Age-dependent TDP-43-mediated motor neuron degeneration requires GSK3, hat-trick, and xmas-2

Current Biology

Volumn 25, Issue 16, 2015, Pages 2130-2136

  Sreedharan, Jemeen ^a,b   Neukomm, Lukas J ^a   Brown, Robert H ^a   Freeman, Marc R ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

WALLERIA;

DNA BINDING PROTEIN; DROSOPHILA PROTEIN; TBPH PROTEIN, DROSOPHILA;

AGING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL; DISEASE MODEL; DROSOPHILA MELANOGASTER; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; LARVA; METABOLISM; MOTONEURON; NERVE DEGENERATION; PATHOPHYSIOLOGY; PHYSIOLOGY;

AGING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HUMANS; LARVA; MOTOR NEURONS; NERVE DEGENERATION;

EID: 84939563998     PISSN: 09609822     EISSN: 18790445     Source Type: Journal    
DOI: 10.1016/j.cub.2015.06.045     Document Type: Article

References (47)

1. M. Neumann, D.M. Sampathu, L.K. Kwong, A.C. Truax, M.C. Micsenyi, T.T. Chou, J. Bruce, T. Schuck, M. Grossman, C.M. Clark, and et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Science 314 2006 130 133
2. T. Arai, M. Hasegawa, H. Akiyama, K. Ikeda, T. Nonaka, H. Mori, D. Mann, K. Tsuchiya, M. Yoshida, Y. Hashizume, and T. Oda TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Biochem. Biophys. Res. Commun. 351 2006 602 611
3. J. Sreedharan, I.P. Blair, V.B. Tripathi, X. Hu, C. Vance, B. Rogelj, S. Ackerley, J.C. Durnall, K.L. Williams, E. Buratti, and et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis Science 319 2008 1668 1672
4. E. Kabashi, P.N. Valdmanis, P. Dion, D. Spiegelman, B.J. McConkey, C. Vande Velde, J.P. Bouchard, L. Lacomblez, K. Pochigaeva, F. Salachas, and et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis Nat. Genet. 40 2008 572 574
5. I. Casci, and U.B. Pandey A fruitful endeavor: modeling ALS in the fruit fly Brain Res. 1607 2015 47 74
6. P. Cohen, and M. Goedert GSK3 inhibitors: development and therapeutic potential Nat. Rev. Drug Discov. 3 2004 479 487
7. A. Chesi, B.T. Staahl, A. Jovičić, J. Couthouis, M. Fasolino, A.R. Raphael, T. Yamazaki, L. Elias, M. Polak, C. Kelly, and et al. Exome sequencing to identify de novo mutations in sporadic ALS trios Nat. Neurosci. 16 2013 851 855
8. H.M. Kaneb, A.W. Folkmann, V.V. Belzil, L.E. Jao, C.S. Leblond, S.L. Girard, H. Daoud, A. Noreau, D. Rochefort, P. Hince, and et al. Deleterious mutations in the essential mRNA metabolism factor, hGle1, in amyotrophic lateral sclerosis Hum. Mol. Genet. 24 2014 1363 1373
9. Y. Li, P. Ray, E.J. Rao, C. Shi, W. Guo, X. Chen, E.A. Woodruff 3rd, K. Fushimi, and J.Y. Wu A Drosophila model for TDP-43 proteinopathy Proc. Natl. Acad. Sci. USA 107 2010 3169 3174
10. J.W. Wang, J.R. Brent, A. Tomlinson, N.A. Shneider, and B.D. McCabe The ALS-associated proteins FUS and TDP-43 function together to affect Drosophila locomotion and life span J. Clin. Invest. 121 2011 4118 4126
11. L. Miguel, T. Frébourg, D. Campion, and M. Lecourtois Both cytoplasmic and nuclear accumulations of the protein are neurotoxic in Drosophila models of TDP-43 proteinopathies Neurobiol. Dis. 41 2011 398 406
12. K. Koles, and V. Budnik Wnt signaling in neuromuscular junction development Cold Spring Harb. Perspect. Biol. 4 2012 a008045
13. T. Lee, and L. Luo Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis Neuron 22 1999 451 461
14. A. Schmid, S. Hallermann, R.J. Kittel, O. Khorramshahi, A.M. Frölich, C. Quentin, T.M. Rasse, S. Mertel, M. Heckmann, and S.J. Sigrist Activity-dependent site-specific changes of glutamate receptor composition in vivo Nat. Neurosci. 11 2008 659 666
