Evidence for JNK-dependent up-regulation of proteoglycan synthesis and for activation of JNK1 following cyclical mechanical stimulation in a human chondrocyte culture model

Osteoarthritis and Cartilage

Volumn 15, Issue 8, 2007, Pages 884-893

  Zhou, Y ^a   Millward Sadler, S J ^a   Lin, H ^a   Robinson, H ^a   Goldring, M ^b   Salter, D M ^a   Nuki, G ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

1 Integrin; Human articular chondrocytes; JNK; MAPK; Mechanical strain; Proteoglycan

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; ANTIBODY; BETA1 INTEGRIN; CARBON DIOXIDE; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; PROTEIN ANTIBODY; STRESS ACTIVATED PROTEIN KINASE 1; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; SULFATE; SULFUR 35;

ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL LINE; CONTROLLED STUDY; DATA ANALYSIS; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MECHANICAL STIMULATION; MONOLAYER CULTURE; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOGLYCAN SYNTHESIS; UPREGULATION; WESTERN BLOTTING;

CARBON DIOXIDE; CELL CULTURE TECHNIQUES; CELL LINE, TRANSFORMED; CHONDROCYTES; DIFFUSION CHAMBERS, CULTURE; ENZYME INHIBITORS; HUMANS; IMIDAZOLES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 8; PHOSPHORYLATION; PROTEOGLYCANS; PYRIDINES; STRESS, MECHANICAL; UP-REGULATION;

EID: 34547676408     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2007.02.001     Document Type: Article

References (72)

