The stress response factor daf-16 /FOXO is required for multiple compound families to prolong the function of neurons with Huntington's disease

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Farina, Francesca ^a,b   Lambert, Emmanuel ^a,b   Commeau, Lucie ^a,b   Lejeune, François Xavier ^a,b   Roudier, Nathalie ^c   Fonte, Cosima ^c   Parker, J Alex ^a,b,f   Boddaert, Jacques ^a,b,d   Verny, Marc ^a,b,d   Baulieu, Etienne Emile ^c,e   Neri, Christian ^a,b  

^a CNRS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSERM   (France)

^d ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^e MAPREG   (France)

^f CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; DAF-16 PROTEIN, C ELEGANS; FORKHEAD TRANSCRIPTION FACTOR; HTT PROTEIN, HUMAN; HUNTINGTIN; ISOQUERCITRIN; LITHIUM CHLORIDE; PREGNENOLONE; QUERCETIN; TRANSCRIPTION FACTOR FKHRL1;

AGING; ANALOGS AND DERIVATIVES; ANIMAL; CAENORHABDITIS ELEGANS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE KNOCK-IN; GENETICS; HUMAN; HUNTINGTON CHOREA; MOUSE; NERVE CELL; PATHOLOGY; PRECLINICAL STUDY; TRANSGENIC ANIMAL;

AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DRUG EVALUATION, PRECLINICAL; FORKHEAD BOX PROTEIN O3; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENE KNOCK-IN TECHNIQUES; HUMANS; HUNTINGTIN PROTEIN; HUNTINGTON DISEASE; LITHIUM CHLORIDE; MICE; NEURONS; PREGNENOLONE; QUERCETIN;

EID: 85021184231     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-04256-w     Document Type: Article

References (99)

