Reduction in glomerular heparan sulfate correlates with complement deposition and albuminuria in active Heymann nephritis

Journal of the American Society of Nephrology

Volumn 10, Issue 8, 1999, Pages 1689-1699

  Raats, C J Ilse ^a   Luca, Mariken E ^b   Bakker, Marinka A H ^a   Van Der Wal, Annemieke ^b   Heeringa, Peter ^c   Van Goor, Harry ^c   Van Der Born, Jacob ^a   De Heer, Emile ^a   Berden, Jo H M ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Nijmegen ^*

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; AUTOANTIBODY; CORE PROTEIN; HEPARAN SULFATE; IMMUNOGLOBULIN G; MEGALIN; MONOCLONAL ANTIBODY; PROTEOGLYCAN;

ANIMAL EXPERIMENT; ARTICLE; BASEMENT MEMBRANE; CELL MEMBRANE; COMPLEMENT DEPOSITION; ELECTRON MICROSCOPY; ENZYME ACTIVITY; GLOMERULONEPHRITIS; GLOMERULUS CAPILLARY; HEYMANN NEPHRITIS; IMMUNE COMPLEX DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; RAT;

EID: 0032842107     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Heymann W, Hackel DB, Harwood S, Wilson SGF, Hunter JLP: Production of nephrotic syndrome in rats by Freund's adjuvants and rat kidney suspensions. Proc Soc Exp Biol Med 100: 660-664, 1959
2. Alousi MA, Post RS, Heymann W: Experimental autoimmune nephrosis in rats. Morphogenesis of the glomerular lesion: Immunohistochemical and electron microscopic studies. Am J Pathol 54: 47-71, 1969
3. Kerjaschki D, Farquhar MG: Immunocytochemical localization of the Heymann nephritis antigen (gp330) in glomerular epithelial cells of normal Lewis rats. J Exp Med 157: 667-686, 1983
4. Luca ME, Deelder AM, Hogendoorn PCW, Daha MR, Galceran M, Van Es LA, De Heer E: Glomerulopathy induced by a single monoclonal autoantibody against gp330. Nephrol Dial Transplant 10: 490-496, 1995
5. Andres G, Brentjes JR, Caldwell PRB, Camussi G, Matsuo S: Formation of immune deposits and disease. Lab Invest 55: 510-520, 1986
6. Kerjaschki D, Miettinen A, Farquhar MG: Initial events in the formation of immune deposits in passive Heymann nephritis: gp330-Anti-gp330 immune complexes form in epithelial coated pits and rapidly become attached to the glomerular basement membrane. J Exp Med 166: 109-128, 1987
7. Kanwar YS, Liu ZZ, Kashihara N, Wallner EI: Current status of the structural and functional basis of glomerular filtration and proteinuria. Semin Nephrol 11: 390-413, 1991
8. Farquhar MG: The glomerular basement membrane: A selective macromolecular filter. In: Cell Biology of Extracellular Matrix, edited by Hay ED, New York, Plenum, 1991, p 365
9. Dworkin LD, Brenner BM: Biophysical basis of glomerular filtration. In: The Kidney: Physiology and Pathophysiology, edited by Seldin DW, Giebisch G, New York, Raven, 1992, p 979
10. Raats CJI, Bakker MAH, Hoch W, Tamboer WPM, Groffen AJA, Van den Heuvel LPWJ, Berden JHM, Van den Born J: Differential expression of agrin in renal basement membranes as revealed by domain-specific antibodies. J Biol Chem 273: 17832-17838, 1998
11. Groffen AJA, Ruegg MA, Dijkman HBPM, Van der Velden TJ, Buskens CA, Van den Born J, Assmann KJM, Monnens LAH, Veerkamp JH, Van den Heuvel LPWJ: Agrin is a major heparan sulfate proteoglycan in the human glomerular basement membrane. J Histochem Cytochem 46: 19-27, 1998
12. Rosenzweig LJ, Kanwar YS: Removal of sulfated (heparan sulfate) or nonsulfated (hyaluronic acid) glycosaminoglycans results in increased permeability of the glomerular basement membrane to 125-I-bovine serum albumin. Lab Invest 47: 177-184, 1982
13. 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 86: 680-693, 1980
