Sequestration of multiple RNA recognition motif-containing proteins by C9orf72 repeat expansions

Brain

Volumn 137, Issue 7, 2014, Pages 2040-2051

  Cooper Knock, Johnathan ^a   Walsh, Matthew J ^a   Higginbottom, Adrian ^a   Highley, J Robin ^a   Dickman, Mark J ^b   Edbauer, Dieter ^c   Ince, Paul G ^a   Wharton, Stephen B ^a   Wilson, Stuart A ^b   Kirby, Janine ^a   Hautbergue, Guillaume M ^a   Shaw, Pamela J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c Germany 3 Munich Cluster for Systems Neurology   (Germany)

Author keywords

amyotrophic lateral sclerosis; fluorescence imaging; genetics; pathology

Indexed keywords

C9ORF72 PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA; NUCLEAR RNA; PROTEIN; RIBONUCLEASE; RNA; UNCLASSIFIED DRUG; ADAPTOR PROTEIN; CELL PROTEIN; DIPEPTIDE; MESSENGER RNA PRECURSOR; RNA BINDING PROTEIN; TAR DNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; LYMPHOBLASTOID CELL; LYMPHOBLASTOID CELL LINE; MASS SPECTROMETRY; PATHOGENESIS; PATHOLOGY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN MOTIF; RNA BINDING; RNA PROCESSING; RNA SPLICING; SIGNAL NOISE RATIO; ASYMPTOMATIC DISEASE; BINDING ASSAY; C9ORF72 GENE; CENTRAL NERVOUS SYSTEM; CEREBELLUM CELL; GENE; GENE LOCATION; GRANULE CELL; HETEROZYGOTE; HUMAN TISSUE; MOLECULAR RECOGNITION; MOTONEURON; NERVE CELL; NUCLEAR EXPORT SIGNAL; NUCLEOTIDE REPEAT; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PROTEIN CROSS LINKING; PROTEIN RNA BINDING; RNA TRANSLATION; ULTRAVIOLET RADIATION;

AMYOTROPHIC LATERAL SCLEROSIS; FLUORESCENCE IMAGING; GENETICS; PATHOLOGY;

ADENOSINE TRIPHOSPHATE; AMYOTROPHIC LATERAL SCLEROSIS; BIOTINYLATION; BRAIN; DNA REPEAT EXPANSION; FEMALE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; MALE; MASS SPECTROMETRY; NEURONS; NUCLEAR PROTEINS; PHOSPHORUS ISOTOPES; PROTEIN BINDING; PROTEINS; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84903513101     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu120     Document Type: Article

References (44)

