Sulforaphane protects against 6-hydroxydopamine-induced cytotoxicity by increasing expression of heme oxygenase-1 in a PI3K/Akt-dependent manner

Molecular Medicine Reports

Volumn 5, Issue 3, 2012, Pages 847-851

  Deng, Chang ^a   Tao, Ran ^b   Yu, Shun Zhi ^c   Jin, Hua ^d  

^a People's Hospital of Guang Du District   (China)

^b People's Hospital of Panlong District   (China)

^c Mental Health Hospital of Prevention and Treatment in Kunming City   (China)

^d First People's Hospital of Yunnan Province   (China)

Author keywords

6 hydroxydopamine; Heme oxygenase 1; Parkinson's disease; Sulforaphane

Indexed keywords

CASPASE 3; HEME OXYGENASE 1; OXIDOPAMINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CELL DEATH; CELL NUCLEUS; CELL PROTECTION; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INDUCTION; GENE TRANSLOCATION; PROTEIN EXPRESSION;

ANIMALS; ANTICARCINOGENIC AGENTS; CASPASE 3; CELL SURVIVAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; NF-E2-RELATED FACTOR 2; OXIDOPAMINE; PC12 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; THIOCYANATES;

EID: 84856257180     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2011.731     Document Type: Article

References (35)

