Advertisement

Mushroom-Mediated Protection from Oxidative Damage to DNA

  • John A. Buswell
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

Oxidative damage to DNA caused by excess generation and accumulation of intracellular reactive oxygen species is widely associated with numerous ailments including cancer, diabetes and various age-related neuropathological conditions such as dementia, Alzheimers and Parkinson’s disease. This damage, and its amelioration, can be readily assessed in vivo and ex vivo with the comet assay, a simple and sensitive method for measuring strand breaks in the DNA of single cells. Use of this assay has revealed that several wild and cultivated mushroom species, including some that are widely consumed as natural dietary components, exhibit varying degrees of protection. These include Agaricus bisporus, A. blazei, Lentinula edodes, Ganoderma lucidum, Phellinus linteus, Inonotus obliquus, and Coriolus versicolor. In view of the huge mushroom resources available, further research focused on the genoprotective effects of this important group of fungi is likely to be particularly fruitful.

Keywords

Reactive oxygen species Oxidative damage to DNA Comet assay Mushroom Genoprotection Agaricus bisporus Ganoderma lucidum 

References

  1. Al-A’Adhmi MA, Al-Awadi BQ, Abass AAA (2013) White mushroom Agaricus bisporus extract inhibits oxidative DNA damage in human lymphocytes as assessed by comet assay. J Gen Environ Res Conserv 1:153–157Google Scholar
  2. Ames BN, Shigenaga MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 90:7915–7922CrossRefGoogle Scholar
  3. Apopa PL, He X, Ma Q (2008) Phosphorylation of Nrf2 in the transcription activation domain by casein kinase 2 (CK2) is critical for the nuclear translocation and transcription activation function of Nrf2 in IMR-32 neuroblastoma cells. J Biochem Mol Toxicol 22:63–76CrossRefGoogle Scholar
  4. Bonner WM, Redo CE, Dickey JS, Nakamura AJ, Sedilnikova OA, Solier S, Pommier Y (2008) γH2AX and cancer. Nat Rev Cancer 8:957–967CrossRefGoogle Scholar
  5. Cadet J, Wagner JR (2013) DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb Perspect Biol 5:a012559CrossRefGoogle Scholar
  6. Chang ST, Miles PG (1992) Mushroom biology: a new discipline. Mycologist 6:64–65CrossRefGoogle Scholar
  7. Chang ST, Wasser SP (2012) The role of culinary-medicinal mushrooms on human welfare with a pyramid model for human health. Int J Med Mushr 14:95–134CrossRefGoogle Scholar
  8. Guterres ZR, Mantovani MS, da Eira AF, Ribeiro LR, Jordão BQ (2005) Genotoxic and antigenotoxic effects of organic extracts of mushroom Agaricus blazei Murrill on V79 cells. Genet Mol Biol 28:458–463CrossRefGoogle Scholar
  9. Halliwell B, Gutteridge JMC (2000) Free radicals in biology and medicine. Oxford University Press, OxfordGoogle Scholar
  10. Han SK, Mytilineou C, Cohen G (1996) L-DOPA up-regulates glutathione and protects mesencephalic cultures against oxidative stress. J Neurochem 66:501–510CrossRefGoogle Scholar
  11. Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, Yamamoto M (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 275:16023–16029CrossRefGoogle Scholar
  12. Katori M, Anselmo DM, Busuttil RW, Kupiec-Weglinski JW (2002) A novel strategy against ischemia and reperfusion injury: cytoprotection with hemeoxygenase system. Transpl Immunol 9:227–233CrossRefGoogle Scholar
  13. Kehrer JP, Klotz L-O (2015) Free radicals and related reactive species as mediators of tissue injury and disease: implications for health. Crit Rev Toxicol 45:765–798CrossRefGoogle Scholar
  14. Kim KC, Kim IG (1999) Ganoderma lucidum extract protects DNA from strand breakage caused by hydroxyl radical and UV irradiation. Int J Mol Med 4:273–277PubMedGoogle Scholar
  15. Kim Y-H, Cho S-M, Hyun J-W, Ryoo I-J, Choo S-J, Lee S, Seok S-J, Hwang JS, Sohn ED, Yun B-S, Bae KH, Yoo I-D (2008) A new antioxidant, clitocybin A, from the culture broth of Clitocybe aurantiaca. J Antibiot 61:573–576CrossRefGoogle Scholar
  16. Kim E-K, Lee S-J, Hwang J-W, Kim CG, Choi DK, Lim BO, Kang H, Moon S-H, Jeon B-T, Park P-J (2011) In vitro investigation on antioxidative effect of Inonotus obliquus extracts against oxidative stress on PC12 cells. J Korean Soc Appl Biol Chem 54:112–117Google Scholar
  17. Kim MJ, Chu WM, Park EJ (2012) Antioxidant and antigenotoxic effects of Shiitake mushrooms affected by different drying methods. J Korean Soc Food Sci Nutr 41:1041–1048CrossRefGoogle Scholar
  18. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi, 10th edn. CABI, WallingfordGoogle Scholar
  19. Kobayashi M, Yamamoto M (2005) Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal 7:385–394CrossRefGoogle Scholar
  20. Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Vunduk J, Petrović P, Niksic M, Vrvic MM, van Griensven L (2015) Antioxidants of edible mushrooms. Molecules 20:19489–19525CrossRefGoogle Scholar
