Motor neuron expression of the voltage-gated calcium channel cacophony restores locomotion defects in a Drosophila, TDP-43 loss of function model of ALS

Brain Research

Volumn 1584, Issue , 2014, Pages 39-51

  Chang, Jer Cherng ^a   Hazelett, Dennis J ^a   Stewart, Judith A ^a   Morton, David B ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

ALS; Cacophony; Calcium channel; Drosophila; Neurodegeneration; TDP 43

Indexed keywords

CACOPHONY; TAR DNA BINDING PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; CAC PROTEIN, DROSOPHILA; CALCIUM CHANNEL; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; TBPH PROTEIN, DROSOPHILA;

ADULT; ALTERNATIVE RNA SPLICING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EXON; GENE MUTATION; IMMUNOPRECIPITATION; LOCOMOTION; MOTONEURON; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; DISEASE MODEL; GENETICS; METABOLISM; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ALTERNATIVE SPLICING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CALCIUM CHANNELS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MOTOR ACTIVITY; MOTOR NEURONS; NEUROMUSCULAR JUNCTION;

EID: 84907697655     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.11.019     Document Type: Article

References (39)

1. P.J. Adams, E. Garcia, L.S. David, K.J. Mulatz, S.D. Spacey, and T.P. Snutch Ca(V)2.1 P/Q-type calcium channel alternative splicing affects the functional impact of familial hemiplegic migraine mutations: implications for calcium channelopathies Channels 3 2009 110 121
2. 2+ channels and spinal analgesia couple to alternative splicing Nat. Neurosci. 13 2010 1249 1256
3. 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
4. G.A.B. Armstrong, and P. Drapeau Calcium channel agonists protect against neuromuscular dysfunction in a genetic model of TDP-43 mutation in ALS J. Neurosci. 33 2013 1741 1752
5. Y.M. Ayala, L. De Conti, S.E. Avendaño-Vázquez, A. Dhir, M. Romano, A. D'Ambrogio, J. Tollervey, J. Ule, M. Baralle, E. Buratti, and F.E. Baralle TDP-43 regulates its mRNA levels through a negative feedback loop EMBO J. 30 2011 277 288
6. E. Buratti, and F.E. Baralle Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, novel splicing regulator of CFTR exon 9 J. Biol. Chem. 276 2001 36337 36343
7. E Buratti, and F.E. Baralle The multiple roles of TDP-43 in pre-mRNA processing and gene expression regulation RNA Biol. 7 2010 420 429
8. E. Buratti, and F.E. Baralle TDP-43: gumming up neurons through protein-protein and protein-RNA interactions Trends Biochem. Sci. 37 2012 237 247
9. D.C. Diaper, Y. Adachi, B. Sutcliffe, B.M. Humphrey, C.J.H. Elliott, A. Stepto, Z.N. Ludlow, L. Vanden Broeck, P. Callaerts, B. Dermaut, A. Al-Chalabi, C.E. Shaw, I.M. Robinson, and F. Hirth 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
10. F. Feiguin, V.K. Godena, G. Romano, A. D'Ambrogio, R. Klima, and F.E. Baralle Depletion of TDP-43 affects Drosophila motor neurons terminals synapsis and locomotive behavior FEBS Lett. 583 2009 1586 1592
11. F.C. Fiesel, and P.J. Kahle TDP-43 and FUS/TLS: cellular functions and implications for neurodegeneration FEBS J. 278 2011 3550 3568
12. F.C. Fiesel, S.S. Weber, J. Supper, A. Zell, and P.J. Kahle TDP-43 regulates global translational yield by splicing of exon junction complex component SKAR Nucleic Acids Res. 40 2012 2668 2682
13. F. Geser, M. Martinez-Lage, J. Robinson, K. Uryu, M. Neumann, N.J. Brandmeir, S.X. Xie, L.K. Kwong, L. Elman, L. McCluskey, C.M. Clark, J. Malunda, B.L. Miller, E.A. Zimmerman, J. Qian, V. Van Deerlin, M. Grossman, V.M.-Y. Lee, and J.Q. Trojanowski Clinical and pathological continuum of multisystem TDP-43 proteinopathies Arch. Neurol. 66 2009 180 189
14. M.A. Gitcho, R.H. Baloh, S. Chakraverty, K. Mayo, J.B. Norton, D. Levitch, K.J. Hatanpaa, C.L. White, E.H. Bigio, R. Caselli, M. Baker, M.T. Al-Lozi, J.C. Morris, A. Pestronk, R. Rademakers, A.M. Goate, and N.J. Cairns TDP-43 A315T mutation in familial motor neuron disease Ann. Neurol. 63 2008 535 538
15. R.J. Greenspan Fly Pushing Ed. 2 2004 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
16. H. Gu, S.A. Jiang, J.M. Campusano, J. Iniguez, H. Su, A.A. Hoang, M. Lavian, X. Sun, and D.K. O'Dowd Cav2-type calcium channels encoded by cac regulate AP-independent neurotransmitter release at cholinergic synapses in adult Drosophila brain J. Neurophysiol. 101 2009 42 53
17. D.J. Hazelett, J.-C. Chang, D.L. Lakeland, and D.B. Morton Comparison of parallel hi-throughput RNA-sequencing between knockout of TDP-43 and its overexpression reveals primarily non-reciprocal and non-overlapping gene expression changes in the central nervous system of Drosophila G3:Genes, Genomes, Genet. 2 2012 789 802
