Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43

Nature Neuroscience

Volumn 14, Issue 4, 2011, Pages 459-468

  Polymenidou, Magdalini ^a   Lagier Tourenne, Clotilde ^a   Hutt, Kasey R ^a   Huelga, Stephanie C ^a   Moran, Jacqueline ^a   Liang, Tiffany Y ^a   Ling, Shuo Chien ^a   Sun, Eveline ^a   Wancewicz, Edward ^b   Mazur, Curt ^b   Kordasiewicz, Holly ^a   Sedaghat, Yalda ^b   Donohue, John Paul ^c   Shiue, Lily ^c   Bennett, C Frank ^b   Yeo, Gene W ^a   Cleveland, Don W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ISIS PHARMACEUTICALS   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; MESSENGER RNA; PROGRANULIN; SORTILIN; TAR DNA BINDING PROTEIN;

3' UNTRANSLATED REGION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ARTICLE; AUTOREGULATION; BINDING SITE; BRAIN; CROSS LINKING; DEGENERATIVE DISEASE; DEPLETION; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; IMMUNOPRECIPITATION; INTRON; MOUSE; NONHUMAN; PRE MRNA DEPLETION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN RNA BINDING; PROTEIN SYNTHESIS; PROTEIN TARGETING; RNA DEGRADATION; RNA SPLICING;

3' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DNA-BINDING PROTEINS; FEMALE; HOMEOSTASIS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE DEGENERATION; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; RNA PRECURSORS; RNA, MESSENGER;

EID: 79953185674     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2779     Document Type: Article

References (50)

