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Suppression of Transglutaminase-2 is Involved in Anti-Inflammatory Actions of Glucosamine in 12-O-Tetradecanoylphorbol-13-Acetate-Induced Skin Inflammation

  • Park, Mi-Kyung (College of Pharmacy, Dongguk University) ;
  • Cho, Sun-A (R & D Center, AmorePacific Corporation) ;
  • Lee, Hye-Ja (College of Pharmacy, Dongguk University) ;
  • Lee, Eun-Ji (College of Pharmacy, Dongguk University) ;
  • Kang, June-Hee (College of Pharmacy, Dongguk University) ;
  • Kim, You-Lee (College of Pharmacy, Dongguk University) ;
  • Kim, Hyun-Ji (College of Pharmacy, Dongguk University) ;
  • Oh, Seung-Hyun (College of Pharmacy, Gachon University of Medicine and Science) ;
  • Choi, Chang-Sun (Department of Food and Nutrition, College of Human Ecology, Chung-Ang University) ;
  • Lee, Ho (College of Pharmacy, Gachon University of Medicine and Science) ;
  • Kim, Soo-Youl (National Cancer Center) ;
  • Lee, Chang-Hoon (College of Pharmacy, Dongguk University)
  • Received : 2012.05.29
  • Accepted : 2012.07.10
  • Published : 2012.07.31

Abstract

Glucosamine (GS) is well known for the treatment of inflammation. However, the mechanism and efficacy of GS for skin inflammation are unclear. The aim of this study was to evaluate the effects and mechanism of GS in the mouse 12-O-tetradecanoyl 13-acetate (TPA)-induced ear edema model. TPA-induced ear edema was evoked in ICR or transglutaminase 2 (Tgase-2) (-/-) mice. GS was administered orally (10-100 mg/kg) or topically (0.5-2.0 w/v %) prior to TPA treatment. Orally administered GS at 10 mg/kg showed a 76 or 57% reduction in ear weight or myeloperoxidase, respectively, and a decreased expression of cyclooxygenase-2 (COX-2), NF-${\kappa}B$ and Tgase-2 in TPA-induced ear edema by western blot and immunohistochemistry. Role of Tgase-2 in TPA ear edema is examined using Tgase-2 (-/-) mice and TPA did not induce COX-2 expression in ear of Tgase-2 (-/-) mice. These observations suggested that Tgase-2 is involved in TPA-induced COX-2 expression in the inflamed ear of mice and antiinflammatory effects of glucosamine is mediated through suppression of Tgase-2 in TPA ear edema.

