Inonotus obliquus protects against oxidative stress-induced apoptosis and premature senescence

Abstract

In this study, we investigated the cytoprotective effects of Inonotus obliquus against oxidative stress-induced apoptosis and premature senescence. Pretreatment with I. obliquus scavenged intracellular ROS and prevented lipid peroxidation in hydrogen peroxide-treated human fibroblasts. As a result, I. obliquus exerted protective effects against hydrogen peroxide-induced apoptosis and premature senescence in human fibroblasts. In addition, I. obliquus suppressed UV-induced morphologic skin changes, such as skin thickening and wrinkle formation, in hairless mice in vivo and increased collagen synthesis through inhibition of MMP-1 and MMP-9 activities in hydrogen peroxide-treated human fibroblasts. Taken together, these results demonstrate that I. obliquus can prevent the aging process by attenuating oxidative stress in a model of stress-induced premature senescence.

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References

  1. Brenneisen, P., Briviba, K., Wlaschek, M., Wenk, J., and Scharffetter-Kochanek, K. (1997). Hydrogen peroxide (H2O2) increases the steady-state mRNA levels of collagenase/MMP-1 in human dermal fibroblasts. Free Radic. Biol. Med. 22, 515–524.

    PubMed  Article  CAS  Google Scholar 

  2. Chen, Q.M. (2000). Replicative senescence and oxidant-induced premature senescence. Beyond the control of cell cycle checkpoints. Ann. N Y Acad. Sci. 908, 111–125.

    PubMed  Article  CAS  Google Scholar 

  3. Cohen, G.M. (1997). Caspases: the executioners of apoptosis. Biochem. J. 326, 1–16.

    PubMed  CAS  Google Scholar 

  4. Dasari, A., Bartholomew, J.N., Volonte, D., and Galbiati, F. (2006). Oxidative stress induces premature senescence by stimulating caveolin-1 gene transcription through p38 mitogen-activated protein kinase/Sp1-mediated activation of two GC-rich promoter elements. Cancer Res. 66, 10805–10814.

    PubMed  Article  CAS  Google Scholar 

  5. Dimri, G.P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E.E., Linskens, M., Rubelj, I., Pereira-Smith, O., et al. (1995). A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92, 9363–9367.

    PubMed  Article  CAS  Google Scholar 

  6. Diplock, A.T., Charleux, J.L., Crfozier-Willi, G., Kok, F.J., Rice-Evans, C., Roberfroid, M., Stahl, W., and Vina-Ribes, J. (1998). Functional food science and defence against reactive oxidative species. Br. J. Nutr. 80, 77–112.

    Article  Google Scholar 

  7. Frippiat, C., Chen, Q.M., Zdanov, S., Magalhaes, J.P., Remacle, J., and Toussaint, O. (2001). Subcytotoxic H2O2 stress triggers a release of transforming growth factor-β1, which induces biomarkers of cellular senescence of human diploid fibroblasts. J. Biol. Chem. 276, 2531–2537.

    PubMed  Article  CAS  Google Scholar 

  8. Gibbs, D.F., Warner, R.L., Weiss, S.J., Johnson, K.J., and Varani, J. (1999). Characterization of matrix metalloproteinases produced by rat alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 20, 1136–1144.

    PubMed  CAS  Google Scholar 

  9. Harman, D. (1956). Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298–300.

    PubMed  CAS  Google Scholar 

  10. Hayflick, L., and Moorhead, P.S. (1961). The serial cultivation of human diploid cell strains. Exp. Cell Res. 25, 585–621.

    Article  Google Scholar 

  11. Ibbotson, S.H., Moran, M.N., Nash, J.F., and Kochevar, I.E. (1999). The effects of radicals compared with UVB as initiating species for the induction of chronic cutaneous photodamage. J. Invest. Dermatol. 112, 933–938.

    PubMed  Article  CAS  Google Scholar 

  12. Jang, J.S., Lee, J.S., Lee, J.H., Kwon, D.S., Lee, K.E., Lee, S.Y., and Hong, E.K. (2010). Hispidin produced from Phellinus linteus protects pancreatic β-cells from damage by hydrogen peroxide. Arch. Pharm. Res. 33, 853–861.

    PubMed  Article  CAS  Google Scholar 

  13. Jeong, J.B., Park, J.H., Lee, H.K., Ju, S.Y., Hong, S.C., Lee, J.R., Chung, G.Y., Lim, J.H., and Jeong, H.J. (2009). Protective effect of the extracts from Cnidium officinale against oxidative damage induced by hydrogen peroxide via antioxidant effect. Food Chem. Toxicol. 47, 525–529.

    PubMed  Article  CAS  Google Scholar 

  14. Kim, Y.O., Park, H.W., Kim, J.H., Lee, J.Y., Moon, S.H., and Shin, C.S. (2006). Anti-cancer effect and structural characterization of endo-polysaccharide from cultivated mycelia of Inonotus obliquus. Life Sci. 79, 72–80.

    PubMed  Article  CAS  Google Scholar 

  15. Kim, H.G., Yoon, D.H., Kim, C.H., Shrestha, B., Chang, W.C., Lim, S.Y., Lee, W.H., Han, S.G., Lee, J.O., Lim, M.H., et al. (2007). Ethanol extract of Inonotus obliquus inhibits lipopolysaccharideinduced inflammation in RAW 264.7 macrophage cells. J. Med. Food 10, 80–89.

