Glycosaminoglycan treatment in glomerulonephritis? An interesting option to investigate

Journal of Nephrology

Volumn 23, Issue 3, 2010, Pages 244-252

  Gambaro, Giovanni ^a   Kong, Norella C T ^b  

^a FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

^b DEPARTMENT OF PHARMACOLOGY   (Malaysia)

Author keywords

Glomerulonephritis; Glycosaminoglycans; Heparanase 1; Heparin; Macrophage; Proteinuria; TGF 1

Indexed keywords

ANTITHROMBOCYTIC AGENT; AZATHIOPRINE; CORTICOSTEROID; CYCLOPHOSPHAMIDE; DALTEPARIN; DANAPAROID; DERMATAN SULFATE; DICOUMAROL; DIPYRIDAMOLE; ENOXAPARIN; FIBROBLAST GROWTH FACTOR 2; GLYCOSAMINOGLYCAN; GROWTH FACTOR; HEPARAN SULFATE; HEPARANASE; HEPARIN; IMMUNOSUPPRESSIVE AGENT; LOW MOLECULAR WEIGHT HEPARIN; PLACEBO; PLATELET DERIVED GROWTH FACTOR; PREDNISOLONE; REVIPARIN; STEROID; SULODEXIDE; TRANSFORMING GROWTH FACTOR BETA1; WARFARIN;

ABSENCE OF SIDE EFFECTS; ANTICOAGULATION; CELL INFILTRATION; CHRONIC GLOMERULONEPHRITIS; CHRONIC GRAFT REJECTION; CLINICAL TRIAL; CONTINUOUS INFUSION; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DISEASE COURSE; DRUG DOSE COMPARISON; DRUG MECHANISM; DRUG MEGADOSE; DRUG SUBSTITUTION; DRUG TARGETING; DRUG WITHDRAWAL; ENZYME INHIBITION; FOCAL GLOMERULOSCLEROSIS; GLOMERULONEPHRITIS; GLOMERULOSCLEROSIS; HIGH RISK PATIENT; HUMAN; IMMUNOGLOBULIN A NEPHROPATHY; KIDNEY FAILURE; KIDNEY GRAFT REJECTION; LOW DRUG DOSE; MACROPHAGE ACTIVATION; MEMBRANOPROLIFERATIVE GLOMERULONEPHRITIS; MICROALBUMINURIA; NEPHROSIS; NEPHROTIC SYNDROME; NONHUMAN; PROLIFERATIVE GLOMERULONEPHRITIS; PROTEINURIA; RAPIDLY PROGRESSIVE GLOMERULONEPHRITIS; RENAL PROTECTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; URETER OBSTRUCTION;

ANTICOAGULANTS; CELL PROLIFERATION; GLOMERULONEPHRITIS; GLUCURONIDASE; GLYCOSAMINOGLYCANS; HUMANS; MACROPHAGES; PLATELET-DERIVED GROWTH FACTOR; PROTEINURIA; RENIN-ANGIOTENSIN SYSTEM; TRANSFORMING GROWTH FACTOR BETA1;

EID: 77951727161     PISSN: 11218428     EISSN: 17246059     Source Type: Journal    
DOI: None     Document Type: Review

References (62)

