Mutant TDP-43 in motor neurons promotes the onset and progression of ALS in rats

Journal of Clinical Investigation

Volumn 122, Issue 1, 2012, Pages 107-118

  Huang, Cao ^a   Tong, Jianbin ^a   Bi, Fangfang ^a   Zhou, Hongxia ^a   Xia, Xu Gang ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TAR DNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENE EXPRESSION; GENE MUTATION; GENE SWITCHING; MOTOR PERFORMANCE; MUSCLE ATROPHY; MUSCLE DENERVATION; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; SPINAL CORD MOTONEURON; SPRAGUE DAWLEY RAT; TRANSGENIC RAT;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DNA PRIMERS; DNA-BINDING PROTEINS; DOXYCYCLINE; HUMANS; MOTOR NEURONS; MUTANT PROTEINS; NERVE DEGENERATION; RATS; RATS, TRANSGENIC; RECOMBINANT PROTEINS; TDP-43 PROTEINOPATHIES;

EID: 84855472423     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI59130     Document Type: Article

References (47)

1. Sreedharan J, et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science. 2008;319(5870):1668-1672. (Pubitemid 351432505)
2. Neumann M, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 2006;314(5796):130-133. (Pubitemid 44547757)
3. Zhou H, et al. Transgenic rat model of neurodegeneration caused by mutation in the TDP gene. PLoS Genet. 2010;6(3):e1000887.
4. Wegorzewska I, Bell S, Cairns NJ, Miller TM, Baloh RH. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A. 2009;106(44):18809-18814.
5. Stallings NR, Puttaparthi K, Luther CM, Burns DK, Elliott JL. Progressive motor weakness in transgenic mice expressing human TDP-43. Neurobiol Dis. 2010;40(2):404-414.
6. Wils H, et al. TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A. 2010;107(8):3858-3863.
7. Igaz LM, et al. Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J Clin Invest. 2011;121(2):726-738.
8. Shan X, Chiang PM, Price DL, Wong PC. Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Proc Natl Acad Sci U S A. 2010;107(37):16325-16330.
9. Tsai KJ, et al. Elevated expression of TDP-43 in the forebrain of mice is sufficient to cause neurological and pathological phenotypes mimicking FTLD-U. J Exp Med. 2010;207(8):1661-1673.
10. Benajiba L, et al. TARDBPmutations in motoneuron disease with frontotemporal lobar degeneration. Ann Neurol. 2009;65(4):470-473.
11. Buratti E, Dork T, Zuccato E, Pagani F, Romano M, Baralle FE. Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. Embo J. 2001;20(7):1774-1784. (Pubitemid 32299413)
12. Bosco DA, et al. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum Mol Genet. 2010;19(21):4160- 4175.
13. Wang I, Wu L, Shen C. TDP-43: an emerging new player in neurodegenerative diseases. Trends Mol Med. 2008;14(11):479-485.
14. Elden AC, et al. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature. 2010;466(7310):1069-1075.
15. Polymenidou M, et al. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci. 2011;14(4):459-468.
16. Tollervey JR, et al. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci. 2011;14(4):452-458.
17. Rothstein JD, et al. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature. 2005;433(7021):73-77. (Pubitemid 40101145)
18. Wang H, et a;. Therapeutic gene silencing delivered by a chemically modified small interfering RNA against mutant SOD1 slows amyotrophic lateral sclerosis progression. J Biol Chem. 2008;283(23):15845-15852.
19. Raoul C, et al. Lentiviral-mediated silencing of SOD1 through RNA interference retards disease onset and progression in a mouse model of ALS. Nat Med. 2005;11(4):423-428. (Pubitemid 40562333)
20. Ralph GS, et al. Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat Med. 2005;11(4):429-433. (Pubitemid 40562334)
21. Williamson TL, Cleveland DW. Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat Neurosci. 1999;2(1):50-56. (Pubitemid 30488940)
22. Gu X, et al. Pathological cell-cell interactions elicited by a neuropathogenic form of mutant Huntingtin contribute to cortical pathogenesis in HD mice. Neuron. 2005;46(3):433-444. (Pubitemid 40616887)
