The endothelial glycocalyx as a barrier to leukocyte adhesion and its mediation by extracellular proteases

Annals of Biomedical Engineering

Volumn 40, Issue 4, 2012, Pages 840-848

  Lipowsky, Herbert H ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Arterioles; Capillaries; Doxycycline; FMLP; Glycan shedding; Glycocalyx; Glycocalyx thickness; Leukocyte adhesion; Leukocyte rolling velocity; Leukocyte endothelium adhesion; Matrix metallopro tease (MMP); Microcirculation; Post capillary venules; Protease; Resistance to blood flow; TNF

Indexed keywords

ARTERIOLES; BLOOD FLOW; CAPILLARIES; DOXYCYCLINE; FMLP; GLYCOCALYX; GLYCOCALYX THICKNESS; LEUKOCYTE ADHESION; LEUKOCYTE ROLLING VELOCITY; POST-CAPILLARY VENULES; PROTEASE;

BLOOD VESSELS; CELL ADHESION; ELASTICITY; ENDOTHELIAL CELLS; ENZYME ACTIVITY; MICROCIRCULATION; PATHOLOGY; SHEAR FLOW;

ADHESION;

CELL ADHESION MOLECULE; CHEMOTACTIC FACTOR; FORMYLMETHIONYLLEUCYLPHENYLALANINE; MATRIX METALLOPROTEINASE; POLYSACCHARIDE;

ANIMAL; CELL ADHESION; CELL MOTION; CYTOLOGY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYMOLOGY; GLYCOCALYX; HUMAN; LEUKOCYTE; METABOLISM; PHYSIOLOGY; REVIEW;

ANIMALS; CELL ADHESION; CELL ADHESION MOLECULES; CELL MOVEMENT; CHEMOTACTIC FACTORS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; GLYCOCALYX; HUMANS; LEUKOCYTES; MATRIX METALLOPROTEINASES; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; POLYSACCHARIDES;

EID: 84862139767     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-011-0427-x     Document Type: Article

References (90)

