Similar dose-dependence of motor neuron cell death caused by wild type human TDP-43 and mutants with ALS-associated amino acid substitutions

Journal of Biomedical Science

Volumn 20, Issue 1, 2013, Pages

  Wu, Lien Szu ^a,b   Cheng, Wei Cheng ^b   Shen, Che Kun James ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

Author keywords

ALS Mutations; Apoptosis; Protein stability; Spinal motor neuron cells; TDP 43

Indexed keywords

PLASMID DNA; TAR DNA BINDING PROTEIN; DNA BINDING PROTEIN; PROTEIN TDP-43;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOTONEURON; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; WESTERN BLOTTING; AMINO ACID SUBSTITUTION; ANIMAL; CELL DEATH; CELL LINE; CYTOLOGY; GENETICS; METABOLISM; MUTATION;

ANIMALIA;

AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL DEATH; CELL LINE; DNA-BINDING PROTEINS; HUMANS; MICE; MOTOR NEURONS; MUTATION;

EID: 84878261613     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1186/1423-0127-20-33     Document Type: Article

References (51)

1. Structural diversity and functional implications of the eukaryotic TDP gene family. Wang HY, Wang IF, Bose J, Shen CK, Genomics 2004 83 130 139 10.1016/S0888-7543(03)00214-3 14667816
2. Human, Drosophila, and C.elegans TDP43: nucleic acid binding properties and splicing regulatory function. Ayala YM, Pantano S, D'Ambrogio A, Buratti E, Brindisi A, Marchetti C, Romano M, Baralle FE, J Mol Biol 2005 348 575 588 10.1016/j.jmb.2005.02.038 15826655
3. Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. Ou SH, Wu F, Harrich D, Garcia-Martinez LF, Gaynor RB, J Virol 1995 69 3584 3596 7745706
4. TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. Wang IF, Wu LS, Chang HY, Shen CK, J Neurochem 2008 105 797 806 10.1111/j.1471-4159.2007.05190.x 18088371
5. Higher order arrangement of the eukaryotic nuclear bodies. Wang IF, Reddy NM, Shen CK, Proc Natl Acad Sci U S A 2002 99 13583 13588 10.1073/pnas. 212483099 12361981
6. TDP-43: an emerging new player in neurodegenerative diseases. Wang IF, Wu LS, Shen CK, Trends Mol Med 2008 14 479 485 10.1016/j.molmed.2008.09.001 18929508
7. Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. Buratti E, Dork T, Zuccato E, Pagani F, Romano M, Baralle FE, EMBO J 2001 20 1774 1784 10.1093/emboj/20.7.1774 11285240
8. TDP-43 overexpression enhances exon 7 inclusion during the survival of motor neuron pre-mRNA splicing. Bose JK, Wang IF, Hung L, Tarn WY, Shen CK, J Biol Chem 2008 283 28852 28859 10.1074/jbc.M805376200 18703504
9. TDP-43, a neuro-pathosignature factor, is essential for early mouse embryogenesis. Wu LS, Cheng WC, Hou SC, Yan YT, Jiang ST, Shen CK, Genesis 2009 48 56 62
10. Deletion of TDP-43 down-regulates Tbc1d1, a gene linked to obesity, and alters body fat metabolism. Chiang PM, Ling J, Jeong YH, Price DL, Aja SM, Wong PC, Proc Natl Acad Sci U S A 2010 107 16320 4 10.1073/pnas.1002176107 20660762
11. Loss of murine TDP-43 disrupts motor function and plays an essential role in embryogenesis. Kraemer BC, Schuck T, Wheeler JM, Robinson LC, Trojanowski JQ, Lee VM, Schellenberg GD, Acta Neuropathol 2010 119 409 419 10.1007/s00401-010-0659-0 20198480
12. TDP-43 is a developmentally regulated protein essential for early embryonic development. Sephton CF, Good SK, Atkin S, Dewey CM, Mayer P 3rd, Herz J, Yu G, J Biol Chem 2010 285 6826 6834 10.1074/jbc.M109.061846 20040602
13. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, Mori H, Mann D, Tsuchiya K, Yoshida M, Hashizume Y, Oda T, Biochem Biophys Res Commun 2006 351 602 611 10.1016/j.bbrc.2006.10.093 17084815
14. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VM, Science 2006 314 130 133 10.1126/science.1134108 17023659
15. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Lee EB, Lee VM, Trojanowski JQ, Nat Rev Neurosci 2011 13 38 50 22127299
16. Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Da Cruz S, Cleveland DW, Curr Opin Neurobiol 2011 21 904 19 10.1016/j.conb.2011.05.029 21813273
