Cited by 139RNA Research and SplicingRNA regulation and diseaseNeuroscience and Neuropharmacology Research

Regulatory consequences of neuronal ELAV-like protein binding to coding and non-coding RNAs in human brain

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Scheckel, Claudia, Drapeau, Elodie, Frias, Maria A, Park, Christopher Y, Fak, John, Zucker-Scharff, Ilana, Kou, Yan, Haroutunian, Vahram +3 more·2016·eLife

Abstract

Neuronal ELAV-like (nELAVL) RNA binding proteins have been linked to numerous neurological disorders. We performed crosslinking-immunoprecipitation and RNAseq on human brain, and identified nELAVL binding sites on 8681 transcripts. Using knockout mice and RNAi in human neuroblastoma cells, we showed that nELAVL intronic and 3' UTR binding regulates human RNA splicing and abundance. We validated hundreds of nELAVL targets among which were important neuronal and disease-associated transcripts, including Alzheimer's disease (AD) transcripts. We therefore investigated RNA regulation in AD brain, and observed differential splicing of 150 transcripts, which in some cases correlated with differential nELAVL binding. Unexpectedly, the most significant change of nELAVL binding was evident on non-coding Y RNAs. nELAVL/Y RNA complexes were specifically remodeled in AD and after acute UV stress in neuroblastoma cells. We propose that the increased nELAVL/Y RNA association during stress may lead to nELAVL sequestration, redistribution of nELAVL target binding, and altered neuronal RNA splicing.

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  • ELAVL4 regulates RNA splicing.

    “ELAVL4 regulates RNA splicing (Scheckel et al., 2016)”

    From ELAVL4, splicing, and glutamatergic dysfunction precede neuron loss in MAPT mutation cerebral organoids (2021) · cites this paper as Scheckel et al., 2016

    The Results section, “nELAVL regulates splicing of human brain targets” (page unavailable), reports altered exon splicing after nELAVL depletion. But the depletion targeted ELAVL2, ELAVL3, and ELAVL4 together, as specified in “nELAVL proteins regulate mRNA abundance of human brain targets” (page unavailable). The paper therefore supports a role for the neuronal ELAVL proteins in splicing, not an independently established role for ELAVL4 alone. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • Published nELAVL CLIP-seq data from human brain found that hCACNA1C, hCACNA1E and hCACNA1I are targets of nELAVL proteins.

    “a published nELAVL CLIP-seq experiment from human brain found that hCACNA1C, hCACNA1E and hCACNA1I are targets of nELAVL proteins66”

    From CYFIP1 governs the development of cortical axons by modulating calcium availability (2025) · cites this paper as [66]

    The Results section, “Identification of nELAVL targets in human brain” (page unavailable), confirms that the authors performed CLIP on human brain samples and identified nELAVL RNA-binding sites. The passages in our copy do not identify CACNA1C, CACNA1E, or CACNA1I as targets; searches for those gene names found no matching passage. Thus the experiment is supported, but the specific target list is not verified. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 92

