Abstract

The endothelial glycocalyx layer is a ~2 µm thick glycosaminoglycan rich pericellular matrix expressed on the luminal surface of vascular endothelial cells, which has implications in vessel mechanics and mechanotransduction. Despite its role in vascular physiology, no direct measurement has of yet been made of vessel glycocalyx material properties. Vaterite microviscometry is a laser tweezers based microrheological method, which has been previously utilized to measure the viscosity of linear and complex fluids under flow. This form of microrheology has until now relied on complete recollection of the forward scattered light. Here we present a novel method to extend vaterite microviscometry to relatively thick samples. We validate our method and its assumptions and measure the apparent viscosity as a function of distance from the vascular endothelium. We observe a differential response in conditions designed to preserve the EGL in comparison to those designed to collapse it.

© 2011 OSA

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  1. P. F. Davies, “Flow-mediated endothelial mechanotransduction,” Physiol. Rev.75(3), 519–560 (1995).
    [PubMed]
  2. S. Chien, “Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell,” Am. J. Physiol. Heart Circ. Physiol.292(3), H1209–H1224 (2007).
    [CrossRef] [PubMed]
  3. S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch.454(3), 345–359 (2007).
    [CrossRef] [PubMed]
  4. S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng.9(1), 121–167 (2007).
    [CrossRef] [PubMed]
  5. H. Vink and B. R. Duling, “Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries,” Circ. Res.79(3), 581–589 (1996).
    [PubMed]
  6. M. D. Savery and E. R. Damiano, “The endothelial glycocalyx is hydrodynamically relevant in arterioles throughout the cardiac cycle,” Biophys. J.95(3), 1439–1447 (2008).
    [CrossRef] [PubMed]
  7. M. L. Smith, D. S. Long, E. R. Damiano, and K. Ley, “Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo,” Biophys. J.85(1), 637–645 (2003).
    [CrossRef] [PubMed]
  8. M. M. Thi, J. M. Tarbell, S. Weinbaum, and D. C. Spray, “The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a “bumper-car” model,” Proc. Natl. Acad. Sci. U.S.A.101(47), 16483–16488 (2004).
    [CrossRef] [PubMed]
  9. J. M. Tarbell and M. Y. Pahakis, “Mechanotransduction and the glycocalyx,” J. Intern. Med.259(4), 339–350 (2006).
    [CrossRef] [PubMed]
  10. A. Oohira, T. N. Wight, and P. Bornstein, “Sulfated proteoglycans synthesized by vascular endothelial cells in culture,” J. Biol. Chem.258(3), 2014–2021 (1983).
    [PubMed]
  11. Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
    [CrossRef] [PubMed]
  12. R. D. Rosenberg, N. W. Shworak, J. Liu, J. J. Schwartz, and L. Zhang, “Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?” J. Clin. Invest.99(9), 2062–2070 (1997).
    [CrossRef] [PubMed]
  13. R. Kokenyesi and M. Bernfield, “Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1,” J. Biol. Chem.269(16), 12304–12309 (1994).
    [PubMed]
  14. N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
    [CrossRef] [PubMed]
  15. N. Nijenhuis, D. Mizuno, J. A. Spaan, and C. F. Schmidt, “Viscoelastic response of a model endothelial glycocalyx,” Phys. Biol.6(2), 025014 (2009).
    [CrossRef] [PubMed]
  16. N. Nijenhuis, D. Mizuno, C. F. Schmidt, H. Vink, and J. A. E. Spaan, “Microrheology of hyaluronan solutions: implications for the endothelial glycocalyx,” Biomacromolecules9(9), 2390–2398 (2008).
    [CrossRef] [PubMed]
  17. C. B. S. Henry and B. R. Duling, “Permeation of the luminal capillary glycocalyx is determined by hyaluronan,” Am. J. Physiol.277(2 Pt 2), H508–H514 (1999).
    [PubMed]
  18. A. Yoneda and J. R. Couchman, “Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans,” Matrix Biol.22(1), 25–33 (2003).
    [CrossRef] [PubMed]
  19. P. V. Jensen and L. I. Larsson, “Actin microdomains on endothelial cells: association with CD44, ERM proteins, and signaling molecules during quiescence and wound healing,” Histochem. Cell Biol.121(5), 361–369 (2004).
    [CrossRef] [PubMed]
  20. D. R. Potter and E. R. Damiano, “The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro,” Circ. Res.102(7), 770–776 (2008).
    [CrossRef] [PubMed]
  21. E. R. Damiano and T. M. Stace, “A mechano-electrochemical model of radial deformation of the capillary glycocalyx,” Biophys. J.82(3), 1153–1175 (2002).
    [CrossRef] [PubMed]
  22. Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech.554(-1), 217–235 (2006).
    [CrossRef]
  23. T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol.281(2), H629–H636 (2001).
    [PubMed]
  24. S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A.100(13), 7988–7995 (2003).
    [CrossRef] [PubMed]
  25. G. Knoner, S. Parkin, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Characterization of optically driven fluid stress fields with optical tweezers,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.72(3), 031507 (2005).
    [CrossRef] [PubMed]
  26. S. J. W. Parkin, G. G. Knoener, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “A constant torque micro-viscometer,” in Nanomanipulation with Light (SPIE, San Jose, CA, USA, 2005), pp. 59–65.
  27. A. I. Bishop, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical microrheology using rotating laser-trapped particles,” Phys. Rev. Lett.92(19), 198104 (2004).
    [CrossRef] [PubMed]
  28. T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-dunlop, “Optical measurement of microscopic torques,” J. Mod. Opt.48, 405–413 (2001).
  29. M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
    [CrossRef] [PubMed]
  30. M. W. Allersma, F. Gittes, M. J. deCastro, R. J. Stewart, and C. F. Schmidt, “Two-dimensional tracking of ncd motility by back focal plane interferometry,” Biophys. J.74(2), 1074–1085 (1998).
    [CrossRef] [PubMed]
  31. K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct.23(1), 247–285 (1994).
    [CrossRef] [PubMed]
  32. B. Schnurr, F. Gittes, F. C. MacKintosh, and C. F. Schmidt, “Determining microscopic viscoelasticity in flexible and semiflexible polymer networks from thermal fluctuations,” Macromolecules30(25), 7781–7792 (1997).
    [CrossRef]
  33. E. J. G. Peterman, F. Gittes, and C. F. Schmidt, “Laser-induced heating in optical traps,” Biophys. J.84(2), 1308–1316 (2003).
    [CrossRef] [PubMed]
  34. D. Mizuno, D. A. Head, F. C. MacKintosh, and C. F. Schmidt, “Active and passive microrheology in equilibrium and nonequilibrium systems,” Macromolecules41(19), 7194–7202 (2008).
    [CrossRef]
  35. F. Gittes, B. Schnurr, P. D. Olmsted, F. C. MacKintosh, and C. F. Schmidt, “Microscopic viscoelasticity: Shear moduli of soft materials determined from thermal fluctuations,” Phys. Rev. Lett.79(17), 3286–3289 (1997).
    [CrossRef]
  36. R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
    [CrossRef] [PubMed]
  37. R. H. Adamson and G. Clough, “Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels,” J. Physiol.445, 473–486 (1992).
    [PubMed]
  38. S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
    [PubMed]
  39. J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
    [CrossRef] [PubMed]
  40. Y. C. Fung, “What are the residual stresses doing in our blood vessels?” Ann. Biomed. Eng.19(3), 237–249 (1991).
    [CrossRef] [PubMed]
  41. A. E. X. Brown, R. I. Litvinov, D. E. Discher, P. K. Purohit, and J. W. Weisel, “Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water,” Science325(5941), 741–744 (2009).
    [CrossRef] [PubMed]
  42. J. P. Winer, S. Oake, and P. A. Janmey, “Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation,” PLoS ONE4(7), e6382 (2009).
    [CrossRef] [PubMed]
  43. E. W. Errill, “Rheology of blood,” Physiol. Rev.49(4), 863–888 (1969).
    [PubMed]
  44. R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
    [CrossRef] [PubMed]

