Donate Help Contact The AHA Sign In Home
American Heart Association
Circulation Research
Search: search_blue_button Advanced Search
Circulation Research. 1996;79:581-589

This Article
Right arrow Full Text
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Vink, H.
Right arrow Articles by Duling, B. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Vink, H.
Right arrow Articles by Duling, B. R.
(Circulation Research. 1996;79:581-589.)
© 1996 American Heart Association, Inc.


Articles

Identification of Distinct Luminal Domains for Macromolecules, Erythrocytes, and Leukocytes Within Mammalian Capillaries

Hans Vink, Brian R. Duling

the Department of Molecular Physiology and Biological Physics, University of Virginia, Health Sciences Center, Charlottesville.

Correspondence to Brian R. Duling, PhD, Department of Molecular Physiology and Biological Physics, University of Virginia, Health Sciences Center, Jordan Hall, Box 449, Charlottesville, VA 22908. E-mail brd@dayhoff.med.virginia.edu.

A thick endothelial surface coat consisting of the glycocalyx and associated plasma proteins has been hypothesized to reduce functional capillary volume available for flowing plasma macromolecules and blood cells. The purpose of this study was to compare anatomic and functional capillary diameters available for macromolecules, RBCs, and WBCs in hamster cremaster muscle capillaries. Bright-field and fluorescence microscopy provided similar estimates (mean±SE) of the anatomic capillary diameter: 5.1±0.1 µm (bright field, 39 capillaries in 10 animals) and 5.1±0.2 µm (membrane dye PKH26, 18 capillaries in 2 animals). Estimates of functional diameters were obtained by measuring the width of RBCs and WBCs and the intracapillary distribution of systemically injected fluorescein isothiocyanate (FITC)–dextran 70. WBCs (5.1±0.2 µm) fully occupied the anatomic capillary cross section. In contrast, the widths of RBCs (3.9±0.2 µm, 21 capillaries in 8 animals) and FITC-dextran (4.3±0.2 µm, 21 capillaries in 8 animals) were significantly smaller than the anatomic capillary diameter. Continuous (1- to 5-minute) excitation of fluorochromes in the capillary lumen (light-dye treatment) increased the width of RBCs passing the treated site from 3.6±0.3 to 4.4±0.3 µm (6 capillaries in 4 animals) and the width of the FITC-dextran column from 4.1±0.2 to 4.6±0.3 µm (10 capillaries in 7 animals). Furthermore, light-dye treatment increased capillary tube hematocrit by 60% in 40-µm-long capillary segments compared with untreated sites in the same capillaries. It is concluded that the wall of skeletal muscle capillaries is decorated with a 0.4- to 0.5-µm-thick endothelial surface coat, which may represent the true active interface between blood and the capillary wall.


Key Words: hamster cremaster muscle • functional capillary diameter • anatomic capillary diameter • bright-field microscopy • fluorescence microscopy




This article has been cited by other articles:


Home page
Biophys. JHome page
M. D. Savery and E. R. Damiano
The Endothelial Glycocalyx is Hydrodynamically Relevant in Arterioles throughout the Cardiac Cycle
Biophys. J., August 1, 2008; 95(3): 1439 - 1447.
[Abstract] [Full Text] [PDF]


Home page
Nephrol Dial TransplantHome page
M. F. Flessner
Distributed model of peritoneal transport: implications of the endothelial glycocalyx
Nephrol. Dial. Transplant., July 1, 2008; 23(7): 2142 - 2146.
[Full Text] [PDF]


Home page
QJMHome page
M.I.M. Noble, A.J. Drake-Holland, and H. Vink
Hypothesis: arterial glycocalyx dysfunction is the first step in the atherothrombotic process
QJM, July 1, 2008; 101(7): 513 - 518.
[Abstract] [Full Text] [PDF]


Home page
J. Physiol.Home page
J. W. G. E. VanTeeffelen, A. A. Constantinescu, J. Brands, J. A. E. Spaan, and H. Vink
Bradykinin- and sodium nitroprusside-induced increases in capillary tube haematocrit in mouse cremaster muscle are associated with impaired glycocalyx barrier properties
J. Physiol., July 1, 2008; 586(13): 3207 - 3218.
[Abstract] [Full Text] [PDF]


Home page
Circ. Res.Home page
D. R. Potter and E. R. Damiano
The Hydrodynamically Relevant Endothelial Cell Glycocalyx Observed In Vivo Is Absent In Vitro
Circ. Res., April 11, 2008; 102(7): 770 - 776.
[Abstract] [Full Text] [PDF]


