1,167
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

The cytoplasmic mRNA degradation factor Pat1 is required for rRNA processing

, &
Pages 455-465 | Received 11 Dec 2015, Accepted 09 Feb 2016, Published online: 28 Mar 2016

References

  • Pérez-Ortín JE, de Miguel-Jiménez L, Chávez S. Genome-wide studies of mRNA synthesis and degradation in eukaryotes. Biochim Biophys Acta 2012; 1819:604–15; PMID:22182827; http://dx.doi.org/10.1016/j.bbagrm.2011.12.002
  • Balagopal V, Fluch L, Nissan T. Ways and means of eukaryotic mRNA decay. Biochim Biophys Acta 2012; 1819:593–603; PMID:22266130; http://dx.doi.org/10.1016/j.bbagrm.2012.01.001
  • Parker R, Song H. The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 2004; 11:121–7; PMID:14749774; http://dx.doi.org/10.1038/nsmb724
  • Franks TM, Lykke-Andersen J. The Control of mRNA Decapping and P-Body Formation. Mol Cell 2008; 32:605–15; PMID:19061636; http://dx.doi.org/10.1016/j.molcel.2008.11.001
  • Nissan T, Rajyaguru P, She M, Song H, Parker R. Decapping Activators in Saccharomyces cerevisiae Act by Multiple Mechanisms. Molecular Cell 2010; 39:773–83; PMID:20832728; http://dx.doi.org/10.1016/j.molcel.2010.08.025
  • Marnef A, Standart N. Pat1 proteins: a life in translation, translation repression and mRNA decay. Biochem Soc Trans 2010; 38:1602; PMID:21118134; http://dx.doi.org/10.1042/BST0381602
  • Coller J, Parker R. General translational repression by activators of mRNA decapping. Cell 2005; 122:875–86; PMID:16179257; http://dx.doi.org/10.1016/j.cell.2005.07.012
  • Holmes LEA, Campbell SG, De Long SK, Sachs AB, Ashe MP. Loss of Translational Control in Yeast Compromised for the Major mRNA Decay Pathway. Mol Cell Biol 2004; 24:2998–3010; PMID:15024087; http://dx.doi.org/10.1128/MCB.24.7.2998-3010.2004
  • Pilkington GR, Parker R. Pat1 Contains Distinct Functional Domains That Promote P-Body Assembly and Activation of Decapping. Mol Cell Biol 2008; 28:1298–312; PMID:18086885; http://dx.doi.org/10.1128/MCB.00936-07
  • Tharun S, He W, Mayes AE, Lennertz P, Beggs JD, Parker R. Yeast Sm-like proteins function in mRNA decapping and decay. Nature 2000; 404:515–8; PMID:10761922; http://dx.doi.org/10.1038/35006-676
  • Bouveret E, Rigaut G, Shevchenko A, Wilm M, Séraphin B. A Sm-like protein complex that participates in mRNA degradation. EMBO J 2000; 19:1661–71; PMID:10747033; http://dx.doi.org/10.1093/emboj/19.7.1661
  • Haimovich G, Medina DA, Causse SZ, Garber M, Millán-Zambrano G, Barkai O, Chávez S, Pérez-Ortín JE, Darzacq X, Choder M. Gene Expression Is Circular: Factors for mRNA Degradation Also Foster mRNA Synthesis. Cell 2013; 153:1000–11; PMID:23706738; http://dx.doi.org/10.1016/j.cell.2013.05.012
  • Teixeira D, Parker R. Analysis of P-body assembly in Saccharomyces cerevisiae. Mol Biol Cell 2007; 18:2274–87; PMID:17429074; http://dx.doi.org/10.1091/mbc.E07-03-0199
  • Marnef A, Weil D, Standart N. RNA-related nuclear functions of human Pat1b, the P-body mRNA decay factor. Mol Biol Cell 2011; 23:213–24; PMID:22090346; http://dx.doi.org/10.1091/mbc.E11-05-0415
  • Wang X, Watt PM, Louis EJ, Borts RH, Hickson ID. Pat1: a topoisomerase II-associated protein required for faithful chromosome transmission in Saccharomyces cerevisiae. Nucleic Acids Res 1996; 24:4791–7; PMID:8972867; http://dx.doi.org/10.1093/nar/24.23.4791
  • Wang X, Watt PM, Borts RH, Louis EJ, Hickson ID. The topoisomerase II-associated protein, Pat1p, is required for maintenance of rDNA locus stability in Saccharomyces cerevisiae. Mol Gen Genet 1999; 261:831–40; PMID:10394921; http://dx.doi.org/10.1007/s004380050027
