Identification of shoulder osteoarthritis biomarkers: Comparison between shoulders with and without osteoarthritis

Journal of Shoulder and Elbow Surgery

Volumn 24, Issue 3, 2015, Pages 382-390

  Casagrande, Danielle ^a   Stains, Joseph P ^a   Murthi, Anand M ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Biomarkers; Connexin 43; Osteoarthritis; Shoulder

Indexed keywords

AGGRECANASE 2; BIOLOGICAL MARKER; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COLLAGENASE 3; CONNEXIN 43; CYCLOOXYGENASE 2; GELATINASE B; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN DERIVATIVE; INTERSTITIAL COLLAGENASE; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TUMOR NECROSIS FACTOR ALPHA; VERSICAN; ADAM PROTEIN; ADAMTS5 PROTEIN, HUMAN; COLLAGEN; GJA1 PROTEIN, HUMAN; MATRIX METALLOPROTEINASE; PTGS2 PROTEIN, HUMAN; TISSUE INHIBITOR OF METALLOPROTEINASE; TUMOR NECROSIS FACTOR; VCAN PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CARTILAGE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMERUS HEAD; MALE; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SHOULDER; SHOULDER OSTEOARTHRITIS; ARTICULAR CARTILAGE; BIOSYNTHESIS; CHEMISTRY; GENETICS; HUMERAL HEAD; METABOLISM; MIDDLE AGED; UPREGULATION;

ADAM PROTEINS; ADULT; AGED; BIOMARKERS; CARTILAGE, ARTICULAR; COLLAGEN; CONNEXIN 43; CYCLOOXYGENASE 2; FEMALE; HUMANS; HUMERAL HEAD; INTERLEUKINS; MALE; MATRIX METALLOPROTEINASES; MIDDLE AGED; NITRIC OXIDE SYNTHASE TYPE II; OSTEOARTHRITIS; SHOULDER JOINT; TISSUE INHIBITOR OF METALLOPROTEINASES; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; VERSICANS;

EID: 84922730186     PISSN: 10582746     EISSN: 15326500     Source Type: Journal    
DOI: 10.1016/j.jse.2014.11.039     Document Type: Article

References (54)