17. TDP-43: gumming up neurons through protein-protein and protein-RNA interactions. Buratti E, Baralle FE, Trends Biochem Sci. 2012 37 237 47 10.1016/j.tibs.2012.03.003 22534659
18. Targeed depletion of TDP-43 expression in the spinal cord motor neurons leads to the development of amyotrophic lateral sclerosis-like phenotypes in mice. Wu LS, Cheng WC, Shen CK, J Biol Chem 2012 287 27335 44 10.1074/jbc.M112.359000 22718760
19. Amyotrophic lateral sclerosis. Wijesekera LC, Leigh PN, Orphanet J Rare Dis 2009 4 3 10.1186/1750-1172-4-3 19192301
20. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Pasinelli P, Brown RH, Nat Rev Neurosci 2006 7 710 723 16924260
21. Amyotrophic lateral sclerosis and frontotemporal lobar degeneration: a spectrum of TDP-43 proteinopathies. Geser F, Lee VM, Trojanowski JQ, Neuropathology 2010 30 103 112 10.1111/j.1440-1789.2009.01091.x 20102519
22. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Kabashi E, Valdmanis PN, Dion P, Spiegelman D, McConkey BJ, Vande Velde C, Bouchard JP, Lacomblez L, Pochigaeva K, Salachas F, Pradat PF, Camu W, Meininger V, Dupre N, Rouleau GA, Nat Genet 2008 40 572 574 10.1038/ng.132 18372902
23. TDP-43 is intrinsically aggregation-prone, and amyotrophic lateral sclerosis-linked mutations accelerate aggregation and increase toxicity. Johnson BS, Snead D, Lee JJ, McCaffery JM, Shorter J, Gitler AD, J Biol Chem 2009 284 20329 20339 10.1074/jbc.M109.010264 19465477
24. Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo. Kabashi E, Lin L, Tradewell ML, Dion PA, Bercier V, Bourgouin P, Rochefort D, Bel Hadj S, Durham HD, Vande Velde C, Rouleau GA, Drapeau P, Hum Mol Genet 2010 19 671 683 10.1093/hmg/ddp534 19959528
25. Cytoplasmic mislocalization of TDP-43 is toxic to neurons and enhanced by a mutation associated with familial amyotrophic lateral sclerosis. Barmada SJ, Skibinski G, Korb E, Rao EJ, Wu JY, Finkbeiner S, J Neurosci 2010 30 639 649 10.1523/JNEUROSCI.4988-09.2010 20071528
26. Mutant TAR DNA-binding protein-43 induces oxidative injury in motor neuron-like cell. Duan W, Li X, Shi J, Guo Y, Li Z, Li C, Neuroscience 2010 169 1621 1629 10.1016/j.neuroscience.2010.06.018 20600671
27. TDP-43-induced death is associated with altered regulation of BIM and BCL-XL and attenuated by caspase-mediated TDP-43 cleavage. Suzuki H, Lee K, Matsuoka M, J Biol Chem 2011 286 13171 83 10.1074/jbc.M110.197483 21339291
28. The biochemistry of apoptosis. Hengartner MO, Nature 2000 407 770 776 10.1038/35037710 11048727
29. Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Cashman NR, Durham HD, Blusztajn JK, Oda K, Tabira T, Shaw IT, Dahrouge S, Antel JP, Dev Dyn 1992 194 209 221 10.1002/aja.1001940306 1467557
30. Characterization and use of the NSC-34 cell line for study of neurotrophin receptor trafficking. Matusica D, Fenech MP, Rogers ML, Rush RA, J Neurosci Res 2008 86 553 565 10.1002/jnr.21507 17896795
31. Neurotransmitter synthesis by neuroblastoma clones (neuroblast differentiation-cell culture-choline acetyltransferase- acetylcholinesterase- tyrosine hydroxylase-axons-dendrites). Amano T, Richelson E, Nirenberg M, Proc Natl Acad Sci U S A 1972 69 258 263 10.1073/pnas.69.1.258 4400294
32. Receptor-mediated endocytosis of a manganese complex of transferrin into neuroblastoma (SHSY5Y) cells in culture. Suárez N, Eriksson H, J Neurochem 1993 61 127 31 10.1111/j.1471-4159.1993.tb03546.x 8515258
33. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. Graham FL, Smiley J, Russell WC, Nairn R, J Gen Virol 1977 36 59 74 10.1099/0022-1317-36-1-59 886304
34. Potentiation of amyotrophic lateral sclerosis (ALS)-associated TDP-43 aggregation by the proteasome-targeting factor, ubiquilin 1. Kim SH, Shi Y, Hanson KA, Williams LM, Sakasai R, Bowler MJ, Tibbetts RS, J Biol Chem 2009 284 8083 8092 10.1074/jbc.M808064200 19112176
35. MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Corsten MF, Miranda R, Kasmieh R, Krichevsky AM, Weissleder R, Shah K, Cancer Res 2007 67 8994 9000 10.1158/0008-5472.CAN-07-1045 17908999
36. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Gao D, Inuzuka H, Tseng A, Chin RY, Toker A, Wei W, Nat Cell Biol 2009 11 397 408 10.1038/ncb1847 19270695
37. ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Ling SC, Albuquerque CP, Han JS, Lagier-Tourenne C, Tokunaga S, Zhou H, Cleveland DW, Proc Natl Acad Sci U S A 2010 107 13318 13323 10.1073/pnas.1008227107 20624952
38. Accelerated disease onset with stabilized familial amyotrophic lateral sclerosis (ALS)-linked mutant TDP-43 proteins. Watanabe S, Kaneko K, Yamanaka K, J Biol Chem 2013 288 3641 3654 10.1074/jbc.M112.433615 23235148
39. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Wegorzewska I, Bell S, Cairns NJ, Miller TM, Baloh RH, Proc Natl Acad Sci U S A 2009 106 18809 18814 10.1073/pnas.0908767106 19833869
40. Elevated expression of TDP-43 in the forebrain of mice is sufficient to cause neurological and pathological phenotypes mimicking FTLD-U. Tsai KJ, Yang CH, Fang YH, Cho KH, Chien WL, Wang WT, Wu TW, Lin CP, Fu WM, Shen CK, J Exp Med 2010 207 1661 1673 10.1084/jem.20092164 20660618
41. TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Wils H, Kleinberger G, Janssens J, Pereson S, Joris G, Cuijt I, Smits V, Ceuterick-de Groote C, Van Broeckhoven C, Kumar-Singh S, Proc Natl Acad Sci U S A 2010 107 3858 3863 10.1073/pnas.0912417107 20133711
42. Wild-Type Human TDP-43 Expression Causes TDP-43 Phosphorylation, Mitochondrial Aggregation, Motor Deficits, and Early Mortality in Transgenic Mice. Xu YF, Gendron TF, Zhang YJ, Lin WL, D'Alton S, Sheng H, Casey MC, Tong J, Knight J, Yu X, Rademakers R, Boylan K, Hutton M, McGowan E, Dickson DW, Lewis J, Petrucelli L, J Neurosci 2010 30 10851 10859 10.1523/JNEUROSCI.1630-10.2010 20702714
43. ALS-linked TDP-43 mutations produce aberrant RNA splicing and adult-onset motor neuron disease without aggregation or loss of nuclear TDP-43. Arnold ES, Ling SC, Huelga SC, Lagier-Tourenne C, Polymenidou M, Ditsworth D, Kordasiewicz HB, McAlonis-Downes M, Platoshyn O, Parone PA, Da Cruz S, Clutario KM, Swing D, Tessarollo L, Marsala M, Shaw CE, Yeo GW, Cleveland DW, Proc Natl Acad Sci U S A 2013 110 736 745 10.1073/pnas.1222809110 23382207
44. Transgenic rat model of neurodegeneration caused by mutation in the TDP gene. Zhou H, Huang C, Chen H, Wang D, Landel CP, Xia PY, Bowser R, Liu YJ, Xia XG, PLoS Genet 2010 6 1000887 10.1371/journal.pgen.1000887 20361056
45. A Drosophila model for TDP-43 proteinopathy. Li Y, Ray P, Rao EJ, Shi C, Guo W, Chen X, Woodruff EA 3rd, Fushimi K, Wu JY, Proc Natl Acad Sci U S A 2010 107 3169 3174 10.1073/pnas.0913602107 20133767
46. Ubiquilin modifies TDP-43 toxicity in a Drosophila model of amyotrophic lateral sclerosis (ALS). Hanson KA, Kim SH, Wassarman DA, Tibbetts RS, J Biol Chem 2010 285 11068 72 10.1074/jbc.C109.078527 20154090
47. Neuronal function and dysfunction of Drosophila dTDP. Lin MJ, Cheng CW, Shen CK, PLoS One 2011 6 20371 10.1371/journal.pone.0020371 21673800
48. Neurotoxic effects of TDP-43 overexpression in C. elegans. Ash PE, Zhang YJ, Roberts CM, Saldi T, Hutter H, Buratti E, Petrucelli L, Link CD, Hum Mol Genet 2010 19 3206 3218 10.1093/hmg/ddq230 20530643
49. An ALS-associated mutation affecting TDP-43 enhances protein aggregation, fibril formation and neurotoxicity. Guo W, Chen Y, Zhou X, Kar A, Ray P, Chen X, Rao EJ, Yang M, Ye H, Zhu L, Liu J, Xu M, Yang Y, Wang C, Zhang D, Bigio EH, Mesulam M, Shen Y, Xu Q, Fushimi K, Wu JY, Nat Struct Mol Biol 2011 18 822 830 10.1038/nsmb.2053 21666678
50. Gene expression analysis of frontotemporal lobar degeneration of the motor neuron disease type with ubiquitinated inclusions. Mishra M, Paunesku T, Woloschak GE, Siddique T, Zhu LJ, Lin S, Greco K, Bigio EH, Acta Neuropathol 2007 114 81 94 10.1007/s00401-007-0240-7 17569064
51. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Strong MJ, Volkening K, Hammond R, Yang W, Strong W, Leystra-Lantz C, Shoesmith C, Mol Cell Neurosci 2007 35 320 327 10.1016/j.mcn.2007.03.007 17481916