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Published in: Rheumatology International 5/2003

01-09-2003 | Original Article

Increased excretions of glycosaminoglycans and heparan sulfate in lupus nephritis and rheumatoid arthritis

Authors: İlhan Biçer, Kenan Aksu, Zuhal Parildar, Tijen Tanyalçin, Eker Doğanavşargil, Fatma Z. Kutay

Published in: Rheumatology International | Issue 5/2003

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Abstract

Urinary glycosaminoglycans (GAG) and heparan sulfate (HS) are considered to be markers of early renal involvement. This study was undertaken to demonstrate their excretion patterns in rheumatoid arthritis (RA) and systemic lupus erythematosus (SLE) with and without arthritis. Serum creatinine and urinary GAG, HS, microalbumin, and creatinine measurements were made in 51 biopsy-proven lupus nephritis (LN) cases, 12 RA patients, and 21 healthy controls. Urinary GAG and HS levels were higher in the LN and RA groups than in controls. Heparan sulfate excretions and SLE disease activity index (SLEDAI) scores were no different between SLE patients with classes 1 and 2 (group A) and those with classes 3, 4, and 5 (group B) renal involvement. However, GAG and microalbumin excretions were significantly high in the latter. There were no differences in GAG and HS excretions between normoalbuminuric, microalbuminuric, and macroproteinuric SLE patients or between those with and without arthritis. In conclusion, urinary GAG and HS, being unrelated to the presence of arthritis, are independent markers of LN. Extrarenal causes or subclinical renal involvement may be responsible in RA due to their increased excretion in these patients.
Literature
1.
go back to reference Kanwar YS, Linker A, Farquhar MG (1980) Increased permeability of the GBM to ferritin after removal of glycosaminoglycans (HS) by enzyme digestion. J Cell Biol 86:688–693PubMed Kanwar YS, Linker A, Farquhar MG (1980) Increased permeability of the GBM to ferritin after removal of glycosaminoglycans (HS) by enzyme digestion. J Cell Biol 86:688–693PubMed
2.
go back to reference Lahita RG (1992) Systemic lupus erythematosus. Churchill Livingstone, New York, pp 1–1,000 Lahita RG (1992) Systemic lupus erythematosus. Churchill Livingstone, New York, pp 1–1,000
3.
go back to reference van den Born J, van den Heuvel LPWJ, Bakker MAH, Veerkamp JH, Assman KJ, Weening JJ (1993) Distribution of GBM heparan sulfate proteoglycan core protein and side chains in human glomerular diseases. Kidney Int 43:454–463PubMed van den Born J, van den Heuvel LPWJ, Bakker MAH, Veerkamp JH, Assman KJ, Weening JJ (1993) Distribution of GBM heparan sulfate proteoglycan core protein and side chains in human glomerular diseases. Kidney Int 43:454–463PubMed
4.
go back to reference De Muro P, Faedda R, Formato M, Re F, Satta A, Cherchi GM, Carcassi A (2001) Urinary glycosaminoglycans in patients with systemic lupus erythematosus. Clin Exp Rheumatol 19:125–130PubMed De Muro P, Faedda R, Formato M, Re F, Satta A, Cherchi GM, Carcassi A (2001) Urinary glycosaminoglycans in patients with systemic lupus erythematosus. Clin Exp Rheumatol 19:125–130PubMed
5.
go back to reference Manganaro M, Bruno M, Ravarino N, Pellerito R, Cosseddu D, Torchio B, Urbano D, Linari F (1994) Renal damage in rheumatoid arthritis. Minerva Urol Nefrol 46:55–60PubMed Manganaro M, Bruno M, Ravarino N, Pellerito R, Cosseddu D, Torchio B, Urbano D, Linari F (1994) Renal damage in rheumatoid arthritis. Minerva Urol Nefrol 46:55–60PubMed
6.
go back to reference Chuck AJ, Murphy J, Weiss JB, Grennan DM (1986) Comparison of urinary glycosaminoglycan excretion in rheumatoid arthritis, osteoarthritis, myocardial infarction, and controls. Ann Rheum Dis 45:162–166PubMed Chuck AJ, Murphy J, Weiss JB, Grennan DM (1986) Comparison of urinary glycosaminoglycan excretion in rheumatoid arthritis, osteoarthritis, myocardial infarction, and controls. Ann Rheum Dis 45:162–166PubMed
7.
go back to reference Mbuyi JM, Dequeker J, Teblick M, Merlevede M (1982) Relevance of urinary excretion of alcian blue-glycosaminoglycans complexes and hydroxyproline to disease activity in rheumatoid arthritis. J Rheumatol 9:579–583PubMed Mbuyi JM, Dequeker J, Teblick M, Merlevede M (1982) Relevance of urinary excretion of alcian blue-glycosaminoglycans complexes and hydroxyproline to disease activity in rheumatoid arthritis. J Rheumatol 9:579–583PubMed
8.
go back to reference Tan EM, Cohen AS, Freis JF (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1277–1277 Tan EM, Cohen AS, Freis JF (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1277–1277