Home page
Physiol. Rev.Home page
B. Haraldsson, J. Nystrom, and W. M. Deen
Properties of the Glomerular Barrier and Mechanisms of Proteinuria
Physiol Rev, April 1, 2008; 88(2): 451 - 487.
[Abstract] [Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
M. Nieuwdorp, M. C. Meuwese, H. L. Mooij, C. Ince, L. N. Broekhuizen, J. J. P. Kastelein, E. S. G. Stroes, and H. Vink
Measuring endothelial glycocalyx dimensions in humans: a potential novel tool to monitor vascular vulnerability
J Appl Physiol, March 1, 2008; 104(3): 845 - 852.
[Abstract] [Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
J. Van Teeffelen, H. Vink, B. T. Ameredes, A. M. Jones, S. Egginton, L. F. Ferreira, G. W. Schmid-Schoenbein, W. L. Murfee, S. S. Segal, K. Tyml, et al.

J Appl Physiol, March 1, 2008; 104(3): 895 - 899.
[Full Text] [PDF]


Home page
J. Am. Soc. Nephrol.Home page
A. Singh, S. C. Satchell, C. R. Neal, E. A. McKenzie, J. E. Tooke, and P. W. Mathieson
Glomerular Endothelial Glycocalyx Constitutes a Barrier to Protein Permeability
J. Am. Soc. Nephrol., November 1, 2007; 18(11): 2885 - 2893.
[Abstract] [Full Text] [PDF]


Home page
CirculationHome page
M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, et al.
Shedding of the Endothelial Glycocalyx in Patients Undergoing Major Vascular Surgery With Global and Regional Ischemia
Circulation, October 23, 2007; 116(17): 1896 - 1906.
[Abstract] [Full Text] [PDF]


Home page
J. Exp. Biol.Home page
P. Koldkjaer and M. Berenbrink
In vivo red blood cell sickling and mechanism of recovery in whiting, Merlangius merlangus
J. Exp. Biol., October 1, 2007; 210(19): 3451 - 3460.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
S. Kim, R. L. Kong, A. S. Popel, M. Intaglietta, and P. C. Johnson
Temporal and spatial variations of cell-free layer width in arterioles
Am J Physiol Heart Circ Physiol, September 1, 2007; 293(3): H1526 - H1535.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
A. P. Stevens, V. Hlady, and R. O. Dull
Fluorescence correlation spectroscopy can probe albumin dynamics inside lung endothelial glycocalyx
Am J Physiol Lung Cell Mol Physiol, August 1, 2007; 293(2): L328 - L335.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
Y. Yao, A. Rabodzey, and C. F. Dewey Jr.
Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress
Am J Physiol Heart Circ Physiol, August 1, 2007; 293(2): H1023 - H1030.
[Abstract] [Full Text] [PDF]


Home page
HypertensionHome page
J. W.G.E. VanTeeffelen, J. Brands, C. Jansen, J. A.E. Spaan, and H. Vink
Heparin Impairs Glycocalyx Barrier Properties and Attenuates Shear Dependent Vasodilation in Mice
Hypertension, July 1, 2007; 50(1): 261 - 267.
[Abstract] [Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
P. Cabrales, B. Y. S. Vazquez, A. G. Tsai, and M. Intaglietta
Microvascular and capillary perfusion following glycocalyx degradation
J Appl Physiol, June 1, 2007; 102(6): 2251 - 2259.
[Abstract] [Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
M. Jacob, P. Conzen, U. Finsterer, A. Krafft, B. F. Becker, and M. Rehm
Technical and physiological background of plasma volume measurement with indocyanine green: a clarification of misunderstandings
J Appl Physiol, March 1, 2007; 102(3): 1235 - 1242.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
S. Bertuglia, F. M. Veronese, and G. Pasut
Polyethylene glycol and a novel developed polyethylene glycol-nitric oxide normalize arteriolar response and oxidative stress in ischemia-reperfusion
Am J Physiol Heart Circ Physiol, October 1, 2006; 291(4): H1536 - H1544.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
B. van den Berg and H. Vink
Glycocalyx perturbation: cause or consequence of damage to the vasculature?
Am J Physiol Heart Circ Physiol, June 1, 2006; 290(6): H2174 - H2175.
[Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
I. Rubio-Gayosso, S. H. Platts, and B. R. Duling
Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury
Am J Physiol Heart Circ Physiol, June 1, 2006; 290(6): H2247 - H2256.
[Abstract] [Full Text] [PDF]


Home page
J. Physiol.Home page
R. Kelly, T. Ruane-O'Hora, M. I. M. Noble, A. J. Drake-Holland, and H. M. Snow
Differential inhibition by hyperglycaemia of shear stress- but not acetylcholine-mediated dilatation in the iliac artery of the anaesthetized pig
J. Physiol., May 15, 2006; 573(1): 133 - 145.
[Abstract] [Full Text] [PDF]