1. Ash PE, Bieniek KF, Gendron TF, Caulfield T, Lin WL, Dejesus-Hernandez M, et al. Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron 2013; 77: 639-46.
2. Bengoechea R, Tapia O, Casafont I, Berciano J, Lafarga M, Berciano MT. Nuclear speckles are involved in nuclear aggregation of PABPN1 and in the pathophysiology of oculopharyngeal muscular dystrophy. Neurobiol Dis 2012; 46: 118-29.
3. Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol 2013; 74: 20-38.
4. Byrne S, Heverin M, Elamin M, Walsh C, Hardiman O. Intermediate repeat expansion length in C9orf72 may be pathological in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 2013; 15: 148-50.
5. Casafont I, Bengoechea R, Tapia O, Berciano MT, Lafarga M. TDP-43 localizes in mRNA transcription and processing sites in mammalian neurons. J Struct Biol 2009; 167: 235-41.
6. Cooper-Knock J, Hewitt C, Highley JR, Brockington A, Milano A, Man S, et al. Clinico-pathological features in amyotrophic lateral sclerosis with expansions in C9ORF72. Brain 2012; 135: 751-64.
7. Cooper-Knock J, Higginbottom A, Connor-Robson N, Bayatti N, Bury JJ, Kirby J, et al. C9ORF72 transcription in a frontotemporal dementia case with two expanded alleles. Neurology 2013; 81: 1719-21.
8. DeJesus-Hernandez M, Mackenzie I, Boeve B, Boxer A, Baker M, Rutherford N, et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-Linked FTD and ALS. Neuron 2011; 72: 245-56.
9. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983; 11: 1475-89.
10. Donnelly CJ, Zhang PW, Pham JT, Heusler AR, Mistry NA, Vidensky S, et al. RNA Toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron 2013; 80: 415-28.
11. Fratta P, Mizielinska S, Nicoll AJ, Zloh M, Fisher EM, Parkinson G, et al. C9orf72 hexanucleotide repeat associated with amyotrophic lateral sclerosis and frontotemporal dementia forms RNA G-quadruplexes. Sci Rep 2012; 2: 1016.
12. Garneau D, Revil T, Fisette JF, Chabot B. Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J Biol Chem 2005; 280: 22641-50. (Pubitemid 40853168)
13. Gendron TF, Bieniek KF, Zhang YJ, Jansen-West K, Ash PE, Caulfield T, et al. Antisense transcripts of the expanded C9ORF72 hexanucleotide repeat form nuclear RNA foci and undergo repeatassociated non-ATG translation in c9FTD/ALS. Acta Neuropathol 2013; 126: 829-44.
14. Gomez-Tortosa E, Gallego J, Guerrero-Lopez R, Marcos A, Gil-Neciga E, Sainz MJ, et al. C9ORF72 hexanucleotide expansions of 20-22 repeats are associated with frontotemporal deterioration. Neurology 2013; 80: 366-70.
15. Hargous Y, Hautbergue GM, Tintaru AM, Skrisovska L, Golovanov AP, Stevenin J, et al. Molecular basis of RNA recognition and TAP binding by the SR proteins SRp20 and 9G8. EMBO J 2006; 25: 5126-37. (Pubitemid 44658530)
16. Harms MB, Cady J, Zaidman C, Cooper P, Bali T, Allred P, et al. Lack of C9ORF72 coding mutations supports a gain of function for repeat expansions in amyotrophic lateral sclerosis. Neurobiol Aging 2013; 34: 2234.e2213-39.
17. Hautbergue GM, Hung ML, Golovanov AP, Lian LY, Wilson SA. Mutually exclusive interactions drive handover of mRNA from export adaptors to TAP. Proc Natl Acad Sci USA 2008; 105: 5154-9. (Pubitemid 351738526)
18. Hautbergue GM, Hung ML, Walsh MJ, Snijders AP, Chang CT, Jones R, et al. UIF, a New mRNA export adaptor that works together with REF/ ALY, requires FACT for recruitment to mRNA. Curr Biol 2009; 19: 1918-24.
19. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009a; 37: 1-13.
20. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009b; 4: 44-57.
21. Huang Y, Gattoni R, Sté venin J, Steitz JA. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol Cell 2003; 11: 837-43.
22. Jiang H, Mankodi A, Swanson MS, Moxley RT, Thornton CA. Myotonic dystrophy type 1 is associated with nuclear foci of mutant RNA, sequestration of muscleblind proteins and deregulated alternative splicing in neurons. Hum Mol Genet 2004; 13: 3079-88. (Pubitemid 40045262)
