Modulation of endothelial glycocalyx structure under inflammatory conditions

. 2014 ; 2014 () : 694312. [epub] 20140403

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid24803742

The glycocalyx of the endothelium is an intravascular compartment that creates a barrier between circulating blood and the vessel wall. The glycocalyx is suggested to play an important role in numerous physiological processes including the regulation of vascular permeability, the prevention of the margination of blood cells to the vessel wall, and the transmission of shear stress. Various theoretical models and experimental approaches provide data about changes to the structure and functions of the glycocalyx under various types of inflammatory conditions. These alterations are suggested to promote inflammatory processes in vessels and contribute to the pathogenesis of number of diseases. In this review we summarize current knowledge about the modulation of the glycocalyx under inflammatory conditions and the consequences for the course of inflammation in vessels. The structure and functions of endothelial glycocalyx are briefly discussed in the context of methodological approaches regarding the determination of endothelial glycocalyx and the uncertainty and challenges involved in glycocalyx structure determination. In addition, the modulation of glycocalyx structure under inflammatory conditions and the possible consequences for pathogenesis of selected diseases and medical conditions (in particular, diabetes, atherosclerosis, ischemia/reperfusion, and sepsis) are summarized. Finally, therapeutic strategies to ameliorate glycocalyx dysfunction suggested by various authors are discussed.

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Gouverneur M, van den Berg B, Nieuwdorp M, Stroes E, Vink H. Vasculoprotective properties of the endothelial glycocalyx: effects of fluid shear stress. Journal of Internal Medicine. 2006;259(4):393–400. PubMed

Reitsma S, Slaaf DW, Vink H, van Zandvoort MAMJ, Oude Egbrink MGA. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Archiv European Journal of Physiology. 2007;454(3):345–359. PubMed PMC

Tarbell JM, Weinbaum S, Kamm RD. Cellular fluid mechanics and mechanotransduction. Annals of Biomedical Engineering. 2005;33(12):1719–1723. PubMed

VanTeeffelen JW, Brands J, Stroes ES, Vink H. Endothelial glycocalyx: sweet shield of blood vessels. Trends in Cardiovascular Medicine. 2007;17(3):101–105. PubMed

Becker BF, Chappell D, Bruegger D, Annecke T, Jacob M. Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential. Cardiovascular Research. 2010;87(2):300–310. PubMed

Becker BF, Chappell D, Jacob M. Endothelial glycocalyx and coronary vascular permeability: the fringe benefit. Basic Research in Cardiology. 2010;105(6):687–701. PubMed

Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflugers Archiv European Journal of Physiology. 2000;440(5):653–666. PubMed

van den Berg B, Vink H. Glycocalyx perturbation: cause or consequence of damage to the vasculature? American Journal of Physiology: Heart and Circulatory Physiology. 2006;290(6):H2174–H2175. PubMed

van den Berg BM, Nieuwdorp M, Stroes ESG, Vink H. Glycocalyx and endothelial (dys) function: from mice to men. Pharmacological Reports. 2006;58:75–80. PubMed

Curry FE, Adamson RH. Endothelial glycocalyx: permeability barrier and mechanosensor. Annals of Biomedical Engineering. 2012;40:828–839. PubMed PMC

Tarbell JM, Pahakis MY. Mechanotransduction and the glycocalyx. Journal of Internal Medicine. 2006;259(4):339–350. PubMed

Alexopoulou AN, Multhaupt HAB, Couchman JR. Syndecans in wound healing, inflammation and vascular biology. International Journal of Biochemistry and Cell Biology. 2007;39(3):505–528. PubMed

Fears CY, Woods A. The role of syndecans in disease and wound healing. Matrix Biology. 2006;25(7):443–456. PubMed

Tkachenko E, Rhodes JM, Simons M. Syndecans: new kids on the signaling block. Circulation Research. 2005;96(5):488–500. PubMed

De Cat B, David G. Developmental roles of the glypicans. Seminars in Cell and Developmental Biology. 2001;12(2):117–125. PubMed

Maksimenko AV, Turashev AD. No-reflow phenomenon and endothelial glycocalyx of microcirculation. Biochemistry Research International. 2012;2012:10 pages.859231 PubMed PMC