1. Abaterusso C, Gambaro G. The role of glycosaminoglycans and sulodexide in the treatment of diabetic nephropathy. Treat Endocrinol. 2006;5:211-222. (Pubitemid 44166672)
2. Striker LJ, Peten EP, Elliot SJ, Doi T, Striker GE. Mesangial cell turnover: effect of heparin and peptide growth factors. Lab Invest. 1991;64:446-456.
3. Floege J, Eng E, Young BA, Couser WG, Johnson RJ. Heparin suppresses mesangial cell proliferation and matrix expansion in experimental mesangioproliferative glomerulonephritis. Kidney Int. 1993;43:369-380. (Pubitemid 23162830)
4. Diamond JR, Karnovsky MJ. Nonanticoagulant protective effect of heparin in chronic aminonucleoside nephrosis. Ren Physiol. 1986;9:366-374. (Pubitemid 17057368)
5. Purkerson ML, Tollefsen DM, Klahr S. N-Desulfated/acetylated heparin ameliorates the progression of renal disease in rats with subtotal renal ablation. J Clin Invest. 1988;81:69-74. (Pubitemid 18092234)
6. Barsotti G, Cupisti A, Gervasi GB, et al. Effects of oral administration of heparan sulphate in the rat remnant kidney model. Nephron. 1999;81:310-316. (Pubitemid 29101457)
7. Purkerson ML, Joist JH, Greenberg JM, Kay D, Hoffsten PE, Klahr S. Inhibition by anticoagulant drugs of the progressive hypertension and uremia associated with renal infarction in rats. Thromb Res. 1982;26:227-240.
8. Coffey AK, Karnovsky MJ. Heparin inhibits mesangial cell proliferation in habu-venom-induced glomerular injury. Am J Pathol. 1985;120:248-255.
9. Pesce C, Purkerson ML, Klahr S, Striker GE. Early changes in glomerular size and 3H-thymidine labeling index in controls and heparin-treated rats following subtotal nephrectomy. Kidney Int. 1991;43:369-380.
10. Peten EP, He CJ, Patel A, Yang CW, Striker GE, Striker LJ. Non-anticoagulant heparin suppresses all collagen mRNA and reduces laminin B1 mRNA expression in sclerotic glomeruli from mice transgenic for growth hormone (GH mice) [abstract]. J Am Soc Nephrol. 1993;4:780.
11. Ballermann BJ. Regulation of bovine glomerular endothelial cell growth in vitro. Am J Physiol. 1989;256:C182-C189.
12. Adler S. Inhibition of rat glomerular visceral epithelial cell growth by heparin. Am J Physiol. 1988;255:F781-F786.
13. Pukac LA, Hirsch GM, Lormeau JC, et al. Antiproliferative effects of novel, nonanticoagulant heparin derivatives on vascular smooth muscle cells in vitro and in vivo. Am J Pathol. 1991;139:1501-1509.
14. Burg M, Ostendorf T, Mooney A, Koch KM, Floege J. Treatment of experimental mesangioproliferative glomerulonephritis with non-anticoagulant heparin: therapeutic efficacy and safety. Lab Invest. 1997;76:505-516. (Pubitemid 27176105)
15. Castellot JJ Jr, Pukac LA, Caleb BL, Wright TC Jr, Karnovsky MJ. Heparin selectively inhibits a protein kinase C-dependent mechanism of cell cycle progression in calf aortic smooth muscle cells. J Cell Biol. 1989;109:3147-3155.
16. Reilly CF, Kindy MS, Brown KE, Rosenberg RD, Sonenshein GE. Heparin prevents vascular smooth muscle cell progression through the G1 phase of the cell cycle. J Biol Chem. 1989;264:6990-6995.
17. Bokemeyer D, Ostendorf T, Kunter U, Lindemann M, Kramer HJ, Floege J. Differential activation of mitogen-activated protein kinases in experimental mesangioproliferative glomerulonephritis. J Am Soc Nephrol. 2000;11:232-240. (Pubitemid 30064846)
18. Iida H, Seifert R, Alpers CE, et al. Platelet-derived growth factor (PDGF) and PDGF receptor are induced in mesangial proliferative nephritis in the rat. Proc Natl Acad Sci USA. 1991;88:6560-6564. (Pubitemid 21914987)
19. Floege J, Eng E, Lindner V, et al. Rat glomerular mesangial cells synthesize basic fibroblast growth factor: release, up-regulated synthesis, and mitogenicity in mesangial proliferative glomerulonephritis. J Clin Invest. 1992;90:2362-2369. (Pubitemid 23010054)
20. Floege J, Burns MW, Alpers CE, et al. Glomerular cell proliferation and PDGF expression precede glomerulosclerosis in the remnant kidney model. Kidney Int. 1992;41:297-309.
