Research Article

You have full text access to this OnlineOpen article

Interleukin-1α induction of tensile weakening associated with collagen degradation in bovine articular cartilage

  1. Michele M. Temple,
  2. Yang Xue,
  3. Michael Q. Chen,
  4. Robert L. Sah*

Article first published online: 28 SEP 2006

DOI: 10.1002/art.22145

Issue

Arthritis & Rheumatism

Arthritis & Rheumatism

Volume 54, Issue 10, pages 3267–3276, October 2006

Additional Information

How to Cite

Temple, M. M., Xue, Y., Chen, M. Q. and Sah, R. L. (2006), Interleukin-1α induction of tensile weakening associated with collagen degradation in bovine articular cartilage. Arthritis & Rheumatism, 54: 3267–3276. doi: 10.1002/art.22145

Author Information

  1. University of California, San Diego

*Department of Bioengineering, University of California, San Diego, 9500 Gilman Drive, Mail Code 0412, La Jolla, CA 92093-0412

Publication History

  1. Issue published online: 28 SEP 2006
  2. Article first published online: 28 SEP 2006
  3. Manuscript Accepted: 30 JUN 2006
  4. Manuscript Received: 27 JAN 2006

Funded by

  • NIH
  • Predoctoral Fellowship from the NSF

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (216K)