  1. Akamatsu W Fujihara H Mitsuhashi T Yano M Shibata S Hayakawa Y Okano HJ Sakakibara S Takano H Takano T Takahashi T Noda T Okano H 2005 The RNA-binding protein HuD regulates neuronal cell identity and maturation Proceedings of the National Academy of Sciences of the United States of America 102 4625 4630 10.1073/pnas.0407523102 15764704 PMC555491 · DOI · Paper page
  2. Akamatsu W Okano HJ Osumi N Inoue T Nakamura S Sakakibara S-I Miura M Matsuo N Darnell RB Okano H 1999 Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous systems Proceedings of the National Academy of Sciences of the United States of America 96 9885 9890 10.1073/pnas.96.17.9885 10449789 PMC22305 · DOI
  3. Anderson KD Morin MA Beckel-Mitchener A Mobarak CD Neve RL Furneaux HM Burry R Perrone-Bizzozero NI 2000 Overexpression of HuD, but not of its truncated form HuD i+II, promotes GAP-43 gene expression and neurite outgrowth in PC12 cells in the absence of nerve growth factor Journal of Neurochemistry 75 1103 1114 10.1046/j.1471-4159.2000.0751103.x 10936192 · DOI
  4. Antic D Lu N Keene JD 1999 ELAV tumor antigen, hel-N1, increases translation of neurofilament m mRNA and induces formation of neurites in human teratocarcinoma cells Genes & Development 13 449 461 10.1101/gad.13.4.449 10049360 PMC316478 · DOI
  5. Aoki KF Kanehisa M 2005 Using the KEGG database resource Current Protocols in Bioinformatics 1 12 10.1002/0471250953.bi0112s11 18428742 · DOI
  6. Aranda B Achuthan P Alam-Faruque Y Armean I Bridge A Derow C Feuermann M Ghanbarian AT Kerrien S Khadake J Kerssemakers J Leroy C Menden M Michaut M Montecchi-Palazzi L Neuhauser SN Orchard S Perreau V Roechert B van Eijk K Hermjakob H 2010 The IntAct molecular interaction database in 2010 Nucleic Acids Research 38 D525 D531 10.1093/nar/gkp878 19850723 PMC2808934 · DOI · Paper page
  7. Aranda-Abreu GE Behar L Chung S Furneaux H Ginzburg I 1999 Embryonic lethal abnormal vision-like RNA-binding proteins regulate neurite outgrowth and tau expression in PC12 cells The Journal of Neuroscience 19 6907 6917 10436048 PMC6782881
  8. Baloh RH 2011 TDP-43: the relationship between protein aggregation and neurodegeneration in amyotrophic lateral sclerosis and frontotemporal lobar degeneration The FEBS Journal 278 3539 3549 10.1111/j.1742-4658.2011.08256.x 21777387 PMC3177991 · DOI
  9. Ben Khalifa N Tyteca D Marinangeli C Depuydt M Collet JF Courtoy PJ Renauld JC Constantinescu S Octave JN Kienlen-Campard P 2012 Structural features of the KPI domain control APP dimerization, trafficking, and processing FASEB Journal 26 855 867 10.1096/fj.11-190207 22085646 · DOI
  10. Bhattacharyya SN Habermacher R Martine U Closs EI Filipowicz W 2006 Relief of microRNA-mediated translational repression in human cells subjected to stress Cell 125 1111 1124 10.1016/j.cell.2006.04.031 16777601 · DOI
  11. Bolognani F Contente-Cuomo T Perrone-Bizzozero NI 2010 Novel recognition motifs and biological functions of the RNA-binding protein HuD revealed by genome-wide identification of its targets Nucleic Acids Research 38 117 130 10.1093/nar/gkp863 19846595 PMC2800223 · DOI · Paper page
  12. Borah S Darricarrère N Darnell A Myoung J Steitz JA 2011 A viral nuclear noncoding RNA binds re-localized poly(A) binding protein and is required for late KSHV gene expression PLoS Pathogens 7 e10421 10.1371/journal.ppat.1002300 PMC3192849 22022268 · DOI
  13. Bruno AE Li L Kalabus JL Pan Y Yu A Hu Z 2012 MiRdSNP: a database of disease-associated SNPs and microRNA target sites on 3'UTRs of human genes BMC Genomics 13 44 10.1186/1471-2164-13-44 22276777 PMC3287127 · DOI
  14. Burry RW Smith CL 2006 HuD distribution changes in response to heat shock but not neurotrophic stimulation The Journal of Histochemistry and Cytochemistry 54 1129 1138 10.1369/jhc.6A6979.2006 16801526 PMC3957809 · DOI
