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Published in: Arthritis Research & Therapy 3/2003

Open Access 01-06-2003 | Research article

Efficacy of treatment with glycosaminoglycans on experimental collagen-induced arthritis in rats

Authors: Giuseppe M Campo, PhD, Angela Avenoso, Salvatore Campo, Alida M Ferlazzo, Domenica Altavilla, Alberto Calatroni

Published in: Arthritis Research & Therapy | Issue 3/2003

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Abstract

To evaluate the antioxidant activity of the glycosaminoglycans hyaluronic acid (HYA) and chondroitin-4-sulphate (C4S), we used a rat model of collagen-induced arthritis (CIA). Arthritis was induced in Lewis rats by multiple intradermal injections of 250 μl of emulsion containing bovine type II collagen in complete Freund's adjuvant at the base of the tail and into three to five other sites on the back. Rats were challenged again with the same antigen preparation 7 days later. Disease developed about 11 days after the second immunization. The effects of treatment in the rats were monitored by biochemical parameters and by macroscopic and histological evaluations in blood, synovial tissue and articular cartilage. Arthritis produced the following symptoms: severe periarticular erythema, edema and inflammation in the hindpaws; membrane peroxidation in the cartilage of the joints; endogenous antioxidant wasting; high tumour necrosis factor-α (TNF-α) plasma levels; and synovial neutrophil accumulation. Treatment with HYA and C4S, starting at the onset of arthritis for 10 days, limited the erosive action of the disease in the articular joints of knee and paw, reduced lipid peroxidation, restored the endogenous antioxidants reduced glutathione (GSH) and superoxide dismutase, decreased plasma TNF-α levels, and limited synovial neutrophil infiltration. These data confirm that erosive destruction of the joint cartilage in CIA is due at least in part to free radicals released by activated neutrophils and produced by other biochemical pathways. The beneficial effects obtained with the treatment suggest that HYA and C4S could be considered natural endogenous macromolecules to limit erosive damage in CIA or as a useful tool with which to study the involvement of free radicals in rheumatoid arthritis.
Literature
1.
go back to reference Feldmann M, Brennan FM, Maini RN: Rheumatoid arthritis. Cell. 1996, 85: 307-310. 10.1016/S0092-8674(00)81109-5.CrossRefPubMed Feldmann M, Brennan FM, Maini RN: Rheumatoid arthritis. Cell. 1996, 85: 307-310. 10.1016/S0092-8674(00)81109-5.CrossRefPubMed
2.
go back to reference Jawaheer D, Thomson W, MacGregor AJ, Carthy D, Davidson J, Dyer PA, Silman AJ, Ollier WE: 'Homozygosity' for the HLA-DR shared epitope contributes the highest risk for rheumatoid arthritis concordance in identical twins. Arthritis Rheum. 1994, 37: 681-6866.CrossRefPubMed Jawaheer D, Thomson W, MacGregor AJ, Carthy D, Davidson J, Dyer PA, Silman AJ, Ollier WE: 'Homozygosity' for the HLA-DR shared epitope contributes the highest risk for rheumatoid arthritis concordance in identical twins. Arthritis Rheum. 1994, 37: 681-6866.CrossRefPubMed
3.
go back to reference Wooley PH, Luthra HS, Stuart JM, David CS: Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates. J Exp Med. 1981, 154: 688-700. 10.1084/jem.154.3.688.CrossRefPubMed Wooley PH, Luthra HS, Stuart JM, David CS: Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates. J Exp Med. 1981, 154: 688-700. 10.1084/jem.154.3.688.CrossRefPubMed
4.
go back to reference Blake DR, Merry P, Unsworth J, Kidd BL, Outhwaite JM, Ballard R, Morris CJ, Gray L, Lunec J: Hypoxic-reperfusion injury in the inflamed human joint. Lancet. 1989, i: 289-293. 10.1016/S0140-6736(89)91305-6.CrossRef Blake DR, Merry P, Unsworth J, Kidd BL, Outhwaite JM, Ballard R, Morris CJ, Gray L, Lunec J: Hypoxic-reperfusion injury in the inflamed human joint. Lancet. 1989, i: 289-293. 10.1016/S0140-6736(89)91305-6.CrossRef
5.
go back to reference Lunec J: Free radicals: their involvement in disease processes. Ann Clin Biochem. 1990, 27: 173-182.CrossRefPubMed Lunec J: Free radicals: their involvement in disease processes. Ann Clin Biochem. 1990, 27: 173-182.CrossRefPubMed
6.
go back to reference Dormandy TL: Free-radical pathology and medicine. A review. J R Coll Physicians Lond. 1989, 23: 221-227.PubMed Dormandy TL: Free-radical pathology and medicine. A review. J R Coll Physicians Lond. 1989, 23: 221-227.PubMed
7.
go back to reference Halliwell B, Gutteridge JM: The antioxidants of human extracellular fluids. Arch Biochem Biophys. 1990, 280: 1-8. 10.1016/0003-9861(90)90510-6.CrossRefPubMed Halliwell B, Gutteridge JM: The antioxidants of human extracellular fluids. Arch Biochem Biophys. 1990, 280: 1-8. 10.1016/0003-9861(90)90510-6.CrossRefPubMed
8.
