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Changes in Cartilage Metabolism in Arthritis Are Reflected by Altered Serum and Synovial Fluid Levels of the Cartilage Proteoglycan Aggrecan

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Changes in Cartilage Metabolism in Arthritis Are Reflected by Altered Serum and Synovial Fluid Levels of the Cartilage Proteoglycan Aggrecan Changes in cartilage metabolism in arthritis are reflected by altered serum and synovial fluid levels of the cartilage proteoglycan aggrecan. Implications for pathogenesis. A R Poole, … , A Swan, P A Dieppe J Clin Invest. 1994;94(1):25-33. https://doi.org/10.1172/JCI117314. Research Article The metabolism of the cartilage proteoglycan aggrecan was studied in patients with osteoarthritis (OA, n = 83), rheumatoid arthritis (RA, n = 127), and in controls (n = 117) using monoclonal antibody-based radioimmunoassays for glycosaminoglycans in the serum and synovial fluid (SF) to detect epitope 846 on chondroitin sulfate (probably only on recently synthesized molecules) and a keratan sulfate (KS) epitope AN9PI, present on intact and degraded molecules. Epitope 846 levels were always elevated in SF over serum (mean 38-fold in OA and 8.6-fold in RA) being highest in OA patients with the longest disease duration and greatest loss of cartilage, and lowest in RA joints with high leucocyte counts. Serum levels were more often elevated in RA (56%) than in OA (19%) and probably reflect increased aggrecan synthesis in diseased joints. KS levels were higher in SF than in serum in 69% of patients (up to 2.3-fold); levels were inversely (OA) and directly (RA) related to SF leucocyte counts. Serum KS was reduced in both diseases and in RA was inversely related to both systemic and joint inflammation markers. SF 846 levels were inversely related to SF KS in both diseases. These epitopes may provide a measure of the balance between cartilage synthesis and degradation in these diseases. Find the latest version: https://jci.me/117314/pdf Changes in Cartilage Metabolism in Arthritis Are Reflected by Altered Serum and Synovial Fluid Levels of the Cartilage Proteoglycan Aggrecan Implications for Pathogenesis A. Robin Poole,* Mirela lonescu,* Angela Swan,* and Paul A. Dieppe* * Joint Diseases Laboratory, Shriners Hospital for Crippled Children, Montreal, Quebec, Canada H3G IA6; Division of Surgical Research Department of Surgery, McGill University, Montreal, Quebec, Canada H3G IA6; and tDepartment of Rheumatology, University of Bristol Medical School, Bristol Royal Infirmary, BS2 8HW Bristol, United Kingdom Abstract in both the human disease (1, 2) and in experimental models (3, 4). In contrast, intra-articular inflammation is a major feature The metabolism of the cartilage proteoglycan aggrecan was of RA, resulting in polymorphonuclear (PMN)-rich cellular studied in patients with osteoarthritis (OA, n = 83), rheu- exudates in the joints. But relatively little is known about carti- matoid arthritis (RA, n = 127), and in controls (n = 117) lage proteoglycan changes in this disease, or what influence the using monoclonal antibody-based radioimmunoassays for inflammation and the effects PMN products may have on matrix glycosaminoglycans in the serum and synovial fluid (SF) to synthesis. In RA there is excessive production of cytokines detect epitope 846 on chondroitin sulfate (probably only on such as interleukin la and 13 (5, 6), and these may stimulate recently synthesised molecules) and a keratan sulfate (KS) chondrocyte-mediated matrix degradation (7-9). There is both epitope AN9PI, present on intact and degraded molecules. in vivo (10) and in vitro (11-14) evidence that these same Epitope 846 levels were always elevated in SF over serum cytokines can act as potent inhibitors of matrix synthesis, at (mean 38-fold in OA and 8.6-fold in RA) being highest in concentrations at least an order of magnitude less than those OA patients with the longest disease duration and greatest required to stimulate degradation ( 11). loss of cartilage, and lowest in RA joints with high leucocyte The extensive extracellular matrix of hyaline cartilage con- counts. Serum levels were more often elevated in RA (56%) tains a dense network of composite collagen fibrils composed than in OA (19%) and probably reflect increased aggrecan mainly of type II, together with type IX and XI collagens (9). synthesis in diseased joints. KS levels were higher in SF Contained within this network are large proteoglycans (called than in serum in 69% of patients (up to 2.3-fold); levels aggrecan) many of which can aggregate with hyaluronic acid. were inversely (OA) and directly (RA) related to SF leuco- In adult cartilage, these molecules contain a relatively large cyte counts. Serum KS was reduced in both diseases and in proportion of the glycosaminoglycan keratan sulfate (KS) in RA was inversely related to both systemic and joint in- addition to chondroitin sulfate (CS) (15). Proteoglycans iso- flammation markers. SF 846 levels were inversely related lated from adult articular cartilage consist of partially degraded to SF KS in both diseases. molecules containing the KS rich region of aggrecan (16, 17). These epitopes may provide a measure of the balance Previous studies of aggrecan from fetal, immature, and adult between cartilage synthesis and degradation in these dis- articular cartilage revealed that an epitope identified by a mono- eases. (J. Clin. Invest. 