  • Sun M, Schwalb B, Pirkl N, Maier KC, Schenk A, Failmezger H, Tresch A, Cramer P. Global Analysis of Eukaryotic mRNA Degradation Reveals Xrn1-Dependent Buffering of Transcript Levels. Mol Cell 2013; 52:52–62; PMID:24119399; http://dx.doi.org/10.1016/j.molcel.2013.09.010
  • Hurto RL, Hopper AK. P-body components, Dhh1 and Pat1, are involved in tRNA nuclear-cytoplasmic dynamics. RNA 2011; 17:912–24; PMID:21398402; http://dx.doi.org/10.1261/rna.2558511
  • Kramer EB, Hopper AK. Retrograde transfer RNA nuclear import provides a new level of tRNA quality control in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2013; 110:21042–21047; PMID:24297920; http://dx.doi.org/10.1073/pnas.1316579110
  • Mishra PK, Ottmann AR, Basrai MA. Structural integrity of centromeric chromatin and faithful chromosome segregation requires Pat1. Genetics 2013; 195:369–79; PMID:23893485; http://dx.doi.org/10.1534/genetics.113.155291
  • Sharif H, Conti E. Architecture of the lsm1-7-pat1 complex: a conserved assembly in eukaryotic mRNA turnover. Cell Rep 2013; 5:283–91; PMID:24139796; http://dx.doi.org/10.1016/j.celrep.2013.10.004
  • He W, Parker R. Functions of Lsm proteins in mRNA degradation and splicing. Curr Opin Cell Biol 2000; 12:346–50; PMID:10801455; http://dx.doi.org/10.1016/S0955-0674(00)00098-3
  • Kufel J, Bousquet-Antonelli C, Beggs JD, Tollervey D. Nuclear pre-mRNA decapping and 5' degradation in yeast require the Lsm2-8p complex. Mol Cell Biol 2004; 24:9646–57; PMID:15485930; http://dx.doi.org/10.1128/MCB.24.21.9646-9657.2004
  • Kufel J. Lsm Proteins Are Required for Normal Processing and Stability of Ribosomal RNAs. J Biol Chem 2003; 278:2147–56; PMID:12438310; http://dx.doi.org/10.1074/jbc.M208856200
  • Séraphin B. Sm and Sm-like proteins belong to a large family: identification of proteins of the U6 as well as the U1, U2, U4 and U5 snRNPs. EMBO J 1995; 14:2089–98; PMID:7744014
  • Mayes AE. Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J 1999; 18:4321–31; PMID:10428970; http://dx.doi.org/10.1093/emboj/18.15.4321
  • Luhtala N, Parker R. LSM1 over-expression in Saccharomyces cerevisiae depletes U6 snRNA levels. Nucleic Acids Res 2009; 37:5529–36; PMID:19596813; http://dx.doi.org/10.1093/nar/gkp572
  • Bousquet-Antonelli C, Presutti C, Tollervey D. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 2000; 102:765–75; PMID:11030620; http://dx.doi.org/10.1016/S0092-8674(00)00065-9
  • Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 1999; 18:5399–410; PMID:10508172; http://dx.doi.org/10.1093/emboj/18.19.5399
  • Tollervey D, Kiss T. Function and synthesis of small nucleolar RNAs. Curr Opin Cell Biol 1997; 9:337–42; PMID:9159079; http://dx.doi.org/10.1016/S0955-0674(97)80005-1
  • Kufel J. A complex pathway for 3' processing of the yeast U3 snoRNA. Nucleic Acids Res 2003; 31:6788–97; PMID:14627812; http://dx.doi.org/10.1093/nar/gkg904
  • Antic S, Wolfinger MT, Skucha A, Hosiner S, Dorner S. General and MicroRNA-Mediated mRNA Degradation Occurs on Ribosome Complexes in Drosophila Cells. Mol Cell Biol 2015; 35:2309–20; PMID:25918245; http://dx.doi.org/10.1128/MCB.01346-14
  • Wyers F, Minet M, Dufour ME, Vo LT, Lacroute F. Deletion of the PAT1 gene affects translation initiation and suppresses a PAB1 gene deletion in yeast. Mol Cell Biol 2000; 20:3538–49; PMID:10779343; http://dx.doi.org/10.1128/MCB.20.10.3538-3549.2000
  • Wu D, Muhlrad D, Bowler MW, Jiang S, Liu Z, Parker R, Song H. Lsm2 and Lsm3 bridge the interaction of the Lsm1-7 complex with Pat1 for decapping activation. Cell Res 2014; 24:233–46; PMID:24247251; http://dx.doi.org/10.1038/cr.2013.152
  • Woolford JL, Baserga SJ. Ribosome Biogenesis in the Yeast Saccharomyces cerevisiae. Genetics 2013; 195:643–81; PMID:24190922; http://dx.doi.org/10.1534/genetics.113.153197