  15. Castello A Fischer B Eichelbaum K Horos R Beckmann BM Strein C Davey NE Humphreys DT Preiss T Steinmetz LM Krijgsveld J Hentze MW 2012 Insights into RNA biology from an atlas of mammalian mRNA-binding proteins Cell 149 1393 1406 10.1016/j.cell.2012.04.031 22658674 · DOI · Paper page
  16. Cazalla D Yario T Steitz JA Steitz J 2010 Down-regulation of a host microRNA by a herpesvirus saimiri noncoding RNA Science 328 1563 1566 10.1126/science.1187197 20558719 PMC3075239 · DOI · Paper page
  17. Ceol A Chatr Aryamontri A Licata L Peluso D Briganti L Perfetto L Castagnoli L Cesareni G 2010 MINT, the molecular interaction database: 2009 update Nucleic Acids Research 38 D532 D539 10.1093/nar/gkp983 19897547 PMC2808973 · DOI
  18. Charizanis K Lee KY Batra R Goodwin M Zhang C Yuan Y Shiue L Cline M Scotti MM Xia G Kumar A Ashizawa T Clark HB Kimura T Takahashi MP Fujimura H Jinnai K Yoshikawa H Gomes-Pereira M Gourdon G Sakai N Nishino S Foster TC Ares M Darnell RB Swanson MS 2012 Muscleblind-like 2-mediated alternative splicing in the developing brain and dysregulation in myotonic dystrophy Neuron 75 437 450 10.1016/j.neuron.2012.05.029 22884328 PMC3418517 · DOI
  19. Chen EY Xu H Gordonov S Lim MP Perkins MH Ma'ayan A 2012 Expression2Kinases: mRNA profiling linked to multiple upstream regulatory layers Bioinformatics 28 105 111 10.1093/bioinformatics/btr625 22080467 PMC3244772 · DOI
  20. Chen H Boutros PC 2011 VennDiagram: a package for the generation of highly-customizable venn and euler diagrams in r BMC Bioinformatics 12 35 10.1186/1471-2105-12-35 21269502 PMC3041657 · DOI
  21. Chen X Quinn AM Wolin SL 2000 Ro ribonucleoproteins contribute to the resistance of deinococcus radiodurans to ultraviolet irradiation Genes & Development 14 777 782 10766734 PMC316496
  22. Chen X Smith JD Shi H Yang DD Flavell RA Wolin SL 2003 The ro autoantigen binds misfolded U2 small nuclear RNAs and assists mammalian cell survival after UV irradiation Current Biology 13 2206 2211 10.1016/j.cub.2003.11.028 14680639 · DOI
  23. Chen X Wolin SL 2004 The Ro 60 kDa autoantigen: insights into cellular function and role in autoimmunity Journal of Molecular Medicine 82 232 239 10.1007/s00109-004-0529-0 15168680 · DOI
  24. Chen YZ Bennett CL Huynh HM Blair IP Puls I Irobi J Dierick I Abel A Kennerson ML Rabin BA Nicholson GA Auer-Grumbach M Wagner K De Jonghe P Griffin JW Fischbeck KH Timmerman V Cornblath DR Chance PF 2004 DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (aLS4) American Journal of Human Genetics 74 1128 1135 10.1086/421054 15106121 PMC1182077 · DOI
  25. Clermont O Burlet P Lefebvre S Bürglen L Munnich A Melki J 1995 SMN gene deletions in adult-onset spinal muscular atrophy The Lancet 346 1712 1713 10.1016/S0140-6736(95)92881-2 8551862 · DOI
  26. Darnell RB 2013 RNA protein interaction in neurons Annual Review of Neuroscience 36 243 270 10.1146/annurev-neuro-062912-114322 PMC3889695 23701460 · DOI · Paper page
  27. DeStefano AL Latourelle J Lew MF Suchowersky O Klein C Golbe LI Mark MH Growdon JH Wooten GF Watts R Guttman M Racette BA Perlmutter JS Marlor L Shill HA Singer C Goldwurm S Pezzoli G Saint-Hilaire MH Hendricks AE Gower A Williamson S Nagle MW Wilk JB Massood T Huskey KW Baker KB Itin I Litvan I Nicholson G Corbett A Nance M Drasby E Isaacson S Burn DJ Chinnery PF Pramstaller PP Al-Hinti J Moller AT Ostergaard K Sherman SJ Roxburgh R Snow B Slevin JT Cambi F Gusella JF Myers RH 2008 Replication of association between ELAVL4 and parkinson disease: the GenePD study Human Genetics 124 95 99 10.1007/s00439-008-0526-4 18587682 PMC2716559 · DOI · Paper page
  28. Elden AC Kim HJ Hart MP Chen-Plotkin AS Johnson BS Fang X Armakola M Geser F Greene R Lu MM Padmanabhan A Clay-Falcone D McCluskey L Elman L Juhr D Gruber PJ Rüb U Auburger G Trojanowski JQ Lee VM Van Deerlin VM Bonini NM Gitler AD 2010 Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS Nature 466 1069 1075 10.1038/nature09320 20740007 PMC2965417 · DOI