21. Gambaro G, Cavazzana AO, Luzi P, et al. Glycosaminoglycans prevent morphological renal alterations and albuminuria in diabetic rats. Kidney Int. 1992;42:285-291.
22. Gambaro G, Venturini AP, Noonan DM, et al. Treatment with a glycosaminoglycan formulation ameliorates experimental diabetic nephropathy. Kidney Int. 1994;46:797-806. (Pubitemid 24272038)
23. Oshima Y, Isogai S, Mogama K, Ohuchi H, Ohe K. Protective effect of heparin on renal glomerular anionic sites of streptozotocin-injected rats. Diabetes Res Clin Pract. 1994;25:83-89. (Pubitemid 24306145)
24. Oturai PS, Rasch R, Hasseleger E, et al. Effects of heparin and aminoguanidine on glomerular basement membrane thickening in diabetic rats. APMIS. 1996;104:259-264. (Pubitemid 26165047)
25. Gambaro G, D'Angelo A, Del Prete D, et al. Mesangial cell proliferation in long-term streptozotocin-induced diabetes mellitus in the rat and the renoprotective activity of heparin. Am J Nephrol. 1999;19:530-534. (Pubitemid 29397088)
26. Gambaro G, Baggio B. Glycosaminoglycans: a new paradigm in the prevention of proteinuria and progression of glomerular disease. Nephrol Dial Transplant. 1996;11:762-764. (Pubitemid 26148239)
27. Gambaro G, van der Woude FJ. Glycosaminoglycans: use in treatment of diabetic nephropathy. J Am Soc Nephrol. 2000;11:359-368. (Pubitemid 30064860)
28. Caenazzo C, Garbisa S, Ceol M, et al. Heparin modulates proliferation and proteoglycan biosynthesis in murine mesangial cells: molecular clues for its activity in nephropathy. Nephrol Dial Transplant. 1995;10:175-184.
29. Ceol M, Nerlich A, Baggio B, et al. Increased glomerular α1(IV) collagen expression and deposition in long-term diabetic rats is prevented by chronic glycosaminoglycan treatment. Lab Invest. 1996;74:484-495. (Pubitemid 126425670)
30. Ceol M, Gambaro G, Nerlich A, et al. Glycosaminoglycan therapy prevents TGF-β1 over-expression and pathological changes in renal tissue of long-term diabetic rats. J Am Soc Nephrol. 2000;11:2324-2336.
31. Weigert C, Brodbeck K, Häring HU, Gambaro G, Schleicher ED. Low-molecular-weight heparin prevents high glucose- and phorbol ester-induced TGF-beta 1 gene activation. Kidney Int. 2001;60:935-943.
32. Pecly IM, Gonçalves RG, Rangel EP, et al. Effects of low molecular weight heparin in obstructed kidneys: decrease of collagen, fibronectin and TGF-beta, and increase of chondroitin/dermatan sulfate proteoglycans and macrophage infiltration. Nephrol Dial Transplant. 2006;21:1212-1222.
33. Bernardini N, Cupisti A, Mattii L, et al. Effect of heparan sulphate on kidney tissue expression of TGF-beta, rhoA, laminin and fibronectin in subtotally nephrectomized rats. J Nephrol. 2002;15:530-538. (Pubitemid 35396518)
34. Lewis EJ, Xu X. Abnormal glomerular permeability characteristics in diabetic nephropathy: implications for the therapeutic use of low-molecular weight heparin. Diabetes Care. 2008;31(Suppl 2):S202-S207.
35. Van den Hoven MJ, Rops A, Vlodavsky I, et al. Heparanase in glomerular disease. Kidney Int. 2007;72:543-548.
36. Goldshmidt O, Zacharia E, Cohen M, et al. Heparanase mediates cell adhesion independent of its enzymatic activity. FASEB J. 2003;17:1015-1025. (Pubitemid 36676388)
37. Levidiotis V, Freeman C, Tikellis C, Cooper ME, Power DA. Heparanase inhibition reduces proteinuria in a model of accelerated anti-glomerular basement membrane antibody disease. Nephrology (Carlton). 2005;10:167-173. (Pubitemid 40776277)
38. Ceol M, Vianello D, Schleicher E, et al. Heparin reduces glomerular infiltration and TGF-beta protein expression by macrophages in puromycin glomerulosclerosis. J Nephrol. 2003;16:210-218. (Pubitemid 37304077)
39. Webb LM, Ehrengruber MU, Clark-Lewis I, Baggiolini M, Rot A. Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. Proc Natl Acad Sci U S A. 1993;90:7158-7162. (Pubitemid 23222408)
40. Brady HR. Leukocyte adhesion molecules and kidney diseases. Kidney Int. 1994;45:1285-1300. (Pubitemid 24135013)
