Spatio-temporal development of the endothelial glycocalyx layer and its mechanical property in vitro

Journal of the Royal Society Interface

Volumn 9, Issue 74, 2012, Pages 2290-2298

  Bai, Ke ^a   Wang, Wen ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Atomic force microscopy nano indentation; Confocal microscopy; The glycocalyx; Vascular endothelium; Young's modulus

Indexed keywords

ATOMIC FORCE MICROSCOPY; CELL CULTURE; CELL MEMBRANES; CONFOCAL MICROSCOPY; ELASTIC MODULI; ENDOTHELIAL CELLS; GLYCOPROTEINS;

AFM; APICAL MEMBRANES; CONFOCAL MICROSCOPES; FORCE-DISTANCE CURVES; HEPARANASE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; IN-VITRO; NEURAMINIDASE; POLYSACCHARIDE MATRIX; PROTEOGLYCANS; SPATIO-TEMPORAL; TEMPORAL DEVELOPMENT; THE GLYCOCALYX; THIN LAYERS; TIME PROGRESS; VASCULAR ENDOTHELIUM; YOUNG'S MODULUS;

BIOMECHANICS;

HEPARANASE; SIALIDASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CELL CULTURE; CELL MEMBRANE; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GLYCOCALYX; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; SHEAR STRESS; THORACIC AORTA; UMBILICAL VEIN ENDOTHELIAL CELL; YOUNG MODULUS;

EID: 84866181957     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2011.0901     Document Type: Article

References (45)

