blitterswijk, "Tissue deformation spatially
modulates VEGF signaling and angiogenesis," Proc. Natl. Acad. Sci. U
S A, vol. 109, no. 18, pp. 6886-6891, May 2012.
[4] A. Shay-salit, M. Shushy, E. Wolfovitz, H. Yahav, F. Breviario, E.
Dejana and N. Resnick, "VEGF receptor 2 and the adherens junction as
a mechanical transducer in vascular endothelial cells," Proc. Natl. Acad.
Sci. U S A, vol. 99, pp. 9462-9467, Jul. 2002.
[5] D. L. Christiansen, E. K. Huang and F. H. Silver, "Assembly of type I
collagen: fusion of fibril subunits and the influence of fibril diameter on
mechanical properties," Matrix Biol., vol. 19, pp. 409-420, Sep. 2000.
[6] S. Kanzawa, H. Endo and N. Shioya, "Improved in vitro angiogenesis
model by collagen density reduction and the use of type III collagen,"
Ann. Plast. Surg., vol. 30, no. 3, pp. 244-251, Mar. 1993.
[7] A. L. Sieminski, R. P. Hebbel and K. J. Gooch, "The relative magnitude
of endothelial force generation and matrix stiffness modulate capillary
morphogenesis," Exp. Cell Res., vol. 297, no. 2, pp. 574-584, Jul 2004.
[8] A. Stéphanou, G. Meskaoui, B. Vailhé and P. Tracqui, "The rigidity in
fibrin gels as a contributing factor to the dynamics of in vitro vascular
cord formation," Microvasc. Res.,vol. 73, no. 3, pp. 182-190, Dec 2007.
[9] C. Y. Chen Peter, S. C. Herath, Dong-An Wang, K. Su, K. Liao and H.
Asada, "Active manipulation of uniaxial ECM stiffness by magnetic
anchoring of bio-conjugated beads," in Proc. ASME Summer Bioengin.
Conf., Pennsylvania, 2011, pp. 1-14.
[10] M. C. Kim, C. Kim, L. Wood, D. Neal, R. D. Kamm and H. H. Asada,
"Integrating focal adhesion dynamics, cytoskeleton remodeling, and
actin motor activity for predicting cell migration on 3D curved surfaces
of the extracellular matrix," Integr. Biol., vol. 4, pp. 1386-1397, Oct
2012.
[11] C. Franck, S. A. Masharinec, D. A. Tirrell and G. Ravichandran "Three-
Dimensional Traction Force Microscopy: A New Tool for Quantifying
Cell-Matrix Interactions," PLoS One, vol. 6, pp. e17833, Mar 2011.
[12] W. A. Farahat, L. B. Wood, I. K. Zervantonakis, A. Schor, S. Ong, D.
Neal, R. D. Kamm and H. H. Asada, "Ensemble Analysis of Angiogenic
Growth in Three-Dimensional Microfluidic Cell Cultures," PLoS One
vol.7, pp. e37333, May 2012.
[13] Adrian RJ, "Twenty years of particle image velocimetry," Exp. Fluids,
vol. 39, pp. 159-169, 2005.
[14] M. Raffel, C. Willert, S. Wereley and J. Kompenhans, Particle Image
Velocimetry: A PracticleGuide. New York: Springer-Verlag, 2007, ch.
3.
[15] S. A. Maskarinec, C. Frank, D. A. Tirrell and G. Ravichandran,
"Quantifying cellular traction forces in three dimensions," Proc. Natl.
Acad. Sci. U S A, vol. 106, no.52, pp. 22108-22113, Dec 2009..
[16] N. D. Kirkpatrick, S. Andreou, J. B. Hoying and U. Utzinger, "Live
imaging of collagen remodeling during angiogenesis," Am. J. Physiol.
Heart Circ. Physiol., vol. 292, pp. H3198-H3206, Jun 2007.
[17] L. B. Wood, R. Ge, R. D. Kamn and H. H. Asada, "Nascent vessel
elongation rate is inversely related to diameter in in vitro angiogenesis"
Integr. Biol., vol. 4, pp. 1081-1089, Sep 2012.
[18] A. N. Stratman, W. B. Saunders, A. Sacharidou, W. Koh, K. E. Fisher,
D. C. Zawieja, M. J. Davis and G. E. Davis, " Endothelial cell lumen
and vascular guidance tunnel ormation requires MT1-MMP-dependent
proteolysis in 3-dimensional collagen matrices," Blood, vol. 114, pp.
237-247, Apr 2009.
[19] T. H. Chun, F. Sabeh, I. Ota, H. Murphy, K. T. McDonagh, K.
Holmbeck, H. Birkedal-Hansen, E. D. Allen and S. J. Weiss, "MT1-
MMP-dependent neovessel formation within the confines of the threedimensional
extracellular matrix," J. Cell Biol., vol. 167, pp. 757-767,
Nov 2004.
@article{"International Journal of Biological, Life and Agricultural Sciences:56600", author = "Yue Du and Sahan C. B. Herath and Qing-Guo Wang and Harry Asada and Peter C. Y. Chen", title = "Endothelial-Cell-Mediated Displacement of Extracellular Matrix during Angiogenesis", abstract = "Mechanical interaction between endothelial cells (ECs) and the extracellular matrix (or collagen gel) is known to influence the sprouting response of endothelial cells during angiogenesis. This influence is believed to impact on the capability of endothelial cells to sense soluble chemical cues. Quantitative analysis of endothelial-cell-mediated displacement of the collagen gel provides a means to explore this mechanical interaction. Existing analysis in this context is generally limited to 2D settings. In this paper, we investigate the mechanical interaction between endothelial cells and the extracellular matrix in terms of the endothelial-cellmediated displacement of the collagen gel in both 2D and 3D. Digital image correlation and Digital volume correlation are applied on confocal reflectance image stacks to analyze cell-mediated displacement of the gel. The skeleton of the sprout is extracted from phase contrast images and superimposed on the displacement field to further investigate the link between the development of the sprout and the displacement of the gel.
", keywords = "Angiogenesis, digital image correlation, digital
volume correlation, interaction between ECs and ECM.", volume = "6", number = "12", pages = "1102-6", }