1. Bassiouni H.M., El-Deeb M., Kenawy N., Abdul-Azim E., Khairy M. Phonoarthrography, musculoskeletal ultrasonography, and biochemical biomarkers for the evaluation of knee cartilage in osteoarthritis. Mod Rheumatol 2011, 21:500-508. 10.1007/s10165-011-0441-8.
2. Bauer M., Jackson R.W. Chondral lesions of the femoral condyles: a system of arthroscopic classification. Arthroscopy 1988, 4:97-102.
3. Benito M.J., Veale D.J., FitzGerald O., van den Berg W.B., Bresnihan B. Synovial tissue inflammation in early and late osteoarthritis. Ann Rheum Dis 2005, 64:1263-1267. 10.1136/ard.2004.025270.
4. Caterson B., Flannery C.R., Hughes C.E., Little C.B. Mechanisms involved in cartilage proteoglycan catabolism. Matrix Biol 2000, 19:333-344.
5. Cherian P.P., Siller-Jackson A.J., Gu S., Wang X., Bonewald L.F., Sprague E., et al. Mechanical strain opens connexin 43 hemichannels in osteocytes: a novel mechanism for the release of prostaglandin. Mol Biol Cell 2005, 16:3100-3106. 10.1091/mbc.E04-10-0912.
6. Chevalier X. Upregulation of enzymatic activity by interleukin-1 in osteoarthritis. Biomed Pharmacother 1997, 51:58-62.
7. Chockalingam P.S., Sun W., Rivera-Bermudez M.A., Zeng W., Dufield D.R., Larsson S., et al. Elevated aggrecanase activity in a rat model of joint injury is attenuated by an aggrecanase specific inhibitor. Osteoarthr Cartil 2011, 19:315-323. 10.1016/j.joca.2010.12.004.
8. Cs-Szabò G., Melching L.I., Roughley P.J., Glant T.T. Changes in messenger RNA and protein levels of proteoglycans and link protein in human osteoarthritic cartilage samples. Arthritis Rheum 1997, 40:1037-1045.
9. de Boer T.N., Huisman A.M., Polak A.A., Niehoff A.G., van Rinsum A.C., Saris D., et al. The chondroprotective effect of selective Cox-2 inhibition in osteoarthritis: exvivo evaluation of human cartilage tissue after invivo treatment. Osteoarthr Cartil 2009, 17:482-488. 10.1016./j.joca.2008.09.002.
10. de Isla N.G., Mainard D., Muller S., Stoltz J.F. Invitro effects of diacerein on NO production by chondrocytes in response to proinflammatory mediators. Biomed Mater Eng 2008, 18(Suppl 1):S99-S104.
11. Fotopoulos V.C., Tzinia A., Tzurbakis M., Kalfakakou V., Levidiotou-Stefanou S., Georgoulis A. Expression levels of matrix metalloproteinase (MMP)-9 and its specific inhibitor TIMP-1, in septic and aseptic arthritis of the knee. Knee Surg Sports Traumatol Arthrosc 2012, 20:1159-1167. 10.1007/s00167-011-1676-9.
12. Green C.R., Nicholson L.F. Interrupting the inflammatory cycle in chronic diseases: do gap junctions provide the answer?. Cell Biol Int 2008, 32:1578-1583. 10.1016/j.cellbi.2008.09.006.
13. Hamada K., Fukuda H., Mikasa M., Kobayashi Y. Roentgenographic findings in massive rotator cuff tears: a long-term observation. Clin Orthop Relat Res 1990, 254:92-96.
14. Hiraiwa H., Sakai T., Mitsuyama H., Hamada T., Yamamoto R., Omachi T., et al. Inflammatory effect of advanced glycation end products on human meniscal cells from osteoarthritic knees. Inflamm Res 2011, 60:1039-1048. 10.1007/s00011-011-0365-y.
15. Jiang J.X., Siller-Jackson A.J., Burra S. Roles of gap junctions and hemichannels in bone cell functions and in signal transmission of mechanical stress. Front Biosci 2007, 12:1450-1462. 10.2741/2159.
16. Jingushi S., Lohmander L.S., Shinmei M., Hoerrner L.A., Lark M.W., Sugioka Y., et al. Markers of joint tissue turnover in joint fluids from hips with osteonecrosis of the femoral head. J Orthop Res 2000, 18:728-733.
17. Klatt A.R., Klinger G., Paul-Klausch B., Kuhn G., Renno J.H., Wagener R., et al. Matrilin-3 activates the expression of osteoarthritis-associated genes in primary human chondrocytes. FEBS Lett 2009, 583:3611-3617. 10.1016/j.febslet.2009.10.035.
18. Kobayashi M., Squires G.R., Mousa A., Tanzer M., Zukor D.J., Antoniou J., et al. Role of interleukin-1 and tumor necrosis factor alpha in matrix degradation of human osteoarthritic cartilage. Arthritis Rheum 2005, 52:128-135. 10.1002/art.20776.
19. Kolomytkin O.V., Marino A.A., Waddell D.D., Mathis J.M., Wolf R.E., Sadasivan K.K., et al. IL-1beta-induced production of metalloproteinases by synovial cells depends on gap junction conductance. Am J Physiol, Cell Physiol 2002, 282:C1254-C1260. 10.1152/ajpcell.01166.2000.
