Motor neurons and glia exhibit specific individualized responses to TDP-43 expression in a Drosophila model of amyotrophic lateral sclerosis

DMM Disease Models and Mechanisms

Volumn 6, Issue 3, 2013, Pages 721-733

  Estes, Patricia S ^a   Daniel, Scott G ^a   Mccallum, Abigail P ^a   Boehringer, Ashley V ^a   Sukhina, Alona S ^a   Zwick, Rebecca A ^a   Zarnescu, Daniela C ^a,b,c  

^a University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TAR DNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DROSOPHILA; GLIA; LOCOMOTION; MISSENSE MUTATION; MOTONEURON; NERVE DEGENERATION; NEUROEPITHELIUM; NEUROMUSCULAR SYNAPSE; NEUROTOXICITY; NONHUMAN; NUCLEAR SHAPE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SLEEP;

AGING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXONS; BIOLOGICAL MARKERS; CELL NUCLEUS; CELL NUCLEUS SHAPE; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; EYE; HUMANS; MOTOR ACTIVITY; MOTOR NEURONS; MUTANT PROTEINS; NERVE DEGENERATION; NEUROEPITHELIAL CELLS; NEUROGLIA; NEUROMUSCULAR JUNCTION; PHENOTYPE; PROTEIN TRANSPORT; SLEEP; SYNAPSES;

EID: 84877832189     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.010710     Document Type: Article

References (60)

