期刊论文详细信息
BMC Molecular Biology
3′ terminal diversity of MRP RNA and other human noncoding RNAs revealed by deep sequencing
Thomas R Cech1  Katherine C Goldfarb2 
[1] Howard Hughes Medical Institute, University of Colorado, Boulder, CO, USA;Department of Chemistry and Biochemistry, BioFrontiers Institute, University of Colorado, Boulder, CO, USA
关键词: Telomerase RNA;    Oligo(A);    Oligo(U);    3′ RACE deep sequencing;    RNase MRP RNA;   
Others  :  1090664
DOI  :  10.1186/1471-2199-14-23
 received in 2013-08-02, accepted in 2013-09-13,  发布年份 2013
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【 摘 要 】

Background

Post-transcriptional 3′ end processing is a key component of RNA regulation. The abundant and essential RNA subunit of RNase MRP has been proposed to function in three distinct cellular compartments and therefore may utilize this mode of regulation. Here we employ 3′ RACE coupled with high-throughput sequencing to characterize the 3′ terminal sequences of human MRP RNA and other noncoding RNAs that form RNP complexes.

Results

The 3′ terminal sequence of MRP RNA from HEK293T cells has a distinctive distribution of genomically encoded termini (including an assortment of U residues) with a portion of these selectively tagged by oligo(A) tails. This profile contrasts with the relatively homogenous 3′ terminus of an in vitro transcribed MRP RNA control and the differing 3′ terminal profiles of U3 snoRNA, RNase P RNA, and telomerase RNA (hTR).

Conclusions

3′ RACE coupled with deep sequencing provides a valuable framework for the functional characterization of 3′ terminal sequences of noncoding RNAs.

