Expression of mutant TDP-43 induces neuronal dysfunction in transgenic mice

Molecular Neurodegeneration

Volumn 6, Issue 1, 2011, Pages

  Xu, Ya Fei ^a   Zhang, Yong Jie ^a   Lin, Wen Lang ^a   Cao, Xiangkun ^a   Stetler, Caroline ^a   Dickson, Dennis W ^a   Lewis, Jada ^a,b   Petrucelli, Leonard ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

aggregation; ALS; mitochondria; mouse model; tau

Indexed keywords

LOW MOLECULAR WEIGHT HEPARIN; TAR DNA BINDING PROTEIN; DNA BINDING PROTEIN; PROTEIN TDP-43; TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; BRAIN NERVE CELL; BRAIN WEIGHT; CHROMATOLYSIS; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; EOSINOPHIL; GAIT DISORDER; GLIOSIS; IMMUNOHISTOCHEMISTRY; LETHALITY; MOTOR DYSFUNCTION; MOUSE; MUTATIONAL ANALYSIS; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SPINAL CORD NERVE CELL; UBIQUITINATION; ANIMAL; CYTOLOGY; DEGENERATIVE DISEASE; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; MUTATION; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD; TRANSGENIC MOUSE; ULTRASTRUCTURE;

MAMMALIA; MUS; MUS MUSCULUS;

ANIMALS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; HUMANS; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MOVEMENT DISORDERS; MUTATION; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; NEURONS; SPINAL CORD; TAU PROTEINS;

EID: 81255177581     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-6-73     Document Type: Article

References (32)

