A microscopic view on the renal endothelial glycocalyx

American Journal of Physiology - Renal Physiology

Volumn 308, Issue 9, 2015, Pages F956-F966

  Dane, Martijn J C ^a   Van Den Berg, Bernard M ^a   Lee, Dae Hyun ^a   Boels, Margien G S ^a   Tiemeier, Gesa L ^a   Avramut, M Cristina ^a   Van Zonneveld, Anton Jan ^a   Van Der Vlag, Johan ^b   Vink, Hans ^c   Rabelink, Ton J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Endothelial glycocalyx; Endothelial surface layer; Glomerular endothelium; Imaging; Renal

Indexed keywords

ALBUMIN; HEPARAN SULFATE; HYALURONIC ACID; REACTIVE OXYGEN METABOLITE;

ANTICOAGULATION; ATOMIC FORCE MICROSCOPY; CELL FUNCTION; CELL STRUCTURE; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; ERYTHROCYTE; FLUORESCENCE MICROSCOPY; GLOMERULAR FILTRATION BARRIER; GLOMERULUS BASEMENT MEMBRANE; GLOMERULUS CAPILLARY; GLOMERULUS FILTRATION; GLYCOCALYX; HUMAN; INFLAMMATION; KIDNEY BLOOD VESSEL; KIDNEY CELL; KIDNEY TRANSPLANTATION; LEUKOCYTE MIGRATION; MACROMOLECULE; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SHEAR STRESS; ANIMAL; KIDNEY; KIDNEY DISEASE; LABORATORY DIAGNOSIS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; STAINING; ULTRASTRUCTURE; VASCULARIZATION;

ANIMALS; ENDOTHELIAL CELLS; GLYCOCALYX; HUMANS; KIDNEY; KIDNEY DISEASES; MICROSCOPY; SPECIMEN HANDLING; STAINING AND LABELING;

EID: 84930827364     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00532.2014     Document Type: Review

References (118)

1. Adamson RH, Lenz JF, Zhang X, Adamson GN, Weinbaum S, Curry FE. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol 557: 889–907, 2004
2. Aird WC. Phenotypic heterogeneity of the endothelium. II. Representative vascular beds. Circ Res 100: 174–190, 2007
3. Amraoui F, Olde Engberink RH, van Gorp J, Ramdani A, Vogt L, van den Born BJ. Microvascular glycocalyx dimension estimated by automated SDF imaging is not related to cardiovascular disease. Microcirculation 21: 499–505, 2014
4. Arkill KP, Knupp C, Michel CC, Neal CR, Qvortrup K, Rostgaard J, Squire JM. Similar endothelial glycocalyx structures in microvessels from a range of mammalian tissues: evidence for a common filtering mechanism? Biophys J 101: 1046–1056, 2011
5. Axelsson J, Xu D, Kang BN, Nussbacher JK, Handel TM, Ley K, Sriramarao P, Esko JD. Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood 120: 1742–1751, 2012
6. Becker BF, Chappell D, Jacob M. Endothelial glycocalyx and coronary vascular permeability: the fringe benefit. Basic Res Cardiol 105: 687–701, 2010
7. Bhalla G, Deen WM. Effects of charge on osmotic reflection coefficients of macromolecules in fibrous membranes. Biophys J 97: 1595–1605, 2009
8. Boels MG, Lee DH, van den Berg BM, Dane MJ, van der Vlag J, Rabelink TJ. The endothelial glycocalyx as a potential modifier of the hemolytic uremic syndrome. Eur J Intern Med 24: 503–509, 2013
9. Broekhuizen LN, Lemkes BA, Mooij HL, Meuwese MC, Verberne H, Holleman F, Schlingemann RO, Nieuwdorp M, Stroes ES, Vink H. Effect of sulodexide on endothelial glycocalyx and vascular permeability in patients with type 2 diabetes mellitus. Diabetologia 53: 2646–2655, 2010
10. Bruegger D, Jacob M, Rehm M, Loetsch M, Welsch U, Conzen P, Becker BF. 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