1. Kennedy, B. K. et al. Geroscience: linking aging to chronic disease. Cell 159, 709-713, doi:10.1016/j.cell.2014.10.039 (2014).
2. Rafalski, V. A., Mancini, E. & Brunet, A. Energy metabolism and energy-sensing pathways in mammalian embryonic and adult stem cell fate. J Cell Sci 125, 5597-5608, doi:10.1242/jcs.114827 (2012).
3. Calabrese, V., Cornelius, C., Dinkova-Kostova, A. T., Calabrese, E. J. & Mattson, M. P. Cellular Stress Responses, The Hormesis Paradigm, and Vitagenes: Novel Targets for Therapeutic Intervention in Neurodegenerative Disorders. Antioxid Redox Sign 13, 1763-1811, doi:10.1089/ars.2009.3074 (2010).
4. Parker, J. A. et al. Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat Genet 37, 349-350 (2005).
5. Cohen, E., Bieschke, J., Perciavalle, R. M., Kelly, J. W. & Dillin, A. Opposing activities protect against age-onset proteotoxicity. Science (New York, N.Y 313, 1604-1610, doi:10.1126/science.1124646 (2006).
6. Parker, J. A. et al. Integration of beta-Catenin, Sirtuin, and FOXO Signaling Protects from Mutant Huntingtin Toxicity. J Neurosci 32, 12630-12640, doi:10.1523/JNEUROSCI.0277-12.2012 (2012).
7. Jiang, M. et al. Neuroprotective role of Sirt1 in mammalian models of Huntington's disease through activation of multiple Sirt1 targets. Nat Med 18, 153-158, doi:10.1038/nm.2558 (2012).
8. Jeong, H. et al. Sirt1 mediates neuroprotection from mutant huntingtin by activation of the TORC1 and CREB transcriptional pathway. Nat Med. doi:10.1038/nm.2559 (2011).
9. Pino, E. et al. FOXO3 determines the accumulation of alpha-synuclein and controls the fate of dopaminergic neurons in the substantia nigra. Hum Mol Genet 23, 1435-1452, doi:10.1093/hmg/ddt530 (2014).
10. Kim, D. et al. SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis. The EMBO journal 26, 3169-3179 (2007).
11. Vazquez-Manrique, R. P. et al. AMPK activation protects from neuronal dysfunction and vulnerability across nematode, cellular and mouse models of Huntington's disease. Hum Mol Genet. doi:10.1093/hmg/ddv513 (2015).
12. Longo, V. D. et al. Interventions to Slow Aging in Humans: Are We Ready? Aging Cell 14, 497-510, doi:10.1111/acel.12338 (2015).
13. Antebi, A., Yeh, W. H., Tait, D., Hedgecock, E. M. & Riddle, D. L. daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 14, 1512-1527 (2000).
14. Motola, D. L. et al. Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124, 1209-1223 (2006).
15. Gerisch, B. et al. A bile acid-like steroid modulates Caenorhabditis elegans lifespan through nuclear receptor signaling. Proceedings of the National Academy of Sciences of the United States of America 104, 5014-5019 (2007).
16. Parker, J. A. et al. Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death. Proc Natl Acad Sci USA 98, 13318-13323 (2001).
17. Parker, J. A. et al. Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death. Proceedings of the National Academy of Sciences of the United States of America 98, 13318-13323, doi:10.1073/pnas.231476398 (2001).
18. Tourette, C. et al. The Wnt receptor Ryk reduces neuronal and cell survival capacity by repressing FOXO activity during the early phases of mutant huntingtin pathogenicity. PLoS Biol 12, e1001895, doi:10.1371/journal.pbio.1001895 (2014).
19. Fontaine-Lenoir, V. et al. Microtubule-associated protein 2 (MAP2) is a neurosteroid receptor. Proceedings of the National Academy of Sciences of the United States of America 103, 4711-4716 (2006).
20. Trettel, F. et al. Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum Mol Genet 9, 2799-2809 (2000).
21. Magalingam, K. B., Radhakrishnan, A. & Haleagrahara, N. Protective effects of quercetin glycosides, rutin, and isoquercetrin against 6-hydroxydopamine (6-OHDA)-induced neurotoxicity in rat pheochromocytoma (PC-12) cells. Int J Immunopathol Pharmacol 29, 30-39, doi:10.1177/0394632015613039 (2016).
22. Pouladi, M. A. et al. NP03, a novel low-dose lithium formulation, is neuroprotective in the YAC128 mouse model of Huntington disease. Neurobiol Dis 48, 282-289, doi:10.1016/j.nbd.2012.06.026 (2012).
23. Vazquez-Manrique, R. P. et al. AMPK activation protects from neuronal dysfunction and vulnerability across nematode, cellular and mouse models of Huntington's disease. Hum Mol Genet 25, 1043-1058, doi:10.1093/hmg/ddv513 (2016).
