Reactive Oxygen Species Modulate the Barrier Function of the Human Glomerular Endothelial Glycocalyx

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Singh, Anurag ^a,b   Ramnath, Raina D ^a   Foster, Rebecca R ^a   Wylie, Emma C ^a   Fridén, Vincent ^c   Dasgupta, Ishita ^a   Haraldsson, Borje ^c   Welsh, Gavin I ^a   Mathieson, Peter W ^a   Satchell, Simon C ^a  

^a SOUTHMEAD HOSPITAL   (United Kingdom)

^b Chilliwack General Hospital   (Canada)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CATALASE; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HYDROGEN PEROXIDE; LECTIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; ALBUMINOID; WHEAT GERM AGGLUTININ;

ARTICLE; CARBOHYDRATE SYNTHESIS; CELL FUNCTION; CELL IMMORTALIZATION; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME INHIBITION; GLOMERULAR FILTRATION BARRIER; GLYCOCALYX; HUMAN; HUMAN CELL; QUANTITATIVE ANALYSIS; CELL LINE; CELL SURVIVAL; GLOMERULUS; METABOLISM;

ALBUMINS; CELL LINE; CELL SURVIVAL; ENDOTHELIAL CELLS; GLYCOCALYX; GLYCOSAMINOGLYCANS; HUMANS; KIDNEY GLOMERULUS; REACTIVE OXYGEN SPECIES; WHEAT GERM AGGLUTININS;

EID: 84874005376     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055852     Document Type: Article

References (39)