1. Adamson, R. H., and G. Clough. Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric micro-vessels. J. Physiol. 445:473-486, 1992.
2. Alon, R., D. A. Hammer, and T. A. Springer. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 374:539-542, 1995.
3. Arfors, K. E., C. Lundberg, L. Lindbom, K. Lundberg, P. G. Beatty, and J. M. Harlan. A monoclonal antibody to the membrane glycoprotein complex CD18 inhibits poly-morphonuclear leukocyte accumulation and plasma leakage in vivo. Blood 69:338-340, 1987. (Pubitemid 17007118)
4. Arisaka, T., M. Mitsumata, M. Kawasumi, T. Tohjima, S. Hirose, and Y. Yoshida. Effects of shear stress on glycos-aminoglycan synthesis in vascular endothelial cells. Ann. N. Y. Acad. Sci. 748:543-554, 1995.
5. Barabino, G. A., M. O. Platt, and D. K. Kaul. Sickle cell biomechanics. Annu. Rev. Biomed. Eng. 12:345-367, 2010.
6. Bennett, H. S., J. H. Luft, and J. C. Hampton. Morphological classifications of vertebrate blood capillaries. Am. J. Physiol. 196:381-390, 1959.
7. Bruegger, D., M. Jacob, M. Rehm, M. Loetsch, U. Welsch, P. Conzen, and B. F. Becker. Atrial natriuretic peptide induces shedding of endothelial glycocalyx in coronary vascular bed of guinea pig hearts. Am. J. Physiol. Heart Circ. Physiol. 289:H1993-H1999, 2005. (Pubitemid 41507349)
8. Brule, S., N. Charnaux, A. Sutton, D. Ledoux, T. Chaig-neau, L. Saffar, and L. Gattegno. The shedding of synd-ecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/CXCL12 and mediated by the matrix metalloproteinase-9. Glycobi-ology 16:488-501, 2006. (Pubitemid 43779045)
9. Cabrales, P., B. Y. Vazquez, A. G. Tsai, and M. Intagli-etta. Microvascular and capillary perfusion following gly-cocalyx degradation. J. Appl. Physiol. 102:2251-2259, 2007. (Pubitemid 47080757)
10. Chappell, D., K. Hofmann-Kiefer, M. Jacob, M. Rehm, J. Briegel, U. Welsch, P. Conzen, and B. F. Becker. TNF-alpha induced shedding of the endothelial glycocalyx is prevented by hydrocortisone and antithrombin. Basic Res. Cardiol. 104:78-89, 2009.
11. Chappell, D., M. Jacob, O. Paul, M. Rehm, U. Welsch, M. Stoeckelhuber, P. Conzen, and B. F. Becker. The glycoca-lyx of the human umbilical vein endothelial cell: an impressive structure ex vivo but not in culture. Circ. Res. 104:1313-1317, 2009.
12. Colburn, P., E. Kobayashi, and V. Buonassisi. Depleted level of heparan sulfate proteoglycan in the extracellular matrix of endothelial cell cultures exposed to endotoxin. J. Cell. Physiol. 159:121-130, 1994. (Pubitemid 24234584)
13. Constantinescu, A. A., H. Vink, and J. A. Spaan. Elevated capillary tube hematocrit reflects degradation of endothe-lial cell glycocalyx by oxidized LDL. Am. J. Physiol. Heart Circ. Physiol. 280:H1051-H1057, 2001.
14. Constantinescu, A. A., H. Vink, and J. A. Spaan. Endo-thelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arterioscler. Thromb. Vasc. Biol. 23:1541-1547, 2003. (Pubitemid 37108195)
15. Danielli, J. F. Capillary permeability and oedema in the perfused frog. J. Physiol. 98:109-129, 1940.
16. DeLano, F. A., and G. W. Schmid-Schonbein. Proteinase activity and receptor cleavage: mechanism for insulin resistance in the spontaneously hypertensive rat. Hypertension 52:415-423, 2008.
17. Desjardins, C., and B. R. Duling. Heparinase treatment suggests a role for the endothelial cell glycocalyx in regulation of capillary hematocrit. Am. J. Physiol. 258:H647-H654, 1990. (Pubitemid 20103193)
18. Ding, K., M. Lopez-Burks, J. A. Sanchez-Duran, M. Korc, and A. D. Lander. Growth factor-induced shedding of syndecan-1 confers glypican-1 dependence on mitogenic responses of cancer cells. J. Cell Biol. 171:729-738, 2005. (Pubitemid 41668731)
19. Endo, K., T. Takino, H. Miyamori, H. Kinsen, T. Yoshi-zaki, M. Furukawa, and H. Sato. Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278:40764-40770, 2003. (Pubitemid 37280893)
20. Fahraeus, R. The suspension stability of blood. Physiol. Rev. 9:241-274, 1929.
21. Fitzgerald, M. L., Z. Wang, P. W. Park, G. Murphy, and M. Bernfield. Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J. Cell Biol. 148:811-824, 2000.