1. Alexander, M. D., Traynor, B. J., Miller, N., Corr, B., Frost, E., McQuaid, S., Brett, F. M., Green, A. and Hardiman, O. (2002). "True" sporadic ALS associated with a novel SOD-1 mutation. Ann. Neurol. 52, 680-683.
2. Ayala, Y. M., Misteli, T. and Baralle, F. E. (2008). TDP-43 regulates retinoblastoma protein phosphorylation through the repression of cyclin-dependent kinase 6 expression. Proc. Natl. Acad. Sci. USA 105, 3785-3789.
3. Ayala, Y. M., De Conti, L., Avendaño-Vázquez, S. E., Dhir, A., Romano, M., D'Ambrogio, A., Tollervey, J., Ule, J., Baralle, M., Buratti, E. et al. (2011). TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J. 30, 277-288.
4. Baloh, R. H. (2011). TDP-43: the relationship between protein aggregation and neurodegeneration in amyotrophic lateral sclerosis and frontotemporal lobar degeneration. FEBS J. 278, 3539-3549.
5. Banks, G. T., Kuta, A., Isaacs, A. M. and Fisher, E. M. (2008). TDP-43 is a culprit in human neurodegeneration, and not just an innocent bystander. Mamm. Genome 19, 299-305.
6. Beleza-Meireles, A. and Al-Chalabi, A. (2009). Genetic studies of amyotrophic lateral sclerosis: controversies and perspectives. Amyotroph. Lateral Scler. 10, 1-14.
7. Bronk, P., Nie, Z., Klose, M. K., Dawson-Scully, K., Zhang, J., Robertson, R. M., Atwood, H. L. and Zinsmaier, K. E. (2005). The multiple functions of cysteine-string protein analyzed at Drosophila nerve terminals. J. Neurosci. 25, 2204-2214.
8. Buratti, E. and Baralle, F. E. (2001). Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. J. Biol. Chem. 276, 36337-36343.
9. Carpenter, A. E., Jones, T. R., Lamprecht, M. R., Clarke, C., Kang, I. H., Friman, O., Guertin, D. A., Chang, J. H., Lindquist, R. A., Moffat, J. et al. (2006). CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 7, R100.
10. Colombrita, C., Onesto, E., Tiloca, C., Ticozzi, N., Silani, V. and Ratti, A. (2011). RNA-binding proteins and RNA metabolism: a new scenario in the pathogenesis of Amyotrophic lateral sclerosis. Arch. Ital. Biol. 149, 83-99.
11. Couthouis, J., Hart, M. P., Shorter, J., DeJesus-Hernandez, M., Erion, R., Oristano, R., Liu, A. X., Ramos, D., Jethava, N., Hosangadi, D. et al. (2011). A yeast functional screen predicts new candidate ALS disease genes. Proc. Natl. Acad. Sci. USA 108, 20881-20890.
12. Dahl, K. N., Ribeiro, A. J. and Lammerding, J. (2008). Nuclear shape, mechanics, and mechanotransduction. Circ. Res. 102, 1307-1318.
13. DeJesus-Hernandez, M., Mackenzie, I. R., Boeve, B. F., Boxer, A. L., Baker, M., Rutherford, N. J., Nicholson, A. M., Finch, N. A., Flynn, H., Adamson, J. et al. (2011). Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72, 245-256.
14. Dewey, C. M., Cenik, B., Sephton, C. F., Dries, D. R., Mayer, P., 3rd, Good, S. K., Johnson, B. A., Herz, J. and Yu, G. (2011). TDP-43 is directed to stress granules by sorbitol, a novel physiological osmotic and oxidative stressor. Mol. Cell. Biol. 31, 1098-1108.
15. Dormann, D. and Haass, C. (2011). TDP-43 and FUS: a nuclear affair. Trends Neurosci. 34, 339-348.
16. Estes, P. S., O'Shea, M., Clasen, S. and Zarnescu, D. C. (2008). Fragile X protein controls the efficacy of mRNA transport in Drosophila neurons. Mol. Cell. Neurosci. 39, 170-179.
17. Estes, P. S., Boehringer, A., Zwick, R., Tang, J. E., Grigsby, B. and Zarnescu, D. C. (2011). Wild-type and A315T mutant TDP-43 exert differential neurotoxicity in a Drosophila model of ALS. Hum. Mol. Genet. 20, 2308-2321.
18. Fallini, C., Bassell, G. J. and Rossoll, W. (2012). The ALS disease protein TDP-43 is actively transported in motor neuron axons and regulates axon outgrowth. Hum. Mol. Genet. 21, 3703-3718.
19. Feiguin, F., Godena, V. K., Romano, G., D'Ambrogio, A., Klima, R. and Baralle, F. E. (2009). Depletion of TDP-43 affects Drosophila motoneurons terminal synapsis and locomotive behavior. FEBS Lett. 583, 1586-1592.
20. Fiesel, F. C. and Kahle, P. J. (2011). TDP-43 and FUS/TLS: cellular functions and implications for neurodegeneration. FEBS J. 278, 3550-3568.
21. Freibaum, B. D., Chitta, R. K., High, A. A. and Taylor, J. P. (2010). Global analysis of TDP-43 interacting proteins reveals strong association with RNA splicing and translation machinery. J. Proteome Res. 9, 1104-1120.
