The antagonistic actions of endogenous interleukin-1β and 15-deoxy-Δ12,14-prostaglandin J2 regulate the temporal synthesis of matrix metalloproteinase-9 in sheared chondrocytes

Journal of Biological Chemistry

Volumn 287, Issue 38, 2012, Pages 31877-31893

  Wang, Pu ^a,c   Zhu, Fei ^a   Konstantopoulos, Konstantinos ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c NORTHEASTERN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTAGONISTIC EFFECTS; ARTICULAR CARTILAGES; BASAL LEVELS; CHONDROCYTE CELLS; CHONDROCYTES; DEVELOPING STRATEGY; EXPOSURE TIME; FLUID SHEAR; FLUID SHEAR STRESS; HUMAN CHONDROCYTES; HYDROSTATIC STRESS; INTERLEUKIN-1; LATE STAGE; MATRIX METALLOPROTEINASE-9; MODEL SYSTEM; PROINFLAMMATORY CYTOKINES; SIGNALING NETWORKS; UNDERLYING MECHANISM;

BODY FLUIDS; CARTILAGE; CELL CULTURE; CHEMICAL ACTIVATION; SIGNALING; STRESSES;

SHEAR FLOW;

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; SHEAR STRESS; SIGNAL TRANSDUCTION;

CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-1BETA; MATRIX METALLOPROTEINASE 9; MODELS, BIOLOGICAL; OSTEOARTHRITIS; PROSTAGLANDIN D2; SHEAR STRENGTH; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; TIME FACTORS;

EID: 84866392795     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.362731     Document Type: Article

References (46)