22. Fux, L., N. Ilan, R. D. Sanderson, and I. Vlodavsky. Heparanase: busy at the cell surface. Trends Biochem. Sci. 34:511-519, 2009.
23. Gao, L., and H. H. Lipowsky. Composition of the endo-thelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvasc. Res. 80:394-401, 2010.
24. Golub, L. M., H. M. Lee, M. E. Ryan, W. V. Giannobile, J. Payne, and T. Sorsa. Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms. Adv. Dent. Res. 12:12-26, 1998.
25. Gotte, M. Syndecans in inflammation. FASEB J. 17:575-591, 2003. (Pubitemid 37221142)
26. Gouverneur, M., J. A. Spaan, H. Pannekoek, R. D. Fon-tijn, and H. Vink. Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx. Am. J. Physiol. Heart Circ. Physiol. 290:H458-H462, 2006.
27. Grimm, J., R. Keller, and P. G. de Groot. Laminar flow induces cell polarity and leads to rearrangement of pro-teoglycan metabolism in endothelial cells. Thromb. Hae-most. 60:437-441, 1988. (Pubitemid 19023737)
28. Gronski, Jr., T. J., R. L. Martin, D. K. Kobayashi, B. C. Walsh, M. C. Holman, M. Huber, H. E. Van Wart, and S. D. Shapiro. Hydrolysis of a broad spectrum of extracellular matrix proteins by human macrophage elastase. J. Biol. Chem. 272:12189-12194, 1997. (Pubitemid 27202803)
29. Haas, T. L., M. Milkiewicz, S. J. Davis, A. L. Zhou, S. Egginton, M. D. Brown, J. A. Madri, and O. Hudlicka. Matrix metalloproteinase activity is required for activity- induced angiogenesis in rat skeletal muscle. Am. J. Physiol. Heart Circ. Physiol. 279:1540-1547, 2000.
30. Hafezi-Moghadam, A., K. L. Thomas, A. J. Prorock, Y. Huo, and K. Ley. L-Selectin shedding regulates leukocyte recruitment. J. Exp. Med. 193:863-872, 2001. (Pubitemid 32524536)
31. Haldenby, K. A., D. C. Chappell, C. P. Winlove, K. H. Parker, and J. A. Firth. Focal and regional variations in the composition of the glycocalyx of large vessel endothelium. J. Vasc. Res. 31:2-9, 1994. (Pubitemid 24026294)
32. Hayward, R., R. Scalia, B. Hopper, J. Z. Appel, III, and A. M. Lefer. Cellular mechanisms of heparinase III protection in rat traumatic shock. Am. J. Physiol. 275:H23-H30, 1998.
33. Henry, C. B., and B. R. Duling. TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx. Am. J. Physiol. Heart Circ. Physiol. 279:H2815-H2823, 2000. (Pubitemid 32005870)
34. Hofmann-Kiefer, K. F., G. I. Kemming, D. Chappell, M. Flondor, H. Kisch-Wedel, A. Hauser, S. Pallivathukal, P. Conzen, and M. Rehm. Serum heparan sulfate levels are elevated in endotoxemia. Eur. J. Med. Res. 14:526-531, 2009.
35. Hoover, R. L., R. Folger, W. A. Haering, B. R. Ware, and M. J. Karnovsky. Adhesion of leukocytes to endothelium: roles of divalent cations, surface charge, chemotactic agents and substrate. J. Cell Sci. 45:73-86, 1980. (Pubitemid 11208491)
36. House, S. D., and H. H. Lipowsky. Leukocyte-endothe-lium adhesion: microhemodynamics in mesentery of the cat. Microvasc. Res. 34:363-379, 1987. (Pubitemid 17162156)
37. House, S. D., and H. H. Lipowsky. Microvascular hematocrit and red cell flux in rat cremaster muscle. Am. J. Physiol. 252:H211-H222, 1987.
38. Huxley, V. H., and F. E. Curry. Differential actions of albumin and plasma on capillary solute permeability. Am. J. Physiol. 260:H1645-H1654, 1991.
39. Ihrcke, N. S., and J. L. Platt. Shedding of heparan sulfate proteoglycan by stimulated endothelial cells: evidence for proteolysis of cell-surface molecules. J. Cell. Physiol. 168:625-637, 1996. (Pubitemid 26302869)
40. Ihrcke, N. S., L. E. Wrenshall, B. J. Lindman, and J. L. Platt. Role of heparan sulfate in immune system-blood vessel interactions. Immunol. Today 14:500-505, 1993. (Pubitemid 23301001)
41. Iigo, Y., M. Suematsu, T. Higashida, J. Oheda, K. Mat-sumoto, Y. Wakabayashi, Y. Ishimura, M. Miyasaka, and T. Takashi. Constitutive expression of ICAM-1 in rat microvascular systems analyzed by laser confocal microscopy. Am. J. Physiol. 273:H138-H147, 1997.
42. Jung, U., K. E. Norman, K. Scharffetter-Kochanek, A. L. Beaudet, and K. Ley. Transit time of leukocytes rolling through venules controls cytokine-induced inflammatory cell recruitment in vivo. J. Clin. Invest. 102:1526-1533, 1998. (Pubitemid 28492219)
