Pathways to decoding the clinical potential of stress response FOXO-interaction networks for Huntington's disease: Of gene prioritization and context dependence

Frontiers in Aging Neuroscience

Volumn 5, Issue JUN, 2013, Pages

  Parmentier, Frédéric ^a   Lejeune, François Xavier ^a   Neri, Christian ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

Cellular stress response; Clinical potential; Entropy; FOXO network; Gene prioritization; Huntington's disease; System level approach

Indexed keywords

HUNTINGTIN; TRANSCRIPTION FACTOR FOXO;

ACTIN FILAMENT; ARTICLE; CAUDATE NUCLEUS; CELL CYCLE; CELLULAR STRESS RESPONSE; CHRONIC STRESS; ENTROPY; FOCAL ADHESION; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUNTINGTON CHOREA; NEURAL STEM CELL; NONHUMAN; PATHOGENESIS; PLURIPOTENT STEM CELL; STRESS;

EID: 84883515877     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2013.00022     Document Type: Article

References (60)

1. Anselmi, C. V., Malovini, A., Roncarati, R., Novelli, V., Villa, F., Condorelli, G., et al. (2009). Association of the FOXO3A locus with extreme longevity in a southern Italian centenarian study. Rejuvenation Res. 12, 95-104. doi: 10.1089/rej.2008.0827
2. Bandyopadhyay, S., Mehta, M., Kuo, D., Sung, M. K., Chuang, R., Jaehnig, E. J., et al. (2010). Rewiring of genetic networks in response to DNA damage. Science 330, 1385-1389. doi: 10.1126/science.1195618
3. Borovecki, F., Lovrecic, L., Zhou, J., Jeong, H., Then, F., Rosas, H. D., et al. (2005). Genome-wide expression profiling of human blood reveals biomarkers for Huntington's disease. Proc. Natl. Acad. Sci. U.S.A. 102, 11023-11028. doi: 10.1073/pnas.0504921102
4. Burnett, C., Valentini, S., Cabreiro, F., Goss, M., Somogyvari, M., Piper, M. D., et al. (2011). Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila. Nature 477, 482-485. doi: 10.1038/nature10296
5. Califano, A. (2011). Rewiring makes the difference. Mol. Syst. Biol. 7, 463. doi: 10.1038/msb.2010.117
6. Calixto, A., Jara, J. S., and Court, F. A. (2012). Diapause formation and downregulation of insulin-like signaling via DAF-16/FOXO delays axonal degeneration and neuronal loss. PLoS Genet. 8:e1003141. doi: 10.1371/journal.pgen.1003141
7. Calnan, D. R., and Brunet, A. (2008). The FoxO code. Oncogene 27, 2276-2288. doi: 10.1038/onc.2008.21
8. Catoire, H., Pasco, M. Y., Abu-Baker, A., Holbert, S., Tourette, C., Brais, B., et al. (2008). Sirtuin inhibition protects from the polyalanine muscular dystrophy protein PABPN1. Hum. Mol. Genet. 17, 2108-2117. doi: 10.1093/hmg/ddn109
9. Chiang, W. C., Ching, T. T., Lee, H. C., Mousigian, C., and Hsu, A. L. (2012). HSF-1 regulators DDL-1/2 link insulin-like signaling to heat-shock responses and modulation of longevity. Cell 148, 322-334. doi: 10.1016/j.cell.2011.12.019
10. Christensen, R., De La Torre-Ubieta, L., Bonni, A., and Colon-Ramos, D. A. (2011). A conserved PTEN/FOXO pathway regulates neuronal morphology during C. elegans development. Development 138, 5257-5267. doi: 10.1242/dev.069062
11. 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. doi: 10.1126/science.1124646
12. Cohen, E., Du, D., Joyce, D., Kapernick, E. A., Volovik, Y., Kelly, J. W., et al. (2010). Temporal requirements of insulin/IGF-1 signaling for proteotoxicity protection. Aging Cell 9, 126-134. doi: 10.1111/j.1474-9726.2009.00541.x
