Genetic activation of Nrf2 signaling is sufficient to ameliorate neurodegenerative phenotypes in a Drosophila model of Parkinson's disease

DMM Disease Models and Mechanisms

Volumn 4, Issue 5, 2011, Pages 701-707

  Barone, Maria Cecilia ^a   Sykiotis, Gerasimos P ^b   Bohmann, Dirk ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF PATRAS   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; KEAP 1; MAF S PROTEIN; PROTEIN; PROTEIN INHIBITOR; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL LOSS; CONTROLLED STUDY; DIMERIZATION; DNA BINDING; DOPAMINERGIC NERVE CELL; DOWN REGULATION; DROSOPHILA; GENE ACTIVATION; GENE OVEREXPRESSION; HETEROZYGOSITY; IN VIVO STUDY; LOCOMOTION; MALE; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PHENOTYPE; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION;

ALPHA-SYNUCLEIN; ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LOCOMOTION; NERVE DEGENERATION; NF-E2-RELATED FACTOR 2; PARKINSON DISEASE; PHENOTYPE; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TRANSGENES;

EID: 80052277569     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.007575     Document Type: Article

References (59)

1. Asanuma, M., Hirata, H. and Cadet, J. L. (1998). Attenuation of 6-hydroxydopamine-induced dopaminergic nigrostriatal lesions in superoxide dismutase transgenic mice. Neuroscience 85, 907-917. (Pubitemid 28223651)
2. Auluck, P. K. and Bonini, N. M. (2002). Pharmacological prevention of Parkinson disease in Drosophila. Nat. Med. 8, 1185-1186. (Pubitemid 35373534)
3. Auluck, P. K., Meulener, M. C. and Bonini, N. M. (2005). Mechanisms of suppression of {alpha}-synuclein neurotoxicity by geldanamycin in Drosophila. J. Biol. Chem. 280, 2873-2878. (Pubitemid 40189396)
4. Auluck, P. K., Caraveo, G. and Lindquist, S. (2010). alpha-Synuclein: Membrane interactions and toxicity in Parkinson's disease. Annu. Rev. Cell Dev. Biol. 26, 211-233.
5. Barkats, M., Horellou, P., Colin, P., Millecamps, S., Faucon-Biguet, N. and Mallet, J. (2006). 1-methyl-4-phenylpyridinium neurotoxicity is attenuated by adenoviral gene transfer of human Cu/Zn superoxide dismutase. J. Neurosci. Res. 83, 233-242. (Pubitemid 43184387)
6. Blank, V. (2008). Small Maf proteins in mammalian gene control:Mere dimerization partners or dynamic transcriptional regulators? J. Mol. Biol. 376, 913-925.
7. Botella, J. A., Bayersdorfer, F. and Schneuwly, S. (2008). Superoxide dismutase overexpression protects dopaminergic neurons in a Drosophila model of Parkinson's disease. Neurobiol. Dis. 30, 65-73.
8. Burton, N. C., Kensler, T. W. and Guilarte, T. R. (2006). In vivo modulation of the Parkinsonian phenotype by Nrf2. Neurotoxicology 27, 1094-1100. (Pubitemid 44838961)
9. Callio, J., Oury, T. D. and Chu, C. T. (2005). Manganese superoxide dismutase protects against 6-hydroxydopamine injury in mouse brains. J. Biol. Chem. 280, 18536-18542. (Pubitemid 41389104)
10. Chen, P. C., Vargas, M. R., Pani, A. K., Smeyne, R. J., Johnson, D. A., Kan, Y. W. and Johnson, J. A. (2009). Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease:Critical role for the astrocyte. Proc. Natl. Acad. Sci. USA 106, 2933-2938.
11. Clark, J. and Simon, D. K. (2009). Transcribe to survive:Transcriptional control of antioxidant defense programs for neuroprotection in Parkinson's disease. Antioxid. Redox Signal. 11, 509-528.
