Home LiteratureArticle Details
PMID: 20702714 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

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

Abstract

Transactivation response DNA-binding protein 43 (TDP-43) is a principal component of ubiquitinated inclusions in frontotemporal lobar degeneration with ubiquitin-positive inclusions and in amyotrophic lateral sclerosis (ALS). Mutations in TARDBP, the gene encoding TDP-43, are associated with sporadic and familial ALS, yet multiple neurodegenerative diseases exhibit TDP-43 pathology without known TARDBP mutations. While TDP-43 has been ascribed a number of roles in normal biology, including mRNA splicing and transcription regulation, elucidating disease mechanisms associated with this protein is hindered by the lack of models to dissect such functions. We have generated transgenic (TDP-43PrP) mice expressing full-length human TDP-43 (hTDP-43) driven by the mouse prion promoter to provide a tool to analyze the role of wild-type hTDP-43 in the brain and spinal cord. Expression of hTDP-43 caused a dose-dependent downregulation of mouse TDP-43 RNA and protein. Moderate overexpression of hTDP-43 resulted in TDP-43 truncation, increased cytoplasmic and nuclear ubiquitin levels, and intranuclear and cytoplasmic aggregates that were immunopositive for phosphorylated TDP-43. Of note, abnormal juxtanuclear aggregates of mitochondria were observed, accompanied by enhanced levels of Fis1 and phosphorylated DLP1, key components of the mitochondrial fission machinery. Conversely, a marked reduction in mitofusin 1 expression, which plays an essential role in mitochondrial fusion, was observed in TDP-43PrP mice. Finally, TDP-43PrP mice showed reactive gliosis, axonal and myelin degeneration, gait abnormalities, and early lethality. This TDP-43 transgenic line provides a valuable tool for identifying potential roles of wild-type TDP-43 within the CNS and for studying TDP-43-associated neurotoxicity.