Moreth K, Iozzo RV, Schaefer L. Small leucine-rich proteoglycans orchestrate receptor crosstalk during inflammation. Cell Cycle. 2012;11:2084–2091. PubMed PMC

Chen S, Birk DE. The regulatory roles of small leucine-rich proteoglycans in extracellular matrix assembly. FEBS Journal. 2013;280:2120–2137. PubMed PMC

Nastase MV, Young MF, Schaefer L. Biglycan: a multivalent proteoglycan providing structure and signals. Journal of Histochemistry & Cytochemistry. 2012;60:963–975. PubMed PMC

Gandhi NS, Mancera RL. The structure of glycosaminoglycans and their interactions with proteins. Chemical Biology and Drug Design. 2008;72(6):455–482. PubMed

Götte M. Syndecans in inflammation. The FASEB Journal. 2003;17(6):575–591. PubMed

Xian X, Gopal S, Couchman JR. Syndecans as receptors and organizers of the extracellular matrix. Cell and Tissue Research. 2010;339(1):31–46. PubMed

Mikami T, Kitagawa H. Biosynthesis and function of chondroitin sulfate. Biochimica et Biophysica Acta. 2013;1830:4719–4733. PubMed

Kwok JCF, Warren P, Fawcett JW. Chondroitin sulfate: a key molecule in the brain matrix. International Journal of Biochemistry and Cell Biology. 2012;44(4):582–586. PubMed

Lennon FE, Singleton PA. Hyaluronan regulation of vascular integrity. American Journal of Cardiovascular Disease. 2011;1:200–213. PubMed PMC

Takagi J. Structural basis for ligand recognition by integrins. Current Opinion in Cell Biology. 2007;19(5):557–564. PubMed

Ehrhardt C, Kneuer C, Bakowsky U. Selectins—an emerging target for drug delivery. Advanced Drug Delivery Reviews. 2004;56(4):527–549. PubMed

Jubeli E, Moine L, Vergnaud-Gauduchon J, Barratt G. E-selectin as a target for drug delivery and molecular imaging. Journal of Controlled Release. 2012;158(2):194–206. PubMed

Luo B-H, Springer TA. Integrin structures and conformational signaling. Current Opinion in Cell Biology. 2006;18(5):579–586. PubMed PMC

Nieuwdorp M, Meuwese MC, Vink H, Hoekstra JBL, Kastelein JJP, Stroes ESG. The endothelial glycocalyx: a potential barrier between health and vascular disease. Current Opinion in Lipidology. 2005;16(5):507–511. PubMed

Ebong EE, MacAluso FP, Spray DC, Tarbell JM. Imaging the endothelial glycocalyx in vitro by rapid freezing/freeze substitution transmission electron microscopy. Arteriosclerosis, Thrombosis, and Vascular Biology. 2011;31(8):1908–1915. PubMed PMC

Luft JH. Fine structures of capillary and endocapillary layer as revealed by ruthenium red. Federation Proceedings. 1966;25(6):1773–1783. PubMed

Janczyk P, Hansen S, Bahramsoltani M, Plendl J. The glycocalyx of human, bovine and murine microvascular endothelial cells cultured in vitro. Journal of Electron Microscopy. 2010;59(4):291–298. PubMed

Ueda A, Shimomura M, Ikeda M, Yamaguchi R, Tanishita K. Effect of glycocalyx on shear-dependent albumin uptake in endothelial cells. American Journal of Physiology: Heart and Circulatory Physiology. 2004;287(5):H2287–H2294. PubMed

Devaraj S, Yun J-M, Adamson G, Galvez J, Jialal I. C-reactive protein impairs the endothelial glycocalyx resulting in endothelial dysfunction. Cardiovascular Research. 2009;84(3):479–484. PubMed PMC

Chappell D, Jacob M, Paul O, et al. The glycocalyx of the human umbilical vein endothelial cell: an impressive structure ex vivo but not in culture. Circulation Research. 2009;104(11):1313–1317. PubMed