1. Palmoski M.J., Colyer R.A., and Brandt K.D. Joint motion in the absence of normal loading does not maintain normal articular cartilage. Arthritis Rheum 23 (1980) 325-334
2. Kiviranta I., Jurvelin J., Tammi M., Saamanen A.M., and Helminen H.J. Weight bearing controls glycosaminoglycan concentration and articular cartilage thickness in the knee joints of young beagle dogs. Arthritis Rheum 30 (1987) 801-809
3. Hall A.C., Urban J.P., and Gehl K.A. The effects of hydrostatic pressure on matrix synthesis in articular cartilage. J Orthop Res 9 (1991) 1-10
4. Saamanen A.M., Tammi M., Jurvelin J., Kiviranta I., and Helminen H.J. Proteoglycan alterations following immobilization and remobilization in the articular cartilage of young canine knee (stifle) joint. J Orthop Res 8 (1990) 863-873
5. Sah R.L.-Y., Grodzinsky A.J., Plaas A.H.K., and Sandy J.D. Effect of static and dynamic compression on matrix metabolism in cartilage explants. In: Kuettner K., Schleyerbach R., and Peyron J. (Eds). Articular Cartilage and Osteoarthritis (1992), Raven Press, New York 373-392
6. Larsson T., Aspden R.M., and Heinegard D. Effects of mechanical load on cartilage matrix biosynthesis in vitro. Matrix 11 (1991) 388-394
7. Korver T.H., van de Stadt R.J., Kiljan E., van Kampen G.P., and van der Korst J.K.V. Effects of loading on the synthesis of proteoglycans in different layers of anatomically intact articular cartilage in vitro. J Rheumatol 19 (1992) 905-912
8. Steinmeyer J., and Knue S. The proteoglycan metabolism of mature bovine articular cartilage explants superimposed to continuously applied cyclic mechanical loading. Biochem Biophys Res Commun 240 (1997) 216-221
9. Veldhuijzen J.P., Bourret L.A., and Rodan G.A. In vitro studies of the effect of intermittent compressive forces on cartilage cell proliferation. J Cell Physiol 98 (1979) 299-306
10. Buschmann M.D., Gluzband Y.A., Grodzinsky A.J., and Hunziker E.B. Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. J Cell Sci 108 (1995) 1497-1508
11. Guilak F., Meyer B.C., Ratcliffe A., and Mow V.C. The effects of matrix compression on proteoglycan metabolism in articular cartilage explants. Osteoarthritis Cartilage 2 (1994) 91-101
12. Ragan P.M., Badger A.M., Cook M., Chin V.I., Gowen M., Grodzinsky A.J., et al. Down-regulation of chondrocyte aggrecan and type-II collagen gene expression correlates with increases in static compression magnitude and duration. J Orthop Res 17 (1999) 836-842
13. Valhmu W.B., Stazzone E.J., Bachrach N.M., Saed-Nejad F., Fischer S.G., Mow V.C., et al. Load-controlled compression of articular cartilage induces a transient stimulation of aggrecan gene expression. Arch Biochem Biophys 353 (1998) 29-36
14. Blain E.J., Mason D.J., and Duance V.C. The effect of cyclical compressive loading on gene expression in articular cartilage. Biorheology 40 (2003) 111-117
15. Millward-Sadler S.J., Wright M.O., Davies L.W., Nuki G., and Salter D.M. Mechanotransduction via integrins and interleukin-4 results in altered aggrecan and matrix metalloproteinase 3 gene expression in normal, but not osteoarthritic, human articular chondrocytes. Arthritis Rheum 43 (2000) 2091-2099
16. Lee H.S., Millward-Sadler S.J., Wright M.O., Nuki G., and Salter D.M. Integrin and mechanosensitive ion channel-dependent tyrosine phosphorylation of focal adhesion proteins and beta-catenin in human articular chondrocytes after mechanical stimulation. J Bone Miner Res 15 (2000) 1501-1509
17. Bavington C.D., Wright M.O., Jobanputra P., Lin H., Morrison P.T., Brennan F.R., et al. Increased chondrocyte proteoglycan synthesis following cyclical microstrain: regulation by β1 integrin and stretch activated ion channels. Trans ORS 22 (1997) 705
18. Lee H.S., Millward-Sadler S.J., Wright M.O., Nuki G., Al-Jamal R., and Salter D.M. Activation of Integrin-RACK1/PKCalpha signalling in human articular chondrocyte mechanotransduction. Osteoarthritis Cartilage 10 (2002) 890-897
19. Millward-Sadler S.J., Wright M.O., Lee H., Caldwell H., Nuki G., and Salter D.M. Altered electrophysiological responses to mechanical stimulation and abnormal signalling through alpha5beta1 integrin in chondrocytes from osteoarthritic cartilage. Osteoarthritis Cartilage 8 (2000) 272-278
20. Dedhar S. Cell-substrate interactions and signaling through ILK. Curr Opin Cell Biol 12 (2000) 250-256
21. Ip Y.T., and Davis R.J. Signal transduction by the c-Jun N-terminal kinase (JNK) - from inflammation to development. Curr Opin Cell Biol 10 (1998) 205-219
22. Fanning P.J., Emkey G., Smith R.J., Grodzinsky A.J., Szasz N., and Trippel S.B. Mechanical regulation of mitogen-activated protein kinase signaling in articular cartilage. J Biol Chem 278 (2003) 50940-50948
23. Vincent T.L., Hermansson M.A., Hansen U.N., Amis A.A., and Saklatvala J. Basic fibroblast growth factor mediates transduction of mechanical signals when articular cartilage is loaded. Arthritis Rheum 50 (2004) 526-533
