The role of heparanase and the endothelial glycocalyx in the development of proteinuria

Nephrology Dialysis Transplantation

Volumn 29, Issue 1, 2014, Pages 49-55

  Garsen, Marjolein ^a   Rops, Angelique L W M M ^a   Rabelink, Ton J ^b   Berden, Jo H M ^a   Van Der Vlag, Johan ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

glomerular filtration barrier; glycocalyx; heparan sulphate; heparanase

Indexed keywords

GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARANASE; MUPARFOSTAT; PROTEOHEPARAN SULFATE;

ALBUMINURIA; DIABETIC NEPHROPATHY; ENDOTHELIAL GLYCOCALYX; ENDOTHELIUM; ENDOTHELIUM CELL; GLOMERULAR FILTRATION BARRIER; GLOMERULUS BASEMENT MEMBRANE; GLOMERULUS FILTRATION; GLYCOCALYX; HEYMANN NEPHRITIS; HUMAN; HYPERGLYCEMIA; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; MEMBRANOUS GLOMERULONEPHRITIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; PODOCYTE; PRIORITY JOURNAL; PROTEINURIA; REVIEW; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS;

GLOMERULAR FILTRATION BARRIER; GLYCOCALYX; HEPARAN SULPHATE; HEPARANASE;

ANIMALS; DIABETIC NEPHROPATHIES; FEMALE; GLOMERULAR BASEMENT MEMBRANE; GLUCURONIDASE; GLYCOCALYX; HEPARITIN SULFATE; HUMANS; KIDNEY GLOMERULUS; MALE; PODOCYTES; PROTEINURIA;

EID: 84892769772     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gft410     Document Type: Review

References (49)