9.
go back to reference Gambhir JK, Lali P, Jain AK: Correlation between blood antioxidant levels and lipid peroxidation in rheumatoid arthritis. Clin Biochem. 1997, 30: 351-355. 10.1016/S0009-9120(96)00007-0.CrossRefPubMed Gambhir JK, Lali P, Jain AK: Correlation between blood antioxidant levels and lipid peroxidation in rheumatoid arthritis. Clin Biochem. 1997, 30: 351-355. 10.1016/S0009-9120(96)00007-0.CrossRefPubMed
10.
go back to reference Iozzo RV: Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem. 1998, 67: 609-652. 10.1146/annurev.biochem.67.1.609.CrossRefPubMed Iozzo RV: Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem. 1998, 67: 609-652. 10.1146/annurev.biochem.67.1.609.CrossRefPubMed
11.
go back to reference Friman C, Eronen I, Videman T: Plasma glycosaminoglycans in experimental osteoarthritis caused by immobilization. J Rheumatol. 1982, 9: 292-294.PubMed Friman C, Eronen I, Videman T: Plasma glycosaminoglycans in experimental osteoarthritis caused by immobilization. J Rheumatol. 1982, 9: 292-294.PubMed
12.
go back to reference Reddy GK, Dhar SC: Metabolism of glycosaminoglycans in tissue of arthritic rat. Mol Cell Biochem. 1991, 106: 117-124.PubMed Reddy GK, Dhar SC: Metabolism of glycosaminoglycans in tissue of arthritic rat. Mol Cell Biochem. 1991, 106: 117-124.PubMed
13.
go back to reference Caterson B, Flannery CR, Hughes CE, Little CB: Mechanisms involved in cartilage proteoglycan catabolism. Matrix Biol. 2000, 19: 333-344. 10.1016/S0945-053X(00)00078-0.CrossRefPubMed Caterson B, Flannery CR, Hughes CE, Little CB: Mechanisms involved in cartilage proteoglycan catabolism. Matrix Biol. 2000, 19: 333-344. 10.1016/S0945-053X(00)00078-0.CrossRefPubMed
14.
go back to reference Campo GM, Squadrito F, Altavilla D, Squadrito Giov, Avenoso A, Canale P, Ioculano M, Sperandeo A, Caputi AP: Protection of ischemic and reperfused rat myocardium by the nonglucocorticoid 21-aminosteroid U-74389G, a new inhibitor of lipid peroxidation. J Pharmacol Exp Ther. 1996, 277: 333-340.PubMed Campo GM, Squadrito F, Altavilla D, Squadrito Giov, Avenoso A, Canale P, Ioculano M, Sperandeo A, Caputi AP: Protection of ischemic and reperfused rat myocardium by the nonglucocorticoid 21-aminosteroid U-74389G, a new inhibitor of lipid peroxidation. J Pharmacol Exp Ther. 1996, 277: 333-340.PubMed
15.
go back to reference Kroger H, Miesel R, Dietrich A, Ohde M, Altrichter S, Braun C, Ockenfels H: Suppression of type II collagen-induced arthritis by N-acetyl-L-cysteine in mice. Gen Pharmacol. 1997, 29: 671-674. 10.1016/S0306-3623(96)00570-8.CrossRefPubMed Kroger H, Miesel R, Dietrich A, Ohde M, Altrichter S, Braun C, Ockenfels H: Suppression of type II collagen-induced arthritis by N-acetyl-L-cysteine in mice. Gen Pharmacol. 1997, 29: 671-674. 10.1016/S0306-3623(96)00570-8.CrossRefPubMed
16.
go back to reference Campo GM, Squadrito F, Campo S, Altavilla D, Quartarone C, Ceccarelli S, Ferlito M, Avenoso A, Squadrito G, Saitta A, Caputi AP: Beneficial effect of Raxofelast, an hydrophilic vitamin E analogue, in the rat heart after ischemia and reperfusion injury. J Mol Cell Cardiol. 1998, 30: 1493-1503. 10.1006/jmcc.1998.0713.CrossRefPubMed Campo GM, Squadrito F, Campo S, Altavilla D, Quartarone C, Ceccarelli S, Ferlito M, Avenoso A, Squadrito G, Saitta A, Caputi AP: Beneficial effect of Raxofelast, an hydrophilic vitamin E analogue, in the rat heart after ischemia and reperfusion injury. J Mol Cell Cardiol. 1998, 30: 1493-1503. 10.1006/jmcc.1998.0713.CrossRefPubMed
17.
go back to reference Campo GM, Squadrito F, Ceccarelli S, Calò M, Avenoso A, Campo S, Squadrito G, Altavilla D: Reduction of Carbon tetrachloride-induced rat liver injury by IRFI 042, a novel dual vitamin E-like antioxidant. Free Radic Res. 2001, 34: 379-393.CrossRefPubMed Campo GM, Squadrito F, Ceccarelli S, Calò M, Avenoso A, Campo S, Squadrito G, Altavilla D: Reduction of Carbon tetrachloride-induced rat liver injury by IRFI 042, a novel dual vitamin E-like antioxidant. Free Radic Res. 2001, 34: 379-393.CrossRefPubMed
18.
