Sulforaphane induces autophagy through ERK activation in neuronal cells

FEBS Letters

Volumn 588, Issue 17, 2014, Pages 3081-3088

  Jo, Chulman ^a   Kim, Sunhyo ^a   Cho, Sun Jung ^a   Choi, Ki Ju ^a   Yun, Sang Moon ^a   Koh, Young Ho ^a   Johnson, Gail V W ^b   Park, Sang Ick ^a  

^a Korea National Institute of Health   (South Korea)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Autophagy; Extracellular signal regulated kinase; Nuclear factor E2 related factor 2; Reactive oxygen species; Sulforaphane

Indexed keywords

ACETYLCYSTEINE; ANTIOXIDANT; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 27; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; DRUG MECHANISM; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LYSOSOME; NEURAL STEM CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION;

AUTOPHAGY; EXTRACELLULAR SIGNAL-REGULATED KINASE; NUCLEAR FACTOR E2-RELATED FACTOR 2; REACTIVE OXYGEN SPECIES; SULFORAPHANE;

ANIMALS; AUTOPHAGY; CELL LINE, TUMOR; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; ISOTHIOCYANATES; MICE; NEURONS; REACTIVE OXYGEN SPECIES;

EID: 84906219165     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.06.036     Document Type: Article

References (45)

