Evolutionarily Conserved Polyadenosine RNA Binding Protein Nab2 Cooperates with Splicing Machinery To Regulate the Fate of Pre-mRNA

REFERENCES

• Moore MJ. 2005. From birth to death: the complex lives of eukaryotic mRNAs. Science 309:1514–1518. http://dx.doi.org/10.1126/science.1111443.
   PubMed Web of Science ®Google Scholar
• Singh G, Pratt G, Yeo GW, Moore MJ. 2015. The clothes make the mRNA: past and present trends in mRNP fashion. Annu Rev Biochem 84:325–354. http://dx.doi.org/10.1146/annurev-biochem-080111-092106.
   PubMed Web of Science ®Google Scholar
• Dreyfuss G, Kim VN, Kataoka N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3:195–205. http://dx.doi.org/10.1038/nrm760.
   PubMed Web of Science ®Google Scholar
• Niwa M, Berget SM. 1991. Mutation of the AAUAAA polyadenylation signal depresses in vitro splicing of proximal but not distal introns. Genes Dev 5:2086–2095. http://dx.doi.org/10.1101/gad.5.11.2086.
   PubMed Web of Science ®Google Scholar
• Nesic D, Cheng J, Maquat LE. 1993. Sequences within the last intron function in RNA 3′-end formation in cultured cells. Mol Cell Biol 13:3359–3369. http://dx.doi.org/10.1128/MCB.13.6.3359.
   PubMed Web of Science ®Google Scholar
• Cooke C, Hans H, Alwine JC. 1999. Utilization of splicing elements and polyadenylation signal elements in the coupling of polyadenylation and last-intron removal. Mol Cell Biol 19:4971–4979. http://dx.doi.org/10.1128/MCB.19.7.4971.
   PubMedGoogle Scholar
• Lutz CS, Alwine JC. 1994. Direct interaction of the U1 snRNP-A protein with the upstream efficiency element of the SV40 late polyadenylation signal. Genes Dev 8:576–586. http://dx.doi.org/10.1101/gad.8.5.576.
   PubMed Web of Science ®Google Scholar
• Gunderson SI, Beyer K, Martin G, Keller W, Boelens WC, Mattaj LW. 1994. The human U1A snRNP protein regulates polyadenylation via a direct interaction with poly(A) polymerase. Cell 76:531–541. http://dx.doi.org/10.1016/0092-8674(94)90116-3.
   PubMed Web of Science ®Google Scholar
• Gunderson SI, Polycarpou-Schwarz M, Mattaj IW. 1998. U1 snRNP inhibits pre-mRNA polyadenylation through a direct interaction between U1 70K and poly(A) polymerase. Mol Cell 1:255–264. http://dx.doi.org/10.1016/S1097-2765(00)80026-X.
   PubMed Web of Science ®Google Scholar
• Kyburz A, Friedlein A, Langen H, Keller W. 2006. Direct interactions between subunits of CPSF and the U2 snRNP contribute to the coupling of pre-mRNA 3′ end processing and splicing. Mol Cell 23:195–205. http://dx.doi.org/10.1016/j.molcel.2006.05.037.
   PubMedGoogle Scholar
• Vagner S, Vagner C, Mattaj IW. 2000. The carboxyl terminus of vertebrate poly(A) polymerase interacts with U2AF 65 to couple 3′-end processing and splicing. Genes Dev 14:403–413.
   PubMed Web of Science ®Google Scholar
• Millevoi S, Loulergue C, Dettwiler S, Karaa SZ, Keller W, Antoniou M, Vagner S. 2006. An interaction between U2AF 65 and CF I(m) links the splicing and 3′ end processing machineries. EMBO J 25:4854–4864. http://dx.doi.org/10.1038/sj.emboj.7601331.
   PubMed Web of Science ®Google Scholar
• Lykke-Andersen S, Jensen TH. 2015. Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat Rev Mol Cell Biol 16:665–677. http://dx.doi.org/10.1038/nrm4063.
   PubMed Web of Science ®Google Scholar
• Siwaszek A, Ukleja M, Dziembowski A. 2014. Proteins involved in the degradation of cytoplasmic mRNA in the major eukaryotic model systems. RNA Biol 11:1122–1136. http://dx.doi.org/10.4161/rna.34406.
   PubMed Web of Science ®Google Scholar
• van Hoof A, Wagner EJ. 2011. A brief survey of mRNA surveillance. Trends Biochem Sci 36:585–592. http://dx.doi.org/10.1016/j.tibs.2011.07.005.