go back to reference Sato H, Takahashi T, Ide H, Fukushima T, Tabata M, Sekine F, Kobayashi K, Negishi M, Niwa Y: Antioxidant activity of synovial fluid, hyaluronic acid, and two subcomponents of hyaluronic acid. Synovial fluid scavenging effect is enhanced in rheumatoid arthritis patients. Arthritis Rheum. 1988, 31: 63-71.CrossRefPubMed Sato H, Takahashi T, Ide H, Fukushima T, Tabata M, Sekine F, Kobayashi K, Negishi M, Niwa Y: Antioxidant activity of synovial fluid, hyaluronic acid, and two subcomponents of hyaluronic acid. Synovial fluid scavenging effect is enhanced in rheumatoid arthritis patients. Arthritis Rheum. 1988, 31: 63-71.CrossRefPubMed
19.
go back to reference Presti D, Scott JE: Hyaluronan-mediated protective effect against cell damage caused by enzymatically produced hydroxyl (OH) radicals is dependent on hyaluronan molecular mass. Cell Biochem Funct. 1994, 12: 281-288.CrossRefPubMed Presti D, Scott JE: Hyaluronan-mediated protective effect against cell damage caused by enzymatically produced hydroxyl (OH) radicals is dependent on hyaluronan molecular mass. Cell Biochem Funct. 1994, 12: 281-288.CrossRefPubMed
20.
go back to reference Cortivo R, Brun P, Cardarelli L, O'Regan M, Radice M, Abatan-gelo G: Antioxidant effects of hyaluronan and its alpha-methyl-prednisolone derivative in chondrocyte and cartilage cultures. Semin Arthritis Rheum. 1996, 26: 492-501. 10.1016/S0049-0172(96)80030-8.CrossRefPubMed Cortivo R, Brun P, Cardarelli L, O'Regan M, Radice M, Abatan-gelo G: Antioxidant effects of hyaluronan and its alpha-methyl-prednisolone derivative in chondrocyte and cartilage cultures. Semin Arthritis Rheum. 1996, 26: 492-501. 10.1016/S0049-0172(96)80030-8.CrossRefPubMed
21.
go back to reference Albertini R, De Luca G, Passi A, Moratti R, Abuja PM: Chondroitin-4-sulfate protects high-density lipoprotein against copper-dependent oxidation. Arch Biochem Biophys. 1999, 365: 143-149. 10.1006/abbi.1999.1150.CrossRefPubMed Albertini R, De Luca G, Passi A, Moratti R, Abuja PM: Chondroitin-4-sulfate protects high-density lipoprotein against copper-dependent oxidation. Arch Biochem Biophys. 1999, 365: 143-149. 10.1006/abbi.1999.1150.CrossRefPubMed
22.
go back to reference Sela S, Shurtz-Swirski R, Shapiro G, Nasser L, Hamzi M, Shasha SM, Kristal B: Oxidative stress during hemodialysis: effect of heparin. Kidney Int. 2001, 78: S159-S163. 10.1046/j.1523-1755.2001.07830.x.CrossRef Sela S, Shurtz-Swirski R, Shapiro G, Nasser L, Hamzi M, Shasha SM, Kristal B: Oxidative stress during hemodialysis: effect of heparin. Kidney Int. 2001, 78: S159-S163. 10.1046/j.1523-1755.2001.07830.x.CrossRef
23.
go back to reference Cremer M: Type II collagen-induced arthritis in rats. In Handbook of Animal Models for the Rheumatic Diseases. Edited by: Greenwald RA, Diamond HS. 1988, Boca Raton, FL: CRC Press, 1: 17-27. Cremer M: Type II collagen-induced arthritis in rats. In Handbook of Animal Models for the Rheumatic Diseases. Edited by: Greenwald RA, Diamond HS. 1988, Boca Raton, FL: CRC Press, 1: 17-27.
24.
go back to reference Campo GM, Campo S, Ferlazzo AM, Vinci R, Calatroni A: Improved high-performance liquid chromatographic method to estimate aminosugars and its application to glycosaminoglycan determination in plasma and serum. J Chromatogr. 2001, 765: 151-160. 10.1016/S0378-4347(01)00427-3.CrossRef Campo GM, Campo S, Ferlazzo AM, Vinci R, Calatroni A: Improved high-performance liquid chromatographic method to estimate aminosugars and its application to glycosaminoglycan determination in plasma and serum. J Chromatogr. 2001, 765: 151-160. 10.1016/S0378-4347(01)00427-3.CrossRef
25.
go back to reference Larsson P, Kleinau S, Holmdahl R, Klareskog L: Homologous type II collagen-induced arthritis in rats. Characterization of the disease and demonstration of clinically distinct forms of arthritis in two strains of rats after immunization with the same collagen preparation. Arthritis Rheum. 1990, 33: 693-701.CrossRefPubMed Larsson P, Kleinau S, Holmdahl R, Klareskog L: Homologous type II collagen-induced arthritis in rats. Characterization of the disease and demonstration of clinically distinct forms of arthritis in two strains of rats after immunization with the same collagen preparation. Arthritis Rheum. 1990, 33: 693-701.CrossRefPubMed
26.