2011 (1)

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

2009 (5)

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

N. Nijenhuis, D. Mizuno, J. A. Spaan, and C. F. Schmidt, “Viscoelastic response of a model endothelial glycocalyx,” Phys. Biol.6(2), 025014 (2009).
[CrossRef] [PubMed]

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

A. E. X. Brown, R. I. Litvinov, D. E. Discher, P. K. Purohit, and J. W. Weisel, “Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water,” Science325(5941), 741–744 (2009).
[CrossRef] [PubMed]

J. P. Winer, S. Oake, and P. A. Janmey, “Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation,” PLoS ONE4(7), e6382 (2009).
[CrossRef] [PubMed]

2008 (4)

N. Nijenhuis, D. Mizuno, C. F. Schmidt, H. Vink, and J. A. E. Spaan, “Microrheology of hyaluronan solutions: implications for the endothelial glycocalyx,” Biomacromolecules9(9), 2390–2398 (2008).
[CrossRef] [PubMed]

M. D. Savery and E. R. Damiano, “The endothelial glycocalyx is hydrodynamically relevant in arterioles throughout the cardiac cycle,” Biophys. J.95(3), 1439–1447 (2008).
[CrossRef] [PubMed]

D. Mizuno, D. A. Head, F. C. MacKintosh, and C. F. Schmidt, “Active and passive microrheology in equilibrium and nonequilibrium systems,” Macromolecules41(19), 7194–7202 (2008).
[CrossRef]

D. R. Potter and E. R. Damiano, “The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro,” Circ. Res.102(7), 770–776 (2008).
[CrossRef] [PubMed]

2007 (4)

S. Chien, “Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell,” Am. J. Physiol. Heart Circ. Physiol.292(3), H1209–H1224 (2007).
[CrossRef] [PubMed]

S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch.454(3), 345–359 (2007).
[CrossRef] [PubMed]

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng.9(1), 121–167 (2007).
[CrossRef] [PubMed]

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

2006 (2)

J. M. Tarbell and M. Y. Pahakis, “Mechanotransduction and the glycocalyx,” J. Intern. Med.259(4), 339–350 (2006).
[CrossRef] [PubMed]

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech.554(-1), 217–235 (2006).
[CrossRef]

2005 (1)

G. Knoner, S. Parkin, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Characterization of optically driven fluid stress fields with optical tweezers,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.72(3), 031507 (2005).
[CrossRef] [PubMed]

2004 (4)

A. I. Bishop, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical microrheology using rotating laser-trapped particles,” Phys. Rev. Lett.92(19), 198104 (2004).
[CrossRef] [PubMed]

P. V. Jensen and L. I. Larsson, “Actin microdomains on endothelial cells: association with CD44, ERM proteins, and signaling molecules during quiescence and wound healing,” Histochem. Cell Biol.121(5), 361–369 (2004).
[CrossRef] [PubMed]

Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
[CrossRef] [PubMed]

M. M. Thi, J. M. Tarbell, S. Weinbaum, and D. C. Spray, “The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a “bumper-car” model,” Proc. Natl. Acad. Sci. U.S.A.101(47), 16483–16488 (2004).
[CrossRef] [PubMed]

2003 (5)

M. L. Smith, D. S. Long, E. R. Damiano, and K. Ley, “Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo,” Biophys. J.85(1), 637–645 (2003).
[CrossRef] [PubMed]

A. Yoneda and J. R. Couchman, “Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans,” Matrix Biol.22(1), 25–33 (2003).
[CrossRef] [PubMed]

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A.100(13), 7988–7995 (2003).
[CrossRef] [PubMed]

E. J. G. Peterman, F. Gittes, and C. F. Schmidt, “Laser-induced heating in optical traps,” Biophys. J.84(2), 1308–1316 (2003).
[CrossRef] [PubMed]

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

2002 (1)

E. R. Damiano and T. M. Stace, “A mechano-electrochemical model of radial deformation of the capillary glycocalyx,” Biophys. J.82(3), 1153–1175 (2002).
[CrossRef] [PubMed]

2001 (2)

T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol.281(2), H629–H636 (2001).
[PubMed]

T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-dunlop, “Optical measurement of microscopic torques,” J. Mod. Opt.48, 405–413 (2001).