Home page
DiabetesHome page
M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A.E. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B.L. Hoekstra, et al.
Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes.
Diabetes, April 1, 2006; 55(4): 1127 - 1132.
[Abstract] [Full Text] [PDF]


Home page
DiabetesHome page
M. Nieuwdorp, T. W. van Haeften, M. C.L.G. Gouverneur, H. L. Mooij, M. H.P. van Lieshout, M. Levi, J. C.M. Meijers, F. Holleman, J. B.L. Hoekstra, H. Vink, et al.
Loss of Endothelial Glycocalyx During Acute Hyperglycemia Coincides With Endothelial Dysfunction and Coagulation Activation In Vivo
Diabetes, February 1, 2006; 55(2): 480 - 486.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
B. M. van den Berg, J. A. E. Spaan, T. M. Rolf, and H. Vink
Atherogenic region and diet diminish glycocalyx dimension and increase intima-to-media ratios at murine carotid artery bifurcation
Am J Physiol Heart Circ Physiol, February 1, 2006; 290(2): H915 - H920.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
X. Zhang, F.-R. Curry, and S. Weinbaum
Mechanism of osmotic flow in a periodic fiber array
Am J Physiol Heart Circ Physiol, February 1, 2006; 290(2): H844 - H852.
[Abstract] [Full Text] [PDF]


Home page
Physiol. Rev.Home page
D. Mehta and A. B. Malik
Signaling Mechanisms Regulating Endothelial Permeability
Physiol Rev, January 1, 2006; 86(1): 279 - 367.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Renal Physiol.Home page
M. Jeansson and B. Haraldsson
Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier
Am J Physiol Renal Physiol, January 1, 2006; 290(1): F111 - F116.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
M. Gouverneur, J. A. E. Spaan, H. Pannekoek, R. D. Fontijn, and H. Vink
Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx
Am J Physiol Heart Circ Physiol, January 1, 2006; 290(1): H458 - H452.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
P. M. A. van Haaren, E. VanBavel, H. Vink, and J. A. E. Spaan
Charge modification of the endothelial surface layer modulates the permeability barrier of isolated rat mesenteric small arteries
Am J Physiol Heart Circ Physiol, December 1, 2005; 289(6): H2503 - H2507.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
J. W. G. E. VanTeeffelen, S. Dekker, D. S. Fokkema, M. Siebes, H. Vink, and J. A. E. Spaan
Hyaluronidase treatment of coronary glycocalyx increases reactive hyperemia but not adenosine hyperemia in dog hearts
Am J Physiol Heart Circ Physiol, December 1, 2005; 289(6): H2508 - H2513.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
A. R. Pries and T. W. Secomb
Microvascular blood viscosity in vivo and the endothelial surface layer
Am J Physiol Heart Circ Physiol, December 1, 2005; 289(6): H2657 - H2664.
[Abstract] [Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
C. J. Zuurbier, C. Demirci, A. Koeman, H. Vink, and C. Ince
Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells
J Appl Physiol, October 1, 2005; 99(4): 1471 - 1476.
[Abstract] [Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
Y. Kano, D. J. Padilla, B. J. Behnke, K. S. Hageman, T. I. Musch, and D. C. Poole
Effects of eccentric exercise on microcirculation and microvascular oxygen pressures in rat spinotrapezius muscle
J Appl Physiol, October 1, 2005; 99(4): 1516 - 1522.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
D. R. Hyduke and J. C. Liao
Analysis of nitric oxide donor effectiveness in resistance vessels
Am J Physiol Heart Circ Physiol, May 1, 2005; 288(5): H2390 - H2399.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Renal Physiol.Home page
A. Bjornson, J. Moses, A. Ingemansson, B. Haraldsson, and J. Sorensson
Primary human glomerular endothelial cells produce proteoglycans, and puromycin affects their posttranslational modification
Am J Physiol Renal Physiol, April 1, 2005; 288(4): F748 - F756.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Renal Physiol.Home page
M. F. Flessner
The transport barrier in intraperitoneal therapy
Am J Physiol Renal Physiol, March 1, 2005; 288(3): F433 - F442.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
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
PNAS, November 23, 2004; 101(47): 16483 - 16488.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
D. S. Long, M. L. Smith, A. R. Pries, K. Ley, and E. R. Damiano
Microviscometry reveals reduced blood viscosity and altered shear rate and shear stress profiles in microvessels after hemodilution
PNAS, July 6, 2004; 101(27): 10060 - 10065.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
A. W. Mulivor and H. H. Lipowsky
Inflammation- and ischemia-induced shedding of venular glycocalyx
Am J Physiol Heart Circ Physiol, May 1, 2004; 286(5): H1672 - H1680.
[Abstract] [Full Text] [PDF]