1. Y. Zhang, P. Talalay, C.G. Cho, and G.H. Posner A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure Proc. Natl. Acad. Sci. U S A 89 1992 2399 2403
2. J.W. Fahey, and P. Talalay Antioxidant functions of sulforaphane: a potent inducer of Phase II detoxication enzymes Food Chem. Toxicol. 37 1999 973 979
3. I. Misiewicz, K. Skupinska, E. Kowalska, J. Lubinski, and T. Kasprzycka-Guttman Sulforaphane-mediated induction of a phase 2 detoxifying enzyme NAD(P)H:quinone reductase and apoptosis in human lymphoblastoid cells Acta Biochim. Pol. 51 2004 711 721
4. M. McMahon, K. Itoh, M. Yamamoto, and J.D. Hayes Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression J. Biol. Chem. 278 2003 21592 21600
5. A.L. Eggler, K.A. Gay, and A.D. Mesecar Molecular mechanisms of natural products in chemoprevention: induction of cytoprotective enzymes by Nrf2 Mol. Nutr. Food Res. 52 Suppl. 1 2008 S84 94
6. D.D. Zhang, and M. Hannink 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. 23 2003 8137 8151
7. Y. Li, J.D. Paonessa, and Y. Zhang Mechanism of chemical activation of Nrf2 PLoS ONE 7 2012 e35122
8. N. Gan, Y.C. Wu, M. Brunet, C. Garrido, F.L. Chung, C. Dai, and L. Mi Sulforaphane activates heat shock response and enhances proteasome activity through up-regulation of Hsp27 J. Biol. Chem. 285 2010 35528 35536
9. E. Heiss, C. Herhaus, K. Klimo, H. Bartsch, and C. Gerhauser Nuclear factor kappa B is a molecular target for sulforaphane-mediated anti-inflammatory mechanisms J. Biol. Chem. 276 2001 32008 32015
10. N.G. Innamorato, A.I. Rojo, A.J. Garcia-Yague, M. Yamamoto, M.L. de Ceballos, and A. Cuadrado The transcription factor Nrf2 is a therapeutic target against brain inflammation J. Immunol. 181 2008 680 689
11. L.T. Chuang, S.T. Moqattash, H.F. Gretz, F. Nezhat, J. Rahaman, and J.W. Chiao Sulforaphane induces growth arrest and apoptosis in human ovarian cancer cells Acta Obstet. Gynecol. Scand. 86 2007 1263 1268
12. T.A. Matsui, H. Murata, T. Sakabe, Y. Sowa, N. Horie, R. Nakanishi, T. Sakai, and T. Kubo Sulforaphane induces cell cycle arrest and apoptosis in murine osteosarcoma cells in vitro and inhibits tumor growth in vivo Oncol. Rep. 18 2007 1263 1268
13. N. Mizushima Autophagy: process and function Genes Dev. 21 2007 2861 2873
14. H. Weidberg, E. Shvets, and Z. Elazar Biogenesis and cargo selectivity of autophagosomes Annu. Rev. Biochem. 80 2011 125 156
15. E. Wong, and A.M. Cuervo Autophagy gone awry in neurodegenerative diseases Nat. Neurosci. 13 2010 805 811
16. R.A. Nixon Autophagy in neurodegenerative disease: friend, foe or turncoat? Trends Neurosci. 29 2006 528 535
17. M. Valko, D. Leibfritz, J. Moncol, M.T. Cronin, M. Mazur, and J. Telser Free radicals and antioxidants in normal physiological functions and human disease Int. J. Biochem. Cell Biol. 39 2007 44 84
18. M.B. Azad, Y. Chen, and S.B. Gibson Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment Antioxid. Redox Signal. 11 2009 777 790
19. Y. Chen, M.B. Azad, and S.B. Gibson Superoxide is the major reactive oxygen species regulating autophagy Cell Death Differ. 16 2009 1040 1052
20. J. Huang, V. Canadien, G.Y. Lam, B.E. Steinberg, M.C. Dinauer, M.A. Magalhaes, M. Glogauer, S. Grinstein, and J.H. Brumell Activation of antibacterial autophagy by NADPH oxidases Proc. Natl. Acad. Sci. U S A 106 2009 6226 6231
21. R. Scherz-Shouval, E. Shvets, E. Fass, H. Shorer, L. Gil, and Z. Elazar Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4 EMBO J. 26 2007 1749 1760
22. S.V. Singh, S.K. Srivastava, S. Choi, K.L. Lew, J. Antosiewicz, D. Xiao, Y. Zeng, S.C. Watkins, C.S. Johnson, D.L. Trump, Y.J. Lee, H. Xiao, and A. Herman-Antosiewicz Sulforaphane-induced cell death in human prostate cancer cells is initiated by reactive oxygen species J. Biol. Chem. 280 2005 19911 19924
23. D. Xiao, A.A. Powolny, J. Antosiewicz, E.R. Hahm, A. Bommareddy, Y. Zeng, D. Desai, S. Amin, A. Herman-Antosiewicz, and S.V. Singh Cellular responses to cancer chemopreventive agent D,L-sulforaphane in human prostate cancer cells are initiated by mitochondrial reactive oxygen species Pharm. Res. 26 2009 1729 1738
24. Y.J. Lee, and S.H. Lee Sulforaphane induces antioxidative and antiproliferative responses by generating reactive oxygen species in human bronchial epithelial BEAS-2B cells J. Korean Med. Sci. 26 2011 1474 1482
25. P. Naumann, F. Fortunato, H. Zentgraf, M.W. Buchler, I. Herr, and J. Werner Autophagy and cell death signaling following dietary sulforaphane act independently of each other and require oxidative stress in pancreatic cancer Int. J. Oncol. 39 2011 101 109
26. C. Jo, S. Gundemir, S. Pritchard, Y.N. Jin, I. Rahman, and G.V. Johnson Nrf2 reduces levels of phosphorylated tau protein by inducing autophagy adaptor protein NDP52 Nat. Commun. 5 2014 3496