1999 (2)

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

C. B. S. Henry and B. R. Duling, “Permeation of the luminal capillary glycocalyx is determined by hyaluronan,” Am. J. Physiol.277(2 Pt 2), H508–H514 (1999).
[PubMed]

1998 (1)

M. W. Allersma, F. Gittes, M. J. deCastro, R. J. Stewart, and C. F. Schmidt, “Two-dimensional tracking of ncd motility by back focal plane interferometry,” Biophys. J.74(2), 1074–1085 (1998).
[CrossRef] [PubMed]

1997 (3)

B. Schnurr, F. Gittes, F. C. MacKintosh, and C. F. Schmidt, “Determining microscopic viscoelasticity in flexible and semiflexible polymer networks from thermal fluctuations,” Macromolecules30(25), 7781–7792 (1997).
[CrossRef]

F. Gittes, B. Schnurr, P. D. Olmsted, F. C. MacKintosh, and C. F. Schmidt, “Microscopic viscoelasticity: Shear moduli of soft materials determined from thermal fluctuations,” Phys. Rev. Lett.79(17), 3286–3289 (1997).
[CrossRef]

R. D. Rosenberg, N. W. Shworak, J. Liu, J. J. Schwartz, and L. Zhang, “Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?” J. Clin. Invest.99(9), 2062–2070 (1997).
[CrossRef] [PubMed]

1996 (1)

H. Vink and B. R. Duling, “Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries,” Circ. Res.79(3), 581–589 (1996).
[PubMed]

1995 (1)

P. F. Davies, “Flow-mediated endothelial mechanotransduction,” Physiol. Rev.75(3), 519–560 (1995).
[PubMed]

1994 (2)

R. Kokenyesi and M. Bernfield, “Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1,” J. Biol. Chem.269(16), 12304–12309 (1994).
[PubMed]

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct.23(1), 247–285 (1994).
[CrossRef] [PubMed]

1992 (1)

R. H. Adamson and G. Clough, “Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels,” J. Physiol.445, 473–486 (1992).
[PubMed]

1991 (1)

Y. C. Fung, “What are the residual stresses doing in our blood vessels?” Ann. Biomed. Eng.19(3), 237–249 (1991).
[CrossRef] [PubMed]

1983 (1)

A. Oohira, T. N. Wight, and P. Bornstein, “Sulfated proteoglycans synthesized by vascular endothelial cells in culture,” J. Biol. Chem.258(3), 2014–2021 (1983).
[PubMed]

1969 (1)

E. W. Errill, “Rheology of blood,” Physiol. Rev.49(4), 863–888 (1969).
[PubMed]

Adamson, R. H.

R. H. Adamson and G. Clough, “Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels,” J. Physiol.445, 473–486 (1992).
[PubMed]

Allersma, M. W.

M. W. Allersma, F. Gittes, M. J. deCastro, R. J. Stewart, and C. F. Schmidt, “Two-dimensional tracking of ncd motility by back focal plane interferometry,” Biophys. J.74(2), 1074–1085 (1998).
[CrossRef] [PubMed]

Alvarez-Elizondo, M. B.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Atzenhofer, W.

Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
[CrossRef] [PubMed]

Bernfield, M.

R. Kokenyesi and M. Bernfield, “Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1,” J. Biol. Chem.269(16), 12304–12309 (1994).
[PubMed]

Bishop, A. I.

A. I. Bishop, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical microrheology using rotating laser-trapped particles,” Phys. Rev. Lett.92(19), 198104 (2004).
[CrossRef] [PubMed]

Block, S. M.

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct.23(1), 247–285 (1994).
[CrossRef] [PubMed]

Bornstein, P.

A. Oohira, T. N. Wight, and P. Bornstein, “Sulfated proteoglycans synthesized by vascular endothelial cells in culture,” J. Biol. Chem.258(3), 2014–2021 (1983).
[PubMed]

Botvinick, E. L.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Brown, A. E. X.

A. E. X. Brown, R. I. Litvinov, D. E. Discher, P. K. Purohit, and J. W. Weisel, “Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water,” Science325(5941), 741–744 (2009).
[CrossRef] [PubMed]

Chien, S.

S. Chien, “Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell,” Am. J. Physiol. Heart Circ. Physiol.292(3), H1209–H1224 (2007).
[CrossRef] [PubMed]

Clough, G.

R. H. Adamson and G. Clough, “Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels,” J. Physiol.445, 473–486 (1992).
[PubMed]

Cooper, J. M.

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

Couchman, J. R.

A. Yoneda and J. R. Couchman, “Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans,” Matrix Biol.22(1), 25–33 (2003).
[CrossRef] [PubMed]

Cowin, S. C.

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A.100(13), 7988–7995 (2003).
[CrossRef] [PubMed]

Damiano, E. R.

D. R. Potter and E. R. Damiano, “The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro,” Circ. Res.102(7), 770–776 (2008).
[CrossRef] [PubMed]

M. D. Savery and E. R. Damiano, “The endothelial glycocalyx is hydrodynamically relevant in arterioles throughout the cardiac cycle,” Biophys. J.95(3), 1439–1447 (2008).
[CrossRef] [PubMed]

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng.9(1), 121–167 (2007).
[CrossRef] [PubMed]

M. L. Smith, D. S. Long, E. R. Damiano, and K. Ley, “Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo,” Biophys. J.85(1), 637–645 (2003).
[CrossRef] [PubMed]

E. R. Damiano and T. M. Stace, “A mechano-electrochemical model of radial deformation of the capillary glycocalyx,” Biophys. J.82(3), 1153–1175 (2002).
[CrossRef] [PubMed]

Davies, P. F.

P. F. Davies, “Flow-mediated endothelial mechanotransduction,” Physiol. Rev.75(3), 519–560 (1995).
[PubMed]

De Mey, J. G.

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

deCastro, M. J.

M. W. Allersma, F. Gittes, M. J. deCastro, R. J. Stewart, and C. F. Schmidt, “Two-dimensional tracking of ncd motility by back focal plane interferometry,” Biophys. J.74(2), 1074–1085 (1998).
[CrossRef] [PubMed]

Di Leonardo, R.

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

Discher, D. E.

A. E. X. Brown, R. I. Litvinov, D. E. Discher, P. K. Purohit, and J. W. Weisel, “Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water,” Science325(5941), 741–744 (2009).
[CrossRef] [PubMed]

Duling, B. R.

C. B. S. Henry and B. R. Duling, “Permeation of the luminal capillary glycocalyx is determined by hyaluronan,” Am. J. Physiol.277(2 Pt 2), H508–H514 (1999).
[PubMed]

H. Vink and B. R. Duling, “Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries,” Circ. Res.79(3), 581–589 (1996).
[PubMed]

Errill, E. W.