1994. 94:25-33.) Key words: carti- clonal antibody called 846 (which is chondroitin ABC lyase lage aggrecan rheumatoid arthritis osteoarthritis labile), is most concentrated in the fetus (18). This CS-related epitope disappears progressively with aging, alongside a relative Introduction increase in the amount of KS in cartilage; the 846 epitope is almost absent from mature adult cartilage (17, 18). However, Destruction and remodeling of articular cartilage are features in OA this epitope is usually present in increased content, lo- of both rheumatoid arthritis (RA) ' and osteoarthritis (OA) ( 1 ). cated on the largest of the aggrecan molecules (17). It may be In OA, where there is relatively little synovial inflammation, confined to the most intact and recently synthesized aggrecan the cartilage matrix degradation is usually accompanied by en- molecules, and may therefore be a marker of aggrecan synthesis. hanced synthesis of proteoglycans. This has been demonstrated Related native CS epitopes also appear in the articular cartilage of dogs with experimental OA ( 19), and in human OA cartilage (20). These CS epitopes, including the 846 epitope, have not Address correspondence to Professor P. A. Dieppe, Department of Rheu- been detected in other adult tissues (Poole, A. R., and A. Reiner, matology, University of Bristol, Medical School, Bristol Royal Infir- unpublished results). mary, BS2 8HW Bristol, U.K. Using antibodies to core protein and KS epitopes on ag- Received for publication 9 August 1993 and in revised form 15 grecan, we and others have shown that degradation products February 1994. can be found in synovial fluids (SF) and sera of patients with a variety of different types of arthritis (21-30). KS-containing 1. Abbreviations used in this paper: CS, chondroitin sulfate; ECP, eo- fragments, measured by ELISA, have been shown to be present sinophil cationic protein; KS, keratan sulfate; MPO, myeloperoxidase; in increased amounts in the SF, and possibly in the serum, of OA, osteoarthritis; PMN, polymorphonuclear leucocytes; RA, rheuma- toid arthritis; SF, synovial fluid. patients with OA (22-25), although they may be unchanged or decreased in content in the sera of patients with RA (29, J. Clin. Invest. 30). Our previous studies using an immunoassay which detects ©D The American Society for Clinical Investigation, Inc. relatively large PG fragments containing KS (31 ), revealed that 002 1-9738/94/07/0025/09 $2.00 there was an inverse correlation between the content of these Volume 94, July 1994, 25-33 molecules and the acute phase reactant orosomucoid in the sera Cartilage Markers in Arthritis 25 of patients with RA (29). A similar observation has since been Table 1. Details of Patient Groups Examined recorded by another group using a different KS assay (30). More recently an inverse correlation has been observed between Non-arthritic serum KS (32) and TNFa levels, indicating an effect of in- Age normals Osteoarthritis Rheumatoid arthritis flammation on systemic cartilage metabolism. However, 20-30 2 2 changes in the content of KS-rich degradation products in arthri- 30-40 2 - 8 tis could also result from differences in the reactivity of antibod- 40-50 25 5 7 ies to KS in large and small fragments, as a result of changes 50-60 25 23 34 in epitope density, an effect that can be minimized by the use 60-70 34 21 44 of monovalent Fab fragments (31). 70-80 12 27 30 In the present study, we have studied patients with RA and 80-90 16 7 2 OA, as well as a group of subjects without arthritis. We have Total 117 83 127 shown that proteoglycan fragments bearing the CS epitope 846, as well as KS, are detectable in sera and SFs. We demonstrate significant differences in the levels of these fragments in patients with OA and RA. The 846 epitope is strikingly elevated in sera of patients with RA in contrast to reduced KS levels. In SF the Radiographs. A radiograph of the knee joint from which SF had 846 epitope also shows marked elevations in this case over been aspirated was obtained within three months of the time of aspira- tion. Different radiographic features, including joint space narrowing, serum levels, and especially in OA. We have specifically inves- erosions, and osteophytosis were scored on a 0-1-2 scale (absent, tigated the hypothesis that the SF concentration of these ag- present, severe). grecan fragments will be related to the degree of local inflam- Total joint score. These were determined as previously described mation and severity of joint damage, whereas serum levels will (34). Scores for each affected joint are totaled. relate to the degree of systemic disease activity. Inflammation markers. In addition to assays of total and differential leucocyte counts in the SF, immunoassays of PMN and eosinophil de- Methods granulation were used. Both eosinophilic cationic protein (ECP) and myeloperoxidase (MPO) levels were estimated with assay kits obtained Subjects.
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