  21. Lee MY, Han J-H, Kang M-H (2016a) Protective effect of Korean diet food groups on lymphocyte DNA damage and contribution of each food group to total dietary antioxidant capacity (TDAC). J Nutr Health 49:277–287 (In Korean with English abstract)CrossRefGoogle Scholar
  22. Lee Y-H, Kim J-H, Song C-H, Jang K-J, Kim C-H, Kang J-S, Choi Y-H, Yoon H-M (2016b) Ethanol extract of Ganoderm alucidum augments cellular anti-oxidant defense through activation of Nrf2/HO-1. J Pharmacopuncture 19:59–69CrossRefGoogle Scholar
  23. Menoli RCRN, Mantovani MS, Ribeiro LR, Speit G, Jordão BQ (2001) Antimutagenic effects of the mushroom Agaricus blazei Murrill extracts on V79 cells. Mutat Res 496:5–13CrossRefGoogle Scholar
  24. Motterlini R, Foresti R (2014) Heme oxygenase-1 as a target for drug discovery. Antioxid Redox Signal 20:1810–1826CrossRefGoogle Scholar
  25. Mytilineou C, Han SK, Cohen G (1993) Toxic and protective effects of L-DOPA on mesencephalic cell cultures. J Neurochem 61:1470–1478CrossRefGoogle Scholar
  26. Ostling O, Johanson KJ (1984) Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophys Res Commun 123:291–298CrossRefGoogle Scholar
  27. Park E, Jeon K-I, Byun B-H (2005) Ethanol extract of Inonotus obliquus shows antigenotoxic effect on hydrogen peroxide induced DNA damage in human lymphocytes. Cancer Prev Res 10:54–59Google Scholar
  28. Park BJ, Lim YS, Lee HJ, Eum WS, Park J, Han KH, Choi SY, Lee KS (2009) Anti-oxidative effects of Phellinus linteus and red ginseng extracts on oxidative stress-induced DNA damage. BMB Rep 42:500–505CrossRefGoogle Scholar
  29. Pi J, Bai Y, Reece JM, Williams J, Liu D, Freeman ML, Fahl WE, Shugar D, Liu J, Qu W, Collins S, Waalkes MP (2007) Molecular mechanism of human Nrf2 activation and degradation: role of sequential phosphorylation by protein kinase CK2. Free Radic Biol Med 42:1797–1806CrossRefGoogle Scholar
  30. Ray PD, Huang B-W, Tsuji Y (2012) Reactive Oxygen Species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–990CrossRefGoogle Scholar
  31. Ruiz-Rodriguez A, Santoyo S, Soler-Rivas C (2009) Antioxidant properties of edible mushrooms. Funct Plant Sci Biotechnol 3:92–102Google Scholar
  32. Sanchez C (2017) Reactive oxygen species and antioxidant properties from mushrooms. Syn Sys Biotechnol 2:13–22CrossRefGoogle Scholar
  33. Scapagnini G, Butterfield DA, Colombrita C, Sultana R, Pascale A, Calabrese V (2004) Ethyl ferulate, a lipophilic polyphenol, induces HO-1 and protects rat neurons against oxidative stress. Antioxid Redox Signal 6:811–818PubMedGoogle Scholar
  34. Shi MM, Iwamoto T, Forman HJ (1994) γ-Glutamyl cysteine synthetase and GSH increase in quinone-induced oxidative stress in BPAEC. Amer J Physiol 267:414–421Google Scholar
  35. Shi YL, James AE, Benzie IFF, Buswell JA (2001) Prevention of oxidative damage to cellular DNA by mushroom-derived components. Int J Med Mushrooms 3:100CrossRefGoogle Scholar
  36. Shi Y-L, Benzie IFF, Buswell JA (2002a) L-DOPA oxidation products prevent H2O2-induced oxidative damage to cellular DNA. Life Sci 71:3047–3057CrossRefGoogle Scholar
  37. Shi Y-L, Benzie IFF, Buswell JA (2002b) Role of tyrosinase in the genoprotective effect of the edible mushroom, Agaricus bisporus. Life Sci 70:1595–1608CrossRefGoogle Scholar
  38. Shi YL, James AE, Benzie IFF, Buswell JA (2002c) Mushroom-derived preparations in the prevention of H2O2-induced oxidative damage to cellular DNA. Teratog Carcinog Mutagen 22:103–111CrossRefGoogle Scholar
  39. Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191CrossRefGoogle Scholar
  40. Stajić M, Vukojević J, Knežević A, Laušević SD, Milovanović I (2013) Antioxidant protective effects of mushroom metabolites. Curr Top Med Chem 13:2660–2676CrossRefGoogle Scholar
  41. Szeto YT, Collins AR, Benzie IFF (2002) Effects of dietary antioxidants on DNA damage in lysed cells using a modified comet assay procedure. Mutat Res 500:31–38CrossRefGoogle Scholar
  42. Szeto YT, Lau PC, Kalle W, Pak SC (2013) Direct human DNA protection by Coriolus versicolor (Yunzhi) extract. Pharm Biol 51:851–855CrossRefGoogle Scholar
  43. Wang LH, Tsai SJ, Lin SY (2004) Aqueous extract from Taiwanese Agrocybe cylindracea strain B protects DNA against •OH-mediated strand breaks. J Food Drug Anal 12:277–285Google Scholar
  44. Wong VWC, Szeto YT, Collins AR, Benzie IF (2005) The comet assay: a biomonitoring tool for nutraceutical research. Curr Top Nutraceutical Res 3:1–14Google Scholar
  45. Živkoviƈ L, Borozan S, Čabarkapa A, Topaloviƈ D, Ciptasari U, Bajiƈ V, Spremo-Potpareviƈ B (2017) Antigenotoxic properties of Agaricus blazei against hydrogen peroxide in human peripheral blood cells. Oxidative Med Cell Longev 2017:1–9.  https://doi.org/10.1155/2017/8759764CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • John A. Buswell
    • 1
  1. 1.Institute of Edible FungiShanghai Academy of Agricultural SciencesShanghaiChina

Personalised recommendations