9.
go back to reference Golbus J, McCune WJ (1994) Lupus nephritis. Classification, prognosis, immunopathogenesis and treatment. Rheum Dis Clin North Am 20:213–242PubMed Golbus J, McCune WJ (1994) Lupus nephritis. Classification, prognosis, immunopathogenesis and treatment. Rheum Dis Clin North Am 20:213–242PubMed
10.
go back to reference Kashgarian M (1982) New approaches to clinical pathologic correlation in lupus nephritis. Am J Kidney Dis 2:164–169PubMed Kashgarian M (1982) New approaches to clinical pathologic correlation in lupus nephritis. Am J Kidney Dis 2:164–169PubMed
11.
go back to reference Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS et al (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–328PubMed Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS et al (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–328PubMed
12.
go back to reference Teller WM, Burke EC, Rosevear JW, McKenzie BF (1962) Urinary excretion of acid mucopolysaccharides in normal children and patients with gorgolism. J Lab Clin Med 95–101 Teller WM, Burke EC, Rosevear JW, McKenzie BF (1962) Urinary excretion of acid mucopolysaccharides in normal children and patients with gorgolism. J Lab Clin Med 95–101
13.
go back to reference Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489PubMed Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489PubMed
14.
go back to reference Bonavita N, Reed P, Donelly PV, Hill LL, Diferrante N (1984) The urinary excretion of heparan sulfate by juvenile and adult-onset diabetic patients. Connective Tissue Res 13:83–87 Bonavita N, Reed P, Donelly PV, Hill LL, Diferrante N (1984) The urinary excretion of heparan sulfate by juvenile and adult-onset diabetic patients. Connective Tissue Res 13:83–87
15.
go back to reference Smith RL, Gilkerson E (1979) Quantitation of glycosaminoglycan hexosamine using 3-methyl-2-benzothiazolone hydrazone hydrochloride. Anal Biochem 98:478–480PubMed Smith RL, Gilkerson E (1979) Quantitation of glycosaminoglycan hexosamine using 3-methyl-2-benzothiazolone hydrazone hydrochloride. Anal Biochem 98:478–480PubMed
16.
go back to reference Camussi G, Tetta C, Mazzucco G, Monga G, Roffinello C, Alberton M et al (1986) Platelet cationic proteins are present in glomeruli of lupus nephritis patients. Kidney Int 30:555–565PubMed Camussi G, Tetta C, Mazzucco G, Monga G, Roffinello C, Alberton M et al (1986) Platelet cationic proteins are present in glomeruli of lupus nephritis patients. Kidney Int 30:555–565PubMed
17.
go back to reference Jackson RL, Busch SJ, Cardin AD (1991) Glycosaminoglycans: molecular properties, protein interactions, and role in physiologic processes. Physiol Rev 71:481–539PubMed Jackson RL, Busch SJ, Cardin AD (1991) Glycosaminoglycans: molecular properties, protein interactions, and role in physiologic processes. Physiol Rev 71:481–539PubMed
18.
go back to reference Hunsicker LG, Shearer TP, Shaffer SJ (1981) Acute reversible proteinuria induced by infusion of the polycation hexadimethrine. Kidney Int 20:7PubMed Hunsicker LG, Shearer TP, Shaffer SJ (1981) Acute reversible proteinuria induced by infusion of the polycation hexadimethrine. Kidney Int 20:7PubMed
19.
go back to reference Sakane T, Steinberg AD, Green I (1978) Studies of immune functions of patients with systemic lupus erythematosus. I. Dysfunction of suppressor T-cell activity related to impaired generation of, rather than response to, suppressor cells. Arthritis Rheum 21:657PubMed Sakane T, Steinberg AD, Green I (1978) Studies of immune functions of patients with systemic lupus erythematosus. I. Dysfunction of suppressor T-cell activity related to impaired generation of, rather than response to, suppressor cells. Arthritis Rheum 21:657PubMed
20.
go back to reference Parildar Z, Tanyalcin T, Cetinkalp S, Tüzün M, Kutay F (1999) Effect of enalapril on urinary glycosaminoglycan, heparan sulfate and microalbuminuria in type II diabetic patients. Biomarkers 4:351–360CrossRef Parildar Z, Tanyalcin T, Cetinkalp S, Tüzün M, Kutay F (1999) Effect of enalapril on urinary glycosaminoglycan, heparan sulfate and microalbuminuria in type II diabetic patients. Biomarkers 4:351–360CrossRef
21.
go back to reference Tencer J, Torffvit O, Bjornsson S, Thysell H, Grubb A, Rippe B (1997) Decreased excretion of glycosaminoglycans in patients with primary glomerular diseases. Clin Nephrol 48:212–219PubMed Tencer J, Torffvit O, Bjornsson S, Thysell H, Grubb A, Rippe B (1997) Decreased excretion of glycosaminoglycans in patients with primary glomerular diseases. Clin Nephrol 48:212–219PubMed