14. Van den Born J, Van den Heuvel LPWJ, Bakker MAH, Veerkamp JH, Assmann KJM, Berden JHM: A monoclonal antibody against GBM heparan sulfate induces an acute selective proteinuria in rgts. Kidney Int 41: 115-123, 1992
15. Van den Born J, Van den Heuvel LPWJ, Bakker MAH, Veerkamp JH, Assmann KJM, Weening JJ, Berden JHM: Distribution of GBM heparan sulfate proteoglycan core protein and side chains in human glomerular diseases. Kidney Int 43: 454-463, 1993
16. Schneeberger EE, Stavrakis G, McCarthy K: Alterations in glomerular anionic sites in autologous immune complex nephritis Lab Invest 49: 445-452, 1983
17. Okada K, Kawakami K, Miyao M, Oite T: Ultrastructural alter ations of glomerular anionic sites in idiopathic membranous glomerulonephritis. Clin Nephrol 26: 7-14, 1986
18. Duan H, Nakazawa K, Ishigame H, Itoh N, Shigematsu H: Masking of anionic sites by deposits in lamina rara externa in immune complex nephritis in rats. Virchows Arch B 60: 165-171, 1991
19. Suzuki Y, Maesawa A, Matsui K, Oite T, Koda Y, Arakawa M: Alteration of glomerular anionic sites by the development of subepithelial deposits in experimental glomerulonephritis in the rat. Virchows Arch B 44: 209-222, 1983
20. Laurell CB: Quantitative estimation of proteins of electrophoresis in agarose gel containing antibodies. Anal Biochem 15: 45-52, 1966
21. Van Leer EHG, Ronco P, Verroust P, Van der Wal AM, Hoedemaeker PJ, De Heer E: Epitope specificity of anti-gp330 autoantibodies determines the development of proteinuria in active Heymann nephritis. Am J Pathol 142: 821-829, 1993
22. Raats CJI, Bakker MAH, Van den Born J, Berden JHM: Hydroxyl radicals depolymerize glomerular heparan sulfate in vitro and in experimental nephrotic syndrome. J Biol Chem 272: 26734 -26741, 1997
23. Van den Born J, Gunnarsson K, Bakker MAH, Kjellen L, Kusche-Gullberg M, Maccarana M, Berden JHM, Lindahl U: Presence of N-unsubstituted glucosamine units in native heparan sulfate revealed by a monoclonal antibody. J Biol Chem 270: 31303-31309, 1995
24. Van den Born J, Jann K, Assmann KJM, Lindahl U, Berden JHM: N-acetylated domains in heparan sulfates revealed by a monoclonal antibody against the Escherichia coli K5 capsular polysaccharide. J Biol Chem 271: 22802-22809, 1996
25. Van den Heuvel LPWJ, Van den Born J, Van de Velden TJAM, Veerkamp JH, Monnens LAH, Schroder CH, Berden JHM: Isolation and partial characterization of heparan sulfate proteoglycan from the human glomerular basement membrane. Biochem J 264: 457-465, 1989
26. David G, Bai XM, Van der Schueren B, Cassiman J, Van den Berghe H: Developmental changes in heparan sulfate expression: In situ detection with mAbs. J Cell Biol 119: 961-975, 1992
27. Hassell JR, Gehron Robey P, Barrach HJ, Wilczek J, Rennard SI, Martin GR: Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci USA 77: 4494-4498, 1980
28. McCarthy KJ, Accavitti MA, Couchman JR: Immunological characterization of a basement membrane-specific chondroitin sulfate proteoglycan. J Cell Biol 109: 3187-3198, 1989
29. Neale TJ, Ullrich R, Ojha P, Poczewski H, Verhoeven AJ, Kerjaschki D: Reactive oxygen species and neutrophil respiratory burst cytochrome b558 are produced by kidney glomerular cells in passive Heymann nephritis. Proc Natl Acad Sci USA 90: 3645-3649, 1993
30. Vos TA, Gouw ASH, Klok PA, Havinga R, Van Goor H, Huitema S, Roelofsen H, Kuijpers F, Jansen PLM, Moshage H: Differential effects of nitric oxide synthase inhibitors on endotoxin-induced liver damage in rats. Gastroenterology 113: 1323-1333, 1997
31. Briggs RT, Robinson JM, Karnovsky ML: Superoxide production by polymorphonuclear leukocytes: A cytochemical approach. Histochemistry 84: 371-378, 1986
