DOI QR코드

DOI QR Code

Suppression of TNF-alpha-induced MMP-9 expression by a cell-permeable superoxide dismutase in keratinocytes

  • Song, Ha-Yong (Department of Biomedical Science, Research Institute for Bioscience & Biotechnology, Hallym University) ;
  • Ju, Sung-Mi (Department of Biomedical Science, Research Institute for Bioscience & Biotechnology, Hallym University) ;
  • Goh, Ah-Ra (Department of Biomedical Science, Research Institute for Bioscience & Biotechnology, Hallym University) ;
  • Kwon, Dong-Joo (Department of Biomedical Science, Research Institute for Bioscience & Biotechnology, Hallym University) ;
  • Choi, Soo-Young (Department of Biomedical Science, Research Institute for Bioscience & Biotechnology, Hallym University) ;
  • Park, Jin-Seu (Department of Biomedical Science, Research Institute for Bioscience & Biotechnology, Hallym University)
  • Received : 2011.05.02
  • Accepted : 2011.05.06
  • Published : 2011.07.31

Abstract

Up-regulation of selected matrix metalloproteinases (MMPs) such as MMP-9 contributes to inflammatory processes during the development of various skin diseases, such as atopic dermatitis. In this study, we examined the effect of a cell-permeable superoxide dismutase (Tat-SOD) on TNF-${\alpha}$-induced MMP-9 expression in human keratinocyte cells (HaCaT). When Tat-SOD was added to the culture medium of HaCaT cells, it rapidly entered the cells in dose- and time-dependent manners. Tat-SOD decreased TNF-${\alpha}$-induced reactive oxygen species (ROS) generation. Tat-SOD also inhibited TNF-${\alpha}$-induced NF-${\kappa}B$ DNA binding activity. Treatment of HaCaT cells with Tat-SOD significantly inhibited TNF-${\alpha}$-induced mRNA and protein expression of MMP-9, as measured by RT-PCR and Western blot analysis. In addition, Tat-SOD suppressed TNF-${\alpha}$-induced gelatinolytic activity of MMP-9. Taken together, our results indicate that Tat-SOD can suppress TNF-${\alpha}$-induced MMP-9 expression via ROS-NF-${\kappa}B$-dependent mechanisms in keratinocytes, and therefore can be used as an immunomodulatory agent against inflammatory skin diseases related to oxidative stress.