1. 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 (Pubitemid 44708852)
2. 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, et al. Science 2006 314 130 133 10.1126/science.1134108 17023659 (Pubitemid 44547757)
3. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B, Ackerley S, Durnall JC, Williams KL, Buratti E, et al. Science 2008 319 1668 1672 10.1126/science.1154584 18309045 (Pubitemid 351432505)
4. 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, et al. Nat Genet 2008 40 572 574 10.1038/ng.132 18372902 (Pubitemid 351601218)
5. TDP-43 A315T mutation in familial motor neuron disease. Gitcho MA, Baloh RH, Chakraverty S, Mayo K, Norton JB, Levitch D, Hatanpaa KJ, White CL, Bigio EH, Caselli R, et al. Ann Neurol 2008 63 535 538 10.1002/ana.21344 18288693 (Pubitemid 351614720)
6. Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. Rutherford NJ, Zhang YJ, Baker M, Gass JM, Finch NA, Xu YF, Stewart H, Kelley BJ, Kuntz K, Crook RJ, et al. PLoS Genet 2008 4 1000193 10.1371/journal.pgen.1000193 18802454
7. TDP-43 mutation in familial amyotrophic lateral sclerosis. Yokoseki A, Shiga A, Tan CF, Tagawa A, Kaneko H, Koyama A, Eguchi H, Tsujino A, Ikeuchi T, Kakita A, et al. Ann Neurol 2008 63 538 542 10.1002/ana.21392 18438952 (Pubitemid 351614721)
8. 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 (Pubitemid 32299413)
9. Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Buratti E, Baralle FE, Front Biosci 2008 13 867 878 10.2741/2727 17981595 (Pubitemid 351594732)
10. 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 USA 2010 107 3858 3863 10.1073/pnas.0912417107 20133711
11. 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, et al. J Neurosci 2010 30 10851 10859 10.1523/JNEUROSCI.1630- 10.2010 20702714
12. 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 USA 2009 106 18809 18814 10.1073/pnas.0908767106 19833869
13. Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Shan X, Chiang PM, Price DL, Wong PC, Proc Natl Acad Sci USA 2010 107 16325 16330 10.1073/pnas.1003459107 20736350
14. Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. Igaz LM, Kwong LK, Lee EB, Chen-Plotkin A, Swanson E, Unger T, Malunda J, Xu Y, Winton MJ, Trojanowski JQ, Lee VM, J Clin Invest 2011 121 726 738 10.1172/JCI44867 21206091
15. 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
16. Pathological hallmarks of amyotrophic lateral sclerosis/frontotemporal lobar degeneration in transgenic mice produced with TDP-43 genomic fragments. Swarup V, Phaneuf D, Bareil C, Robertson J, Rouleau GA, Kriz J, Julien JP, Brain 2011 134 2610 2626 10.1093/brain/awr159 21752789
17. A vector for expressing foreign genes in the brains and hearts of transgenic mice. Borchelt DR, Davis J, Fischer M, Lee MK, Slunt HH, Ratovitsky T, Regard J, Copeland NG, Jenkins NA, Sisodia SS, Price DL, Genet Anal 1996 13 159 163 9117892 (Pubitemid 27063321)
18. 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
19. TDP-43 regulates its mRNA levels through a negative feedback loop. Ayala YM, De Conti L, Avendano-Vazquez SE, Dhir A, Romano M, D'Ambrogio A, Tollervey J, Ule J, Baralle M, Buratti E, Baralle FE, EMBO J 2011 30 277 288 10.1038/emboj.2010.310 21131904
20. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Polymenidou M, Lagier-Tourenne C, Hutt KR, Huelga SC, Moran J, Liang TY, Ling SC, Sun E, Wancewicz E, Mazur C, et al. Nat Neurosci 2011
21. Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. Sephton CF, Cenik C, Kucukural A, Dammer EB, Cenik B, Han Y, Dewey CM, Roth FP, Herz J, Peng J, et al. J Biol Chem 2011 286 1204 1215 10.1074/jbc.M110.190884 21051541
22. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Tollervey JR, Curk T, Rogelj B, Briese M, Cereda M, Kayikci M, Konig J, Hortobagyi T, Nishimura AL, Zupunski V, et al. Nat Neurosci 2011
23. The role of tau in neurodegeneration. Gendron TF, Petrucelli L, Mol Neurodegener 2009 4 13 10.1186/1750-1326-4-13 19284597
24. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Rothstein JD, Ann Neurol 2009 65 Suppl 1 3 9 19191304
25. Role of axonal transport in neurodegenerative diseases. De Vos KJ, Grierson AJ, Ackerley S, Miller CC, Annu Rev Neurosci 2008 31 151 173 10.1146/annurev.neuro.31.061307.090711 18558852
26. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. De Vos KJ, Chapman AL, Tennant ME, Manser C, Tudor EL, Lau KF, Brownlees J, Ackerley S, Shaw PJ, McLoughlin DM, et al. Hum Mol Genet 2007 16 2720 2728 10.1093/hmg/ddm226 17725983 (Pubitemid 350018514)
27. Mutant SOD1 impairs axonal transport of choline acetyltransferase and acetylcholine release by sequestering KAP3. Tateno M, Kato S, Sakurai T, Nukina N, Takahashi R, Araki T, Hum Mol Genet 2009 18 942 955 19088126
28. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, Harada A, Hirokawa N, Cell 1998 93 1147 1158 10.1016/S0092-8674(00)81459-2 9657148 (Pubitemid 28307420)
29. Morphometry of spinal motor neurons in amyotrophic lateral sclerosis with special reference to chromatolysis and intracytoplasmic inclusion bodies. Wakayama I, Brain Res 1992 586 12 18 10.1016/0006-8993(92)91365-L 1324776
30. Tau protein hyperphosphorylation in sporadic ALS with cognitive impairment. Strong MJ, Yang W, Strong WL, Leystra-Lantz C, Jaffe H, Pant HC, Neurology 2006 66 1770 1771 10.1212/01.wnl.0000218161.15834.db 16769962 (Pubitemid 43964644)
31. Microtubule-associated tau protein positive neuronal and glial inclusions in ALS. Yang W, Sopper MM, Leystra-Lantz C, Strong MJ, Neurology 2003 61 1766 1773 14694044 (Pubitemid 38020826)
32. Epitope mapping of 2E2-D3, a monoclonal antibody directed against human TDP-43. Zhang HX, Tanji K, Mori F, Wakabayashi K, Neurosci Lett 2008 434 170 174 10.1016/j.neulet.2008.01.060 18304732