13. Cohen, E., Paulsson, J. F., Blinder, P., Burstyn-Cohen, T., Du, D., Estepa, G., et al. (2009). Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139, 1157-1169. doi: 10.1016/j.cell.2009.11.014
14. De La Torre-Ubieta, L., Gaudilliere, B., Yang, Y., Ikeuchi, Y., Yamada, T., Dibacco, S., et al. (2010). A FOXO-Pak1 transcriptional pathway controls neuronal polarity. Genes Dev. 24, 799-813. doi: 10.1101/gad.1880510
15. Eijkelenboom, A., and Burgering, B. M. (2013). FOXOs: signalling integrators for homeostasis maintenance. Nat. Rev. Mol. Cell Biol. 14, 83-97. doi: 10.1038/nrm3507
16. HD iPSC Consortium. (2012). Induced pluripotent stem cells from patients with Huntington's disease show CAG-repeat-expansion-associated phenotypes. Cell Stem Cell 11, 264-278.
17. Flachsbart, F., Caliebe, A., Kleindorp, R., Blanche, H., Von Eller-Eberstein, H., Nikolaus, S., et al. (2009). Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc. Natl. Acad. Sci. U.S.A. 106, 2700-2705. doi: 10.1073/pnas.0809594106
18. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., et al. (2013). STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808-D815. doi: 10.1093/nar/gks1094
19. Freude, S., Hettich, M. M., Schumann, C., Stohr, O., Koch, L., Kohler, C., et al. (2009). Neuronal IGF-1 resistance reduces Abeta accumulation and protects against premature death in a model of Alzheimer's disease. FASEB J. 23, 3315-3324. doi: 10.1096/fj.09-132043
20. Fu, J., Jin, J., Cichewicz, R. H., Hageman, S. A., Ellis, T. K., Xiang, L., et al. (2012). trans-(-)-epsilon-Viniferin increases mitochondrial sirtuin 3 (SIRT3), activates AMP-activated protein kinase (AMPK), and protects cells in models of Huntington Disease. J. Biol. Chem. 287, 24460-24472. doi: 10.1074/jbc.M112.382226
21. Fuhrman, S., Cunningham, M. J., Wen, X., Zweiger, G., Seilhamer, J. J., and Somogyi, R. (2000). The application of shannon entropy in the identification of putative drug targets. Biosystems 55, 5-14. doi: 10.1016/S0303-264700077-5
22. Greer, E. L., and Brunet, A. (2005). FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24, 7410-7425. doi: 10.1038/sj.onc.1209086
23. Hodges, A., Strand, A. D., Aragaki, A. K., Kuhn, A., Sengstag, T., Hughes, G., et al. (2006). Regional and cellular gene expression changes in human Huntington's disease brain. Hum. Mol. Genet. 15, 965-977. doi: 10.1093/hmg/ddl013
24. Kanehisa, M., Goto, S., Kawashima, S., and Nakaya, A. (2002). The KEGG databases at GenomeNet. Nucleic Acids Res. 30, 42-46. doi: 10.1093/nar/30.1.42
25. 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. doi: 10.1038/366461a0
26. Killick, R., Scales, G., Leroy, K., Causevic, M., Hooper, C., Irvine, E. E., et al. (2009). Deletion of Irs2 reduces amyloid deposition and rescues behavioural deficits in APP transgenic mice. Biochem. Biophys. Res. Commun. 386, 257-262. doi: 10.1016/j.bbrc.2009.06.032
27. Kim, D., Nguyen, M. D., Dobbin, M. M., Fischer, A., Sananbenesi, F., Rodgers, J. T., et al. (2007). SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis. EMBO J. 26, 3169-3179. doi: 10.1038/sj.emboj.7601758
28. Jeong, H., Cohen, D. E., Cui, L., Supinski, A., Savas, J. N., Mazzulli, J. R., et al. (2011). Sirt1 mediates neuroprotection from mutant huntingtin by activation of the TORC1 and CREB transcriptional pathway. Nat. Med. 18, 159-165. doi: 10.1038/nm.2559
