499
Views
22
CrossRef citations to date
0
Altmetric
Research Article

Effects of high mobility group box protein-1, interleukin-1β, and interleukin-6 on cartilage matrix metabolism in three-dimensional equine chondrocyte cultures

, , , , , & show all
Pages 290-300 | Received 19 Feb 2010, Accepted 10 Sep 2010, Published online: 30 Nov 2010

REFERENCES

  • Pool, R.R., and Meagher, D.M. (1990). Pathologic findings and pathogenesis of racetrack injuries. In The Veterinary Clinics of North America: Equine Practice, A.S. Turner and N.L. Goodman ( eds.) pp. 1–30. Philadelphia: W.B. Saunders Company.
  • Frisbie, D.D. (2006). Synovial joint biology and pathobiology. In Equine Surgery, J.A. Auer and J.A. Stick ( eds.) pp. 1036–1055. St. Louis: Saunders Elsevier.
  • McIlwraith, C.W. (1996). General pathobiology of the joint and response to injury. In Joint Disease in the Horse, C.W. McIlwraith and G.W. Trotter ( eds.) pp. 40–70. Philadelphia: W.B. Saunders Company.
  • Murray, R.C., Birch, H.L., Lakhani, K., and Goodship, A.E. (2001). Biochemical composition of equine carpal articular cartilage is influenced by short-term exercise in a site-specific manner. Osteoarthr. Cartil. 9:625–632.
  • Palmer, J.L., Bertone, A.L., Malemud, C.J., Carter, B.G., Papay, R.S., and Mansour, J. (1995). Site-specific proteoglycan characteristics of third carpal articular cartilage in exercised and nonexercised horses. Am. J. Vet. Res. 56: 1570–1576.
  • Palmer, J.L., Bertone, A.L., and Litsky, A.S. (1994). Contact area and pressure distribution changes of the equine third carpal bone during loading. Equine Vet. J. 26:197–202.
  • Little, C.B., Ghosh, P., and Rose, R. (1997). The effect of strenuous versus moderate exercise on the metabolism of proteoglycans in articular cartilage from different weight-bearing regions of the equine third carpal bone. Osteoarthr. Cartil. 5:161–172.
  • Morris, E.A., McDonald, B.S., Webb, A.C., and Rosenwasser, L.J. (1990). Identification of interleukin-1 in equine osteoarthritic joint effusions. Am. J. Vet. Res. 51:59–64.
  • Alwan, W.H., Carter, S.D., Dixon, J.B., Bennett, D., May, S.A., and Edwards, G.B. (1991). Interleukin-1-like activity in synovial fluids and sera of horses with arthritis. Res. Vet. Sci. 51:72–77.
  • Caron, J.P., Tardif, G., Martel-Pelletier, J., DiBattista, J.A., Geng, C., and Pelletier, J.P. (1996). Modulation of matrix metalloprotease 13 (collagenase 3) gene expression in equine chondrocytes by interleukin 1 and corticosteroids. Am. J. Vet. Res. 57:1631–1634.
  • Richardson, D.W., and Dodge, G.R. (2000). Effects of interleukin-1β and tumor necrosis factor-α on expression of matrix-related genes by cultured equine articular chondrocytes. Am. J. Vet. Res. 61:624–630.
  • Tung, J.T., Fenton, J.I., Arnold, C., Alexander, L., Yuzbasiyan-Gurkan, V., Venta, P.J., Peters, T.L., Orth, M.W., Richardson, D.W., and Caron, J.P. (2002). Recombinant equine interleukin-1β induces putative mediators of articular cartilage degradation in equine chondrocytes. Can. J. Vet. Res. 66:19–25.
  • Little, C.B., Flannery, C.R., Hughes, C.E., Goodship, A., and Caterson, B. (2005). Cytokine induced metalloproteinase expression and activity does not correlate with focal susceptibility of articular cartilage to degeneration. Osteoarthr. Cartil. 13:162–170.
  • Takafuji, V.A., Howard, R.D., Ward, D.L., Sharova, L.V., and Crisman, M.V. (2005). Modulation of equine articular chondrocyte messenger RNA levels following brief exposures to recombinant equine interleukin-1β. Vet. Immunol. Immunopathol. 106:23–38.