  29. Fan XC Steitz JA 1998b HNS, a nuclear-cytoplasmic shuttling sequence in HuR Proceedings of the National Academy of Sciences of the United States of America 95 15293 15298 10.1073/pnas.95.26.15293 9860962 PMC28036 · DOI
  30. Fan XC Steitz JA 1998a Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the invivo stability of ARE-containing mRNAs The EMBO Journal 17 3448 3460 10.1093/emboj/17.12.3448 9628880 PMC1170681 · DOI · Paper page
  31. Gallouzi I-E Brennan CM Stenberg MG Swanson MS Eversole A Maizels N Steitz JA 2000 HuR binding to cytoplasmic mRNA is perturbed by heat shock Proceedings of the National Academy of Sciences of the United States of America 97 3073 3078 10.1073/pnas.97.7.3073 10737787 PMC16194 · DOI
  32. Gentleman RC Carey VJ Bates DM Bolstad B Dettling M Dudoit S Ellis B Gautier L Ge Y Gentry J Hornik K Hothorn T Huber W Iacus S Irizarry R Leisch F Li C Maechler M Rossini AJ Sawitzki G Smith C Smyth G Tierney L Yang JY Zhang J 2004 Bioconductor: open software development for computational biology and bioinformatics Genome Biology 5 R80 10.1186/gb-2004-5-10-r80 15461798 PMC545600 · DOI
  33. Ghani M Pinto D Lee JH Grinberg Y Sato C Moreno D Scherer SW Mayeux R St George-Hyslop P Rogaeva E 2012 Genome-wide survey of large rare copy number variants in alzheimer's disease among caribbean hispanics G3 2 71 78 10.1534/g3.111.000869 22384383 PMC3276183 · DOI
  34. Glaz J Naus J Wallenstein S 2013 Scan Statistics and Applications Springer New York, NY
  35. Hansen TB Jensen TI Clausen BH Bramsen JB Finsen B Damgaard CK Kjems J 2013 Natural RNA circles function as efficient microRNA sponges Nature 495 384 388 10.1038/nature11993 23446346 · DOI · Paper page
  36. Heinz S Benner C Spann N Bertolino E Lin YC Laslo P Cheng JX Murre C Singh H Glass CK 2010 Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and b cell identities Molecular Cell 38 576 589 10.1016/j.molcel.2010.05.004 20513432 PMC2898526 · DOI · Paper page
  37. Hermjakob H Montecchi-Palazzi L Bader G Wojcik J Salwinski L Ceol A Moore S Orchard S Sarkans U von Mering C Roechert B Poux S Jung E Mersch H Kersey P Lappe M Li Y Zeng R Rana D Nikolski M Husi H Brun C Shanker K Grant SG Sander C Bork P Zhu W Pandey A Brazma A Jacq B Vidal M Sherman D Legrain P Cesareni G Xenarios I Eisenberg D Steipe B Hogue C Apweiler R 2004 The HUPO PSI's molecular interaction format--a community standard for the representation of protein interaction data Nature Biotechnology 22 177 183 10.1038/nbt926 14755292 · DOI · Paper page
  38. Ihaka R Gentleman R 1996 R: a language for data analysis and graphics Journal of Computational and Graphical Statistics 5 299 314
  39. Ince-Dunn G Okano HJ Jensen KB Park WY Zhong R Ule J Mele A Fak JJ Yang C Zhang C Yoo J Herre M Okano H Noebels JL Darnell RB 2012 Neuronal elav-like (hu) proteins regulate RNA splicing and abundance to control glutamate levels and neuronal excitability Neuron 75 1067 –1080 10.1016/j.neuron.2012.07.009 22998874 PMC3517991 · DOI · Paper page
  40. Isserlin R El-Badrawi RA Bader GD 2011 The biomolecular interaction network database in PSI-MI 2.5 Database 2011 baq037 10.1093/database/baq037 21233089 PMC3021793 · DOI
  41. Kang MJ Abdelmohsen K Hutchison ER Mitchell SJ Grammatikakis I Guo R Noh JH Martindale JL Yang X Lee EK Faghihi MA Wahlestedt C Troncoso JC Pletnikova O Perrone-Bizzozero N Resnick SM de Cabo R Mattson MP Gorospe M 2014 HuD regulates coding and noncoding RNA to induce APP→a processingg Cell Reports 7 1401 1409 10.1016/j.celrep.2014.04.050 24857657 PMC4074355 · DOI
  42. Kasashima K Terashima K Yamamoto K Sakashita E Sakamoto H 1999 Cytoplasmic localization is required for the mammalian ELAV-like protein HuD to induce neuronal differentiation Genes to Cells 4 667 683 10.1046/j.1365-2443.1999.00292.x 10620013 · DOI · Paper page
