Tumor necrosis factor-α- and interleukin-1β-dependent matrix metalloproteinase-3 expression in nucleus pulposus cells requires cooperative signaling via syndecan 4 and mitogen-activated protein kinase-NF-κB axis: Implications in inflammatory disc disease

American Journal of Pathology

Volumn 184, Issue 9, 2014, Pages 2560-2572

  Wang, Xin ^a,b   Wang, Hua ^a,c   Yang, Hao ^a,c   Li, Jun ^a,d   Cai, Qiqing ^b   Shapiro, Irving M ^a   Risbud, Makarand V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b ZHENGZHOU UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LENTIVIRUS VECTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 11; MITOGEN ACTIVATED PROTEIN KINASE 12; MITOGEN ACTIVATED PROTEIN KINASE 13; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; SHORT HAIRPIN RNA; STROMELYSIN; SYNAPTOTAGMIN I; SYNDECAN 4; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATORY DISEASE; INTERVERTEBRAL DISK DEGENERATION; INTRACELLULAR SIGNALING; LOSS OF FUNCTION MUTATION; NONHUMAN; NUCLEUS PULPOSUS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; UPREGULATION; ANIMAL; IMMUNOLOGY; INTERVERTEBRAL DISK; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADULT; ANIMALS; BLOTTING, WESTERN; FEMALE; HUMANS; INTERLEUKIN-1BETA; INTERVERTEBRAL DISC; INTERVERTEBRAL DISC DEGENERATION; MALE; MATRIX METALLOPROTEINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; RATS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SYNDECAN-4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84906222579     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.06.006     Document Type: Article

References (49)

