Loss of extracellular matrix from articular cartilage is mediated by the synovium and ligament after anterior cruciate ligament injury

Osteoarthritis and Cartilage

Volumn 21, Issue 12, 2013, Pages 1950-1957

  Haslauer, C M ^a   Elsaid, K A ^b   Fleming, B C ^c   Proffen, B L ^a   Johnson, V M ^a   Murray, M M ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MASSACHUSETTS COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

ACL; Aggrecanase; Cartilage; Joint tissues; Metalloproteinases

Indexed keywords

AGGRECANASE 1; CASPASE 3; CHONDROITIN 6 SULFATE; COLLAGENASE 3; INTERSTITIAL COLLAGENASE; MESSENGER RNA; TISSUE SCAFFOLD;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CRUCIATE LIGAMENT; ANTERIOR CRUCIATE LIGAMENT INJURY; ANTERIOR CRUCIATE LIGAMENT RECONSTRUCTION; ARTHROTOMY; ARTICLE; ARTICULAR CARTILAGE; BONE TURNOVER; CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; COLLAGEN DEGRADATION; ENZYME DEGRADATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; IMMUNE MEDIATED INJURY; IMMUNOHISTOCHEMISTRY; JOINT; LIGAMENT; MINIPIG; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNOVIUM;

ACL; AGGRECANASE; CARTILAGE; JOINT TISSUES; METALLOPROTEINASES;

ADAM PROTEINS; AGGRECANS; ANIMALS; ANTERIOR CRUCIATE LIGAMENT; CARTILAGE, ARTICULAR; COLLAGEN TYPE II; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; KNEE JOINT; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 13; PROCOLLAGEN N-ENDOPEPTIDASE; SWINE; SWINE, MINIATURE; SYNOVIAL FLUID; SYNOVIAL MEMBRANE; UP-REGULATION;

EID: 84888866475     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2013.09.003     Document Type: Article

References (43)