22. Fuentes-Medel, Y., Logan, M. A., Ashley, J., Ataman, B., Budnik, V. and Freeman, M. R. (2009). Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris. PLoS Biol. 7, e1000184.
23. Gilestro, G. F. and Cirelli, C. (2009). pySolo: a complete suite for sleep analysis in Drosophila. Bioinformatics 25, 1466-1467.
24. Gustafson, K. and Boulianne, G. L. (1996). Distinct expression patterns detected within individual tissues by the GAL4 enhancer trap technique. Genome 39, 174-182.
25. Ince, P. G., Highley, J. R., Kirby, J., Wharton, S. B., Takahashi, H., Strong, M. J. and Shaw, P. J. (2011). Molecular pathology and genetic advances in amyotrophic lateral sclerosis: an emerging molecular pathway and the significance of glial pathology. Acta Neuropathol. 122, 657-671.
26. Johnson, B. S., McCaffery, J. M., Lindquist, S. and Gitler, A. D. (2008). A yeast TDP-43 proteinopathy model: Exploring the molecular determinants of TDP-43 aggregation and cellular toxicity. Proc. Natl. Acad. Sci. USA 105, 6439-6444.
27. Kabashi, E., Valdmanis, P. N., Dion, P., Spiegelman, D., McConkey, B. J., Vande Velde, C., Bouchard, J. P., Lacomblez, L., Pochigaeva, K., Salachas, F. et al. (2008). TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 40, 572-574.
28. Kittel, R. J., Wichmann, C., Rasse, T. M., Fouquet, W., Schmidt, M., Schmid, A., Wagh, D. A., Pawlu, C., Kellner, R. R., Willig, K. I. et al. (2006). Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312, 1051-1054.
29. Koh, Y. H., Gramates, L. S. and Budnik, V. (2000). Drosophila larval neuromuscular junction: molecular components and mechanisms underlying synaptic plasticity. Microsc. Res. Tech. 49, 14-25.
30. Kwiatkowski, T. J., Jr, Bosco, D. A., Leclerc, A. L., Tamrazian, E., Vanderburg, C. R., Russ, C., Davis, A., Gilchrist, J., Kasarskis, E. J., Munsat, T. et al. (2009). Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323, 1205-1208.
31. Lagier-Tourenne, C. and Cleveland, D. W. (2009). Rethinking ALS: the FUS about TDP-43. Cell 136, 1001-1004.
32. Lanson, N. A., Jr, Maltare, A., King, H., Smith, R., Kim, J. H., Taylor, J. P., Lloyd, T. E., and Pandey, U. B. (2011). A Drosophila model of FUS-related neurodegeneration reveals genetic interaction between FUS and TDP-43. Hum. Mol. Genet. 20, 2510-2523.
33. Li, Y., Ray, P., Rao, E. J., Shi, C., Guo, W., Chen, X., Woodruff, E. A., 3rd, Fushimi, K. and Wu, J. Y. (2010). A Drosophila model for TDP-43 proteinopathy. Proc. Natl. Acad. Sci. USA 107, 3169-3174.
34. Liachko, N. F., Guthrie, C. R. and Kraemer, B. C. (2010). Phosphorylation promotes neurotoxicity in a Caenorhabditis elegans model of TDP-43 proteinopathy. J. Neurosci. 30, 16208-16219.
35. Liu-Yesucevitz, L., Bilgutay, A., Zhang, Y. J., Vanderweyde, T., Citro, A., Mehta, T., Zaarur, N., McKee, A., Bowser, R., Sherman, M. et al. (2010). Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLoS ONE 5, e13250.
36. Lo Coco, D., Mattaliano, P., Spataro, R., Mattaliano, A. and La Bella, V. (2011). Sleep-wake disturbances in patients with amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 82, 839-842.
37. Lu, Y., Ferris, J. and Gao, F. B. (2009). Frontotemporal dementia and amyotrophic lateral sclerosis-associated disease protein TDP-43 promotes dendritic branching. Mol. Brain 2, 30.
38. Maekawa, S., Leigh, P. N., King, A., Jones, E., Steele, J. C., Bodi, I., Shaw, C. E., Hortobagyi, T. and Al-Sarraj, S. (2009). TDP-43 is consistently co-localized with ubiquitinated inclusions in sporadic and Guam amyotrophic lateral sclerosis but not in familial amyotrophic lateral sclerosis with and without SOD1 mutations. Neuropathology 29, 672-683.
39. Marrus, S. B. and DiAntonio, A. (2004). Preferential localization of glutamate receptors opposite sites of high presynaptic release. Curr. Biol. 14, 924-931.
40. McDonald, K. K., Aulas, A., Destroismaisons, L., Pickles, S., Beleac, E., Camu, W., Rouleau, G. A. and Vande Velde, C. (2011). TAR DNA-binding protein 43 (TDP-43) regulates stress granule dynamics via differential regulation of G3BP and TIA-1. Hum. Mol. Genet. 20, 1400-1410.