1. Neumann, M. et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130-133 (2006). (Pubitemid 44547757)
2. Arai, T. et al. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 351, 602-611 (2006). (Pubitemid 44708852)
3. Lagier-Tourenne, C., Polymenidou, M. & Cleveland, D.W. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet. 19, R46-R64 (2010).
4. Gitcho, M.A. et al. TDP-43 A315T mutation in familial motor neuron disease. Ann. Neurol. 63, 535-538 (2008). (Pubitemid 351614720)
5. Kabashi, E. et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 40, 572-574 (2008). (Pubitemid 351601218)
6. Sreedharan, J. et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319, 1668-1672 (2008). (Pubitemid 351432505)
7. Van Deerlin, V.M. et al. TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol. 7, 409-416 (2008).
8. Buratti, E. et al. Nuclear factor TDP-43 can affect selected microRNA levels. FEBS J. 277, 2268-2281 (2010).
9. Cooper, T.A., Wan, L. & Dreyfuss, G. RNA and Disease. Cell 136, 777-793 (2009).
10. Kwiatkowski, T.J. Jr. et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323, 1205-1208 (2009).
11. Vance, C. et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323, 1208-1211 (2009).
12. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008). (Pubitemid 351911867)
13. Ule, J. et al. CLIP identifies Nova-regulated RNA networks in the brain. Science 302, 1212-1215 (2003). (Pubitemid 37421026)
14. Licatalosi, D.D. et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456, 464-469 (2008). (Pubitemid 352759008)
15. Yeo, G.W. et al. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat. Struct. Mol. Biol. 16, 130-137 (2009).
16. Ling, S.C. et al. ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Proc. Natl. Acad. Sci. USA 107, 13318-13323 (2010).
17. Zisoulis, D.G. et al. Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 17, 173-179 (2010).
18. Sephton, C.F. et al. Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J. Biol. Chem. 286, 1204-1215 (2011).
19. Mili, S. & Steitz, J.A. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 10, 1692-1694 (2004). (Pubitemid 39426366)
20. Buratti, E. et al. Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J. 20, 1774-1784 (2001). (Pubitemid 32299413)
21. Chi, S.W., Zang, J.B., Mele, A. & Darnell, R.B. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460, 479-486 (2009).
22. Parkhomchuk, D. et al. Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res. 37, e123 (2009).
23. Pang, K.C. et al. RNAdb-a comprehensive mammalian noncoding RNA database. Nucleic Acids Res. 33, D125-D130 (2005). (Pubitemid 40207844)
24. Wang, E.T. et al. Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476 (2008). (Pubitemid 352759009)
25. Hu, F. et al. Sortilin-mediated endocytosis determines levels of the frontotemporal dementia protein, progranulin. Neuron 68, 654-667 (2010).
26. Carrasquillo, M.M. et al. Genome-wide screen identifies rs646776 near sortilin as a regulator of progranulin levels in human pasma. Am. J. Hum. Genet. 87, 890-897 (2010).
27. Du, H. et al. Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat. Struct. Mol. Biol. 17, 187-193 (2010).
28. Ayala, Y.M. et al. TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J. 30, 277-288 (2011).
29. Le Hir, H., Moore, M.J. & Maquat, L.E. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev. 14, 1098-1108 (2000). (Pubitemid 30324423)
30. Wollerton, M.C., Gooding, C., Wagner, E.J., Garcia-Blanco, M.A. & Smith, C.W. Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol. Cell 13, 91-100 (2004). (Pubitemid 38117118)
31. Sureau, A., Gattoni, R., Dooghe, Y., Stevenin, J. & Soret, J. SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. EMBO J. 20, 1785-1796 (2001). (Pubitemid 32299414)
32. Perlick, H.A., Medghalchi, S.M., Spencer, F.A., Kendzior, R.J. Jr. & Dietz, H.C. Mammalian orthologs of a yeast regulator of nonsense transcript stability. Proc. Natl. Acad. Sci. USA 93, 10928-10932 (1996). (Pubitemid 26333094)
33. Baker, M. et al. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442, 916-919 (2006). (Pubitemid 44285946)
34. Cruts, M. et al. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442, 920-924 (2006). (Pubitemid 44285947)
35. Fiesel, F.C. et al. Knockdown of transactive response DNA-binding protein (TDP-43) downregulates histone deacetylase 6. EMBO J. 29, 209-221 (2010).
36. Strong, M.J. et al. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol. Cell. Neurosci. 35, 320-327 (2007). (Pubitemid 46843567)
37. Bergeron, C. et al. Neurofilament light and polyadenylated mRNA levels are decreased in amyotrophic lateral sclerosis motor neurons. J. Neuropathol. Exp. Neurol. 53, 221-230 (1994). (Pubitemid 24146859)
38. Hutton, M. et al. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393, 702-705 (1998).
39. MacDonald, M.E. et al. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72, 971-983 (1993). (Pubitemid 23110238)
40. Schwab, C., Arai, T., Hasegawa, M., Yu, S. & McGeer, P.L. Colocalization of transactivation- responsive DNA-binding protein 43 and huntingtin in inclusions of Huntington disease. J. Neuropathol. Exp. Neurol. 67, 1159-1165 (2008).
41. Valdmanis, P.N. et al. A mutation that creates a pseudoexon in SOD1 causes familial ALS. Ann. Hum. Genet. 73, 652-657 (2009).
42. Birve, A. et al. A novel SOD1 splice site mutation associated with familial ALS revealed by SOD activity analysis. Hum. Mol. Genet. 19, 4201-4206 (2010).
43. Mercado, P.A., Ayala, Y.M., Romano, M., Buratti, E. & Baralle, F.E. Depletion of TDP 43 overrides the need for exonic and intronic splicing enhancers in the human apoA-II gene. Nucleic Acids Res. 33, 6000-6010 (2005). (Pubitemid 41742619)
44. Dreumont, N. et al. Antagonistic factors control the unproductive splicing of SC35 terminal intron. Nucleic Acids Res. 38, 1353-1366 (2009).
45. Lin, S., Coutinho-Mansfield, G., Wang, D., Pandit, S. & Fu, X.D. The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 15, 819-826 (2008).
46. Tollervey, J.R. et al. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci. advance online publication, doi:10.1038/nn.2778 (27 February 2011).
47. Xu, Y.F. et al. Wild-type human TDP-43 expression causes TDP-43 phosphorylation, mitochondrial aggregation, motor deficits, and early mortality in transgenic mice. J. Neurosci. 30, 10851-10859 (2010).
48. Igaz, L.M. et al. Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J. Clin. Invest. 121, 726-738 (2011).
49. Yeo, G.W., Van Nostrand, E.L. & Liang, T.Y. Discovery and analysis of evolutionarily conserved intronic splicing regulatory elements. PLoS Genet. 3, e85 (2007).
50. Su, A.I. et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. USA 101, 6062-6067 (2004). (Pubitemid 38520528)