1. Lohmander L.S., Englund P.M., Dahl L.L., Roos E.M. The long-term consequence of anterior cruciate ligament and meniscus injuries: osteoarthritis. Am J Sports Med 2007, 35(10):1756-1769.
2. Fleming B.C., Oksendahl H.L., Mehan W.A., Portnoy R., Fadale P.D., Hulstyn M.J., et al. Delayed Gadolinium-Enhanced MR Imaging of Cartilage (dGEMRIC) following ACL injury. Osteoarthritis Cartilage 2010, 18(5):662-667.
3. Catterall J.B., Stabler T.V., Flannery C.R., Kraus V.B. Changes in serum and synovial fluid biomarkers after acute injury (NCT00332254). Arthritis Res Ther 2010, 12(6):R229.
4. Murray M.M., Spindler K.P., Devin C., Snyder B.S., Muller J., Takahashi M., et al. Use of a collagen-platelet rich plasma scaffold to stimulate healing of a central defect in the canine ACL. JOrthop Res 2006, 24(4):820-830.
5. Murray M.M., Magarian E., Harrison S.L., Mastrangelo A., Zurakowski D., Fleming B.C. The effect of skeletal maturity on functional healing of the anterior cruciate ligament. JBone Joint Surg 2010, 92(11):2039-2049.
6. Tchetverikov I., Lohmander L.S., Verzijl N., Huizinga T.W., TeKoppele J.M., Hanemaaijer R., et al. MMP protein and activity levels in synovial fluid from patients with joint injury, inflammatory arthritis, and osteoarthritis. Ann Rheum Dis 2005, 64(5):694-698.
7. Billinghurst R.C., Dahlberg L., Ionescu M., Reiner A., Bourne R., Rorabeck C., et al. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. JClin Invest 1997, 99(7):1534-1545.
8. Burrage P.S., Mix K.S., Brinckerhoff C.E. Matrix metalloproteinases: role in arthritis. Front Biosci A J Virtual Libr 2006, 11:529-543.
9. Poole A.R., Ionescu M., Fitzcharles M.A., Billinghurst R.C. The assessment of cartilage degradation invivo: development of an immunoassay for the measurement in body fluids of type II collagen cleaved by collagenases. JImmunological Methods 2004, 294(1-2):145-153.
10. Nelson F., Dahlberg L., Laverty S., Reiner A., Pidoux I., Ionescu M., et al. Evidence for altered synthesis of type II collagen in patients with osteoarthritis. JClin Invest 1998, 102(12):2115-2125.
11. Karsdal M.A., Madsen S.H., Christiansen C., Henriksen K., Fosang A.J., Sondergaard B.C. Cartilage degradation is fully reversible in the presence of aggrecanase but not matrix metalloproteinase activity. Arthritis Res Ther 2008, 10(3):R63.
12. Poole A.R., Ionescu M., Swan A., Dieppe P.A. Changes in cartilage metabolism in arthritis are reflected by altered serum and synovial fluid levels of the cartilage proteoglycan aggrecan. Implications for pathogenesis. JClin Invest 1994, 94(1):25-33.
13. Lohmander L.S., Ionescu M., Jugessur H., Poole A.R. Changes in joint cartilage aggrecan after knee injury and in osteoarthritis. Arthritis Rheum 1999, 42(3):534-544.
14. Kraus V.B., Birmingham J., Stabler T.V., Feng S., Taylor D.C., Moorman C.T., et al. Effects of intraarticular IL1-Ra for acute anterior cruciate ligament knee injury: a randomized controlled pilot trial (NCT00332254). Osteoarthritis Cartilage 2012, 20(4):271-278.
15. Murray M.M., Spindler K.P., Abreu E., Muller J.A., Nedder A., Kelly M., et al. Collagen-platelet rich plasma hydrogel enhances primary repair of the porcine anterior cruciate ligament. JOrthop Res 2007, 25(1):81-91.
16. Magarian E.M., Fleming B.C., Harrison S.L., Mastrangelo A.N., Badger G.J., Murray M.M. Delay of 2 or 6 weeks adversely affects the functional outcome of augmented primary repair of the porcine anterior cruciate ligament. Am J Sports Med 2010, 38(12):2528-2534.
17. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3(6):1101-1108.
18. Frantz N.Z., Friesen K.G., Andrews G.A., Tokach M.D., Yamka R.M., Loughin T.L., et al. Use of serum biomarkers to predict the development and severity of osteochondrosis lesions in the distal portion of the femur in pigs. Am J Vet Res 2010, 71(8):946-952.
19. Hembry R.M., Dyce J., Driesang I., Hunziker E.B., Fosang A.J., Tyler J.A., et al. Immunolocalization of matrix metalloproteinases in partial-thickness defects in pig articular cartilage. A preliminary report. JBone Jt Surg Am Volume 2001, 83-A(6):826-838.
20. Fosang A.J., Last K., Stanton H., Weeks D.B., Campbell I.K., Hardingham T.E., et al. Generation and novel distribution of matrix metalloproteinase-derived aggrecan fragments in porcine cartilage explants. JBiol Chem 2000, 275(42):33027-33037.
21. Pritzker K.P., Gay S., Jimenez S.A., Ostergaard K., Pelletier J.P., Revell P.A., et al. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage 2006, 14(1):13-29.
22. Jay G.D., Fleming B.C., Watkins B.A., McHugh K.A., Anderson S.C., Zhang L.X., et al. Prevention of cartilage degeneration and restoration of chondroprotection by lubricin tribosupplementation in the rat following anterior cruciate ligament transection. Arthritis Rheum 2010, 62(8):2382-2391.