Vogel J, Sperandio M, Pries AR, Linderkamp O, Gaehtgens P, Kuschinsky W. Influence of the endothelial glycocalyx on cerebral blood flow in mice. Journal of Cerebral Blood Flow and Metabolism. 2000;20(11):1571–1578. PubMed

Singh A, Satchell SC, Neal CR, McKenzie EA, Tooke JE, Mathieson PW. Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. Journal of the American Society of Nephrology. 2007;18(11):2885–2893. PubMed

van den Berg BM, Vink H, Spaan JAE. The endothelial glycocalyx protects against myocardial edema. Circulation Research. 2003;92(6):592–594. PubMed

van den Berg BM, Spaan JAE, Vink H. Impaired glycocalyx barrier properties contribute to enhanced intimal low-density lipoprotein accumulation at the carotid artery bifurcation in mice. Pflugers Archiv European Journal of Physiology. 2009;457(6):1199–1206. PubMed

Rostgaard J, Qvortrup K, Poulsen SS. Improvements in the technique of vascular perfusion-fixation employing a fluorocarbon-containing perfusate and a peristaltic pump controlled by pressure feedback. Journal of Microscopy. 1993;172(2):137–151. PubMed

Sims DE, Horne MM. Non-aqueous fixative preserves macromolecules on the endothelial cell surface: an in situ study. European Journal of Morphology. 1993;31(4):251–256. PubMed

Reitsma S, Oude Egbrink MGA, Vink H, et al. Endothelial glycocalyx structure in the intact carotid artery: a two-photon laser scanning microscopy study. Journal of Vascular Research. 2011;48(4):297–306. PubMed

de Mesy Bentley KL. An 11-mum-thick glycocalyx?: it's all in the technique! Arteriosclerosis, Thrombosis, and Vascular Biology. 2011;31:1712–1713. PubMed

Savery MD, Jiang JX, Park PW, Damiano ER. The endothelial glycocalyx in syndecan-1 deficient mice. Microvascular Research. 2013;87:83–91. PubMed PMC

Vanteeffelen JWGE, Brands J, Vink H. Agonist-induced impairment of glycocalyx exclusion properties: contribution to coronary effects of adenosine. Cardiovascular Research. 2010;87(2):311–319. PubMed

Vink H, Duling BR. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circulation Research. 1996;79(3):581–589. PubMed

Vink H, Duling BR. Capillary endothelial surface layer selectively reduces plasma solute distribution volume. American Journal of Physiology: Heart and Circulatory Physiology. 2000;278(1):H285–H289. PubMed

Henry CBS, Duling BR. Permeation of the luminal capillary glycocalyx is determined by hyaluronan. American Journal of Physiology: Heart and Circulatory Physiology. 1999;277(2):H508–H514. PubMed

Gao L, Lipowsky Herbert H. HH. Composition of the endothelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvascular Research. 2010;80(3):394–401. PubMed PMC

Yen W-Y, Cai B, Zeng M, Tarbell JM, Fu BM. Quantification of the endothelial surface glycocalyx on rat and mouse blood vessels. Microvascular Research. 2012;83(3):337–346. PubMed PMC

Torres Filho I, Torres LN, Sondeen JL, Polykratis IA, Dubick MA. In vivo evaluation of venular glycocalyx during hemorrhagic shock in rats using intravital microscopy. Microvascular Research. 2013;85:128–133. PubMed

Potter DR, Damiano ER. The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro. Circulation Research. 2008;102(7):770–776. PubMed

Smith ML, Long DS, Damiano ER, Ley K. Near-wall μ-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo. Biophysical Journal. 2003;85(1):637–645. PubMed PMC

den Uil CA, Klijn E, Lagrand WK, et al. The microcirculation in health and critical disease. Progress in Cardiovascular Diseases. 2008;51(2):161–170. PubMed

Nieuwdorp M, Meuwese MC, Mooij HL, et al. Measuring endothelial glycocalyx dimensions in humans: a potential novel tool to monitor vascular vulnerability. Journal of Applied Physiology. 2008;104(3):845–852. PubMed

Nieuwdorp M, Meuwese MC, Mooij HL, et al. Tumor necrosis factor-α inhibition protects against endotoxin-induced endothelial glycocalyx perturbation. Atherosclerosis. 2009;202(1):296–303. PubMed