go back to reference Durie FH, Fava RA, Foy TM, Aruffo A, Ledbetter JA, Noelle RJ: Prevention of collagen-induced arthritis with an antibody to gp39, the ligand for CD40. Science. 1993, 261: 1328-1330.CrossRefPubMed Durie FH, Fava RA, Foy TM, Aruffo A, Ledbetter JA, Noelle RJ: Prevention of collagen-induced arthritis with an antibody to gp39, the ligand for CD40. Science. 1993, 261: 1328-1330.CrossRefPubMed
27.
go back to reference Ellman GL: Tissue sulphydryl groups. Arch Biochem Biophys. 1959, 82: 70-77. 10.1016/0003-9861(59)90090-6.CrossRefPubMed Ellman GL: Tissue sulphydryl groups. Arch Biochem Biophys. 1959, 82: 70-77. 10.1016/0003-9861(59)90090-6.CrossRefPubMed
28.
go back to reference Lefkowitz DL, Gelderman MP, Fuhrmann SR, Grahams Starnes JD, Lefkowitz SS, Bollen A, Moguilevsky N: Neutrophil myeloperoxidase-macrophage interactions perpetuate chronic inflammation associated with experimental arthritis. Clin Immun. 1999, 91: 145-155. 10.1006/clim.1999.4696.CrossRef Lefkowitz DL, Gelderman MP, Fuhrmann SR, Grahams Starnes JD, Lefkowitz SS, Bollen A, Moguilevsky N: Neutrophil myeloperoxidase-macrophage interactions perpetuate chronic inflammation associated with experimental arthritis. Clin Immun. 1999, 91: 145-155. 10.1006/clim.1999.4696.CrossRef
29.
go back to reference Mullane KM, Kraemer R, Smith B: Myeloperoxidase activity as a quantitative assessment of neutrophil infiltration into ischaemic myocardium. J Pharmacol Methods. 1985, 14: 157-167. 10.1016/0160-5402(85)90029-4.CrossRefPubMed Mullane KM, Kraemer R, Smith B: Myeloperoxidase activity as a quantitative assessment of neutrophil infiltration into ischaemic myocardium. J Pharmacol Methods. 1985, 14: 157-167. 10.1016/0160-5402(85)90029-4.CrossRefPubMed
30.
go back to reference Bauerova K, Bezek A: Role of reactive oxygen and nitrogen species in etiopathogenesis of rheumatoid arthritis. Gen Physiol Biophys. 1999, 18: 15-20.PubMed Bauerova K, Bezek A: Role of reactive oxygen and nitrogen species in etiopathogenesis of rheumatoid arthritis. Gen Physiol Biophys. 1999, 18: 15-20.PubMed
31.
go back to reference VanderBorght A, Geusens P, Raus J, Stinissen P: The autoimmune pathogenesis of rheumatoid arthritis: role of autoreactive T cells and new immunotherapies. Semin Arthritis Rheum. 2001, 31: 160-175. 10.1053/sarh.2001.27736.CrossRefPubMed VanderBorght A, Geusens P, Raus J, Stinissen P: The autoimmune pathogenesis of rheumatoid arthritis: role of autoreactive T cells and new immunotherapies. Semin Arthritis Rheum. 2001, 31: 160-175. 10.1053/sarh.2001.27736.CrossRefPubMed
32.
go back to reference Knight JA: Free radicals, antioxidants, and the immune system. Ann Clin Lab Sci. 2000, 30: 145-158.PubMed Knight JA: Free radicals, antioxidants, and the immune system. Ann Clin Lab Sci. 2000, 30: 145-158.PubMed
33.
go back to reference Babior BM: Phagocytes and oxidative stress. Am J Med. 2000, 109: 33-44. 10.1016/S0002-9343(00)00481-2.CrossRefPubMed Babior BM: Phagocytes and oxidative stress. Am J Med. 2000, 109: 33-44. 10.1016/S0002-9343(00)00481-2.CrossRefPubMed
34.
go back to reference Haqqi TM, Anthony DD, Gupta S, Ahmad N, Lee MS, Kumars GK, Mukhtar H: Prevention of collagen-induced arthritis in mice by a polyphenolic fraction from green tea. Proc Natl Acad Sci USA. 1999, 96: 4524-4529. 10.1073/pnas.96.8.4524.PubMedCentralCrossRefPubMed Haqqi TM, Anthony DD, Gupta S, Ahmad N, Lee MS, Kumars GK, Mukhtar H: Prevention of collagen-induced arthritis in mice by a polyphenolic fraction from green tea. Proc Natl Acad Sci USA. 1999, 96: 4524-4529. 10.1073/pnas.96.8.4524.PubMedCentralCrossRefPubMed
35.