11. Casu B, Lindahl U. Structure and biological interactions of heparin and heparan sulfate. Advan Carbohydr Chem Biochem 57: 159–206, 2001
12. Chang RL, Deen WM, Robertson CR, Brenner BM. Permselectivity of the glomerular capillary wall. III. Restricted transport of polyanions. Kidney Int 8: 212–218, 1975
13. Chang RL, Ueki IF, Troy JL, Deen WM, Robertson CR, Brenner BM. Permselectivity of the glomerular capillary wall to macromolecules. II. Experimental studies in rats using neutral dextran. Biophys J 15: 887–906, 1975
14. Chappell D, Jacob M, Paul O, Rehm M, Welsch U, Stoeckelhuber M, Conzen P, Becker BF. The glycocalyx of the human umbilical vein endothelial cell: an impressive structure ex vivo but not in culture. Circ Res 104: 1313–1317, 2009
15. Comper WD. Albuminuria is controlled primarily by proximal tubules. Nat Rev Nephrol 10: 180, 2014
16. Comper WD, Laurent TC. Physiological function of connective tissue polysaccharides. Physiol Rev 58: 255–315, 1978
17. Constantinescu AA, Vink H, Spaan JA. Elevated capillary tube hematocrit reflects degradation of endothelial cell glycocalyx by oxidized LDL. Am J Physiol Heart Circ Physiol 280: H1051–H1057, 2001
18. Dane MJ, Khairoun M, Lee DH, van den Berg BM, Eskens BJ, Boels MG, van Teeffelen JW, Rops AL, van der Vlag J, van Zonneveld AJ, Reinders ME, Vink H, Rabelink TJ. Association of kidney function with changes in the endothelial surface layer. Clin J Am Soc Nephrol 9: 698–704, 2014
19. Dane MJ, van den Berg BM, Avramut MC, Faas FG, van der Vlag J, Rops AL, Ravelli RB, Koster BJ, van Zonneveld AJ, Vink H, Rabelink TJ. Glomerular endothelial surface layer acts as a barrier against albumin filtration. Am J Pathol 182: 1532–1540, 2013
20. Day AJ, Sheehan JK. Hyaluronan: polysaccharide chaos to protein organisation. Curr Opin Struct Biol 11: 617–622, 2001
21. Donati A, Damiani E, Domizi R, Romano R, Adrario E, Pelaia P, Ince C, Singer M. Alteration of the sublingual microvascular glycocalyx in critically ill patients. Microvasc Res 90: 86–89, 2013
22. Dyer DP, Thomson JM, Hermant A, Jowitt TA, Handel TM, Proudfoot AE, Day AJ, Milner CM. TSG-6 inhibits neutrophil migration via direct interaction with the chemokine CXCL8. J Immunol 192: 2177–2185, 2014
23. Erlandsen SL, Kristich CJ, Dunny GM, Wells CL. High-resolution visualization of the microbial glycocalyx with low-voltage scanning electron microscopy: dependence on cationic dyes. J Histochem Cytochem 52: 1427–1435, 2004
24. Esko JD, Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest 108: 169–173, 2001
25. Esko JD, Selleck SB. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem 71: 435–471, 2002
26. Faas FG, Avramut MC, van den Berg BM, Mommaas AM, Koster AJ, Ravelli RB. Virtual nanoscopy: generation of ultra-large high resolution electron microscopy maps. J Cell Biol 198: 457–469, 2012
27. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93: e136–e142, 2003
28. Foster RR, Armstrong L, Baker S, Wong DW, Wylie EC, Ramnath R, Jenkins R, Singh A, Steadman R, Welsh GI, Mathieson PW, Satchell SC. Glycosaminoglycan regulation by VEGFA and VEGFC of the glomerular microvascular endothelial cell glycocalyx in vitro. Am J Pathol 183: 604–616, 2013
29. Friden V, Oveland E, Tenstad O, Ebefors K, Nystrom J, Nilsson UA, Haraldsson B. The glomerular endothelial cell coat is essential for glomerular filtration. Kidney Int 79: 1322–1330, 2011