【 授权许可】

   
2013 Goldfarb and Cech; licensee BioMed Central Ltd.

【 预 览 】
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【 参考文献 】
  • [1]Jones MR, Quinton LJ, Blahna MT, Neilson JR, Fu S, Ivanov AR, Wolf DA, Mizgerd JP: Zcchc11-dependent uridylation of microRNA directs cytokine expression. Nat Cell Biol 2009, 11:1157-1163.
  • [2]Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, Baek D, Johnston WK, Russ C, Luo S, Babiarz JE, et al.: Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev 2010, 24:992-1009.
  • [3]Heo I, Ha M, Lim J, Yoon MJ, Park JE, Kwon SC, Chang H, Kim VN: Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs. Cell 2012, 151:521-532.
  • [4]Choi YS, Patena W, Leavitt AD, McManus MT: Widespread RNA 3′-end oligouridylation in mammals. RNA 2012, 18:394-401.
  • [5]Chen Y, Sinha K, Perumal K, Reddy R: Effect of 3′ terminal adenylic acid residue on the uridylation of human small RNAs in vitro and in frog oocytes. RNA 2000, 6:1277-1288.
  • [6]Katoh T, Sakaguchi Y, Miyauchi K, Suzuki T, Kashiwabara S, Baba T, Suzuki T: Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev 2009, 23:433-438.
  • [7]Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Nishibu T, Ukekawa R, Funakoshi T, Kurokawa T, Suzuki H, Hayashizaki Y, Daub CO: A comprehensive survey of 3′ animal miRNA modification events and a possible role for 3′ adenylation in modulating miRNA targeting effectiveness. Genome Res 2010, 20:1398-1410.
  • [8]Lund E, Dahlberg JE: Cyclic 2′,3′-phosphates and nontemplated nucleotides at the 3′ end of spliceosomal U6 small nuclear RNA’s. Science 1992, 255:327-330.
  • [9]Grzechnik P, Kufel J: Polyadenylation linked to transcription termination directs the processing of snoRNA precursors in yeast. Mol Cell 2008, 32:247-258.
  • [10]van Hoof A, Lennertz P, Parker R: Yeast exosome mutants accumulate 3′-extended polyadenylated forms of U4 small Nuclear RNA and small nucleolar RNAs. Mol Cell Biol 2000, 20:441-452.
  • [11]Kiss T, Fayet E, Jady BE, Richard P, Weber M: Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. Cold Spring Harb Symp Quant Biol 2006, 71:407-417.
  • [12]Yuan Y, Reddy R: 5′ Flanking sequences of human MRP/7-2 RNA gene are required and sufficient for the transcription by RNA polymerase Ill. Biochim Biophys Acta 1991, 1089:33-39.
  • [13]Shadel GS, Buckenmeyer GA, Clayton DA, Schmitt ME: Mutational analysis of the RNA component of Saccharomyces cerevisiae RNase MRP reveals distinct nuclear phenotypes. Gene 2000, 245:175-184.
  • [14]Ridanpää M, van Eenennaam H, Pelin K, Chadwick R, Johnson C, Yuan B, van Venrooij W, Pruijn G, Salmela R, Rockas S, Mäkitie O, Kaitila I, de la Chapelle A: Mutations in the RNA component of RNase MRP cause a pleiotropic human disease, cartilage-hair hypoplasia. Cell 2001, 104:195-203.
  • [15]Welting TJ, Kikkert BJ, van Venrooij WJ, Pruijn GJ: Differential association of protein subunits with the human RNase MRP and RNase P complexes. RNA 2006, 12:1373-1382.
  • [16]Lopez MD, Rosenblad MA, Samuelsson T: Conserved and variable domains of RNase MRP RNA. RNA Biol 2009, 6:208-220.
  • [17]Chang DD, Clayton DA: A novel endoribonuclease cleaves at a priming site of mouse mitochondrial DNA replication. EMBO J 1987, 6:409-417.
  • [18]Chang DD, Clayton DA: A Mammalian mitochondrial RNA processing activity contains nucleus-encoded RNA. Science 1987, 235:1178-1184.
  • [19]Schmitt ME, Clayton DA: Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae. Mol Cell Biol 1993, 13:7935-7941.
  • [20]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, 15:1407-1416.
  • [21]Cai T, Aulds J, Gill T, Cerio M, Schmitt ME: The saccharomyces cerevisiae RNase mitochondrial RNA processing is critical for cell cycle progression at the end of mitosis. Genetics 2002, 161:1029-1042.
  • [22]Gill T, Cai T, Aulds J, Wierzbicki S, Schmitt ME: RNase MRP Cleaves the CLB2 mRNA to promote cell cycle progression: novel method of mRNA degradation. Mol Cell Biol 2004, 24:945-953.
  • [23]Jaag HM, Lu Q, Schmitt ME, Nagy PD: Role of RNase MRP in viral RNA degradation and RNA recombination. J Virol 2011, 85:243-253.
  • [24]Mattijssen S, Hinson ER, Onnekink C, Hermanns P, Zabel B, Cresswell P, Pruijn GJ: Viperin mRNA is a novel target for the human RNase MRP/RNase P endoribonuclease. Cell Mol Life Sci 2011, 68:2469-2480.
