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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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NF-κB-dependent Regulation of Matrix Metalloproteinase-9 Gene Expression by Lipopolysaccharide in a Macrophage Cell Line RAW 264.7

  • Rhee, Jae-Won (Department of Biochemistry and Institute of Life Science and Biotechnology, College of Science, Yonsei University) ;
  • Lee, Keun-Wook (Center for Medical Science Research, College of Medicine, Hallym University) ;
  • Kim, Dong-Bum (Center for Medical Science Research, College of Medicine, Hallym University) ;
  • Lee, Young-Hee (Department of Biochemistry, College of Natural Science, Chungbuk National University) ;
  • Jeon, Ok-Hee (Department of Biochemistry and Institute of Life Science and Biotechnology, College of Science, Yonsei University) ;
  • Kwon, Hyung-Joo (Center for Medical Science Research, College of Medicine, Hallym University) ;
  • Kim, Doo-Sik (Department of Biochemistry and Institute of Life Science and Biotechnology, College of Science, Yonsei University)
  • Published : 2007.01.31
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Abstract

Matrix metalloproteinase-9 (MMP-9) plays a pivotal role in the turnover of extracellular matrix (ECM) and in the migration of normal and tumor cells in response to normal physiologic and numerous pathologic conditions. Here, we show that the transcription of the MMP-9 gene is induced by lipopolysaccharide (LPS) stimulation in cells of a macrophage lineage (RAW 264.7 cells). We provide evidence that the NF-$\kappa$B binding site of the MMP-9 gene contributes to its expression in the LPS-signaling pathway, since mutation of NF-$\kappa$B binding site of MMP-9 promoter leads to a dramatic reduction in MMP-9 promoter activation. In addition, the degradation of l$\kappa$B$\alpha$;, and the presences of myeloid differentiation protein (MyD88) and tumor necrosis factor receptor-associated kinase 6 (TRAF6) were found to be required for LPS-activated MMP-9 expression. Chromatin immunoprecipitation (ChIP) assays showed that functional interaction between NF-$\kappa$B and the MMP-9 promoter element is necessary for LPS-activated MMP-9 induction in RAW 264.7 cells. In conclusion, our observations demonstrate that NF-$\kappa$B contributes to LPS-induced MMP-9 gene expression in a mouse macrophage cell line.