E. W. Errill, “Rheology of blood,” Physiol. Rev.49(4), 863–888 (1969).
[PubMed]

Estrada, L. C.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Feng, C.

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

Fung, Y. C.

Y. C. Fung, “What are the residual stresses doing in our blood vessels?” Ann. Biomed. Eng.19(3), 237–249 (1991).
[CrossRef] [PubMed]

Gittes, F.

E. J. G. Peterman, F. Gittes, and C. F. Schmidt, “Laser-induced heating in optical traps,” Biophys. J.84(2), 1308–1316 (2003).
[CrossRef] [PubMed]

M. W. Allersma, F. Gittes, M. J. deCastro, R. J. Stewart, and C. F. Schmidt, “Two-dimensional tracking of ncd motility by back focal plane interferometry,” Biophys. J.74(2), 1074–1085 (1998).
[CrossRef] [PubMed]

B. Schnurr, F. Gittes, F. C. MacKintosh, and C. F. Schmidt, “Determining microscopic viscoelasticity in flexible and semiflexible polymer networks from thermal fluctuations,” Macromolecules30(25), 7781–7792 (1997).
[CrossRef]

F. Gittes, B. Schnurr, P. D. Olmsted, F. C. MacKintosh, and C. F. Schmidt, “Microscopic viscoelasticity: Shear moduli of soft materials determined from thermal fluctuations,” Phys. Rev. Lett.79(17), 3286–3289 (1997).
[CrossRef]

Gratton, E.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Halden, Y.

Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
[CrossRef] [PubMed]

Hamaguchi, M.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Han, Y.

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech.554(-1), 217–235 (2006).
[CrossRef]

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A.100(13), 7988–7995 (2003).
[CrossRef] [PubMed]

Head, D. A.

D. Mizuno, D. A. Head, F. C. MacKintosh, and C. F. Schmidt, “Active and passive microrheology in equilibrium and nonequilibrium systems,” Macromolecules41(19), 7194–7202 (2008).
[CrossRef]

Heckenberg, N. R.

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

G. Knoner, S. Parkin, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Characterization of optically driven fluid stress fields with optical tweezers,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.72(3), 031507 (2005).
[CrossRef] [PubMed]

A. I. Bishop, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical microrheology using rotating laser-trapped particles,” Phys. Rev. Lett.92(19), 198104 (2004).
[CrossRef] [PubMed]

T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-dunlop, “Optical measurement of microscopic torques,” J. Mod. Opt.48, 405–413 (2001).

Henry, C. B. S.

C. B. S. Henry and B. R. Duling, “Permeation of the luminal capillary glycocalyx is determined by hyaluronan,” Am. J. Physiol.277(2 Pt 2), H508–H514 (1999).
[PubMed]

Hilgers, R. H.

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

Hiramatsu, O.

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

Hsu, R.

T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol.281(2), H629–H636 (2001).
[PubMed]

Imagawa, M.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Itano, N.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Janmey, P. A.

J. P. Winer, S. Oake, and P. A. Janmey, “Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation,” PLoS ONE4(7), e6382 (2009).
[CrossRef] [PubMed]

Jensen, P. V.

P. V. Jensen and L. I. Larsson, “Actin microdomains on endothelial cells: association with CD44, ERM proteins, and signaling molecules during quiescence and wound healing,” Histochem. Cell Biol.121(5), 361–369 (2004).
[CrossRef] [PubMed]

Kajita, T.

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

Kajiya, F.

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

Keen, S.

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

Kimata, K.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Kniazeva, E.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Knoner, G.

G. Knoner, S. Parkin, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Characterization of optically driven fluid stress fields with optical tweezers,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.72(3), 031507 (2005).
[CrossRef] [PubMed]

Kokenyesi, R.

R. Kokenyesi and M. Bernfield, “Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1,” J. Biol. Chem.269(16), 12304–12309 (1994).
[PubMed]

Kotlarchyk, M. A.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Kungl, A. J.

Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
[CrossRef] [PubMed]

Larsson, L. I.

P. V. Jensen and L. I. Larsson, “Actin microdomains on endothelial cells: association with CD44, ERM proteins, and signaling molecules during quiescence and wound healing,” Histochem. Cell Biol.121(5), 361–369 (2004).
[CrossRef] [PubMed]

Leach, J.

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

Lenas, P.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Ley, K.

M. L. Smith, D. S. Long, E. R. Damiano, and K. Ley, “Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo,” Biophys. J.85(1), 637–645 (2003).
[CrossRef] [PubMed]

Litvinov, R. I.

A. E. X. Brown, R. I. Litvinov, D. E. Discher, P. K. Purohit, and J. W. Weisel, “Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water,” Science325(5941), 741–744 (2009).
[CrossRef] [PubMed]

Liu, J.

R. D. Rosenberg, N. W. Shworak, J. Liu, J. J. Schwartz, and L. Zhang, “Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?” J. Clin. Invest.99(9), 2062–2070 (1997).
[CrossRef] [PubMed]

Long, D. S.

M. L. Smith, D. S. Long, E. R. Damiano, and K. Ley, “Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo,” Biophys. J.85(1), 637–645 (2003).
[CrossRef] [PubMed]

MacKintosh, F. C.

D. Mizuno, D. A. Head, F. C. MacKintosh, and C. F. Schmidt, “Active and passive microrheology in equilibrium and nonequilibrium systems,” Macromolecules41(19), 7194–7202 (2008).
[CrossRef]

F. Gittes, B. Schnurr, P. D. Olmsted, F. C. MacKintosh, and C. F. Schmidt, “Microscopic viscoelasticity: Shear moduli of soft materials determined from thermal fluctuations,” Phys. Rev. Lett.79(17), 3286–3289 (1997).
[CrossRef]

B. Schnurr, F. Gittes, F. C. MacKintosh, and C. F. Schmidt, “Determining microscopic viscoelasticity in flexible and semiflexible polymer networks from thermal fluctuations,” Macromolecules30(25), 7781–7792 (1997).
[CrossRef]

McDonald, J. A.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Megens, R. T.

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

Miyauchi, S.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Mizuno, D.