Vlahu CA, Lemkes BA, Struijk DG, et al. Damage of the endothelial glycocalyx in dialysis patients. Journal of the American Society of Nephrology. 2012;23:1900–1908. PubMed PMC

Barker KN, Flynn EA, Pepper GA. Observation method of detecting medication errors. American Journal of Health-System Pharmacy. 2002;59(23):2314–2316. PubMed

Megens RTA, Oude Egbrink MGA, Merkx M, Slaaf DW, van Zandvoort MAMJ. Two-photon microscopy on vital carotid arteries: imaging the relationship between collagen and inflammatory cells in atherosclerotic plaques. Journal of Biomedical Optics. 2008;13(4)044022 PubMed

Megens RTA, Reitsma S, Prinzen L, et al. In vivo high-resolution structural imaging of large arteries in small rodents using two-photon laser scanning microscopy. Journal of Biomedical Optics. 2010;15(1)011108 PubMed

Bai K, Wang W. Spatio-temporal development of the endothelial glycocalyx layer and its mechanical property in vitro. Journal of the Royal Society Interface. 2012;9(74):2290–2298. PubMed PMC

Potter DR, Jiang J, Damiano ER. The recovery time course of the endothelial cell glycocalyx in vivo and its implications in vitro. Circulation Research. 2009;104(11):1318–1325. PubMed PMC

Bai K, Wang W. Shear stress-induced redistribution of the glycocalyx on endothelial cells in vitro. Biomechanics and Modeling in Mechanobiology. 2013 PubMed

Yao Y, Rabodzey A, Dewey CF., Jr. Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress. American Journal of Physiology: Heart and Circulatory Physiology. 2007;293(2):H1023–H1030. PubMed

Rosenberg RD, Shworak NW, Liu J, Schwartz JJ, Zhang L. Heparan sulfate proteoglycans of the cardiovascular system: specific structures emerge but how is synthesis regulated? Journal of Clinical Investigation. 1997;100(11):S67–S75. PubMed

Chappell D, Hofmann-Kiefer K, Jacob M, et al. TNF-α induced shedding of the endothelial glycocalyx is prevented by hydrocortisone and antithrombin. Basic Research in Cardiology. 2009;104(1):78–89. PubMed

Chappell D, Jacob M, Hofmann-Kiefer K, et al. Antithrombin reduces shedding of the endothelial glycocalyx following ischaemia/reperfusion. Cardiovascular Research. 2009;83(2):388–396. PubMed

Henrich M, Gruss M, Weigand MA. Sepsis-induced degradation of endothelial glycocalix. TheScientificWorldJournal. 2010;10:917–923. PubMed PMC

van Golen RF, van Gulik TM, Heger M. Mechanistic overview of reactive species-induced degradation of the endothelial glycocalyx during hepatic ischemia/reperfusion injury. Free Radical Biology and Medicine. 2012;52(8):1382–1402. PubMed

Nieuwdorp M, Mooij HL, Kroon J, et al. Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes. Diabetes. 2006;55(4):1127–1132. PubMed

Nieuwdorp M, van Haeften TW, Gouverneur MCLG, et al. Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes. 2006;55(2):480–486. PubMed

Rehm M, Haller M, Orth V, et al. Changes in blood volume and hematocrit during acute preoperative volume loading with 5% albumin or 6% hetastarch solutions in patients before radical hysterectomy. Anesthesiology. 2001;95(4):849–856. PubMed

Perrin RM, Harper SJ, Bates DO. A role for the endothelial glycocalyx in regulating microvascular permeability in diabetes mellitus. Cell Biochemistry and Biophysics. 2007;49(2):65–72. PubMed PMC

Mulivor AW, Lipowsky HH. Role of glycocalyx in leukocyte-endothelial cell adhesion. American Journal of Physiology: Heart and Circulatory Physiology. 2002;283(4):H1282–H1291. PubMed

Lipowsky HH. The endothelial glycocalyx as a barrier to leukocyte adhesion and its mediation by extracellular proteases. Annals of Biomedical Engineering. 2012;40:840–848. PubMed PMC