29. Jiang, M., Wang, J., Fu, J., Du, L., Jeong, H., West, T., et al. (2011). 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
30. Kleindorp, R., Flachsbart, F., Puca, A. A., Malovini, A., Schreiber, S., and Nebel, A. (2011). Candidate gene study of FOXO1, FOXO4, and FOXO6 reveals no association with human longevity in Germans. Aging Cell 10, 622-628. doi: 10.1111/j.1474-9726.2011.00698.x
31. Kuhn, A., Goldstein, D. R., Hodges, A., Strand, A. D., Sengstag, T., Kooperberg, C., et al. (2007). Mutant huntingtin's effects on striatal gene expression in mice recapitulate changes observed in human Huntington's disease brain and do not differ with mutant huntingtin length or wild-type huntingtin dosage. Hum. Mol. Genet. 16, 1845-1861. doi: 10.1093/hmg/ddm133
32. Landis, J. N., and Murphy, C. T. (2010). Integration of diverse inputs in the regulation of Caenorhabditis elegans DAF-16/FOXO. Dev. Dyn. 239, 1405-1412.
33. Lefebvre, C., Rieckhof, G., and Califano, A. (2012). Reverse-enginering human regulatory networks. Wiley Interdiscip. Rev. Syst. Biol. Med. 4, 311-325 doi: 10.1002/wsbm.1159
34. Lejeune, F. X., Mesrob, L., Parmentier, F., Bicep, C., Vazquez-Manrique, R. P., Parker, J. A., et al. (2012). 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
35. Li, Y., Wang, W. J., Cao, H., Lu, J., Wu, C., Hu, F. Y., et al. (2009). Genetic association of FOXO1A and FOXO3A with longevity trait in Han Chinese populations. Hum. Mol. Genet. 18, 4897-4904. doi: 10.1093/hmg/ddp459
36. Mielke, P. W. Jr., and Berry, K. J. (2007). Permutation Methods: a Distance Function Approach. New York, NY: Springer.
37. Mei, Y., Wang, Z., Zhang, L., Zhang, Y., Li, X., Liu, H., et al. (2012). Regulation of neuroblastoma differentiation by forkhead transcription factors FOXO1/3/4 through the receptor tyrosine kinase PDGFRA. Proc. Natl. Acad. Sci. U.S.A. 109, 4898-4903. doi: 10.1073/pnas.1119535109
38. 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 Caenorhabditiselegans. Proc. Natl. Acad. Sci. U.S.A. 16, 16. doi: 10.1073/pnas.152161099
39. Neri, C. (2012). Role and therapeutic potential of the pro-longevity factor FOXO and its regulators in neurodegenerative disease. Front. Pharmacol. 3:15. doi: 10.3389/fphar.2012.00015
40. Orth, M., Handley, O. J., Schwenke, C., Dunnett, S., Wild, E. J., Tabrizi, S. J., et al. (2011). Observing Huntington's disease: the European Huntington's disease network's REGISTRY. J. Neurol. Neurosurg. Psychiatry 82, 1409-1412. doi: 10.1136/jnnp.2010.209668
41. Paik, J. H., Ding, Z., Narurkar, R., Ramkissoon, S., Muller, F., Kamoun, W. S., et al. (2009). FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5, 540-553. doi: 10.1016/j.stem.2009.09.013
42. Parker, J. A., Arango, M., Abderrahmane, S., Lambert, E., Tourette, C., Catoire, H., et al. (2005). Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat. Genet. 37, 349-350. doi: 10.1038/ng1534
43. Parker, J. A., Vazquez-Manrique, R. P., Tourette, C., Farina, F., Offner, N., Mukhopadhyay, A., et al. (2012). 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
44. Pasco, M. Y., Catoire, H., Parker, J. A., Brais, B., Rouleau, G. A., and Neri, C. (2010). Cross-talk between canonical Wnt signaling and the sirtuin-FoxO longevity pathway to protect against muscular pathology induced by mutant PABPN1 expression in C. elegans. Neurobiol. Dis. 38, 425-433. doi: 10.1016/j.nbd.2010.03.002
