The endothelial glycocalyx: composition, functions, and visualization

Algenstaedt P, Schaefer C, Biermann T, Hamann A, Schwarzloh B, Greten H, Ruther W, Hansen-Algenstaedt N (2003) Microvascular alterations in diabetic mice correlate with level of hyperglycemia. Diabetes 52:542–549

Ali S, Fritchley SJ, Chaffey BT, Kirby JA (2002) Contribution of the putative heparan sulfate-binding motif BBXB of RANTES to transendothelial migration. Glycobiology 12:535–543

Allen BL, Filla MS, Rapraeger AC (2001) Role of heparan sulfate as a tissue-specific regulator of FGF-4 and FGF receptor recognition. J Cell Biol 155:845–858

Ballinger ML, Nigro J, Frontanilla KV, Dart AM, Little PJ (2004) Regulation of glycosaminoglycan structure and atherogenesis. Cell Mol Life Sci 61:1296–1306

Barker AL, Konopatskaya O, Neal CR, Macpherson JV, Whatmore JL, Winlove CP, Unwin PR, Shore AC (2004) Observation and characterisation of the glycocalyx of viable human endothelial cells using confocal laser scanning microscopy. Phys Chem Chem Phys 6:1006–1011

Beresewicz A, Czarnowska E, Maczewski M (1998) Ischemic preconditioning and superoxide dismutase protect against endothelial dysfunction and endothelium glycocalyx disruption in the postischemic guinea-pig hearts. Mol Cell Biochem 186:87–97

Berndt MC, Shen Y, Dopheide SM, Gardiner EE, Andrews RK (2001) The vascular biology of the glycoprotein Ib-IX–V complex. Thromb Haemost 86:178–188

Beuk RJ, Heineman E, Tangelder GJ, Quaedackers JS, Marks WH, Lieberman JM, oude Egbrink MG (2000) Total warm ischemia and reperfusion impairs flow in all rat gut layers but increases leukocyte–vessel wall interactions in the submucosa only. Ann Surg 231:96–104

Bode L, Eklund EA, Murch S, Freeze HH (2005) Heparan sulfate depletion amplifies TNF-alpha-induced protein leakage in an in vitro model of protein-losing enteropathy. Am J Physiol Gastrointest Liver Physiol 288:G1015–G1023

Bode L, Murch S, Freeze HH (2006) Heparan sulfate plays a central role in a dynamic in vitro model of protein-losing enteropathy. J Biol Chem 281:7809–7815

Bombeli T, Schwartz BR, Harlan JM (1998) Adhesion of activated platelets to endothelial cells: evidence for a GPIIbIIIa-dependent bridging mechanism and novel roles for endothelial intercellular adhesion molecule 1 (ICAM-1), alphavbeta3 integrin, and GPIbalpha. J Exp Med 187:329–339

Carey DJ (1997) Syndecans: multifunctional cell-surface co-receptors. Biochem J 327(Pt 1):1–16

Constantinescu AA, Vink H, Spaan JA (2003) Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arterioscler Thromb Vasc Biol 23:1541–1547

Curry FR (2005) Microvascular solute and water transport. Microcirculation 12:17–31

Das S, Deb TB, Kumar R, Datta K (1997) Multifunctional activities of human fibroblast 34-kDa hyaluronic acid-binding protein. Gene 190:223–225

Davies PF (1995) Flow-mediated endothelial mechanotransduction. Physiol Rev 75:519–560

Desjardins C, Duling BR (1990) Heparinase treatment suggests a role for the endothelial cell glycocalyx in regulation of capillary hematocrit. Am J Physiol 258:H647–H654

Dewey CF Jr, Bussolari SR, Gimbrone MA Jr, Davies PF (1981) The dynamic response of vascular endothelial cells to fluid shear stress. J Biomech Eng 103:177–185