go back to reference Corvo ML, Boerman OC, Oyen WJG, Van Bloois LV, Cruz MEM, Crommelin DJA, Storm G: Intravenous administration of superoxide dismutase entrapped in long circulating liposomes. II. In vivo fate in a rat model of adjuvant arthritis. Biochim Biophys Acta. 1999, 1419: 325-334. 10.1016/S0005-2736(99)00081-4.CrossRefPubMed Corvo ML, Boerman OC, Oyen WJG, Van Bloois LV, Cruz MEM, Crommelin DJA, Storm G: Intravenous administration of superoxide dismutase entrapped in long circulating liposomes. II. In vivo fate in a rat model of adjuvant arthritis. Biochim Biophys Acta. 1999, 1419: 325-334. 10.1016/S0005-2736(99)00081-4.CrossRefPubMed
36.
go back to reference Sakai A, Hirano T, Okazaki R, Okimoto N, Tanaka K, Nakamura T: Large-dose ascorbic acid administration suppresses the development of arthritis in adjuvant-infected rats. Arch Orthop Trauma Surg. 1999, 119: 121-126. 10.1007/s004020050374.CrossRefPubMed Sakai A, Hirano T, Okazaki R, Okimoto N, Tanaka K, Nakamura T: Large-dose ascorbic acid administration suppresses the development of arthritis in adjuvant-infected rats. Arch Orthop Trauma Surg. 1999, 119: 121-126. 10.1007/s004020050374.CrossRefPubMed
37.
go back to reference Darlington LG, Stone TW: Antioxidants and fatty acids in the amelioration of rheumatoid arthritis and related disorders. Br J Nutr. 2001, 85: 251-269.CrossRefPubMed Darlington LG, Stone TW: Antioxidants and fatty acids in the amelioration of rheumatoid arthritis and related disorders. Br J Nutr. 2001, 85: 251-269.CrossRefPubMed
38.
go back to reference Ostrakhovitch EA, Afanas'ev IB: Oxidative stress in rheumatoid arthritis leukocytes: suppression by rutin and other antioxidants and chelators. Biochem Pharmacol. 2001, 62: 743-746. 10.1016/S0006-2952(01)00707-9.CrossRefPubMed Ostrakhovitch EA, Afanas'ev IB: Oxidative stress in rheumatoid arthritis leukocytes: suppression by rutin and other antioxidants and chelators. Biochem Pharmacol. 2001, 62: 743-746. 10.1016/S0006-2952(01)00707-9.CrossRefPubMed
41.
go back to reference Ferlazzo AM, Campo S, Vinci R, Ferrlazzo A, Calatroni A: Concentration and composition of serum and plasma glycosaminoglycans in domestic animal species. Comp Biochem Physiol. 1997, 118B: 935-942.CrossRef Ferlazzo AM, Campo S, Vinci R, Ferrlazzo A, Calatroni A: Concentration and composition of serum and plasma glycosaminoglycans in domestic animal species. Comp Biochem Physiol. 1997, 118B: 935-942.CrossRef
42.
go back to reference Calatroni A, Vinci R, Ferlazzo AM: Characteristics of the interactions between acid glycosaminoglycans and proteins in normal human plasma as revealed by the behaviour of the protein-polysaccharide complexes in ultrafiltration and chromatographic procedures. Clin Chim Acta. 1992, 206: 167-180. 10.1016/0009-8981(92)90086-6.CrossRefPubMed Calatroni A, Vinci R, Ferlazzo AM: Characteristics of the interactions between acid glycosaminoglycans and proteins in normal human plasma as revealed by the behaviour of the protein-polysaccharide complexes in ultrafiltration and chromatographic procedures. Clin Chim Acta. 1992, 206: 167-180. 10.1016/0009-8981(92)90086-6.CrossRefPubMed
43.
go back to reference Friman C, Nordstrom D, Eronen I: Plasma glycosaminoglycans in systemic lupus erythematosus. J Rheumatol. 1987, 14: 1132-1134.PubMed Friman C, Nordstrom D, Eronen I: Plasma glycosaminoglycans in systemic lupus erythematosus. J Rheumatol. 1987, 14: 1132-1134.PubMed
44.
go back to reference Laurent TC, Laurent UBG, Fraser JRE: Serum hyaluronan as a disease marker. Ann Med. 1996, 28: 241-253.CrossRefPubMed Laurent TC, Laurent UBG, Fraser JRE: Serum hyaluronan as a disease marker. Ann Med. 1996, 28: 241-253.CrossRefPubMed
45.
go back to reference Radhakrishnamurthy B, Tracy RE, Dalferes ER, Berenson GS: Proteoglycans in human coronary arteriosclerotic lesions. Exp Mol Pathol. 1998, 65: 1-8. 10.1006/exmp.1998.2222.CrossRefPubMed Radhakrishnamurthy B, Tracy RE, Dalferes ER, Berenson GS: Proteoglycans in human coronary arteriosclerotic lesions. Exp Mol Pathol. 1998, 65: 1-8. 10.1006/exmp.1998.2222.CrossRefPubMed
46.
go back to reference Gambaro G, van der Woude FJ: Glycosaminoglycans: use in treatment of diabetic nephropathy. J Am Soc Nephrol. 2000, 11: 359-368. 10.1159/000017267.PubMed Gambaro G, van der Woude FJ: Glycosaminoglycans: use in treatment of diabetic nephropathy. J Am Soc Nephrol. 2000, 11: 359-368. 10.1159/000017267.PubMed
47.
