FOXO3 determines the accumulation of α-synuclein and controls the fate of dopaminergic neurons in the substantia nigra

Human Molecular Genetics

Volumn 23, Issue 6, 2014, Pages 1435-1452

  Pino, Emilda ^a   Amamoto, Ryoji ^a   Zheng, Lu ^a   Cacquevel, Matthias ^a   Sarria, Juan Carlos ^a   Knott, Graham W ^a   Schneider, Bernard L ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA-SYNUCLEIN; ANIMALS; CELL DEATH; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DNA DAMAGE; DOPAMINERGIC NEURONS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENETIC VECTORS; HUMANS; OXIDATION-REDUCTION; RATS; SUBSTANTIA NIGRA;

EID: 84894293156     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt530     Document Type: Article

References (61)

1. Conway, K.A., Lee, S.J., Rochet, J.C., Ding, T.T., Williamson, R.E. and Lansbury, P.T. Jr. (2000) Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. USA, 97, 571-576.
2. Lashuel, H.A., Petre, B.M., Wall, J., Simon, M., Nowak, R.J., Walz, T. and Lansbury, P.T. Jr (2002) Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol., 322, 1089-1102.
3. Polymeropoulos, M.H., Lavedan, C., Leroy, E., Ide, S.E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R. et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science, 276, 2045-2047.
4. Singleton, A.B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R. et al. (2003) Alpha-synuclein locus triplication causes Parkinson's disease. Science, 302, 841.
5. Chartier-Harlin, M.C., Kachergus, J., Roumier, C., Mouroux, V., Douay, X., Lincoln, S., Levecque, C., Larvor, L., Andrieux, J., Hulihan, M. et al. (2004) Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet, 364, 1167-1169.
6. Harman, D. (1956) Aging: a theory based on free radical and radiation chemistry. J. Gerontol., 11, 298-300.
7. Storz, P. (2006) Reactive oxygen species-mediated mitochondria-to-nucleus signaling: a key to aging and radical-caused diseases. Sci. STKE, 2006, re3.
8. Kenyon, C. (2005) The plasticity of aging: insights from long-lived mutants. Cell, 120, 449-460.
9. Masoro, E.J. (2000) Caloric restriction and aging: an update. Exp. Gerontol., 35, 299-305.
10. Greer, E.L. and Brunet, A. (2005) FOXO Transcription factors at the interface between longevity and tumor suppression. Oncogene, 24, 7410-7425.
11. Chung, W.H., Dao, R.L., Chen, L.K. and Hung, S.I. (2010) The role of genetic variants in human longevity. Ageing Res. Rev., 9(Suppl. 1), S67-S78.
12. Kenyon, C., Chang, J., Gensch, E., Rudner, A. and Tabtiang, R. (1993) A C. elegans mutant that lives twice as long as wild type. Nature, 366, 461-464.
13. Kimura, K.D., Tissenbaum, H.A., Liu, Y. and Ruvkun, G. (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science, 277, 942-946.
14. Brunet, A., Sweeney, L.B., Sturgill, J.F., Chua, K.F., Greer, P.L., Lin, Y., Tran, H., Ross, S.E., Mostoslavsky, R., Cohen, H.Y. et al. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science, 303, 2011-2015.
15. Wang, F., Nguyen, M., Qin, F.X. and Tong, Q. (2007) SIRT2 deacetylates FOXO3ain response to oxidative stress and caloric restriction. Aging Cell, 6, 505-514.
16. Lehtinen, M.K., Yuan, Z., Boag, P.R., Yang, Y., Villen, J., Becker, E.B., DiBacco, S., de la Iglesia, N., Gygi, S., Blackwell, T.K. et al. (2006) A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell, 125, 987-1001.
17. Oh, S.W., Mukhopadhyay, A., Svrzikapa, N., Jiang, F., Davis, R.J. and Tissenbaum, H.A. (2005)JNKRegulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc. Natl. Acad. Sci. USA, 102, 4494-4499.
18. Greer, E.L., Oskoui, P.R., Banko, M.R., Maniar, J.M., Gygi, M.P., Gygi, S.P. and Brunet, A. (2007) The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J. Biol. Chem., 282, 30107-30119.
19. Tran, H., Brunet, A., Grenier, J.M., Datta, S.R., Fornace, A.J. Jr, DiStefano, P.S., Chiang, L.W. and Greenberg, M.E. (2002) DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science, 296, 530-534.
20. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S.H. and Goldberg, A.L. (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell, 117, 399-412.
21. Gilley, J., Coffer, P.J. and Ham, J. (2003) FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J. Cell Biol., 162, 613-622.