Dole VS, Bergmeier W, Mitchell HA, Eichenberger SC, Wagner DD (2005) Activated platelets induce Weibel–Palade-body secretion and leukocyte rolling in vivo: role of P-selectin. Blood 106:2334–2339

Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M (2001) Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest 108:1341–1348

Egbrink MG, Van Gestel MA, Broeders MA, Tangelder GJ, Heemskerk JM, Reneman RS, Slaaf DW (2005) Regulation of microvascular thromboembolism in vivo. Microcirculation 12:287–300

Esko JD, Selleck SB (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem 71:435–471

Evanko SP, Wight TN (1999) Intracellular localization of hyaluronan in proliferating cells. J Histochem Cytochem 47:1331–1342

Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM (2003) Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93:e136–e142

Fransson LA, Belting M, Cheng F, Jonsson M, Mani K, Sandgren S (2004) Novel aspects of glypican glycobiology. Cell Mol Life Sci 61:1016–1024

Fromm JR, Hileman RE, Weiler JM, Linhardt RJ (1997) Interaction of fibroblast growth factor-1 and related peptides with heparan sulfate and its oligosaccharides. Arch Biochem Biophys 346:252–262

Funderburgh JL (2000) Keratan sulfate: structure, biosynthesis, and function. Glycobiology 10:951–958

Ghitescu L, Robert M (2002) Diversity in unity: the biochemical composition of the endothelial cell surface varies between the vascular beds. Microsc Res Tech 57:381–389

Gibson RM, Kansas GS, Tedder TF, Furie B, Furie BC (1995) Lectin and epidermal growth factor domains of P-selectin at physiologic density are the recognition unit for leukocyte binding. Blood 85:151–158

Gouverneur M, Spaan JA, Pannekoek H, Fontijn RD, Vink H (2006) Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 290:H452–H458

Grammatikakis N, Grammatikakis A, Yoneda M, Yu Q, Banerjee SD, Toole BP (1995) A novel glycosaminoglycan-binding protein is the vertebrate homologue of the cell cycle control protein, Cdc37. J Biol Chem 270:16198–16205

Granger DN (1999) Ischemia–reperfusion: mechanisms of microvascular dysfunction and the influence of risk factors for cardiovascular disease. Microcirculation 6:167–178

Han YF, Weinbaum S, Spaan JAE, Vink H (2006) Large-deformation analysis of the elastic recoil of fibre layers in a Brinkman medium with application to the endothelial glycocalyx. J Fluid Mech 554:217–235

Hansson GK (2005) Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352:1685–1695

Henry CB, Duling BR (1999) Permeation of the luminal capillary glycocalyx is determined by hyaluronan. Am J Physiol 277:H508–H514

Henry CB, Duling BR (2000) TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 279:H2815–H2823

Hjalmarsson C, Johansson BR, Haraldsson B (2004) Electron microscopic evaluation of the endothelial surface layer of glomerular capillaries. Microvasc Res 67:9–17

Ho G, Broze GJ Jr, Schwartz AL (1997) Role of heparan sulfate proteoglycans in the uptake and degradation of tissue factor pathway inhibitor–coagulation factor Xa complexes. J Biol Chem 272:16838–16844

Hoogewerf AJ, Kuschert GS, Proudfoot AE, Borlat F, Clark-Lewis I, Power CA, Wells TN (1997) Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 36:13570–13578

Hu X, Weinbaum S (1999) A new view of Starling’s hypothesis at the microstructural level. Microvasc Res 58:281–304

Huang MT, Mason JC, Birdsey GM, Amsellem V, Gerwin N, Haskard DO, Ridley AJ, Randi AM (2005) Endothelial intercellular adhesion molecule (ICAM)-2 regulates angiogenesis. Blood 106:1636–1643

Huxley VH, Curry FE (1991) Differential actions of albumin and plasma on capillary solute permeability. Am J Physiol 260:H1645–H1654