41. Neumann, M. (2009). Molecular neuropathology of TDP-43 proteinopathies. Int. J. Mol. Sci. 10, 232-246.
42. Neumann, M., Sampathu, D. M., Kwong, L. K., Truax, A. C., Micsenyi, M. C., Chou, T. T., Bruce, J., Schuck, T., Grossman, M., Clark, C. M. et al. (2006). Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130-133.
43. Parker, S. J., Meyerowitz, J., James, J. L., Liddell, J. R., Crouch, P. J., Kanninen, K. M. and White, A. R. (2012). Endogenous TDP-43 localized to stress granules can subsequently form protein aggregates. Neurochem. Int. 60, 415-424.
44. Polymenidou, M., Lagier-Tourenne, C., Hutt, K. R., Huelga, S. C., Moran, J., Liang, T. Y., Ling, S. C., Sun, E., Wancewicz, E., Mazur, C. et al. (2011). Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat. Neurosci. 14, 459-468.
45. Renton, A. E., Majounie, E., Waite, A., Simón-Sánchez, J., Rollinson, S., Gibbs, J. R., Schymick, J. C., Laaksovirta, H., van Swieten, J. C., Myllykangas, L. et al. (2011). A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72, 257-268.
46. Rutherford, N. J., Zhang, Y. J., Baker, M., Gass, J. M., Finch, N. A., Xu, Y. F., Stewart, H., Kelley, B. J., Kuntz, K., Crook, R. J. et al. (2008). Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. PLoS Genet. 4, e1000193.
47. Sehgal, A. and Mignot, E. (2011). Genetics of sleep and sleep disorders. Cell 146, 194-207.
48. Sephton, C. F., Cenik, C., Kucukural, A., Dammer, E. B., Cenik, B., Han, Y., Dewey, C. M., Roth, F. P., Herz, J., Peng, J. et al. (2011). Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J. Biol. Chem. 286, 1204-1215.
49. Sreedharan, J., Blair, I. P., Tripathi, V. B., Hu, X., Vance, C., Rogelj, B., Ackerley, S., Durnall, J. C., Williams, K. L., Buratti, E. et al. (2008). TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319, 1668-1672.
50. Tan, C. F., Eguchi, H., Tagawa, A., Onodera, O., Iwasaki, T., Tsujino, A., Nishizawa, M., Kakita, A. and Takahashi, H. (2007). TDP-43 immunoreactivity in neuronal inclusions in familial amyotrophic lateral sclerosis with or without SOD1 gene mutation. Acta Neuropathol. 113, 535-542.
51. Tollervey, J. R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., König, J., Hortobágyi, T., Nishimura, A. L., Zupunski, V. et al. (2011). Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci. 14, 452-458.
52. Vance, C., Rogelj, B., Hortobágyi, T., De Vos, K. J., Nishimura, A. L., Sreedharan, J., Hu, X., Smith, B., Ruddy, D., Wright, P. et al. (2009). Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323, 1208-1211.
53. Voigt, A., Herholz, D., Fiesel, F. C., Kaur, K., Müller, D., Karsten, P., Weber, S. S., Kahle, P. J., Marquardt, T. and Schulz, J. B. (2010). TDP-43-mediated neuron loss in vivo requires RNA-binding activity. PLoS ONE 5, e12247.
54. Vucic, S., Nicholson, G. A. and Kiernan, M. C. (2008). Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain 131, 1540-1550.
55. Wagh, D. A., Rasse, T. M., Asan, E., Hofbauer, A., Schwenkert, I., Dürrbeck, H., Buchner, S., Dabauvalle, M. C., Schmidt, M., Qin, G. et al. (2006). Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49, 833-844.
56. Wang, I. F., Wu, L. S., Chang, H. Y. and Shen, C. K. (2008). TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J. Neurochem. 105, 797-806.
57. Wegorzewska, I., Bell, S., Cairns, N. J., Miller, T. M. and Baloh, R. H. (2009). TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc. Natl. Acad. Sci. USA 106, 18809-18814.
58. Wu, C. H., Fallini, C., Ticozzi, N., Keagle, P. J., Sapp, P. C., Piotrowska, K., Lowe, P., Koppers, M., McKenna-Yasek, D., Baron, D. M. et al. (2012). Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 488, 499-503.
59. Xiong, W. C., Okano, H., Patel, N. H., Blendy, J. A. and Montell, C. (1994). repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 8, 981-994.
60. Yu, Z., Fan, D., Gui, B., Shi, L., Xuan, C., Shan, L., Wang, Q., Shang, Y. and Wang, Y. (2012). Neurodegeneration-associated TDP-43 interacts with fragile X mental retardation protein (FMRP)/Staufen (STAU1) and regulates SIRT1 expression in neuronal cells. J. Biol. Chem. 287, 22560-22572.