Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-28T09:22:05.113Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of endothelial glycocalyx layer microstructure upon its role as a mechanotransducer

Published online by Cambridge University Press:  22 April 2020

T. C. Lee Open the ORCID record for T. C. Lee [Opens in a new window] ,
V. Suresh Open the ORCID record for V. Suresh [Opens in a new window]  and
R. J. Clarke Open the ORCID record for R. J. Clarke [Opens in a new window]
T. C. Lee
Affiliation:
Department of Engineering Science, University of Auckland, Auckland, New Zealand
V. Suresh
Affiliation:
Department of Engineering Science, University of Auckland, Auckland, New Zealand Auckland Bioengineering Institute, University of Auckland, Auckland, New Zealand
R. J. Clarke*
Affiliation:
Department of Engineering Science, University of Auckland, Auckland, New Zealand
*
†Email address for correspondence: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The endothelial glycocalyx layer (EGL) is a brush-like layer that lines the internal surfaces of blood vessels. It is thought to serve a number of physiological functions, including as a mechanotransducer of fluid loadings to the vessel wall. However, the fragility of the EGL makes it difficult to examine experimentally, and so there is much value in theoretical models that can help to explain the dynamical behaviour of the EGL. Most previous models have employed mixture theory to mechanically describe the layer, which treats the EGL as a isotropic linearly poroelastic layer. However, there is increasing experimental evidence to suggest that the EGL has a well-defined organisational structure that might not necessarily be well captured by such mixture theory descriptions. We therefore employ homogenisation theory to incorporate into the models some of the possible EGL microstructure suggested by the current biological literature. We explore how mechanotransduction varies under the different possible EGL microstructures, which potentially has important consequences to our understanding of how structural changes to the EGL might affect a vessel’s ability to respond to hemodynamical cues. We also find that, whereas mechanotransduction through the solid components of the EGL is dominated by the fluid tractions applied at the lumen–EGL interface, the component carried through its fluid phase is most sensitive to pressure gradients within the bulk EGL. This is relevant, since it is known that the underlying endothelial cells respond differently to these two different forms of mechanical loading.

