Position-specific binding of FUS to nascent RNA regulates mRNA length

Genes and Development

Volumn 29, Issue 10, 2015, Pages 1045-1057

  Masuda, Akio ^a   Takeda, Jun Ichi ^a   Okuno, Tatsuya ^a   Okamoto, Takaaki ^a   Ohkawara, Bisei ^a   Ito, Mikako ^a   Ishigaki, Shinsuke ^a   Sobue, Gen ^a   Ohno, Kinji ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Alternative polyadenylation; CLIP; FUS; mRNA length; RNA polymerase II

Indexed keywords

CPSF160 PROTEIN; FUSED IN SARCOMA PROTEIN; MESSENGER RNA; PROTEIN; RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; PROTEIN BINDING; RNA BINDING PROTEIN; TRANSCRIPTOME;

3' UNTRANSLATED REGION; ALTERNATIVE POLYADENYLATION; ANALYTIC METHOD; ANIMAL CELL; ARTICLE; CAP ANALYSIS OF GENE EXPRESSION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CROSS LINKING IMMUNOPRECIPITATION; DOWN REGULATION; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; MOUSE; NERVE CELL; NONHUMAN; POLYA SEQUENCE; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN RNA BINDING; QUANTITATIVE ANALYSIS; RNA ANALYSIS; RNA PROCESSING; RNA SEQUENCE; RNA STRUCTURE; RNA TRANSCRIPTION; SEQUENCE ANALYSIS; UPREGULATION; ANIMAL; GENE EXPRESSION REGULATION; GENE SILENCING; HEK293 CELL LINE; HUMAN; METABOLISM; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; MICE; POLYADENYLATION; PROTEIN BINDING; RNA; RNA POLYMERASE II; RNA, MESSENGER; RNA-BINDING PROTEIN FUS; TRANSCRIPTOME;

EID: 84929584026     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.255737.114     Document Type: Article

References (55)