12. Clark, J., Clore, E. L., Zheng, K., Adame, A., Masliah, E. and Simon, D. K. (2010). Oral N-acetyl-cysteine attenuates loss of dopaminergic terminals in alpha-synuclein overexpressing mice. PLoS ONE 5, e12333.
13. Cuadrado, A., Moreno-Murciano, P. and Pedraza-Chaverri, J. (2009). The transcription factor Nrf2 as a new therapeutic target in Parkinson's disease. Expert Opin. Ther. Targets 13, 319-329.
14. Dawson, T. M., Ko, H. S. and Dawson, V. L. (2010). Genetic animal models of Parkinson's disease. Neuron 66, 646-661.
15. De Vries, H. E., Witte, M., Hondius, D., Rozemuller, A. J., Drukarch, B., Hoozemans, J. and Van Horssen, J. (2008). Nrf2-induced antioxidant protection:A promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic. Biol. Med. 45, 1375-1383.
16. Dexter, D. T., Carter, C. J., Wells, F. R., Javoy-Agid, F., Agid, Y., Lees, A., Jenner, P. and Marsden, C. D. (1989). Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J. Neurochem. 52, 381-389. (Pubitemid 19037600)
17. Du, G., Liu, X., Chen, X., Song, M., Yan, Y., Jiao, R. and Wang, C. C. (2010). Drosophila histone deacetylase 6 protects dopaminergic neurons against {alpha}-synuclein toxicity by promoting inclusion formation. Mol. Biol. Cell 21, 2128-2137.
18. Duffy, J. B. (2002). The GAL4 system in Drosophila:A fly geneticist's swiss army knife. Genesis 34, 1-15.
19. Feany, M. B. and Bender, W. W. (2000). A Drosophila model of Parkinson's disease. Nature 404, 394-398. (Pubitemid 30164341)
20. Franssens, V., Boelen, E., Anandhakumar, J., Vanhelmont, T., Buttner, S. and Winderickx, J. (2010). Yeast unfolds the road map toward alpha-synuclein-induced cell death. Cell Death Differ. 17, 746-753.
21. Friggi-Grelin, F., Coulom, H., Meller, M., Gomez, D., Hirsh, J. and Birman, S. (2003). Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54, 618-627. (Pubitemid 36232667)
22. Hara, H., Ohta, M. and Adachi, T. (2006). Apomorphine protects against 6-hydroxydopamine-induced neuronal cell death through activation of the Nrf2-ARE pathway. J. Neurosci. Res. 84, 860-866. (Pubitemid 44366687)
23. Hindle, J. V. (2010). Ageing, neurodegeneration and Parkinson's disease. Age Ageing 39, 156-161.
24. Horowitz, M. P. and Greenamyre, J. T. (2010). Gene-environment interactions in Parkinson's disease:The importance of animal modeling. Clin. Pharmacol. Ther. 88, 467-474.
25. Hwang, Y. P. and Jeong, H. G. (2008). 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.
26. Ischiropoulos, H. (2003). Oxidative modifications of alpha-synuclein. Ann. N. Y. Acad. Sci. 991, 93-100.
27. Jakel, R. J., Townsend, J. A., Kraft, A. D. and Johnson, J. A. (2007). Nrf2-mediated protection against 6-hydroxydopamine. Brain Res. 1144, 192-201. (Pubitemid 46440842)
28. Jenner, P. (1998). Oxidative mechanisms in nigral cell death in Parkinson's disease. Mov. Disord. 13 Suppl. 1, 24-34.
29. Johnson, J. A., Johnson, D. A., Kraft, A. D., Calkins, M. J., Jakel, R. J., Vargas, M. R. and Chen, P. C. (2008). The Nrf2-ARE pathway:An indicator and modulator of oxidative stress in neurodegeneration. Ann. N. Y. Acad. Sci. 1147, 61-69.
30. Jomova, K., Vondrakova, D., Lawson, M. and Valko, M. (2010). Metals, oxidative stress and neurodegenerative disorders. Mol. Cell. Biochem. 345, 91-104.