    PubMed  Article  CAS  Google Scholar 

  16. Lee, J.S., and Hong, E.K. (2010). Hericium erinaceus enhances doxorubicin-induced apoptosis in human hepatocellular carcinoma cells. Cancer Lett. 297, 144–154.

    PubMed  Article  CAS  Google Scholar 

  17. Lee, I.K., Kim, Y.S., Jang, Y.W., Jung, J.Y., and Yun, B.S. (2007). New antioxidant polyphenols from the medicinal mushroom Inonotus obliquus. Bioorg. Med. Chem. Lett. 17, 6678–6681.

    PubMed  Article  CAS  Google Scholar 

  18. Lee, J.S., Cho, J.Y., and Hong, E.K. (2009). Study on macrophage activation and structural characteristics of purified polysaccharides from the liquid culture broth of Hericium erinaceus. Carbohydr. Polym. 78, 162–168.

    Article  CAS  Google Scholar 

  19. Nakajima, Y., Nishida, H., Nakamura, Y., and Konishi, T. (2009). Prevention of hydrogen peroxide-induced oxidative stress in PC12 cells by 3,4-dihydroxybenzalacetone isolated from Chaga (Inonotus obliquus (persoon) Pilat). Free Radic. Biol. Med. 47, 1154–1161.

    PubMed  Article  CAS  Google Scholar 

  20. Nobel, C.I., Kimland, M., Lind, B., Orrenius, S., and Slater, A.F. (1995). Dithiocarbamates induce apoptosis in thymocytes by raising the intracellular level of redox active copper. J. Biol. Chem. 270, 26202–26208.

    PubMed  Article  CAS  Google Scholar 

  21. Ohshima, S. (2004). Apoptosis in stress-induced and spontaneously senescent human fibroblasts. Biochem. Biophys. Res. Commun. 324, 241–246.

    PubMed  Article  CAS  Google Scholar 

  22. Park, Y.K., Lee, H.B., Jeon, E.J., Jung, H.S., and Kang, M.H. (2004). Chaga mushroom extract inhibits oxidative DNA damage in human lymphocytes as assessed by comet assay. BioFactors 21, 109–112.

    PubMed  Article  CAS  Google Scholar 

  23. Rhee, S.G. (2006). Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882–1883.

    PubMed  Article  Google Scholar 

  24. Saito, M., Sakagami, H., and Fujisawa, S. (2003). Cytotoxicity and apoptosis induction by butylated hydroxyanisole (BHA) and butylated hydroxytoluene (BHT). Anticancer Res. 23, 4693–4701.

    PubMed  CAS  Google Scholar 

  25. Saraste, A., and Pulkki, K. (2000). Morphologic and biochemical hallmarks of apoptosis. Cardiovasc. Res. 45, 528–537.

    PubMed  Article  CAS  Google Scholar 

  26. Scharffetter-Kochanek, K., Wlaschek, M., Brenneisen, P., Schauen, M., Blaudschun, R., and Wenk, J. (1997). UV-induced reactive oxygen species in photocarcinogenesis and photoaging. Biol. Chem. 378, 1247–1257.

    PubMed  CAS  Google Scholar 

  27. Schindowski, K., Leutner, S., Kressmann, S., Eckert, A., and Muller, W.E. (2001). Age-related increase of oxidative stress-induced apoptosis in mice prevention by Ginkgo biloba extract (EGb761). J. Neural Transm. 108, 969–978.

    PubMed  Article  CAS  Google Scholar 

  28. Scorrano, L. (2009). Opening the doors to cytochrome c: changes in mitochondrial shape and apoptosis. Int. J. Biochem. Cell Biol. 41, 1875–1883.

    PubMed  Article  CAS  Google Scholar 

  29. Serrano, M., and Blasco, M.A. (2001). Putting the stress on senescence. Curr. Opin. Cell Biol. 13, 748–753.

    PubMed  Article  CAS  Google Scholar 

  30. Touissant, O., Dumont, P., Dierick, J.F., Pascal, T., Frippiat, C., Chainiaux, F., Sluse, F., Eliaers, F., and Remacle, J. (2000). Stress-induced premature senescence. Ann. N Y Acad. Sci. 908, 85–98.

    Article  Google Scholar 

  31. Yu, J.Y., Kim, J.H., Kim, T.G., Kim, B.T., Jang, Y.S., and Lee, J.C. (2010) (E)-1-(3,4-dihydroxyphenethyl)-3-styrylurea inhibits proliferation of MCF-7 cells through G1 cell cycle arrest and mitochondria-mediated apoptosis. Mol. Cells 30, 303–310.

    PubMed  Article  CAS  Google Scholar 

  32. Yuan, J., Murrell, G.A., Trickett, A., and Wang, M.X. (2003). Involvement of cytochrome c release and caspase-3 activation in the oxidative stress-induced apoptosis in human tendon fibroblasts. Biochim. Biophys. Acta 1641, 35–41.

    PubMed  Article  CAS  Google Scholar 

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Correspondence to Eock Kee Hong.

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Yun, J.S., Pahk, J.W., Lee, J.S. et al. Inonotus obliquus protects against oxidative stress-induced apoptosis and premature senescence. Mol Cells 31, 423–429 (2011). https://doi.org/10.1007/s10059-011-0256-7

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Keywords

  • antioxidant
  • apoptosis
  • Inonotus obliquus
  • reactive oxygen species (ROS) stress-induced premature senescence