Home page
Circ. Res.Home page
S. H. Platts and B. R. Duling
Adenosine A3 Receptor Activation Modulates the Capillary Endothelial Glycocalyx
Circ. Res., January 9, 2004; 94(1): 77 - 82.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
P. M. A. van Haaren, E. VanBavel, H. Vink, and J. A. E. Spaan
Localization of the permeability barrier to solutes in isolated arteries by confocal microscopy
Am J Physiol Heart Circ Physiol, December 1, 2003; 285(6): H2848 - H2856.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
E. Chaigneau, M. Oheim, E. Audinat, and S. Charpak
Two-photon imaging of capillary blood flow in olfactory bulb glomeruli
PNAS, October 28, 2003; 100(22): 13081 - 13086.
[Abstract] [Full Text] [PDF]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
A. A. Constantinescu, H. Vink, and J. A.E. Spaan
Endothelial Cell Glycocalyx Modulates Immobilization of Leukocytes at the Endothelial Surface
Arterioscler. Thromb. Vasc. Biol., September 1, 2003; 23(9): 1541 - 1547.
[Abstract] [Full Text] [PDF]


Home page
Biophys. JHome page
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., July 1, 2003; 85(1): 637 - 645.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin
Inaugural Article: Mechanotransduction and flow across the endothelial glycocalyx
PNAS, June 24, 2003; 100(13): 7988 - 7995.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
S. H. Platts, J. Linden, and B. R. Duling
Rapid modification of the glycocalyx caused by ischemia-reperfusion is inhibited by adenosine A2A receptor activation
Am J Physiol Heart Circ Physiol, June 1, 2003; 284(6): H2360 - H2367.
[Abstract] [Full Text] [PDF]


Home page
Circ. Res.Home page
B. M. van den Berg, H. Vink, and J. A.E. Spaan
The Endothelial Glycocalyx Protects Against Myocardial Edema
Circ. Res., April 4, 2003; 92(6): 592 - 594.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
B. M. Fu, B. Chen, and W. Chen
An electrodiffusion model for effects of surface glycocalyx layer on microvessel permeability
Am J Physiol Heart Circ Physiol, April 1, 2003; 284(4): H1240 - H1250.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Renal Physiol.Home page
J. Sorensson, A. Bjornson, M. Ohlson, B. J. Ballermann, and B. Haraldsson
Synthesis of sulfated proteoglycans by bovine glomerular endothelial cells in culture
Am J Physiol Renal Physiol, February 1, 2003; 284(2): F373 - F380.
[Abstract] [Full Text] [PDF]


Home page
Biophys. JHome page
M. Bathe, A. Shirai, C. M. Doerschuk, and R. D. Kamm
Neutrophil Transit Times through Pulmonary Capillaries: The Effects of Capillary Geometry and fMLP-Stimulation
Biophys. J., October 1, 2002; 83(4): 1917 - 1933.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
A. W. Mulivor and H. H. Lipowsky
Role of glycocalyx in leukocyte-endothelial cell adhesion
Am J Physiol Heart Circ Physiol, October 1, 2002; 283(4): H1282 - H1291.
[Abstract] [Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
J. R. Sanders, N. A. Pou, and R. J. Roselli
Neutral and DEAE dextrans as tracers for assessing lung microvascular barrier permeability and integrity
J Appl Physiol, July 1, 2002; 93(1): 251 - 262.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
K. Osterloh, U. Ewert, and A. R. Pries
Interaction of albumin with the endothelial cell surface
Am J Physiol Heart Circ Physiol, July 1, 2002; 283(1): H398 - H405.
[Abstract] [Full Text] [PDF]


Home page
J. Appl. Physiol.Home page
C. A. Kindig, T. E. Richardson, and D. C. Poole
Skeletal muscle capillary hemodynamics from rest to contractions: implications for oxygen transfer
J Appl Physiol, June 1, 2002; 92(6): 2513 - 2520.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
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, August 1, 2001; 281(2): H629 - H636.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
A. A. Constantinescu, H. Vink, and J. A. E. Spaan
Elevated capillary tube hematocrit reflects degradation of endothelial cell glycocalyx by oxidized LDL
Am J Physiol Heart Circ Physiol, March 1, 2001; 280(3): H1051 - H1057.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
C. B. S. Henry and B. R. Duling
TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx
Am J Physiol Heart Circ Physiol, December 1, 2000; 279(6): H2815 - H2823.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Heart Circ. Physiol.Home page
X. Hu, R. H. Adamson, B. Liu, F. E. Curry, and S. Weinbaum
Starling forces that oppose filtration after tissue oncotic pressure is increased
Am J Physiol Heart Circ Physiol, October 1, 2000; 279(4): H1724 - H1736.
[Abstract] [Full Text] [PDF]


Home page
Circulation