22. Kops, G.J., Dansen, T.B., Polderman, P.E., Saarloos, I., Wirtz, K.W., Coffer, P.J., Huang, T.T., Bos, J.L., Medema, R.H. and Burgering, B.M. (2002) Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature, 419, 316-321.
23. Paik, J.H., Ding, Z., Narurkar, R., Ramkissoon, S., Muller, F., Kamoun, W.S., Chae, S.S., Zheng, H., Ying, H., Mahoney, J. et al. (2009) Foxos cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell, 5, 540-553.
24. Renault, V.M., Rafalski, V.A., Morgan, A.A., Salih, D.A., Brett, J.O., Webb, A.E., Villeda, S.A., Thekkat, P.U., Guillerey, C., Denko, N.C. et al. (2009) Foxo3 regulates neural stem cell homeostasis. Cell Stem Cell, 5, 527-539.
25. Brunet, A., Bonni, A., Zigmond, M.J., Lin, M.Z., Juo, P., Hu, L.S., Anderson, M.J., Arden, K.C., Blenis, J. and Greenberg, M.E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell, 96, 857-868.
26. Zhao, J., Brault, J.J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S.H. and Goldberg, A.L. (2007) Foxo3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab., 6, 472-483.
27. Dumitriu, A., Latourelle, J.C., Hadzi, T.C., Pankratz, N., Garza, D., Miller, J.P., Vance, J.M., Foroud, T., Beach, T.G. and Myers, R.H. (2012) Gene expression profiles in Parkinson disease prefrontal cortex implicate FOXO1 and genes under its transcriptional regulation. PLoS Genet., 8, e1002794.
28. Cohen, E., Bieschke, J., Perciavalle, R.M., Kelly, J.W. and Dillin, A. (2006) Opposing activities protect against age-onset proteotoxicity. Science, 313, 1604-1610.
29. Morley, J.F., Brignull, H.R., Weyers, J.J. and Morimoto, R.I. (2002) The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA, 99, 10417-10422.
30. Brunet, A., Park, J., Tran, H., Hu, L.S., Hemmings, B.A. and Greenberg, M.E. (2001) Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factorFKHRL1(FOXO3a).Mol. Cell. Biol., 21, 952-965.
31. Tothova, Z., Kollipara, R., Huntly, B.J., Lee, B.H., Castrillon, D.H., Cullen, D.E., McDowell, E.P., Lazo-Kallanian, S., Williams, I.R., Sears, C. et al. (2007) Foxos are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell, 128, 325-339.
32. Xie, Q., Hao, Y., Tao, L., Peng, S., Rao, C., Chen, H., You, H., Dong, M.Q. and Yuan, Z. (2012) Lysine methylation of FOXO3 regulates oxidative stress-induced neuronal cell death. EMBO Rep., 13, 371-377.
33. Sulzer, D., Mosharov, E., Talloczy, Z., Zucca, F.A., Simon, J.D. and Zecca, L. (2008) Neuronal pigmented autophagic vacuoles: lipofuscin, neuromelanin, and ceroid as macroautophagic responses during aging and disease. J. Neurochem., 106, 24-36.
34. Choubey, V., Safiulina, D., Vaarmann, A., Cagalinec, M., Wareski, P., Kuum, M., Zharkovsky, A. and Kaasik, A. (2011) Mutant A53T alpha-synuclein induces neuronal death by increasing mitochondrial autophagy. J. Biol. Chem., 286, 10814-10824.
35. Mizushima, N., Yoshimori, T. and Levine, B. (2010) Methodsin mammalian autophagy research. Cell, 140, 313-326.
36. Tanida, I., Yamaji, T., Ueno, T., Ishiura, S., Kominami, E. and Hanada, K. (2008) Consideration about negative controls for LC3 and expression vectors for four colored fluorescent protein-LC3 negative controls. Autophagy, 4, 131-134.
37. Shvets, E., Fass, E. and Elazar, Z. (2008) Utilizingflowcytometry to monitor autophagy in living mammalian cells. Autophagy, 4, 621-628.
38. Gao, W., Ding, W.X., Stolz, D.B. and Yin, X.M. (2008) Induction of macroautophagy by exogenously introduced calcium. Autophagy, 4, 754-761.
39. Seglen, P.O. and Gordon, P.B. (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA, 79, 1889-1892.
40. Barthelemy, C., Henderson, C.E. and Pettmann, B. (2004) Foxo3a induces motoneuron death through the Fas pathway in cooperation with JNK. BMC Neurosci., 5, 48.
41. Qin, Z., Hu, D., Han, S., Reaney, S.H., Di Monte, D.A. and Fink, A.L. (2007) Effect of 4-hydroxy-2-nonenal modification on alpha-synuclein aggregation. J. Biol. Chem., 282, 5862-5870.
42. Xiang, W., Schlachetzki, J.C., Helling, S., Bussmann, J.C., Berlinghof, M., Schaffer, T.E., Marcus, K., Winkler, J., Klucken, J. and Becker, C.M. (2013) Oxidative stress-induced posttranslational modifications of alpha-synuclein: specific modification of alpha-synuclein by 4-hydroxy-2-nonenal increases dopaminergic toxicity. Mol. Cell Neurosci., 54, 71-83.