N. Nijenhuis, D. Mizuno, J. A. Spaan, and C. F. Schmidt, “Viscoelastic response of a model endothelial glycocalyx,” Phys. Biol.6(2), 025014 (2009).
[CrossRef] [PubMed]

N. Nijenhuis, D. Mizuno, C. F. Schmidt, H. Vink, and J. A. E. Spaan, “Microrheology of hyaluronan solutions: implications for the endothelial glycocalyx,” Biomacromolecules9(9), 2390–2398 (2008).
[CrossRef] [PubMed]

D. Mizuno, D. A. Head, F. C. MacKintosh, and C. F. Schmidt, “Active and passive microrheology in equilibrium and nonequilibrium systems,” Macromolecules41(19), 7194–7202 (2008).
[CrossRef]

Mochizuki, S.

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

Mushfique, H.

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

Nieminen, T. A.

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

A. I. Bishop, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical microrheology using rotating laser-trapped particles,” Phys. Rev. Lett.92(19), 198104 (2004).
[CrossRef] [PubMed]

T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-dunlop, “Optical measurement of microscopic torques,” J. Mod. Opt.48, 405–413 (2001).

Nijenhuis, N.

N. Nijenhuis, D. Mizuno, J. A. Spaan, and C. F. Schmidt, “Viscoelastic response of a model endothelial glycocalyx,” Phys. Biol.6(2), 025014 (2009).
[CrossRef] [PubMed]

N. Nijenhuis, D. Mizuno, C. F. Schmidt, H. Vink, and J. A. E. Spaan, “Microrheology of hyaluronan solutions: implications for the endothelial glycocalyx,” Biomacromolecules9(9), 2390–2398 (2008).
[CrossRef] [PubMed]

Oake, S.

J. P. Winer, S. Oake, and P. A. Janmey, “Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation,” PLoS ONE4(7), e6382 (2009).
[CrossRef] [PubMed]

Ohnuki, Y.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Olmsted, P. D.

F. Gittes, B. Schnurr, P. D. Olmsted, F. C. MacKintosh, and C. F. Schmidt, “Microscopic viscoelasticity: Shear moduli of soft materials determined from thermal fluctuations,” Phys. Rev. Lett.79(17), 3286–3289 (1997).
[CrossRef]

Oohira, A.

A. Oohira, T. N. Wight, and P. Bornstein, “Sulfated proteoglycans synthesized by vascular endothelial cells in culture,” J. Biol. Chem.258(3), 2014–2021 (1983).
[PubMed]

oude Egbrink, M. G.

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

oude Egbrink, M. G. A.

S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch.454(3), 345–359 (2007).
[CrossRef] [PubMed]

Padgett, M. J.

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

Pahakis, M. Y.

J. M. Tarbell and M. Y. Pahakis, “Mechanotransduction and the glycocalyx,” J. Intern. Med.259(4), 339–350 (2006).
[CrossRef] [PubMed]

Parkin, S.

G. Knoner, S. Parkin, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Characterization of optically driven fluid stress fields with optical tweezers,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.72(3), 031507 (2005).
[CrossRef] [PubMed]

Parkin, S. J.

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

Persson, M.

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

Peterman, E. J. G.

E. J. G. Peterman, F. Gittes, and C. F. Schmidt, “Laser-induced heating in optical traps,” Biophys. J.84(2), 1308–1316 (2003).
[CrossRef] [PubMed]

Potter, D. R.

D. R. Potter and E. R. Damiano, “The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro,” Circ. Res.102(7), 770–776 (2008).
[CrossRef] [PubMed]

Pries, A. R.

T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol.281(2), H629–H636 (2001).
[PubMed]

Purohit, P. K.

A. E. X. Brown, R. I. Litvinov, D. E. Discher, P. K. Purohit, and J. W. Weisel, “Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water,” Science325(5941), 741–744 (2009).
[CrossRef] [PubMed]

Putnam, A. J.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Reitsma, S.

S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch.454(3), 345–359 (2007).
[CrossRef] [PubMed]

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

Rek, A.

Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
[CrossRef] [PubMed]

Rosenberg, R. D.

R. D. Rosenberg, N. W. Shworak, J. Liu, J. J. Schwartz, and L. Zhang, “Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?” J. Clin. Invest.99(9), 2062–2070 (1997).
[CrossRef] [PubMed]

Rubinsztein-Dunlop, H.

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

G. Knoner, S. Parkin, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Characterization of optically driven fluid stress fields with optical tweezers,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.72(3), 031507 (2005).
[CrossRef] [PubMed]

A. I. Bishop, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical microrheology using rotating laser-trapped particles,” Phys. Rev. Lett.92(19), 198104 (2004).
[CrossRef] [PubMed]

T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-dunlop, “Optical measurement of microscopic torques,” J. Mod. Opt.48, 405–413 (2001).

Ruocco, G.

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

Savery, M. D.

M. D. Savery and E. R. Damiano, “The endothelial glycocalyx is hydrodynamically relevant in arterioles throughout the cardiac cycle,” Biophys. J.95(3), 1439–1447 (2008).
[CrossRef] [PubMed]

Sawai, T.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Schiffers, P. H.

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

Schmidt, C. F.

N. Nijenhuis, D. Mizuno, J. A. Spaan, and C. F. Schmidt, “Viscoelastic response of a model endothelial glycocalyx,” Phys. Biol.6(2), 025014 (2009).
[CrossRef] [PubMed]

N. Nijenhuis, D. Mizuno, C. F. Schmidt, H. Vink, and J. A. E. Spaan, “Microrheology of hyaluronan solutions: implications for the endothelial glycocalyx,” Biomacromolecules9(9), 2390–2398 (2008).
[CrossRef] [PubMed]

D. Mizuno, D. A. Head, F. C. MacKintosh, and C. F. Schmidt, “Active and passive microrheology in equilibrium and nonequilibrium systems,” Macromolecules41(19), 7194–7202 (2008).
[CrossRef]

E. J. G. Peterman, F. Gittes, and C. F. Schmidt, “Laser-induced heating in optical traps,” Biophys. J.84(2), 1308–1316 (2003).
[CrossRef] [PubMed]

M. W. Allersma, F. Gittes, M. J. deCastro, R. J. Stewart, and C. F. Schmidt, “Two-dimensional tracking of ncd motility by back focal plane interferometry,” Biophys. J.74(2), 1074–1085 (1998).
[CrossRef] [PubMed]

B. Schnurr, F. Gittes, F. C. MacKintosh, and C. F. Schmidt, “Determining microscopic viscoelasticity in flexible and semiflexible polymer networks from thermal fluctuations,” Macromolecules30(25), 7781–7792 (1997).
[CrossRef]

F. Gittes, B. Schnurr, P. D. Olmsted, F. C. MacKintosh, and C. F. Schmidt, “Microscopic viscoelasticity: Shear moduli of soft materials determined from thermal fluctuations,” Phys. Rev. Lett.79(17), 3286–3289 (1997).
[CrossRef]

Schnurr, B.