45. Rapaport, F., Zinovyev, A., Dutreix, M., Barillot, E., and Vert, J. P. (2007). Classification of microarray data using gene networks. BMC Bioinformatics 8:35. doi: 10.1186/1471-2105-8-35
46. Renault, V. M., Rafalski, V. A., Morgan, A. A., Salih, D. A., Brett, J. O., Webb, A. E., et al. (2009). FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5, 527-539. doi: 10.1016/j.stem.2009.09.014
47. Ro, S. H., Liu, D., Yeo, H., and Paik, J. H. (2012). FoxOs in neural stem cell fate decision. Arch. Biochem. Biophys. 534, 55-63. doi: 10.1016/j.abb.2012.07.017
48. Russ, A. P., and Lampel, S. (2005). The druggable genome: an update. Drug Discov. Today 10, 1607-1610. doi: 10.1016/S1359-6446(05)03666-4
49. Salih, D. A., Rashid, A. J., Colas, D., De La Torre-Ubieta, L., Zhu, R. P., Morgan, A. A., et al. (2012). FoxO6 regulates memory consolidation and synaptic function. Genes Dev. 26, 2780-2801. doi: 10.1101/gad.208926.112
50. Shou, C., Bhardwaj, N., Lam, H. Y., Yan, K. K., Kim, P. M., Snyder, M., et al. (2011). Measuring the evolutionary rewiring of biological networks. PLoS Comput. Biol. 7:e1001050. doi: 10.1371/journal.pcbi.1001050
51. Soerensen, M., Dato, S., Christensen, K., McGue, M., Stevnsner, T., Bohr, V. A., et al. (2010). Replication of an association of variation in the FOXO3A gene with human longevity using both case-control and longitudinal data. Aging Cell 9, 1010-1017. doi: 10.1111/j.1474-9726.2010.00627.x
52. Tang, H. Y., Smith-Caldas, M. S., Driscoll, M. V., Salhadar, S., and Shingleton, A. W. (2011). FOXO regulates organ-specific phenotypic plasticity in Drosophila. PLoS Genet. 7:e1002373. doi: 10.1371/journal.pgen.1002373
53. Teixeira-Castro, A., Ailion, M., Jalles, A., Brignull, H. R., Vilaca, J. L., Dias, N., et al. (2011). Neuron-specific proteotoxicity of mutant ataxin-3 in C. elegans: rescue by the DAF-16 and HSF-1 pathways. Hum. Mol. Genet. 20, 2996-3009. doi: 10.1093/hmg/ddr203
54. Thomas, E. A., Coppola, G., Tang, B., Kuhn, A., Kim, S., Geschwind, D. H., et al. (2011). In vivo cell-autonomous transcriptional abnormalities revealed in mice expressing mutant huntingtin in striatal but not cortical neurons. Hum. Mol. Genet. 20, 1049-1060. doi: 10.1093/hmg/ddq548
55. Walker, F. O. (2007). Huntington's disease. Lancet 369, 218-228. doi: 10.1016/S0140-6736(07)60111-1
56. West, J., Bianconi, G., Severini, S., and Teschendorff, A. E. (2012). Differential network entropy reveals cancer system hallmarks. Sci. Rep. 2, 802. doi: 10.1038/srep00802
57. Willcox, B. J., Donlon, T. A., He, Q., Chen, R., Grove, J. S., Yano, K., et al. (2008). FOXO3A genotype is strongly associated with human longevity. Proc. Natl. Acad. Sci. U.S.A. 105, 13987-13992. doi: 10.1073/pnas.0801030105
58. Yen, K., Narasimhan, S. D., and Tissenbaum, H. A. (2011). DAF-16/Forkhead box O transcription factor: many paths to a single Fork(head) in the road. Antioxid. Redox. Signal. 14, 623-634. doi: 10.1089/ars.2010.3490
59. Zhang, T., Mullane, P. C., Periz, G., and Wang, J. (2011). TDP-43 neurotoxicity and protein aggregation modulated by heat shock factor and insulin/IGF-1 signaling. Hum. Mol. Genet. 20, 1952-1965. doi: 10.1093/hmg/ddr076
60. Zuccato, C., Valenza, M., and Cattaneo, E. (2010). Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol. Rev. 90, 905-981. doi: 10.1152/physrev.00041.2009