1. Avendano-Vazquez SE, Dhir A, Bembich S, Buratti E, Proudfoot N, Baralle FE. 2012. Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selection. Genes Dev 26: 1679–1684.
2. Bataille AR, Jeronimo C, Jacques PE, Laramee L, Fortin ME, Forest A, Bergeron M, Hanes SD, Robert F. 2012. A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Mol Cell 45: 158–170.
3. Beaudoing E, Freier S, Wyatt JR, Claverie JM, Gautheret D. 2000. Patterns of variant polyadenylation signal usage in human genes. Genome Res 10: 1001–1010.
4. Berg MG, Singh LN, Younis I, Liu Q, Pinto AM, Kaida D, Zhang Z, Cho S, Sherrill-Mix S, Wan L, et al. 2012. U1 snRNP determines mRNA length and regulates isoform expression. Cell 150: 53–64.
5. Bertolotti A, Lutz Y, Heard DJ, Chambon P, Tora L. 1996. hTAF(II) 68, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins TLS/FUS and EWS is associated with both TFIID and RNA polymerase II. EMBO J 15: 5022–5031.
6. Cernilogar FM, Onorati MC, Kothe GO, Burroughs AM, Parsi KM, Breiling A, Lo Sardo F, Saxena A, Miyoshi K, Siomi H, et al. 2011. Chromatin-associated RNA interference components contribute to transcriptional regulation in Drosophila. Nature 480: 391–395.
7. Couthouis J, Hart MP, Erion R, King OD, Diaz Z, Nakaya T, Ibrahim F, Kim HJ, Mojsilovic-Petrovic J, Panossian S, et al. 2012. Evaluating the role of the FUS/TLS-related gene EWSR1 in amyotrophic lateral sclerosis. Hum Mol Genet 21: 2899–2911.
8. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. 2003. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 4: P3.
9. Derti A, Garrett-Engele P, Macisaac KD, Stevens RC, Sriram S, Chen R, Rohl CA, Johnson JM, Babak T. 2012. A quantitative atlas of polyadenylation in five mammals. Genome Res 22: 1173–1183.
10. Di Giammartino DC, Nishida K, Manley JL. 2011. Mechanisms and consequences of alternative polyadenylation. Mol Cell 43: 853–866.
11. Fujioka Y, Ishigaki S, Masuda A, Iguchi Y, Udagawa T, Watanabe H, Katsuno M, Ohno K, Sobue G. 2013. FUS-regulated regionand cell-type-specific transcriptome is associated with cell selectivity in ALS/FTLD. Sci Rep 3: 2388.
12. Grosso AR, de Almeida SF, Braga J, Carmo-Fonseca M. 2012. Dynamic transitions in RNA polymerase II density profiles during transcription termination. Genome Res 22: 1447–1456.
13. Gruber AR, Martin G, Keller W, Zavolan M. 2014. Means to an end: mechanisms of alternative polyadenylation of messenger RNA precursors. Wiley Interdiscip Rev RNA 5: 183–196.
14. 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. Mol Cell 38: 576–589.
15. Hoell JI, Larsson E, Runge S, Nusbaum JD, Duggimpudi S, Farazi TA, Hafner M, Borkhardt A, Sander C, Tuschl T. 2011. RNA targets of wild-type and mutant FET family proteins. Nat Struct Mol Biol 18: 1428–1431.
16. Hsin JP, Manley JL. 2012. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev 26: 2119–2137.
17. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57.
18. Ishigaki S, Masuda A, Fujioka Y, Iguchi Y, Katsuno M, Shibata A, Urano F, Sobue G, Ohno K. 2012. Position-dependent FUS– RNA interactions regulate alternative splicing events and transcriptions. Sci Rep 2: 529.
19. Jenal M, Elkon R, Loayza-Puch F, van Haaften G, Kuhn U, Menzies FM, Oude Vrielink JA, Bos AJ, Drost J, Rooijers K, et al. 2012. The poly(A)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites. Cell 149: 538–553.
20. Ji X, Zhou Y, Pandit S, Huang J, Li H, Lin CY, Xiao R, Burge CB, Fu XD. 2013. SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell 153: 855–868.
21. Kaida D, Berg MG, Younis I, Kasim M, Singh LN, Wan L, Dreyfuss G. 2010. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468: 664–668.
22. Kanamori-Katayama M, Itoh M, Kawaji H, Lassmann T, Katayama S, Kojima M, Bertin N, Kaiho A, Ninomiya N, Daub CO, et al. 2011. Unamplified cap analysis of gene expression on a single-molecule sequencer. Genome Res 21: 1150–1159.
23. Kuehner JN, Pearson EL, Moore C. 2011. Unravelling the means to an end: RNA polymerase II transcription termination. Nat Rev Mol Cell Biol 12: 283–294.
24. Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C, Davis A, Gilchrist J, Kasarskis EJ, Munsat T, et al. 2009. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323: 1205–1208.
25. Lagier-Tourenne C, Polymenidou M, Cleveland DW. 2010. TDP 43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum Mol Genet 19: R46–R64.
26. Lagier-Tourenne C, Polymenidou M, Hutt KR, Vu AQ, Baughn M, Huelga SC, Clutario KM, Ling SC, Liang TY, Mazur C, et al. 2012. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat Neurosci 15: 1488–1497.
27. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, et al. 2008. HITSCLIP yields genome-wide insights into brain alternative RNA processing. Nature 456: 464–469.