  43. Kawai T Lal A Yang X Galban S Mazan-Mamczarz K Gorospe M 2006 Translational control of cytochrome c by RNA-binding proteins TIA-1 and HuR Molecular and Cellular Biology 26 3295 3307 10.1128/MCB.26.8.3295-3307.2006 16581801 PMC1446930 · DOI
  44. Kim HH Kuwano Y Srikantan S Lee EK Martindale JL Gorospe M 2009 HuR recruits let-7/RISC to repress c-myc expression Genes & Development 23 1743 1748 10.1101/gad.1812509 19574298 PMC2720259 · DOI
  45. Labbé JC Hekimi S Rokeach LA 1999 The levels of the RoRNP-associated y RNA are dependent upon the presence of ROP-1, the caenorhabditis elegans Ro60 protein Genetics 151 143 150 9872955 PMC1460465
  46. Lal A Mazan-Mamczarz K Kawai T Yang X Martindale JL Gorospe M 2004 Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs The EMBO Journal 23 3092 3102 10.1038/sj.emboj.7600305 15257295 PMC514922 · DOI · Paper page
  47. Langmead B Trapnell C Pop M Salzberg SL 2009 Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biology 10 R25 10.1186/gb-2009-10-3-r25 19261174 PMC2690996 · DOI · Paper page
  48. Lee EB Lee VM-Y Trojanowski JQ 2012 Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration Nature Reviews Neuroscience 13 38 50 10.1038/nrn3121 10.1038/nrn3121 22127299 PMC3285250 · DOI · Paper page
  49. Lerner M Boyle J Hardin J Steitz J 1981 Two novel classes of small ribonucleoproteins detected by antibodies associated with lupus erythematosus Science 211 400 402 10.1126/science.6164096 6164096 · DOI
  50. Licatalosi DD Darnell RB 2006 Splicing regulation in neurologic disease Neuron 52 93 101 10.1016/j.neuron.2006.09.017 17015229 · DOI
  51. Licatalosi DD Darnell RB 2010 RNA processing and its regulation: global insights into biological networks Nature Reviews. Genetics 11 75 87 10.1038/nrg2673 PMC3229837 20019688 · DOI
  52. Licatalosi DD Yano M Fak JJ Mele A Grabinski SE Zhang C Darnell RB 2012 Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain Genes & Development 26 1626 1642 10.1101/gad.191338.112 22802532 PMC3404389 · DOI · Paper page
  53. Lynn DJ Winsor GL Chan C Richard N Laird MR Barsky A Gardy JL Roche FM Chan TH Shah N Lo R Naseer M Que J Yau M Acab M Tulpan D Whiteside MD Chikatamarla A Mah B Munzner T Hokamp K Hancock RE Brinkman FS 2008 InnateDB: facilitating systems-level analyses of the mammalian innate immune response Molecular Systems Biology 4 218 10.1038/msb.2008.55 18766178 PMC2564732 · DOI
  54. Ma'ayan A Jenkins SL Webb RL Berger SI Purushothaman SP Abul-Husn NS Posner JM Flores T Iyengar R 2009 SNAVI: desktop application for analysis and visualization of large-scale signaling networks BMC Systems Biology 3 10 10.1186/1752-0509-3-10 19154595 PMC2637233 · DOI
  55. Machanick P Bailey TL 2011 MEME-ChIP: motif analysis of large DNA datasets Bioinformatics 27 1696 1697 10.1093/bioinformatics/btr189 21486936 PMC3106185 · DOI
  56. Manley G Wong E Dalmau J Elkon K Posner J Furneaux H 1994 Sera from some patients with antibody-associated paraneoplastic encephalomyelitis/sensory neuronopathy recognize the ro-52K antigen Journal of Neuro-Oncology 19 105 112 7964985
  57. McCarthy DJ Chen Y Smyth GK 2012 Differential expression analysis of multifactor RNA-seq experiments with respect to biological variation Nucleic Acids Research 40 4288 4297 10.1093/nar/gks042 22287627 PMC3378882 · DOI · Paper page
  58. Mobarak CD Anderson KD Morin M Beckel-Mitchener A Rogers SL Furneaux H King P Perrone-Bizzozero NI 2000 The RNA-binding protein HuD is required for GAP-43 mRNA stability, GAP-43 gene expression, and PKC-dependent neurite outgrowth in PC12 cells Molecular Biology of the Cell 11 3191 3203 10.1091/mbc.11.9.3191 10982410 PMC14985 · DOI · Paper page
  59. Moffat J Grueneberg DA Yang X Kim SY Kloepfer AM Hinkle G Piqani B Eisenhaure TM Luo B Grenier JK Carpenter AE Foo SY Stewart SA Stockwell BR Hacohen N Hahn WC Lander ES Sabatini DM Root DE 2006 A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen Cell 124 1283 1298 10.1016/j.cell.2006.01.040 16564017 · DOI