30. Giantsos-Adams KM, Koo AJ, Song S, Sakai J, Sankaran J, Shin JH, Garcia-Cardena G, Dewey CF Jr. Heparan sulfate regrowth profiles under laminar shear flow following enzymatic degradation. Cell Mol Bioeng 6: 160–174, 2013
31. Groner W, Winkelman JW, Harris AG, Ince C, Bouma GJ, Messmer K, Nadeau RG. Orthogonal polarization spectral imaging: a new method for study of the microcirculation. Nat Med 5: 1209–1212, 1999
32. Guimaraes MA, Nikolovski J, Pratt LM, Greive K, Comper WD. Anomalous fractional clearance of negatively charged Ficoll relative to uncharged Ficoll. Am J Physiol Renal Physiol 285: F1118–F1124, 2003
33. Han Y, Weinbaum S, Spaan JA, Vink H. 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, 2006
34. Haraldsson B, Nystrom J, Deen WM. Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 88: 451–487, 2008
35. He L, Vicente CP, Westrick RJ, Eitzman DT, Tollefsen DM. Heparin cofactor II inhibits arterial thrombosis after endothelial injury. J Clin Invest 109: 213–219, 2002
36. Hjalmarsson C, Johansson BR, Haraldsson B. Electron microscopic evaluation of the endothelial surface layer of glomerular capillaries. Microvasc Res 67: 9–17, 2004
37. Ikeda Y, Charef S, Ouidja MO, Barbier-Chassefiere V, Sineriz F, Duchesnay A, Narasimprakash H, Martelly I, Kern P, Barritault D, Petit E, Papy-Garcia D. Synthesis and biological activities of a library of glycosaminoglycans mimetic oligosaccharides. Biomaterials 32: 769–776, 2011
38. Isermann B, Vinnikov IA, Madhusudhan T, Herzog S, Kashif M, Blautzik J, Corat MA, Zeier M, Blessing E, Oh J, Gerlitz B, Berg DT, Grinnell BW, Chavakis T, Esmon CT, Weiler H, Bierhaus A, Nawroth PP. Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat Med 13: 1349–1358, 2007
39. Iwashima Y, Sato T, Watanabe K, Ooshima E, Hiraishi S, Ishii H, Kazama M, Makino I. Elevation of plasma thrombomodulin level in diabetic patients with early diabetic nephropathy. Diabetes 39: 983–988, 1990
40. Jacob M, Bruegger D, Rehm M, Welsch U, Conzen P, Becker BF. Contrasting effects of colloid and crystalloid resuscitation fluids on cardiac vascular permeability. Anesthesiology 104: 1223–1231, 2006
41. Jeansson M, Bjorck K, Tenstad O, Haraldsson B. Adriamycin alters glomerular endothelium to induce proteinuria. J Am Soc Nephrol 20: 114–122, 2009
42. Jeansson M, Haraldsson B. Glomerular size and charge selectivity in the mouse after exposure to glucosaminoglycan-degrading enzymes. J Am Soc Nephrol 14: 1756–1765, 2003
43. Jeansson M, Haraldsson B. Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. Am J Physiol Renal Physiol 290: F111–F116, 2006
44. Jiang D, Liang J, Noble PW. Hyaluronan as an immune regulator in human diseases. Physiol Rev 91: 221–264, 2011
45. Kim MY, Muto J, Gallo RL. Hyaluronic acid oligosaccharides suppress TLR3-dependent cytokine expression in a TLR4-dependent manner. PloS One 8: e72421, 2013
46. Kliment CR, Tobolewski JM, Manni ML, Tan RJ, Enghild J, Oury TD. Extracellular superoxide dismutase protects against matrix degradation of heparan sulfate in the lung. Antioxid Redox Signal 10: 261–268, 2008
47. Laurent T. The biology of hyaluronan. Introduction. Ciba Found Symp 143: 1–20, 1989
48. Laurent TC, Fraser JR. Hyaluronan. FASEB J 6: 2397–2404, 1992
49. Laurent TC, Laurent UB, Fraser JR. Functions of hyaluronan. Ann Rheum Dis 54: 429–432, 1995