go back to reference Engstrom-Laurent A, Hallgren R: Circulating hyaluronate in rheumatoid arthritis: relationship to inflammatory activity and the effect of corticosteroid therapy. Ann Rheum Dis. 1985, 44: 83-88.PubMedCentralCrossRefPubMed Engstrom-Laurent A, Hallgren R: Circulating hyaluronate in rheumatoid arthritis: relationship to inflammatory activity and the effect of corticosteroid therapy. Ann Rheum Dis. 1985, 44: 83-88.PubMedCentralCrossRefPubMed
48.
go back to reference Roughley PJ: Articular cartilage and changes in arthritis: non-collagenous proteins and proteoglycans in the extracellular matrix of cartilage. Arthritis Res. 2001, 3: 342-347. 10.1186/ar326.PubMedCentralCrossRefPubMed Roughley PJ: Articular cartilage and changes in arthritis: non-collagenous proteins and proteoglycans in the extracellular matrix of cartilage. Arthritis Res. 2001, 3: 342-347. 10.1186/ar326.PubMedCentralCrossRefPubMed
49.
go back to reference Bjork J, Kleinau S, Tengblad A, Smedegard G: Elevated levels of serum hyaluronate and correlation with disease activity in experimental models of arthritis. Arthritis Rheum. 1989, 32: 306-311.CrossRefPubMed Bjork J, Kleinau S, Tengblad A, Smedegard G: Elevated levels of serum hyaluronate and correlation with disease activity in experimental models of arthritis. Arthritis Rheum. 1989, 32: 306-311.CrossRefPubMed
50.
go back to reference Van der Kraan PM, de Lange J, Vitters EL, van Beuningen HM, van Osch GJ, van Lent PL, van den Berg WB: Analysis of changes in proteoglycan content in murine articular cartilage using image analysis. Osteoarthritis Cartilage. 1994, 2: 207-214.CrossRefPubMed Van der Kraan PM, de Lange J, Vitters EL, van Beuningen HM, van Osch GJ, van Lent PL, van den Berg WB: Analysis of changes in proteoglycan content in murine articular cartilage using image analysis. Osteoarthritis Cartilage. 1994, 2: 207-214.CrossRefPubMed
51.
go back to reference Thonar EJ, Lenz ME, Klintworth GK, Caterson B, Pachman LM, Glickman P, Katz R, Huff J, Kuettner KE: Quantification of keratan sulfate in blood as a marker of cartilage catabolism. Arthritis Rheum. 1985, 28: 1367-1376.CrossRefPubMed Thonar EJ, Lenz ME, Klintworth GK, Caterson B, Pachman LM, Glickman P, Katz R, Huff J, Kuettner KE: Quantification of keratan sulfate in blood as a marker of cartilage catabolism. Arthritis Rheum. 1985, 28: 1367-1376.CrossRefPubMed
52.
go back to reference Ruoslahti E, Yamaguchi Y: Proteoglycans as modulators of growth factor activities. Cell. 1991, 64: 867-869. 10.1016/0092-8674(91)90308-L.CrossRefPubMed Ruoslahti E, Yamaguchi Y: Proteoglycans as modulators of growth factor activities. Cell. 1991, 64: 867-869. 10.1016/0092-8674(91)90308-L.CrossRefPubMed
53.
go back to reference Vestweber D, Blanks J: Mechanisms that regulate the function of the selectins and their ligands. Physiol Rev. 1999, 79: 181-213.PubMed Vestweber D, Blanks J: Mechanisms that regulate the function of the selectins and their ligands. Physiol Rev. 1999, 79: 181-213.PubMed
54.
go back to reference Haslinger B, Mandl-Weber S, Sellmayer A, Sitter T: Hyaluronan fragments induce the synthesis of MCP-1 and IL-8 in cultured human peritoneal mesothelial cells. Cell Tissue Res. 2001, 305: 79-86. 10.1007/s004410100409.CrossRefPubMed Haslinger B, Mandl-Weber S, Sellmayer A, Sitter T: Hyaluronan fragments induce the synthesis of MCP-1 and IL-8 in cultured human peritoneal mesothelial cells. Cell Tissue Res. 2001, 305: 79-86. 10.1007/s004410100409.CrossRefPubMed
55.
go back to reference Sconocchia G, Campagnano L, Adorno D, Iacona A, Cococcetta NY, Boffo V, Amadori S, Casciani CU: CD44 ligation on peripheral blood polymorphonuclear cells induces interleukin-6 production. Blood. 2001, 97: 3621-3627. 10.1182/blood.V97.11.3621.CrossRefPubMed Sconocchia G, Campagnano L, Adorno D, Iacona A, Cococcetta NY, Boffo V, Amadori S, Casciani CU: CD44 ligation on peripheral blood polymorphonuclear cells induces interleukin-6 production. Blood. 2001, 97: 3621-3627. 10.1182/blood.V97.11.3621.CrossRefPubMed
56.