32. Van Bruggen MCJ, Kramers K, Hylkema MN, Van den Born J, Bakker MAH, Assmann KJM, Smeenk RJT, Berden JHM: Decrease of heparan sulfate in the glomerular basement membrane in murine lupus nephritis. Am J Pathol 146: 753-763, 1995
33. Van den Born J, Van den Heuvel LPWJ, Bakker MAH, Veerkamp JH, Assmann KJM, Berden JHM: Production and characterization of a monoclonal antibody against human glomerular heparan sulfate. Lab Invest 65: 287-297, 1991
34. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the folin phenol reagent. J Biol Chem 193: 265-275, 1951
35. Farndale RW, Buttle DJ, Barrett AJ: Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883: 173-177, 1986
36. Van den Born J, Van den Heuvel LPWJ, Bakker MAH, Veerkamp JH, Assmann KJM, Berden JHM: Monoclonal antibodies against the protein core and glycosaminoglycan side chain of glomerular basement membrane heparan sulfate proteoglycan: Characterization and immunohistological application in human tissues. J Histochem Cytochem 42: 89-102, 1994
37. Schulze M, Pruchno CJ, Burns M, Baker PJ, Johnson RJ, Couser WG: Glomerular C3c localization indicates ongoing immune deposit formation and complement activation in experimental glomerulonephritis. Am J Pathol 142: 179-187, 1993
38. De Heer E, Daha MR, Bhakdi S, Bazin H, Es van LA: Possible involvement of terminal complement complex in active Heymann nephritis. Kidney Int 27: 388-393, 1985
39. Adler S, Baker PJ, Pritzel P, Couser WG: Detection of terminal complement components in experimental immune glomerular injury. Kidney Int 26: 830-837, 1984
40. Couser WG: Mediation of immune glomerular injury. J Am Soc Nephrol 1: 13-29, 1990
41. Leenaerts PL, Hall BM, Van Damme BJC, Daha MR, Vanrenterghem YF: Active Heymann nephritis in complement component C6 deficient rats. Kidney Int 47: 1604-1614, 1995
42. Timpl R: Proteoglycans of basement membranes. Experientia 49: 417-428, 1993
43. Tamsma JT, Van den Born J, Bruijn JA, Assmann KJM, Weening JJ, Berden JHM, Wielander J, Schrama E, Hermans J, Veerkamp JH, Lemkes HHPJ, Van den Woúde FJ: Expression of glomerular extracellular matrix components in human diabetic nephropathy: Decrease of heparan sulphate in the glomerular basement membrane. Diabetologia 37: 313-320, 1994
44. Orlando RA, Farquhar MG: Identification of a cell line that expresses a cell surface and a soluble form of the gp330/receptor-associated protein (RAP) Heymann nephritis antigenic complex. Proc Natl Acad Sci USA 90: 4082-4086, 1993
45. Vassiliou O, Stanley KK: Exogenous receptor-associated protein binds to distinct sites on human fibroblast but does not bind to the glycosaminoglycan residues of heparan sulfate proteoglycans. J Biol Chem 269: 15172-15178, 1994
46. Orlando RA, Kerjaschki D, Farquhar MG: Megalin (gp330) possesses an antigenic epitope capable of inducing passive Heymann nephritis independent of the nephritogenic epitope in receptor-associated protein. J Am Soc Nephrol 6: 61-67, 1995
47. Malle E, Woenckhaus C, Waeg G, Esterbauer H, Grone EF, Grone H-J: Immunological evidence for hypochlorite-modified proteins in human kidney. Am J Pathol 150: 603-615, 1997
48. Cattell V, Largen P, De Heer E, Cook T: Glomeruli synthesize nitrite in active Heymann nephritis: The source is infiltrating macrophages. Kidney Int 40: 847-851, 1991
49. Shah SV: Evidence suggesting a role for hydroxyl radical in passive Heymann nephritis in rats. Am J Physiol 254: F337-F344, 1988
50. Platt JL, Vercellotti GM, Lindman BJ, Oegema TR, Bach FH, Dalmasso AP: Release of heparan sulfate from endothelial cells: Implications for pathogenesis of hyperacute rejection. J Exp Med 171: 1363-1368, 1990