Abstract
Blood vessels often have an undulatory morphology, with excessive bending, kinking, and coiling occuring in diseased vasculature. The underlying physical causes of these morphologies are generally attributed, in combination, to changes in blood pressure, blood flow rate, and cell proliferation or apoptosis. However, pathological vascular morphologies often start during developmental vasculogenesis. At early stages of vasculogenesis, angioblasts (vascular endothelial cells that have not formed a lumen) assemble into primitive vessel-like fibers before blood flow occurs. If loose, fibrous aggregates of endothelial cells can generate multi-cellular undulations through mechanical instabilities, driven by the cytoskeleton, new insight into vasculature morphology may be achieved with simple in vitro models of endothelial cell fibers. Here we study mechanical instabilities in vessel-like structures made from endothelial cells embedded in a collagen matrix. We find that endothelial cell fibers contract radially over time, and undulate at two dominant wavelengths: approximately 1cm and 1mm. Simple mechanical models suggest that the long-wavelength undulation is Euler buckling in rigid confinement, while the short-wavelength buckle may arise from a mismatch between fiber bending energy and matrix deformation. These results suggest a combination of fiber-like geometry, cystoskeletal contractions, and extracellular matrix elasticity may contribute to undulatory blood vessel morphology in the absence of a lumen or blood pressure.
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D.E. Discher, P. Janmey, Y.-l. Wang, Science 310, 5751 (2005).
A. Harris, P. Wild, D. Stopak, Science 208, 4440 (1980).
M. Dembo, Y.-L. Wang, Biophys. J. 76, 4 (1999).
S. Lehoux, A. Tedgui, J. Biomech. 36, 5 (2003).
B. Langille, R. Brownlee, S. Adamson, Am. J. Physiol. 259, 28 (1990).
R.A. Bomberger et al., J. Surgical Res. 28, 5 (1980).
J.R. Guyton, C.J. Hartley, Am. J. Physiol. 248, H540 (1985).
L. Pellegrino, G. Prencipe, F. Vairo, Minerva Cardioangiol. 46, 3 (1998).
D. Mukherjee, T. Inahara, Am. J. Surgery 149, 5 (1985).
P. Pancera et al., Int. Angiol. 17, 1 (1998).
A.M. Waxman, Microvascular Res. 22, 1 (1981).
R. Beigelman et al., Angiology 61, 1 (2010).
C. Tickle, Principles of development (Oxford University Press, 2011).
W. Risau, Nature 386, 6626 (1997).
E. Bell, B. Ivarsson, C. Merrill, Proc. Natl. Acad. Sci. U.S.A. 76, 3 (1979).
J. Howard, Mechanics of motor proteins and the cytoskeleton (Sinauer Associates Inc., 2001).
C.P. Brangwynne et al., Biophys. J. 93, 1 (2007).
C.P. Brangwynne et al., J. Cell Biol. 173, 5 (2006).
L. Cipelletti, D. Weitz, Rev. Sci. Instrum. 70, 8 (1999).
L.D. Landau, E.M. Lifshitz, Course of Theoretical Physics, Vol. 7: Theory and Elasticity (Pergamon Press, 1959).
D. Vader et al., PLoS ONE 4, 6 (2009).
N. Wang et al., Proc. Natl. Acad. Sci. U.S.A. 98, 14 (2001).
J. Wu et al., Mol. Biol. Cell 22, 24 (2011).
N. Shekhar et al., Cell. Mol. Bioengin. 6, 2 (2013).
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Frketic, J.B., DeLaPeña, A., Suaris, M.G. et al. Multi-scale undulations in human aortic endothelial cell fibers. Eur. Phys. J. E 38, 12 (2015). https://doi.org/10.1140/epje/i2015-15012-9
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DOI: https://doi.org/10.1140/epje/i2015-15012-9