  • Garvican, E.R., Vaughan-Thomas, A., Redmond, C., and Clegg, P.D. (2008). MT3-MMP (MMP-16) is downregulated by in vitro cytokine stimulation of cartilage, but unaltered in naturally occurring equine osteoarthritis and osteochondrosis. Connect. Tissue Res. 49:62–67.
  • MacDonald, M.H., Stover, S.M., Willits, N.H., and Benton, H.P. (1992). Regulation of matrix metabolism in equine cartilage explant cultures by interleukin 1. Am. J. Vet. Res. 53:2278–2285.
  • Morris, E.A., and Treadwell, B.V. (1994). Effect of interleukin 1 on articular cartilage from young and aged horses and comparison with metabolism of osteoarthritic cartilage. Am. J. Vet. Res. 55:138–146.
  • Platt, D., and Bayliss, M.T. (1994). An investigation of the proteoglycan metabolism of mature equine articular cartilage and its regulation by interleukin-1. Equine Vet. J. 26:297–303.
  • Bird, J.L., Wells, T., Platt, D., and Bayliss, M.T. (1997). IL-1β induces the degradation of equine articular cartilage by a mechanism that is not mediated by nitric oxide. Biochem. Biophys. Res. Commun. 238:81–85.
  • Frean, S.P., Gettinby, G., May, S.A., and Lees, P. (2000). Influence of interleukin-1β and hyaluronan on proteoglycan release from equine navicular hyaline cartilage and fibrocartilage. J. Vet. Pharmacol. Therap. 23:67–72.
  • Gregg, A.J., Fortier, L.A., Mohammed, H.O., Mayr, K.G., Miller, B.J., and Haupt, J.L. (2006). Assessment of the catabolic effects of interleukin-1β on proteoglycan metabolism in equine cartilage cocultured with synoviocytes. Am. J. Vet. Res. 67:957–962.
  • Richardson D.W., and Dodge, G.R. (1997). Cloning of equine type II procollagen and the modulation of its expression in cultured equine articular chondrocytes. Matrix Biol. 16:59–64.
  • von Rechenberg, B., Leutenegger, C., Zlinsky, K., McIlwraith, C.W., Akens, M.K., and Auer, J.A. (2001). Upregulation of mRNA of interleukin-1 and -6 in subchondral cystic lesions of four horses. Equine Vet. J. 33:143–149.
  • Ley, C., Ekman, S., Ronéus, B., and Eloranta, M.L. (2009). Interleukin-6 and high mobility group box protein-1 in synovial membranes and osteochondral fragments in equine osteoarthritis. Res. Vet. Sci. 86:490–497.
  • Ley, C., Ekman, S., Elmén, A., Nilsson, G., and Eloranta, M.L. (2007). Interleukin-6 and tumour necrosis factor in synovial fluid from horses with carpal joint pathology. J. Vet. Med. A. Physiol. Pathol. Clin. Med. 54:346–351.
  • Andersson, U., and Erlandsson-Harris, H. (2004). HMGB1 is a potent trigger of arthritis. J. Intern. Med. 255:344–350.
  • Brown, M.P., Trumble, T.N., and Merritt, K.A. (2009). High-mobility group box chromosomal protein 1 as a potential inflammatory biomarker of joint injury in Thoroughbreds. Am. J. Vet. Res. 70:1230–1235.
  • McIlwraith, C.W., and Bramlage, L.R. (1996). Surgical treatment of joint injury. In Joint Disease in the Horse, C.W. McIlwraith and G.W. Trotter ( eds.) pp. 292–317. Philadelphia: W.B. Saunders Company.
  • Skiöldebrand, E., Heinegård, D., Eloranta, M.-L., Nilsson, G., Dudhia, J., Sandgren, B., and Ekman, S. (2005). Enhanced concentration of COMP (cartilage oligomeric matrix protein) in osteochondral fractures from racing Thoroughbreds. J. Orthop. Res. 23:156–163.
  • Frisbie, D.D., Ray, C.S., Ionescu, M., Poole, A.R., Chapman, P.L., and McIlwraith, C.W. (1999). Measurement of synovial fluid and serum concentrations of the 846 epitope of chondroitin sulfate and of carboxy propeptides of type II procollagen for diagnosis of osteochondral fragmentation in horses. Am. J. Vet. Res. 60:306–309.