Constantinescu AA, Vink H, Spaan JAE. Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arteriosclerosis, Thrombosis, and Vascular Biology. 2003;23(9):1541–1547. PubMed

Drake-Holland AJ, Noble MI. Update on the important new drug target in cardiovascular medicine—the vascular glycocalyx. Cardiovascular & Hematological Disorders-Drug Targets. 2012;12(1):76–81. PubMed

Broekhuizen LN, Mooij HL, Kastelein JJP, Stroes ESG, Vink H, Nieuwdorp M. Endothelial glycocalyx as potential diagnostic and therapeutic target in cardiovascular disease. Current Opinion in Lipidology. 2009;20(1):57–62. PubMed

Chappell D, Westphal M, Jacob M. The impact of the glycocalyx on microcirculatory oxygen distribution in critical illness. Current Opinion in Anaesthesiology. 2009;22(2):155–162. PubMed

Henry CBS, Duling BR. TNF-α increases entry of macromolecules into luminal endothelial cell glycocalyx. American Journal of Physiology: Heart and Circulatory Physiology. 2000;279(6):H2815–H2823. PubMed

Pejler G, Åbrink M, Ringvall M, Wernersson S. Mast Cell Proteases. Advances in Immunology. 2007;95:167–255. PubMed

Chappell D, Jacob M, Hofmann-Kiefer K, et al. Hydrocortisone preserves the vascular barrier by protecting the endothelial glycocalyx. Anesthesiology. 2007;107(5):776–784. PubMed

Chappell D, Jacob M, Rehm M, et al. Heparinase selectively sheds heparan sulphate from the endothelial glycocalyx. Biological Chemistry. 2008;389(1):79–82. PubMed

Singh A, Ramnath RD, Foster RR, et al. Reactive oxygen species modulate the barrier function of the human glomerular endothelial glycocalyx. PLoS ONE. 2013;8e55852 PubMed PMC

Lipowsky HH. Protease activity and the role of the endothelial glycocalyx in inflammation. Drug Discovery Today: Disease Models. 2011;8(1):57–62. PubMed PMC

Lipowsky HH, Lescanic A. The effect of doxycycline on shedding of the glycocalyx due to reactive oxygen species. Microvascular Research. 2013;90:80–85. PubMed PMC

Mulivor AW, Lipowsky HH. Inhibition of glycan shedding and leukocyte-endothelial adhesion in postcapillary venules by suppression of matrixmetalloprotease activity with doxycycline. Microcirculation. 2009;16(8):657–666. PubMed

Yu W-H, Woessner JF., Jr. Heparan sulfate proteoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7) The Journal of Biological Chemistry. 2000;275(6):4183–4191. PubMed

Endo K, Takino T, Miyamori H, et al. Cleavage of Syndecan-1 by Membrane Type Matrix Metalloproteinase-1 Stimulates Cell Migration. The Journal of Biological Chemistry. 2003;278(42):40764–40770. PubMed

Gronski TJ, Jr., Martin RL, Kobayashi DK, et al. Hydrolysis of a broad spectrum of extracellular matrix proteins by human macrophage elastase. The Journal of Biological Chemistry. 1997;272(18):12189–12194. PubMed

Suenaga N, Mori H, Itoh Y, Seiki M. CD44 binding through the hemopexin-like domain is critical for its shedding by membrane-type 1 matrix metalloproteinase. Oncogene. 2005;24(5):859–868. PubMed

Mulivor AW, Lipowsky HH. Inflammation- and ischemia-induced shedding of venular glycocalyx. American Journal of Physiology: Heart and Circulatory Physiology. 2004;286(5):H1672–H1680. PubMed

Constantinescu AA, Vink H, Spaan JAE. Elevated capillary tube hematocrit reflects degradation of endothelial cell glycocalyx by oxidized LDL. American Journal of Physiology: Heart and Circulatory Physiology. 2001;280(3):H1051–H1057. PubMed

Vink H, Constantinescu AA, Spaan JAE. Oxidized lipoproteins degrade the endothelial surface layer: implications for platelet-endothelial cell adhesion. Circulation. 2000;101(13):1500–1502. PubMed

