High glucose causes dysfunction of the human glomerular endothelial glycocalyx

American Journal of Physiology - Renal Physiology

Volumn 300, Issue 1, 2011, Pages

  Singh, A ^a   Friden V ^b   Dasgupta, I ^a   Foster, R R ^a   Welsh, G I ^a   Tooke, J E ^c   Haraldsson, B ^b   Mathieson, P W ^a   Satchell, S C ^a  

^a SOUTHMEAD HOSPITAL   (United Kingdom)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c PLYMOUTH UNIVERSITY PENINSULA SCHOOLS OF MEDICINE AND DENTISTRY   (United Kingdom)

Author keywords

Glycosaminoglycan; Heparan sulfate; Proteinuria; Proteoglycans

Indexed keywords

ALBUMIN; GLUCOSE; GLYCOSAMINOGLYCAN; GLYPICAN 1; HEPARAN SULFATE; PERLECAN; PROTEOGLYCAN; SYNDECAN 1; SYNDECAN 4; VERSICAN;

ARTICLE; CELL JUNCTION; CELL STRUCTURE; CELL SURVIVAL; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; GLOMERULUS; GLYCOCALYX; GLYCOSAMINOGLYCAN METABOLISM; HUMAN; HUMAN CELL; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT;

EID: 78651323207     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00103.2010     Document Type: Article

References (47)