23. Ko DC, Milenkovic L, Beier SM, Manuel H, Buchanan J, Scott MP. Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet. 2005;1(1):81-95.
24. Custer SK, et al. Bergmann glia expression of polyglutamine-expanded ataxin-7 produces neurodegeneration by impairing glutamate transport. Nat NeuroSci. 2006;9(10):1302-1311. (Pubitemid 44454272)
25. Wang L, et al. Restricted expression of mutant SOD1 in spinal motor neurons and interneurons induces motor neuron pathology. Neurobiol Dis. 2008;29(3):400-408. (Pubitemid 351258350)
26. Boillee S. Onset and progression in inherited ALS determined by motor neurons and microglia. Science. 2006;312(5778):1389-1392. (Pubitemid 43839552)
27. Gurney ME, et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science. 1994;264(5166):1772-1775. (Pubitemid 24227760)
28. Mackenzie IR, et al. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol. 2007;61(5):427-434. (Pubitemid 46878770)
29. Zhou H, et al. Developing tTA transgenic rats for inducible and reversible gene expression. Int J Biol Sci. 2009;2(4):171-181.
30. Hirasawa M, Cho A, Sreenath T, Sauer B, Julien JP, Kulkarni AB. Neuron-specific expression of Cre recombinase during the late phase of brain development. Neurosci Res. 2001;40(2):125-132. (Pubitemid 32506843)
31. Huang C, et al. FUS transgenic rats develop the phenotypes of Amyotrophic Lateral Sclerosis and frontotemporal lobar degeneration. PLoS Genet. 2011;7(3):e1002011.
32. Tallini YN, et al. BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. Physiol Genomics. 2006;27(3):391-397. (Pubitemid 46708790)
33. Wiese S, et al. Isolation and enrichment of embryonic mouse motoneurons from the lumbar spinal cord of individual mouse embryos. Nat Protoc. 2010;5(1):31-38.
34. Yamanaka K, et al. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci. 2008;11(3):251-253. (Pubitemid 351311795)
35. Boillee S, et al. Onset and progression in inherited ALS determined by motor neurons and microglia. Science. 2006;312(5778):1389-1392. (Pubitemid 43839552)
36. Lobsiger CS, et al. Schwann cells expressing dismutase active mutant SOD1 unexpectedly slow disease progression in ALS mice. Proc Natl Acad Sci U S A. 2009;106(11):4465-4470.
37. Rutherford NJ, et al. Novel mutations in TARDBP (TDP-43) in patients with familial Amyotrophic Lateral Sclerosis. PLoS Genet. 2008;4(9):e1000193.
38. Yokoseki A, et al. TDP-43mutation in familial amyotrophic lateral sclerosis. Ann Neurol. 2008;63(4):538-542. (Pubitemid 351614721)
39. Van Deerlin VM, et al. TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol. 2008;7(5):409-416.
40. Xu YF, et al. Wild-type human TDP-43 expression causes TDP-43 phosphorylation, mitochondrial aggregation, motor deficits, and early mortality in transgenic mice. J Neurosci. 2010;30(32):10851-10859.
41. Lino MM, Schneider C, Caroni P. Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J Neurosci. 2002;22(12):4825-4832. (Pubitemid 37465597)
42. Ravits J, Laurie P, Fan Y, Moore DH. Implications of ALS focality: rostral-caudal distribution of lower motor neuron loss postmortem. Neurology. 2007;68(19):1576-1582. (Pubitemid 46717981)
43. Ravits J, Paul P, Jorg C. Focality of upper and lower motor neuron degeneration at the clinical onset of ALS. Neurology. 2007;68(19):1571-1575. (Pubitemid 46717980)
44. Bruijn LI, et al. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron. 1997;18(2):327-338. (Pubitemid 27111114)
45. Wong PC, et al. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron. 1995;14(6):1105-1116.
46. Gitcho MA, et al. TARDBP 3′-UTR variant in autopsy-confirmed frontotemporal lobar degeneration with TDP-43 proteinopathy. Acta Neuropathol. 2009;118(5):633-645.
47. Ling SC, et al. ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Proc Natl Acad Sci U S A. 2010;107(30):13318-13323.