   PubMed Web of Science ®Google Scholar
• Legrain P, Seraphin B, Rosbash M. 1988. Early commitment of yeast pre-mRNA to the spliceosome pathway. Mol Cell Biol 8:3755–3760. http://dx.doi.org/10.1128/MCB.8.9.3755.
   PubMedGoogle Scholar
• Rutz B, Seraphin B. 1999. Transient interaction of BBP/ScSF1 and Mud2 with the splicing machinery affects the kinetics of spliceosome assembly. RNA 5:819–831. http://dx.doi.org/10.1017/S1355838299982286.
   PubMedGoogle Scholar
• Abovich N, Rosbash M. 1997. Cross-intron bridging interactions in the yeast commitment complex are conserved in mammals. Cell 89:403–412. http://dx.doi.org/10.1016/S0092-8674(00)80221-4.
   PubMed Web of Science ®Google Scholar
• Kistler AL, Guthrie C. 2001. Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for sub2, an essential spliceosomal ATPase. Genes Dev 15:42–49. http://dx.doi.org/10.1101/gad.851301.
   PubMed Web of Science ®Google Scholar
• Rymond BC. 2010. The branchpoint binding protein: in and out of the spliceosome cycle. Adv Exp Med Biol 693:123–141. http://dx.doi.org/10.1007/978-1-4419-7005-3_9.
   PubMedGoogle Scholar
• Palancade B, Zuccolo M, Loeillet S, Nicolas A, Doye V. 2005. Pml39, a novel protein of the nuclear periphery required for nuclear retention of improper messenger ribonucleoparticles. Mol Biol Cell 16:5258–5268. http://dx.doi.org/10.1091/mbc.E05-06-0527.
   PubMed Web of Science ®Google Scholar
• Galy V, Gadal O, Fromont-Racine M, Romano A, Jacquier A, Nehrbass U. 2004. Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 116:63–73. http://dx.doi.org/10.1016/S0092-8674(03)01026-2.
   PubMed Web of Science ®Google Scholar
• Saroufim MA, Bensidoun P, Raymond P, Rahman S, Krause MR, Oeffinger M, Zenklusen D. 2015. The nuclear basket mediates perinuclear mRNA scanning in budding yeast. J Cell Biol 211:1131–1140. http://dx.doi.org/10.1083/jcb.201503070.
   PubMed Web of Science ®Google Scholar
• Fasken MB, Corbett AH. 2005. Process or perish: quality control in mRNA biogenesis. Nat Struct Mol Biol 12:482–488. http://dx.doi.org/10.1038/nsmb945.
   PubMed Web of Science ®Google Scholar
• Hilleren PJ, Parker R. 2003. Cytoplasmic degradation of splice-defective pre-mRNAs and intermediates. Mol Cell 12:1453–1465. http://dx.doi.org/10.1016/S1097-2765(03)00488-X.
   PubMedGoogle Scholar
• Semlow DR, Staley JP. 2012. Staying on message: ensuring fidelity in pre-mRNA splicing. Trends Biochem Sci 37:263–273. http://dx.doi.org/10.1016/j.tibs.2012.04.001.
   PubMed Web of Science ®Google Scholar
• Chlebowski A, Lubas M, Jensen TH, Dziembowski A. 2013. RNA decay machines: the exosome. Biochim Biophys Acta 1829:552–560. http://dx.doi.org/10.1016/j.bbagrm.2013.01.006.
   PubMed Web of Science ®Google Scholar
• Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D. 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 91:457–466. http://dx.doi.org/10.1016/S0092-8674(00)80432-8.
   PubMed Web of Science ®Google Scholar
• Garneau NL, Wilusz J, Wilusz CJ. 2007. The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8:113–126. http://dx.doi.org/10.1038/nrm2104.
   PubMed Web of Science ®Google Scholar
• Abovich N, Liao XC, Rosbash M. 1994. The yeast MUD2 protein: an interaction with PRP11 defines a bridge between commitment complexes and U2 snRNP addition. Genes Dev 8:843–854. http://dx.doi.org/10.1101/gad.8.7.843.
   PubMed Web of Science ®Google Scholar
• Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D. 1999. Functions of the exosome in rRNA, snoRNA, and snRNA synthesis. EMBO J 18:5399–5410. http://dx.doi.org/10.1093/emboj/18.19.5399.