Keywords

References

  1. Bradley, P. P., Priebat, D. A., Christensen, R. D. and Rothstein, G. (1982) Measurement of cutaneous infl ammation: estimation of neutrophil content with an enzyme marker. J. Invest. Dermatol. 78, 206-209. https://doi.org/10.1111/1523-1747.ep12506462
  2. Choi, Y. H., Son, K. H., Chang, H. W., Bae, K., Kang, S. S. and Kim, H. P. (2005) New anti-infl ammatory formulation containing Synurus deltoides extract. Arch. Pharm. Res. 28, 848-853. https://doi.org/10.1007/BF02977352
  3. Chung, W. Y., Park, J. H., Kim, M. J., Kim, H. O., Hwang, J. K., Lee, S. K. and Park, K. K. (2007) Xanthorrhizol inhibits 12-O-tetradecanoylphorbol- 13-acetate-induced acute infl ammation and twostage mouse skin carcinogenesis by blocking the expression of ornithine decarboxylase, cyclooxygenase-2 and inducible nitric oxide synthase through mitogen-activated protein kinases and/or the nuclear factor-kappa B. Carcinogenesis 28, 1224-1231. https://doi.org/10.1093/carcin/bgm005
  4. D'Ambrosio, E., Casa, B., Bompani, R., Scali, G. and Scali, M. (1981) Glucosamine sulphate: a controlled clinical investigation in arthrosis. Pharmatherapeutica 2, 504-508.
  5. De Young, L. M., Kheifets, J. B., Ballaron, S. J. and Young, J. M. (1989) Edema and cell infi ltration in the phorbol ester-treated mouse ear are temporally separate and can be differentially modulated by pharmacologic agents. Agents Actions 26, 335-341. https://doi.org/10.1007/BF01967298
  6. Eckert, R. L., Sturniolo, M. T., Broome, A. M., Ruse, M. and Rorke, E. A. (2005) Transglutaminase function in epidermis. J. Invest. Dermatol. 124, 481-492. https://doi.org/10.1111/j.0022-202X.2005.23627.x
  7. Hua, J., Sakamoto, K. and Nagaoka, I. (2002) Inhibitory actions of glucosamine, a therapeutic agent for osteoarthritis, on the functions of neutrophils. J. Leukoc. Biol. 71, 632-640.
  8. Jeong, K. C., Ahn, K. O., Lee, B. I., Lee, C. H. and Kim, S. Y. (2010) The mechanism of transglutaminase 2 inhibition with glucosamine: implications of a possible anti-infl ammatory effect through transglutaminase inhibition. J. Cancer Res. Clin. Oncol. 136, 143-150. https://doi.org/10.1007/s00432-009-0645-x
  9. Kim, C. H., Cheong, K. A., Park, C. D. and Lee, A. Y. (2011a) Glucosamine improved atopic dermatitis-like skin lesions in NC/Nga mice by inhibition of Th2 cell development. Scand. J. Immunol. 73, 536-545. https://doi.org/10.1111/j.1365-3083.2011.02526.x
  10. Kim, C. H., Cheong, K. A., Park, C. D. and Lee, A. Y. (2012) Therapeutic effects of combination using glucosamine plus tacrolimus (FK-506) on the development of atopic dermatitis-like skin lesions in NC/Nga mice. Scand. J. Immunol. 75, 471-478. https://doi.org/10.1111/j.1365-3083.2011.02659.x
  11. Kim, D. S., Kim, B., Tahk, H., Kim, D. H., Ahn, E. R., Choi, C., Jeon, Y., Park, S. Y., Lee, H., Oh, S. H. and Kim, S. Y. (2010) Transglutaminase 2 gene ablation protects against renal ischemic injury by blocking constant NF-${\kappa}B$ activation. Biochem. Biophys. Res. Commun. 403, 479-484. https://doi.org/10.1016/j.bbrc.2010.11.063
  12. Kim, D. S., Park, K. S., Jeong, K. C., Lee, B. I., Lee, C. H. and Kim, S. Y. (2009) Glucosamine is an effective chemo-sensitizer via transglutaminase 2 inhibition. Cancer Lett. 273, 243-249. https://doi.org/10.1016/j.canlet.2008.08.015
  13. Kim, J. C., Shin, J. Y., Shin, D. H., Kim, S. H., Park, S. H., Park, R. D., Park, S. C., Kim, Y. B. and Shin, Y. C. (2005) Synergistic antiinfl ammatory effects of pinitol and glucosamine in rats. Phytother. Res. 19, 1048-1051.
  14. Kim, M. H., Nugroho, A., Choi, J., Park, J. H. and Park, H. J. (2011b) Rhododendrin, an analgesic/anti-infl ammatory arylbutanoid glycoside, from the leaves of Rhododendron aureum. Arch. Pharm. Res. 34, 971-978. https://doi.org/10.1007/s12272-011-0614-1
  15. Largo, R., Alvarez-Soria, M. A., Díez-Ortego, I., Calvo, E., Sanchez- Pernaute, O., Egido, J. and Herrero-Beaumont, G. (2003) Glucosamine inhibits IL-1beta-induced NFkappaB activation in human osteoarthritic chondrocytes. Osteoarthritis Cartilage 11, 290-298. https://doi.org/10.1016/S1063-4584(03)00028-1
  16. Lee, C. H. and Kim, S. Y. (2009) NF-kappaB and therapeutic approach. Biomol. Ther. 17, 219-240. https://doi.org/10.4062/biomolther.2009.17.3.219
  17. Lee, J., Kim, Y. S., Choi, D. H., Bang, M. S., Han, T. R., Joh, T. H. and Kim, S. Y. (2004) Transglutaminase 2 induces nuclear factorkappaB activation via a novel pathway in BV-2 microglia. J. Biol. Chem. 279, 53725-53735. https://doi.org/10.1074/jbc.M407627200
  18. Lorand, L. and Graham, R. M. (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4, 140-156. https://doi.org/10.1038/nrm1014
  19. Mehta, K. (2005) Mammalian transglutaminases: a family portrait. Prog. Exp. Tumor Res. 38, 1-18. https://doi.org/10.1159/000084229
  20. Mehta, K., Kumar, A. and Kim, H. I. (2010) Transglutaminase 2: a multi-tasking protein in the complex circuitry of infl ammation and cancer. Biochem. Pharmacol. 80, 1921-1929. https://doi.org/10.1016/j.bcp.2010.06.029
  21. Mhaouty-Kodja, S. (2004) Ghalpha/tissue transglutaminase 2: an emerging G protein in signal transduction. Biol. Cell 96, 363-367. https://doi.org/10.1111/j.1768-322X.2004.tb01427.x
  22. Park, M. K. and Lee, C. H. (2011) Alpinia katsumadai suppresses migration and 12-O-tetradecanoylphorbol-13-acetate-induced invasion of HT-1080 cells through suppression of transglutaminase-2, matrix metalloproteinase-2, and matrix metalloproteinase-9 expression. Cancer Prevention Research 16, 326-332.
  23. Rafi , M. M., Yadav, P. N. and Rossi, A. O. (2007) Glucosamine inhibits LPS-induced COX-2 and iNOS expression in mouse macrophage cells (RAW 264.7) by inhibition of p38-MAP kinase and transcription factor NF-kappaB. Mol. Nutr. Food Res. 51, 587-593. https://doi.org/10.1002/mnfr.200600226
  24. Shikhman, A. R., Kuhn, K., Alaaeddine, N. and Lotz, M. (2001) N-acetylglucosamine prevents IL-1 beta-mediated activation of human chondrocytes. J. Immunol. 166, 5155-5160. https://doi.org/10.4049/jimmunol.166.8.5155
  25. Singh, S., Khajuria, A., Taneja, S. C., Khajuria, R. K., Singh, J. and Qazi, G. N. (2007) Boswellic acids and glucosamine show synergistic effect in preclinical anti-infl ammatory study in rats. Bioorg. Med. Chem. Lett. 17, 3706-3711. https://doi.org/10.1016/j.bmcl.2007.04.034
  26. 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 infl ammation in mice. Biochem. Pharmacol. 75, 1348-1357. https://doi.org/10.1016/j.bcp.2007.11.015
  27. Wangroongsub, Y., Tanavalee, A., Wilairatana, V. and Ngarmukos, S. (2010) Comparable clinical outcomes between glucosamine sulfate- potassium chloride and glucosamine sulfate sodium chloride in patients with mild and moderate knee osteoarthritis: a randomized, double-blind study. J. Med. Assoc. Thai. 93, 805-811.

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