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References

  1. Bacon, K. R., Camp, R. D., Cunningham, F. M. and Woollard, P. M. (1988) Contrasting in vitro lymphocyte chemotactic activity of the hydroxyl enantiomers of 12-hydroxy-5,8,10,14-eicosatetraenoic acid. Br. J. Pharmacol. 95, 966-974. https://doi.org/10.1111/j.1476-5381.1988.tb11727.x
  2. Baek, K. H., Ha, S. J. and Sung, Y. C. (2001) A novel function of phosphorothioate oligodeoxynucleotides as chemoattractants for primary macrophages. J. Immunol. 167, 2847-2854. https://doi.org/10.4049/jimmunol.167.5.2847
  3. Bond, M., Fabunmi, R. P., Baker, A. H. and Newby, A. C. (1998) Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-$\kappa$B. FEBS Lett. 435, 29-34. https://doi.org/10.1016/S0014-5793(98)01034-5
  4. Burns, K., Martinon, F., Esslinger, C., Pahl, H., Schneider, P., Bodmer, J. L., Marco, F. D., French, L. and Tschopp, J. (1998) MyD88, an adaptor protein involved in interleukin-1 signaling. J. Biol. Chem. 273, 12203-1229. https://doi.org/10.1074/jbc.273.20.12203
  5. Cao, Z., Xiong, J., Takeuchi, M., Kurama, T. and Goeddel, D. V. (1996) TRAF6 is a signal transducer for interleukin-1. Nature 383, 443-446. https://doi.org/10.1038/383443a0
  6. Dubois, B., Starckx, S., Pagenstecher, A., Oord, J., Arnold, B. and Opdenakker, G. (2002) Gelatinase B deficiency protects against endotoxin shock. Eur. J. Immunol. 32, 2163-2171. https://doi.org/10.1002/1521-4141(200208)32:8<2163::AID-IMMU2163>3.0.CO;2-Q
  7. Galis, Z. S., Sukhova, G. K., Kranzhofer, R., Clark, S. and Libby, P. (1995) Macrophage foam cells from experimental atheroma constitutively produce matrix-degrading proteinase. Proc. Natl. Acad. Sci. USA 92, 402-406. https://doi.org/10.1073/pnas.92.2.402
  8. Holvoet, S., Vincent, C., Schmitt, D. and Serres, M. (2003) The inhibition of MAPK pathway is correlated with downregulation of MMP-9 secretion induced by TNF-$\alpha$ in human keratinocytes. Exp. Cell. Res. 290, 108-119. https://doi.org/10.1016/S0014-4827(03)00293-3
  9. Hoshino, M., Nakamura, Y., Sim, J., Shimojo, J. and Isogai, S. (1998) Bronchial subepithelial fibrosis and expression of matrix metalloproteinase-9 in asthmatic airway inflammation. J. Allergy Clin. Immunol. 102, 783-788. https://doi.org/10.1016/S0091-6749(98)70018-1
  10. Islam, L. N. and Nabi, A. H. M. N. (2003) Endotoxins of enteric pathogens modulate the functions of human neutrophils and lymphocytes. J. Biochem. Mol. Biol. 36, 565-571. https://doi.org/10.5483/BMBRep.2003.36.6.565
  11. Jing, Z., Liu, Y., Dong, M., Hu, S. and Huang, S. (2004) Identification of the DNA binding element of the human ZNF333 protein. J. Biochem. Mol. Biol. 37, 663-670. https://doi.org/10.5483/BMBRep.2004.37.6.663
  12. Kim, D. S., Han, J. H. and Kwon, H. J. (2003) NF-$\kappa$B and c-Jundependent regulation of macrophage inflammatory protein-2 gene expression in response to lipopolysaccharide in RAW 264.7 cells. Mol. Immunol. 40, 633-634. https://doi.org/10.1016/j.molimm.2003.07.001
  13. Klein, G., Vellenga, E., Fraaije, M. W., Kamps, W. A. and de Bont, E. S. J. M. (2004) The possible role of matrix metalloproteinase (MMP)-2 and MMP-9 in cancer, e.g. acute leukemia. Crit. Rev. Oncol. Hematol. 50, 87-100. https://doi.org/10.1016/j.critrevonc.2003.09.001
  14. Kwon, H. J., Lee, K. W., Yu, S. H., Han, J. H. and Kin, D. S. (2003) NF-$\kappa$B-dependent regulation of tumor necrosis factor-a gene expression by CpG-oligodeoxynucleotides. Biochem. Biophys. Res. Commun. 311, 129-138. https://doi.org/10.1016/j.bbrc.2003.09.168
  15. Lai, W. C., Zhou, M., Shankavaram, U., Peng, G. and Wahl, L. M. (2003) Differential regulation of lipopolysaccharide-induced monocyte matrix metalloproteinases (MMP)-1 and MMP-9 by p38 and extracellular signal-regulated kinase 1/2 mitogenactivated protein kinases. J. Immunol. 170, 6244-6249. https://doi.org/10.4049/jimmunol.170.12.6244
  16. Lee, K. W., Lee, Y., Kim, D. S. and Kwon, H. J. (2006) Direct role of NF-kB activation in Toll-like receptor-triggered HLADRA expression. Eur. J. Immunol. 36, 1254-1266. https://doi.org/10.1002/eji.200535577