   PubMed Web of Science ®Google Scholar
• Allmang C, Mitchell P, Petfalski E, Tollervey D. 2000. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res 28:1684–1691. http://dx.doi.org/10.1093/nar/28.8.1684.
   PubMed Web of Science ®Google Scholar
• Milligan L, Torchet C, Allmang C, Shipman T, Tollervey D. 2005. A nuclear surveillance pathway for mRNAs with defective polyadenylation. Mol Cell Biol 25:9996–10004. http://dx.doi.org/10.1128/MCB.25.22.9996-10004.2005.
   PubMedGoogle Scholar
• Bousquet-Antonelli C, Presutti C, Tollervey D. 2000. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102:765–775. http://dx.doi.org/10.1016/S0092-8674(00)00065-9.
   PubMed Web of Science ®Google Scholar
• Jensen TH, Dower K, Libri D, Rosbash M. 2003. Early formation of mRNP: license for export or quality control? Mol Cell 11:1129–1138. http://dx.doi.org/10.1016/S1097-2765(03)00191-6.
   PubMedGoogle Scholar
• Vinciguerra P, Stutz F. 2004. mRNA export: an assembly line from genes to nuclear pores. Curr Opin Cell Biol 16:285–292. http://dx.doi.org/10.1016/j.ceb.2004.03.013.
   PubMedGoogle Scholar
• Lykke-Andersen S, Tomecki R, Jensen TH, Dziembowski A. 2011. The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol 8:61–66. http://dx.doi.org/10.4161/rna.8.1.14237.
   PubMed Web of Science ®Google Scholar
• LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, Tollervey D. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121:713–724. http://dx.doi.org/10.1016/j.cell.2005.04.029.
   PubMed Web of Science ®Google Scholar
• Hector RE, Nykamp KR, Dheur S, Anderson JT, Non PJ, Urbinati CR, Wilson SM, Minvielle-Sebastia L, Swanson MS. 2002. Dual requirement for yeast hnRNP Nab2p in mRNA poly(A) tail length control and nuclear export. EMBO J 21:1800–1810. http://dx.doi.org/10.1093/emboj/21.7.1800.
   PubMed Web of Science ®Google Scholar
• Green DM, Marfatia KA, Crafton EB, Zhang X, Cheng X, Corbett AH. 2002. Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p. J Biol Chem 277:7752–7760. http://dx.doi.org/10.1074/jbc.M110053200.
   PubMed Web of Science ®Google Scholar
• Kelly SM, Pabit SA, Kitchen CM, Guo P, Marfatia KA, Murphy TJ, Corbett AH, Berland KM. 2007. Recognition of polyadenosine RNA by zinc finger proteins. Proc Natl Acad Sci U S A 104:12306–12311. http://dx.doi.org/10.1073/pnas.0701244104.
   PubMed Web of Science ®Google Scholar
• Anderson JT, Wilson SM, Datar KV, Swanson MS. 1993. NAB2: a yeast nuclear polyadenylated RNA-binding protein essential for cell viability. Mol Cell Biol 13:2730–2741. http://dx.doi.org/10.1128/MCB.13.5.2730.
   PubMed Web of Science ®Google Scholar
• Schmid M, Poulsen MB, Olszewski P, Pelechano V, Saguez C, Gupta I, Steinmetz LM, Moore C, Jensen TH. 2012. Rrp6p controls mRNA poly(A) tail length and its decoration with poly(A) binding proteins. Mol Cell 47:267–280. http://dx.doi.org/10.1016/j.molcel.2012.05.005.
   PubMed Web of Science ®Google Scholar
• Schmid M, Olszewski P, Pelechano V, Gupta I, Steinmetz LM, Jensen TH. 2015. The nuclear polyA-binding protein Nab2p is essential for mRNA production. Cell Rep 12:128–139. http://dx.doi.org/10.1016/j.celrep.2015.06.008.
   PubMed Web of Science ®Google Scholar
• Perreault A, Lemieux C, Bachand F. 2007. Regulation of the nuclear poly(A)-binding protein by arginine methylation in fission yeast. J Biol Chem 282:7552–7562.
   PubMed Web of Science ®Google Scholar
• Lemieux C, Marguerat S, Lafontaine J, Barbezier N, Bahler J, Bachand F. 2011. A pre-mRNA degradation pathway that selectively targets intron-containing genes requires the nuclear poly(A)-binding protein. Mol Cell 44:108–119. http://dx.doi.org/10.1016/j.molcel.2011.06.035.