23. Lagier-Tourenne C, Baughn M, Rigo F, Sun S, Liu P, Li HR, et al. Targeted degradation of sense and antisense C9orf72 RNA foci as therapy for ALS and frontotemporal degeneration. Proc Natl Acad Sci USA 2013; 110: E4530-9.
24. Lee YB, Chen HJ, Peres JN, Gomez-Deza J, Attig J, Stalekar M, et al. Hexanucleotide repeats in ALS/FTD form length-dependent RNA foci, sequester RNA binding proteins, and are neurotoxic. Cell Rep 2013; 5: 1178-86.
25. Linder P. mRNA export: RNP remodeling by DEAD-box proteins. Curr Biol 2008; 18: R297-9. (Pubitemid 351458691)
26. Mackenzie IR, Arzberger T, Kremmer E, Troost D, Lorenzl S, Mori K, et al. Dipeptide repeat protein pathology in C9ORF72 mutation cases: clinico-pathological correlations. Acta Neuropathol 2013; 126: 859-79.
27. Mili S, Steitz JA. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 2004; 10: 1692-4. (Pubitemid 39426366)
28. Mizielinska S, Lashley T, Norona FE, Clayton EL, Ridler CE, Fratta P, et al. C9orf72 frontotemporal lobar degeneration is characterised by frequent neuronal sense and antisense RNA foci. Acta Neuropathol 2013; 126: 845-57.
29. Mori K, Lammich S, Mackenzie IR, Forne I, Zilow S, Kretzschmar H, et al. hnRNP A3 binds to GGGGCC repeats and is a constituent of p62-positive/TDP43- negative inclusions in the hippocampus of patients with C9orf72 mutations. Acta Neuropathol 2013a; 125: 413-23.
30. Mori K, Weng SM, Arzberger T, May S, Rentzsch K, Kremmer E, et al. The C9orf72 GGGGCC repeat is translated into aggregating dipeptiderepeat proteins in FTLD/ALS. Science 2013b; 339: 1335-8.
31. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314: 130-3. (Pubitemid 44547757)
32. Reddy K, Zamiri B, Stanley SY, Macgregor RB Jr, Pearson CE. The disease-associated r(GGGGCC)n repeat from the C9orf72 gene forms tract length-dependent uni- and multimolecular RNA G-quadruplex structures. J Biol Chem 2013; 288: 9860-6.
33. Renton AE, Majounie E, Waite A, Simón-Sánchez J, Rollinson S, Gibbs JR, et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011; 72: 257-68.
34. Saitoh N, Spahr CS, Patterson SD, Bubulya P, Neuwald AF, Spector DL. Proteomic analysis of interchromatin granule clusters. Mol Biol Cell 2004; 15: 3876-90. (Pubitemid 38989721)
35. Sareen D, O'Rourke JG, Meera P, Muhammad AK, Grant S, Simpkinson M, et al. Targeting RNA foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci Transl Med 2013; 5: 208ra149.
36. Smith KP, Byron M, Johnson C, Xing Y, Lawrence JB. Defining early steps in mRNA transport: mutant mRNA in myotonic dystrophy type I is blocked at entry into SC-35 domains. J Cell Biol 2007; 178: 951-64. (Pubitemid 47443319)
37. Spector DL, Lamond AI. Nuclear speckles. Cold Spring Harb Perspecti Biol 2011; 3: pii: a000646.
38. Stutz F, Bachi A, Doerks T, Braun IC, Seraphin B, Wilm M, et al. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 2000; 6: 638-50. (Pubitemid 30212241)
39. Tintaru AM, Hautbergue GM, Hounslow AM, Hung ML, Lian LY, Craven CJ, et al. Structural and functional analysis of RNA and TAP binding to SF2/ASF. EMBO Rep 2007; 8: 756-62. (Pubitemid 47202455)
40. Walsh MJ, Hautbergue GM, Wilson SA. Structure and function of mRNA export adaptors. Biochem Soc Trans 2010; 38: 232-6.
41. Xi Z, Zinman L, Moreno D, Schymick J, Liang Y, Sato C, et al. Hypermethylation of the CpG island near the GC repeat in ALS with a C9orf72 expansion. Am J Hum Genet 2013; 92: 981-9.
42. Xu Z, Poidevin M, Li X, Li Y, Shu L, Nelson DL, et al. Expanded GGGGCC repeat RNA associated with amyotrophic lateral sclerosis and frontotemporal dementia causes neurodegeneration. Proc Natl Acad Sci USA 2013; 110: 7778-83.
43. Zhou Z, Luo MJ, Straesser K, Katahira J, Hurt E, Reed R. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature 2000; 407: 401-5.
44. Zu T, Liu Y, Banez-Coronel M, Reid T, Pletnikova O, Lewis J, et al. RAN proteins and RNA foci from antisense transcripts in C9ORF72 ALS and frontotemporal dementia. Proc Natl Acad Sci USA 2013; 110: E4968-77.