Keywords

References

  1. Deane, J. A. and Hickey, M. J. (2009) Molecular mechanisms of leukocyte trafficking in T-cell-mediated skin inflammation: insights from intravital imaging. Expert. Rev. Mol. Med. 11, e25. https://doi.org/10.1017/S146239940900115X
  2. Lawley, T. J. and Kubota, Y. (1991) Cell adhesion molecules and cutaneous inflammation. Semin. Dermatol. 10, 256-259.
  3. Pilcher, B. K., Wang, M., Qin, X. J., Parks, W. C., Senior, R. M. and Welgus, H. G. (1999) Role of matrix metalloproteinases and their inhibition in cutaneous wound healing and allergic contact hypersensitivity. Ann. N. Y. Acad. Sci. 878, 12-24. https://doi.org/10.1111/j.1749-6632.1999.tb07671.x
  4. Hofmann, U. B., Westphal, J. R., Van Muijen, G. N. and Ruiter, D. J. (2000) Matrix metalloproteinases in human melanoma. J. Invest. Dermatol. 115, 337-344. https://doi.org/10.1046/j.1523-1747.2000.00068.x
  5. Devillers, A. C., van Toorenenbergen, A. W., Klein, Heerenbrink, G. J., Muldert, P. G. and Oranje, A. P. (2007) Elevated levels of plasma matrix metalloproteinase- 9 in patients with atopic dermatitis: a pilot study. Clin. Exp. Dermatol. 32, 311-313. https://doi.org/10.1111/j.1365-2230.2007.02378.x
  6. Harper, J. I., Godwin, H., Green, A., Wilkes, L. E., Holden, N. J., Moffatt, M., Cookson, W. O., Layton, G. and Chandler, S. (2010) A study of matrix metalloproteinase expression and activity in atopic dermatitis using a novel skin wash sampling assay for functional biomarker analysis. Br. J. Dermatol. 162, 397-403. https://doi.org/10.1111/j.1365-2133.2009.09467.x
  7. Bahar-Shany, K., Ravid, A. and Koren, R. (2010) Upregulation of MMP-9 production by TNFalpha in keratinocytes and its attenuation by vitamin D. J. Cell. Physiol. 222, 729-737.
  8. Kim, H. H., Lee, Y., Eun, H. C. and Chung, J. H. (2008) Eicosapentaenoic acid inhibits TNF-alpha-induced matrix metalloproteinase-9 expression in human keratinocytes, HaCaT cells. Biochem. Biophys. Res. Commun. 368, 343-349. https://doi.org/10.1016/j.bbrc.2008.01.062
  9. Dhar, A., Young, M. R. and Colburn, N. H. (2002) The role of AP-1, NF-kappaB and ROS/NOS in skin carcinogenesis: the JB6 model is predictive. Mol. Cell. Biochem. 234-235, 185-193. https://doi.org/10.1023/A:1015948505117
  10. Kohler, H. B., Huchzermeyer, B., Martin, M., De Bruin, A., Meier, B. and Nolte, I. (2001) TNF-alpha dependent NF-kappa B activation in cultured canine keratinocytes is partly mediated by reactive oxygen species. Vet. Dermatol. 12, 129-137. https://doi.org/10.1046/j.1365-3164.2001.00237.x
  11. Young, C. N., Koepke, J. I., Terlecky, L. J., Borkin, M. S., Boyd Savoy, L. and Terlecky, S. R. (2008) Reactive oxygen species in tumor necrosis factor-alpha-activated primary human keratinocytes: implications for psoriasis and inflammatory skin disease. J. Invest. Dermatol. 128, 2606-2614. https://doi.org/10.1038/jid.2008.122
  12. Brenneisen, P., Sies, H. and Scharffetter-Kochanek, K. (2001) Ultraviolet-B irradiation and matrix metalloproteinases: from induction via signaling to initial events. Ann. N. Y. Acad. Sci. 973, 31-43.
  13. Schulze-Osthoff, K., Bauer, M. K., Vogt, M. and Wesselborg, S. (1997) Oxidative stress and signal transduction. Int. J. Vitam. Nutr. Res. 67, 336-342.
  14. Schwarze, S. R. and Dowdy, S. F. (2000) In vivo protein transduction: intracellular delivery of biologically active proteins, compounds and DNA. Trends Pharmacol. Sci. 21, 45-48. https://doi.org/10.1016/S0165-6147(99)01429-7
  15. Schwarze, S. R., Ho, A., Vocero-Akbani, A. and Dowdy, S. F. (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285, 1569-1572. https://doi.org/10.1126/science.285.5433.1569
  16. Lee, J. A., Song, H. Y., Ju, S. M., Lee, S. J., Kwon, H. J., Eum, W. S., Jang, S. H., Choi, S. Y. and Park, J. (2009) Differential regulation of inducible nitric oxide synthase and cyclooxygenase-2 expression by superoxide dismutase in lipopolysaccharide stimulated RAW 264.7 cells. Exp. Mol. Med. 41, 629-637. https://doi.org/10.3858/emm.2009.41.9.069
  17. Lee, J. A., Song, H. Y., Ju, S. M., Lee, S. J., Seo, W. Y., Sin, D. H., Goh, A. R., Choi, S. Y. and Park, J. (2010) Suppression of inducible nitric oxide synthase and cyclooxygenase- 2 by cell-permeable superoxide dismutase in lipopolysaccharide-stimulated BV-2 microglial cells. Mol. Cells 29, 245-250. https://doi.org/10.1007/s10059-010-0031-1
  18. Song, H. Y., Lee, J. A., Ju, S. M., Yoo, K. Y., Won, M. H., Kwon, H. J., Eum, W. S., Jang, S. H., Choi, S. Y. and Park, J. (2008) Topical transduction of superoxide dismutase mediated by HIV-1 Tat protein transduction domain ameliorates 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced inflammation in mice. Biochem. Pharmacol. 75, 1348-1357. https://doi.org/10.1016/j.bcp.2007.11.015
  19. Okayama, Y. (2005) Oxidative stress in allergic and inflammatory skin diseases. Curr. Drug Targets Inflamm. Allergy 4, 517-519. https://doi.org/10.2174/1568010054526386
  20. Greenwald, R. A. (1990) Superoxide dismutase and catalase as therapeutic agents for human diseases. A critical review. Free Radic. Biol. Med. 8, 201-209. https://doi.org/10.1016/0891-5849(90)90092-W
  21. Bickers, D. R. and Athar, M. (2006) Oxidative stress in the pathogenesis of skin disease. J. Invest. Dermatol. 126, 2565-2575. https://doi.org/10.1038/sj.jid.5700340
  22. Vincenti, M. P. and Brinckerhoff, C. E. (2007) Signal transduction and cell-type specific regulation of matrix metalloproteinase gene expression: can MMPs be good for you? J. Cell. Physiol. 213, 355-364. https://doi.org/10.1002/jcp.21208
  23. Park, L. J., Ju, S. M., Song, H. Y., Lee, J. A., Yang, M. Y., Kang, Y. H., Kwon, H. J., Kim, T. Y., Choi, S. Y. and Park, J. (2006) The enhanced monocyte adhesiveness after UVB exposure requires ROS and NF-kappaB signaling in human keratinocyte. J. Biochem. Mol. Biol. 39, 618-625. https://doi.org/10.5483/BMBRep.2006.39.5.618
  24. Seo, W. Y., Goh, A. R., Ju, S. M., Song, H. Y., Kwon, D. J., Jun, J. G., Kim, B. C., Choi, S. Y. and Park, J. (2011) Celastrol induces expression of heme oxygenase-1 through ROS/Nrf2/ARE signaling in the HaCaT cells. Biochem. Biophys. Res. Commun. 407, 535-540. https://doi.org/10.1016/j.bbrc.2011.03.053
  25. Ju, S. M., Song, H. Y., Lee, J. A., Lee, S. J., Choi, S. Y. and Park, J. (2009) Extracellular HIV-1 Tat up-regulates expression of matrix metalloproteinase-9 via a MAPK-NFkappaB dependent pathway in human astrocytes. Exp. Mol. Med. 41, 86-93. https://doi.org/10.3858/emm.2009.41.2.011