MeSH Terms
Analysis of Variance Animals Body Weight/genetics Brain/metabolism,pathology,ultrastructure DNA-Binding Proteins/genetics,metabolism Dynamins GTP Phosphohydrolases/metabolism Gene Expression Regulation/genetics Humans Mice Mice, Transgenic Microscopy, Electron, Transmission/methods Microtubule-Associated Proteins/metabolism Mitochondria/genetics,metabolism,pathology Mitochondrial Proteins/metabolism Motor Neurons/metabolism,pathology,ultrastructure Movement Disorders/genetics,metabolism,mortality Mutation/genetics Nerve Degeneration/genetics,mortality,pathology Phosphorylation/genetics Prions/genetics,metabolism Silver Staining/methods Spinal Cord/metabolism,pathology,ultrastructure
Chemicals
DNA-Binding Proteins Microtubule-Associated Proteins Mitochondrial Proteins Prions GTP Phosphohydrolases Mfn1 protein, mouse DNM1L protein, human Dynamins
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Xu Ya-Fei
Department of Neuroscience, Mayo Clinic, Jacksonville, Florida 32224, USA.
Gendron Tania F
Zhang Yong-Jie
Lin Wen-Lang
D'Alton Simon
Sheng Hong
Casey Monica Castanedes
Tong Jimei
Knight Joshua
Yu Xin
Rademakers Rosa
Boylan Kevin
Hutton Mike
McGowan Eileen
Dickson Dennis W
Lewis Jada
Petrucelli Leonard
References (28)
28 references, click to expand
  1. Dynamin-like protein 1 reduction underlies mitochondrial morphology and distribution abnormalities in fibroblasts from sporadic Alzheimer's disease patients.
    Am J Pathol. 2008 Aug;173(2):470-82 PMID: 18599615
  2. Ultrastructural change of synapses of Betz cells in patients with amyotrophic lateral sclerosis.
    Neurosci Lett. 1999 Jun 11;268(1):29-32 PMID: 10400070
  3. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis.
    Biochem Biophys Res Commun. 2006 Dec 22;351(3):602-11 PMID: 17084815
  4. TDP-43 A315T mutation in familial motor neuron disease.
    Ann Neurol. 2008 Apr;63(4):535-8 PMID: 18288693
  5. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis.
    Science. 2008 Mar 21;319(5870):1668-72 PMID: 18309045
  6. TDP-43 mutation in familial amyotrophic lateral sclerosis.
    Ann Neurol. 2008 Apr;63(4):538-42 PMID: 18438952
  7. Maturation process of TDP-43-positive neuronal cytoplasmic inclusions in amyotrophic lateral sclerosis with and without dementia.
    Acta Neuropathol. 2008 Aug;116(2):193-203 PMID: 18560845
  8. Emerging functions of mammalian mitochondrial fusion and fission.
    Hum Mol Genet. 2005 Oct 15;14 Spec No. 2:R283-9 PMID: 16244327
  9. Spred1 is required for synaptic plasticity and hippocampus-dependent learning.
    J Neurosci. 2008 Dec 31;28(53):14443-9 PMID: 19118178
  10. Progressive white matter pathology in the spinal cord of transgenic mice expressing mutant (P301L) human tau.
    J Neurocytol. 2005 Dec;34(6):397-410 PMID: 16902761
  11. Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis.
    Ann Neurol. 2008 Jul;64(1):60-70 PMID: 18546284
  12. A yeast TDP-43 proteinopathy model: Exploring the molecular determinants of TDP-43 aggregation and cellular toxicity.
    Proc Natl Acad Sci U S A. 2008 Apr 29;105(17):6439-44 PMID: 18434538
  13. Axonal mitochondrial clusters containing mutant SOD1 in transgenic models of ALS.
    Antioxid Redox Signal. 2009 Jul;11(7):1535-45 PMID: 19344250
  14. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration.
    Proc Natl Acad Sci U S A. 2009 Nov 3;106(44):18809-14 PMID: 19833869
  15. Epitope mapping of 2E2-D3, a monoclonal antibody directed against human TDP-43.
    Neurosci Lett. 2008 Mar 28;434(2):170-4 PMID: 18304732
  16. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis.
    Nat Genet. 2008 May;40(5):572-4 PMID: 18372902
  17. Evidence that TDP-43 is not the major ubiquitinated target within the pathological inclusions of amyotrophic lateral sclerosis.
    J Neuropathol Exp Neurol. 2007 Dec;66(12):1147-53 PMID: 18090923
  18. Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43.
    J Neurosci. 2007 Sep 26;27(39):10530-4 PMID: 17898224
  19. 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 Feb 23;107(8):3858-63 PMID: 20133711
  20. Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations.
    J Neurosci. 2007 Jan 10;27(2):422-30 PMID: 17215403
  21. Proteolytic processing of TAR DNA binding protein-43 by caspases produces C-terminal fragments with disease defining properties independent of progranulin.
    J Neurochem. 2009 Aug;110(3):1082-94 PMID: 19522733
  22. Mitochondrial clustering induced by overexpression of the mitochondrial fusion protein Mfn2 causes mitochondrial dysfunction and cell death.
    Eur J Cell Biol. 2007 Jun;86(6):289-302 PMID: 17532093
  23. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy.
    Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):378-83 PMID: 19966284
  24. Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis.
    PLoS Genet. 2008 Sep 19;4(9):e1000193 PMID: 18802454
  25. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis.
    Science. 2006 Oct 6;314(5796):130-3 PMID: 17023659
  26. Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity.
    Proc Natl Acad Sci U S A. 2009 May 5;106(18):7607-12 PMID: 19383787
  27. A vector for expressing foreign genes in the brains and hearts of transgenic mice.
    Genet Anal. 1996 Dec;13(6):159-63 PMID: 9117892
  28. Phosphorylation of S409/410 of TDP-43 is a consistent feature in all sporadic and familial forms of TDP-43 proteinopathies.
    Acta Neuropathol. 2009 Feb;117(2):137-49 PMID: 19125255
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2010-08-11
Pages
10851-9
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC3056148
Subset
IM
Grants
NIA NIH HHS · R56 AG026251-03A1 · United States
NIA NIH HHS · P50 AG016574 · United States
NIA NIH HHS · P01-AG17216-08 · United States
NINDS NIH HHS · R01 NS 063964-01 · United States
NIA NIH HHS · R01AG026251 · United States
NIA NIH HHS · P01 AG017216-089001 · United States
NIA NIH HHS · P50 AG016574-12 · United States
NIA NIH HHS · P50 AG016574-126177 · United States
NIA NIH HHS · R01 AG026251 · United States
NIA NIH HHS · R56 AG026251 · United States
NIA NIH HHS · P50 AG016574-126180 · United States
NIA NIH HHS · P50AG16574 · United States
NINDS NIH HHS · R01 NS063964 · United States
NIA NIH HHS · 2R56AG026251- 03A1 · United States
NIA NIH HHS · P01 AG017216 · United States
NIA NIH HHS · R01 AG026251-04 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com