  60. O'Reilly RC 2010 The what and how of prefrontal cortical organization Trends in Neurosciences 33 355 361 10.1016/j.tins.2010.05.002 20573407 PMC2916029 · DOI
  61. Okano HJ Darnell RB 1997 A hierarchy of hu RNA binding proteins in developing and adult neurons The Journal of Neuroscience 17 3024 3037 9096138 PMC6573636
  62. Parikh I Fardo DW Estus S 2014 Genetics of PICALM expression and alzheimer's disease PloS One 9 e10421 10.1371/journal.pone.0091242 PMC3949918 24618820 · DOI
  63. Pascale A Gusev PA Amadio M Dottorini T Govoni S Alkon DL Quattrone A 2004 Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory Proceedings of the National Academy of Sciences of the United States of America 101 1217 1222 10.1073/pnas.0307674100 14745023 PMC337033 · DOI · Paper page
  64. Perreault J Noël JF Brière F Cousineau B Lucier JF Perreault JP Boire G 2005 Retropseudogenes derived from the human Ro/SS-a autoantigen-associated hY RNAs Nucleic Acids Research 33 2032 2041 10.1093/nar/gki504 15817567 PMC1074747 · DOI
  65. Prasad TS Kandasamy K Pandey A 2009 Human protein reference database and human proteinpedia as discovery tools for systems biology Methods in Molecular Biology 577 67 79 10.1007/978-1-60761-232-2_6 19718509 · DOI
  66. Richter JD Klann E 2009 Making synaptic plasticity and memory last: mechanisms of translational regulation Genes & Development 23 1 11 10.1101/gad.1735809 19136621 · DOI
  67. Robinson MD McCarthy DJ Smyth GK 2010 EdgeR: a bioconductor package for differential expression analysis of digital gene expression data Bioinformatics 26 139 140 10.1093/bioinformatics/btp616 19910308 PMC2796818 · DOI · Paper page
  68. Robinson MD Oshlack A 2010 A scaling normalization method for differential expression analysis of RNA-seq data Genome Biology 11 R25 10.1186/gb-2010-11-3-r25 20196867 PMC2864565 · DOI · Paper page
  69. Robinson MD Smyth GK 2008 Small-sample estimation of negative binomial dispersion, with applications to SAGE data Biostatistics 9 321 332 10.1093/biostatistics/kxm030 17728317 · DOI · Paper page
  70. Sim S Weinberg DE Fuchs G Choi K Chung J Wolin SL 2009 The subcellular distribution of an RNA quality control protein, the ro autoantigen, is regulated by noncoding y RNA binding Molecular Biology of the Cell 20 1555 1564 10.1091/mbc.E08-11-1094 19116308 PMC2649258 · DOI
  71. Sim S Wolin SL 2011 Emerging roles for the ro 60-kDa autoantigen in noncoding RNA metabolism Wiley Interdisciplinary Reviews. RNA 2 686 699 10.1002/wrna.85 21823229 PMC3154076 · DOI
  72. Sim S Yao J Weinberg DE Niessen S Yates JR Wolin SL 2012 The zipcode-binding protein ZBP1 influences the subcellular location of the ro 60-kDa autoantigen and the noncoding Y3 RNA RNA 18 100 110 10.1261/rna.029207.111 22114317 PMC3261732 · DOI
  73. Sreedharan J Blair IP Tripathi VB Hu X Vance C Rogelj B Ackerley S Durnall JC Williams KL Buratti E Baralle F de Belleroche J Mitchell JD Leigh PN Al-Chalabi A Miller CC Nicholson G Shaw CE 2008 TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis Science 319 1668 1672 10.1126/science.1154584 18309045 PMC7116650 · DOI · Paper page
  74. Stark C Breitkreutz BJ Chatr-Aryamontri A Boucher L Oughtred R Livstone MS Nixon J Van Auken K Wang X Shi X Reguly T Rust JM Winter A Dolinski K Tyers M 2011 The BioGRID interaction database: 2011 update Nucleic Acids Research 39 D698 D704 10.1093/nar/gkq1116 21071413 PMC3013707 · DOI
  75. Stergachis AB Neph S Sandstrom R Haugen E Reynolds AP Zhang M Byron R Canfield T Stelhing-Sun S Lee K Thurman RE Vong S Bates D Neri F Diegel M Giste E Dunn D Vierstra J Hansen RS Johnson AK Sabo PJ Wilken MS Reh TA Treuting PM Kaul R Groudine M Bender MA Borenstein E Stamatoyannopoulos JA 2014 Conservation of trans-acting circuitry during mammalian regulatory evolution Nature 515 365 370 10.1038/nature13972 25409825 PMC4405208 · DOI · Paper page