Ihrcke NS, Wrenshall LE, Lindman BJ, Platt JL (1993) Role of heparan sulfate in immune system–blood vessel interactions. Immunol Today 14:500–505

Iozzo RV (1994) Perlecan: a gem of a proteoglycan. Matrix Biology 14:203–208

Jacob M, Bruegger D, Rehm M, Welsch U, Conzen P, Becker BF (2006) Contrasting effects of colloid and crystalloid resuscitation fluids on cardiac vascular permeability. Anesthesiology 104:1223–1231

Janssen GH, Tangelder GJ, Oude Egbrink MG, Reneman RS (1994) Spontaneous leukocyte rolling in venules in untraumatized skin of conscious and anesthetized animals. Am J Physiol 267:H1199–H1204

Jung U, Ley K (1997) Regulation of E-selectin, P-selectin, and intercellular adhesion molecule 1 expression in mouse cremaster muscle vasculature. Microcirculation 4:311–319

Kansas GS, Saunders KB, Ley K, Zakrzewicz A, Gibson RM, Furie BC, Furie B, Tedder TF (1994) A role for the epidermal growth factor-like domain of P-selectin in ligand recognition and cell adhesion. J Cell Biol 124:609–618

Kato H (2002) Regulation of functions of vascular wall cells by tissue factor pathway inhibitor: basic and clinical aspects. Arterioscler Thromb Vasc Biol 22:539–548

Kinsella MG, Bressler SL, Wight TN (2004) The regulated synthesis of versican, decorin, and biglycan: extracellular matrix proteoglycans that influence cellular phenotype. Crit Rev Eukaryot Gene Expr 14:203–234

Klitzman B, Duling BR (1979) Microvascular hematocrit and red cell flow in resting and contracting striated muscle. Am J Physiol 237:H481–H490

Klitzman B, Johnson PC (1982) Capillary network geometry and red cell distribution in hamster cremaster muscle. Am J Physiol 242:H211–H219

Koedam JA, Cramer EM, Briend E, Furie B, Furie BC, Wagner DD (1992) P-selectin, a granule membrane protein of platelets and endothelial cells, follows the regulated secretory pathway in AtT-20 cells. J Cell Biol 116:617–625

Kresse H, Hausser H, Schonherr E, Bittner K (1994) Biosynthesis and interactions of small chondroitin/dermatan sulphate proteoglycans. Eur J Clin Chem Clin Biochem 32:259–264

Kupinski AM, Shah DM, Bell DR (1993) Transvascular albumin flux in rabbit hindlimb after tourniquet ischemia. Am J Physiol 264:H901–H908

Kurose I, Argenbright LW, Wolf R, Lianxi L, Granger DN (1997) Ischemia/reperfusion-induced microvascular dysfunction: role of oxidants and lipid mediators. Am J Physiol 272:H2976–H2982

Laurent TC, Fraser JR (1992) Hyaluronan. Faseb J 6:2397–2404

Lee JY, Spicer AP (2000) Hyaluronan: a multifunctional, megaDalton, stealth molecule. Curr Opin Cell Biol 12:581–586

Li Q, Bolli R, Qiu Y, Tang XL, Murphree SS, French BA (1998) Gene therapy with extracellular superoxide dismutase attenuates myocardial stunning in conscious rabbits. Circulation 98:1438–1448

Libby P (2002) Inflammation in atherosclerosis. Nature 420:868–874

Lin X (2004) Functions of heparan sulfate proteoglycans in cell signaling during development. Development 131:6009–6021

Lipowsky HH (2005) Microvascular rheology and hemodynamics. Microcirculation 12:5–15

Lipowsky HH, Kovalcheck S, Zweifach BW (1978) The distribution of blood rheological parameters in the microvasculature of cat mesentery. Circ Res 43:738–749

Lopez-Casillas F, Wrana JL, Massague J (1993) Betaglycan presents ligand to the TGF beta signaling receptor. Cell 73:1435–1444