  • Stenhamre, H., Slynarski, K., Petrén, C., Tallheden, T., and Lindahl, A. (2008). Topographic variation in redifferentiation capacity of chondrocytes in the adult human knee joint. Osteoarthr. Cartil. 16:1356–1362.
  • Tallheden, T., Karlsson, C., Brunner, A., van der Lee, J., Hagg, R., Tommasini, R., and Lindahl, A. (2004). Gene expression during redifferentiation of human articular chondrocytes. Osteoarthr. Cartil. 12:525–535.
  • Penick, K.J., Solchaga, L.A., and Welter, J.F. (2005). High-throughput aggregate culture system to assess the chondrogenic potential of mesenchymal stem cells. Biotechniques 39:687–691.
  • Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCTmethod. Methods 25:402–408.
  • Hedbom, E., Antonsson, P., Hjerpe, A., Aeschlimann, D., Paulsson, M., Rosa-Pimentel, E., Sommarin, Y., Wendel, M., Oldberg, Å., and Heinegård, D. (1992). Cartilage matrix proteins. An acidic oligomeric protein (COMP) detected only in cartilage. J. Biol. Chem. 267:6132–6136.
  • Skiöldebrand, E., Lorenzo, P., Zunino, L., Rucklidge, G.J., Sandgren, B., Carlsten, J., and Ekman, S. (2001). Concentration of collagen, aggrecan and cartilage oligomeric matrix protein (COMP) in synovial fluid from equine middle carpal joints. Equine Vet. J. 33:394–402.
  • Södersten, F., Ekman, S., Eloranta, M.L., Heinegård, D., Dudhia, J., and Hultenby, K. (2005). Ultrastructural immunolocalization of cartilage oligomeric matrix protein (COMP) in relation to collagen fibrils in the equine tendon. Matrix Biol. 24:376–385.
  • Lefebvre, V., Huang, W., Harley, V.R., Goodfellow, P.N., and de Crombrugghe, B. (1997). SOX9 is a potent activator of the chondrocyte-specific enhancer of the proα1(II) collagen gene. Mol. Cell. Biol. 17:2336–2346.
  • Bridgewater, L.C., Lefebvre, V., and de Crombrugghe, B. (1998). Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J. Biol. Chem. 273:14998–15006.
  • Sekiya, I., Tsuji, K., Koopman, P., Watanabe, H., Yamada, Y., Shinomiya, K., Nifuji. A., and Noda, M. (2000). SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. J. Biol. Chem. 275:10738–10744.
  • Zhang, P., Jimenez, S.A., and Stokes, D.G. (2003). Regulation of human COL9A1 gene expression. Activation of the proximal promoter region by SOX9. J. Biol. Chem. 278:117–123.
  • Kou, I., and Ikegawa, S. (2004). SOX9-dependent and -independent transcriptional regulation of human cartilage link protein. J. Biol. Chem. 279:50942–50948.
  • Bi, W., Deng, J.M., Zhang, Z., Behringer, R.R., and de Crombrugghe, B. (1999). Sox9 is required for cartilage formation. Nat. Genet. 22:85–89.
  • Murakami, S., Lefebvre, V., and de Crombrugghe, B. (2000). Potent inhibition of the master chondrogenic factor Sox9 gene by interleukin-1 and tumor necrosis factor-α. J. Biol. Chem. 275:3687–3692.
  • Iqbal, J., Bird, J.L., Hollander, A.P., and Bayliss, M.T. (2004). Effect of matrix depleting agents on the expression of chondrocyte metabolism by equine chondrocytes. Res. Vet. Sci. 77:249–256.
  • Iqbal, J., Dudhia, J., Bird, J.L.E., and Bayliss, M.T. (2000). Age-related effects of TGF-β on proteoglycan synthesis in equine articular cartilage. Biochem. Biophys. Res. Commun. 274:467–471.
  • Taniguchi, N., Yoshida, K., Ito, T., Tsuda, M., Mishima, Y., Furumatsu, T., Ronfani, L., Abeyama, K., Kawahara, K., Komiya, S., Maruyama, I., Lotz, M., Bianchi, M.E., and Asahara, H. (2007). Stage-specific secretion of HMGB1 in cartilage regulates endochondral ossification. Mol. Cell. Biol. 27:5650–5663.