Colburn P, Kobayashi E, Buonassisi V. Depleted level of heparan sulfate proteoglycan in the extracellular matrix of endothelial cell cultures exposed to endotoxin. Journal of Cellular Physiology. 1994;159(1):121–130. PubMed

Huxley VH, Williams DA. Role of a glycocalyx on coronary arteriole permeability to proteins: evidence from enzyme treatments. American Journal of Physiology: Heart and Circulatory Physiology. 2000;278(4):H1177–H1185. PubMed

Jeansson M, Granqvist AB, Nyström JS, Haraldsson B. Functional and molecular alterations of the glomerular barrier in long-term diabetes in mice. Diabetologia. 2006;49(9):2200–2209. PubMed

Jeansson M, Haraldsson B. Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. American Journal of Physiology: Renal Physiology. 2006;290(1):F111–F116. PubMed

Mochizuki S, Vink H, Hiramatsu O, et al. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. American Journal of Physiology: Heart and Circulatory Physiology. 2003;285(2):H722–H726. PubMed

VanTeeffelen JWGE, Brands J, Jansen C, Spaan JAE, Vink H. Heparin impairs glycocalyx barrier properties and attenuates shear dependent vasodilation in mice. Hypertension. 2007;50(1):261–267. PubMed

Bernfield M, Götte M, Park PW, et al. Functions of cell surface heparan sulfate proteoglycans. Annual Review of Biochemistry. 1999;68:729–777. PubMed

Termeer CC, Hennies J, Voith U, et al. Oligosaccharides of hyaluronan are potent activators of dendritic cells. Journal of Immunology. 2000;165(4):1863–1870. PubMed

Nelson A, Berkestedt I, Schmidtchen A, Ljunggren L, Bodelsson M. Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma. Shock. 2008;30(6):623–627. PubMed

Onat D, Brillon D, Colombo PC, Schmidt AM. Human vascular endothelial cells: a model system for studying vascular inflammation in diabetes and atherosclerosis. Current Diabetes Reports. 2011;11(3):193–202. PubMed PMC

Salmon AH, Satchell SC. Endothelial glycocalyx dysfunction in disease: albuminuria and increased microvascular permeability. Journal of Pathology. 2012;226(4):562–574. PubMed

Yuan SY, Ustinova EE, Wu MH, et al. Protein kinase C activation contributes to microvascular barrier dysfunction in the heart at early stages of diabetes. Circulation Research. 2000;87(5):412–417. PubMed

Zuurbier CJ, Demirci C, Koeman A, Vink H, Ince C. Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells. Journal of Applied Physiology. 2005;99(4):1471–1476. PubMed

Kelly R, Ruane-O’Hora T, Noble MIM, Drake-Holland AJ, Snow HM. Differential inhibition by hyperglycaemia of shear stress- but not acetylcholine-mediated dilatation in the iliac artery of the anaesthetized pig. Journal of Physiology. 2006;573(1):133–145. PubMed PMC

Title LM, Cummings PM, Giddens K, Nassar BA. Oral glucose loading acutely attenuates endothelium-dependent vasodilation in healthy adults without diabetes: an effect prevented by vitamins C and E. Journal of the American College of Cardiology. 2000;36(7):2185–2191. PubMed

Deckert T, Kofoed-Enevoldsen A, Vidal P, Norgaard K, Andreasen HB, Feldt-Rasmussen B. Size- and charge selectivity of glomerular filtration in Type 1 (insulin-dependent) diabetic patients with and without albuminuria. Diabetologia. 1993;36(3):244–251. PubMed

Broekhuizen LN, Lemkes BA, Mooij HL, et al. Effect of sulodexide on endothelial glycocalyx and vascular permeability in patients with type 2 diabetes mellitus. Diabetologia. 2010;53(12):2646–2655. PubMed PMC

Singh A, Fridén V, Dasgupta I, et al. High glucose causes dysfunction of the human glomerular endothelial glycocalyx. American Journal of Physiology: Renal Physiology. 2011;300(1):F40–F48. PubMed PMC

Nieuwdorp M, Holleman F, De Groot E, et al. Perturbation of hyaluronan metabolism predisposes patients with type 1 diabetes mellitus to atherosclerosis. Diabetologia. 2007;50(6):1288–1293. PubMed PMC