Lopez JA (1994) The platelet glycoprotein Ib-IX complex. Blood Coagul Fibrinolysis 5:97–119

Luft JH (1966) Fine structures of capillary and endocapillary layer as revealed by ruthenium red. Fed Proc 25:1773–1783

Megens RTA, Reitsma S, Schiffers PHM, Hilgers RHP, De Mey JGR, Slaaf DW, oude Egbrink MGA, van Zandvoort MAMJ (2007) Two-photon microscopy of vital murine elastic and muscular arteries. J Vasc Res 44:87–98

Michel CC (1997) Starling: the formulation of his hypothesis of microvascular fluid exchange and its significance after 100 years. Exp Physiol 82:1–30

Mochizuki S, Vink H, Hiramatsu O, Kajita T, Shigeto F, Spaan JA, Kajiya F (2003) Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am J Physiol Heart Circ Physiol 285:H722–H726

Mulivor AW, Lipowsky HH (2004) Inflammation- and ischemia-induced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol 286:H1672–H1680

Muller AM, Hermanns MI, Cronen C, Kirkpatrick CJ (2002) Comparative study of adhesion molecule expression in cultured human macro- and microvascular endothelial cells. Exp Mol Pathol 73:171–180

Nandi A, Estess P, Siegelman MH (2000) Hyaluronan anchoring and regulation on the surface of vascular endothelial cells is mediated through the functionally active form of CD44. J Biol Chem 275:14939–14948

Nathan DM, Lachin J, Cleary P, Orchard T, Brillon DJ, Backlund JY, O’Leary DH, Genuth S (2003) Intensive diabetes therapy and carotid intima–media thickness in type 1 diabetes mellitus. N Engl J Med 348:2294–2303

Nieuwdorp M, Meuwese MC, Vink H, Hoekstra JB, Kastelein JJ, Stroes ES (2005) The endothelial glycocalyx: a potential barrier between health and vascular disease. Curr Opin Lipidol 16:507–511

Nieuwdorp M, Mooij HL, Kroon J, Atasever B, Spaan JA, Ince C, Holleman F, Diamant M, Heine RJ, Hoekstra JB, Kastelein JJ, Stroes ES, Vink H (2006) Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes. Diabetes 55:1127–1132

Nieuwdorp M, van Haeften TW, Gouverneur MC, Mooij HL, van Lieshout MH, Levi M, Meijers JC, Holleman F, Hoekstra JB, Vink H, Kastelein JJ, Stroes ES (2006) Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes 55:480–486

Oliver MG, Specian RD, Perry MA, Granger DN (1991) Morphologic assessment of leukocyte–endothelial cell interactions in mesenteric venules subjected to ischemia and reperfusion. Inflammation 15:331–346

oude Egbrink MG, Janssen GH, Ookawa K, Slaaf DW, Reneman RS, Wehrens XH, Maaijwee KJ, Ohshima N, Struijker Boudier HA, Tangelder GJ (2002) Especially polymorphonuclear leukocytes, but also monomorphonuclear leukocytes, roll spontaneously in venules of intact rat skin: involvement of E-selectin. J Invest Dermatol 118:323–326

Pappenheimer JR, Renkin EM, Borrero LM (1951) Filtration, diffusion and molecular sieving through peripheral capillary membranes; a contribution to the pore theory of capillary permeability. Am J Physiol 167:13–46

Parker KA, Tollefsen DM (1985) The protease specificity of heparin cofactor II. Inhibition of thrombin generated during coagulation. J Biol Chem 260:3501–3505

Patel KD, Nollert MU, McEver RP (1995) P-selectin must extend a sufficient length from the plasma membrane to mediate rolling of neutrophils. J Cell Biol 131:1893–1902

Perrimon N, Bernfield M (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404:725–728

Pries AR, Ley K, Gaehtgens P (1986) Generalization of the Fahraeus principle for microvessel networks. Am J Physiol 251:H1324–H1332