   PubMed Web of Science ®Google Scholar
• St-Sauveur VG, Soucek S, Corbett AH, Bachand F. 2013. Poly(A) tail-mediated gene regulation by opposing roles of Nab2 and Pab2 nuclear poly(A)-binding proteins in pre-mRNA decay. Mol Cell Biol 33:4718–4731. http://dx.doi.org/10.1128/MCB.00887-13.
   PubMedGoogle Scholar
• Leung S, Apponi L, Cornejo O, Kitchen C, Valentini S, Pavlath G, Dunham C, Corbett A. 2009. Splice variants of the human ZC3H14 gene generate multiple isoforms of a zinc finger polyadenosine RNA binding protein. Gene 439:71–78. http://dx.doi.org/10.1016/j.gene.2009.02.022.
   PubMedGoogle Scholar
• Kelly SM, Leung SW, Pak C, Banerjee A, Moberg KH, Corbett AH. 2014. A conserved role for the zinc finger polyadenosine RNA binding protein, ZC3H14, in control of poly(A) tail length. RNA 20:681–688. http://dx.doi.org/10.1261/rna.043984.113.
   PubMed Web of Science ®Google Scholar
• Pak C, Garshasbi M, Kahrizi K, Gross C, Apponi LH, Noto JJ, Kelly SM, Leung SW, Tzschach A, Behjati F, Abedini SS, Mohseni M, Jensen LR, Hu H, Huang B, Stahley SN, Liu G, Williams KR, Burdick S, Feng Y, Sanyal S, Bassell GJ, Ropers HH, Najmabadi H, Corbett AH, Moberg KH, Kuss AW. 2011. Mutation of the conserved polyadenosine RNA binding protein, ZC3H14/dNab2, impairs neural function in Drosophila and humans. Proc Natl Acad Sci U S A 108:12390–12395. http://dx.doi.org/10.1073/pnas.1107103108.
   PubMed Web of Science ®Google Scholar
• Kelly S, Pak C, Garshasbi M, Kuss A, Corbett AH, Moberg K. 2012. New kid on the ID block: neural functions of the Nab2/ZC3H14 class of Cys(3)His tandem zinc-finger polyadenosine RNA binding proteins. RNA Biol 9:555–562. http://dx.doi.org/10.4161/rna.20187.
   PubMed Web of Science ®Google Scholar
• Guthrie CR, Greenup L, Leverenz JB, Kraemer BC. 2011. MSUT2 is a determinant of susceptibility to tau neurotoxicity. Hum Mol Genet 20:1989–1999. http://dx.doi.org/10.1093/hmg/ddr079.
   PubMedGoogle Scholar
• Miyakura S, Hara M. 2015. Molecular characterization of UKp83/68, a widespread nuclear proteins that bind poly(A) and colocalize with a nuclear Speckle's component. J Med Dent Sci 62:43–56. http://dx.doi.org/10.11480/620203.
   PubMedGoogle Scholar
• Klass DM, Scheibe M, Butter F, Hogan GJ, Mann M, Brown PO. 2013. Quantitative proteomic analysis reveals concurrent RNA-protein interactions and identifies new RNA-binding proteins in Saccharomyces cerevisiae. Genome Res 23:1028–1038. http://dx.doi.org/10.1101/gr.153031.112.
   PubMed Web of Science ®Google Scholar
• Ausubel MF, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 2001. Current protocols in molecular biology. John Wiley & Sons, New York, NY.
   Google Scholar
• Wach A, Brachat A, Pohlmann R, Philippsen P. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793–1808. http://dx.doi.org/10.1002/yea.320101310.
   PubMed Web of Science ®Google Scholar
• Chang J, Schwer B, Shuman S. 2010. Mutational analyses of trimethylguanosine synthase (Tgs1) and Mud2: proteins implicated in pre-mRNA splicing. RNA 16:1018–1031. http://dx.doi.org/10.1261/rna.2082610.
   PubMedGoogle Scholar
• Chomczynski P. 1993. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 15:532–537.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. http://dx.doi.org/10.1006/meth.2001.1262.
   PubMed Web of Science ®Google Scholar
• Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. 2007. Rapid, transcript-specific changes in splicing in response to environmental stress. Mol Cell 27:928–937. http://dx.doi.org/10.1016/j.molcel.2007.07.018.