  • Li Z, Lee I, Moradi E, Hung N-J, Johnson AW, Marcotte EM. Rational Extension of the Ribosome Biogenesis Pathway Using Network-Guided Genetics. PLoS Biol 2009; 7:e1000213; PMID:19806183; http://dx.doi.org/10.1371/journal.pbio.1000213
  • KoS M, Koš M, Tollervey D. Yeast Pre-rRNA Processing and Modification Occur Cotranscriptionally. Molecular Cell 2010; 37:809–20; PMID:20347423; http://dx.doi.org/10.1016/j.molcel.2010.02.024
  • Venema J, Tollervey D. Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet 1999; 33:261–311; PMID:10690410; http://dx.doi.org/10.1146/annurev.genet.33.1.261
  • Kressler D, Linder P, la Cruz de J. Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol 1999; 19:7897–912; PMID:10567516; http://dx.doi.org/10.1128/MCB.19.12.7897
  • Allmang C, Mitchell P, Petfalski E, Tollervey D. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res 2000; 28:1684–91; PMID:10734186; http://dx.doi.org/10.1093/nar/28.8.1684
  • Kuai L, Fang F, Butler JS, Sherman F. Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2004; 101:8581–6; PMID:15173578; http://dx.doi.org/10.1073/pnas.0402888101
  • Wery M, Ruidant S, Schillewaert S, Lepore N, Lafontaine DL. The nuclear poly(A) polymerase and Exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA 2009; 15:406–19; PMID:19141608; http://dx.doi.org/10.1261/rna.1402709
  • Cole SE, LaRiviere FJ, Merrikh CN, Moore MJ. A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol Cell 2009; 34:440–50; PMID:19481524; http://dx.doi.org/10.1016/j.molcel.2009.04.017
  • He W, Parker R. The yeast cytoplasmic LsmI/Pat1p complex protects mRNA 3′ termini from partial degradation. Genetics 2001; 158:1445–55; PMID:11514438
  • Tansey WP. 6-azauracil sensitivity assay for yeast. CSH Protoc 2006; 2006; PMID:22484669
  • Laribee RN, Hosni-Ahmed A, Workman JJ, Chen H. Ccr4-Not Regulates RNA Polymerase I Transcription and Couples Nutrient Signaling to the Control of Ribosomal RNA Biogenesis; PLoS Genetics; 11(3); e1005113; PMID:25815716; http://dx.doi.org/10.1371/journal.pgen.1005113
  • Hage el A, French SL, Beyer AL, Tollervey D. Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev 2010; 24:1546–58; PMID:20634320; http://dx.doi.org/10.1101/gad.573310
  • Chowdhury A, Kalurupalle S, Tharun S. Pat1 contributes to the RNA binding activity of the Lsm1-7-Pat1 complex. RNA 2014; 20:1465–75; PMID:25035297; http://dx.doi.org/10.1261/rna.045252.114
  • Grzechnik P, Kufel J. Polyadenylation linked to transcription termination directs the processing of snoRNA precursors in yeast. Mol Cell 2008; 32:247–58; PMID:18951092; http://dx.doi.org/10.1016/j.molcel.2008.10.003
  • Schmid M, Poulsen M, Olszewski P, Pelechano V, Saguez C, Gupta I, Steinmetz L, Moore C, Jensen T, Poulsen M, et al. Rrp6p Controls mRNA Poly(A) Tail Length and Its Decoration with Poly(A) Binding Proteins. Molecular Cell 2012; 47:267–80; PMID:22683267; http://dx.doi.org/10.1016/j.molcel.2012.05.005
  • Tudek A, Porrua O, Kabzinski T, Lidschreiber M, Kubicek K, Fortova A, Lacroute F, Vanacova S, Cramer P, Stefl R, et al. Molecular basis for coordinating transcription termination with noncoding RNA degradation. Mol Cell 2014; 55:467–81; PMID:25066235; http://dx.doi.org/10.1016/j.molcel.2014.05.031
  • Houseley J, Kotovic K, Hage El A, Tollervey D. Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO J 2007; 26:4996–5006; PMID:18007593; http://dx.doi.org/10.1038/sj.emboj.7601921
  • Sadoff BU, Heath-Pagliuso S, Castaño IB, Zhu Y, Kieff FS, Christman MF. Isolation of mutants of Saccharomyces cerevisiae requiring DNA topoisomerase I. Genetics 1995; 141:465–79; PMID:8647385
  • Castaño IB, Brzoska PM, Sadoff BU, Chen H, Christman MF. Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae.