24. Burnett, C. et al. Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila. Nature 477, 482-485, doi:10.1038/nature10296 (2011).
25. Bianchi, M. & Baulieu, E. E. 3beta-Methoxy-pregnenolone (MAP4343) as an innovative therapeutic approach for depressive disorders. Proceedings of the National Academy of Sciences of the United States of America 109, 1713-1718, doi:10.1073/ pnas.1121485109 (2012).
26. Essers, M. A. et al. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308, 1181-1184 (2005).
27. Matyash, V. et al. Sterol-derived hormone(s) controls entry into diapause in Caenorhabditis elegans by consecutive activation of DAF-12 and DAF-16. PLoS Biol 2, e280 (2004).
28. Gordon, P. et al. The invertebrate microtubule-associated protein PTL-1 functions in mechanosensation and development in Caenorhabditis elegans. Dev Genes Evol 218, 541-551 (2008).
29. Rubinsztein, D. C. Lessons from animal models of Huntington's disease. Trends Genet 18, 202-209 (2002).
30. Levine, M. S., Cepeda, C., Hickey, M. A., Fleming, S. M. & Chesselet, M. F. Genetic mouse models of Huntington's and Parkinson's diseases: illuminating but imperfect. Trends Neurosci 27, 691-697 (2004).
31. Richard, T. et al. Neuroprotective properties of resveratrol and derivatives. Ann N Y Acad Sci 1215, 103-108, doi:10.1111/j.1749- 6632.2010.05865.x (2011).
32. Patel, K. R. et al. Clinical trials of resveratrol. Ann N Y Acad Sci 1215, 161-169, doi:10.1111/j.1749-6632.2010.05853.x (2011).
33. Morselli, E. et al. Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis 1, e10, doi:10.1038/cddis.2009.8 (2010).
34. Baur, J. A. et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444, 337-342 (2006).
35. Price, N. L. et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab 15, 675-690, doi:10.1016/j.cmet.2012.04.003 (2012).
36. Pacholec, M. et al. SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J Biol Chem 285, 8340-8351, doi:10.1074/jbc.M109.088682 (2010).
37. Sinclair, D. A. & Guarente, L. Small-molecule allosteric activators of sirtuins. Annu Rev Pharmacol Toxicol 54, 363-380, doi:10.1146/ annurev-pharmtox-010611-134657 (2014).
38. Hubbard, B. P. et al. Evidence for a common mechanism of SIRT1 regulation by allosteric activators. Science (New York, NY 339, 1216-1219, doi:10.1126/science.1231097 (2013).
39. Lee, S. S., Kennedy, S., Tolonen, A. C. & Ruvkun, G. DAF-16 target genes that control C. elegans life-span and metabolism. Science (New York, NY 300, 644-647 (2003).
40. Murphy, C. T. et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277-283 (2003).
41. Neves, A. R., Lucio, M., Lima, J. L. & Reis, S. Resveratrol in medicinal chemistry: a critical review of its pharmacokinetics, drugdelivery, and membrane interactions. Curr Med Chem 19, 1663-1681 (2012).
42. Fernandez, C. et al. Synthesis of glycosyl derivatives as dopamine prodrugs: interaction with glucose carrier GLUT-1. Org Biomol Chem 1, 767-771 (2003).
43. Von Stetina, S. E. & Mango, S. E. Wormnet: a crystal ball for Caenorhabditis elegans. Genome Biol 9, 226 (2008).
44. Parmentier, F., Lejeune, F. X. & Neri, C. Pathways to decoding the clinical potential of stress response FOXO-interaction networks for Huntington's disease: of gene prioritization and context dependence. Front Aging Neurosci 5, 22, doi:10.3389/fnagi.2013.00022 (2013).
45. Mojsilovic-Petrovic, J. et al. FOXO3a is broadly neuroprotective in vitro and in vivo against insults implicated in motor neuron diseases. J Neurosci 29, 8236-8247, doi:10.1523/JNEUROSCI.1805-09.2009 (2009).
46. Chen, X. et al. Ethosuximide ameliorates neurodegenerative disease phenotypes by modulating DAF-16/FOXO target gene expression. Mol Neurodegener 10, 51, doi:10.1186/s13024-015-0046-3 (2015).
47. Salih, D. A. & Brunet, A. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol 20, 126-136, doi:10.1016/j.ceb.2008.02.005 (2008).
48. Parker, J. A., Holbert, S., Lambert, E., Abderrahmane, S. & Neri, C. Genetic and pharmacological suppression of polyglutaminedependent neuronal dysfunction in Caenorhabditis elegans. J Mol Neurosci 23, 61-68, doi:10.1385/JMN:23:1-2:061 (2004).
49. Paulsen, J. S. et al. Clinical and Biomarker Changes in Premanifest Huntington Disease Show Trial Feasibility: A Decade of the PREDICT-HD Study. Front Aging Neurosci 6, 78, doi:10.3389/fnagi.2014.00078 (2014).