20. Lawrence J.T., Birmingham J., Toth A.P. Emerging ideas: prevention of posttraumatic arthritis through interleukin-1 and tumor necrosis factor-alpha inhibition. Clin Orthop Relat Res 2011, 469:3522-3526. 10.1007/s11999-010-1699-4.
21. Lee A.S., Ellman M.B., Yan D., Kroin J.S., Cole B.J., Van Wijnen A.J., et al. A current review of molecular mechanisms regarding osteoarthritis and pain. Gene 2013, 527:440-447. 10.1016/j.gene.2013.05.069.
22. LeGrand A., Fermor B., Fink C., Pisetsky D.S., Weinberg J.B., Vail T.P., et al. Interleukin-1, tumor necrosis factor alpha, and interleukin-17 synergistically up-regulate nitric oxide and prostaglandin E2 production in explants of human osteoarthritic knee menisci. Arthritis Rheum 2001, 44:2078-2083.
23. Lima F., Niger C., Hebert C., Stains J.P. Connexin43 potentiates osteoblast responsiveness to fibroblast growth factor 2 via a protein kinase C-delta/Runx2-dependent mechanism. Mol Biol Cell 2009, 20:2697-2708. 10.1091/mbc.E08-10-1079.
24. Lo I.K., Marchuk L.L., Hollinshead R., Hart D.A., Frank C.B. Matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase mRNA levels are specifically altered in torn rotator cuff tendons. Am J Sports Med 2004, 32:1223-1229. 10.1177/0363546503262200.
25. Marino A.A., Waddell D.D., Kolomytkin O.V., Meek W.D., Wolf R., Sadasivan K.K., et al. Increased intercellular communication through gap junctions may contribute to progression of osteoarthritis. Clin Orthop Relat Res 2004, 422:224-232. 10.1097/01.blo.0000129346.29945.3b.
26. Martel-Pelletier J., McCollum R., Fujimoto N., Obata K., Cloutier J.M., Pelletier J.P. Excess of metalloproteases over tissue inhibitor of metalloprotease may contribute to cartilage degradation in osteoarthritis and rheumatoid arthritis. Lab Invest 1994, 70:807-815.
27. Martin I., Jakob M., Schäfer D., Dick W., Spagnoli G., Heberer M. Quantitative analysis of gene expression in human articular cartilage from normal and osteoarthritic joints. Osteoarthr Cartil 2001, 9:112-118.
28. Mastbergen S.C., Bijlsma J.W., Lafeber F.P. Selective Cox-2 inhibition is favorable to human early and late-stage osteoarthritis cartilage: a human invitro study. Osteoarthr Cartil 2005, 13:519-526. 10.1016/j.joca.2005.02.004.
29. Masuhara K., Nakai T., Yamaguchi K., Yamasaki S., Sasaguri Y. Significant increases in serum and plasma concentrations of matrix metalloproteinases 3 and 9 in patients with rapidly destructive osteoarthritis of the hip. Arthritis Rheum 2002, 46:2625-2631. 10.1002/art.10547.
30. Mayan M.D., Carpintero-Fernandez P., Gago-Fuentes R., Martinez-de-Ilarduya O., Wang H.Z., Valiunas V., et al. Human articular chondrocytes express multiple gap junction proteins: differential expression of connexins in normal and osteoarthritic cartilage. Am J Pathol 2013, 182:1337-1346. 10.1016/j.ajpath.2012.12.018.
31. Miosge N., Hartmann M., Maelicke C., Herken R. Expression of collagen type I and type II in consecutive stages of human osteoarthritis. Histochem Cell Biol 2004, 122:229-236. 10.1007/s00418-004-0697-6.
32. Neer C.S., Craig E.V., Fukuda H. Cuff-tear arthropathy. J Bone Joint Surg Am 1983, 65:1232-1244.
33. Niger C., Buo A.M., Hebert C., Duggan B.T., Williams M.S., Stains J.P. ERK acts in parallel to PKCδ to mediate the connexin43-dependent potentiation of Runx2 activity by FGF2 in MC3T3 osteoblasts. Am J Physiol, Cell Physiol 2012, 302:C1035-C1044. 10.1152/ajpcell.00262.2011.
34. Niger C., Howell F.D., Stains J.P. Interleukin-1beta increases gap junctional communication among synovial fibroblasts via the extracellular-signal-regulated kinase pathway. Biol Cell 2009, 102:37-49. 10.1042/BC20090056.
35. Niger C., Luciotti M.A., Buo A.M., Hebert C., Ma V., Stains J.P. The regulation of runt-related transcription factor 2 by fibroblast growth factor-2 and connexin43 requires the inositol polyphosphate/protein kinase Cδ cascade. J Bone Miner Res 2013, 28:1468-1477. 10.1002/jbmr.1867.