1. Carter, D. R., Beaupré, G. S., Wong, M., Smith, R. L., Andriacchi, T. P., and Schurman, D. J. (2004) The mechanobiology of articular cartilage development and degeneration. Clin. Orthop. Relat. Res. 427, (suppl.) S69-S77 (Pubitemid 39362804)
2. Buckwalter, J. A., Martin, J. A., and Brown, T. D. (2006) Perspectives on chondrocyte mechanobiology and osteoarthritis. Biorheology 43, 603-609 (Pubitemid 44221940)
3. Zhu, F., Wang, P., Lee, N. H., Goldring, M. B., and Konstantopoulos, K. (2010) Prolonged application of high fluid shear to chondrocytes recapitulates gene expression profiles associated with osteoarthritis. PLoSONE5, e15174
4. Goldring, M. B. (2000) Osteoarthritis and cartilage: the role of cytokines. Curr. Rheumatol. Rep. 2, 459-465
5. Daheshia, M., and Yao, J. Q. (2008) The interleukin 1β pathway in the pathogenesis of osteoarthritis. J. Rheumatol. 35, 2306-2312
6. Akhtar, N., Miller, M. J., and Haqqi, T. M. (2011) Effect of a herbal-leucine mix on the IL-1β-induced cartilage degradation and inflammatory gene expression in human chondrocytes. BMC Complement. Altern. Med. 11, 66
7. Söder, S., Roach, H. I., Oehler, S., Bau, B., Haag, J., and Aigner, T. (2006) MMP-9/gelatinase B is a gene product of human adult articular chondrocytes and increased in osteoarthritic cartilage. Clin. Exp. Rheumatol. 24, 302-304 (Pubitemid 44151150)
8. Tsuchiya, K., Maloney, W. J., Vu, T., Hoffman, A. R., Huie, P., Sibley, R., Schurman, D. J., and Smith, R. L. (1997) Osteoarthritis: differential expression of matrix metalloproteinase-9 mRNA in nonfibrillated and fibrillated cartilage. J. Orthop. Res. 15, 94-100 (Pubitemid 27111206)
9. Tetlow, L. C., Adlam, D. J., and Woolley, D. E. (2001) Matrix metalloproteinase and proinflammatory cytokine production by chondrocytes of human osteoarthritic cartilage: associations with degenerative changes. Arthritis Rheum. 44, 585-594 (Pubitemid 32234617)
10. Naito, K., Takahashi, M., Kushida, K., Suzuki, M., Ohishi, T., Miura, M., Inoue, T., and Nagano, A. (1999) Measurement of matrix metalloproteinases (MMPs) and tissue inhibitor of metalloproteinases-1 (TIMP-1) in patients with knee osteoarthritis: comparison with generalized osteoarthritis. Rheumatology (Oxford) 38, 510-515 (Pubitemid 29504835)
11. Freemont, A. J., Hampson, V., Tilman, R., Goupille, P., Taiwo, Y., and Hoyland, J. A. (1997) Gene expression of matrix metalloproteinases 1, 3, and 9 by chondrocytes in osteoarthritic human knee articular cartilage is zone- and grade-specific. Ann. Rheum. Dis. 56, 542-549 (Pubitemid 27428477)
12. Pelletier, J. P., Martel-Pelletier, J., and Abramson, S. B. (2001) Osteoarthritis, an inflammatory disease: potential implication for the selection of new therapeutic targets. Arthritis Rheum. 44, 1237-1247 (Pubitemid 32537520)
13. Wang, P., Zhu, F., Lee, N. H., and Konstantopoulos, K. (2010) Shearinduced interleukin-6 synthesis in chondrocytes: roles of E prostanoid (EP) 2 and EP3 in cAMP/protein kinase A- and PI3K/Akt-dependent NF-κB activation. J. Biol. Chem. 285, 24793-24804
14. Wang, P., Zhu, F., Tong, Z., and Konstantopoulos, K. (2011) Response of chondrocytes to shear stress: antagonistic effects of the binding partners Toll-like receptor 4 and caveolin-1. FASEB J. 25, 3401-3415
15. Zhu, F., Wang, P., Kontrogianni-Konstantopoulos, A., and Konstantopoulos, K. (2010) Prostaglandin (PG)D(2) and 15-deoxy-Δ(12,14)-PGJ(2), but not PGE(2), mediate shear-induced chondrocyte apoptosis via protein kinase A-dependent regulation of Polo-like kinases. Cell Death Differ. 17, 1325-1334