Pries AR, Secomb TW (2003) Rheology of the microcirculation. Clin Hemorheol Microcirc 29:143–148

Pries AR, Secomb TW (2005) Microvascular blood viscosity in vivo and the endothelial surface layer. Am J Physiol Heart Circ Physiol 289:H2657–H2664

Pries AR, Secomb TW, Gaehtgens P (2000) The endothelial surface layer. Pflugers Arch 440:653–666

Quinsey NS, Greedy AL, Bottomley SP, Whisstock JC, Pike RN (2004) Antithrombin: in control of coagulation. Int J Biochem Cell Biol 36:386–389

Raman R, Sasisekharan V, Sasisekharan R (2005) Structural insights into biological roles of protein–glycosaminoglycan interactions. Chem Biol 12:267–277

Rapraeger A (1989) 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

Rapraeger A, Jalkanen M, Endo E, Koda J, Bernfield M (1985) The cell surface proteoglycan from mouse mammary epithelial cells bears chondroitin sulfate and heparan sulfate glycosaminoglycans. J Biol Chem 260:11046–11052

Rehm M, Zahler S, Lotsch M, Welsch U, Conzen P, Jacob M, Becker BF (2004) Endothelial glycocalyx as an additional barrier determining extravasation of 6% hydroxyethyl starch or 5% albumin solutions in the coronary vascular bed. Anesthesiology 100:1211–1223

Robinson CJ, Stringer SE (2001) The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci 114:853–865

Ross R (1999) Atherosclerosis-an inflammatory disease. N Engl J Med 340:115–126

Rostgaard J, Qvortrup K (1997) Electron microscopic demonstrations of filamentous molecular sieve plugs in capillary fenestrae. Microvasc Res 53:1–13

Rostgaard J, Qvortrup K (2002) Sieve plugs in fenestrae of glomerular capillaries—site of the filtration barrier? Cells Tissues Organs 170:132–138

Rubanyi GM, Romero JC, Vanhoutte PM (1986) Flow-induced release of endothelium-derived relaxing factor. Am J Physiol 250:H1145–H1149

Rubio-Gayosso I, Platts SH, Duling BR (2006) Reactive oxygen species mediate modification of glycocalyx during ischemia–reperfusion injury. Am J Physiol Heart Circ Physiol 290:H2247–H2256

Ruegg C, Mariotti A (2003) Vascular integrins: pleiotropic adhesion and signaling molecules in vascular homeostasis and angiogenesis. Cell Mol Life Sci 60:1135–1157

Ruggeri ZM (2003) Von Willebrand factor, platelets and endothelial cell interactions. J Thromb Haemost 1:1335–1342

Salek-Ardakani S, Arrand JR, Shaw D, Mackett M (2000) Heparin and heparan sulfate bind interleukin-10 and modulate its activity. Blood 96:1879–1888

Sarelius IH, Duling BR (1982) Direct measurement of microvessel hematocrit, red cell flux, velocity, and transit time. Am J Physiol 243:H1018–H1026

Sasaki K, Okouchi Y, Rothkotter HJ, Pabst R (1998) Three-dimensional distribution of intercellular adhesion molecule-1 on lymphocytes in the high endothelial venule analyzed by backscatter electron imaging. Acta Anat (Basel) 162:33–39

Scott JE, Heatley F (1999) Hyaluronan forms specific stable tertiary structures in aqueous solution: a 13C NMR study. Proc Natl Acad Sci USA 96:4850–4855

Scott JE, Thomlinson AM, Prehm P (2003) Supramolecular organization in streptococcal pericellular capsules is based on hyaluronan tertiary structures. Exp Cell Res 285:1–8

Seal JB, Gewertz BL (2005) Vascular dysfunction in ischemia–reperfusion injury. Ann Vasc Surg 19:572–584

