Advertisement

Cytotechnology

, Volume 70, Issue 3, pp 1001–1008 | Cite as

Mushroom extract inhibits ultraviolet B-induced cellular senescence in human keratinocytes

  • Zhao Chong
  • Haruka Matsuo
  • Mai Kuroda
  • Shuntaro Yamashita
  • Gopal Prasad Parajuli
  • Hira Kaji Manandhar
  • Kuniyoshi Shimizu
  • Yoshinori Katakura
Short Communication

Abstract

Mushrooms possess various bioactivities and are used as nutritional supplements and medicinal products. Twenty-nine bioactive components have been extracted recently from mushrooms grown in Nepal. In this study, we evaluated the ability of these mushroom extracts to augment SIRT1, a mammalian SIR2 homologue localized in cytosol and nuclei. We established a system for screening food ingredients that augment the SIRT1 promoter in HaCaT cells, and identified a SIRT1-augmenting mushroom extract (number 28, Trametes versicolor). UVB irradiation induced cellular senescence in HaCaT cells, as evidenced by increased activity and expression of cellular senescence markers including senescence-associated β-galactosidase, p21, p16, phosphorylated p38, and γH2AX. Results clearly showed that the mushroom extract (No. 28) suppressed the ultraviolet B irradiation-induced cellular senescence in HaCaT cells possibly through augmenting SIRT1 expression.

Keywords

SIRT1 Mushroom Cellular senescence Keratinocytes Skin Ultraviolet B 

Notes

Acknowledgements

The authors like to thank Dr. K. Fukami (Kyushu Univ.) and T. H. Bang (Kyushu Univ.) for their assistance.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10616_2018_229_MOESM1_ESM.pdf (38 kb)
Supplementary material 1 (PDF 38 kb)