15. M. Baek, and R.S. Mann Lineage and birth date specify motor neuron targeting and dendritic architecture in adult Drosophila J. Neurosci. 29 2009 6904 6916
16. L.J. Neukomm, T.C. Burdett, M.A. Gonzalez, S. Züchner, and M.R. Freeman Rapid in vivo forward genetic approach for identifying axon death genes in Drosophila Proc. Natl. Acad. Sci. USA 111 2014 9965 9970
17. R.J. Kittel, C. Wichmann, T.M. Rasse, W. Fouquet, M. Schmidt, A. Schmid, D.A. Wagh, C. Pawlu, R.R. Kellner, K.I. Willig, and et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release Science 312 2006 1051 1054
18. W. Tsao, Y.H. Jeong, S. Lin, J. Ling, D.L. Price, P.M. Chiang, and P.C. Wong Rodent models of TDP-43: recent advances Brain Res. 1462 2012 26 39
19. D.C. Diaper, Y. Adachi, B. Sutcliffe, D.M. Humphrey, C.J. Elliott, A. Stepto, Z.N. Ludlow, L. Vanden Broeck, P. Callaerts, B. Dermaut, and et al. Loss and gain of Drosophila TDP-43 impair synaptic efficacy and motor control leading to age-related neurodegeneration by loss-of-function phenotypes Hum. Mol. Genet. 22 2013 1539 1557
20. Y. Lu, J. Ferris, and F.B. Gao Frontotemporal dementia and amyotrophic lateral sclerosis-associated disease protein TDP-43 promotes dendritic branching Mol. Brain 2 2009 30
21. A. Voigt, D. Herholz, F.C. Fiesel, K. Kaur, D. Müller, P. Karsten, S.S. Weber, P.J. Kahle, T. Marquardt, and J.B. Schulz TDP-43-mediated neuron loss in vivo requires RNA-binding activity PLoS ONE 5 2010 e12247
22. L.R. Fischer, D.G. Culver, P. Tennant, A.A. Davis, M. Wang, A. Castellano-Sanchez, J. Khan, M.A. Polak, and J.D. Glass Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man Exp. Neurol. 185 2004 232 240
23. M.P. Coleman, and M.R. Freeman Wallerian degeneration, wld(s), and nmnat Annu. Rev. Neurosci. 33 2010 245 267
24. T.G. Mack, M. Reiner, B. Beirowski, W. Mi, M. Emanuelli, D. Wagner, D. Thomson, T. Gillingwater, F. Court, L. Conforti, and et al. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene Nat. Neurosci. 4 2001 1199 1206
25. J.M. MacDonald, M.G. Beach, E. Porpiglia, A.E. Sheehan, R.J. Watts, and M.R. Freeman The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons Neuron 50 2006 869 881
26. J.M. Osterloh, J. Yang, T.M. Rooney, A.N. Fox, R. Adalbert, E.H. Powell, A.E. Sheehan, M.A. Avery, R. Hackett, M.A. Logan, and et al. dSarm/Sarm1 is required for activation of an injury-induced axon death pathway Science 337 2012 481 484
27. X. Xiong, Y. Hao, K. Sun, J. Li, X. Li, B. Mishra, P. Soppina, C. Wu, R.I. Hume, and C.A. Collins The Highwire ubiquitin ligase promotes axonal degeneration by tuning levels of Nmnat protein PLoS Biol. 10 2012 e1001440
28. E. Babetto, B. Beirowski, E.V. Russler, J. Milbrandt, and A. DiAntonio The Phr1 ubiquitin ligase promotes injury-induced axon self-destruction Cell Rep. 3 2013 1422 1429
29. A. Ferri, J.R. Sanes, M.P. Coleman, J.M. Cunningham, and A.C. Kato Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease Curr. Biol. 13 2003 669 673
30. A. Sajadi, B.L. Schneider, and P. Aebischer Wlds-mediated protection of dopaminergic fibers in an animal model of Parkinson disease Curr. Biol. 14 2004 326 330
31. G.R. Howell, R.T. Libby, T.C. Jakobs, R.S. Smith, F.C. Phalan, J.W. Barter, J.M. Barbay, J.K. Marchant, N. Mahesh, V. Porciatti, and et al. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma J. Cell Biol. 179 2007 1523 1537