  • Sorci, G., Riuzzi, F., Arcuri, C., Giambanco, I., and Donato, R. (2004). Amphoterin stimulates myogenesis and counteracts the antimyogenic factors basic fibroblast growth factor and S100B via RAGE binding. Mol. Cell. Biol. 24:4880–4894.
  • Mitola, S., Belleri, M., Urbinati, C., Coltrini, D., Sparatore, B., Pedrazzi, M., Melloni, E., and Presta, M. (2006). Cutting edge: Extracellular high mobility group box-1 protein is a proangiogenic cytokine. J. Immunol. 176:12–15.
  • Namba, A., Aida, Y., Suzuki, N., Watanabe, Y., Kawato, T., Motohashi, M., Maeno, M., Matsumura, H., and Matsumoto, M. (2007). Effects of IL-6 and soluble IL-6 receptor on the expression of cartilage matrix proteins in human chondrocytes. Connect. Tissue Res. 48:263–270.
  • Porée, B., Kypriotou, M., Chadjichristos, C., Beauchef, G., Renard, E., Legendre, F., Melin, M., Gueret, S., Hartmann, D.-J., Malléin-Gerin, F., Pujol, J.P., Boumediene, K., and Galéra, P. (2008). Interleukin-6 (IL-6) and/or soluble IL-6 receptor down-regulation of human type II collagen gene expression in articular chondrocytes requires a decrease of Sp1·Sp3 ratio and of the binding activity of both factors to the COL2A1 promoter. J. Biol. Chem. 283:4850–4865.
  • Legendre, F., Dudhia, J., Pujol, J.P., and Bogdanowicz, P. (2003). JAK/STAT but not ERK1/ERK2 pathway mediates interleukin (IL)-6/soluble IL-6R down-regulation of type II collagen, aggrecan core, and link protein transcription in articular chondrocytes. Association with a down-regulation of SOX9 expression. J. Biol. Chem. 278:2903–2912.
  • Loeser, R.F., Yammani, R.R., Carlson, C.S., Chen, H., Cole, A., Im, H.J., Bursch, L.S., and Yan, S.D. (2005). Articular chondrocytes express the receptor for advanced glycation end products. Potential role in osteoarthritis. Arthritis Rheum. 52:2376–2385.
  • Legendre, F., Bogdanowicz, P., Boumediene, K., and Pujol, J.P. (2005). Role of interleukin 6 (IL-6)/IL-6R-induced signal transducers and activators of transcription and mitogen-activated protein kinase/extracellular signal-related kinase in upregulation of matrix metalloproteinase and ADAMTS gene expression in articular chondrocytes. J. Rheumatol. 32:1307–1316.
  • Dickinson, S.C., Vankemmelbeke, M.N., Buttle, D.J., Rosenberg, K., Heinegård, D., and Hollander, A.P. (2003). Cleavage of cartilage oligomeric matrix protein (thrombospondin-5) by matrix metalloproteinases and a disintegrin and metalloproteinase with thrombospondin motifs. Matrix Biol. 22:267–278.
  • Brama, P.A.J., TeKoppele, J.M., Bank, R.A., van Weeren, P.R., and Barneveld, A. (1999). Influence of different exercise levels and age on the biochemical characteristics of immature equine articular cartilage. Equine Vet. J. Suppl. 31:55–61.
  • Brama, P.A.J., TeKoppele, J.M., Bank, R.A., Barneveld, A., Firth, E.C., and van Weeren, P.R. (2000). The influence of strenuous exercise on collagen characteristics of articular cartilage in Thoroughbreds age 2 years. Equine Vet. J. 32:551–554.
  • Brama, P.A.J., TeKoppele, J.M., Bank, R.A., Barneveld, A., and van Weeren, P.R. (2000). Functional adaptation of equine articular cartilage: The formation of regional biochemical characteristics up to age one year. Equine Vet. J. 32:217–221.
  • Brama, P.A.J., TeKoppele, J.M., Bank, R.A., Karssenberg, D., Barneveld, A., and van Weeren, P.R. (2000). Topographical mapping of biochemical properties of articular cartilage in the equine fetlock joint. Equine Vet. J. 32:19–26.
  • Brama, P.A.J., TeKoppele, J.M., Bank, R.A., Barneveld, A., and van Weeren, P.R. (2002). Development of biochemical heterogeneity of articular cartilage: Influences of age and exercise. Equine Vet. J. 34:265–269.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.