   PubMed Web of Science ®Google Scholar
• de Hoon MJ, Imoto S, Nolan J, Miyano S. 2004. Open source clustering software. Bioinformatics 20:1453–1454. http://dx.doi.org/10.1093/bioinformatics/bth078.
   PubMed Web of Science ®Google Scholar
• Umen JG, Guthrie C. 1995. Prp16p, Slu7p, and Prp8p interact with the 3′ splice site in two distinct stages during the second catalytic step of pre-mRNA splicing. RNA 1:584–597.
   PubMedGoogle Scholar
• Boeke JD, Trueheart J, Natsoulis G, Fink GR. 1987. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol 154:164–175. http://dx.doi.org/10.1016/0076-6879(87)54076-9.
   PubMed Web of Science ®Google Scholar
• Chekanova JA, Belostotsky DA. 2003. Evidence that poly(A) binding protein has an evolutionarily conserved function in facilitating mRNA biogenesis and export. RNA 9:1476–1490. http://dx.doi.org/10.1261/rna.5128903.
   PubMedGoogle Scholar
• Minvielle-Sebastia L, Winsor B, Bonneaud N, Lacroute F. 1991. Mutations in the yeast RNA14 and RNA15 genes result in an abnormal mRNA decay rate: sequence analysis reveals an RNA-binding domain in the RNA15 protein. Mol Cell Biol 11:3075–3087. http://dx.doi.org/10.1128/MCB.11.6.3075.
   PubMedGoogle Scholar
• Wong DH, Corbett AH, Kent HM, Stewart M, Silver PA. 1997. Interaction between the small GTPase Ran/Gsp1p and Ntf2p is required for nuclear transport. Mol Cell Biol 17:3755–3767. http://dx.doi.org/10.1128/MCB.17.7.3755.
   PubMedGoogle Scholar
• Dammer EB, Duong DM, Diner I, Gearing M, Feng Y, Lah JJ, Levey AI, Seyfried NT. 2013. Neuron enriched nuclear proteome isolated from human brain. J Proteome Res 12:3193–3206. http://dx.doi.org/10.1021/pr400246t.
   PubMed Web of Science ®Google Scholar
• Herskowitz JH, Seyfried NT, Gearing M, Kahn RA, Peng J, Levey AI, Lah JJ. 2011. Rho kinase II phosphorylation of the lipoprotein receptor LR11/SORLA alters amyloid-beta production. J Biol Chem 286:6117–6127. http://dx.doi.org/10.1074/jbc.M110.167239.
   PubMed Web of Science ®Google Scholar
• Zambon AC, Gaj S, Ho I, Hanspers K, Vranizan K, Evelo CT, Conklin BR, Pico AR, Salomonis N. 2012. GO-Elite: a flexible solution for pathway and ontology over-representation. Bioinformatics 28:2209–2210. http://dx.doi.org/10.1093/bioinformatics/bts366.
   PubMed Web of Science ®Google Scholar
• Marfatia KA, Crafton EB, Green DM, Corbett AH. 2003. Domain analysis of the Saccharomyces cerevisiae heterogeneous nuclear ribonucleoprotein, Nab2p: dissecting the requirements for Nab2p-facilitated poly(A) RNA export. J Biol Chem 278:6731–6740.
   PubMedGoogle Scholar
• Kelly SM, Leung SW, Apponi LH, Bramley AM, Tran EJ, Chekanova JA, Wente SR, Corbett AH. 2010. Recognition of polyadenosine RNA by the zinc finger domain of nuclear poly(A) RNA-binding protein 2 (Nab2) is required for correct mRNA 3′-end formation. J Biol Chem 285:26022–26032. http://dx.doi.org/10.1074/jbc.M110.141127.
   PubMedGoogle Scholar
• Kim SH, Lin RJ. 1996. Spliceosome activation by PRP2 ATPase prior to the first transesterification reaction of pre-mRNA splicing. Mol Cell Biol 16:6810–6819. http://dx.doi.org/10.1128/MCB.16.12.6810.
   PubMed Web of Science ®Google Scholar
• King DS, Beggs JD. 1990. Interactions of PRP2 protein with pre-mRNA splicing complexes in Saccharomyces cerevisiae. Nucleic Acids Res 18:6559–6564. http://dx.doi.org/10.1093/nar/18.22.6559.