Secomb TW, Hsu R, Pries AR (1998) A model for red blood cell motion in glycocalyx-lined capillaries. Am J Physiol 274:H1016–H1022

Shimada K, Kobayashi M, Kimura S, Nishinaga M, Takeuchi K, Ozawa T (1991) Anticoagulant heparin-like glycosaminoglycans on endothelial cell surface. Jpn Circ J 55:1016–1021

Sperandio M (2006) Selectins and glycosyltransferases in leukocyte rolling in vivo. Febs J 273:4377–4389

Sperandio M, Ley K (2005) The physiology and pathophysiology of P-selectin. Mod Asp Immunobiol 15:24–26

Spillmann D, Witt D, Lindahl U (1998) Defining the interleukin-8-binding domain of heparan sulfate. J Biol Chem 273:15487–15493

Springer TA (1990) Adhesion receptors of the immune system. Nature 346:425–434

Starling EH (1896) On the absorption of fluids from the connective tissue spaces. J Physiol 19:312–326

Stewart RJ, Kashour TS, Marsden PA (1996) Vascular endothelial platelet endothelial adhesion molecule-1 (PECAM-1) expression is decreased by TNF-alpha and IFN-gamma. Evidence for cytokine-induced destabilization of messenger ribonucleic acid transcripts in bovine endothelial cells. J Immunol 156:1221–1228

Sugahara K, Mikami T, Uyama T, Mizuguchi S, Nomura K, Kitagawa H (2003) Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr Opin Struct Biol 13:612–620

Tan L, Kowalska MA, Romo GM, Lopez JA, Darzynkiewicz Z, Niewiarowski S (1999) Identification and characterization of endothelial glycoprotein Ib using viper venom proteins modulating cell adhesion. Blood 93:2605–2616

Tarbell JM, Pahakis MY (2006) Mechanotransduction and the glycocalyx. J Intern Med 259:339–350

Tarbell JM, Weinbaum S, Kamm RD (2005) Cellular fluid mechanics and mechanotransduction. Ann Biomed Eng 33:1719–1723

Title LM, Cummings PM, Giddens K, Nassar BA (2000) Oral glucose loading acutely attenuates endothelium-dependent vasodilation in healthy adults without diabetes: an effect prevented by vitamins C and E. J Am Coll Cardiol 36:2185–2191

Tkachenko E, Rhodes JM, Simons M (2005) Syndecans: new kids on the signaling block. Circ Res 96:488–500

Tovar AM, de Mattos DA, Stelling MP, Sarcinelli-Luz BS, Nazareth RA, Mourao PA (2005) Dermatan sulfate is the predominant antithrombotic glycosaminoglycan in vessel walls: implications for a possible physiological function of heparin cofactor II. Biochim Biophys Acta 1740:45–53

Ueda A, Shimomura M, Ikeda M, Yamaguchi R, Tanishita K (2004) Effect of glycocalyx on shear-dependent albumin uptake in endothelial cells. Am J Physiol Heart Circ Physiol 287:H2287–H2294

van den Berg B, Vink H (2006) Glycocalyx perturbation: cause or consequence of damage to the vasculature? Am J Physiol Heart Circ Physiol 290:H2174–H2175

van den Berg BM, Spaan JA, Rolf TM, Vink H (2006) Atherogenic region and diet diminish glycocalyx dimension and increase intima-to-media ratios at murine carotid artery bifurcation. Am J Physiol Heart Circ Physiol 290:H915–H920

van den Berg BM, Vink H, Spaan JA (2003) The endothelial glycocalyx protects against myocardial edema. Circ Res 92:592–594

van Haaren PM, VanBavel E, Vink H, Spaan JA (2003) Localization of the permeability barrier to solutes in isolated arteries by confocal microscopy. Am J Physiol Heart Circ Physiol 285:H2848–H2856

van Haaren PM, VanBavel E, Vink H, Spaan JA (2005) Charge modification of the endothelial surface layer modulates the permeability barrier of isolated rat mesenteric small arteries. Am J Physiol Heart Circ Physiol 289:H2503–H2507

van Zandvoort M, Engels W, Douma K, Beckers L, Oude Egbrink M, Daemen M, Slaaf DW (2004) Two-photon microscopy for imaging of the (atherosclerotic) vascular wall: a proof of concept study. J Vasc Res 41:54–63