go back to reference Syrokou A, Tzanakakis G, Tsegenidis T, Hjerpe A, Karamanos NK: Effects of glycosaminoglycans on proliferation of epithelial and fibroblast human malignant mesothelioma cells: a structure-function relationship. Cell Prolif. 1999, 32: 85-99. 10.1046/j.1365-2184.1999.32230085.x.CrossRefPubMed Syrokou A, Tzanakakis G, Tsegenidis T, Hjerpe A, Karamanos NK: Effects of glycosaminoglycans on proliferation of epithelial and fibroblast human malignant mesothelioma cells: a structure-function relationship. Cell Prolif. 1999, 32: 85-99. 10.1046/j.1365-2184.1999.32230085.x.CrossRefPubMed
57.
go back to reference Foschi D, Castoldi L, Radaelli E, Abelli P, Calderini G, Rastrelli A, Mariscotti C, Marazzi M, Trabucchi E: Hyaluronic acid prevents oxygen free-radical damage to granulation tissue: a study in rats. Int J Tissue React. 1990, 12: 333-339.PubMed Foschi D, Castoldi L, Radaelli E, Abelli P, Calderini G, Rastrelli A, Mariscotti C, Marazzi M, Trabucchi E: Hyaluronic acid prevents oxygen free-radical damage to granulation tissue: a study in rats. Int J Tissue React. 1990, 12: 333-339.PubMed
58.
go back to reference Arai H, Kashiwagi S, Nagasaka Y, Uchida K, Hoshii Y, Nakamura K: Oxidative modification of apolipoprotein E in human very-low-density lipoprotein and its inhibition by glycosaminoglycans. Arch Biochem Biophys. 1999, 367: 1-8. 10.1006/abbi.1999.1222.CrossRefPubMed Arai H, Kashiwagi S, Nagasaka Y, Uchida K, Hoshii Y, Nakamura K: Oxidative modification of apolipoprotein E in human very-low-density lipoprotein and its inhibition by glycosaminoglycans. Arch Biochem Biophys. 1999, 367: 1-8. 10.1006/abbi.1999.1222.CrossRefPubMed
59.
go back to reference Albertini R, Passi A, Abuja PM, De Luca G: The effect of glycosaminoglycans and proteoglycans on lipid peroxidation. Int J Mol Med. 2000, 6: 129-136.PubMed Albertini R, Passi A, Abuja PM, De Luca G: The effect of glycosaminoglycans and proteoglycans on lipid peroxidation. Int J Mol Med. 2000, 6: 129-136.PubMed
60.
go back to reference Graf J, Neusel E, Schneider E, Niethard FU: Intra-articular treatment with hyaluronic acid in osteoarthritis of the knee joint: a controlled clinical trial versus mucopolysaccharide polysulfuric acid ester. Clin Exp Rheumatol. 1993, 11: 367-372.PubMed Graf J, Neusel E, Schneider E, Niethard FU: Intra-articular treatment with hyaluronic acid in osteoarthritis of the knee joint: a controlled clinical trial versus mucopolysaccharide polysulfuric acid ester. Clin Exp Rheumatol. 1993, 11: 367-372.PubMed
61.
go back to reference Breborowicz A, Wieczorowska K, Martis L, Oreopoulos DG: Glycosaminoglycan chondroitin sulphate prevents loss of ultrafiltration during peritoneal dialysis in rats. Nephron. 1994, 67: 346-350.CrossRefPubMed Breborowicz A, Wieczorowska K, Martis L, Oreopoulos DG: Glycosaminoglycan chondroitin sulphate prevents loss of ultrafiltration during peritoneal dialysis in rats. Nephron. 1994, 67: 346-350.CrossRefPubMed
62.
go back to reference Shankland WE: The effects of glucosamine and chondroitin sulfate on osteoarthritis of the TMJ: a preliminary report of 50 patients. Cranio. 1998, 16: 230-235.PubMed Shankland WE: The effects of glucosamine and chondroitin sulfate on osteoarthritis of the TMJ: a preliminary report of 50 patients. Cranio. 1998, 16: 230-235.PubMed
63.
go back to reference Leffler CT, Philippi AF, Leffler SG, Mosure JC, Kim PD: Glucosamine, chondroitin, and manganese ascorbate for degenerative joint disease of the knee or low back: a randomized, double-blind, placebo-controlled pilot study. Mil Med. 1999, 164: 85-91.PubMed Leffler CT, Philippi AF, Leffler SG, Mosure JC, Kim PD: Glucosamine, chondroitin, and manganese ascorbate for degenerative joint disease of the knee or low back: a randomized, double-blind, placebo-controlled pilot study. Mil Med. 1999, 164: 85-91.PubMed
64.
go back to reference Beren J, Hill SL, Diener-West M, Rose NR: Effect of preloading oral glucosamine HCl/chondroitin sulfate/manganese ascorbate combination on experimental arthritis in rats. Exp Biol Med. 2001, 226: 144-151. Beren J, Hill SL, Diener-West M, Rose NR: Effect of preloading oral glucosamine HCl/chondroitin sulfate/manganese ascorbate combination on experimental arthritis in rats. Exp Biol Med. 2001, 226: 144-151.
