Glutathione biosynthesis via activation of the nuclear factor E2-related factor 2 (Nrf2) - Antioxidant-response element (ARE) pathway is essential for neuroprotective effects of sulforaphane and 6-(methylsulfinyl) hexyl isothiocyanate

Journal of Pharmacological Sciences

Volumn 115, Issue 3, 2011, Pages 320-328

  Mizuno, Keita ^a   Kume, Toshiaki ^a   Muto, Chie ^a   Takada Takatori, Yuki ^b   Izumi, Yasuhiko ^a   Sugimoto, Hachiro ^a   Akaike, Akinori ^a  

^a KYOTO UNIVERSITY   (Japan)

^b DOSHISHA WOMEN'S COLLEGE OF LIBERAL ARTS   (Japan)

Author keywords

Isothiocyanate; Neuroprotection; Nuclear factor E2 related factor 2 (Nrf2); Oxidative stress

Indexed keywords

6 (METHYLSULFINYL)HEXYL ISOTHIOCYANATE; ACETYLCYSTEINE; BUTHIONINE SULFOXIMINE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; HEME OXYGENASE 1; HYDROGEN PEROXIDE; ISOTHIOCYANIC ACID DERIVATIVE; PARAQUAT; PROTOPORPHYRIN ZINC; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL NUCLEUS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORPUS STRIATUM; CYTOTOXICITY; DRUG EFFECT; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PEPTIDE SYNTHESIS; PROTEIN TRANSPORT; RAT;

EID: 79952792525     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.10257FP     Document Type: Article

References (36)

1. Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature. 2006;443:787-795. (Pubitemid 44622683)
2. Droge W, Schipper HM. Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell. 2007;6:361-370. (Pubitemid 46785141)
3. Blomgren K, Hagberg H. Free radicals, mitochondria and hypoxia-ischemia in the developing brain. Free Radic Biol Med. 2006;40:388-397. (Pubitemid 43139674)
4. Trushina E, Mcmurray CT. Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases. Neuroscience. 2007;145:1233-1248. (Pubitemid 46602738)
5. MyzaK MC, Dashwood RH. Chemoprotection by sulforaphane: keep one eye beyond Keap1. Cancer Lett. 2006;233:208-218. (Pubitemid 43327375)
6. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999;13:76-86. (Pubitemid 29045117)
7. Zhang Y, Talalay P, Cho CG, Posner GH. A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc Natl Acad Sci U S A. 1992;89:2399-2403.
8. Morimitsu Y, Nakagawa Y, Hayashi K, Fujii H, Kumagai T, Nakagawa Y, et al. A sulforaphane analogue that potently activates the Nrf2-dependent detoxification pathway. J Biol Chem. 2002;277:3456-3463. (Pubitemid 34953214)
9. Matton MP, Cheng A. Neurohormetic phytochemicals: Low-dose toxins that induce adaptive neuronal stress responses. Trends Neurosci. 2006;29:632-639. (Pubitemid 44602260)
10. Misiewicz I, Skupinska K, Kowalska E, Lubinski J, Kasuprzycka GT. Sulforaphane-mediated induction of a phase 2 detoxifying enzyme NAD(P)H:quinone reductase and apoptosis in human lymphoblastoid cells. Acta Biochim Pol. 2004;51:711-721. (Pubitemid 39296925)
11. Gao X, Dinkova-kostova AT, Talalay P. Powerful and prolonged protection of human retinal pigment epithelial cells, keratinocytes, and mouse leukemia cells against oxidative damage: the indirect antioxidant effects of sulforaphane. Proc Natl Acad Sci U S A. 2001;98:15221-15226. (Pubitemid 34013995)
12. Nomura T, Shinoda S, Yamori T, Sawaki S, Nagata I, Ryoyama K, et al. Selective sensitivity to wasabi-derived 6-(methylsulfinyl) hexyl isothiocyanate of human breast cancer and melanoma cell lines studied in vitro. Cancer Detect Prev. 2005;29:155-160.
13. Kraft AD, Johnson DA, Johnson JA. Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. J Neurosci. 2004;24:1101-1112. (Pubitemid 38177017)
14. Zhao J, Kobori N, Aronowski J, Dash PK. Sulforaphane reduces infarct volume following focal cerebral ischemia in rodents. Neurosci Lett. 2006;393:108-112. (Pubitemid 41821089)
15. Zhao X, Sun G, Zhang J, Strong R, Dash PK, Kan YW, et al. Transcription factor Nrf2 protects the brain from damage produced by intracerebral hemorrhage. Stroke. 2007;38:3280-3286. (Pubitemid 350175749)
16. Osakada F, Hashino A, Kume T, Katsuki H, Kaneko S, Akaike A. Alpha-tocotrienol provides the most potent neuroprotection among vitamin E analogs on cultured striatal neurons. Neuropharmacology. 2004;47:904-915. (Pubitemid 39440984)
17. Yamamoto N, Sawada H, Izumi Y, Kume T, Katsuki H, Shimohama S, et al. Proteasome inhibition induces glutathione synthesis and protects cells from oxidative stress: relevance to Parkinson disease. J Biol Chem. 2007;282:4364-4372. (Pubitemid 47101000)
18. Day BJ, Shawen S, Liochev SI, Crapo JD. A metalloporphyrin superoxide dismutasemimetic protects against paraquat-induced endothelial cell injury, in vitro. J Pharmacol Exp Ther. 1995;275:1227-1232. (Pubitemid 26130633)
19. Cocheme HM, Murphy MP. Complex I is the major site of mitochondrial superoxide production by paraquat. J Biol Chem. 2008;283:1786-1798.
20. Shinkai Y, Sumi D, Fukami I, Ishii T, Kumagai Y. Sulforaphane, an activator of Nrf2, suppresses cellular accumulation of arsenic and its cytotoxicity in primary mouse hepatocytes. FEBS Lett. 2006;580:1771-1774.
21. Xu C, Yuan X, Pan Z, Shen G, Kim JH, Yu S, et al. Mechanism of action of isothiocyanates: the induction of ARE-regulated genes is associated with activation of ERK and JNK and the phosphorylation and nuclear translocation of Nrf2. Mol Cancer Ther. 2006;5:1918-1926. (Pubitemid 44336562)
22. Dringen R. Metabolism and functions of glutathione in brain. Prog Neurobiol. 2000;62:649-671. (Pubitemid 30407139)
23. Aoyama K, Watabe M, Nakaki T. Regulation of neuronal glutathione synthesis. J Pharmacol Sci. 2008;108:227-238.
24. Morse D, Choi AM. Heme oxygenase-1: the "emerging molecule" has arrived. Am J Respir Cell Mol Biol. 2002;27:8-16.
25. Li HY, Zhong YF, Wu SY, Shi N. NF-E2 related factor 2 activation and heme oxygenase-1 induction by tert-butylhydroquinone protect against deltamethrin-mediated oxidative stress in PC12 cells. Chem Res Toxicol. 2007;20:1242-1251. (Pubitemid 47548292)
26. Farrera JA, Jauma A, Ribo JM, Peire MA, Parellada PP, Roques-Choua S, et al. The antioxidant role of bile pigments evaluated by chemical tests. Bioorg Med Chem. 1994;2:181-185.
27. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, et al. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci U S A. 1999;96:2445-2450. (Pubitemid 29117935)
28. Fimognari C, Hrelia P. Sulforaphane as a promising molecule for fighting cancer. Mutat Res. 2007;635:90-104. (Pubitemid 46756397)
29. Pham NA, Jacobberger JW, Schimmer AD, Cao P, Gronda M, Hedley DW. The dietary isothiocyanate sulforaphane targets pathways of apoptosis, cell cycle arrest, and oxidative stress in human pancreatic cancer cells and inhibits tumor growth in severe combined immunodeficient mice. Mol Cancer Ther. 2004;3:1239-1248. (Pubitemid 39440169)
30. Singh SV, Srivastava SK, Choi S, Lew KL, Antosiewicz J, Xiao D, et al. Sulforaphane-induced cell death in human prostate cancer cells is initiated by reactive oxygen species. J Biol Chem. 2005;280:19911-19924. (Pubitemid 41379520)
31. Numazawa S, Yoshida T. Nrf2-dependent gene expressions: a molecular toxicological aspect. J Toxicol Sci. 2004;29:81-89. (Pubitemid 38855920)
32. Zhang DD, Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol. 2003;23:8137-8151. (Pubitemid 37377505)
33. Yu R, Lei W, Mandlekar S, Weber MJ, Der CJ, Wu J, et al. Role of a mitogen-activated protein kinase pathway in the induction of phase II detoxifying enzymes by chemicals. J Biol Chem. 1999;274:27545-27552.
34. Schipper HM. Heme oxygenase expression in human central nervous system disorders. Free Radic Biol Med. 2004;37:1995-2011. (Pubitemid 39491319)
35. Moon MK, Choi BM, Oh GS, Pae HO, Kim JD, Oh H, et al. Catalposide protects Neuro 2A cells from hydrogen peroxide-induced cytotoxicity via the expression of heme oxygenase-1. Toxicol Lett. 2003;145:46-54. (Pubitemid 38366128)
36. Hon DX, Fukuda M, Fujii M, Fuke Y. Transcriptional regulation of nicotinamide adenine dinucleotide phosphate: quinone oxidoreductase in murine hepatoma cells by 6-(methylsufinyl) hexyl isothiocyanate, an active principle of wasabi (Eutrema wasabi Maxim). Cancer Lett. 2000;161:195-200.