31. Jung, K. A. and Kwak, M. K. (2010). The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 15, 7266-7291.
32. Kraft, A. D., Johnson, D. A. and Johnson, J. A. (2004). 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. 24, 1101-1112. (Pubitemid 38177017)
33. Mao, Z. and Davis, R. L. (2009). Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil:Anatomical and physiological heterogeneity. Front. Neural Circuits 3, 5.
34. Marzec, J. M., Christie, J. D., Reddy, S. P., Jedlicka, A. E., Vuong, H., Lanken, P. N., Aplenc, R., Yamamoto, T., Yamamoto, M., Cho, H. Y. et al. (2007). Functional polymorphisms in the transcription factor NRF2 in humans increase the risk of acute lung injury. FASEB J. 21, 2237-2246. (Pubitemid 47026458)
35. McGeer, P. L., Itagaki, S., Boyes, B. E. and McGeer, E. G. (1988). Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38, 1285-1291.
36. Minelli, A., Conte, C., Grottelli, S., Bellezza, I., Emiliani, C. and Bolanos, J. P. (2009). Cyclo(His-Pro) up-regulates heme oxygenase 1 via activation of Nrf2-ARE signalling. J. Neurochem. 111, 956-966.
37. Motohashi, H., O'Connor, T., Katsuoka, F., Engel, J. D. and Yamamoto, M. (2002). Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors. Gene 294, 1-12. (Pubitemid 35291008)
38. Niso-Santano, M., Gonzalez-Polo, R. A., Bravo-San Pedro, J. M., Gomez-Sanchez, R., Lastres-Becker, I., Ortiz-Ortiz, M. A., Soler, G., Moran, J. M., Cuadrado, A. and Fuentes, J. M. (2010). Activation of apoptosis signal-regulating kinase 1 is a key factor in paraquat-induced cell death:Modulation by the Nrf2/Trx axis. Free Radic. Biol. Med. 48, 1370-1381.
39. Oien, D. B., Shinogle, H. E., Moore, D. S. and Moskovitz, J. (2009). Clearance and phosphorylation of alpha-synuclein are inhibited in methionine sulfoxide reductase a null yeast cells. J. Mol. Neurosci. 39, 323-332.
40. Outeiro, T. F., Kontopoulos, E., Altmann, S. M., Kufareva, I., Strathearn, K. E., Amore, A. M., Volk, C. B., Maxwell, M. M., Rochet, J. C., McLean, P. J. et al. (2007). Sirtuin 2 inhibitors rescue alpha-synuclein- mediated toxicity in models of Parkinson's disease. Science 317, 516-519. (Pubitemid 47196116)
41. Ridet, J. L., Bensadoun, J. C., Deglon, N., Aebischer, P. and Zurn, A. D. (2006). Lentivirus-mediated expression of glutathione peroxidase: Neuroprotection in murine models of Parkinson's disease. Neurobiol. Dis. 21, 29-34. (Pubitemid 41817302)
42. Shaltiel-Karyo, R., Frenkel-Pinter, M., Egoz-Matia, N., Frydman-Marom, A., Shalev, D. E., Segal, D. and Gazit, E. (2010). Inhibiting alpha-synuclein oligomerization by stable cell-penetrating beta-synuclein fragments recovers phenotype of Parkinson's disease model flies. PLoS ONE 5, e13863.
43. Siebert, A., Desai, V., Chandrasekaran, K., Fiskum, G. and Jafri, M. S. (2009). Nrf2 activators provide neuroprotection against 6-hydroxydopamine toxicity in rat organotypic nigrostriatal cocultures. J. Neurosci. Res. 87, 1659-1669.
44. Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R. and Goedert, M. (1997). Alpha-synuclein in Lewy bodies. Nature 388, 839-840.
45. Sykiotis, G. P. and Bohmann, D. (2008). Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev. Cell 14, 76-85.
46. Sykiotis, G. P. and Bohmann, D. (2010). Stress-activated cap'n'collar transcription factors in aging and human disease. Sci. Signal. 3, re3.