References

  1. Adhikari MK, Devkota S, Tiwari RD (2006) Ethnomycolgical knowledge on uses of wild mushrooms in western and central Nepal. Our Nat 3:13–19.  https://doi.org/10.3126/on.v3i1.329 Google Scholar
  2. Ahmed NU, Ueda M, Ichihashi M (1999) Induced expression of p16 and p21 proteins in UVB-irradiated human epidermis and cultured keratinocytes. J Dermatol Sci 19:175–181CrossRefGoogle Scholar
  3. Ajith TA, Janardhanan KK (2007) Indian medicinal mushrooms as a source of antioxidant and antitumor agents. J Clin Biochem Nutr 40:157–162.  https://doi.org/10.3164/jcbn.40.157 CrossRefGoogle Scholar
  4. Barros L, Cruz T, Baptista P et al (2008) Wild and commercial mushrooms as source of nutrients and nutraceuticals. Food Chem Toxicol 46:2742–2747.  https://doi.org/10.1016/j.fct.2008.04.030 CrossRefGoogle Scholar
  5. Calvo MS, Babu US, Garthoff LH et al (2013) Vitamin D2 from light-exposed edible mushrooms is safe, bioavailable and effectively supports bone growth in rats. Osteoporos Int 24:197–207.  https://doi.org/10.1007/s00198-012-1934-9 CrossRefGoogle Scholar
  6. Cao C, Lu S, Kivlin R et al (2009) SIRT1 confers protection against UVB- and H2O2-induced cell death via modulation of p53 and JNK in cultured skin keratinocytes. J Cell Mol Med 13:3632–3643.  https://doi.org/10.1111/j.1582-4934.2008.00453.x CrossRefGoogle Scholar
  7. Chen C-H, Kang L, Lo H-C et al (2015) Polysaccharides of Trametes versicolor improve bone properties in diabetic rats. J Agric Food Chem 63:9232–9238.  https://doi.org/10.1021/acs.jafc.5b02668 CrossRefGoogle Scholar
  8. Chung KW, Choi YJ, Park MH et al (2015) Molecular insights into SIRT1 protection against UVB-induced skin fibroblast senescence by suppression of oxidative stress and p53 acetylation. J Gerontol A Biol Sci Med Sci 70:959–968.  https://doi.org/10.1093/gerona/glu137 CrossRefGoogle Scholar
  9. Frye RA (2000) Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun 273:793–798.  https://doi.org/10.1006/bbrc.2000.3000 CrossRefGoogle Scholar
  10. Hai Bang T, Suhara H, Doi K et al (2014) Wild mushrooms in Nepal: some potential candidates as antioxidant and ACE-inhibition sources. Evid Based Complement Altern Med 2014:195305–195311.  https://doi.org/10.1155/2014/195305 CrossRefGoogle Scholar
  11. Harada G, Pattarawat P, Ito K et al (2016) Lactobacillus brevis T2102 suppresses the growth of colorectal cancer cells by activating SIRT1. J Funct Foods 23:444–452.  https://doi.org/10.1016/j.jff.2016.01.016 CrossRefGoogle Scholar
  12. Hattori Y, Nishigori C, Tanaka T et al (1996) 8-hydroxy-2′-deoxyguanosine is increased in epidermal cells of hairless mice after chronic ultraviolet B exposure. J Invest Dermatol 107:733–737CrossRefGoogle Scholar
  13. Huang J, Gan Q, Han L et al (2008) SIRT1 overexpression antagonizes cellular senescence with activated ERK/S6k1 signaling in human diploid fibroblasts. PLoS ONE 3:e1710.  https://doi.org/10.1371/journal.pone.0001710 CrossRefGoogle Scholar
  14. Jhan M-H, Yeh C-H, Tsai C-C et al (2016) Enhancing the antioxidant ability of Trametes versicolor polysaccharopeptides by an enzymatic hydrolysis process. Molecules 21:1215.  https://doi.org/10.3390/molecules21091215 CrossRefGoogle Scholar
  15. Kaeberlein M, McVey M, Guarente L (1999) The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev 13:2570–2580CrossRefGoogle Scholar
  16. Kalaras MD, Beelman RB, Elias RJ (2012) Effects of postharvest pulsed UV light treatment of white button mushrooms (Agaricus bisporus) on vitamin D2 content and quality attributes. J Agric Food Chem 60:220–225.  https://doi.org/10.1021/jf203825e CrossRefGoogle Scholar
  17. Kim M, Park KY, Lee M-K et al (2016) Adiponectin suppresses UVB-induced premature senescence and hBD2 overexpression in human keratinocytes. PLoS ONE 11:e0161247.  https://doi.org/10.1371/journal.pone.0161247 CrossRefGoogle Scholar
  18. Kowalczewska M, Piotrowski J, Jędrzejewski T, Kozak W (2016) Polysaccharide peptides from Coriolus versicolor exert differential immunomodulatory effects on blood lymphocytes and breast cancer cell line MCF-7 in vitro. Immunol Lett 174:37–44.  https://doi.org/10.1016/j.imlet.2016.04.010 CrossRefGoogle Scholar