43. Kinashi, T., and K. Katagiri. Regulation of lymphocyte adhesion and migration by the small GTPase Rap1 and its effector molecule, RAPL. Immunol. Lett. 93:1-5, 2004. (Pubitemid 38591512)
44. Klitzman, B., and B. R. Duling. Microvascular hematocrit and red cell flow in resting and contracting striated muscle. Am. J. Physiol. 237:H481-H490, 1979. (Pubitemid 10249652)
45. Laudanna, C., J. Y. Kim, G. Constantin, and E. Butcher. Rapid leukocyte integrin activation by chemokines. Immunol. Rev. 186:37-46, 2002.
46. Laurent, T. C., and J. R. Fraser. Hyaluronan. FASEB J. 6:2397-2404, 1992.
47. Lawrence, M. B., L. V. McIntire, and S. G. Eskin. Effect of flow on polymorphonuclear leukocyte/endothelial cell adhesion. Blood 70:1284-1290, 1987. (Pubitemid 18026127)
48. Lawrence, M. B., and T. A. Springer. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65:859-873, 1991. (Pubitemid 121001317)
49. Lawrence, M. B., and T. A. Springer. Neutrophils roll on E-selectin. J. Immunol. 151:6338-6346, 1993. (Pubitemid 23340380)
50. Ley, K., D. C. Bullard, M. L. Arbones, R. Bosse, D. Vestweber, T. F. Tedder, and A. L. Beaudet. Sequential contribution of L- and P-selectin to leukocyte rolling in vivo. J. Exp. Med. 181:669-675, 1995.
51. Li, Z., L. Li, H. R. Zielke, L. Cheng, R. Xiao, M. T. Crow, W. G. Stetler-Stevenson, J. Froehlich, and E. G. Lakatta. Increased expression of 72-kd type IV collagenase (MMP-2) in human aortic atherosclerotic lesions. Am. J. Pathol. 148:121-128, 1996. (Pubitemid 26019650)
52. Li, Q., P. W. Park, C. L. Wilson, and W. C. Parks. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111:635-646, 2002. (Pubitemid 35441246)
53. Lipowsky, H. H., R. Sah, and A. Lescanic. Relative roles of doxycycline and cation chelation in endothelial glycan shedding and adhesion of leukocytes. Am. J. Physiol. Heart Circ. Physiol. 300:H415-H422, 2011.
54. Luft, J. H. Fine structures of capillary and endocapillary layer as revealed by ruthenium red. Fed. Proc. 25:1773-1783, 1966.
55. Luo, B. H., C. V. Carman, and T. A. Springer. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25:619-647, 2007. (Pubitemid 46697919)
56. Mulivor, A. W., and H. H. Lipowsky. Role of glycocalyx in leukocyte-endothelial cell adhesion. Am. J. Physiol. Heart Circ. Physiol. 283:H1282-H1291, 2002.
57. Mulivor, A. W., and H. H. Lipowsky. Inflammation- and ischemia-induced shedding of venular glycocalyx. Am. J. Physiol. Heart Circ. Physiol. 286:H1672-H1680, 2004. (Pubitemid 38525453)
58. Mulivor, A. W., and H. H. Lipowsky. Inhibition of glycan shedding and leukocyte-endothelial adhesioninpostcapillary venulesbysuppressionofmatrixmetalloprotease activity with doxycycline. Microcirculation 16:657-666, 2009.
59. Park, P. W., O. Reizes, and M. Bernfield. Cell surface heparan sulfate proteoglycans: selective regulators of ligand-receptor encounters. J. Biol. Chem. 275:29923-29926, 2000.
60. Platt, J. L., A. P. Dalmasso, B. J. Lindman, N. S. Ihrcke, and F. H. Bach. The role of C5a and antibody in the release of heparan sulfate from endothelial cells. Eur. J. Immunol. 21:2887-2890, 1991.
61. Platt, J. L., G. M. Vercellotti, B. J. Lindman, T. R. Oeg-ema, Jr., F. H. Bach, and A. P. Dalmasso. Release of heparan sulfate from endothelial cells. Implications for pathogenesis of hyperacute rejection. J. Exp. Med. 171:1363-1368, 1990. (Pubitemid 20120153)
62. Platts, S. H., and B. R. Duling. Adenosine A3 receptor activation modulates the capillary endothelial glycocalyx. Circ. Res. 94:77-82, 2004. (Pubitemid 38064101)
63. Platts, S. H., 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. 284:H2360-H2367, 2003. (Pubitemid 36622452)
64. Poiseuille, J. L. M. Recherches sur les causes du mouvement du sang dans les vaisseaux capillaries. C. R. Acad. Sci. 6:554-560, 1835.
65. Potter, D. R., and E. R. Damiano. The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro. Circ. Res. 102:770-776, 2008. (Pubitemid 351521584)
66. Pries, A. R., T. W. Secomb, and P. Gaehtgens. The endothelial surface layer. Pflugers Arch. 440:653-666, 2000.
67. Pries, A. R., T. W. Secomb, P. Gaehtgens, and J. F. Gross. Blood flow in microvascular networks. Experiments and simulation. Circ. Res. 67:826-834, 1990. (Pubitemid 20315014)