1. Tryggvason K, Pettersson E. Causes and consequences of protei-nuria: the kidney filtration barrier and progressive renal failure. J Intern Med 2003; 254: 216-224
2. Haraldsson B, Nystrom J, Deen WM. Properties of the glomeru-lar barrier and mechanisms of proteinuria. Physiol Rev 2008; 88: 451-487
3. Jarad G, Miner JH. Update on the glomerular filtration barrier. Curr Opin Nephrol Hypertens 2009; 18: 226-232
4. Patrakka J, Tryggvason K. Molecular make-up of the glomerular filtration barrier. Biochem Biophys Res Commun 2010; 396: 164-169
5. van den Hoven MJ, Rops AL, Vlodavsky I et al. Heparanase in glomerular diseases. Kidney Int 2007; 72: 543-548
6. Satchell SC, Braet F. Glomerular endothelial cell fenestrations: an integral component of the glomerular filtration barrier. Am J Physiol Renal Physiol 2009; 296: F947-F956
7. Sison K, Eremina V, Baelde H et al. Glomerular structure and function require paracrine, not autocrine, VEGF-VEGFR-2 signaling. J Am Soc Nephrol 2010; 21: 1691-1701
8. Reitsma S, Slaaf DW, Vink H et al. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch 2007; 454: 345-359
9. Friden V, Oveland E, Tenstad O et al. The glomerular endothelial cell coat is essential for glomerular filtration. Kidney Int 2011; 79: 1322-1330
10. Lennon FE, Singleton PA. Hyaluronan regulation of vascular integrity. Am J Cardiovasc Dis 2011; 1: 200-213
11. Tarbell JM, Pahakis MY. Mechanotransduction and the glycoca-lyx. J Intern Med 2006; 259: 339-350
12. Jeansson M, Bjorck K, Tenstad O et al. Adriamycin alters glomer-ular endothelium to induce proteinuria. J Am Soc Nephrol 2009; 20: 114-122
13. Singh A, Satchell SC, Neal CR et al. Glomerular endothelial gly-cocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol 2007; 18: 2885-2893
14. Vink H, Duling BR. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ Res 1996; 79: 581-589
15. Rops AL, van der Vlag J, Lensen JF et al. Heparan sulfate proteoglycans in glomerular inflammation. Kidney Int 2004; 65: 768-785
16. Nieuwdorp M, Mooij HL, Kroon J et al. Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes. Diabetes 2006; 55: 1127-1132
17. Schmidt EP, Yang Y, Janssen WJ et al. The pulmonary endo-thelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nat Med 2012; 18: 1217-1223
18. Lipowsky HH. The endothelial glycocalyx as a barrier to leukocyte adhesion and its mediation by extracellular proteases. Ann Biomed Eng 2012; 40: 840-848
19. Salmon AH, Satchell SC. Endothelial glycocalyx dysfunction in disease: albuminuria and increased microvascular permeability. J Pathol 2012; 226: 562-574
20. Esko JD, Selleck SB. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem 2002; 71: 435-471
21. Morimoto-Tomita M, Uchimura K, Werb Z et al. Cloning and characterization of two extracellular heparin-degrading en-dosulfatases in mice and humans. J Biol Chem 2002; 277: 49175-49185
22. Kanwar YS, Linker A, Farquhar MG. Increased permeability of the glomerular basement membrane to ferritin after removal of glycosaminoglycans (heparan sulfate) by enzyme digestion. J Cell Biol 1980; 86: 688-693
23. Rosenzweig LJ, Kanwar YS. Removal of sulfated (heparan sulfate) or nonsulfated (hyaluronic acid) glycosaminoglycans results in increased permeability of the glomerular basement membrane to 125I-bovine serum albumin. Lab Invest 1982; 47: 177-184
24. van den Born J, van den Heuvel LP, Bakker MA et al. A monoclonal antibody against GBM heparan sulfate induces an acute selective proteinuria in rats. Kidney Int 1992; 41: 115-123
25. van den Born J, van den Heuvel LP, Bakker MA et al. Distribution of GBM heparan sulfate proteoglycan core protein and side chains in human glomerular diseases. Kidney Int 1993; 43: 454-463
26. Harvey SJ, Jarad G, Cunningham J et al. Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Pathol 2007; 171: 139-152
27. Goldberg S, Harvey SJ, Cunningham J et al. Glomerular filtration is normal in the absence of both agrin and perlecan-heparan sulfate from the glomerular basement membrane. Nephrol Dial Transplant 2009; 24: 2044-2051
28. Rops AL, Gotte M, Baselmans MH et al. Syndecan-1 deficiency aggravates anti-glomerular basement membrane nephritis. Kidney Int 2007; 72: 1204-1215
29. Chen S, Wassenhove-McCarthy DJ, Yamaguchi Y et al. Loss of heparan sulfate glycosaminoglycan assembly in podocytes does not lead to proteinuria. Kidney Int 2008; 74: 289-299
30. van den Hoven MJ, Wijnhoven TJ, Li JP et al. Reduction of anionic sites in the glomerular basement membrane by hepara-nase does not lead to proteinuria. Kidney Int 2008; 73: 278-287
31. Smith RJ, Alexander J, Barlow PN et al. New approaches to the treatment of dense deposit disease. J Am Soc Nephrol 2007; 18: 2447-2456
32. Abboud-Jarrous G, Atzmon R, Peretz T et al. Cathepsin L is responsible for processing and activation of proheparanase through multiple cleavages of a linker segment. J Biol Chem 2008; 283: 18167-18176
33. Nasser NJ. Heparanase involvement in physiology and disease. Cell Mol Life Sci 2008; 65: 1706-1715
34. Levidiotis V, Kanellis J, Ierino FL et al. Increased expression of heparanase in puromycin aminonucleoside nephrosis. Kidney Int 2001; 60: 1287-1296
35. Levidiotis V, Freeman C, Tikellis C et al. Heparanase is involved in the pathogenesis of proteinuria as a result of glomerulonephri-tis. J Am Soc Nephrol 2004; 15: 68-78
36. Levidiotis V, Freeman C, Punler M et al. A synthetic heparanase inhibitor reduces proteinuria in passive Heymann nephritis. J Am Soc Nephrol 2004; 15: 2882-2892
37. van den Hoven MJ, Rops AL, Bakker MA et al. Increased expression of heparanase in overt diabetic nephropathy. Kidney Int 2006; 70: 2100-2108
38. Kramer A, van den Hoven M, Rops A et al. Induction of glomer-ular heparanase expression in rats with adriamycin nephropathy is regulated by reactive oxygen species and the renin-angiotensin system. J Am Soc Nephrol 2006; 17: 2513-2520
39. Gil N, Goldberg R, Neuman T et al. Heparanase is essential for the development of diabetic nephropathy in mice. Diabetes 2012; 61: 208-216
40. Ten Dam GB, Kurup S, van de Westerlo EM et al. 3-O-sulfated Oligosaccharide structures are recognized by anti-heparan sulfate antibody HS4C3. J Biol Chem 2006; 281: 4654-4662
41. Kuwabara A, Satoh M, Tomita N et al. Deterioration of glomeru-lar endothelial surface layer induced by oxidative stress is implicated in altered permeability of macromolecules in Zucker fatty rats. Diabetologia 2010; 53: 2056-2065
42. Haraldsson B, Nystrom J. The glomerular endothelium: new insights on function and structure. Curr Opin Nephrol Hypertens 2012; 21: 258-263
43. Salmon AH, Ferguson JK, Burford JL et al. Loss of the endothelial glycocalyx links albuminuria and vascular dysfunction. J Am Soc Nephrol 2012; 23: 1339-1350
44. Dane MJ, van den Berg BM, Avramut MC et al. Glomerular endothelial surface layer acts as a barrier against albumin filtration. Am J Pathol 2013; 182: 1532-1540
45. 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: 2646-2655
46. Rops AL, van den Hoven MJ, Veldman BA et al. Urinary hepara-nase activity in patients with type 1 and type 2 diabetes. Nephrol Dial Transplant 2012; 27: 2853-2861
47. Singh A, Friden V, Dasgupta I et al. High glucose causes dysfunction of the human glomerular endothelial glycocalyx. Am J Physiol Renal Physiol 2011; 300: F40-F48
48. Singh A, Ramnath RD, Foster RR et al. Reactive oxygen species modulate the barrier function of the human glomerular endo-thelial glycocalyx. PLoS One 2013; 8: e55852
49. van den Hoven MJ, Waanders F, Rops AL et al. Regulation of glo-merular heparanase expression by aldosterone, angiotensin II and reactive oxygen species. Nephrol Dial Transplant 2009; 24: 2637-2645