36. Nishida Y., Shinomura T., Iwata H., Miura T., Kimata K. Abnormal occurrence of a large chondroitin sulfate proteoglycan, PG-M/versican in osteoarthritic cartilage. Osteoarthr Cartil 1994, 2:43-49.
37. Noyes F.R., Stabler C.L. A system for grading articular cartilage lesions at arthroscopy. Am J Sports Med 1989, 17:505-513.
38. Omura K., Takahashi M., Omura T., Miyamoto S., Kushida K., Sano Y., et al. Changes in the concentration of plasma matrix metalloproteinases (MMPs) and tissue inhibitor of metalloproteinases-1 (TIMP-1) after total joint replacement in patients with arthritis. Clin Rheumatol 2002, 21:448-492.
39. Pelletier J.P., Martel-Pelletier J., Abramson S.B. Osteoarthritis, an inflammatory disease: potential implication for the selection of new therapeutic targets. Arthritis Rheum 2001, 44:1237-1247.
40. Ratcliffe A., Flatow E.L., Roth N., Saed-Nejad F., Bigliani L.U. Biochemical markers in synovial fluid identify early osteoarthritis ofthe glenohumeral joint. Clin Orthop Relat Res 1996, 330:45-53.
41. Rosa S.C., Judas F., Lopes M.C., Mendes A.F. Nitric oxide synthase isoforms and NF-kappaB activity in normal and osteoarthritic human chondrocytes: regulation by inducible nitric oxide. Nitric Oxide 2008, 19:276-283. 10.1016/j.niox.2008.07.005.
42. Sanchez C., Pesesse L., Gabay O., Delcour J.P., Msika P., Baudouin C., et al. Regulation of subchondral bone osteoblast metabolism by cyclic compression. Arthritis Rheum 2012, 64:1193-1203. 10.1002/art.33445.
43. Settle S., Vickery L., Nemirovskiy O., Vidmar T., Bendele A., Messing D., et al. Cartilage degradation biomarkers predict efficacy of a novel, highly selective matrix metalloproteinase 13 inhibitor in a dog model of osteoarthritis: confirmation by multivariate analysis that modulation of type II collagen and aggrecan degradation peptides parallels pathologic changes. Arthritis Rheum 2010, 62:3006-3015. 10.1002/art.27596.
44. Stains J.P., Civitelli R. Gap junctions regulate extracellular signal-regulated kinase signaling to affect gene transcription. Mol Biol Cell 2005, 16:64-72. 10.1091/mbc.E04-04-0339.
45. Stains J.P., Lecanda F., Screen J., Towler D.A., Civitelli R. Gap junctional communication modulates gene transcription by altering the recruitment of Sp1 and Sp3 to connexin-response elements in osteoblast promoters. J Biol Chem 2003, 278:24377-24387. 10.1074/jbc.M212554200.
46. Stannus O., Jones G., Cicuttini F., Parameswaran V., Quinn S., Burgess J., et al. Circulating levels of IL-6 and TNFα are associated with knee radiographic osteoarthritis and knee cartilage loss in older adults. Osteoarthr Cartil 2010, 18:1441-1447. 10.1016/j.joca.2010.08.016.
47. Stannus O.P., Jones G., Blizzard L., Cicuttini F.M., Ding C. Associations between serum levels of inflammatory markers and change in knee pain over 5 years in older adults: a prospective cohort study. Ann Rheum Dis 2013, 72:535-540. 10.1136/annrheumdis-2011-201047.
48. Su S., Grover J., Roughley P.J., DiBattista J.A., Martel-Pelletier J., Pelletier J.P., et al. Expression of the tissue inhibitor of metalloproteinases (TIMP) gene family in normal and osteoarthritic joints. Rheumatol Int 1999, 18:183-191.
49. 2+-dependent mechanism. Biorheology 2002, 39:153-160.
50. 2+-dependent mechanism. J Bone Miner Res 2000, 15:1669-1677.
51. Tsuchida S., Arai Y., Kishida T., Takahashi K.A., Honjo K., Terauchi R., et al. Silencing the expression of connexin 43 decreases inflammation and joint destruction in experimental arthritis. J Orthop Res 2013, 31:525-530. 10.1002/jor.22263.
52. van den Berg W.B. The role of cytokines and growth factors in cartilage destruction in osteoarthritis and rheumatoid arthritis. Z Rheumatol 1999, 58:136-141.
53. Voloshin I., Gelinas J., Maloney M.D., O'Keefe R.J., Bigliani L.U., Blaine T.A. Proinflammatory cytokines and metalloproteases are expressed in the subacromial bursa in patients with rotator cuff disease. Arthroscopy 2005, 21:1076.e1-1076.e9. 10.1016/j.arthro.2005.05.017.
54. Yoshihara Y., Hamada K., Nakajima T., Fujikawa K., Fukuda H. Biochemical markers in the synovial fluid of glenohumeral joints from patients with rotator cuff tear. J Orthop Res 2001, 19:573-579.