Adamson RH, Zeng M, Adamson GN, Lenz JF, Curry FE. PAF- and bradykinin-induced hyperpermeability of rat venules is independent of actin-myosin contraction. American Journal of Physiology: Heart and Circulatory Physiology. 2003;285(1):H406–H417. PubMed

Satchell SC, Tooke JE. What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia. 2008;51(5):714–725. PubMed PMC

Nagy N, Freudenberger T, Melchior-Becker A, et al. Inhibition of hyaluronan synthesis accelerates murine atherosclerosis: novel insights into the role of hyaluronan synthesis. Circulation. 2010;122(22):2313–2322. PubMed

van den Berg BM, Spaan JAE, Rolf TM, Vink H. Atherogenic region and diet diminish glycocalyx dimension and increase intima-to-media ratios at murine carotid artery bifurcation. American Journal of Physiology: Heart and Circulatory Physiology. 2006;290(2):H915–H920. PubMed

van Haaren PMA, VanBavel E, Vink H, Spaan JAE. Localization of the permeability barrier to solutes in isolated arteries by confocal microscopy. American Journal of Physiology: Heart and Circulatory Physiology. 2003;285(6):H2848–H2856. PubMed

Caro CG, Fitz-Gerald JM, Schroter RC. Arterial wall shear and distribution of early atheroma in man. Nature. 1969;223(5211):1159–1161. PubMed

Rubio-Gayosso I, Platts SH, Duling BR. Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. American Journal of Physiology: Heart and Circulatory Physiology. 2006;290(6):H2247–H2256. PubMed

Bruegger D, Rehm M, Jacob M, et al. Exogenous nitric oxide requires an endothelial glycocalyx to prevent postischemic coronary vascular leak in guinea pig hearts. Critical Care. 2008;12(3, article R73) PubMed PMC

Bruegger D, Rehm M, Abicht J, et al. Shedding of the endothelial glycocalyx during cardiac surgery: on-pump versus off-pump coronary artery bypass graft surgery. Journal of Thoracic and Cardiovascular Surgery. 2009;138(6):1445–1447. PubMed

Rehm M, Bruegger D, Christ F, et al. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation. 2007;116(17):1896–1906. PubMed

Schmidt EP, Yang Y, Janssen WJ, et al. The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nature Medicine. 2012;18:1217–1223. PubMed PMC

Marechal X, Favory R, Joulin O, et al. Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress. Shock. 2008;29(5):572–576. PubMed

Hayashida K, Parks WC, Pyong WP. Syndecan-1 shedding facilitates the resolution of neutrophilic inflammation by removing sequestered CXC chemokines. Blood. 2009;114(14):3033–3043. PubMed PMC

Donati A, Damiani E, Domizi R, et al. Alteration of the sublingual microvascular glycocalyx in critically ill patients. Microvascular Research. 2013;90:86–89. PubMed

Sallisalmi M, Tenhunen J, Yang R, Oksala N, Pettilä V. Vascular adhesion protein-1 and syndecan-1 in septic shock. Acta Anaesthesiologica Scandinavica. 2012;56(3):316–322. PubMed

Steppan J, Hofer S, Funke B, et al. Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix. Journal of Surgical Research. 2011;165(1):136–141. PubMed

Johansson PI, Stensballe J, Rasmussen LS, Ostrowski SR. A high admission syndecan-1 Level, a marker of endothelial glycocalyx degradation, is associated with inflammation, protein C depletion, fibrinolysis, and increased mortality in trauma patients. Annals of Surgery. 2011;254(2):194–200. PubMed

Ostrowski SR, Sorensen AM, Windelov NA, et al. High levels of soluble VEGF receptor 1 early after trauma are associated with shock, sympathoadrenal activation, glycocalyx degradation and inflammation in severely injured patients: a prospective study. Scandinavian Journal of Trauma, Resuscitation and Emergency Medicine. 2012;20, article 27 PubMed PMC

Hiebert LM, Jaques LB. The observation of heparin on endothelium after injection. Thrombosis Research. 1976;8(2):195–204. PubMed