   PubMedGoogle Scholar
• Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. 2007. Transcript specificity in yeast pre-mRNA splicing revealed by mutations in core spliceosomal components. PLoS Biol 5:e90. http://dx.doi.org/10.1371/journal.pbio.0050090.
   PubMed Web of Science ®Google Scholar
• Yan D, Perriman R, Igel H, Howe KJ, Neville M, Ares M, Jr. 1998. CUS2, a yeast homolog of human Tat-SF1, rescues function of misfolded U2 through an unusual RNA recognition motif. Mol Cell Biol 18:5000–5009. http://dx.doi.org/10.1128/MCB.18.9.5000.
   PubMed Web of Science ®Google Scholar
• Wang Q, Zhang L, Lynn B, Rymond BC. 2008. A BBP-Mud2p heterodimer mediates branchpoint recognition and influences splicing substrate abundance in budding yeast. Nucleic Acids Res 36:2787–2798. http://dx.doi.org/10.1093/nar/gkn144.
   PubMed Web of Science ®Google Scholar
• Rain JC, Legrain P. 1997. In vivo commitment to splicing in yeast involves the nucleotide upstream from the branch site conserved sequence and the Mud2 protein. EMBO J 16:1759–1771. http://dx.doi.org/10.1093/emboj/16.7.1759.
   PubMedGoogle Scholar
• Xu YZ, Query CC. 2007. Competition between the ATPase Prp5 and branch region-U2 snRNA pairing modulates the fidelity of spliceosome assembly. Mol Cell 28:838–849. http://dx.doi.org/10.1016/j.molcel.2007.09.022.
   PubMed Web of Science ®Google Scholar
• Perriman R, Ares M, Jr. 2010. Invariant U2 snRNA nucleotides form a stem loop to recognize the intron early in splicing. Mol Cell 38:416–427. http://dx.doi.org/10.1016/j.molcel.2010.02.036.
   PubMed Web of Science ®Google Scholar
• Moehle EA, Ryan CJ, Krogan NJ, Kress TL, Guthrie C. 2012. The yeast SR-like protein Npl3 links chromatin modification to mRNA processing. PLoS Genet 8:e1003101. http://dx.doi.org/10.1371/journal.pgen.1003101.
   PubMed Web of Science ®Google Scholar
• Dziembowski A, Ventura AP, Rutz B, Caspary F, Faux C, Halgand F, Laprevote O, Seraphin B. 2004. Proteomic analysis identifies a new complex required for nuclear pre-mRNA retention and splicing. EMBO J 23:4847–4856. http://dx.doi.org/10.1038/sj.emboj.7600482.
   PubMed Web of Science ®Google Scholar
• Rain JC, Rafi Z, Rhani Z, Legrain P, Kramer A. 1998. Conservation of functional domains involved in RNA binding and protein-protein interactions in human and Saccharomyces cerevisiae pre-mRNA splicing factor SF1. RNA 4:551–565. http://dx.doi.org/10.1017/S1355838298980335.
   PubMedGoogle Scholar
• Valcarcel J, Gaur RK, Singh R, Green MR. 1996. Interaction of U2AF65 RS region with pre-mRNA branch point and promotion of base pairing with U2 snRNA. Science 273:1706–1709. http://dx.doi.org/10.1126/science.273.5282.1706.
   PubMed Web of Science ®Google Scholar
• Sickmier EA, Frato KE, Shen H, Paranawithana SR, Green MR, Kielkopf CL. 2006. Structural basis for polypyrimidine tract recognition by the essential pre-mRNA splicing factor U2AF65. Mol Cell 23:49–59. http://dx.doi.org/10.1016/j.molcel.2006.05.025.
   PubMed Web of Science ®Google Scholar
• Selenko P, Gregorovic G, Sprangers R, Stier G, Rhani Z, Kramer A, Sattler M. 2003. Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Mol Cell 11:965–976. http://dx.doi.org/10.1016/S1097-2765(03)00115-1.
   PubMed Web of Science ®Google Scholar
• Chang J, Schwer B, Shuman S. 2012. Structure-function analysis and genetic interactions of the yeast branchpoint binding protein Msl5. Nucleic Acids Res 40:4539–4552. http://dx.doi.org/10.1093/nar/gks049.
   PubMedGoogle Scholar
• Apponi LH, Kelly SM, Harreman MT, Lehner AN, Corbett AH, Valentini SR. 2007. An interaction between two RNA binding proteins, Nab2 and Pub1, links mRNA processing/export and mRNA stability. Mol Cell Biol 27:6569–6579. http://dx.doi.org/10.1128/MCB.00881-07.