Cited by

  1. Paracrine Activity from Adipose-Derived Stem Cells on In Vitro Wound Healing in Human Tympanic Membrane Keratinocytes vol.26, pp.6, 2017, https://doi.org/10.1089/scd.2016.0204
  2. Nuclear Rac1 regulates the bFGF-induced neurite outgrowth in PC12 cells vol.46, pp.12, 2013, https://doi.org/10.5483/BMBRep.2013.46.12.114
  3. trans-Chalcone, a flavonoid precursor, inhibits UV-induced skin inflammation and oxidative stress in mice by targeting NADPH oxidase and cytokine production vol.16, pp.7, 2017, https://doi.org/10.1039/C6PP00442C
  4. Curcumin ameliorates TNF-α-induced ICAM-1 expression and subsequent THP-1 adhesiveness via the induction of heme oxygenase-1 in the HaCaT cells vol.46, pp.8, 2013, https://doi.org/10.5483/BMBRep.2013.46.8.014
  5. DT-13 suppresses MDA-MB-435 cell adhesion and invasion by inhibiting MMP-2/9 via the p38 MAPK pathway vol.6, pp.5, 2012, https://doi.org/10.3892/mmr.2012.1047
  6. Biofunctional activities of squid milt hydrolysate vol.72, pp.OCE4, 2013, https://doi.org/10.1017/S0029665113003261
  7. Epidermal cells help coordinate leukocyte migration during inflammation through fatty acid-fuelled matrix metalloproteinase production vol.5, 2014, https://doi.org/10.1038/ncomms4880
  8. Oxidative stress and antioxidant strategies in dermatology 2016, https://doi.org/10.1179/1351000215Y.0000000015
  9. Therapeutic evaluation of HIV transduction basic domain-conjugated superoxide dismutase solution on suppressive effects of the formation of peroxynitrite and expression of COX-2 in murine skin vol.23, pp.1, 2016, https://doi.org/10.1186/s12929-016-0226-7
  10. Intravenous superoxide dismutase as a protective agent to prevent impairment of lung function induced by high tidal volume ventilation vol.17, pp.1, 2017, https://doi.org/10.1186/s12890-017-0448-9
  11. Anti-invasive effects of decitabine, a DNA methyltransferase inhibitor, through tightening of tight junctions and inhibition of matrix metalloproteinase activities in AGS human gastric carcinoma cells vol.28, pp.3, 2012, https://doi.org/10.3892/or.2012.1858
  12. Role of oxidative stress in chemical allergens induced skin cells activation vol.61, 2013, https://doi.org/10.1016/j.fct.2013.02.038
  13. Blockade of monocyte-endothelial trafficking by transduced Tat-superoxide dismutase protein vol.37, pp.2, 2016, https://doi.org/10.3892/ijmm.2015.2444