65.
go back to reference Jira W, Spiteller G, Richter A: Increased levels of lipid oxidation products in low density lipoproteins of patients suffering from rheumatoid arthritis. Chem Phys Lipids. 1997, 87: 81-89. 10.1016/S0009-3084(97)00030-3.CrossRefPubMed Jira W, Spiteller G, Richter A: Increased levels of lipid oxidation products in low density lipoproteins of patients suffering from rheumatoid arthritis. Chem Phys Lipids. 1997, 87: 81-89. 10.1016/S0009-3084(97)00030-3.CrossRefPubMed
66.
go back to reference Wills ED: Evaluation of lipid peroxidation in lipid and biological membranes. In Biochemical Toxicology; a Practical Approach. Edited by: Snell K, Mullock B. 1987, Oxford: IRL Press, 127-152. Wills ED: Evaluation of lipid peroxidation in lipid and biological membranes. In Biochemical Toxicology; a Practical Approach. Edited by: Snell K, Mullock B. 1987, Oxford: IRL Press, 127-152.
67.
go back to reference Kizilntuc A, Cogalgil S, Cerrahoglu L: Carnitine and antioxidants levels in patients with rheumatoid arthritis. Scand J Rheumatol. 1998, 27: 441-445. 10.1080/030097498442271.CrossRef Kizilntuc A, Cogalgil S, Cerrahoglu L: Carnitine and antioxidants levels in patients with rheumatoid arthritis. Scand J Rheumatol. 1998, 27: 441-445. 10.1080/030097498442271.CrossRef
68.
go back to reference Hassan MQ, Hadi RA, Al-Rawi ZS, Padron VA, Stohs SJ: The glutathione defense system in the pathogenesis of rheumatoid arthritis. J Appl Toxicol. 2001, 21: 69-73. 10.1002/jat.736.CrossRefPubMed Hassan MQ, Hadi RA, Al-Rawi ZS, Padron VA, Stohs SJ: The glutathione defense system in the pathogenesis of rheumatoid arthritis. J Appl Toxicol. 2001, 21: 69-73. 10.1002/jat.736.CrossRefPubMed
69.
go back to reference Feldmann M, Brennan FM, Foxwell BM, Maini RN: The role of TNF-alpha and IL-1 in rheumatoid arthritis. Curr Dir Autoimmun. 2001, 3: 188-199.CrossRefPubMed Feldmann M, Brennan FM, Foxwell BM, Maini RN: The role of TNF-alpha and IL-1 in rheumatoid arthritis. Curr Dir Autoimmun. 2001, 3: 188-199.CrossRefPubMed
70.
go back to reference Volpi N, Tarugi P: Influence of chondroitin sulfate charge density, sulfate group position, and molecular mass on Cu++-mediated oxidation of human low-density lipoproteins: effect of normal human plasma-derived chondroitin sulfate. J Biochem (Tokyo). 1999, 125: 297-304.CrossRef Volpi N, Tarugi P: Influence of chondroitin sulfate charge density, sulfate group position, and molecular mass on Cu++-mediated oxidation of human low-density lipoproteins: effect of normal human plasma-derived chondroitin sulfate. J Biochem (Tokyo). 1999, 125: 297-304.CrossRef
71.
go back to reference Palmieri L, Conte A, Giovannini L, Lualdi P, Ronca G: Metabolic fate of exogenous chondroitin sulfate in the experimental animal. Arzneimittelforschung. 1990, 40: 319-323.PubMed Palmieri L, Conte A, Giovannini L, Lualdi P, Ronca G: Metabolic fate of exogenous chondroitin sulfate in the experimental animal. Arzneimittelforschung. 1990, 40: 319-323.PubMed
72.
go back to reference Gustafson S, Bjorkman T: Circulating hyaluronan, chondroitin sulphate and dextran sulphate bind to a liver receptor that does not recognize heparin. Glycoconj J. 1997, 14: 561-568. 10.1023/A:1018528308132.CrossRefPubMed Gustafson S, Bjorkman T: Circulating hyaluronan, chondroitin sulphate and dextran sulphate bind to a liver receptor that does not recognize heparin. Glycoconj J. 1997, 14: 561-568. 10.1023/A:1018528308132.CrossRefPubMed
73.
go back to reference Omata T, Itokazu Y, Inoue N, Segawa Y: Effects of chondroitin sulfate-C on articular cartilage destruction in murine collagen-induced arthritis. Arzneimittelforschung. 2000, 50: 148-153.PubMed Omata T, Itokazu Y, Inoue N, Segawa Y: Effects of chondroitin sulfate-C on articular cartilage destruction in murine collagen-induced arthritis. Arzneimittelforschung. 2000, 50: 148-153.PubMed
Metadata
Title
Efficacy of treatment with glycosaminoglycans on experimental collagen-induced arthritis in rats
Authors
Giuseppe M Campo, PhD
Angela Avenoso
Salvatore Campo
Alida M Ferlazzo
Domenica Altavilla
Alberto Calatroni
Publication date
01-06-2003
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 3/2003
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar748

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