23. Hornik K. The R FAQ 2012, ISBN: 3-900051-08-9. http://cranr-projectorg/doc/FAQ/R-FAQhtml.
24. Matyas J.R., Atley L., Ionescu M., Eyre D.R., Poole A.R. Analysis of cartilage biomarkers in the early phases of canine experimental osteoarthritis. Arthritis Rheum 2004, 50(2):543-552.
25. Chu Q., Lopez M., Hayashi K., Ionescu M., Billinghurst R.C., Johnson K.A., et al. Elevation of a collagenase generated type II collagen neoepitope and proteoglycan epitopes in synovial fluid following induction of joint instability in the dog. Osteoarthritis Cartilage 2002, 10(8):662-669.
26. Kojima T., Mwale F., Yasuda T., Girard C., Poole A.R., Laverty S. Early degradation of type IX and type II collagen with the onset of experimental inflammatory arthritis. Arthritis Rheum 2001, 44(1):120-127.
27. Bluteau G., Conrozier T., Mathieu P., Vignon E., Herbage D., Mallein-Gerin F. Matrix metalloproteinase-1, -3, -13 and aggrecanase-1 and -2 are differentially expressed in experimental osteoarthritis. Biochim biophys acta 2001, 1526(2):147-158.
28. Wu W., Billinghurst R.C., Pidoux I., Antoniou J., Zukor D., Tanzer M., et al. Sites of collagenase cleavage and denaturation of type II collagen in aging and osteoarthritic articular cartilage and their relationship to the distribution of matrix metalloproteinase 1 and matrix metalloproteinase 13. Arthritis Rheum 2002, 46(8):2087-2094.
29. Attia E., Brown H., Henshaw R., George S., Hannafin J.A. Patterns of gene expression in a rabbit partial anterior cruciate ligament transection model: the potential role of mechanical forces. Am J Sports Med 2010, 38(2):348-356.
30. Tang Z., Yang L., Zhang J., Xue R., Wang Y., Chen P.C., et al. Coordinated expression of MMPs and TIMPs in rat knee intra-articular tissues after ACL injury. Connect Tissue Res 2009, 50(5):315-322.
31. Burleigh A., Chanalaris A., Gardiner M.D., Driscoll C., Boruc O., Saklatvala J., et al. Joint immobilization prevents murine osteoarthritis and reveals the highly mechanosensitive nature of protease expression invivo. Arthritis Rheum 2012, 64(7):2278-2288.
32. Sward P., Frobell R., Englund M., Roos H., Struglics A. Cartilage and bone markers and inflammatory cytokines are increased in synovial fluid in the acute phase of knee injury (hemarthrosis) - a cross-sectional analysis. Osteoarthritis Cartilage 2012, 20(11):1302-1308.
33. Lohmander L.S., Atley L.M., Pietka T.A., Eyre D.R. The release of crosslinked peptides from type II collagen into human synovial fluid is increased soon after joint injury and in osteoarthritis. Arthritis Rheum 2003, 48(11):3130-3139.
34. Anderson D.D., Chubinskaya S., Guilak F., Martin J.A., Oegema T.R., Olson S.A., et al. Post-traumatic osteoarthritis: improved understanding and opportunities for early intervention. JOrthopaedic Res Official Publ Orthopaedic Res Soc 2011, 29(6):802-809.
35. Chamberlain C.S., Crowley E.M., Kobayashi H., Eliceiri K.W., Vanderby R. Quantification of collagen organization and extracellular matrix factors within the healing ligament. Microsc Microanal 2011, 17(5):779-787.
36. Kraft J., Blanchette V., Babyn P., Feldman B., Cloutier S., Israels S., et al. Magnetic resonance imaging and joint outcomes in boys with severe hemophilia A treated with tailored primary prophylaxis in Canada. JThromb Haemost 2012, 10(12):2494-2502.
37. Uchibori M., Nishida Y., Tabata I., Sugiura H., Nakashima H., Yamada Y., et al. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in pigmented villonodular synovitis suggests their potential role for joint destruction. JRheumatol 2004, 31(1):110-119.
38. Potter H.G., Jain S.K., Ma Y., Black B.R., Fung S., Lyman S. Cartilage injury after acute, isolated anterior cruciate ligament tear: immediate and longitudinal effect with clinical/MRI follow-up. Am J Sports Med 2012, 40(2):276-285.
39. Andriacchi T.P., Briant P.L., Bevill S.L., Koo S. Rotational changes at the knee after ACL injury cause cartilage thinning. Clin Orthop Relat Res 2006, 442:39-44.
40. Levy A.S., Meier S.W. Approach to cartilage injury in the anterior cruciate ligament-deficient knee. Orthop Clin North Am 2003, 34(1):149-167.
41. Sharma L., Lou C., Felson D.T., Dunlop D.D., Kirwan-Mellis G., Hayes K.W., et al. Laxity in healthy and osteoarthritic knees. Arthritis Rheum 1999, 42(5):861-870.
42. Seitz H., Hausner T., Schlenz I., Lang S., Eschberger J. Vascular anatomy of the ovine anterior cruciate ligament. A macroscopic, histological and radiographic study. Arch Orthop Trauma Surg 1997, 116(1-2):19-21.
43. Oiestad B.E., Holm I., Engebretsen L., Aune A.K., Gunderson R., Risberg M.A. The prevalence of patellofemoral osteoarthritis 12 years after anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc 2013, 21(4):942-990.