18. E. Kabashi, P.N. Valdmanis, P. Dion, D. Spiegelman, B.J. McConkey, C. Vande Velde, J.P. Bouchard, L. Lacomblez, K. Pochigaeva, F. Salachas, P.F. Pradat, W. Camu, V. Meininger, N. Dupre, and G.A. Rouleau TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis Nat. Genet. 40 5 2008 572 574
19. F. Kawasaki, S.C. Collins, and R.W. Ordway Synaptic calcium-channel function in Drosophila: analysis and transformation rescue of temperature-sensitive paralytic and lethal mutations of cacophony J. Neurosci. 22 2002 5856 5864
20. F. Kawasaki, B. Zou, X. Xu, and R.W. Ordway Active zone localization of presynaptic calcium channels encoded by the cacophony locus of Drosophila J. Neurosci. 24 2004 282 285
21. 2+ channel clustering, and vesicle release Science 312 2006 1051 1054
22. A.M. Krecic, and M.S. Swanson hnRNP complexes: composition, structure, and function Curr. Opin. Cell Biol. 11 1999 363 371
23. P. Kurdyak, H.L. Atwood, B.A. Stewart, and C.-F. Wu Differential physiology and morphology of motor axons to ventral longtitudinal muscles in larval Drosophila J. Comp. Neurol. 350 1994 463 472
24. E.B. Lee, V.M.-Y. Lee, and J.Q. Trojanowski Gains and losses: molecular mechanisms of TDP43-mediated neurodegeneration Nat. Rev. Neurosci. 13 2012 38 50
25. D. Lipscombe, S.E. Allen, and C.P. Toro Control of neuronal voltage-gated calcium ion channels from RNA to protein Trends Neurosci. 36 2013 598 609
26. D. Lipscombe, A. Andrade, and S.E. Allen Alternative splicing: functional diversity among voltage-gated calcium channels and behavioral consequences Biochim. Biophys. Acta 1828 2013 1522 1529
27. V2.1 channel inactivation Eur. J. Neurosci. 23 2006 3230 3244
28. M. Neumann, D.M. Samputhu, L.K. Kwong, A.K. Truax, M.C. Micsenyi, T.T. Chou, J. Bruce, T. Schuck, M. Grossman, C.M. Clark, L.F. McCluskey, B.L. Miller, E. Masliah, I.R. Mackenzie, H. Feldman, W. Feiden, H.A. Kretzschmar, J.Q. Trojanowski, and V.M.-Y. Lee Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Science 314 2006 130 133
29. S.H. Ou, F. Wu, D. Harrich, L.F. Garcia-Martinez, and R.B. Gaynor Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs J Virol. 69 1995 3584 3596
30. + channel homeostatic regulation J. Neurosci. 27 2007 1072 1081
31. M. Polymenidou, C. Lagieer-Tourenne, K. Hutt, S.C. Huelga, J. Moran, T.Y. Liang, S.C. Ling, E. Sun, E. Wancewicz, H. Kordasiewicz, Y. Sedaghat, J.P. Donohue, L. Shiue, C.F. Bennett, G.W. Yeo, and D.W. Cleveland Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43 Nat. Neurosci. 14 2011 459 468
32. G.E. Rieckhof, M. Yoshihara, Z. Guan, and J.T. Littleton Presynaptic N-type calcium channels regulate synaptic growth J. Biol. Chem. 278 2003 41099 41108
33. C.F. Sephton, C. Cenik, A. Kucukural, E.B. Dammer, and B. Cenik Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes J. Biol. Chem. 286 2011 1204 1215
34. I. Splawski, K.W. Timothy, L.M. Sharpe, N. Decher, P. Kumar, R. Bloise, C. Napolitano, P.J. Schwartz, R.M. Joseph, K. Condouris, H. Tager-Flusberg, S.G. Priori, M.C. Sanguinetti, and M.T. Keating Ca(V)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism Cell 119 2004 19 31
35. J. Sreedharan, I.P. Blair, V.B. Tripathi, X. Hu, C. Vance, B. Rogelj, S. Ackerley, J.C. Durnall, K.L. Williams, E. Buratti, F. Baralle, J. de Belleroche, and J.D. Mitchell TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis Science 319 5870 2008 1668 1672
36. M.R. Turner, O. Hardiman, M. Benatar, B.R. Brooks, Chio, A.M. de Carvalho, P.G. Ince, C. Lin, R.G. Miller, H. Mitsumoto, G. Nicholson, J. Ravits, P.J. Shaw, M. Swash, K. Talbot, B.J. Traynor, L.H. Van den Berg, J.H. Veldink, S. Vucic, and M.C. Kiernan Controversies and priorities in amyotrophic lateral sclerosis Lancet Neurol. 12 2013 310 322
37. K. Volkening, C. Leystra-Lantz, W. Yang, H. Jaffee, and M.J. Strong Tar DNA binding protein of 43 kDa (TDP-43), 14-3-3 proteins and copper/zinc superoxide dismutase (SOD1) interact to modulate NFL mRNA stability. Implications for altered RNA processing in amyotrophic lateral sclerosis (ALS) Brain Res. 1305 2009 168 182
38. I.-F. Wang, L.-S. Wu, and C.-K.J. Shen TDP-43: and emerging new player in neurodegenerative diseases Trends Mol. Med. 14 2008 479 485
39. A. Yokoseki, A. Shiga, C.F. Tan, A. Tagawa, H. Kaneko, A. Koyama, H. Eguchi, A. Tsujino, T. Ikeuchi, A. Kakita, K. Okamoto, M. Nishizawa, H. Takahashi, and O. Onodera TDP-43 mutation in amyotrophic lateral sclerosis Ann. Neurol. 63 2008 538 542