1. F. Balague, A.F. Mannion, F. Pellise, and C. Cedraschi Non-specific low back pain Lancet 379 2012 482 491
2. J.N. Katz Lumbar disc disorders and low-back pain: socioeconomic factors and consequences J Bone Joint Surg Am 88 2006 21 24
3. E. Arana, L. Marti-Bonmati, E. Molla, and S. Costa Upper thoracic-spine disc degeneration in patients with cervical pain Skeletal Radiol 33 2004 29 33
4. G. Livshits, M. Popham, I. Malkin, P.N. Sambrook, A.J. Macgregor, T. Spector, and F.M. Williams Lumbar disc degeneration and genetic factors are the main risk factors for low back pain in women: the UK Twin Spine Study Ann Rheum Dis 70 2011 1740 1745
5. H. Feng, M. Danfelter, B. Stromqvist, and D. Heinegard Extracellular matrix in disc degeneration J Bone Joint Surg Am 88 2006 25 29
6. J.P. Urban, and S. Roberts Degeneration of the intervertebral disc Arthritis Res Ther 5 2003 120 130
7. J.P. Rutges, J.A. Kummer, F.C. Oner, A.J. Verbout, R.J. Castelein, H.J. Roestenburg, W.J. Dhert, and L.B. Creemers Increased MMP-2 activity during intervertebral disc degeneration is correlated to MMP-14 levels J Pathol 214 2008 523 530
8. S. Roberts, B. Caterson, J. Menage, E.H. Evans, D.C. Jaffray, and S.M. Eisenstein Matrix metalloproteinases and aggrecanase: their role in disorders of the human intervertebral disc Spine (Phila Pa 1976) 25 2000 3005 3013
9. A.J. Pockert, S.M. Richardson, C.L. Le Maitre, M. Lyon, J.A. Deakin, D.J. Buttle, A.J. Freemont, and J.A. Hoyland Modified expression of the ADAMTS enzymes and tissue inhibitor of metalloproteinases 3 during human intervertebral disc degeneration Arthritis Rheum 60 2009 482 491
10. G. Murphy, R.M. Hembry, C.E. Hughes, A.J. Fosang, and T.E. Hardingham Role and regulation of metalloproteinases in connective tissue turnover Biochem Soc Trans 18 1990 812 815
11. J. Liu, P.J. Roughley, and J.S. Mort Identification of human intervertebral disc stromelysin and its involvement in matrix degradation J Orthop Res 9 1991 568 575
12. J.R. Chin, G. Murphy, and Z. Werb Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fibroblasts in parallel with collagenase: biosynthesis, isolation, characterization, and substrates J Biol Chem 260 1985 12367 12376
13. M. Durigova, H. Nagase, J.S. Mort, and P.J. Roughley MMPs are less efficient than ADAMTS5 in cleaving aggrecan core protein Matrix Biol 30 2011 145 153
14. R.K. Studer, L.G. Gilbertson, H. Georgescu, G. Sowa, N. Vo, and J.D. Kang p38 MAPK inhibition modulates rabbit nucleus pulposus cell response to IL-1 J Orthop Res 26 2008 991 998
15. J.J. Wu, M.W. Lark, L.E. Chun, and D.R. Eyre Sites of stromelysin cleavage in collagen types II, IX, X, and XI of cartilage J Biol Chem 266 1991 5625 5628
16. G. Murphy, M.I. Cockett, P.E. Stephens, B.J. Smith, and A.J. Docherty Stromelysin is an activator of procollagenase: a study with natural and recombinant enzymes Biochem J 248 1987 265 268
17. K. Imai, Y. Yokohama, I. Nakanishi, E. Ohuchi, Y. Fujii, N. Nakai, and Y. Okada Matrix metalloproteinase 7 (matrilysin) from human rectal carcinoma cells: activation of the precursor, interaction with other matrix metalloproteinases and enzymic properties J Biol Chem 270 1995 6691 6697
18. Y. Ogata, J.J. Enghild, and H. Nagase Matrix metalloproteinase3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9 J Biol Chem 267 1992 3581 3584
19. J. Wang, D. Markova, D.G. Anderson, Z. Zheng, I.M. Shapiro, and M.V. Risbud TNF-alpha and IL-1beta promote a disintegrin-like and metalloprotease with thrombospondin type I motif-5-mediated aggrecan degradation through syndecan-4 in intervertebral disc J Biol Chem 286 2011 39738 39749
20. C.L. Le Maitre, J.A. Hoyland, and A.J. Freemont Catabolic cytokine expression in human IVD degeneration: IL-1b and TNFa expression profile Arthritis Res Ther 9 2007 R77
21. M.V. Risbud, and I.M. Shapiro Role of cytokines in intervertebral disc degeneration: pain and disc content Nat Rev Rheumatol 10 2014 44 56
22. C.A. Séguin, R.M. Pilliar, P.J. Roughley, and R.A. Kandel Tumor necrosis factor-alpha modulates matrix production and catabolism in nucleus pulposus tissue Spine (Phila Pa 1976) 30 2005 1940 1948
23. H.J. Kim, J.S. Yeom, Y.G. Koh, J.E. Yeo, K.T. Kang, Y.M. Kang, B.S. Chang, and C.K. Lee Anti-inflammatory effect of platelet-rich plasma on nucleus pulposus cells with response of TNF-α and IL-1 J Orthop Res 32 2013 551 556
24. S.J. Millward-Sadler, P.W. Costello, A.J. Freemont, and J.A. Hoyland Regulation of catabolic gene expression in normal and degenerate human intervertebral disc cells: implications for the pathogenesis of intervertebral disc degeneration Arthritis Res Ther 11 2009 R65
25. J.S. Kim, M.B. Ellman, D. Yan, H.S. An, R. Kc, X. Li, D. Chen, G. Xiao, G. Cs-Szabo, D.W. Hoskin, D.D. Buechter, A.J. Van Wijnen, and H.J. Im Lactoferricin mediates anti-inflammatory and anti-catabolic effects via inhibition of IL-1 and LPS activity in the intervertebral disc J Cell Physiol 228 2013 1884 1896
26. K.L. Phillips, N. Jordan-Mahy, M.J. Nicklin, and C.L. Le Maitre Interleukin-1 receptor antagonist deficient mice provide insights into pathogenesis of human intervertebral disc degeneration Ann Rheum Dis 72 2013 1860 1867
27. K. Fujita, T. Ando, T. Ohba, M. Wako, N. Sato, Y. Nakamura, Y. Ohnuma, Y. Hara, R. Kato, A. Nakao, and H. Haro Age-related expression of MCP-1 and MMP-3 in mouse intervertebral disc in relation to TWEAK and TNF-α stimulation J Orthop Res 30 2012 599 605