REFERENCES

  • 1
    Kempson GE. Relationship between the tensile properties of articular cartilage from the human knee and age. Ann Rheum Dis 1982; 41: 508–11.
  • 2
    Akizuki S, Mow VC, Muller F, Pita JC, Howell DS, Manicourt DH. Tensile properties of human knee joint cartilage. I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J Orthop Res 1986; 4: 379–92.
    Direct Link:
  • 3
    Bank RA, Soudry M, Maroudas A, Mizrahi J, TeKoppele JM. The increased swelling and instantaneous deformation of osteoarthritic cartilage is highly correlated with collagen degradation. Arthritis Rheum 2000; 43: 2202–10.
    Direct Link:
  • 4
    Basser PJ, Schneiderman R, Bank RA, Wachtel E, Maroudas A. Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique. Arch Biochem Biophys 1998; 351: 207–19.
  • 5
    Maroudas A. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 1976; 260: 808–9.
  • 6
    Bank RA, Krikken M, Beekman B, Stoop R, Maroudas A, Lafeber FP, et al. A simplified measurement of degraded collagen in tissues: application in healthy, fibrillated and osteoarthritic cartilage. Matrix Biol 1997; 16: 233–43.
  • 7
    Billinghurst RC, Dahlberg L, Ionescu M, Reiner A, Bourne R, Rorabeck C, et al. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest 1997; 99: 1534–45.
  • 8
    Hollander AP, Heathfield TF, Webber C, Iwata Y, Bourne R, Rorabeck C, et al. Increased damage to type II collagen in osteoarthritic articular cartilage detected by a new immunoassay. J Clin Invest 1994; 93: 1722–32.
  • 9
    Bader DL, Kempson GE, Barrett AJ, Webb W. The effects of leucocyte elastase on the mechanical properties of adult human articular cartilage in tension. Biochim Biophys Acta 1981; 677: 103–8.
  • 10
    Kempson GE, Tuke MA, Dingle JT, Barrett AJ, Horsfield PH. The effects of proteolytic enzymes on the mechanical properties of adult human articular cartilage. Biochim Biophys Acta 1976; 428: 741–60.
  • 11
    Towle CA, Hung HH, Bonassar LJ, Treadwell BV, Mangham DG. Detection of interleukin-1 in the cartilage of patients with osteoarthritis: a possible autocrine/paracrine role in pathogenesis. Osteoarthritis Cartilage 1997; 5: 293–300.
  • 12
    Smith MD, Triantafillou S, Parker A, Youssef PP, Coleman M. Synovial membrane inflammation and cytokine production in patients with early osteoarthritis. J Rheumatol 1997; 24: 365–71.
  • 13
    Ollivierre F, Gubler U, Towle CA, Laurencin C, Treadwell BV. Expression of IL-1 genes in human and bovine chondrocytes: a mechanism for autocrine control of cartilage matrix degradation. Biochem Biophys Res Commun 1986; 141: 904–11.
  • 14
    Wood DD, Ihrie EJ, Dinarello CA, Cohen PL. Isolation of an interleukin-1–like factor from human joint effusions. Arthritis Rheum 1983; 26: 975–83.
    Direct Link:
  • 15
    Farahat MN, Yanni G, Poston R, Panayi GS. Cytokine expression in synovial membranes of patients with rheumatoid arthritis and osteoarthritis. Ann Rheum Dis 1993; 52: 870–5.
  • 16
    Pettipher ER, Higgs GA, Henderson B. Interleukin 1 induces leukocyte infiltration and cartilage proteoglycan degradation in the synovial joint. Proc Natl Acad Sci U S A 1986; 83: 8749–53.
  • 17
    Pettipher ER, Henderson B, Hardingham T, Ratcliffe A. Cartilage proteoglycan depletion in acute and chronic antigen-induced arthritis. Arthritis Rheum 1989; 32: 601–7.
    Direct Link:
  • 18
    Henderson B, Thompson RC, Hardingham T, Lewthwaite J. Inhibition of interleukin-1-induced synovitis and articular cartilage proteoglycan loss in the rabbit knee by recombinant human interleukin-1 receptor antagonist. Cytokine 1991; 3: 246–9.
  • 19
    Sah RL, Trippel SB, Grodzinsky AJ. Differential effects of serum, IGF-I, and FGF-2 on the maintenance of cartilage physical properties during long-term culture. J Orthop Res 1996; 14: 44–52.
    Direct Link:
  • 20
    Bonassar LJ, Sandy JD, Lark MW, Plaas AH, Frank EH, Grodzinsky AJ. Inhibition of cartilage degradation and changes in physical properties induced by IL-1α and retinoic acid using matrix metalloproteinase inhibitors. Arch Biochem Biophys 1997; 344: 404–12.
  • 21
    Plaas AH, Sandy JD. Proteoglycan anabolism and catabolism in articular cartilage. In: KuettnerKE, GoldbergVM, editors. Osteoarthritic disorders. Rosemont (IL): American Academy of Orthopaedic Surgeons; 1995. p. 103–16.
  • 22
    Saklatvala J, Curry VA, Sarsfield SJ. Purification to homogeneity of pig leucocyte catabolin, a protein that causes cartilage resorption in vitro. Biochem J 1983; 215: 385–92.
  • 23
    Billinghurst RC, Wu W, Ionescu M, Reiner A, Dahlberg L, Chen J, et al. Comparison of the degradation of type II collagen and proteoglycan in nasal and articular cartilages induced by interleukin-1 and the selective inhibition of type II collagen cleavage by collagenase. Arthritis Rheum 2000; 43: 664–72.
    Direct Link:
  • 24
    Kozaci LD, Buttle DJ, Hollander AP. Degradation of type II collagen, but not proteoglycan, correlates with matrix metalloproteinase activity in cartilage explant cultures. Arthritis Rheum 1997; 40: 164–74.
    Direct Link:
  • 25
    Jasin HE, Dingle JT. Human mononuclear cell factors mediate cartilage matrix degradation through chondrocyte activation. J Clin Invest 1981; 68: 571–81.
  • 26
    Patwari P, Gao G, Lee JH, Grodzinsky AJ, Sandy JD. Analysis of ADAMTS4 and MT4-MMP indicates that both are involved in aggrecanolysis in interleukin-1-treated bovine cartilage. Osteoarthritis Cartilage 2005; 13: 269–77.