Gambaro G, Venturini AP, Noonan DM, et al. Treatment with a glycosaminoglycan formulation ameliorates experimental diabetic nephropathy. Kidney International. 1994;46(3):797–806. PubMed

Achour A, Kacem M, Dibej K, Skhiri H, Bouraoui S, El May M. One year course of oral sulodexide in the management of diabetic nephropathy. Journal of Nephrology. 2005;18(5):568–574. PubMed

Lauver DA, Booth EA, White AJ, Poradosu E, Lucchesi BR. Sulodexide attenuates myocardial ischemia/reperfusion injury and the deposition of C-reactive protein in areas of infarction without affecting hemostasis. Journal of Pharmacology and Experimental Therapeutics. 2005;312(2):794–800. PubMed

Myrup B, Yokoyama H, Kristiansen OP, Østergaard PB, Olivecrona T. Release of endothelium-associated protein into blood by injection of heparin in normal subjects and in patients with Type 1 diabetes. Diabetic Medicine. 2004;21(10):1135–1140. PubMed

Jacob M, Paul O, Mehringer L, et al. Albumin augmentation improves condition of guinea pig hearts after 4 hr of cold ischemia. Transplantation. 2009;87(7):956–965. PubMed

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. 2006;104(6):1223–1231. PubMed

Czarnowska E, Karwatowska-Prokopczuk E. Ultrastructural demonstration of endothelial glycocalyx disruption in the reperfused rat heart. Involvement of oxygen free radicals. Basic Research in Cardiology. 1995;90(5):357–364. PubMed

Subramanian SV, Fitzgerald ML, Bernfield M. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. The Journal of Biological Chemistry. 1997;272(23):14713–14720. PubMed

Chappell D, Dörfler N, Jacob M, et al. Glycocalyx protection reduces leukocyte adhesion after ischemia/reperfusion. Shock. 2010;34(2):133–139. PubMed

Kilger E, Weis F, Briegel J, et al. Stress doses of hydrocortisone reduce severe systemic inflammatory response syndrome and improve early outcome in a risk group of patients after cardiac surgery. Critical Care Medicine. 2003;31(4):1068–1074. PubMed

Chappell D, Heindl B, Jacob M, et al. Sevoflurane reduces leukocyte and platelet adhesion after ischemia-reperfusion by protecting the endothelial glycocalyx. Anesthesiology. 2011;115(3):483–491. PubMed

Annecke T, Chappell D, Chen C, et al. Sevoflurane preserves the endothelial glycocalyx against ischaemia-reperfusion injury. British Journal of Anaesthesia. 2010;104(4):414–421. PubMed

Annecke T, Rehm M, Bruegger D, et al. Ischemia-reperfusion-induced unmeasured anion generation and glycocalyx shedding: sevoflurane versus propofol anesthesia. Journal of Investigative Surgery. 2012;25(3):162–168. PubMed

Wacker J, Lucchinetti E, Jamnicki M, et al. Delayed inhibition of agonist-induced granulocyte-platelet aggregation after low-dose sevoflurane inhalation in humans. Anesthesia and Analgesia. 2008;106(6):1749–1758. PubMed

Lucchinetti E, Aguirre J, Feng J, et al. Molecular evidence of late preconditioning after sevoflurane inhalation in healthy volunteers. Anesthesia and Analgesia. 2007;105(3):629–640. PubMed

Lucchinetti E, Ambrosio S, Aguirre J, et al. Sevoflurane inhalation at sedative concentrations provides endothelial protection against ischemia-reperfusion injury in humans. Anesthesiology. 2007;106(2):262–268. PubMed

De Klaver MJM, Buckingham M-G, Rich GF. Isoflurane pretreatment has immediate and delayed protective effects against cytokine-induced injury in endothelial and vascular smooth muscle cells. Anesthesiology. 2003;99(4):896–903. PubMed

Meuwese MC, Mooij HL, Nieuwdorp M, et al. Partial recovery of the endothelial glycocalyx upon rosuvastatin therapy in patients with heterozygous familial hypercholesterolemia. Journal of Lipid Research. 2009;50(1):148–153. PubMed

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