  76. Storey JD Tibshirani R 2003 Statistical significance for genomewide studies Proceedings of the National Academy of Sciences of the United States of America 100 9440 9445 10.1073/pnas.1530509100 12883005 PMC170937 · DOI · Paper page
  77. Szabo A Dalmau J Manley G Rosenfeld M Wong E Henson J Posner JB Furneaux HM 1991 HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to elav and sex-lethal Cell 67 325 333 10.1016/0092-8674(91)90184-Z 1655278 · DOI · Paper page
  78. Tan MS Yu JT Tan L 2013 Bridging integrator 1 (bIN1): form, function, and alzheimer's disease Trends in Molecular Medicine 19 594 603 10.1016/j.molmed.2013.06.004 23871436 · DOI
  79. Ule J Jensen K Mele A Darnell RB 2005 CLIP: a method for identifying protein-RNA interaction sites in living cells Methods 37 376 386 10.1016/j.ymeth.2005.07.018 16314267 · DOI
  80. Vance C Rogelj B Hortobágyi T De Vos KJ Nishimura AL Sreedharan J Hu X Smith B Ruddy D Wright P Ganesalingam J Williams KL Tripathi V Al-Saraj S Al-Chalabi A Leigh PN Blair IP Nicholson G de Belleroche J Gallo JM Miller CC Shaw CE 2009 Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6 Science 323 1208 1211 10.1126/science.1165942 19251628 PMC4516382 · DOI
  81. Ward AJ Cooper TA 2009 The pathobiology of splicing The Journal of Pathology 10.1002/path.2649 PMC2855871 19918805 · DOI
  82. Wei WJ Mu SR Heiner M Fu X Cao LJ Gong XF Bindereif A Hui J 2012 YB-1 binds to CAUC motifs and stimulates exon inclusion by enhancing the recruitment of U2AF to weak polypyrimidine tracts Nucleic Acids Research 40 8622 8636 10.1093/nar/gks579 22730292 PMC3458536 · DOI · Paper page
  83. Wickham H 2007 Reshaping data with the reshape package Journal of Statistical Software 21 10.18637/jss.v021.i12 · DOI
  84. Wickham H 2009 Ggplot2: elegant graphics for data analysis Springer New York 10.1007/978-0-387-98141-3 10.1007/978-0-387-98141-3 · DOI · Paper page
  85. Wickham H 2011 The split-apply-combine strategy for data analysis Journal of Statistical Software 40 10.18637/jss.v040.i01 · DOI
  86. Wolin SL Belair C Boccitto M Chen X Sim S Taylor DW Wang HW 2013 Non-coding y RNAs as tethers and gates: insights from bacteria RNA Biology 10 10.4161/rna.26166 PMC3866240 24036917 · DOI
  87. Wurtmann EJ Wolin SL 2010 A role for a bacterial ortholog of the ro autoantigen in starvation-induced rRNA degradation Proceedings of the National Academy of Sciences of the United States of America 107 4022 4027 10.1073/pnas.1000307107 20160119 PMC2840137 · DOI
  88. Xenarios I Salwínski L Duan XJ Higney P Kim SM Eisenberg D 2002 DIP, the database of interacting proteins: a research tool for studying cellular networks of protein interactions Nucleic Acids Research 30 303 305 10.1093/nar/30.1.303 11752321 PMC99070 · DOI
  89. Xue D Shi H Smith JD Chen X Noe DA Cedervall T Yang DD Eynon E Brash DE Kashgarian M Flavell RA Wolin SL 2003 A lupus-like syndrome develops in mice lacking the ro 60-kDa protein, a major lupus autoantigen Proceedings of the National Academy of Sciences of the United States of America 100 7503 7508 10.1073/pnas.0832411100 12788971 PMC164616 · DOI
  90. Young LE Sanduja S Bemis-Standoli K Pena EA Price RL Dixon DA 2009 The mRNA binding proteins HuR and tristetraprolin regulate cyclooxygenase 2 expression during colon carcinogenesis Gastroenterology 136 1669 1679 10.1053/j.gastro.2009.01.010 19208339 PMC3742387 · DOI
  91. Yu TX Rao JN Zou T Liu L Xiao L Ouyang M Cao S Gorospe M Wang JY 2013 Competitive binding of CUGBP1 and HuR to occludin mRNA controls its translation and modulates epithelial barrier function Molecular Biology of the Cell 24 85 99 10.1091/mbc.E12-07-0531 23155001 PMC3541967 · DOI
  92. Zhang H Ma Q Zhang Yun-wu Xu H 2012 Proteolytic processing of alzheimer’s β-amyloid precursor protein Journal of Neurochemistry 120 9 21 10.1111/j.1471-4159.2011.07519.x 22122372 PMC3254787 · DOI