50. Tabrizi, S. J. et al. Biological and clinical changes in premanifest and early stage Huntington's disease in the TRACK-HD study: the 12-month longitudinal analysis. Lancet Neurol 10, 31-42, doi:10.1016/S1474-4422(10)70276-3 (2011).
51. Schumacher, M. et al. Steroid hormones and neurosteroids in normal and pathological aging of the nervous system. Prog Neurobiol 71, 3-29 (2003).
52. Roglio, I. et al. Neuroactive steroids and peripheral neuropathy. Brain Res Rev 57, 460-469 (2008).
53. Gonzalez Deniselle, M. C. et al. Progesterone neuroprotection in the Wobbler mouse, a genetic model of spinal cord motor neuron disease. Neurobiol Dis 11, 457-468 (2002).
54. North, B. J., Marshall, B. L., Borra, M. T., Denu, J. M. & Verdin, E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell 11, 437-444 (2003).
55. Yogev, S., Cooper, R., Fetter, R., Horowitz, M. & Shen, K. Microtubule Organization Determines Axonal Transport Dynamics. Neuron 92, 449-460, doi:10.1016/j.neuron.2016.09.036 (2016).
56. Ehrnhoefer, D. E., Wong, B. K. & Hayden, M. R. Convergent pathogenic pathways in Alzheimer's and Huntington's diseases: shared targets for drug development. Nat Rev Drug Discov 10, 853-867, doi:10.1038/nrd3556 (2011).
57. Catoire, H. et al. Sirtuin Inhibition Protects from the Polyalanine Muscular Dystrophy Protein PABPN1. Hum Mol Genet (2008).
58. Lagouge, M. et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127, 1109-1122 (2006).
59. Dasgupta, B. & Milbrandt, J. Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci USA (2007).
60. Yang, Y. J. et al. Resveratrol suppresses glial activation and alleviates trigeminal neuralgia via activation of AMPK. J Neuroinflammation 13, 84, doi:10.1186/s12974-016-0550-6 (2016).
61. Maher, P. et al. ERK activation by the polyphenols fisetin and resveratrol provides neuroprotection in multiple models of Huntington's disease. Hum Mol Genet 20, 261-270, doi:10.1093/hmg/ddq460 (2011).
62. Ho, D. J., Calingasan, N. Y., Wille, E., Dumont, M. & Beal, M. F. Resveratrol protects against peripheral deficits in a mouse model of Huntington's disease. Exp Neurol 225, 74-84, doi:10.1016/j.expneurol.2010.05.006 (2010).
63. Walle, T., Hsieh, F., DeLegge, M. H., Oatis, J. E. Jr. & Walle, U. K. High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab Dispos 32, 1377-1382 (2004).
64. Wang, Q. et al. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res 958, 439-447 (2002).
65. Heemskerk, J., Tobin, A. J. & Bain, L. J. Teaching old drugs new tricks. Meeting of the Neurodegeneration Drug Screening Consortium, 7-8 April 2002, Washington, DC, USA. Trends in neurosciences 25, 494-496 (2002).
66. Youdim, K. A., Qaiser, M. Z., Begley, D. J., Rice-Evans, C. A. & Abbott, N. J. Flavonoid permeability across an in situ model of the blood-brain barrier. Free Radic Biol Med 36, 592-604 (2004).
67. Kampkotter, A. et al. Investigations of protective effects of the flavonoids quercetin and rutin on stress resistance in the model organism Caenorhabditis elegans. Toxicology 234, 113-123 (2007).
68. Seidler, J., McGovern, S. L., Doman, T. N. & Shoichet, B. K. Identification and prediction of promiscuous aggregating inhibitors among known drugs. J Med Chem 46, 4477-4486, doi:10.1021/jm030191r (2003).
69. Shukla, V. et al. Iridoid compound 10-O-trans-p-coumaroylcatalpol extends longevity and reduces alpha synuclein aggregation in Caenorhabditis elegans. CNS Neurol Disord Drug Targets 11, 984-992 (2012).
70. Keowkase, R., Aboukhatwa, M. & Luo, Y. Fluoxetine protects against amyloid-beta toxicity, in part via daf-16 mediated cell signaling pathway, in Caenorhabditis elegans. Neuropharmacology 59, 358-365, doi:10.1016/j.neuropharm.2010.04.008 (2010).
71. Voisine, C. et al. Identification of potential therapeutic drugs for huntington's disease using Caenorhabditis elegans. PLoS One 2, e504, doi:10.1371/journal.pone.0000504 (2007).
72. Keeler, A. M. et al. Cellular Analysis of Silencing the Huntington's Disease Gene Using AAV9 Mediated Delivery of Artificial Micro RNA into the Striatum of Q140/Q140 Mice. J Huntingtons Dis 5, 239-248, doi:10.3233/JHD-160215 (2016).