F. Gittes, B. Schnurr, P. D. Olmsted, F. C. MacKintosh, and C. F. Schmidt, “Microscopic viscoelasticity: Shear moduli of soft materials determined from thermal fluctuations,” Phys. Rev. Lett.79(17), 3286–3289 (1997).
[CrossRef]

B. Schnurr, F. Gittes, F. C. MacKintosh, and C. F. Schmidt, “Determining microscopic viscoelasticity in flexible and semiflexible polymer networks from thermal fluctuations,” Macromolecules30(25), 7781–7792 (1997).
[CrossRef]

Schwartz, J. J.

R. D. Rosenberg, N. W. Shworak, J. Liu, J. J. Schwartz, and L. Zhang, “Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?” J. Clin. Invest.99(9), 2062–2070 (1997).
[CrossRef] [PubMed]

Secomb, T. W.

T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol.281(2), H629–H636 (2001).
[PubMed]

Shigeto, F.

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

Shinomura, T.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Shreim, S. G.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Shworak, N. W.

R. D. Rosenberg, N. W. Shworak, J. Liu, J. J. Schwartz, and L. Zhang, “Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?” J. Clin. Invest.99(9), 2062–2070 (1997).
[CrossRef] [PubMed]

Singh, R.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Slaaf, D. W.

S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch.454(3), 345–359 (2007).
[CrossRef] [PubMed]

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

Smith, M. L.

M. L. Smith, D. S. Long, E. R. Damiano, and K. Ley, “Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo,” Biophys. J.85(1), 637–645 (2003).
[CrossRef] [PubMed]

Spaan, J. A.

N. Nijenhuis, D. Mizuno, J. A. Spaan, and C. F. Schmidt, “Viscoelastic response of a model endothelial glycocalyx,” Phys. Biol.6(2), 025014 (2009).
[CrossRef] [PubMed]

Spaan, J. A. E.

N. Nijenhuis, D. Mizuno, C. F. Schmidt, H. Vink, and J. A. E. Spaan, “Microrheology of hyaluronan solutions: implications for the endothelial glycocalyx,” Biomacromolecules9(9), 2390–2398 (2008).
[CrossRef] [PubMed]

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech.554(-1), 217–235 (2006).
[CrossRef]

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

Spicer, A. P.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Spray, D. C.

M. M. Thi, J. M. Tarbell, S. Weinbaum, and D. C. Spray, “The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a “bumper-car” model,” Proc. Natl. Acad. Sci. U.S.A.101(47), 16483–16488 (2004).
[CrossRef] [PubMed]

Stace, T. M.

E. R. Damiano and T. M. Stace, “A mechano-electrochemical model of radial deformation of the capillary glycocalyx,” Biophys. J.82(3), 1153–1175 (2002).
[CrossRef] [PubMed]

Stewart, R. J.

M. W. Allersma, F. Gittes, M. J. deCastro, R. J. Stewart, and C. F. Schmidt, “Two-dimensional tracking of ncd motility by back focal plane interferometry,” Biophys. J.74(2), 1074–1085 (1998).
[CrossRef] [PubMed]

Svoboda, K.

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct.23(1), 247–285 (1994).
[CrossRef] [PubMed]

Szilak, L.

Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
[CrossRef] [PubMed]

Tarbell, J. M.

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng.9(1), 121–167 (2007).
[CrossRef] [PubMed]

J. M. Tarbell and M. Y. Pahakis, “Mechanotransduction and the glycocalyx,” J. Intern. Med.259(4), 339–350 (2006).
[CrossRef] [PubMed]

M. M. Thi, J. M. Tarbell, S. Weinbaum, and D. C. Spray, “The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a “bumper-car” model,” Proc. Natl. Acad. Sci. U.S.A.101(47), 16483–16488 (2004).
[CrossRef] [PubMed]

Thi, M. M.

M. M. Thi, J. M. Tarbell, S. Weinbaum, and D. C. Spray, “The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a “bumper-car” model,” Proc. Natl. Acad. Sci. U.S.A.101(47), 16483–16488 (2004).
[CrossRef] [PubMed]

Valdevit, L.

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

van Zandvoort, M. A.

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

van Zandvoort, M. A. M. J.

S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch.454(3), 345–359 (2007).
[CrossRef] [PubMed]

Vink, H.

N. Nijenhuis, D. Mizuno, C. F. Schmidt, H. Vink, and J. A. E. Spaan, “Microrheology of hyaluronan solutions: implications for the endothelial glycocalyx,” Biomacromolecules9(9), 2390–2398 (2008).
[CrossRef] [PubMed]

S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch.454(3), 345–359 (2007).
[CrossRef] [PubMed]

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech.554(-1), 217–235 (2006).
[CrossRef]

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A.100(13), 7988–7995 (2003).
[CrossRef] [PubMed]

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

H. Vink and B. R. Duling, “Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries,” Circ. Res.79(3), 581–589 (1996).
[PubMed]

Vogel, R.

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

Wabnig, A.

Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
[CrossRef] [PubMed]

Weinbaum, S.

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng.9(1), 121–167 (2007).
[CrossRef] [PubMed]

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech.554(-1), 217–235 (2006).
[CrossRef]

M. M. Thi, J. M. Tarbell, S. Weinbaum, and D. C. Spray, “The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a “bumper-car” model,” Proc. Natl. Acad. Sci. U.S.A.101(47), 16483–16488 (2004).
[CrossRef] [PubMed]

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A.100(13), 7988–7995 (2003).
[CrossRef] [PubMed]

Weisel, J. W.

A. E. X. Brown, R. I. Litvinov, D. E. Discher, P. K. Purohit, and J. W. Weisel, “Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water,” Science325(5941), 741–744 (2009).
[CrossRef] [PubMed]

Wight, T. N.

A. Oohira, T. N. Wight, and P. Bornstein, “Sulfated proteoglycans synthesized by vascular endothelial cells in culture,” J. Biol. Chem.258(3), 2014–2021 (1983).
[PubMed]

Winer, J. P.