Vink H, Constantinescu AA, Spaan JA (2000) Oxidized lipoproteins degrade the endothelial surface layer: implications for platelet–endothelial cell adhesion. Circulation 101:1500–1502

Vink H, Duling BR (1996) Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ Res 79:581–589

Vink H, Duling BR (2000) Capillary endothelial surface layer selectively reduces plasma solute distribution volume. Am J Physiol Heart Circ Physiol 278:H285–H289

Vogl-Willis CA, Edwards IJ (2004) High-glucose-induced structural changes in the heparan sulfate proteoglycan, perlecan, of cultured human aortic endothelial cells. Biochim Biophys Acta 1672:36–45

Vollmar B, Glasz J, Menger MD, Messmer K (1995) Leukocytes contribute to hepatic ischemia/reperfusion injury via intercellular adhesion molecule-1-mediated venular adherence. Surgery 117:195–200

Wang CS, Hartsuck J, McConathy WJ (1992) Structure and functional properties of lipoprotein lipase. Biochim Biophys Acta 1123:1–17

Ward BJ, Donnelly JL (1993) Hypoxia induced disruption of the cardiac endothelial glycocalyx: implications for capillary permeability. Cardiovasc Res 27:384–389

Weigel PH, Hascall VC, Tammi M (1997) Hyaluronan synthases. J Biol Chem 272:13997–14000

Weiler H, Isermann BH (2003) Thrombomodulin. J Thromb Haemost 1:1515–1524

Weinbaum S (1998) 1997 Whitaker distinguished lecture: models to solve mysteries in biomechanics at the cellular level; a new view of fiber matrix layers. Ann Biomed Eng 26:627–643

Weinbaum S, Zhang X, Han Y, Vink H, Cowin SC (2003) Mechanotransduction and flow across the endothelial glycocalyx. Proc Natl Acad Sci USA 100:7988–7995

Weninger W, Ulfman LH, Cheng G, Souchkova N, Quackenbush EJ, Lowe JB, von Andrian UH (2000) Specialized contributions by alpha(1,3)-fucosyltransferase-IV and FucT-VII during leukocyte rolling in dermal microvessels. Immunity 12:665–676

Wilsie LC, Orlando RA (2003) The low density lipoprotein receptor-related protein complexes with cell surface heparan sulfate proteoglycans to regulate proteoglycan-mediated lipoprotein catabolism. J Biol Chem 278:15758–15764

Wu G, Essex DW, Meloni FJ, Takafuta T, Fujimura K, Konkle BA, Shapiro SS (1997) Human endothelial cells in culture and in vivo express on their surface all four components of the glycoprotein Ib/IX/V complex. Blood 90:2660–2669

Xiong JP, Stehle T, Goodman SL, Arnaout MA (2003) Integrins, cations and ligands: making the connection. J Thromb Haemost 1:1642–1654

Yamashita K, Fukushima K (2004) The carbohydrate recognition by cytokines modulates their physiological activities. Glycoconj J 21:31–34

Zhang X, Adamson RH, Curry FR, Weinbaum S (2006) A 1-D model to explore the effects of tissue loading and tissue concentration gradients in the revised Starling principle. Am J Physiol Heart Circ Physiol 291:H2950–H2964

Zhuo L, Hascall VC, Kimata K (2004) Inter-alpha-trypsin inhibitor, a covalent protein–glycosaminoglycan–protein complex. J Biol Chem 279:38079–38082