50. Lee DH, Dane MJ, van den Berg BM, Boels MG, van Teeffelen JW, de Mutsert R, den Heijer M, Rosendaal FR, van der Vlag J, van Zonneveld AJ, Vink H, Rabelink TJ, and group NEOs. Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion. PloS One 9: e96477, 2014
51. Lennon FE, Singleton PA. Hyaluronan regulation of vascular integrity. Am J Cardiovasc Dis 1: 200–213, 2011
52. Lensen JF, Rops AL, Wijnhoven TJ, Hafmans T, Feitz WF, Oosterwijk E, Banas B, Bindels RJ, van den Heuvel LP, van der Vlag J, Berden JH, van Kuppevelt TH. Localization and functional characterization of glycosaminoglycan domains in the normal human kidney as revealed by phage display-derived single chain antibodies. J Am Soc Nephrol 16: 1279–1288, 2005
53. Li W, Huntington JA. The heparin binding site of protein C inhibitor is protease-dependent. J Biol Chem 283: 36039–36045, 2008
54. Li W, Johnson DJ, Esmon CT, Huntington JA. Structure of the antithrombin-thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol 11: 857–862, 2004
55. Lin JH, McLean K, Morser J, Young TA, Wydro RM, Andrews WH, Light DR. Modulation of glycosaminoglycan addition in naturally expressed and recombinant human thrombomodulin. J Biol Chem 269: 25021–25030, 1994
56. Lindahl B, Eriksson L, Lindahl U. Structure of heparan sulphate from human brain, with special regard to Alzheimer’s disease. Biochem J 306: 177–184, 1995
57. Lindstrom KE, Blom A, Johnsson E, Haraldsson B, Fries E. High glomerular permeability of bikunin despite similarity in charge and hydrodynamic size to serum albumin. Kidney Int 51: 1053–1058, 1997
58. Lindstrom KE, Johnsson E, Haraldsson B. Glomerular charge selectivity for proteins larger than serum albumin as revealed by lactate dehydrogenase isoforms. Acta Physiol Scand 162: 481–488, 1998
59. Lipowsky HH, Gao L, Lescanic A. Shedding of the endothelial glycocalyx in arterioles, capillaries, and venules and its effect on capillary hemodynamics during inflammation. Am J Physiol Heart Circ Physiol 301: H2235–H2245, 2011
60. Lipowsky HH, Lescanic A. The effect of doxycycline on shedding of the glycocalyx due to reactive oxygen species. Microvasc Res 90: 80–85, 2013
61. Lopez-Quintero SV, Cancel LM, Pierides A, Antonetti D, Spray DC, Tarbell JM. High glucose attenuates shear-induced changes in endothelial hydraulic conductivity by degrading the glycocalyx. PloS One 8: e78954, 2013
62. Luft JH. Fine structures of capillary and endocapillary layer as revealed by ruthenium red. Fed Proc 25: 1773–1783, 1966
63. Massena S, Christoffersson G, Hjertstrom E, Zcharia E, Vlodavsky I, Ausmees N, Rolny C, Li JP, Phillipson M. A chemotactic gradient sequestered on endothelial heparan sulfate induces directional intraluminal crawling of neutrophils. Blood 116: 1924–1931, 2010
64. Miner JH. Glomerular filtration: the charge debate charges ahead. Kidney Int 74: 259–261, 2008
65. Mochizuki S, Vink H, Hiramatsu O, Kajita T, Shigeto F, Spaan JA, Kajiya F. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am J Physiol Heart Circ Physiol 285: H722–H726, 2003
66. Mulders TA, Nieuwdorp M, Stroes ES, Vink H, Pinto-Sietsma SJ. Non-invasive assessment of microvascular dysfunction in families with premature coronary artery disease. Int J Cardiol 168: 5026–5028, 2013
67. Mulivor AW, Lipowsky HH. Inflammation- and ischemia-induced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol 286: H1672–H1680, 2004