16. Tacon, C. E., Wiehler, S., Holden, N. S., Newton, R., Proud, D., and Leigh, R. (2010) Human rhinovirus infection up-regulates MMP-9 production in airway epithelial cells via NF-κB. Am. J. Respir. Cell Mol. Biol. 43, 201-209
17. Abulencia, J. P., Gaspard, R., Healy, Z. R., Gaarde, W. A., Quackenbush, J., and Konstantopoulos, K. (2003) Shear-induced cyclooxygenase-2 via a JNK2/c-Jun-dependent pathway regulates prostaglandin receptor expression in chondrocytic cells. J. Biol. Chem. 278, 28388-28394 (Pubitemid 36935739)
18. Healy, Z. R., Lee, N. H., Gao, X., Goldring, M. B., Talalay, P., Kensler, T. W., and Konstantopoulos, K. (2005) Divergent responses of chondrocytes and endothelial cells to shear stress: cross-talk among COX-2, the phase 2 response, and apoptosis. Proc. Natl. Acad. Sci. U.S.A. 102, 14010-14015 (Pubitemid 41377694)
19. Healy, Z. R., Zhu, F., Stull, J. D., and Konstantopoulos, K. (2008) Elucidation of the signaling network of COX-2 induction in sheared chondrocytes: COX-2 is induced via a Rac/MEKK1/MKK7/JNK2/c-Jun-C/EBPβ-dependent pathway. Am. J. Physiol. Cell Physiol. 294, C1146-C1157
20. Wang, P., Zhu, F., and Konstantopoulos, K. (2010) Prostaglandin E2 induces interleukin-6 expression in human chondrocytes via cAMP/protein kinase A- and phosphatidylinositol 3-kinase-dependent NF-κB activation. Am. J. Physiol. Cell Physiol. 298, C1445-C1456
21. Wang, P., Zhu, F., and Konstantopoulos, K. (2011) Interleukin-6 synthesis in human chondrocytes is regulated via the antagonistic actions of prostaglandin (PG)E2 and 15-deoxy-Δ(12,14)-PGJ2. PLoS ONE 6, e27630
22. Hu, D., Man, Z., Wang, P., Tan, X., Wang, X., Takaku, S., Hyuga, S., Sato, T., Yao, X., Yamagata, S., and Yamagata, T. (2007) Ganglioside GD1a negatively regulates matrix metalloproteinase-9 expression in mouse FBJ cell lines at the transcriptional level. Connect. Tissue Res. 48, 198-205 (Pubitemid 47189883)
23. Goldring, M. B., Birkhead, J. R., Suen, L. F., Yamin, R., Mizuno, S., Glowacki, J., Arbiser, J. L., and Apperley, J. F. (1994) Interleukin-1β- modulated gene expression in immortalized human chondrocytes. J. Clin. Invest. 94, 2307-2316
24. Martel-Pelletier, J. (2004) Pathophysiology of osteoarthritis. Osteoarthr. Cartil. 12, Suppl. A, S31-S33
25. Hashimoto, K., Ethridge, R. T., and Evers, B. M. (2002) Peroxisome proliferator- activated receptor γ ligand inhibits cell growth and invasion of human pancreatic cancer cells. Int. J. Gastrointest. Cancer 32, 7-22 (Pubitemid 36323098)
26. Marx, N., Schönbeck, U., Lazar, M. A., Libby, P., and Plutzky, J. (1998) Peroxisome proliferator-activated receptor γ activators inhibit gene expression and migration in human vascular smooth muscle cells. Circ. Res. 83, 1097-1103 (Pubitemid 28533518)
27. Wada, T., and Penninger, J. M. (2004) Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23, 2838-2849 (Pubitemid 38638846)
28. Forman, B. M., Tontonoz, P., Chen, J., Brun, R. P., Spiegelman, B. M., and Evans, R. M. (1995) 15-Deoxy-Δ12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPARγ. Cell 83, 803-812 (Pubitemid 3006324)
29. Pearle, A. D., Warren, R. F., and Rodeo, S. A. (2005) Basic science of articular cartilage and osteoarthritis. Clin. Sports Med. 24, 1-12 (Pubitemid 43073031)
30. Lu, Y. C., Jayakumar, T., Duann, Y. F., Chou, Y. C., Hsieh, C. Y., Yu, S. Y., Sheu, J. R., and Hsiao, G. (2011) Chondroprotective role of sesamol by inhibiting MMPs expression via retaining NF-κB signaling in activated SW1353 cells. J. Agric. Food Chem. 59, 4969-4978