1. Franco M, Cooper RS, Bilal U, Fuster V, (2011) Challenges and opportunities for cardiovascular disease prevention. Am J Med 124: 95-102.
2. Stehouwer CD, Smulders YM, (2006) Microalbuminuria and risk for cardiovascular disease: Analysis of potential mechanisms. J Am Soc Nephrol 17: 2106-2111.
3. Amann K, Wanner C, Ritz E, (2006) Cross-talk between the kidney and the cardiovascular system. J Am Soc Nephrol 17: 2112-2119.
4. Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, et al. (2001) Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 286: 421-426.
5. Satchell SC, Tooke JE, (2008) What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia 51: 714-725.
6. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H, (2003) Role of oxidative stress in atherosclerosis. Am J Cardiol 91: 7A-11A.
7. Harrison DG, Cai H, Landmesser U, Griendling KK, (2003) Interactions of angiotensin II with. J Renin Angiotensin Aldosterone Syst 4: 51-61.
8. Forbes JM, Coughlan MT, Cooper ME, (2008) Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 57: 1446-1454.
9. Brenner BM, Bohrer MP, Baylis C, Deen WM, (1977) Determinants of glomerular permselectivity: Insights derived from observations in vivo. Kidney Int 12: 229-237.
10. Deen WM, Lazzara MJ, Myers BD, (2001) Structural determinants of glomerular permeability. Am J Physiol Renal Physiol 281: F579-596.
11. Haraldsson B, Nystrom J, Deen WM, (2008) Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 88: 451-487.
12. Satchell SC, Tasman CH, Singh A, Ni L, Geelen J, et al. (2006) Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF. Kidney Int 69: 1633-1640.
13. Ballermann BJ, Stan RV, (2007) Resolved: capillary endothelium is a major contributor to the glomerular filtration barrier. J Am Soc Nephrol 18: 2432-2438.
14. Singh A, Satchell SC, Neal CR, McKenzie EA, Tooke JE, et al. (2007) Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol 18: 2885-2893.
15. Satchell SC, Braet F, (2009) Glomerular endothelial cell fenestrations: an integral component of the glomerular filtration barrier. Am J Physiol Renal Physiol 296: F947-956.
16. Jeansson M, Haraldsson B, (2006) Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. Am J Physiol Renal Physiol 290: F111-116.
17. Hjalmarsson C, Johansson BR, Haraldsson B, (2004) Electron microscopic evaluation of the endothelial surface layer of glomerular capillaries. Microvasc Res 67: 9-17.
18. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG, (2007) The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch 454: 345-359.
19. Mulivor AW, Lipowsky HH, (2004) Inflammation- and ischemia-induced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol 286: H1672-1680.
20. Henry CB, Duling BR, (2000) TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 279: H2815-2823.
21. Moseley R, Waddington RJ, Embery G, (1997) Degradation of glycosaminoglycans by reactive oxygen species derived from stimulated polymorphonuclear leukocytes. Biochim Biophys Acta 1362: 221-231.
22. Adachi T, Fukushima T, Usami Y, Hirano K, (1993) Binding of human xanthine oxidase to sulphated glycosaminoglycans on the endothelial-cell surface. Biochem J 289 (Pt 2): 523-527.
23. Becker M, Menger MD, Lehr HA, (1994) Heparin-released superoxide dismutase inhibits postischemic leukocyte adhesion to venular endothelium. Am J Physiol 267: H925-930.
24. Shasby DM, Lind SE, Shasby SS, Goldsmith JC, Hunninghake GW, (1985) Reversible oxidant-induced increases in albumin transfer across cultured endothelium: alterations in cell shape and calcium homeostasis. Blood 65: 605-614.
25. Kevil CG, Ohno N, Gute DC, Okayama N, Robinson SA, et al. (1998) Role of cadherin internalization in hydrogen peroxide-mediated endothelial permeability. Free Radic Biol Med 24: 1015-1022.
26. Siflinger-Birnboim A, Lum H, Del Vecchio PJ, Del Vecchio PJ, Malik AB, (1996) Involvement of Ca2+ in the H2O2-induced increase in endothelial permeability. Am J Physiol 270: L973-978.
27. Rops AL, van der Vlag J, Lensen JF, Wijnhoven TJ, van den Heuvel LP, et al. (2004) Heparan sulfate proteoglycans in glomerular inflammation. Kidney Int 65: 768-785.
28. Moseley R, Waddington R, Evans P, Halliwell B, Embery G, (1995) The chemical modification of glycosaminoglycan structure by oxygen-derived species in vitro. Biochim Biophys Acta 1244: 245-252.
29. Edge AS, Spiro RG, (2000) A specific structural alteration in the heparan sulphate of human glomerular basement membrane in diabetes. Diabetologia 43: 1056-1059.
30. Halliwell B, Clement MV, Long LH, (2000) Hydrogen peroxide in the human body. FEBS Lett 486: 10-13.
31. Witting PK, Rayner BS, Wu BJ, Ellis NA, Stocker R, (2007) Hydrogen peroxide promotes endothelial dysfunction by stimulating multiple sources of superoxide anion radical production and decreasing nitric oxide bioavailability. Cell Physiol Biochem 20: 255-268.
32. Yoshioka T, Ichikawa I, Fogo A, (1991) Reactive oxygen metabolites cause massive, reversible proteinuria and glomerular sieving defect without apparent ultrastructural abnormality. J Am Soc Nephrol 2: 902-912.
33. Andersson M, Nilsson U, Hjalmarsson C, Haraldsson B, Nyström JS, (2007) Mild renal ischemia-reperfusion reduces charge and size selectivity of the glomerular barrier. Am J Physiol Renal Physiol 292: F1802-1809.
34. Tay M, Comper WD, Vassiliou P, Glasgow EF, Baker MS, et al. (1990) The inhibitory action of oxygen radical scavengers on proteinuria and glomerular heparan sulphate loss in the isolated perfused kidney. Biochem Int 20: 767-778.
35. Raats CJ, Bakker MA, van den Born J, Berden JH, (1997) Hydroxyl radicals depolymerize glomerular heparan sulfate in vitro and in experimental nephrotic syndrome. J Biol Chem 272: 26734-26741.
36. Foley RN, Parfrey PS, Sarnak MJ, (1998) Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J Kidney Dis 32: S112-119.
37. Ysebaert DK, De Greef KE, Vercauteren SR, Ghielli M, Verpooten GA, et al. (2000) Identification and kinetics of leukocytes after severe ischaemia/reperfusion renal injury. Nephrol Dial Transplant 15: 1562-1574.
38. Granger DN, Hollwarth ME, Parks DA (1986) Ischemia-reperfusion injury: role of oxygen-derived free radicals. Acta Physiol Scand Suppl 548: 47-63.
39. Alonso de Vega JM, Diaz J, Serrano E, Carbonell LF, (2002) Oxidative stress in critically ill patients with systemic inflammatory response syndrome. Crit Care Med 30: 1782-1786.