J. P. Winer, S. Oake, and P. A. Janmey, “Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation,” PLoS ONE4(7), e6382 (2009).
[CrossRef] [PubMed]

Wood, B.

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

Yamada, Y.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Yoneda, A.

A. Yoneda and J. R. Couchman, “Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans,” Matrix Biol.22(1), 25–33 (2003).
[CrossRef] [PubMed]

Yoshida, M.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Yoshida, Y.

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

Zhang, L.

R. D. Rosenberg, N. W. Shworak, J. Liu, J. J. Schwartz, and L. Zhang, “Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?” J. Clin. Invest.99(9), 2062–2070 (1997).
[CrossRef] [PubMed]

Zhang, X.

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A.100(13), 7988–7995 (2003).
[CrossRef] [PubMed]

Am. J. Physiol. (1)

C. B. S. Henry and B. R. Duling, “Permeation of the luminal capillary glycocalyx is determined by hyaluronan,” Am. J. Physiol.277(2 Pt 2), H508–H514 (1999).
[PubMed]

Am. J. Physiol. Heart Circ. Physiol. (3)

S. Chien, “Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell,” Am. J. Physiol. Heart Circ. Physiol.292(3), H1209–H1224 (2007).
[CrossRef] [PubMed]

T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol.281(2), H629–H636 (2001).
[PubMed]

S. Mochizuki, H. Vink, O. Hiramatsu, T. Kajita, F. Shigeto, J. A. E. Spaan, and F. Kajiya, “Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release,” Am. J. Physiol. Heart Circ. Physiol.285(2), H722–H726 (2003).
[PubMed]

Ann. Biomed. Eng. (1)

Y. C. Fung, “What are the residual stresses doing in our blood vessels?” Ann. Biomed. Eng.19(3), 237–249 (1991).
[CrossRef] [PubMed]

Annu. Rev. Biomed. Eng. (1)

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng.9(1), 121–167 (2007).
[CrossRef] [PubMed]

Annu. Rev. Biophys. Biomol. Struct. (1)

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct.23(1), 247–285 (1994).
[CrossRef] [PubMed]

Biochem. J. (1)

Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A. J. Kungl, “Interleukin-8 binds to syndecan-2 on human endothelial cells,” Biochem. J.377(2), 533–538 (2004).
[CrossRef] [PubMed]

Biomacromolecules (1)

N. Nijenhuis, D. Mizuno, C. F. Schmidt, H. Vink, and J. A. E. Spaan, “Microrheology of hyaluronan solutions: implications for the endothelial glycocalyx,” Biomacromolecules9(9), 2390–2398 (2008).
[CrossRef] [PubMed]

Biophys. J. (5)

M. D. Savery and E. R. Damiano, “The endothelial glycocalyx is hydrodynamically relevant in arterioles throughout the cardiac cycle,” Biophys. J.95(3), 1439–1447 (2008).
[CrossRef] [PubMed]

M. L. Smith, D. S. Long, E. R. Damiano, and K. Ley, “Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo,” Biophys. J.85(1), 637–645 (2003).
[CrossRef] [PubMed]

E. J. G. Peterman, F. Gittes, and C. F. Schmidt, “Laser-induced heating in optical traps,” Biophys. J.84(2), 1308–1316 (2003).
[CrossRef] [PubMed]

M. W. Allersma, F. Gittes, M. J. deCastro, R. J. Stewart, and C. F. Schmidt, “Two-dimensional tracking of ncd motility by back focal plane interferometry,” Biophys. J.74(2), 1074–1085 (1998).
[CrossRef] [PubMed]

E. R. Damiano and T. M. Stace, “A mechano-electrochemical model of radial deformation of the capillary glycocalyx,” Biophys. J.82(3), 1153–1175 (2002).
[CrossRef] [PubMed]

Circ. Res. (2)

D. R. Potter and E. R. Damiano, “The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro,” Circ. Res.102(7), 770–776 (2008).
[CrossRef] [PubMed]

H. Vink and B. R. Duling, “Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries,” Circ. Res.79(3), 581–589 (1996).
[PubMed]

Histochem. Cell Biol. (1)

P. V. Jensen and L. I. Larsson, “Actin microdomains on endothelial cells: association with CD44, ERM proteins, and signaling molecules during quiescence and wound healing,” Histochem. Cell Biol.121(5), 361–369 (2004).
[CrossRef] [PubMed]

J. Biol. Chem. (3)

A. Oohira, T. N. Wight, and P. Bornstein, “Sulfated proteoglycans synthesized by vascular endothelial cells in culture,” J. Biol. Chem.258(3), 2014–2021 (1983).
[PubMed]

R. Kokenyesi and M. Bernfield, “Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1,” J. Biol. Chem.269(16), 12304–12309 (1994).
[PubMed]

N. Itano, T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata, “Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties,” J. Biol. Chem.274(35), 25085–25092 (1999).
[CrossRef] [PubMed]

J. Clin. Invest. (1)

R. D. Rosenberg, N. W. Shworak, J. Liu, J. J. Schwartz, and L. Zhang, “Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?” J. Clin. Invest.99(9), 2062–2070 (1997).
[CrossRef] [PubMed]

J. Fluid Mech. (1)

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech.554(-1), 217–235 (2006).
[CrossRef]

J. Intern. Med. (1)

J. M. Tarbell and M. Y. Pahakis, “Mechanotransduction and the glycocalyx,” J. Intern. Med.259(4), 339–350 (2006).
[CrossRef] [PubMed]

J. Mod. Opt. (1)

T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-dunlop, “Optical measurement of microscopic torques,” J. Mod. Opt.48, 405–413 (2001).