73. Mestre, T. A. & Sampaio, C. Huntington Disease: Linking Pathogenesis to the Development of Experimental Therapeutics. Curr Neurol Neurosci Rep 17, 18, doi:10.1007/s11910-017-0711-8 (2017).
74. Precious, S. V., Zietlow, R., Dunnett, S. B., Kelly, C. M. & Rosser, A. E. Is there a place for human fetal-derived stem cells for cell replacement therapy in Huntington's disease? Neurochem Int. doi:10.1016/j.neuint.2017.01.016 (2017).
75. Zou, Y. et al. Forkhead box transcription factor FOXO3a suppresses estrogen-dependent breast cancer cell proliferation and tumorigenesis. Breast Cancer Res 10, R21 (2008).
76. Dowell, P., Otto, T. C., Adi, S. & Lane, M. D. Convergence of peroxisome proliferator-activated receptor gamma and Foxo1 signaling pathways. J Biol Chem 278, 45485-45491, doi:10.1074/jbc.M309069200 (2003).
77. Chew, Y. L., Fan, X., Gotz, J. & Nicholas, H. R. PTL-1 regulates neuronal integrity and lifespan in C. elegans. J Cell Sci 126, 2079-2091, doi:10.1242/jcs.jcs124404 (2013).
78. Chew, Y. L., Fan, X., Gotz, J. & Nicholas, H. R. Regulation of age-related structural integrity in neurons by protein with tau-like repeats (PTL-1) is cell autonomous. Sci Rep 4, 5185, doi:10.1038/srep05185 (2014).
79. Tank, E. M., Rodgers, K. E. & Kenyon, C. Spontaneous age-related neurite branching in Caenorhabditis elegans. J Neurosci 31, 9279-9288, doi:10.1523/JNEUROSCI.6606-10.2011 (2011).
80. Nechipurenko, I. V. & Broihier, H. T. FoxO limits microtubule stability and is itself negatively regulated by microtubule disruption. J Cell Biol 196, 345-362, doi:10.1083/jcb.201105154 (2012).
81. Dasgupta, B. & Milbrandt, J. Resveratrol stimulates AMP kinase activity in neurons. Proceedings of the National Academy of Sciences of the United States of America 104, 7217-7222 (2007).
82. Brunet, A. et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 2011-2015 (2004).
83. Greer, E. L. et al. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17, 1646-1656 (2007).
84. Greer, E. L. et al. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282, 30107-30119 (2007).
85. Jin, T., George Fantus, I. & Sun, J. Wnt and beyond Wnt: multiple mechanisms control the transcriptional property of beta-catenin. Cellular signalling 20, 1697-1704 (2008).
86. Webb, A. E., Kundaje, A. & Brunet, A. Characterization of the direct targets of FOXO transcription factors throughout evolution. Aging Cell 15, 673-685, doi:10.1111/acel.12479 (2016).
87. Renault, V. M. et al. FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5, 527-539, doi:10.1016/j.stem.2009.09.014 (2009).
88. Paik, J. H. et al. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5, 540-553, doi:10.1016/j.stem.2009.09.013 (2009).
89. Kaletsky, R. et al. The C. elegans adult neuronal IIS/FOXO transcriptome reveals adult phenotype regulators. Nature 529, 92-96, doi:10.1038/nature16483 (2016).
90. Salih, D. A. et al. FoxO6 regulates memory consolidation and synaptic function. Genes Dev 26, 2780-2801, doi:10.1101/ gad.208926.112 (2012).
91. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
92. Eisenmann, D. M., Maloof, J. N., Simske, J. S., Kenyon, C. & Kim, S. K. The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. Development (Cambridge, England) 125, 3667-3680 (1998).
93. Ogg, S. et al. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994-999 (1997).
94. Lejeune, F. X. et al. Large-scale functional RNAi screen in C. elegans identifies genes that regulate the dysfunction of mutant polyglutamine neurons. BMC Genomics 13, 91, doi:10.1186/1471-2164-13-91 (2012).
95. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408 (2001).
96. Duerr, J. S. Immunohistochemistry. Wormbook, ed. (2006).
97. Arango, M. et al. CA150 expression delays striatal cell death in overexpression and knock-in conditions for mutant huntingtin neurotoxicity. J Neurosci 26, 4649-4659, doi:10.1523/JNEUROSCI.5409-05.2006 (2006).
98. Lee, I. et al. A single gene network accurately predicts phenotypic effects of gene perturbation in Caenorhabditis elegans. Nat Genet 40, 181-188 (2008).
99. Chew, Y. L., Gotz, J. & Nicholas, H. R. Neuronal protein with tau-like repeats (PTL-1) regulates intestinal SKN-1 nuclear accumulation in response to oxidative stress. Aging Cell 14, 148-151, doi:10.1111/acel.12285 (2015).