68. Pries, A. R., T. W. Secomb, H. Jacobs, M. Sperandio, K. Osterloh, and P. Gaehtgens. Microvascular blood flow resistance: role of endothelial surface layer. Am. J. Physiol. 273:H2272-H2279, 1997.
69. Purushothaman, A., T. Uyama, F. Kobayashi, S. Yamada, K. Sugahara, A. C. Rapraeger, and R. D. Sanderson. Heparanase-enhanced shedding of syndecan-1 by myeloma cells promotes endothelial invasion and angiogenesis. Blood 115:2449-2457, 2010.
70. Rapraeger, A. Transforming growth factor (type beta) promotes the addition of chondroitin sulfate chains to the cell surface proteoglycan (syndecan) of mouse mammary epithelia. J. Cell Biol. 109:2509-2518, 1989. (Pubitemid 19282634)
71. Rehm, M., D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation 116:1896-1906, 2007. (Pubitemid 350287085)
72. Reitsma, S., D. W. Slaaf, H. Vink, M. A. van Zandvoort, and M. G. oude Egbrink. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch. 454:345-359, 2007. (Pubitemid 46742429)
73. Smith, M. L., 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. 85:637-645, 2003. (Pubitemid 36753665)
74. Spinale, F. G. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 87:1285-1342, 2007. (Pubitemid 350041472)
75. Springer, T. A. Adhesion receptors of the immune system. Nature 346:425-434, 1990.
76. Squire, J. M., M. Chew, G. Nneji, C. Neal, J. Barry, and C. Michel. Quasi-periodic substructure in the microvessel endothelial glycocalyx: a possible explanation for molecular filtering? J. Struct. Biol. 136:239-255, 2001.
77. Subramanian, S. V., M. L. Fitzgerald, and M. Bernfield. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J. Biol. Chem. 272:14713-14720, 1997. (Pubitemid 27251736)
78. Sutera, S. P., V. Seshadri, P. A. Croce, and R. M. Hoch-muth. Capillary blood flow. II. Deformable model cells in tube flow. Microvasc. Res. 2:420-433, 1970.
79. Svennevig, K., T. Hoel, A. Thiara, S. Kolset, A. Castel-heim, T. Mollnes, F. Brosstad, E. Fosse, and J. Svennevig. Syndecan-1 plasma levels during coronary artery bypass surgery with and without cardiopulmonary bypass. Perfusion 23:165-171, 2008.
80. Taraboletti, G., S. D'Ascenzo, P. Borsotti, R. Giavazzi, A. Pavan, and V. Dolo. Shedding of the matrix metallopro-teinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am. J. Pathol. 160:673-680, 2002. (Pubitemid 34160345)
81. Vink, H., and B. R. Duling. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ. Res. 79:581-589, 1996. (Pubitemid 26276918)
82. Vogl-Willis, C. A., and I. J. Edwards. High-glucose-induced structural changes in the heparan sulfate proteoglycan, perlecan, ofcultured human aortic endothelial cells. Biochim. Biophys. Acta 1672:36-45, 2004. (Pubitemid 38410966)
83. Weinbaum, S., J. M. Tarbell, and E. R. Damiano. The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Eng. 9:121-167, 2007. (Pubitemid 350246654)
84. Xu, J., D. Qu, N. L. Esmon, and C. T. Esmon. Metallo-proteolytic release of endothelial cell protein C receptor. J. Biol. Chem. 275:6038-6044, 2000. (Pubitemid 30115255)
85. Yaras, N., M. Sariahmetoglu, A. Bilginoglu, A. Aydemir-Koksoy, A. Onay-Besikci, B. Turan, and R. Schulz. Protective action of doxycycline against diabetic cardio-myopathy in rats. Br. J. Pharmacol. 155:1174-1184, 2008.
86. Yu, W. H., and J. F. Woessner, Jr. Heparan sulfate pro-teoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7). J. Biol. Chem. 275:4183-4191, 2000. (Pubitemid 30094653)
87. Zarbock, A., and K. Ley. Neutrophil adhesion and activation under flow. Microcirculation 16:31-42, 2009.
88. Zcharia, E., J. Jia, X. Zhang, L. Baraz, U. Lindahl, T. Peretz, I. Vlodavsky, and J. P. Li. Newly generated hepa-ranase knock-out mice unravel co-regulation of heparanase and matrix metalloproteinases. PLoS One 4:e5181, 2009.
89. Zuurbier, C. J., C. Demirci, A. Koeman, H. Vink, and C. Ince. Short-term hyperglycemia increases endothelial gly-cocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells. J. Appl. Physiol. 99:1471-1476, 2005. (Pubitemid 43014356)
90. Zweifach, B. W. Structural makeup of capillary wall. Ann. N. Y. Acad. Sci. 61:670-677, 1955.