JFM classification

Biological Fluid Dynamics: Blood flow
Type
JFM Papers
Information
Journal of Fluid Mechanics , Volume 893 , 25 June 2020 , A20
Copyright
© The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arkill, K. P., Knupp, C., Michel, C. C., Neal, C. R., Qvortrup, K., Rostgaard, J. & Squire, J. M. 2011 Similar endothelial glycocalyx structures in microvessels from a range of mammalian tissues: evidence for a common filtering mechanism? Biophys. J. 101 (PMC3164174), 1046–1056.CrossRefGoogle ScholarPubMed
Arkill, K. P., Neal, C. R., Mantell, J. M., Michel, C. C., Qvortrup, K., Rostgaard, J., Bates, D. O., Knupp, C. & Squire, J. M. 2012 3D reconstruction of the glycocalyx structure in mammalian capillaries using electron tomography. Microcirculation 19, 343–351.CrossRefGoogle ScholarPubMed
Barbee, K. A., Davies, P. F. & Lal, R. 1994 Shear stress-induced reorganization of the surface topography of living endothelial cells imaged by atomic force microscopy. Circul. Res. 74 (1), 163–171.CrossRefGoogle ScholarPubMed
Becker, B. F., Jacob, M., Leipert, S., Salmon, A. H. J. & Chappell, D. 2015 Degradation of the endothelial glycocalyx in clinical settings: searching for the sheddases. British J. Clin. Pharmacol. 80 (3), 389–402.CrossRefGoogle ScholarPubMed
Curry, F. E. & Adamson, R. H. 2012 Endothelial glycocalyx: permeability barrier and mechanosensor. Ann. Biomed. Engng 40 (4), 828–839.CrossRefGoogle ScholarPubMed
Curry, F. E. & Michel, C. C. 1980 A ber matrix model of capillary permeability. Microvasc. Res. 20, 96–99.CrossRefGoogle Scholar
Damiano, E. R., Duling, B. R., Ley, K. & Skalak, T. C. 1996 Axisymmetric pressure-driven flow of rigid pellets through a cylindrical tube lined with a deformable porous wall layer. J. Fluid Mech. 314 (4), 163–189.CrossRefGoogle Scholar
Damiano, E. R. & Stace, T. M. 2002 A mechano-electrochemical model of radial deformation of the capillary glycocalyx. Biophys. J. 82 (3), 1153–1175.CrossRefGoogle ScholarPubMed
Damiano, E. R. & Stace, T. M. 2005 Flow and deformation of the capillary glycocalyx in the wake of a leukocyte. Phys. Fluids 17 (031509), 1–17.CrossRefGoogle Scholar
Debagh, M., Jalali, P., Butler, P. J. & Tarbell, J. M. 2014 Shear-induced force transmission in a multicomponent, multicell model of the endothelium. J. R. Soc. Interface 1, 20140431.Google Scholar
Florian, J. A., Kosky, J. R., Ainslie, K., Pang, Z., Dull, R. O. & Tarbell, J. M. 2003 Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circul. Res. 93 (10), e136–e142.CrossRefGoogle ScholarPubMed
Fowler, A. C. 1998 Mathematical Models in the Applied Sciences, 2nd edn. Cambridge University Press.CrossRefGoogle Scholar
Hariprasad, D. S. & Secomb, T. W. 2012 Motion of red blood cells near microvesselwalls: effects of a porous wall layer. J. Fluid Mech. 705, 195–212.CrossRefGoogle ScholarPubMed
Hornung, U. 1997 Homogenization and Porous Media, vol. 6. Springer.CrossRefGoogle Scholar
Hu, X. & Weinbaum, S. 1999 A new view of Starling’s hypothesis at the microstructural level. Microvasc. Res. 58 (3), 281–304.CrossRefGoogle ScholarPubMed
Jansen, K. A., Atherton, P. & Ballestrem, C. 2017 Mechanotransduction at the cell–matrix interface. Semin. Cell Dev. Biol. 71, 75–83.CrossRefGoogle ScholarPubMed
Jiang, X. Z., Gong, H., Luo, K. H. & Ventikos, Y. 2017 Large-scale molecular dynamics simulation of coupled dynamics of flow and glycocalyx: towards understanding atomic events on an endothelial cell surface. J. R. Soc. Interface 14 (137), 20170780.CrossRefGoogle ScholarPubMed
Lee, T. C., Long, D. S. & Clarke, R. J. 2016 Effect of endothelial glycocalyx layer redistribution upon microvessel poroelastohydrodynamics. J. Fluid Mech. 798, 812–852.CrossRefGoogle Scholar
Levick, J. R. & Michel, C. C. 2010 Microvascular fluid exchange and the revised starling principle. Cardiovasc. Res. 87 (2), 198–210.CrossRefGoogle ScholarPubMed
Liu, M. & Yang, J. 2009 Electrokinetic effect of the endothelial glycocalyx layer on two-phase blood flow in small blood vessels. Microvasc. Res. 78, 14–19.CrossRefGoogle ScholarPubMed
Papanicolau, G., Bensoussan, A. & Lions, J.-L. 1979 Asymptotic Analysis for Periodic Structures, vol. 5. North Holland.Google Scholar
Pavliotis, G. & Stuart, A. 2008 Multiscale Methods. Springer.Google Scholar
Secomb, T. W., Hsu, R. & Pries, A. R. 2001 Effect of the endothelial surface layer on transmission of fluid shear stress to endothelial cells. Biorheology 38 (2–3), 143–150.Google ScholarPubMed
Squire, J. M., Chew, M., Nneji, G., Barry, J. & Michel, C. 2002 Quasi-periodic substructure in the microvessel endothelial glycocalyx: a possible explanation for molecular filtering? J. Struct. Biol. 136 (3), 229–255.Google Scholar
Squire, J. M., Chew, M., Nneji, G., Neal, C., Barry, J. & Michel, C. 2001 Quasi-periodic substructure in the microvessel endothelial glycocalyx: a possible explanation for molecular filtering? J. Struct. Biol. 136 (3), 239–255.CrossRefGoogle ScholarPubMed
Stace, T. M. & Damiano, E. R. 2001 An electrochemical model of the transport of charged molecules through the capillary glycocalyx. Biophys. J. 80, 1670–1690.CrossRefGoogle ScholarPubMed
Sumets, P. P., Cater, J. E., Long, D. S. & Clarke, R. J. 2015 A boundary-integral representation for biphasic mixture theory, with application to the post-capillary glycocalyx. Proc. R. Soc. Lond. A 471 (2179), 20140955.CrossRefGoogle ScholarPubMed
Sumets, P. P., Cater, J. E., Long, D. S. & Clarke, R. J. 2018 Electro-poroelastohydrodynamics of the endothelial glycocalyx layer. J. Fluid Mech. 838, 284–319.CrossRefGoogle Scholar
Tarbell, J. M. & Pahakis, M. Y. 2006 Mechanotransduction and the glycocalyx. J. Intl Medicine 259 (4), 339–350.CrossRefGoogle ScholarPubMed
Thi, M. M., Tarbell, J. M., Weinbaum, S. & Spray, D. C. 2004 The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a ‘bumper-car’ model. Proc. Natl Acad. Sci. USA 101 (47), 16483–16488.CrossRefGoogle ScholarPubMed
Vink, H., Constantinescu, A. A. & Spaan, J. A. E. 2000 Oxidized lipoproteins degrade the endothelial surface layer. Circulation 101 (13), 1500–1502.CrossRefGoogle ScholarPubMed
Wei, H. H., Waters, S. L., Liu, S. Q. & Grotberg, J. B. 2003 Flow in a wavy-walled channel lined with a poroelastic layer. J. Fluid Mech. 492, 23–45.CrossRefGoogle Scholar
Weinbaum, S., Tarbell, J. M. & Damiano, E. R. 2007 The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Engng 9 (1), 121–167.CrossRefGoogle ScholarPubMed
Weinbaum, S., Zhang, X., Han, Y., Vink, H. & Cowin, S. C. 2003 Mechanotransduction and flow across the endothelial glycocalyx. Proc. Natl Acad. Sci. USA 100 (13), 7988–7995.CrossRefGoogle ScholarPubMed
Yao, Y., Rabodzey, A. & Dewey, C. F. 2007 Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress. Amer. J. Physiol. 293 (2), H1023–H1030; pMID: 17468337.Google ScholarPubMed
Supplementary material: File

Lee et al. supplementary material

Lee et al. supplementary material

Download Lee et al. supplementary material(File)
File 7.2 KB