43. Kuwahara, T., Tonegawa, R., Ito, G., Mitani, S. and Iwatsubo, T. (2012) Phosphorylation of alpha-synuclein protein at Ser-129 reduces neuronal dysfunction by lowering its membrane binding property in Caenorhabditis elegans. J. Biol. Chem., 287, 7098-7109.
44. Kanao, T., Venderova, K., Park, D.S., Unterman, T., Lu, B. and Imai, Y. (2010) Activation of FoxO by LRRK2 induces expression of proapoptotic proteins and alters survival of postmitotic dopaminergic neuron in Drosophila. Hum. Mol. Genet., 19, 3747-3758.
45. Cookson, M.R. (2009) alpha-Synuclein and neuronal cell death. Mol. Neurodegener., 4, 9.
46. Xie, W., Wan, O.W. and Chung, K.K. (2010) New insights into the role of mitochondrial dysfunction and protein aggregation in Parkinson's disease. Biochim. Biophys. Acta, 1802, 935-941.
47. Cohen, E., Paulsson, J.F., Blinder, P., Burstyn-Cohen, T., Du, D., Estepa, G., Adame, A., Pham, H.M., Holzenberger, M., Kelly, J.W. et al. (2009) Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell, 139, 1157-1169.
48. Sengupta, A., Molkentin, J.D. and Yutzey, K.E. (2009) Foxo transcription factors promote autophagy in cardiomyocytes. J. Biol. Chem., 284, 28319-28331.
49. Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., Burden, S.J., Di Lisi, R., Sandri, C., Zhao, J. et al. (2007) Foxo3 controls autophagy in skeletal muscle in vivo. Cell Metab., 6, 458-471.
50. Zhao, Y., Yang, J., Liao, W., Liu, X., Zhang, H., Wang, S., Wang, D., Feng, J., Yu, L. and Zhu, W.G. (2010) Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat. Cell Biol., 12, 665-675.
51. van der Vos, K.E., Eliasson, P., Proikas-Cezanne, T., Vervoort, S.J., van Boxtel, R., Putker, M., van Zutphen, I.J., Mauthe, M., Zellmer, S., Pals, C. et al. (2012) Modulation of glutamine metabolism by the PI(3)K-PKB-FOXO network regulates autophagy. Nat. Cell Biol., 14, 829-837.
52. Warr, M.R., Binnewies, M., Flach, J., Reynaud, D., Garg, T., Malhotra, R., Debnath, J. and Passegue, E. (2013) FOXO3A Directs a protective autophagy program in haematopoietic stem cells. Nature, 494, 323-327.
53. Mei, Y., Zhang, Y., Yamamoto, K., Xie, W., Mak, T.W. and You, H. (2009) FOXO3a-dependent Regulation of Pink1 (Park6) mediates survival signaling in response to cytokine deprivation. Proc. Natl. Acad. Sci. USA, 106, 5153-5158.
54. Lee, H.J., Khoshaghideh, F., Patel, S. and Lee, S.J. (2004) Clearance of alpha-synuclein oligomeric intermediates via the lysosomal degradation pathway. J. Neurosci., 24, 1888-1896.
55. Webb, J.L., Ravikumar, B., Atkins, J., Skepper, J.N. and Rubinsztein, D.C. (2003) Alpha-synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem., 278, 25009-25013.
56. Cuervo, A.M., Stefanis, L., Fredenburg, R., Lansbury, P.T. and Sulzer, D. (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science, 305, 1292-1295.
57. Grimm, D., Kay, M.A. and Kleinschmidt, J.A. (2003) Helper virus-free, optically controllable, and two-plasmid-based production of adeno-associated virus vectors of serotypes 1 to 6. Mol. Ther., 7, 839-850.
58. Dusonchet, J., Bensadoun, J.C., Schneider, B.L. and Aebischer, P. (2009) Targeted overexpression of the parkin substrate Pael-R in the nigrostriatal system of adult rats to model Parkinson's disease. Neurobiol. Dis., 35, 32-41.
59. Azeredo da Silveira, S., Schneider, B.L., Cifuentes-Diaz, C., Sage, D., Abbas-Terki, T., Iwatsubo, T., Unser, M. and Aebischer, P. (2009) Phosphorylation does not prompt, nor prevent, the formation of alpha-synuclein toxic species in a rat model of parkinson's disease. Hum. Mol. Genet., 18, 872-887.
60. Gaugler, M.N., Genc, O., Bobela, W., Mohanna, S., Ardah, M.T., El-Agnaf, O.M., Cantoni, M., Bensadoun, J.C., Schneggenburger, R., Knott, G.W. et al. (2012) Nigrostriatal overabundance of alpha-synuclein leads to decreased vesicle density and deficits in dopamine release that correlate with reduced motor activity. Acta Neuropathol., 123, 653-669.
61. Voutsinos-Porche, B., Knott, G., Tanaka, K., Quairiaux, C., Welker, E. and Bonvento, G. (2003) Glial glutamate transporters and maturation of the mouse somatosensory cortex. Cereb. Cortex, 13, 1110-1121.