  17. Lee, K. W., Lee, Y., Kwon, H. J. and Kim, D. S. (2005) Sp1- associated activation of macrophage inflammatory protein-2 promoter by CpG-oligodeoxynucleotide and lipopolysaccharide. Cell. Mol. Life Sci. 62, 188-198. https://doi.org/10.1007/s00018-004-4399-y
  18. Lee, W. J., Shin, C. Y., Yoo, B. K., Ryu, J. R., Choi, E. Y., Cheong, J. H., Ryu, J. H. and Ko, K. H. (2003) Induction of matrix metalloproteinase-9 (MMP-9) in lipopolysaccharidestimulated primary astrocytes is mediated by extracellular signal-regulated protein kinase 1/2 (Erk1/2). Glia 41, 15-24. https://doi.org/10.1002/glia.10131
  19. Lee, Y., Sohn, W. J., Kim, D. S. and Kwon, H. J. (2004) NF-$\kappa$Band c-Jun-dependent regulation of human cytomegalovirus immediate-early gene enhancer/promoter in response to lipopolysaccharide and bacterial CpG-oligodeoxynucleotides in macrophage cell line RAW 264.7. Eur. J. Biochem. 271, 1094-1105. https://doi.org/10.1111/j.1432-1033.2004.04011.x
  20. Opdenakker, G., Van den Steen, P. E. and Van Damme, J. (2001) Gelatinase B: a tuner and amplifier of immune functions. Trends Immunol. 22, 571-579. https://doi.org/10.1016/S1471-4906(01)02023-3
  21. Rhee, J. W., Lee, K. W., Sohn, W. J., Lee, Y., Jeon, O. H., Kwon, H. J. and Kim, D. S. (2007) Regulation of matrix metalloproteinase-9 gene expression and cell migration by NF- $\kappa$B in response to CpG-oligodeoxynucleotides in RAW 264.7 cells. Mol. Immunol. 44, 1393-1400. https://doi.org/10.1016/j.molimm.2006.05.003
  22. Sato, H. and Seiki, M. (1993) Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells. Oncogene 8, 395-405.
  23. Sohn, W. J., Lee, K. W., Lee, Y., Han, J. H., Choe, Y. K., Kim, D. S. and Kwon, H. J. (2005) Pyrrolidine dithiocarbamateinduced macrophage inflammatory protein-2 gene expression is NF-$\kappa$B-independent but c-Jun-dependent in macrophage cell line RAW 264.7. Mol. Immunol. 42, 1165-1175. https://doi.org/10.1016/j.molimm.2004.11.016
  24. Song, H. Y., Regnier, C. H., Kirschning, C. J., Goeddel, D. V. and Rothe, M. (1997) Tumor necrosis factor (TNF)-mediated kinase cascades: bifurcation of nuclear factor-kappaB and c-jun Nterminal kinase (JNK/SAPK) pathways at TNF receptorassociated factor 2. Proc. Natl. Acad. Sci. USA 94, 9792-9796. https://doi.org/10.1073/pnas.94.18.9792
  25. Underwood, D. C., Osborn, R. R., Bochnowicz, S., Webb, E. F., Rieman, D. J., Lee, J. C., Romanic, A. M., Adams, J. L., Hay, D. W. and Griswold, D. E. (2000) SB 239063, a p38 MAPK inhibitor, reduces neutrophilia, inflammatory cytokines, MMP- 9, and fibrosis in lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, L895-902. https://doi.org/10.1152/ajplung.2000.279.5.L895
  26. Van den Steen, P. E., Dubois, B., Nelissen, I., Rudd, P. M., Dwek, R. A. and Opdenakker, G.. (2002) Biochemistry and molecular biology of gelatinase B or matrix-metalloproteinase-9 (MMP-9). Crit. Rev. Biochem. Mol. Biol. 37, 375-536. https://doi.org/10.1080/10409230290771546
  27. Visse, R. and Nagasse. H. (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92, 827-839. https://doi.org/10.1161/01.RES.0000070112.80711.3D
  28. Woo, C. H., Lim, J. H. and Kim, J. H. (2004) Lipopolysaccharide induces matrix metalloproteinase-9 expression via a mitochondrial reactive oxygen species-p38 kinase-activator protein-1 pathway in Raw 264.7 cells. J. Immunol. 173, 6973-6980. https://doi.org/10.4049/jimmunol.173.11.6973
  29. Yoon, S. O., Park, S. J., Yun, C. H. and Chung, A. S. (2003) Roles of matrix metalloproteinases in tumor metastasis and angiogenesis. J. Biochem. Mol. Biol. 36, 128-137. https://doi.org/10.5483/BMBRep.2003.36.1.128
  30. Zhang, F. X., Kirschning, C. J., Mancinelli, R., Xu, X.-P., Jin, Y., Faure, E., Mantovani, A., Rothe, M., Muzio, M. and Arditi, M. (1999) Bacterial lipopolysaccharide activates nuclear factor-kB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J. Biol. Chem. 274, 7611-7614. https://doi.org/10.1074/jbc.274.12.7611

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