  • Pan X, Ye P, Yuan DS, Wang X, Bader JS, Boeke JD. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 2006; 124:1069–81; PMID:16487579; http://dx.doi.org/10.1016/j.cell.2005.12.036
  • Petfalski E, Dandekar T, Henry Y, Tollervey D. Processing of the precursors to small nucleolar RNAs and rRNAs requires common components. Mol Cell Biol 1998; 18:1181–9; PMID:9488433; http://dx.doi.org/10.1128/MCB.18.3.1181
  • Lindahl L, Bommankanti A, Li X, Hayden L, Jones A, Khan M, Oni T, Zengel JM. RNase MRP is required for entry of 35S precursor rRNA into the canonical processing pathway. RNA 2009; 15:1407–16; PMID:19465684; http://dx.doi.org/10.1261/rna.1302909
  • Arribere J, Doudna J, Gilbert W. Reconsidering Movement of Eukaryotic mRNAs between Polysomes and P Bodies. Mol Cell 2011; 44:745–58; PMID:22152478; http://dx.doi.org/10.1016/j.molcel.2011.09.019
  • Wang Y, Liu CL, Storey JD, Tibshirani RJ, Herschlag D, Brown PO. Precision and functional specificity in mRNA decay. Proc Natl Acad Sci USA 2002; 99:5860–5; PMID:11972065; http://dx.doi.org/10.1073/pnas.092538799
  • Grigull J, Mnaimneh S, Pootoolal J, Robinson MD, Hughes TR. Genome-Wide Analysis of mRNA Stability Using Transcription Inhibitors and Microarrays Reveals Posttranscriptional Control of Ribosome Biogenesis Factors. Mol Cell Biol 2004; 24:5534–47; PMID:15169913; http://dx.doi.org/10.1128/MCB.24.12.5534-5547.2004
  • Shalgi R, Lapidot M, Shamir R, Pilpel Y. A catalog of stability-associated sequence elements in 3' UTRs of yeast mRNAs. Genome Biol 2005; 6:R86; PMID:16207357; http://dx.doi.org/10.1186/gb-2005-6-10-r86
  • Chowdhury A, Tharun S. lsm1 mutations impairing the ability of the Lsm1p-7p-Pat1p complex to preferentially bind to oligoadenylated RNA affect mRNA decay in vivo. RNA 2008; 14:2149–58; PMID:18719247; http://dx.doi.org/10.1261/rna.1094208
  • Kressler D, Hurt E, Baßler J. Driving ribosome assembly. Biochim Biophys Acta 2010; 1803:673–83; PMID:19879902; http://dx.doi.org/10.1016/j.bbamcr.2009.10.009
  • Sopko R, Huang D, Preston N, Chua G, Papp B, Kafadar K, Snyder M, Oliver SG, Cyert M, Hughes TR, et al. Mapping Pathways and Phenotypes by Systematic Gene Overexpression. Molecular Cell 2006; 21:319–30; PMID:16455487; http://dx.doi.org/10.1016/j.molcel.2005.12.011
  • Jorgensen P. A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev 2004; 18:2491–505; PMID:15466158; http://dx.doi.org/10.1101/gad.1228804
  • Muhlrad D, Parker R. Premature translational termination triggers mRNA decapping. Nature 1994; 370:578–81; PMID:8052314; http://dx.doi.org/10.1038/370578a0
  • Nissan T, Parker R. Analyzing P-bodies in Saccharomyces cerevisiae. Meth Enzymol 2008; 448:507–20; PMID:19111192; http://dx.doi.org/10.1016/S0076-6879(08)02625-6
  • Coller JM, Tucker M, Sheth U, Valencia-Sanchez MA, Parker R. The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. RNA 2001; 7:1717–27; PMID:11780629; http://dx.doi.org/10.1017/S135583820101994X
  • Sambrook J, Russell DW. Sambrook: Molecular cloning. A laboratory manual. Third - Google Scholar. Cold pring Harbor Laboratory Press; 2001.
  • Tollervey D. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J 1987; 6:4169–75; PMID:3327689
  • Zhou Y, Chen C, Johansson MJO. The pre-mRNA retention and splicing complex controls tRNA maturation by promoting TAN1 expression. Nucleic Acids Research 2013; 41:5669–78; PMID:23605039; http://dx.doi.org/10.1093/nar/gkt269

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.