41. Koenig A, Norgard-Sumnicht K, Linhardt R, Varki A. Differential interactions of heparin and heparan sulfate glycosaminoglycans with the selectins: implications for the use of unfractionated and low molecular weight heparins as therapeutic agents. J Clin Invest. 1998;101:877-889. (Pubitemid 28096085)
42. Rops AL, Jacobs CW, Linssen PC, et al. Heparan sulfate on activated glomerular endothelial cells and exogenous heparinoids influence the rolling and adhesion of leucocytes. Nephrol Dial Transplant. 2007;22:1070-1077.
43. Wang L, Brown JR, Varki A, Esko JD. Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockage of L- and P-selectins. J Clin Invest. 2002;110:127-136. (Pubitemid 34743473)
44. Braun C, Schultz M, Fang L, et al. Treatment of chronic renal allograft rejection in rats with a low-molecular-weight heparin (reviparin). Transplantation. 2001;72:209-215. (Pubitemid 32729336)
45. Köppel H, Yard BA, Christ M, Wehling M, van der Woude FJ. Modulation of angiotensin II-mediated signalling by heparan sulphate glycosaminoglycans. Nephrol Dial Transplant. 2003;18:2240-2247. (Pubitemid 37336809)
46. Ichikawa I, Yoshida Y, Fogo A, Purkerson ML, Klahr S. Effect of heparin on the glomerular structure and function of remnant nephrons. Kidney Int. 1988;34:638-644.
47. Benck U, Haeckel S, Clorius JH, van der Woude FJ. Proteinuria-lowering effect of heparin therapy in diabetic nephropathy without affecting the renin-angiotensin-aldosterone system. Clin J Am Soc Nephrol. 2007;2:58-67.
48. Olson JL. Role of heparin as a protective agent following reduction of renal mass. Kidney Int. 1984;25:376-382.
49. Gambaro G, Skrha J, Ceriello A. Glycosaminoglycan therapy for long-term diabetic complications? Diabetologia. 1998;41:975-979.
50. Nader HB, Buonassisi V, Colburn P, Dietrich CP. Heparin stimulates the synthesis and modifies the sulfation pattern of heparan sulfate proteoglycan from endothelial cells. J Cell Physiol. 1989;140:305-310. (Pubitemid 19185995)
51. Feldt-Rasmussen B. Microalbuminuria, endothelial dysfunction and cardiovascular risk. Diabetes Metab. 2000;26(Suppl 4):64-66. (Pubitemid 30618358)
52. Gambaro G, Kinalska I, Oksa A, et al. Oral sulodexide reduces albuminuria in microalbuminuric and macroalbuminuric type 1 and type 2 diabetic patients: the Di.N.A.S. randomized trial. J Am Soc Nephrol. 2002;13:1615-1625. (Pubitemid 34579250)
53. Drakeley SJ, Furness PN. Heparin inhibits the binding of immune complexes to cultured rat mesangial cells. Nephrol Dial Transplant. 1994;9:1084-1089. (Pubitemid 24254073)
54. Van Bruggen MC, Walgreen B, Rijke TP, et al. Heparin and heparinoids prevent the binding of immune complexes containing nucleosomal antigens to the GBM and delay nephritis in MRL/lpr mice. Kidney Int. 1996;50:1555-1564. (Pubitemid 26364261)
55. Kincaid-Smith P. Anticoagulants are of value in the treatment of renal disease. Am J Kidney Dis. 1984;3:299-307. (Pubitemid 14151004)
56. Cade JR, DeQuesada AM, Shires DL, et al. The effect of long term high dose heparin treatment on the course of chronic proliferative glomerulonephritis. Nephron. 1971;8:67-80.
57. Lines DR, Coleman M, Gallus A. Focal glomerulosclerosis treated with heparin. Arch Dis Child. 1989;64:855-857.
58. Morita Y, Makino H, Ota K, Akiyama K, Ota Z. Beneficial effect of low molecular weight heparin ("fragmin") on proteinuria of proliferative glomerulonephritis. Clin Nephrol. 1994;42:346-347. (Pubitemid 24343666)
59. Yoshikawa N, Ito H, Sakai T, et al. A controlled trial of combined therapy for newly diagnosed severe childhood IgA nephropathy. The Japanese Pediatric IgA Nephropathy Treatment Study Group. J Am Soc Nephrol. 1999;10:101-109.
60. Baggio B, Gambaro G. Antiproteinuric effect of glycosaminoglycans? Nephron. 1993;64:643-644.
61. Rozita M, Md Shahrir MS, Loo CY, et al. Glycosaminoglycans (sulodexide) for resistant heavy proteinuria of chronic glomerulonephritides [abstract]. 14th Asian Pacific Congress of Nephrology, Kuala Lumpur. NEPHROL. (Suppl) May 2008.
62. Bang K, Lee YS, Kim NO, et al. Anti-proteinuric effect of sulodexide in biopsy-proven IgA nephropathy. World Congress of Nephrology, Milan, 2009, abstract Sa278.