1. Pakkenberg B, Moller A, Gundersen HJ, Mouritzen Dam A and Pakkenberg H: The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson's disease estimated with an unbiased stereological method. J Neurol Neurosurg Psychiatry 54: 30-33, 1991.
2. Sian J, Dexter DT, Lees AJ, et al: Alterations in glutathione levels in Parkinson's disease and other neurodegenerative disorders affecting basal ganglia. Ann Neurol 36: 348-355, 1994. (Pubitemid 24280055)
3. Castellani RJ, Perry G, Siedlak SL, et al: Hydroxynonenal adducts indicate a role for lipid peroxidation in neocortical and brainstem Lewy bodies in humans. Neurosci Lett 319: 25-28, 2002. (Pubitemid 34117635)
4. Hwang YP, Kim HG, Han EH and Jeong HG: Metallothionein-III protects against 6-hydroxydopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a PI3K and ERK/Nrf2-dependent manner. Toxicol Appl Pharmacol 231: 318-327, 2008.
5. Blum D, Torch S, Lambeng N, et al: Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog Neurobiol 65: 135-172, 2001. (Pubitemid 32524182)
6. Kienzl E, Puchinger L, Jellinger K, Linert W, Stachelberger H and Jameson RF: The role of transition metals in the pathogenesis of Parkinson's disease. J Neurol Sci 134 (Suppl): S69-S78, 1995.
7. Linert W, Herlinger E, Jameson RF, Kienzl E, Jellinger K and Youdim MB: Dopamine, 6-hydroxydopamine, iron, and dioxygen - their mutual interactions and possible implication in the development of Parkinson's disease. Biochim Biophys Acta 1316: 160-168, 1996. (Pubitemid 26273700)
8. Cohen G and Heikkila RE: The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J Biol Chem 249: 2447-2452, 1974.
9. Hu X, Weng Z, Chu CT, et al: Peroxiredoxin-2 protects against 6-hydroxydopamine-induced dopaminergic neurodegeneration via attenuation of the apoptosis signal-regulating kinase (ASK1) signaling cascade. J Neurosci 31: 247-261, 2011.
10. Jakel RJ, Townsend JA, Kraft AD and Johnson JA: Nrf2-mediated protection against 6-hydroxydopamine. Brain Res 1144: 192-201, 2007. (Pubitemid 46440842)
11. Alam J and Cook JL: Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9: 2499-2511, 2003. (Pubitemid 37236369)
12. Hung SY, Liou HC, Kang KH, Wu RM, Wen CC and Fu WM: Overexpression of heme oxygenase-1 protects dopaminergic neurons against 1-methyl-4- phenylpyridinium-induced neurotoxicity. Mol Pharmacol 74: 1564-1575, 2008.
13. Otterbein LE, Soares MP, Yamashita K and Bach FH: Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24: 449-455, 2003. (Pubitemid 36928103)
14. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN and Ames BN: Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043-1046, 1987. (Pubitemid 17049750)
15. Ramsey CP, Glass CA, Montgomery MB, et al: Expression of Nrf2 in neurodegenerative diseases. J Neuropathol Exp Neurol 66: 75-85, 2007. (Pubitemid 46066791)
16. Itoh K, Tong KI and Yamamoto M: Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic Biol Med 36: 1208-1213, 2004. (Pubitemid 38526314)
17. Nakaso K, Yano H, Fukuhara Y, Takeshima T, Wada-Isoe K and Nakashima K: PI3K is a key molecule in the Nrf2-mediated regulation of antioxidative proteins by hemin in human neuroblastoma cells. FEBS Lett 546: 181-184, 2003. (Pubitemid 36782407)
18. Salinas M, Diaz R, Abraham NG, Ruiz de Galarreta CM and Cuadrado A: Nerve growth factor protects against 6-hydroxydopamine- induced oxidative stress by increasing expression of heme oxygenase-1 in a phosphatidylinositol 3-kinase-dependent manner. J Biol Chem 278: 13898-13904, 2003. (Pubitemid 36799930)
19. Zhang Y, Talalay P, Cho CG and Posner GH: A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc Natl Acad Sci USA 89: 2399-2403, 1992.
20. Mattson MP, Son TG and Camandola S: Viewpoint: mechanisms of action and therapeutic potential of neurohormetic phytochemicals. Dose Response 5: 174-186, 2007.
21. Ping Z, Liu W, Kang Z, et al: Sulforaphane protects brains against hypoxic-ischemic injury through induction of Nrf2-dependent phase 2 enzyme. Brain Res 1343: 178-185, 2010.
22. Jazwa A, Rojo AI, Innamorato NG, Hesse M, Fernandez-Ruiz J and Cuadrado A: Pharmacological targeting of the transcription factor nrf2 at the basal ganglia provides disease modifying therapy for experimental parkinsonism. Antioxid Redox Signal 14: 2347-2360, 2011.
23. Tarozzi A, Morroni F, Merlicco A, et al: Sulforaphane as an inducer of glutathione prevents oxidative stress-induced cell death in a dopaminergic-like neuroblastoma cell line. J Neurochem 111: 1161-1171, 2009.
24. Han JM, Lee YJ, Lee SY, et al: Protective effect of sulforaphane against dopaminergic cell death. J Pharmacol Exp Ther 321: 249--256, 2007.
25. Soane L, Li Dai W, Fiskum G and Bambrick LL: Sulforaphane protects immature hippocampal neurons against death caused by exposure to hemin or to oxygen and glucose deprivation. J Neurosci Res 88: 1355-1363, 2010.
26. Tanito M, Masutani H, Kim YC, Nishikawa M, Ohira A and Yodoi J: Sulforaphane induces thioredoxin through the anti- oxidant-responsive element and attenuates retinal light damage in mice. Invest Ophthalmol Vis Sci 46: 979-987, 2005. (Pubitemid 41321036)
27. Itoh K, Ishii T, Wakabayashi N and Yamamoto M: Regulatory mechanisms of cellular response to oxidative stress. Free Radic Res 31: 319-324, 1999. (Pubitemid 29452857)
28. Chen XL and Kunsch C: Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr Pharm Des 10: 879-891, 2004.
29. Chen K, Gunter K and Maines MD: Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem 75: 304-313, 2000. (Pubitemid 30418197)
30. Cuadrado A, Moreno-Murciano P and Pedraza-Chaverri J: The transcription factor Nrf2 as a new therapeutic target in Parkinson's disease. Expert Opin Ther Targets 13: 319-329, 2009.
31. Kensler TW, Wakabayashi N and Biswal S: Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
32. Panahian N, Yoshiura M and Maines MD: Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 72: 1187-1203, 1999. (Pubitemid 29085035)
33. Zhao HD, Zhang F, Shen G, et al: Sulforaphane protects liver injury induced by intestinal ischemia reperfusion through Nrf2-ARE pathway. World J Gastroenterol 16: 3002-3010, 2010.
34. Hwang YP and Jeong HG: The coffee diterpene kahweol induces heme oxygenase-1 via the PI3K and p38/Nrf2 pathway to protect human dopaminergic neurons from 6-hydroxydopamine-derived oxidative stress. FEBS Lett 582: 2655-2662, 2008.
35. Hwang YP and Jeong HG: Ginsenoside Rb1 protects against 6-hydroxydopamine-induced oxidative stress by increasing heme oxygenase-1 expression through an estrogen receptor-related PI3K/Akt/Nrf2-dependent pathway in human dopaminergic cells. Toxicol Appl Pharmacol 242: 18-28, 2010.