1. Middleton, J., Neil, S., Wintle, J., Clark-Lewis, I., Moore, H., Lam, C., Auer, M., Hub, E. & Rot, A. 1997 Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91, 385-395. (doi:10.1016/S0092-8674(00) 80422-5)
2. Cai, H. & Harrison, D. G. 2000 Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 87, 840-844. (doi:10.1161/01.RES.87.10.840)
3. Davignon, J. & Ganz, P. 2004 Atherosclerosis: evolving vascular biology and clinical implications. Circulation 109, III-27-III-32. (doi:10.1161/01.CIR.0000131515.03336.f8)
4. 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, 239-255. (doi:10.1006/jsbi.2002.4441)
5. Luft, J. H. 1966 Fine structure of capillary and endocapillary layer as revealed by ruthenium red. Federation Proc. 25, 1773-1783.
6. Oohira, A., Wight, T. N. & Bornstein, P. 1983 Sulfated proteoglycans synthesized by vascular endothelial cells in culture. J. Biol. Chem. 258 , 2014-2021.
7. Jackson, R. L., Busch, S. J. & Cardin, A. D. 1991 Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol. Rev. 71, 481-539.
8. Lipowsky, H. H. 2005 Microvascular rheology and hemodynamics. Microcirculation 12, 5-15. (doi:10.1080/10739680590894966)
9. Gouverneur, M., Van Den Berg, B., Nieuwdorp, M., Stroes, E. & Vink, H. 2006 Vasculoprotective properties of the endothelial glycocalyx: effects of fluid shear stress. J. Intern. Med. 259, 393-400. (doi:10.1111/j.1365-2796.2006. 01625.x)
10. Levick, J. R. & Michel, C. C. 2010 Microvascular fluid exchange and the revised starling principle. Cardiovasc. Res. 87, 198-210. (doi:10.1093/cvr/cvq062)
11. Michel, C. C. & Kendall, S. 1997 Differing effects of histamine and serotonin on microvascular permeability in anaesthetized rats. J. Physiol. 501, 657-662. (doi:10.1111/j.1469-7793.1997.657bm.x)
12. Weinbaum, S. 1998 Whitaker distinguished lecture: models to solve mysteries in biomechanics at the cellular level; a new view of fiber matrix layers. Ann. Biomed. Eng. 26 , 627-643. (doi:10.1114/1.134)
13. Wang, W. & Parker, K. H. 1995 The effect of deformable porous surface layers on the motion of a sphere in a narrow cylindrical tube. J. Fluid Mech. 283, 287-295. (doi:10.1017/S0022112095002321)
14. Mochizuki, S., Vink, H., Hiramatsu, O., Kajita, T., Shigeto, F., Spaan, J. A. E. & Kajiya, F. 2003 Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am. J. Physiol. Heart Circ. Physiol. 285, H722-H726. (doi:10.1152/ajpheart.00691.2002)
15. Damiano, E. R. 1998 The effect of the endothelial-cell glycocalyx on the motion of red blood cells through capillaries. Microvasc. Res. 55, 77-91. (doi:10.1006/mvre.1997.2052)
16. Zhao, Y., Chien, S. & Weinbaum, S. 2001 Dynamic contact forces on leukocyte microvilli and their penetration of the endothelial glycocalyx. Biophys. J. 80, 1124-1140. (doi:10.1016/S0006-3495(01)76090-0)
17. Damiano, E. R. & Stace, T. M. 2002 A mechanoelectrochemical model of radial deformation of the capillary glycocalyx. Biophys. J. 82, 1153-1175. (doi:10.1016/S0006-3495(02)75474-X)
18. Florian, J. A., Kosky, J. R., Alinslie, K., Pang, Z., Dull, R. O. & Tarbell, J. M. 2003 Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ. Res. 93, e136-e142. (doi:10.1161/01.RES.0000101744. 47866.D5)
19. Gouverneur, M., Spaan, J. A., Pannekoek, H., Fontijn, R. D. & Vink, H. 2006 Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx. Am. J. Physiol. Heart Circ. Physiol. 290, H458-H462. (doi:10.1152/ajpheart.00592.2005)
20. 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, 143-150.
21. Tarbell, J., Weinbaum, S. & Kamm, R. 2005 Cellular fluid mechanics and mechanotransduction. Ann. Biomed. Eng. 33, 1719-1723. (doi:10.1007/s10439- 005-8775-z)
22. 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 'bumpercar' model. Proc. Natl Acad. Sci. USA 101, 16 483-16 488.
23. Yao, Y., Rabodzey, A. & Dewey Jr, C. F. 2007 Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress. Am. J. Physiol. Heart Circ. Physiol. 293, H1023-H1030. (doi:10.1152/ajpheart.00162.2007)
24. van den Berg, B. M., Spaan, J. A. E., Rolf, T. M. & Vink, H. 2006 Atherogenic region and diet diminish glycocalyx dimension and increase intima-to-media ratios at murine carotid artery bifurcation. Am. J. Physiol. Heart Circ. Physiol. 290, H915-H920. (doi:10.1152/ajpheart.00051.2005)
25. Guck, J. et al . 2005 Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys. J. 88, 3689-3698. (doi:10.1529/biophysj.104.045476)
26. Yamazaki, D., Kurisu, S. & Takenawa, T. 2005 Regulation of cancer cell motility through actin reorganization. Cancer Sci. 96, 379-386. (doi:10.1111/j.1349-7006.2005.00062.x)