J. Physiol. (1)

R. H. Adamson and G. Clough, “Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels,” J. Physiol.445, 473–486 (1992).
[PubMed]

J. Vasc. Res. (1)

R. T. Megens, S. Reitsma, P. H. Schiffers, R. H. Hilgers, J. G. De Mey, D. W. Slaaf, M. G. oude Egbrink, and M. A. van Zandvoort, “Two-photon microscopy of vital murine elastic and muscular arteries,” J. Vasc. Res.44(2), 87–98 (2007).
[CrossRef] [PubMed]

Langmuir (1)

R. Vogel, M. Persson, C. Feng, S. J. Parkin, T. A. Nieminen, B. Wood, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Synthesis and surface modification of birefringent vaterite microspheres,” Langmuir25(19), 11672–11679 (2009).
[CrossRef] [PubMed]

Macromolecules (2)

D. Mizuno, D. A. Head, F. C. MacKintosh, and C. F. Schmidt, “Active and passive microrheology in equilibrium and nonequilibrium systems,” Macromolecules41(19), 7194–7202 (2008).
[CrossRef]

B. Schnurr, F. Gittes, F. C. MacKintosh, and C. F. Schmidt, “Determining microscopic viscoelasticity in flexible and semiflexible polymer networks from thermal fluctuations,” Macromolecules30(25), 7781–7792 (1997).
[CrossRef]

Matrix Biol. (1)

A. Yoneda and J. R. Couchman, “Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans,” Matrix Biol.22(1), 25–33 (2003).
[CrossRef] [PubMed]

Pflugers Arch. (1)

S. Reitsma, D. W. Slaaf, H. Vink, M. A. M. J. van Zandvoort, and M. G. A. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch.454(3), 345–359 (2007).
[CrossRef] [PubMed]

Phys. Biol. (1)

N. Nijenhuis, D. Mizuno, J. A. Spaan, and C. F. Schmidt, “Viscoelastic response of a model endothelial glycocalyx,” Phys. Biol.6(2), 025014 (2009).
[CrossRef] [PubMed]

Phys. Rev. E Stat. Nonlin. Soft Matter Phys. (2)

G. Knoner, S. Parkin, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Characterization of optically driven fluid stress fields with optical tweezers,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.72(3), 031507 (2005).
[CrossRef] [PubMed]

J. Leach, H. Mushfique, S. Keen, R. Di Leonardo, G. Ruocco, J. M. Cooper, and M. J. Padgett, “Comparison of Faxén’s correction for a microsphere translating or rotating near a surface,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.79(2), 026301 (2009).
[CrossRef] [PubMed]

Phys. Rev. Lett. (2)

F. Gittes, B. Schnurr, P. D. Olmsted, F. C. MacKintosh, and C. F. Schmidt, “Microscopic viscoelasticity: Shear moduli of soft materials determined from thermal fluctuations,” Phys. Rev. Lett.79(17), 3286–3289 (1997).
[CrossRef]

A. I. Bishop, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical microrheology using rotating laser-trapped particles,” Phys. Rev. Lett.92(19), 198104 (2004).
[CrossRef] [PubMed]

Physiol. Rev. (2)

P. F. Davies, “Flow-mediated endothelial mechanotransduction,” Physiol. Rev.75(3), 519–560 (1995).
[PubMed]

E. W. Errill, “Rheology of blood,” Physiol. Rev.49(4), 863–888 (1969).
[PubMed]

PLoS ONE (2)

J. P. Winer, S. Oake, and P. A. Janmey, “Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation,” PLoS ONE4(7), e6382 (2009).
[CrossRef] [PubMed]

M. A. Kotlarchyk, S. G. Shreim, M. B. Alvarez-Elizondo, L. C. Estrada, R. Singh, L. Valdevit, E. Kniazeva, E. Gratton, A. J. Putnam, and E. L. Botvinick, “Concentration independent modulation of local micromechanics in a fibrin gel,” PLoS ONE6(5), e20201 (2011).
[CrossRef] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (2)

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A.100(13), 7988–7995 (2003).
[CrossRef] [PubMed]

M. M. Thi, J. M. Tarbell, S. Weinbaum, and D. C. Spray, “The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a “bumper-car” model,” Proc. Natl. Acad. Sci. U.S.A.101(47), 16483–16488 (2004).
[CrossRef] [PubMed]

Science (1)

A. E. X. Brown, R. I. Litvinov, D. E. Discher, P. K. Purohit, and J. W. Weisel, “Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water,” Science325(5941), 741–744 (2009).
[CrossRef] [PubMed]

Other (1)

S. J. W. Parkin, G. G. Knoener, T. A. Nieminen, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “A constant torque micro-viscometer,” in Nanomanipulation with Light (SPIE, San Jose, CA, USA, 2005), pp. 59–65.

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Figures (3)

Fig. 1
Fig. 1

Schematic of experimental approach. Laser trap stiffness, κ trap , is first measured by trapping a particle of known diameter in water (A), and then determining the corner frequency from a Lorentzian fit to the power spectral density of particle fluctuations (B). κ trap is related to the corner frequency by Eq. (2). The procedure is repeated in the center of an excised vessel slice (C), where the corner frequency of the power spectral density (D) is used to determine the viscosity, η 0 of the culture media by Eq. (2). The apparent viscosity, η i as a function of gap thickness is determined by optically measuring the rotation rate of a vaterite particle rotating under constant optical torque at various distances from the vessel wall (E). For each gap thickness, η i is calculated by measuring vaterite particle rotation rate and Eq. (5) (F).

Fig. 2
Fig. 2

Validating VMV near a glass boundary and linearity of our culture media. (A) A 4.5 µm vaterite microsphere rotating at 6.4 Hz in water at room temperature near a solid boundary comprising a glass wall. The gap thickness is measured as shown. Scale bar is 10 µm (B) Experimental data and fit of relative rotation rates as a function of gap thickness. The residual of fit is 0.0791, mostly due the point closest to the boundary. Note the fine scale on the vertical axis. (C) PMR measurement in EGL collapsing media. (D) PMR measurement in EGL preserving media. PMR confirms linearity of the culture media across observed frequencies.

Fig. 3
Fig. 3

VMV of the EGL in an excised porcine femoral artery. (A) A 4.7 µm vaterite microsphere rotating at 6.0 Hz in EGL preserving media near the endothelium of an excised vessel slice. The gap thickness is measured as shown. Scale bar is 10 µm. (B) Apparent viscosity, η i measured in an excised vessel slice cultured in EGL preserving media (C) Apparent viscosity, η i measured in an excised vessel slice cultured in EGL collapsing media. (D) Representative data for vessel experiments in EGL preserving and collapsing media, as well as the solid glass boundary experiment in water highlight role of the EGL in modulating local apparent viscosity.

Equations (5)

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S( f )= S 0 f c 2 + f 2
f c = κ trap 2πγ
η 0 = ΔσP 8π r 3 ω Ω 0
η i η 0 = ΔσP 8π r 3 ω Ω i ΔσP 8π r 3 ω Ω 0 = Ω 0 Ω i .
η i = Ω 0 Ω i η 0

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