32. L.R. Fischer, D.G. Culver, A.A. Davis, P. Tennant, M. Wang, M. Coleman, S. Asress, R. Adalbert, G.M. Alexander, and J.D. Glass The WldS gene modestly prolongs survival in the SOD1G93A fALS mouse Neurobiol. Dis. 19 2005 293 300
33. C. Vande Velde, M.L. Garcia, X. Yin, B.D. Trapp, and D.W. Cleveland The neuroprotective factor Wlds does not attenuate mutant SOD1-mediated motor neuron disease Neuromolecular Med. 5 2004 193 203
34. S. Yamamoto, M. Jaiswal, W.L. Charng, T. Gambin, E. Karaca, G. Mirzaa, W. Wiszniewski, H. Sandoval, N.A. Haelterman, B. Xiong, and et al. A Drosophila genetic resource of mutants to study mechanisms underlying human genetic diseases Cell 159 2014 200 214
35. B. Franco, L. Bogdanik, Y. Bobinnec, A. Debec, J. Bockaert, M.L. Parmentier, and Y. Grau Shaggy, the homolog of glycogen synthase kinase 3, controls neuromuscular junction growth in Drosophila J. Neurosci. 24 2004 6573 6577
36. M. Bourouis, P. Moore, L. Ruel, Y. Grau, P. Heitzler, and P. Simpson An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2+ subfamily EMBO J. 9 1990 2877 2884
37. S.S. Ambegaokar, and G.R. Jackson Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation Hum. Mol. Genet. 20 2011 4947 4977
38. D. Moujalled, J.L. James, S.J. Parker, G.E. Lidgerwood, C. Duncan, J. Meyerowitz, T. Nonaka, M. Hasegawa, K.M. Kanninen, A. Grubman, and et al. Kinase inhibitor screening identifies cyclin-dependent kinases and glycogen synthase kinase 3 as potential modulators of TDP-43 cytosolic accumulation during cell stress PLoS ONE 8 2013 e67433
39. Y.M. Yang, S.K. Gupta, K.J. Kim, B.E. Powers, A. Cerqueira, B.J. Wainger, H.D. Ngo, K.A. Rosowski, P.A. Schein, C.A. Ackeifi, and et al. A small molecule screen in stem-cell-derived motor neurons identifies a kinase inhibitor as a candidate therapeutic for ALS Cell Stem Cell 12 2013 713 726
40. R. Stoica, K.J. De Vos, S. Paillusson, S. Mueller, R.M. Sancho, K.F. Lau, G. Vizcay-Barrena, W.L. Lin, Y.F. Xu, J. Lewis, and et al. ER-mitochondria associations are regulated by the VAPB-PTPIP51 interaction and are disrupted by ALS/FTD-associated TDP-43 Nat. Commun. 5 2014 3996
41. R.C. Wu, M. Jiang, A.L. Beaudet, and M.Y. Wu ARID4A and ARID4B regulate male fertility, a functional link to the AR and RB pathways Proc. Natl. Acad. Sci. USA 110 2013 4616 4621
42. S. Ranganathan, and R. Bowser Alterations in G(1) to S phase cell-cycle regulators during amyotrophic lateral sclerosis Am. J. Pathol. 162 2003 823 835
43. N.F. Liachko, P.J. McMillan, C.R. Guthrie, T.D. Bird, J.B. Leverenz, and B.C. Kraemer CDC7 inhibition blocks pathological TDP-43 phosphorylation and neurodegeneration Ann. Neurol. 74 2013 39 52
44. L.M. Igaz, L.K. Kwong, E.B. Lee, A. Chen-Plotkin, E. Swanson, T. Unger, J. Malunda, Y. Xu, M.J. Winton, J.Q. Trojanowski, and V.M. Lee Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice J. Clin. Invest. 121 2011 726 738
45. C.A. Konopka, M.N. Locke, P.S. Gallagher, N. Pham, M.P. Hart, C.J. Walker, A.D. Gitler, and R.G. Gardner A yeast model for polyalanine-expansion aggregation and toxicity Mol. Biol. Cell 22 2011 1971 1984
46. V.O. Wickramasinghe, P.I. McMurtrie, A.D. Mills, Y. Takei, S. Penrhyn-Lowe, Y. Amagase, S. Main, J. Marr, M. Stewart, and R.A. Laskey mRNA export from mammalian cell nuclei is dependent on GANP Curr. Biol. 20 2010 25 31
47. S. Wakatsuki, F. Saitoh, and T. Araki ZNRF1 promotes Wallerian degeneration by degrading AKT to induce GSK3B-dependent CRMP2 phosphorylation Nat. Cell Biol. 13 2011 1415 1423