31. Fahmi, H., Di Battista, J. A., Pelletier, J. P., Mineau, F., Ranger, P., and Martel-Pelletier, J. (2001) Peroxisome proliferator-activated receptor γactivators inhibit interleukin-1β-induced nitric oxide and matrix metalloproteinase-13 production in human chondrocytes. Arthritis Rheum. 44, 595-607 (Pubitemid 32234618)
32. 2. Arthritis Rheum. 58, 3530-3540
33. Pustovrh, M. C., Capobianco, E., Martínez, N., Higa, R., White, V., and Jawerbaum, A. (2009) MMP/TIMP balance is modulated in vitro by 15dPGJ(2) in fetuses and placentas from diabetic rats. Eur. J. Clin. Investig. 39, 1082-1090
34. Boyault, S., Bianchi, A., Moulin, D., Morin, S., Francois, M., Netter, P., Terlain, B., and Bordji, K. (2004) 15-Deoxy-Δ(12,14)-prostaglandin J(2) inhibits IL-1β-induced IKK enzymatic activity and IκBα degradation in rat chondrocytes through a PPARγ-independent pathway. FEBS Lett. 572, 33-40 (Pubitemid 39092509)
35. Papageorgiou, E., Pitulis, N., Msaouel, P., Lembessis, P., and Koutsilieris, M. (2007) The non-genomic cross-talk between PPAR-γ ligands and ERK1/2 in cancer cell lines. Expert Opin. Ther. Targets 11, 1071-1085 (Pubitemid 47240680)
36. Ahmed, S., Wang, N., Hafeez, B. B., Cheruvu, V. K., and Haqqi, T. M. (2005) Punica granatum L. extract inhibits IL-1β-induced expression of matrix metalloproteinases by inhibiting the activation of MAP kinases and NF-κB in human chondrocytes in vitro. J. Nutr. 135, 2096-2102 (Pubitemid 41298371)
37. Lin, Y. C., Liang, Y. C., Sheu, M. T., Lin, Y. C., Hsieh, M. S., Chen, T. F., and Chen, C. H. (2008) Chondroprotective effects of glucosamine involving the p38 MAPK and Akt signaling pathways. Rheumatol. Int. 28, 1009-1016
38. Wu, C. Y., Hsieh, H. L., Sun, C. C., Tseng, C. P., and Yang, C. M. (2008) IL-1β induces proMMP-9 expression via c-Src-dependent PDGFR/PI3K/Akt/p300 cascade in rat brain astrocytes. J. Neurochem. 105, 1499-1512
39. Xie, Z., Singh, M., and Singh, K. (2004) Differential regulation of matrix metalloproteinase-2 and -9 expression and activity in adult rat cardiac fibroblasts in response to interleukin-1β. J. Biol. Chem. 279, 39513-39519 (Pubitemid 39258218)
40. Wu, C. Y., Hsieh, H. L., Sun, C. C., and Yang, C. M. (2009) IL-1β induces MMP-9 expression via a Ca2+-dependent CaMKII/JNK/c-JUN cascade in rat brain astrocytes. Glia 57, 1775-1789
41. Liang, K. C., Lee, C. W., Lin, W. N., Lin, C. C., Wu, C. B., Luo, S. F., and Yang, C. M. (2007) Interleukin-1β induces MMP-9 expression via p42/p44 MAPK, p38 MAPK, JNK, and nuclear factor κB signaling pathways in human tracheal smooth muscle cells. J. Cell. Physiol. 211, 759-770
42. Funovics, P., Brostjan, C., Nigisch, A., Fila, A., Grochot, A., Mleczko, K., Was, H., Weigel, G., Dulak, J., and Jozkowicz, A. (2006) Effects of 15d-PGJ(2) on VEGF-induced angiogenic activities and expression of VEGF receptors in endothelial cells. Prostaglandins Other Lipid Mediat. 79, 230-244
43. 2 in colon carcinoma cells: evidence for a redox-sensitive peroxisome proliferator-activated receptor γ-independent mechanism. Cancer Res. 64, 5162-5171
44. 2. J. Biol. Chem. 278, 51251-51260
45. Lianxu, C., Hongti, J., and Changlong, Y. (2006) Lianxu, C., Hongti, J., and Changlong, Y. (2006) NF-κBp65-specific siRNA inhibits expression of genes of COX-2, NOS-2, and MMP-9 in rat IL-1β-induced and TNF-α-induced chondrocytes. Osteoarthr. Cartil. 14, 367-376 (Pubitemid 44268926)
46. Shakibaei, M., John, T., Schulze-Tanzil, G., Lehmann, I., and Mobasheri, A. (2007) Suppression of NF-κB activation by curcumin leads to inhibition of expression of cyclo-oxygenase-2 and matrix metalloproteinase-9 in human articular chondrocytes: implications for the treatment of osteoarthritis. Biochem. Pharmacol. 73, 1434-1445 (Pubitemid 46452591)