24. Schneller M., Vuori K., and Ruoslahti E. Alphavbeta3 integrin associates with activated insulin and PDGFbeta receptors and potentiates the biological activity of PDGF. EMBO J 16 (1997) 5600-5607
25. Gloe T., Sohn H.Y., Meininger G.A., and Pohl U. Shear stress-induced release of basic fibroblast growth factor from endothelial cells is mediated by matrix interaction via integrin alpha(v)beta3. J Biol Chem 277 (2002) 23453-23458
26. Arnoczky S.P., Tian T., Lavagnino M., Gardner K., Schuler P., and Morse P. Activation of stress-activated protein kinases (SAPK) in tendon cells following cyclic strain: the effects of strain frequency, strain magnitude, and cytosolic calcium. J Orthop Res 20 (2002) 947-952
27. Simmons C.A., Matlis S., Thornton A.J., Chen S., Wang C.Y., and Mooney D.J. Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway. J Biomech 36 (2003) 1087-1096
28. Oldenhof A.D., Shynlova O.P., Liu M., Landille B.L., and Lye S.J. Mitogen-activated protein kinases mediate stretch-induced c-fos mRNA expression in myometrial smooth muscle cells. Am J Physiol Cell Physiol 283 (2002) C1530-C1539
29. Kaarniranta K., Elo M., Sironen R., Lammi M.J., Goldring M.B., Eriksson J.E., et al. Hsp70 accumulation in chondrocytic cells exposed to high continuous hydrostatic pressure coincides with mRNA stabilization rather than transcriptional activation. Proc Natl Acad Sci U S A 95 (1998) 2319-2324
30. Nuttall M.E., Nadeau D.P., Fisher P.W., Wang F., Keller P.M., DeWolf Jr. W.E., et al. Inhibition of caspase-3-like activity prevents apoptosis while retaining functionality of human chondrocytes in vitro. J Orthop Res 18 (2000) 356-363
31. Attur M.G., Dave M., Cipolletta C., Kang P., Goldring M.B., Patel I.R., et al. Reversal of autocrine and paracrine effects of interleukin 1 (IL-1) in human arthritis by type II IL-1 decoy receptor. Potential for pharmacological intervention. J Biol Chem 275 (2000) 40307-40315
32. Westacott C.I., Urban J.P., Goldring M.B., and Elson C.J. The effects of pressure on chondrocyte tumour necrosis factor receptor expression. Biorheology 39 (2002) 125-132
33. Osaki M., Tan L., Choy B.K., Yoshida Y., Cheah K.S., Auron P.E., et al. The TATA-containing core promoter of the type II collagen gene (COL2A1) is the target of interferon-gamma-mediated inhibition in human chondrocytes: requirement for Stat1 alpha, Jak1 and Jak2. Biochem J 369 (2003) 103-115
34. Tan L., Peng H., Osaki M., Choy B.K., Auron P.E., Sandell L.J., et al. Egr-1 mediates transcriptional repression of COL2A1 promoter activity by interleukin-1beta. J Biol Chem 278 (2003) 17688-17700
35. Yokota H., Goldring M.B., and Sun H.B. CITED2-mediated regulation of MMP-1 and MMP-13 in human chondrocytes under flow shear. J Biol Chem 278 (2003) 47275-47280
36. Masuko-Hongo K., Berenbaum F., Humbert L., Salvat C., Goldring M.B., and Thirion S. Up-regulation of microsomal prostaglandin E synthase 1 in osteoarthritic human cartilage: critical roles of the ERK-1/2 and p38 signaling pathways. Arthritis Rheum 50 (2004) 2829-2838
37. Oliver B.L., Cronin C.G., Zhang-Benoit Y., Goldring M.B., and Tanzer M.L. Divergent stress responses to IL-1beta, nitric oxide, and tunicamycin by chondrocytes. J Cell Physiol (2004) [Epub ahead of print]
38. Kokenyesi R., Tan L., Robbins J.R., and Goldring M.B. Proteoglycan production by immortalized human chondrocyte cell lines cultured under conditions that promote expression of the differentiated phenotype. Arch Biochem Biophys 383 (2000) 79-90
39. Loeser R.F., Sadiev S., Tan L., and Goldring M.B. Integrin expression by primary and immortalized human chondrocytes: evidence of a differential role for alpha1beta1 and alpha2beta1 integrins in mediating chondrocyte adhesion to types II and VI collagen. Osteoarthritis Cartilage 8 (2000) 96-105
40. Goldring M.B., Birkhead J.B., Suen L.F., Yamin R., Mizuno S., Glowacki J., et al. Interleukin-1β-modulated gene expression in immortalized human chondrocytes. J Clin Invest 94 (1994) 2307-2316
41. Millward-Sadler S.J., and Salter D.M. Integrin dependent signaling cascades in chondrocyte mechanotransduction. Ann Biomed Eng 32 (2004) 435-446
42. Wright M.O., Jobanputra P., Bavington C., Salter D.M., and Nuki G. Effects of intermittent pressure-induced strain on the electrophysiology of cultured human chondrocytes: evidence for the presence of stretch-activated membrane ion channels. Clin Sci 90 (1996) 61-71
43. Wright M.O., Nishida K., Bavington C., Godolpin J.L., Dunne E., Walmsley S., et al. Hyperpolarisation of cultured human chondrocytes following cyclical pressure-induced strain: evidence of a role for alpha 5 beta 1 integrin as a chondrocyte mechanoreceptor. J Orthop Res 15 (1997) 742-747