Cited by

Sorted by citations

Authors
Scheckel, C., Drapeau, E., Frias, M. A., Park, C. Y., Fak, J., Zucker-Scharff, I., Kou, Y., Haroutunian, V., Ma'ayan, A., Buxbaum, J. D., & Darnell, R. B.
Affiliations
  • Howard Hughes Medical Institute (US)
  • Icahn School of Medicine at Mount Sinai (US)
  • Laboratory of Molecular Neuro-Oncology, The Rockefeller University, New York, United States
  • James J. Peters VA Medical Center (US)
  • Department of Pharmacology and Systems Therapeutics, BD2K-LINCS Data Integration and Coordination Center, Mount Sinai Knowledge Management Center for Illuminating the Druggable Genome, Icahn School of Medicine at Mount Sinai, New York, United States
Corresponding author
  • Buxbaum, Joseph D
  • Darnell, Robert B
Venue
eLife
Published
2016-02-19
Volume
5
ISSN
2050-084X (ISSN-L)
OpenAlex
W2296696778
Cited by
139
References
15
Citations by year
2026: 6 · 2025: 10 · 2024: 10 · 2023: 12 · 2022: 15 · 2021: 22 · 2020: 22 · 2019: 11 · 2018: 16 · 2017: 9 · 2016: 6
FWCI
7.45
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • EMBO (Long-Term Fellowship)
  • SNF (Early and Advanced Postdoc Mobility Fellowship)
  • Seaver Foundation (Graduate Fellowship)
  • National Institutes of Health (ADRC AG005138, AG02219, HHSN27120130031C, R01GM098316, U54CA189201, U54HL127624, NS081706, NS34389)
  • G Harold and Leila Y. Mathers Foundation
  • Simons Foundation
  • Howard Hughes Medical Institute
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
RNA-binding proteins, RNA splicing regulation, Alzheimer's disease, differential splicing, 3' UTR binding, UV stress, neuroblastoma cells, human brain transcriptome, RNA-protein interactions
MeSH terms
Alzheimer Disease, Animals, Brain, Gene Expression Regulation, Humans, Neurons, Protein Binding, RNA Splicing, RNA, Messenger, Mice, Knockout, RNA, Untranslated, RNA Interference, Cell Line, Tumor, ELAV Proteins

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