27. Sheetz, M. P. 2006 Cellular plasma membrane domains. Mol. Membr. Biol. 12, 89-91. (doi:10.3109/09687689509038501)
28. Drake, B., Prater, C. B., Weisenhorn, A. L., Gould, S. A., Albrecht, T. R., Quate, C. F., Cannell, D. S., Hansma, H. G. & Hansma, P. K. 1989 Imaging crystals, polymers, and processes in water with the atomic force microscope. Science 243, 1586-1589. (doi:10.1126/science.2928794)
29. Henderson, E. 1994 Imaging of living cells by atomic force microscopy. Progr. Surf. Sci. 46, 39-60. (doi:10.1016/0079-6816(94)90006-X)
30. Sato, H., Katano, M., Takigawa, T. & Masuda, T. 2001 Estimation for the elasticity of vascular endothelial cells on the basis of atomic force microscopy and Young's modulus of gelatin gels. Polym. Bull. 47 , 375-381. (doi:10.1007/s289-001-8195-z)
31. Sato, H., Kataoka, N., Kajiya, F., Katano, M., Takigawa, T. & Masuda, T. 2004 Kinetic study on the elastic change of vascular endothelial cells on collagen matrices by atomic force microscopy. Colloids Surf. B Biointerfaces 34, 141-146. (doi:10.1016/j.colsurfb.2003.12.013)
32. Kataoka, N., Iwaki, K., Hashimoto, K., Mochizuki, S., Ogasawara, Y., Sato, M., Tsujioka, K. & Kajiya, F. 2002 Measurements of endothelial cell-to-cell and cell-tosubstrate gaps and micromechanical properties of endothelial cells during monocyte adhesion. Proc. Natl Acad. Sci. USA 99, 15 638-15 643. (doi:10.1073/pnas.242590799)
33. Guilak, F., Jones, W. R., Ting-Beall, H. P. & Lee, G. M. 1999 The deformation behavior and mechanical properties of chondrocytes in articular cartilage. Osteoarthritis Cartilage 7, 59-70. (doi:10.1053/joca.1998.0162)
34. Rotsch, C., Jacobson, K. & Radmacher, M. 1999 Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proc. Natl Acad. Sci. USA 96, 921-926. (doi:10.1073/pnas.96.3.921)
35. Darling, E. M., Zauscher, S., Block, J. A. & Guilak, F. 2007 A thin-layer model for viscoelastic, stress-relaxation testing of cells using atomic force microscopy: do cell properties reflect metastatic potential? Biophys. J. 92, 1784-1791. (doi:10.1529/biophysj.106.083097)
36. Oberleithner, H., Peters, W., Kusche-Vihrog, K., Korte, S., Schillers, H., Kliche, K. & Oberleithner, K. 2011 Salt overload damages the glycocalyx sodium barrier of vascular endothelium. Archiv. Eur. J. Physiol. 462, 519-528. (doi:10.1007/s00424-011-0999-1)
37. O'Callaghan, R., Job, K. M., Dull, R. O. & Hlady, V. 2011 Stiffness and heterogeneity of the pulmonary endothelial glycocalyx measured by atomic force microscopy. Am. J. Physiol. Lung Cell. Mol. 301, L353-L360. (doi:10.1152/ajplung.00342.2010)
38. Barker, A. L., Konopatskaya, O., Neal, C. R., Macpherson, J. V., Whatmore, J. L., Winlove, C. P., Unwin, P. R. & Shore, A. C. 2004 Observation and characterisation of the glycocalyx of viable human endothelial cells using confocal laser scanning microscopy. Phys. Chem. Chem. Phys. 6, 1006-1011. (doi:10.1039/b312189e)
39. Megens, R. T. A., Reitsma, S., Schiffers, P. H. M., Hilgers, R. H. P., De Mey, J. G. R., Slaaf, D. W., Oudeegbrink, M. G. A. & Van Zandvoort, M. A. M. J. 2007 Twophoton microscopy of vital murine elastic and muscular arteries: combined structural and functional imaging with subcellular resolution. J. Vasc. Res. 44, 87-98. (doi:10.1159/000098259)
40. Muller, D. J. & Dufrene, Y. F. 2008 Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nat. Nanotechnol. 3, 261-269. (doi:10.1038/nnano.2008.100)
41. Hertz, H. 1882 Uber die Beruhrung fester elasticher Korper. J. für die reine Angew. Math. 92, 156-171. (doi:10.1515/crll.1882.92.156)
42. van den Berg, B. M., Vink, H. & Spaan, J. A. E. 2003 The endothelial glycocalyx protects against myocardial edema. Circ. Res. 92, 592-594. (doi:10.1161/01.RES.0000065917.53950.75)
43. Chappell, D., Jacob, M., Paul, O., Rehm, M., Welsch, U., Stoeckelhuber, M., Conzen, P. & Becker, B. F. 2009 The glycocalyx of the human umbilical vein endothelial cell: an impressive structure ex vivo but not in culture. Circ. Res. 104, 1313-1317. (doi:10.1161/CIRCRESAHA.108.187831)
44. Adamson, R. H. & Clough, G. 1992 Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels. J. Physiol. 445, 473-486.
45. Ebong, E. E., Macaluso, F. P., Spray, D. C. & Tarbell, J. M. 2011 Imaging the endothelial glycocalyx in vitro by rapid freezing/freeze substitution transmission electron microscopy. Arterioscler. Thromb. Vasc. Biol. 31, 1908-1915. (doi:10.1161/ATVBAHA.111.225268)