   PubMedGoogle Scholar
• Brockmann C, Soucek S, Kuhlmann SI, Mills-Lujan K, Kelly SM, Yang JC, Iglesias N, Stutz F, Corbett AH, Neuhaus D, Stewart M. 2012. Structural basis for polyadenosine-RNA binding by Nab2 Zn fingers and its function in mRNA nuclear export. Structure 20:1007–1018. http://dx.doi.org/10.1016/j.str.2012.03.011.
   PubMedGoogle Scholar
• Green DM, Johnson CP, Hagan H, Corbett AH. 2003. The C-terminal domain of myosin-like protein 1 (Mlp1p) is a docking site for heterogeneous nuclear ribonucleoproteins that are required for mRNA export. Proc Natl Acad Sci U S A 100:1010–1015. http://dx.doi.org/10.1073/pnas.0336594100.
   PubMed Web of Science ®Google Scholar
• Vinciguerra P, Iglesias N, Camblong J, Zenklusen D, Stutz F. 2005. Perinuclear Mlp proteins downregulate gene expression in response to a defect in mRNA export. EMBO J 24:813–823. http://dx.doi.org/10.1038/sj.emboj.7600527.
   PubMed Web of Science ®Google Scholar
• Wilmes GM, Bergkessel M, Bandyopadhyay S, Shales M, Braberg H, Cagney G, Collins SR, Whitworth GB, Kress TL, Weissman JS, Ideker T, Guthrie C, Krogan NJ. 2008. A genetic interaction map of RNA-processing factors reveals links between Sem1/Dss1-containing complexes and mRNA export and splicing. Mol Cell 32:735–746. http://dx.doi.org/10.1016/j.molcel.2008.11.012.
   PubMed Web of Science ®Google Scholar
• Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, Prinz J, St Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M, Deshpande R, Li Z, Lin ZY, Liang W, Marback M, Paw J, San Luis BJ, Shuteriqi E, Tong AH, van Dyk N, Wallace IM, Whitney JA, Weirauch MT, Zhong G, Zhu H, Houry WA, Brudno M, Ragibizadeh S, Papp B, Pal C, Roth FP, Giaever G, Nislow C, Troyanskaya OG, Bussey H, Bader GD, Gingras AC, Morris QD, Kim PM, Kaiser CA, et al.. 2010. The genetic landscape of a cell. Science 327:425–431. http://dx.doi.org/10.1126/science.1180823.
   PubMed Web of Science ®Google Scholar
• Briggs MW, Burkard KT, Butler JS. 1998. Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J Biol Chem 273:13255–13263. http://dx.doi.org/10.1074/jbc.273.21.13255.
   PubMed Web of Science ®Google Scholar
• van Hoof A, Lennertz P, Parker R. 2000. Yeast exosome mutants accumulate 3′-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol Cell Biol 20:441–452. http://dx.doi.org/10.1128/MCB.20.2.441-452.2000.
   PubMedGoogle Scholar
• Vanacova S, Wolf J, Martin G, Blank D, Dettwiler S, Friedlein A, Langen H, Keith G, Keller W. 2005. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol 3:e189. http://dx.doi.org/10.1371/journal.pbio.0030189.
   PubMed Web of Science ®Google Scholar
• Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, Regnault B, Devaux F, Namane A, Seraphin B, Libri D, Jacquier A. 2005. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121:725–737. http://dx.doi.org/10.1016/j.cell.2005.04.030.
   PubMed Web of Science ®Google Scholar
• Sadoff BU, Heath-Pagliuso S, Castano IB, Zhu Y, Kieff FS, Christman MF. 1995. Isolation of mutants of Saccharomyces cerevisiae requiring DNA topoisomerase I. Genetics 141:465–479.
   PubMed Web of Science ®Google Scholar
• Iwanejko L, Smith KN, Loeillet S, Nicolas A, Fabre F. 1999. Disruption and functional analysis of six ORFs on chromosome XV: YOL117w, YOL115w (TRF4), YOL114c, YOL112w (MSB4), YOL111c, and YOL072w. Yeast 15:1529–1539. http://dx.doi.org/10.1002/(SICI)1097-0061(199910)15:14<1529::AID-YEA457>3.3.CO;2-P.