68. Mulivor AW, Lipowsky HH. Inhibition of glycan shedding and leukocyte- endothelial adhesion in postcapillary venules by suppression of matrixmetalloprotease activity with doxycycline. Microcirculation 16: 657–666, 2009
69. Nieuwdorp M, Meuwese MC, Mooij HL, Ince C, Broekhuizen LN, Kastelein JJ, Stroes ES, Vink H. Measuring endothelial glycocalyx dimensions in humans: a potential novel tool to monitor vascular vulnerability. J Appl Physiol 104: 845–852, 2008
70. 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. Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes. Diabetes 55: 1127–1132, 2006
71. 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. Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes 55: 480–486, 2006
72. Norgard-Sumnicht K, Varki A. Endothelial heparan sulfate proteoglycans that bind to L-selectin have glucosamine residues with unsubstituted amino groups. J Biol Chem 270: 12012–12024, 1995
73. Norgard-Sumnicht KE, Varki NM, Varki A. Calcium-dependent heparin- like ligands for L-selectin in nonlymphoid endothelial cells. Science 261: 480–483, 1993
74. Ohlson M, Sorensson J, Haraldsson B. Glomerular size and charge selectivity in the rat as revealed by FITC-Ficoll and albumin. Am J Physiol Renal Physiol 279: F84–F91, 2000
75. Oida K, Takai H, Maeda H, Takahashi S, Tamai T, Nakai T, Miyabo S, Ishii H. Plasma thrombomodulin concentration in diabetes mellitus. Diabetes Res Clin Pract 10: 193–196, 1990
76. Olson ST, Bjork I. Predominant contribution of surface approximation to the mechanism of heparin acceleration of the antithrombin-thrombin reaction. Elucidation from salt concentration effects. J Biol Chem 266: 6353–6364, 1991
77. Oohira A, Wight TN, Bornstein P. Sulfated proteoglycans synthesized by vascular endothelial cells in culture. J Biol Chem 258: 2014–2021, 1983
78. Padberg JS, Wiesinger A, Marco GSd Reuter S, Grabner A, Kentrup D, Lukasz A, Oberleithner H, Pavenstädt H, Brand M, Kümpers P. Damage of the endothelial glycocalyx in chronic kidney disease. Atherosclerosis 234: 335–343, 2014
79. Pahakis MY, Kosky JR, Dull RO, Tarbell JM. The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem Biophys Res Commun 355: 228–233, 2007
80. Parish CR, Freeman C, Brown KJ, Francis DJ, Cowden WB. Identification of sulfated oligosaccharide-based inhibitors of tumor growth and metastasis using novel in vitro assays for angiogenesis and heparanase activity. Cancer Res 59: 3433–3441, 1999
81. Parkinson JF, Vlahos CJ, Yan SC, Bang NU. Recombinant human thrombomodulin. Regulation of cofactor activity and anticoagulant function by a glycosaminoglycan side chain. Biochem J 283: 151–157, 1992
82. Presanis JS, Hajela K, Ambrus G, Gal P, Sim RB. Differential substrate and inhibitor profiles for human MASP-1 and MASP-2. Mol Immunol 40: 921–929, 2004
83. Ramiro-Diaz J, Barajas-Espinosa A, Chi-Ahumada E, Perez-Aguilar S, Torres-Tirado D, Castillo-Hernandez J, Knabb M, de Rosa AB, Rubio R. Luminal endothelial lectins with affinity for N-acetylglucosamine determine flow-induced cardiac and vascular paracrine-dependent responses. Am J Physiol Heart Circ Physiol 299: H743–H751, 2010
84. Rehm M, Bruegger D, Christ F, Conzen P, Thiel M, Jacob M, Chappell D, Stoeckelhuber M, Welsch U, Reichart B, Peter K, Becker BF. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation 116: 1896–1906, 2007