47. Thiruchelvam, M., Prokopenko, O., Cory-Slechta, D. A., Buckley, B. and Mirochnitchenko, O. (2005). Overexpression of superoxide dismutase or glutathione peroxidase protects against the paraquat + maneb-induced Parkinson disease phenotype. J. Biol. Chem. 280, 22530-22539. (Pubitemid 40827911)
48. Trinh, K., Moore, K., Wes, P. D., Muchowski, P. J., Dey, J., Andrews, L. and Pallanck, L. J. (2008). Induction of the phase II detoxification pathway suppresses neuron loss in Drosophila models of Parkinson's disease. J. Neurosci. 28, 465-472.
49. Trinh, K., Andrews, L., Krause, J., Hanak, T., Lee, D., Gelb, M. and Pallanck, L. (2010). Decaffeinated coffee and nicotine-free tobacco provide neuroprotection in Drosophila models of Parkinson's disease through an NRF2-dependent mechanism. J. Neurosci. 30, 5525-5532.
50. Van Muiswinkel, F. L. and Kuiperij, H. B. (2005). The Nrf2-ARE Signalling pathway:Promising drug target to combat oxidative stress in neurodegenerative disorders. Curr. Drug Targets CNS Neurol. Disord. 4, 267-281.
51. Veraksa, A., McGinnis, N., Li, X., Mohler, J. and McGinnis, W. (2000). Cap 'n' collar B cooperates with a small Maf subunit to specify pharyngeal development and suppress deformed homeotic function in the Drosophila head. Development 127, 4023-4037.
52. Von Otter, M., Landgren, S., Nilsson, S., Celojevic, D., Bergstrom, P., Hakansson, A., Nissbrandt, H., Drozdzik, M., Bialecka, M., Kurzawski, M. et al. (2010). Association of Nrf2-encoding NFE2L2 haplotypes with Parkinson's disease. BMC Med. Genet. 11, 36.
53. Whitworth, A. J., Theodore, D. A., Greene, J. C., Benes, H., Wes, P. D. and Pallanck, L. J. (2005). Increased glutathione S-transferase activity rescues dopaminergic neuron loss in a Drosophila model of Parkinson's disease. Proc. Natl. Acad. Sci. USA 102, 8024-8029. (Pubitemid 40781056)
54. Wruck, C. J., Claussen, M., Fuhrmann, G., Romer, L., Schulz, A., Pufe, T., Waetzig, V., Peipp, M., Herdegen, T. and Gotz, M. E. (2007). Luteolin protects rat PC12 and C6 cells against MPP+ induced toxicity via an ERK dependent Keap1-Nrf2-ARE pathway. J. Neural Transm. Suppl. 72, 57-67.
55. Wu, J. S. and Luo, L. (2006). A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat. Protoc. 1, 2110-2115. (Pubitemid 46773334)
56. Yamamoto, N., Sawada, H., Izumi, Y., Kume, T., Katsuki, H., Shimohama, S. and Akaike, A. (2007). Proteasome inhibition induces glutathione synthesis and protects cells from oxidative stress:Relevance to Parkinson disease. J. Biol. Chem. 282, 4364-4372. (Pubitemid 47101000)
57. Yang, L., Calingasan, N. Y., Thomas, B., Chaturvedi, R. K., Kiaei, M., Wille, E. J., Liby, K. T., Williams, C., Royce, D., Risingsong, R. et al. (2009). Neuroprotective effects of the triterpenoid, CDDO methyl amide, a potent inducer of Nrf2-mediated transcription. PLoS ONE 4, e5757.
58. Yoritaka, A., Hattori, N., Uchida, K., Tanaka, M., Stadtman, E. R. and Mizuno, Y. (1996). Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc. Natl. Acad. Sci. USA 93, 2696-2701. (Pubitemid 26114311)
59. Zhang, M., Shoeb, M., Goswamy, J., Liu, P., Xiao, T. L., Hogan, D., Campbell, G. A. and Ansari, N. H. (2010). Overexpression of aldehyde dehydrogenase 1A1 reduces oxidation-induced toxicity in SH-SY5Y neuroblastoma cells. J. Neurosci. Res. 88, 686-694.