1. Albelda SM, Sampson PM, Haselton FR, McNiff JM, Mueller SN, Williams SK, Fishman AP, Levine EM. Permeability characteristics of cultured endothelial cell monolayers. J Appl Physiol 64: 308-322, 1988. (Pubitemid 18042249)
2. Amann K, Wanner C, Ritz E. Cross-talk between the kidney and the cardiovascular system. J Am Soc Nephrol 17: 2112-2119, 2006.
3. Ballermann BJ, Stan RV. Resolved: capillary endothelium is a major contributor to the glomerular filtration barrier. J Am Soc Nephrol 18: 2432-2438, 2007.
4. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68: 729-777, 1999. (Pubitemid 29449208)
5. Bjornson A, Moses J, Ingemansson A, Haraldsson B, Sorensson J. Primary human glomerular endothelial cells produce proteoglycans, and puromycin affects their posttranslational modification. Am J Physiol Renal Physiol 288: F748-F756, 2005.
6. Chen S, Wassenhove-McCarthy DJ, Yamaguchi Y, Holzman LB, van Kuppevelt TH, Jenniskens GJ, Wijnhoven TJ, Woods AC, McCarthy KJ. Loss of heparan sulfate glycosaminoglycan assembly in podocytes does not lead to proteinuria. Kidney Int 74: 289-299, 2008.
7. Deckert T, Feldt-Rasmussen B, Borch-Johnsen K, Jensen T, Kofoed-Enevoldsen A. Albuminuria reflects widespread vascular damage. The Steno hypothesis. Diabetologia 32: 219-226, 1989.
8. 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 36: 244-251, 1993.
9. Deen WM, Lazzara MJ, Myers BD. Structural determinants of glomerular permeability. Am J Physiol Renal Physiol 281: F579-F596, 2001.
10. Dejana E. Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol 5: 261-270, 2004.
11. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111: 707-716, 2003.
12. Esko JD, Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest 108: 169-173, 2001.
13. Foster RR, Slater SC, Seckley J, Kerjaschki D, Bates DO, Mathieson PW, Satchell SC. Vascular endothelial growth factor-C, a potential paracrine regulator of glomerular permeability, increases glomerular endothelial cell monolayer integrity and intracellular calcium. Am J Pathol 173: 938-948, 2008.
14. Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, Halle JP, Young J, Rashkow A, Joyce C, Nawaz S, Yusuf S. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 286: 421-426, 2001.
15. Ha TS, Duraisamy S, Faulkner JL, Kasinath BS. Regulation of glomerular endothelial cell proteoglycans by glucose. J Korean Med Sci 19: 245-52, 2004. (Pubitemid 38591799)
16. Haraldsson B, Nystrom J, Deen WM. Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 88: 451-487, 2008.
17. Haraldsson B, Sorensson J. Why do we not all have proteinuria? An update of our current understanding of the glomerular barrier. News Physiol Sci 19: 7-10, 2004.
18. Harvey SJ, Jarad G, Cunningham J, Rops AL, van der Vlag J, Berden JH, Moeller MJ, Holzman LB, Burgess RW, Miner JH. Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Pathol 171: 139-152, 2007.
19. Harvey SJ, Miner JH. Revisiting the glomerular charge barrier in the molecular era. Curr Opin Nephrol Hypertens 17: 393-398, 2008.
20. Henry CB, Duling BR. TNF-α increases entry of macromolecules into luminal endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 279: H2815-H2823, 2000.
21. Hjalmarsson C, Johansson BR, Haraldsson B. Electron microscopic evaluation of the endothelial surface layer of glomerular capillaries. Microvasc Res 67: 9-17, 2004.
22. 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.
23. 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.
24. Jho D, Mehta D, Ahmmed G, Gao XP, Tiruppathi C, Broman M, Malik AB. Angiopoietin-1 opposes VEGF-induced increase in endothelial permeability by inhibiting TRPC1-dependent Ca2 influx. Circ Res 96: 1282-1290, 2005.
25. Kanetsuna Y, Takahashi K, Nagata M, Gannon MA, Breyer MD, Harris RC, Takahashi T. Deficiency of endothelial nitric-oxide synthase confers susceptibility to diabetic nephropathy in nephropathy-resistant inbred mice. Am J Pathol 170: 1473-1484, 2007.
26. Langeler EG, van Hinsbergh VW. Characterization of an in vitro model to study the permeability of human arterial endothelial cell monolayers. Thromb Haemost 60: 240-246, 1988.
27. Lemley KV, Blouch K, Abdullah I, Boothroyd DB, Bennett PH, Myers BD, Nelson RG. Glomerular permselectivity at the onset of nephropathy in type 2 diabetes mellitus. J Am Soc Nephrol 11: 2095-2105, 2000.
28. Lo CM, Keese CR, Giaever I. Cell-substrate contact: another factor may influence transepithelial electrical resistance of cell layers cultured on permeable filters. Exp Cell Res 250: 576-580, 1999.
29. Makino H, Yamasaki Y, Haramoto T, Shikata K, Hironaka K, Ota Z, Kanwar YS. Ultrastructural changes of extracellular matrices in diabetic nephropathy revealed by high resolution scanning and immunoelectron microscopy. Lab Invest 68:45-55, 1993.
30. Nieuwdorp M, Meuwese MC, Vink H, Hoekstra JB, Kastelein JJ, Stroes ES. The endothelial glycocalyx: a potential barrier between health and vascular disease. Curr Opin Lipidol 16: 507-511, 2005.
31. 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.
32. Noble MI, Drake-Holland AJ, Vink H. Hypothesis: arterial glycocalyx dysfunction is the first step in the atherothrombotic process. QJM 101: 513-518, 2008.
33. Parving HH. Initiation and progression of diabetic nephropathy. N Engl J Med 335: 1682-1683, 1996.
34. 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.
35. Ritz E. Heart and kidney: fatal twins? Am J Med 119: S31-39, 2006.
36. Rossing P, Hougaard P, Borch-Johnsen K, Parving HH. Predictors of mortality in insulin dependent diabetes: 10 year observational follow up study. BMJ 313: 779-784, 1996.
37. Rostgaard J, Qvortrup K. Sieve plugs in fenestrae of glomerular capillaries-site of the filtration barrier? Cells Tissues Organs 170: 132-138, 2002. (Pubitemid 33151585)
38. Rubio-Gayosso I, Platts SH, Duling BR. Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 290: H2247-H2256, 2006.
39. 2+ signaling in the mechanism of thrombin-induced increase in endothelial permeability. Am J Physiol Lung Cell Mol Physiol 280: L239-L247, 2001.
40. Satchell SC, Anderson KL, Mathieson PW. Angiopoietin 1 and vascular endothelial growth factor modulate human glomerular endothelial cell barrier properties. J Am Soc Nephrol 15: 566-574, 2004.
41. Satchell SC, Braet F. Glomerular endothelial cell fenestrations: an integral component of the glomerular filtration barrier. Am J Physiol Renal Physiol 296: F947-F956, 2009.
42. Satchell SC, Buchatska O, Khan SB, Bhangal G, Tasman CH, Saleem MA, Baker DP, Lobb RR, Smith J, Cook HT, Mathieson PW, Pusey CD. Interferon-beta reduces proteinuria in experimental glomerulonephritis. J Am Soc Nephrol 18: 2875-2884, 2007.
43. Satchell SC, Tasman CH, Singh A, Ni L, Geelen J, von Ruhland CJ, O'Hare MJ, Saleem MA, van den Heuvel LP, Mathieson PW. Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF. Kidney Int 69: 1633-1640, 2006.
44. Satchell SC, Tooke JE. What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia 51: 714-725, 2008.
45. 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.
46. Van Teeffelen JW, Brands J, Stroes ES, Vink H. Endothelial glycocalyx: sweet shield of blood vessels. Trends Cardiovasc Med 17: 101-105, 2007.
47. Vernier RL, Steffes MW, Sisson-Ross S, Mauer SM. Heparan sulfate proteoglycan in the glomerular basement membrane in type 1 diabetes mellitus. Kidney Int 41: 1070-1080, 1992.