  19. Lavker RM, Gerberick GF, Veres D et al (1995) Cumulative effects from repeated exposures to suberythemal doses of UVB and UVA in human skin. J Am Acad Dermatol 32:53–62CrossRefGoogle Scholar
  20. Lavu S, Boss O, Elliott PJ, Lambert PD (2008) Sirtuins–novel therapeutic targets to treat age-associated diseases. Nat Rev Drug Discov 7:841–853.  https://doi.org/10.1038/nrd2665 CrossRefGoogle Scholar
  21. Li L, Ng TB, Song M et al (2007) A polysaccharide-peptide complex from abalone mushroom (Pleurotus abalonus) fruiting bodies increases activities and gene expression of antioxidant enzymes and reduces lipid peroxidation in senescence-accelerated mice. Appl Microbiol Biotechnol 75:863–869.  https://doi.org/10.1007/s00253-007-0865-4 CrossRefGoogle Scholar
  22. Li H, Li Z, Peng L et al (2017) Lycium barbarum polysaccharide protects human keratinocytes against UVB-induced photo-damage. Free Radic Res 51:200–210.  https://doi.org/10.1080/10715762.2017.1294755 CrossRefGoogle Scholar
  23. Lindequist U, Niedermeyer THJ, Jülich W-D (2005) The pharmacological potential of mushrooms. Evid Based Complement Altern Med 2:285–299.  https://doi.org/10.1093/ecam/neh107 CrossRefGoogle Scholar
  24. Oh MC, Piao MJ, Fernando PMDJ et al (2016) Baicalein protects human skin cells against ultraviolet B-induced oxidative stress. Biomol Ther (Seoul) 24:616–622.  https://doi.org/10.4062/biomolther.2016.022 CrossRefGoogle Scholar
  25. Pillai S, Oresajo C, Hayward J (2005) Ultraviolet radiation and skin aging: roles of reactive oxygen species, inflammation and protease activation, and strategies for prevention of inflammation-induced matrix degradation—a review. Int J Cosmet Sci 27:17–34.  https://doi.org/10.1111/j.1467-2494.2004.00241.x CrossRefGoogle Scholar
  26. Tamrakar S, Tran HB, Nishida M et al (2016) Antioxidative activities of 62 wild mushrooms from Nepal and the phenolic profile of some selected species. J Nat Med 70:769–779.  https://doi.org/10.1007/s11418-016-1013-1 CrossRefGoogle Scholar
  27. Udono M, Kadooka K, Yamashita S, Katakura Y (2012) Quantitative analysis of cellular senescence phenotypes using an imaging cytometer. Methods 56:383–388.  https://doi.org/10.1016/j.ymeth.2012.02.012 CrossRefGoogle Scholar
  28. Wasser SP (2002) Review of medicinal mushrooms advances: Good news from old allies. HerbalGram 56:28–33Google Scholar
  29. Yamashita S, Ogawa K, Ikei T et al (2012) SIRT1 prevents replicative senescence of normal human umbilical cord fibroblast through potentiating the transcription of human telomerase reverse transcriptase gene. Biochem Biophys Res Commun 417:630–634.  https://doi.org/10.1016/j.bbrc.2011.12.021 CrossRefGoogle Scholar
  30. Yuan X-Y, Pang X-W, Zhang G-Q, Guo J-Y (2017) Salidroside’s protection against UVB-mediated oxidative damage and apoptosis is associated with the upregulation of Nrf2 expression. Photomed Laser Surg 35:49–56.  https://doi.org/10.1089/pho.2016.4151 CrossRefGoogle Scholar
  31. Zhao C, Sakaguchi T, Fujita K et al (2016) Pomegranate-derived polyphenols reduce reactive oxygen species production via SIRT3-mediated SOD2 activation. Oxid Med Cell Longev 2016:2927131–2927139.  https://doi.org/10.1155/2016/2927131 Google Scholar
  32. Zheng J, Hewage SRKM, Piao MJ et al (2016) Photoprotective effect of carpomitra costata extract against ultraviolet B-induced oxidative damage in human keratinocytes. J Environ Pathol Toxicol Oncol 35:11–28.  https://doi.org/10.1615/JEnvironPatholToxicolOncol.2016014003 CrossRefGoogle Scholar
  33. Zhu X, Li N, Wang Y et al (2017) Protective effects of quercetin on UVB irradiation-induced cytotoxicity through ROS clearance in keratinocyte cells. Oncol Rep 37:209–218.  https://doi.org/10.3892/or.2016.5217 CrossRefGoogle Scholar
  34. Zu Y, Liu L, Lee MYK et al (2010) SIRT1 promotes proliferation and prevents senescence through targeting LKB1 in primary porcine aortic endothelial cells. Circ Res 106:1384–1393.  https://doi.org/10.1161/CIRCRESAHA.109.215483 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Graduate School of Systems Life SciencesKyushu UniversityFukuokaJapan
  2. 2.Plant Pathology DivisionNepal Agriculture Research Council, Khumaltar, Lalitpur, NepalKathmanduNepal
  3. 3.Faculty of AgricultureKyushu UniversityFukuokaJapan

Personalised recommendations