  • 27
    Pratta MA, Yao W, Decicco C, Tortorella MD, Liu RQ, Copeland RA, et al. Aggrecan protects cartilage collagen from proteolytic cleavage. J Biol Chem 2003; 278: 45539–45.
  • 28
    Arner EC, Hughes CE, Decicco CP, Caterson B, Tortorella MD. Cytokine-induced cartilage proteoglycan degradation is mediated by aggrecanase. Osteoarthritis Cartilage 1998; 6: 214–28.
  • 29
    Tortorella MD, Malfait AM, Deccico C, Arner E. The role of ADAM-TS4 (aggrecanase-1) and ADAM-TS5 (aggrecanase-2) in a model of cartilage degradation [published erratum appears in Osteoarthritis Cartilage 2002;10:82]. Osteoarthritis Cartilage 2001; 9: 539–52.
  • 30
    Nguyen Q, Murphy G, Roughley PJ, Mort JS. Degradation of proteoglycan aggregate by a cartilage metalloproteinase: evidence for the involvement of stromelysin in the generation of link protein heterogeneity in situ. Biochem J 1989; 259: 61–7.
  • 31
    Chen AC, Temple MM, Ng DM, Verzijl N, DeGroot J, TeKoppele JM, et al. Induction of advanced glycation end products and alterations of the tensile properties of articular cartilage. Arthritis Rheum 2002; 46: 3212–7.
    Direct Link:
  • 32
    Farndale RW, Buttle DJ, Barrett AJ. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 1986; 883: 173–7.
  • 33
    Woessner JF Jr. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 1961; 93: 440–7.
  • 34
    Herbage D, Bouillet J, Bernengo JC. Biochemical and physicochemical characterization of pepsin-solubilized type-II collagen from bovine articular cartilage. Biochem J 1977; 161: 303–12.
  • 35
    Williamson AK, Chen AC, Masuda K, Thonar EJ, Sah RL. Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components. J Orthop Res 2003; 21: 872–80.
    Direct Link:
  • 36
    Hunziker EB. Articular cartilage structure in humans and experimental animals. In: KuettnerKE, SchleyerbachR, PeyronJG, HascallVC, editors. Articular cartilage and osteoarthritis. New York: Raven Press; 1992. p. 183–99.
  • 37
    Roth V, Mow VC. The intrinsic tensile behavior of the matrix of bovine articular cartilage and its variation with age. J Bone Joint Surg Am 1980; 62: 1102–17.
  • 38
    Kempson GE, Muir H, Pollard C, Tuke M. The tensile properties of the cartilage of human femoral condyles related to the content of collagen and glycosaminoglycans. Biochim Biophys Acta 1973; 297: 456–72.
  • 39
    Maroudas A, Bayliss MT, Venn MF. Further studies on the composition of human femoral head cartilage. Ann Rheum Dis 1980; 39: 514–23.
  • 40
    Kempson GE, Freeman MA, Swanson SA. Tensile properties of articular cartilage. Nature 1968; 220: 1127–8.
  • 41
    Hauselmann HJ, Flechtenmacher J, Michal L, Thonar EJ, Shinmei M, Kuettner KE, et al. The superficial layer of human articular cartilage is more susceptible to interleukin-1–induced damage than the deeper layers. Arthritis Rheum 1996; 39: 478–88.
    Direct Link:
  • 42
    Struglics A, Larsson S, Pratta MA, Kumar S, Lark MW, Lohmander LS. Human osteoarthritis synovial fluid and joint cartilage contain both aggrecanase- and matrix metalloproteinase-generated aggrecan fragments. Osteoarthritis Cartilage 2006; 14: 101–13.
  • 43
    Sandy JD, Neame PJ, Boynton RE, Flannery CR. Catabolism of aggrecan in cartilage explants: identification of a major cleavage site within the interglobular domain. J Biol Chem 1991; 266: 8683–5.
  • 44
    Chubinskaya S, Huch K, Mikecz K, Cs-Szabo G, Hasty KA, Kuettner KE, et al. Chondrocyte matrix metalloproteinase-8: up-regulation of neutrophil collagenase by interleukin-1β in human cartilage from knee and ankle joints. Lab Invest 1996; 74: 232–40.
  • 45
    Koshy PJ, Lundy CJ, Rowan AD, Porter S, Edwards DR, Hogan A, et al. The modulation of matrix metalloproteinase and ADAM gene expression in human chondrocytes by interleukin-1 and oncostatin M: a time-course study using real-time quantitative reverse transcription–polymerase chain reaction. Arthritis Rheum 2002; 46: 961–7.
    Direct Link:
  • 46
    Li JT, Mow VC, Koob TJ, Eyre DR. Effect of chondroitinase ABC treatment on the tensile behavior of bovine articular cartilage [abstract]. Trans Orthop Res Soc 1984; 9: 35.
  • 47
    Schmidt MB, Mow VC, Chun LE, Eyre DR. Effects of proteoglycan extraction on the tensile behavior of articular cartilage. J Orthop Res 1990; 8: 353–63.
    Direct Link:
  • 48
    Bonassar LJ, Stinn JL, Paguio CG, Frank EH, Moore VL, Lark MW, et al. Activation and inhibition of endogenous matrix metalloproteinases in articular cartilage-effects on composition and biophysical properties. Arch Biochem Biophys 1996; 333: 359–67.
  • 49
    Steenvoorden MM, Huizinga TW, Verzijl N, Bank RA, Ronday HK, Luning HA, et al. Activation of receptor for advanced glycation end products in osteoarthritis leads to increased stimulation of chondrocytes and synoviocytes. Arthritis Rheum 2006; 54: 253–63.
    Direct Link:
  • 50
    Squires GR, Okouneff S, Ionescu M, Poole AR. The pathobiology of focal lesion development in aging human articular cartilage and molecular matrix changes characteristic of osteoarthritis. Arthritis Rheum 2003; 48: 1261–70.
    Direct Link:
  • 51
    Aurich M, Mwale F, Reiner A, Mollenhauer JA, Anders JO, Fuhrmann RA, et al. Collagen and proteoglycan turnover in focally damaged human ankle cartilage: evidence for a generalized response and active matrix remodeling across the entire joint surface. Arthritis Rheum 2006; 54: 244–52.
    Direct Link:
View Full Article (HTML) Get PDF (216K)