22.
go back to reference Ueta I, Takamatsu K, Hashimoto K (1994) Urinary glycosaminoglycans in patients with non-insulin-dependent diabetes mellitus, collagen diseases and IgA nephropathy. Nippon Jinzo Gakkai Shi 36:138–145PubMed Ueta I, Takamatsu K, Hashimoto K (1994) Urinary glycosaminoglycans in patients with non-insulin-dependent diabetes mellitus, collagen diseases and IgA nephropathy. Nippon Jinzo Gakkai Shi 36:138–145PubMed
23.
go back to reference Mitsuhashi H, Tsukada Y, Ono K, Yano S, Naruse T (1993) Urine glycosaminoglycans and heparan sulfate excretions in adult patients with glomerular diseases. Clin Nephrol 39:231–237PubMed Mitsuhashi H, Tsukada Y, Ono K, Yano S, Naruse T (1993) Urine glycosaminoglycans and heparan sulfate excretions in adult patients with glomerular diseases. Clin Nephrol 39:231–237PubMed
24.
go back to reference van Brugen MCJ, Kramers C, Walgreen B, Elema JD, Kallenberg CGM, van den Born J et al (1997) Nucleosomes and histones are present in glomerular deposits in human lupus nephritis. Nephrol Dial Transplant 12:57–66CrossRef van Brugen MCJ, Kramers C, Walgreen B, Elema JD, Kallenberg CGM, van den Born J et al (1997) Nucleosomes and histones are present in glomerular deposits in human lupus nephritis. Nephrol Dial Transplant 12:57–66CrossRef
25.
go back to reference Camussi G, Tetta C, Segoloni G, Coda R, Vercellone A (1982) Localization of neutrophil cationic proteins and loss of anionic charges in glomeruli of patients with systemic lupus erythematosus glomerulonephritis. Clin Immunol Immunopathol 24:299–314PubMed Camussi G, Tetta C, Segoloni G, Coda R, Vercellone A (1982) Localization of neutrophil cationic proteins and loss of anionic charges in glomeruli of patients with systemic lupus erythematosus glomerulonephritis. Clin Immunol Immunopathol 24:299–314PubMed
26.
go back to reference van Bruggen MC, Kramers K, Hylkema MN, van den Born J, Bakker MA, Assmann KJ et al (1995) Decrease of heparan sulfate staining in the glomerular basement membrane in murine lupus nephritis. Am J Pathol 146:753–763PubMed van Bruggen MC, Kramers K, Hylkema MN, van den Born J, Bakker MA, Assmann KJ et al (1995) Decrease of heparan sulfate staining in the glomerular basement membrane in murine lupus nephritis. Am J Pathol 146:753–763PubMed
27.
go back to reference Konen JC, Shihabi ZK (1993) Microalbuminuria and diabetes mellitus. Am Fam Physician 48:1421–1428PubMed Konen JC, Shihabi ZK (1993) Microalbuminuria and diabetes mellitus. Am Fam Physician 48:1421–1428PubMed
28.
go back to reference Vernier RL, Steffes MW, Sisson RS, Mauer SM (1992) Heparan sulfate proteoglycan in the glomerular basement membrane in type I diabetes mellitus. Kidney Int 41:1070–1080PubMed Vernier RL, Steffes MW, Sisson RS, Mauer SM (1992) Heparan sulfate proteoglycan in the glomerular basement membrane in type I diabetes mellitus. Kidney Int 41:1070–1080PubMed
29.
go back to reference Gladman DD, Urowitz MB, Cole E, Ritchie S, Chang CH, Churg J (1989) Kidney biopsy in SLE. I. A clinical-morphologic evaluation. Q J Med 72:779–833PubMed Gladman DD, Urowitz MB, Cole E, Ritchie S, Chang CH, Churg J (1989) Kidney biopsy in SLE. I. A clinical-morphologic evaluation. Q J Med 72:779–833PubMed
30.
go back to reference Verstraeten A, Dequeker J (1986) Mineral metabolism in postmenopausal women with active rheumatoid arthritis. J Rheumatol 13:43–46PubMed Verstraeten A, Dequeker J (1986) Mineral metabolism in postmenopausal women with active rheumatoid arthritis. J Rheumatol 13:43–46PubMed
31.
go back to reference Kordonouri O, Dracou C, Papadellis F, Touroutsika P, Muller C, Jorres A (1994) Glomerular microproteinuria in children treated with nonsteroidal anti-inflammatory drugs for juvenile chronic arthritis. Clin Exp Rheumatol 12:567–571PubMed Kordonouri O, Dracou C, Papadellis F, Touroutsika P, Muller C, Jorres A (1994) Glomerular microproteinuria in children treated with nonsteroidal anti-inflammatory drugs for juvenile chronic arthritis. Clin Exp Rheumatol 12:567–571PubMed
Metadata
Title
Increased excretions of glycosaminoglycans and heparan sulfate in lupus nephritis and rheumatoid arthritis
Authors
İlhan Biçer
Kenan Aksu
Zuhal Parildar
Tijen Tanyalçin
Eker Doğanavşargil
Fatma Z. Kutay
Publication date
01-09-2003
Publisher
Springer-Verlag
Published in
Rheumatology International / Issue 5/2003
Print ISSN: 0172-8172
Electronic ISSN: 1437-160X
DOI
https://doi.org/10.1007/s00296-003-0294-3

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