28. Mackenzie IR, Rademakers R, Neumann M. 2010. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol 9: 995–1007.
29. Masuda A, Shen XM, Ito M, Matsuura T, Engel AG, Ohno K. 2008. hnRNP H enhances skipping of a nonfunctional exon P3A in CHRNA1 and a mutation disrupting its binding causes congenital myasthenic syndrome. Hum Mol Genet 17: 4022–4035.
30. Masuda A, Andersen HS, Doktor TK, Okamoto T, Ito M, Andresen BS, Ohno K. 2012. CUGBP1 and MBNL1 preferentially bind to 3′ UTRs and facilitate mRNA decay. Sci Rep 2: 209.
31. Menet JS, Rodriguez J, Abruzzi KC, Rosbash M. 2012. Nascent Seq reveals novel features of mouse circadian transcriptional regulation. eLife 1: e00011.
32. Munoz MJ, de la Mata M, Kornblihtt AR. 2010. The carboxy terminal domain of RNA polymerase II and alternative splicing. Trends Biochem Sci 35: 497–504.
33. Nag A, Narsinh K, Martinson HG. 2007. The poly(A)-dependent transcriptional pause is mediated by CPSF acting on the body of the polymerase. Nat Struct Mol Biol 14: 662–669.
34. Nakaya T, Alexiou P, Maragkakis M, Chang A, Mourelatos Z. 2013. FUS regulates genes coding for RNA-binding proteins in neurons by binding to their highly conserved introns. RNA 19: 498–509.
35. Rappsilber J, Ryder U, Lamond AI, Mann M. 2002. Large-scale proteomic analysis of the human spliceosome. Genome Res 12: 1231–1245.
36. Reppas NB, Wade JT, Church GM, Struhl K. 2006. The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol Cell 24: 747–757.
37. Rogelj B, Easton LE, Bogu GK, Stanton LW, Rot G, Curk T, Zupan B, Sugimoto Y, Modic M, Haberman N, et al. 2012. Widespread binding of FUS along nascent RNA regulates alternative splicing in the brain. Sci Rep 2: 603.
38. Schonemann L, Kuhn U, Martin G, Schafer P, Gruber AR, Keller W, Zavolan M, Wahle E. 2014. Reconstitution of CPSF active in polyadenylation: recognition of the polyadenylation signal by WDR33. Genes Dev 28: 2381–2393.
39. Schor IE, Rascovan N, Pelisch F, Allo M, Kornblihtt AR. 2009. Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing. Proc Natl Acad Sci 106: 4325–4330.
40. Schwartz JC, Ebmeier CC, Podell ER, Heimiller J, Taatjes DJ, Cech TR. 2012. FUS binds the CTD of RNA polymerase II and regulates its phosphorylation at Ser2. Genes Dev 26: 2690–2695.
41. Schwartz JC, Wang X, Podell ER, Cech TR. 2013. RNA seeds higher-order assembly of FUS protein. Cell Rep 5: 918–925.
42. Schwartz JC, Podell ER, Han SS, Berry JD, Eggan KC, Cech TR. 2014. FUS is sequestered in nuclear aggregates in ALS patient fibroblasts. Mol Biol Cell 25: 2571–2578.
43. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. 2005. Gene set enrichment analysis: a knowledgebased approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci 102: 15545–15550.
44. Tan AY, Manley JL. 2009. The TET family of proteins: functions and roles in disease. J Mol Cell Biol 1: 82–92.
45. Tan AY, Riley TR, Coady T, Bussemaker HJ, Manley JL. 2012. TLS/FUS (translocated in liposarcoma/fused in sarcoma) regulates target gene transcription via single-stranded DNA response elements. Proc Natl Acad Sci 109: 6030–6035.
46. Tian B, Manley JL. 2013. Alternative cleavage and polyadenylation: the long and short of it. Trends Biochem Sci 38: 312–320.
47. Ticozzi N, Vance C, Leclerc AL, Keagle P, Glass JD, McKenna Yasek D, Sapp PC, Silani V, Bosco DA, Shaw CE, et al. 2011. Mutational analysis reveals the FUS homolog TAF15 as a candidate gene for familial amyotrophic lateral sclerosis. Am J Med Genet B Neuropsychiatr Genet 156B: 285–290.
48. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L. 2013. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31: 46–53.
49. Vance C, Rogelj B, Hortobagyi T, De Vos KJ, Nishimura AL, Sreedharan J, Hu X, Smith B, Ruddy D, Wright P, et al. 2009. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323: 1208–1211.
50. Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK, Kurokawa R. 2008. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454: 126–130.
51. Yamazaki T, Chen S, Yu Y, Yan B, Haertlein TC, Carrasco MA, Tapia JC, Zhai B, Das R, Lalancette-Hebert M, et al. 2012. FUS–SMN protein interactions link the motor neuron diseases ALS and SMA. Cell Rep 2: 799–806.
52. Yang L, Embree LJ, Tsai S, Hickstein DD. 1998. Oncoprotein TLS interacts with serine-arginine proteins involved in RNA splicing. J Biol Chem 273: 27761–27764.
53. Yao C, Biesinger J, Wan J, Weng L, Xing Y, Xie X, Shi Y. 2012. Transcriptome-wide analyses of CstF64-RNA interactions in global regulation of mRNA alternative polyadenylation. Proc Natl Acad Sci 109: 18773–18778.
54. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. 2008. Model-based analysis of ChIP-seq (MACS). Genome Biol 9: R137.
55. Zhou Z, Licklider LJ, Gygi SP, Reed R. 2002. Comprehensive proteomic analysis of the human spliceosome. Nature 419: 182–185.