85. Reitsma S, Oude Egbrink MG, Heijnen VV, Megens RT, Engels W, Vink H, Slaaf DW, van Zandvoort MA. Endothelial glycocalyx thickness and platelet-vessel wall interactions during atherogenesis. Thromb Haemost 106: 939–946, 2011
86. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, Oude Egbrink MG. The endothelial glycocalyx: composition, functions, and visualization. Pflügers Arch 454: 345–359, 2007
87. Rix DA, Douglas MS, Talbot D, Dark JH, Kirby JA. Role of glycosaminoglycans (GAGs) in regulation of the immunogenicity of human vascular endothelial cells. Clin Exp Immunol 104: 60–65, 1996
88. Rops AL, van den Hoven MJ, Baselmans MM, Lensen JF, Wijnhoven TJ, van den Heuvel LP, van Kuppevelt TH, Berden JH, van der Vlag J. Heparan sulfate domains on cultured activated glomerular endothelial cells mediate leukocyte trafficking. Kidney Int 73: 52–62, 2008
89. Rops AL, van der Vlag J, Lensen JF, Wijnhoven TJ, van den Heuvel LP, van Kuppevelt TH, Berden JH. Heparan sulfate proteoglycans in glomerular inflammation. Kidney Int 65: 768–785, 2004
90. Rops LWMMA, Loeven MA, van Gemst JJ, Eversen I, Van Wijk XM, Dijkman HB, van Kuppevelt TH, Berden JH, Rabelink TJ, Esko JD, van der Vlag J. Modulation of heparan sulfate in the glomerular endothelial glycocalyx decreases leukocyte influx during experimental glomerulonephritis. Kidney Int 86: 932–942, 2014
91. Ruggiero A, Villa CH, Bander E, Rey DA, Bergkvist M, Batt CA, Manova-Todorova K, Deen WM, Scheinberg DA, McDevitt MR. Paradoxical glomerular filtration of carbon nanotubes. Proc Natl Acad Sci USA 107: 12369–12374, 2010
92. Ryan GB, Karnovsky MJ. Distribution of endogenous albumin in the rat glomerulus: role of hemodynamic factors in glomerular barrier function. Kidney Int 9: 36–45, 1976
93. Sahu A, Pangburn MK. Identification of multiple sites of interaction between heparin and the complement system. Mol Immunol 30: 679–684, 1993
94. Shi X, Zaia J. Organ-specific heparan sulfate structural phenotypes. J Biol Chem 284: 11806–11814, 2009
95. Singh A, Friden V, Dasgupta I, Foster RR, Welsh GI, Tooke JE, Haraldsson B, Mathieson PW, Satchell SC. High glucose causes dysfunction of the human glomerular endothelial glycocalyx. Am J Physiol Renal Physiol 300: F40–F48, 2011
96. Singh A, Ramnath RD, Foster RR, Wylie EC, Friden V, Dasgupta I, Haraldsson B, Welsh GI, Mathieson PW, Satchell SC. Reactive oxygen species modulate the barrier function of the human glomerular endothelial glycocalyx. PloS One 8: e55852, 2013
97. Singh A, Satchell SC, Neal CR, McKenzie EA, Tooke JE, Mathieson PW. Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol 18: 2885–2893, 2007
98. Smith ML, Long DS, Damiano ER, Ley K. Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo. Biophys J 85: 637–645, 2003
99. Snoeijs MG, Vink H, Voesten N, Christiaans MH, Daemen JW, Peppelenbosch AG, Tordoir JH, Peutz-Kootstra CJ, Buurman WA, Schurink GW, van Heurn LW. Acute ischemic injury to the renal microvasculature in human kidney transplantation. Am J Physiol Renal Physiol 299: F1134–F1140, 2010
100. Thi MM, Tarbell JM, Weinbaum S, Spray DC. The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a “bumper-car” model. Proc Natl Acad Sci USA 101: 16483–16488, 2004