28. K. Wuertz, L. Quero, M. Sekiguchi, M. Klawitter, A. Nerlich, S. Konno, S. Kikuchi, and N. Boos The red wine polyphenol resveratrol shows promising potential for the treatment of nucleus pulposus-mediated pain in vitro and in vivo Spine (Phila Pa 1976) 36 2011 E1373 E1384
29. S. Canbay, N. Turhan, M. Bozkurt, K. Arda, and S. Caglar Correlation of matrix metalloproteinase-3 expression with patient age, magnetic resonance imaging and histopathological grade in lumbar disc degeneration Turk Neurosurg 23 2013 427 433
30. J. Bertrand, R. Stange, H. Hidding, F. Echtermeyer, G. Nalesso, L. Godmann, M. Timmen, P. Bruckner, F. Dell'Accio, M.J. Raschke, T. Pap, and R. Dreier Syndecan 4 supports bone fracture repair, but not fetal skeletal development, in mice Arthritis Rheum 65 2013 743 752
31. F. Echtermeyer, J. Bertrand, R. Dreier, I. Meinecke, K. Neugebauer, M. Fuerst, Y.J. Lee, Y.W. Song, C. Herzog, G. Theilmeier, and T. Pap Syndecan-4 regulates ADAMTS-5 activation and cartilage breakdown in osteoarthritis Nat Med 15 2009 1072 1076
32. D. Jiang, J. Liang, G.S. Campanella, R. Guo, S. Yu, T. Xie, N. Liu, Y. Jung, R. Homer, E.B. Meltzer, Y. Li, A.M. Tager, P.F. Goetinck, A.D. Luster, and P.W. Noble Inhibition of pulmonary fibrosis in mice by CXCL10 requires glycosaminoglycan binding and syndecan-4 J Clin Invest 120 2010 2049 2057
33. N. Charnaux, S. Brule, M. Hamon, T. Chaigneau, L. Saffar, C. Prost, N. Lievre, and L. Gattegno Syndecan-4 is a signaling molecule for stromal cell-derived factor-1 (SDF-1)/CXCL12 FEBS J 272 2005 1937 1951
34. H. Slimani, N. Charnaux, E. Mbemba, L. Saffar, R. Vassy, C. Vita, and L. Gattegno Binding of the CC-chemokine RANTES to syndecan-1 and syndecan-4 expressed on HeLa cells Glycobiology 13 2003 623 634
35. W.L. Shih, M.H. Liao, F.L. Yu, P.Y. Lin, H.Y. Hsu, and S.J. Chiu AMF/PGI transactivates the MMP-3 gene through the activation of Src-RhoA- phosphatidylinositol 3-kinase signaling to induce hepatoma cell migration Cancer Lett 270 2008 202 217
36. M.V. Risbud, A. Guttapalli, D.G. Stokes, D. Hawkins, K.G. Danielson, T.P. Schaer, T.J. Albert, and I.M. Shapiro Nucleus pulposus cells express HIF-1 alpha under normoxic culture conditions: a metabolic adaptation to the intervertebral disc microenvironment J Cell Biochem 98 2006 152 159
37. M. Kanemoto, S. Hukuda, Y. Komiya, A. Katsuura, and J. Nishioka Immunohistochemical study of matrix metalloproteinase-3 and tissue inhibitor of metalloproteinase-1 human intervertebral discs Spine (Phila Pa 1976) 21 1996 1 8
38. M. Takahashi, H. Haro, Y. Wakabayashi, T. Kawa-uchi, H. Komori, and K. Shinomiya The association of degeneration of the intervertebral disc with 5a/6a polymorphism in the promoter of the human matrix metalloproteinase-3 gene J Bone Joint Surg Br 83 2001 491 495
39. L. Aulisa, P. Papaleo, E. Pola, F. Angelini, A.G. Aulisa, F.C. Tamburrelli, P. Pola, and C.A. Logroscino Association between IL-6 and MMP-3 gene polymorphisms and adolescent idiopathic scoliosis: a case-control study Spine (Phila Pa 1976) 32 2007 2700 2702
40. Y. Tian, W. Yuan, N. Fujita, J. Wang, H. Wang, I.M. Shapiro, and M.V. Risbud Inflammatory cytokines associated with degenerative disc disease control aggrecanase-1 (ADAMTS-4) expression in nucleus pulposus cells through MAPK and NF-kappaB Am J Pathol 182 2013 2310 2321
41. C.L. Le Maitre, A.J. Freemont, and J.A. Hoyland The role of interleukin-1 in the pathogenesis of human intervertebral disc degeneration Arthritis Res Ther 2005 R732 R745
42. C. Fuerer, S.J. Habib, and R. Nusse A study on the interactions between heparan sulfate proteoglycans and Wnt proteins Dev Dyn 239 2010 184 190
43. S.C. Chang, B. Mulloy, A.I. Magee, and J.R. Couchman Two distinct sites in sonic Hedgehog combine for heparan sulfate interactions and cell signaling functions J Biol Chem 286 2011 44391 44402
44. M. Klawitter, L. Quero, J. Klasen, T. Liebscher, A. Nerlich, N. Boos, and K. Wuertz Triptolide exhibits anti-inflammatory, anti-catabolic as well as anabolic effects and suppresses TLR expression and MAPK activity in IL-1β treated human intervertebral disc cells Eur Spine J 21 2012 S850 S859
45. J. Wang, Y. Tian, K.L. Phillips, N. Chiverton, G. Haddock, R.A. Bunning, A.K. Cross, I.M. Shapiro, C.L. Le Maitre, and M.V. Risbud Tumor necrosis factor α- and interleukin-1β-dependent induction of CCL3 expression by nucleus pulposus cells promotes macrophage migration through CCR1 Arthritis Rheum 65 2013 832 842
46. S. Loffek, O. Schilling, and C.W. Franzke Series "matrix metalloproteinases in lung health and disease": biological role of matrix metalloproteinases: a critical balance Eur Respir J 38 2011 191 208
47. el-S. Akool, H. Kleinert, F.M. Hamada, M.H. Abdelwahab, U. Forstermann, J. Pfeilschifter, and W. Eberhardt Nitric oxide increases the decay of matrix metalloproteinase 9 mRNA by inhibiting the expression of mRNA-stabilizing factor HuR Mol Cell Biol 23 2003 4901 4916
48. J. Xie, C. Wang, D.Y. Huang, Y. Zhang, J. Xu, S.S. Kolesnikov, K.L. Sung, and H. Zhao TGF-beta1 induces the different expressions of lysyl oxidases and matrix metalloproteinases in anterior cruciate ligament and medial collateral ligament fibroblasts after mechanical injury J Biomech 46 2013 890 898
49. Y.J. Lee, M.H. Kong, K.Y. Song, K.H. Lee, and S.H. Heo The relation between Sox9, TGF-beta1, and proteoglycan in human intervertebral disc cells J Korean Neurosurg Soc 43 2008 149 154