44. Elliot K.J., Millward-Sadler S.J., Wright M.O., Robb J.E., Wallace W.H., and Salter D.M. Effects of methotrexate on human bone cell responses to mechanical stimulation. Rheumatology 43 (2004) 1226-1231
45. Bavington C.D. The effect of mechanical stimulation on proteoglycan synthesis by articular chondrocytes. PhD thesis, University of Edinburgh, UK, 1997.
46. Parkkinen J.J., Ikonen J., Lammi M.J., Laakkonen J., Tammi M., and Helminen H.J. Effects of cyclic hydrostatic pressure on proteoglycan synthesis in cultured chondrocytes and cartilage explants. Arch Biochem Biophys 300 (1993) 458-465
47. Lipman J.M. Fluorophotometric quantitation of DNA in articular cartilage utilizing Hoechst 33258. Anal Biochem 176 (1989) 128-131
48. Dean J.L., Brook M., Clark A.R., and Saklatvala J. p38 mitogen-activated protein kinase regulates cyclooxygenase-2 mRNA stability and transcription in lipopolysaccharide-treated human monocytes. J Biol Chem 274 (1999) 264-269
49. +-induced c-fos mRNA expression in PC12 cells. Respir Physiol 111 (1997) 127-135
50. Buschmann M.D., Kim Y.J., Wong M., Frank E., Hunziker E.B., and Grodzinsky A.J. Stimulation of aggrecan synthesis in cartilage explants by cyclic loading is localized to regions of high interstitial fluid flow. Arch Biochem Biophys 366 (1999) 1-7
51. Sauerland K., Raiss R.X., and Steinmeyer J. Proteoglycan metabolism and viability of articular cartilage explants as modulated by the frequency of intermittent loading. Osteoarthritis Cartilage 11 (2003) 343-350
52. Lee D.A., Noguchi T., Frean S.P., Lees P., and Bader D.L. The influence of mechanical loading on isolated chondrocytes seeded in agarose constructs. Biorheology 37 (2000) 149-161
53. Urban J.P. The chondrocyte: a cell under pressure. Br J Rheumatol 33 (1994) 901-908
54. Salter D.M., Millward-Sadler S.J., Nuki G., and Wright M.O. Differential responses of chondrocytes from normal and osteoarthritic human articular cartilage to mechanical stimulation. Biorheology 39 (2002) 97-108
55. Lee J.C., Laydon J.T., McDonnell P.C., Gallagher T.F., Kumar S., Green D., et al. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372 (1994) 739-746
56. Alessi D.R., Cuenda A., Cohen P., Dudley D.T., and Saltiel A.R. PD98059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem 270 (1995) 27489-27494
57. Cuenda A., Rouse J., Doza Y.N., Meier R., Cohen P., Gallagher T.F., et al. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 364 (1995) 229-233
58. Davies S.P., Reddy H., Caivano M., and Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351 (2000) 95-105
59. Whitmarsh A.J., Yang S.H., Su M.S., Sharrocks A.D., and Davis R.J. Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol Cell Biol 17 (1997) 2360-2371
60. Clerk A., and Sugden P.H. The p38-MAPK inhibitor, SB203580, inhibits cardiac stress-activated protein kinases/c-Jun N-terminal kinases (SAPKs/JNKS). FEBS Lett 426 (1998) 93-96
61. Han Z., Boyle D.L., Chang L., Bennett B., Karin M., Yang L., et al. C-Jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J Clin Invest 108 (2001) 73-81
62. Matsuda N., Morita N., Matsuda K., and Watanabe M. Proliferation and differentiation of human osteoblastic cells associated with differential activation of MAP kinases in response to epidermal growth factor, hypoxia, and mechanical stress in vitro. Biochem Biophys Res Commun 249 (1998) 350-354
63. 2. J Pharmacol Toxicol Methods 39 (1998) 211-220
64. Swietach P., Browning J.A., and Wilkins R.J. Functional and molecular determination of carbonic anhydrase levels in bovine and cultured human chondrocytes. Comp Biochem Physiol B Biochem Mol Biol 133 (2002) 427-435
65. Wilkins R.J., and Hall A.C. Control of matrix synthesis in isolated bovine chondrocytes by extracellular and intracellular pH. J Cell Physiol 164 (1995) 474-481
66. Whitmarsh A.J., and Davis R.J. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 74 (1996) 589-607
67. Urban J.P., Hall A.C., and Gehl K.A. Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes. J Cell Physiol 154 (1993) 262-270
68. Vincent T., Hermansson M., Bolton M., Wait R., and Saklatvala J. Basic FGF mediates an immediate response of articular cartilage to mechanical injury. Proc Natl Acad Sci U S A 99 (2002) 8259-8264
69. 2-terminal kinase activation by mechanical stretch is integrin-dependent and matrix-specific in rat cardiac fibroblasts. J Clin Invest 101 (1998) 301-310
70. Ishida T., Peterson T.E., Kovach N.L., and Berk B.C. MAP kinase activation by flow in endothelial cells. Role of beta 1 integrins and tyrosine kinases. Circ Res 79 (1996) 310-316
71. Davies P.F. Flow-mediated endothelial mechanotransduction. Physiol Rev 75 (1995) 519-560
72. Wilson E., Sudhir K., and Ives H.E. Mechanical strain of rat vascular smooth muscle cells is sensed by specific extracellular matrix/integrin interactions. J Clin Invest 96 (1995) 2364-2372