101. van den Berg BM, Boels MG, Avramut MC, Jansen E, Meldner S, Dane MJC, van der Vlag J, Vink H, Koster AJ, Van Zonneveld AJ, Grone HJ, De Koning EJ, Rabelink TJ. Genetic deletion of endothelial hyaluronan synthase 2 results in glomerular injury and albuminuria (Abstract). http://www.nefro.nl/uploads/Er/e1/Ere18-CBMxI5GezCbqpivg/141001- Abstracts_NfN-Fall-Symposium-2014_FINALa.pdf
102. van den Berg BM, Nieuwdorp M, Stroes ES, Vink H. Glycocalyx and endothelial (dys) function: from mice to men. Pharmacol Rep 58, Suppl: 75–80, 2006
103. van den Berg BM, Spaan JA, Vink H. Impaired glycocalyx barrier properties contribute to enhanced intimal low-density lipoprotein accumulation at the carotid artery bifurcation in mice. Pflügers Arch 457: 1199–1206, 2009
104. van den Berg BM, Vink H, Spaan JA. The endothelial glycocalyx protects against myocardial edema. Circ Res 92: 592–594, 2003
105. van den Hoven MJ, Wijnhoven TJ, Li JP, Zcharia E, Dijkman HB, Wismans RG, Rops AL, Lensen JF, van den Heuvel LP, van Kuppevelt TH, Vlodavsky I, Berden JH, van der Vlag J. Reduction of anionic sites in the glomerular basement membrane by heparanase does not lead to proteinuria. Kidney Int 73: 278–287, 2008
106. van Kuppevelt TH, Jenniskens GJ, Veerkamp JH, ten Dam GB, Dennissen MA. Phage display technology to obtain antiheparan sulfate antibodies. Methods Mol Biol 171: 519–534, 2001
107. Vink H, Constantinescu AA, Spaan JA. Oxidized lipoproteins degrade the endothelial surface layer: implications for platelet-endothelial cell adhesion. Circulation 101: 1500–1502, 2000
108. Vink H, Duling BR. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ Res 79: 581–589, 1996
109. Vlahu CA, Lemkes BA, Struijk DG, Koopman MG, Krediet RT, Vink H. Damage of the endothelial glycocalyx in dialysis patients. J Am Soc Nephrol 23: 1900–1908, 2012
110. Vogel J, Sperandio M, Pries AR, Linderkamp O, Gaehtgens P, Kuschinsky W. Influence of the endothelial glycocalyx on cerebral blood flow in mice. J Cereb Blood Flow Metab 20: 1571–1578, 2000
111. Wang L, Fuster M, Sriramarao P, Esko JD. Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat Immunol 6: 902–910, 2005
112. Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9: 121–167, 2007
113. Weinbaum S, Zhang X, Han Y, Vink H, Cowin SC. Mechanotransduction and flow across the endothelial glycocalyx. Proc Natl Acad Sci USA 100: 7988–7995, 2003
114. Wuillemin WA, te Velthuis H, Lubbers YT, de Ruig CP, Eldering E, Hack CE. Potentiation of C1 inhibitor by glycosaminoglycans: dextran sulfate species are effective inhibitors of in vitro complement activation in plasma. J Immunol 159: 1953–1960, 1997
115. Ye J, Esmon CT, Johnson AE. The chondroitin sulfate moiety of thrombomodulin binds a second molecule of thrombin. J Biol Chem 268: 2373–2379, 1993
116. Yung S, Thomas GJ, Davies M. Induction of hyaluronan metabolism after mechanical injury of human peritoneal mesothelial cells in vitro. Kidney Int 58: 1953–1962, 2000
117. Zeng Y, Ebong EE, Fu BM, Tarbell JM. The structural stability of the endothelial glycocalyx after enzymatic removal of glycosaminoglycans. PloS One 7: e43168, 2012
118. Zeng Y, Waters M, Andrews A, Honarmandi P, Ebong EE, Rizzo V, Tarbell JM. Fluid shear stress induces the clustering of heparan sulfate via mobility of glypican-1 in lipid rafts. Am J Physiol Heart Circ Physiol 305: H811–H820, 2013.