27. Y. Liu, C.L. Hettinger, D. Zhang, K. Rezvani, X. Wang, and H. Wang Sulforaphane enhances proteasomal and autophagic activities in mice and is a potential therapeutic reagent for Huntington's disease J. Neurochem. 2014
28. Y.N. Jin, W.Y. Hwang, C. Jo, and G.V. Johnson Metabolic state determines sensitivity to cellular stress in Huntington disease: normalization by activation of PPARgamma PLoS ONE 7 2012 e30406
29. D.J. Klionsky, F.C. Abdalla, H. Abeliovich, R.T. Abraham, A. Acevedo-Arozena, K. Adeli, L. Agholme, M. Agnello, P. Agostinis, J.A. Aguirre-Ghiso, H.J. Ahn, O. Ait-Mohamed, S. Ait-Si-Ali, T. Akematsu, S. Akira, H.M. Al-Younes, M.A. Al-Zeer, M.L. Albert, R.L. Albin, J. Alegre-Abarrategui, M.F. Aleo, M. Alirezaei, A. Almasan, M. Almonte-Becerril, A. Amano, R. Amaravadi, S. Amarnath, A.O. Amer, N. Andrieu-Abadie, V. Anantharam, D.K. Ann, S. Anoopkumar-Dukie, H. Aoki, N. Apostolova, G. Arancia, J.P. Aris, K. Asanuma, N.Y. Asare, H. Ashida, V. Askanas, D.S. Askew, P. Auberger, M. Baba, S.K. Backues, E.H. Baehrecke, B.A. Bahr, X.Y. Bai, Y. Bailly, R. Baiocchi, G. Baldini, W. Balduini, A. Ballabio, B.A. Bamber, E.T. Bampton, G. Banhegyi, C.R. Bartholomew, D.C. Bassham, R.C. Bast Jr., H. Batoko, B.H. Bay, I. Beau, D.M. Bechet, T.J. Begley, C. Behl, C. Behrends, S. Bekri, B. Bellaire, L.J. Bendall, L. Benetti, L. Berliocchi, H. Bernardi, F. Bernassola, S. Besteiro, I. Bhatia-Kissova, X. Bi, M. Biard-Piechaczyk, J.S. Blum, L.H. Boise, P. Bonaldo, D.L. Boone, B.C. Bornhauser, K.R. Bortoluci, I. Bossis, F. Bost, J.P. Bourquin, P. Boya, M. Boyer-Guittaut, P.V. Bozhkov, N.R. Brady, C. Brancolini, A. Brech, J.E. Brenman, A. Brennand, E.H. Bresnick, P. Brest, D. Bridges, M.L. Bristol, P.S. Brookes, E.J. Brown, and J.H. Brumell et al. Guidelines for the use and interpretation of assays for monitoring autophagy Autophagy 8 2012 445 544
30. N. Mizushima The role of the Atg1/ULK1 complex in autophagy regulation Curr. Opin. Cell Biol. 22 2010 132 139
31. C.H. Wong, K.B. Iskandar, S.K. Yadav, J.L. Hirpara, T. Loh, and S. Pervaiz Simultaneous induction of non-canonical autophagy and apoptosis in cancer cells by ROS-dependent ERK and JNK activation PLoS ONE 5 2010 e9996
32. J. Huang, G.Y. Lam, and J.H. Brumell Autophagy signaling through reactive oxygen species Antioxid. Redox Signal. 14 2011 2215 2231
33. J.W. Ramos The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells Int. J. Biochem. Cell Biol. 40 2008 2707 2719
34. L.O. Murphy, and J. Blenis MAPK signal specificity: the right place at the right time Trends Biochem. Sci. 31 2006 268 275
35. S. Cagnol, and J.C. Chambard ERK and cell death: mechanisms of ERK-induced cell death - apoptosis, autophagy and senescence FEBS J. 277 2010 2 21
36. P. Cheng, I. Alberts, and X. Li The role of ERK1/2 in the regulation of proliferation and differentiation of astrocytes in developing brain Int. J. Dev. Neurosci. 31 2013 783 789
37. S. Pattingre, C. Bauvy, and P. Codogno Amino acids interfere with the ERK1/2-dependent control of macroautophagy by controlling the activation of Raf-1 in human colon cancer HT-29 cells J. Biol. Chem. 278 2003 16667 16674
38. S. Pattingre, A. Petiot, and P. Codogno Analyses of Galpha-interacting protein and activator of G-protein-signaling-3 functions in macroautophagy Methods Enzymol. 390 2004 17 31
39. A. Jain, T. Lamark, E. Sjottem, K.B. Larsen, J.A. Awuh, A. Overvatn, M. McMahon, J.D. Hayes, and T. Johansen P62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription J. Biol. Chem. 285 2010 22576 22591
40. L.M. Zipper, and R.T. Mulcahy Erk activation is required for Nrf2 nuclear localization during pyrrolidine dithiocarbamate induction of glutamate cysteine ligase modulatory gene expression in HepG2 cells Toxicol. Sci. 73 2003 124 134
41. C. Xu, X. Yuan, Z. Pan, G. Shen, J.H. Kim, S. Yu, T.O. Khor, W. Li, J. Ma, and A.N. Kong 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. 5 2006 1918 1926
42. A. Tarozzi, C. Angeloni, M. Malaguti, F. Morroni, S. Hrelia, and P. Hrelia Sulforaphane as a potential protective phytochemical against neurodegenerative diseases Oxid. Med. Cell Longev. 2013 2013 415078
43. A.L. Benedict, A. Mountney, A. Hurtado, K.E. Bryan, R.L. Schnaar, A.T. Dinkova-Kostova, and P. Talalay Neuroprotective effects of sulforaphane after contusive spinal cord injury J. Neurotrauma 29 2012 2576 2586
44. P.K. Dash, J. Zhao, S.A. Orsi, M. Zhang, and A.N. Moore Sulforaphane improves cognitive function administered following traumatic brain injury Neurosci. Lett. 460 2009 103 107
45. H.V. Kim, H.Y. Kim, H.Y. Ehrlich, S.Y. Choi, D.J. Kim, and Y. Kim Amelioration of Alzheimer's disease by neuroprotective effect of sulforaphane in animal model Amyloid 20 2013 7 12