   PubMedGoogle Scholar
• Burkard KT, Butler JS. 2000. A nuclear 3′-5′ exonuclease involved in mRNA degradation interacts with poly(A) polymerase and the hnRNA protein Npl3p. Mol Cell Biol 20:604–616. http://dx.doi.org/10.1128/MCB.20.2.604-616.2000.
   PubMed Web of Science ®Google Scholar
• Warkocki Z, Odenwalder P, Schmitzova J, Platzmann F, Stark H, Urlaub H, Ficner R, Fabrizio P, Luhrmann R. 2009. Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat Struct Mol Biol 16:1237–1243. http://dx.doi.org/10.1038/nsmb.1729.
   PubMed Web of Science ®Google Scholar
• Schneider C, Kudla G, Wlotzka W, Tuck A, Tollervey D. 2012. Transcriptome-wide analysis of exosome targets. Mol Cell 48:422–433. http://dx.doi.org/10.1016/j.molcel.2012.08.013.
   PubMed Web of Science ®Google Scholar
• Gudipati RK, Xu Z, Lebreton A, Seraphin B, Steinmetz LM, Jacquier A, Libri D. 2012. Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell 48:409–421. http://dx.doi.org/10.1016/j.molcel.2012.08.018.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Aguilera C, Tous C, Babiano R, de la Cruz J, Luna R, Aguilera A. 2011. Nab2 functions in the metabolism of RNA driven by polymerases II and III. Mol Biol Cell 22:2729–2740. http://dx.doi.org/10.1091/mbc.E11-01-0055.
   PubMedGoogle Scholar
• Batisse J, Batisse C, Budd A, Bottcher B, Hurt E. 2009. Purification of nuclear poly(A)-binding protein Nab2 reveals association with the yeast transcriptome and a messenger ribonucleoprotein core structure. J Biol Chem 284:34911–34917. http://dx.doi.org/10.1074/jbc.M109.062034.
   PubMedGoogle Scholar
• Kuhlmann SI, Valkov E, Stewart M. 2014. Structural basis for the molecular recognition of polyadenosine RNA by Nab2 Zn fingers. Nucleic Acids Res 42:672–680. http://dx.doi.org/10.1093/nar/gkt876.
   PubMedGoogle Scholar
• Kim Guisbert K, Duncan K, Li H, Guthrie C. 2005. Functional specificity of shuttling hnRNPs revealed by genome-wide analysis of their RNA binding profiles. RNA 11:383–393. http://dx.doi.org/10.1261/rna.7234205.
   PubMed Web of Science ®Google Scholar
• Martinez-Lumbreras S, Santiveri CM, Mirassou Y, Zorrilla S, Perez-Canadillas JM. 2013. Two singular types of CCCH tandem zinc finger in Nab2p contribute to polyadenosine RNA recognition. Structure 21:1800–1811. http://dx.doi.org/10.1016/j.str.2013.07.019.
   PubMedGoogle Scholar
• Gabunilas J, Chanfreau G. 2016. Splicing-Mediated Autoregulation modulates Rpl22p expression in Saccharomyces cerevisiae. PLoS Genet 12:e1005999. http://dx.doi.org/10.1371/journal.pgen.1005999.
   PubMed Web of Science ®Google Scholar
• Hooks KB, Naseeb S, Parker S, Griffiths-Jones S, Delneri D. 2016. Novel intronic RNA structures contribute to maintenance of phenotype in Saccharomyces cerevisiae. Genetics 203:1469–1481. http://dx.doi.org/10.1534/genetics.115.185363.
   PubMedGoogle Scholar
• Tuck AC, Tollervey D. 2013. A transcriptome-wide atlas of RNP composition reveals diverse classes of mRNAs and lncRNAs. Cell 154:996–1009. http://dx.doi.org/10.1016/j.cell.2013.07.047.
   PubMed Web of Science ®Google Scholar
• Turowski TW, Lesniewska E, Delan-Forino C, Sayou C, Boguta M, Tollervey D. 2016. Global analysis of transcriptionally engaged yeast RNA polymerase III reveals extended tRNA transcripts. Genome Res 26:933–944. http://dx.doi.org/10.1101/gr.205492.116.
   PubMedGoogle Scholar
• Kress TL, Krogan NJ, Guthrie C. 2008. A single SR-like protein, Npl3, promotes pre-mRNA splicing in budding yeast. Mol Cell 32:727–734. http://dx.doi.org/10.1016/j.molcel.2008.11.013.
   PubMed Web of Science ®Google Scholar