  • [25]Kiss T, Marshallsay C, Filipowicz W: 7-2/MRP RNAs in plant and mammalian cells: association with higher order structures in the nucleolus. EMBO J 1992, 11:3737-3746.
  • [26]Jacobson MR, Cao L, Wang Y, Pederson T: Dynamic localization of RNase MRP RNA in the nucleolus observed by fluorescent RNA cytochemistry in living cells. J Cell Biol 1995, 131:1649-1658.
  • [27]Gill T, Aulds J, Schmitt ME: A specialized processing body that is temporally and asymmetrically regulated during the cell cycle in Saccharomyces cerevisiae. J Cell Biol 2006, 173:35-45.
  • [28]Li K, Smagula CS, Parsons WJ, Richardson JA, Gonzalez M, Hagler HK, Williams RS: Subcellular partitioning of MRP RNA assessed by ultrastructural and biochemical analysis. J Cell Biology 1994, 124:871-882.
  • [29]Kiss T, Filipowicz W: Evidence against a mitochondrial location of the 7-2/MRP RNA in mammalian cells. Cell 1992, 70:11-16.
  • [30]Rosenblad MA, Lopez MD, Piccinelli P, Samuelsson T: Inventory and analysis of the protein subunits of the ribonucleases P and MRP provides further evidence of homology between the yeast and human enzymes. Nucleic Acids Res 2006, 34:5145-5156.
  • [31]Maida Y, Yasukawa M, Furuuchi M, Lassmann T, Possemato R, Okamoto N, Kasim V, Hayashizaki Y, Hahn WC, Masutomi K: An RNA-dependent RNA polymerase formed by TERT and the RMRP RNA. Nature 2009, 461:230-235.
  • [32]Zhuang F, Fuchs RT, Sun Z, Zheng Y, Robb GB: Structural bias in T4 RNA ligase-mediated 3′-adapter ligation. Nucleic Acids Res 2012, 40:e54.
  • [33]Wilusz JE, Whipple JM, Phizicky EM, Sharp PA: tRNAs marked with CCACCA are targeted for degradation. Science 2011, 334:817-821.
  • [34]Newman MA, Mani V, Hammond SM: Deep sequencing of microRNA precursors reveals extensive 3′ end modification. RNA 2011, 17:1795-1803.
  • [35]Hafner M, Renwick N, Brown M, Mihailovic A, Holoch D, Lin C, Pena JT, Nusbaum JD, Morozov P, Ludwig J, et al.: RNA-ligase-dependent biases in miRNA representation in deep-sequenced small RNA cDNA libraries. RNA 2011, 17:1697-1712.
  • [36]Scott DD, Norbury CJ: RNA decay via 3′ uridylation. Biochim Biophys Acta 1829, 2013:654-665.
  • [37]Cazenave C, Uhlenbeck OC: RNA template-directed RNA synthesis by T7 RNA polymerase. Proc Natl Acad Sci USA 1994, 91:6972-6976.
  • [38]Wagner SD, Yakovchuk P, Gilman B, Ponicsan SL, Drullinger LF, Kugel JF, Goodrich JA: RNA polymerase II acts as an RNA-dependent RNA polymerase to extend and destabilize a non-coding RNA. EMBO J 2013, 32:781-790.
  • [39]Mitchell JR, Cheng J, Collins K: A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3′ end. Mol Cell Biol 1999, 19:567-576.
  • [40]Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, et al.: The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 2012, 22:1775-1789.
  • [41]Tilgner H, Knowles DG, Johnson R, Davis CA, Chakrabortty S, Djebali S, Curado J, Snyder M, Gingeras TR, Guigo R: Deep sequencing of subcellular RNA fractions shows splicing to be predominantly co-transcriptional in the human genome but inefficient for lncRNAs. Genome Res 2012, 22:1616-1625.
  • [42]Li M, Wang IX, Li Y, Bruzel A, Richards AL, Toung JM, Cheung VG: Widespread RNA and DNA sequence differences in the human transcriptome. Science 2011, 333:53-58.
  • [43]Shchepachev V, Wischnewski H, Missiaglia E, Soneson C, Azzalin CM: Mpn1, mutated in poikiloderma with neutropenia protein 1, is a conserved 3′-to-5′ RNA exonuclease processing U6 small nuclear RNA. Cell Rep 2012, 2:855-865.
  • [44]Mroczek S, Krwawicz J, Kutner J, Lazniewski M, Kucinski I, Ginalski K, Dziembowski A: C16orf57, a gene mutated in poikiloderma with neutropenia, encodes a putative phosphodiesterase responsible for the U6 snRNA 3′ end modification. Genes Dev 2012, 26:1911-1925.
  • [45]Verheggen C, Lafontaine DL, Samarsky D, Mouaikel J, Blanchard JM, Bordonne R, Bertrand E: Mammalian and yeast U3 snoRNPs are matured in specific and related nuclear compartments. EMBO J 2002, 21:2736-2745.
  • [46]Boulon S, Marmier-Gourrier N, Pradet-Balade B, Wurth L, Verheggen C, Jady BE, Rothe B, Pescia C, Robert MC, Kiss T, et al.: The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 2008, 180:579-595.
  • [47]Zaug AJ, Lingner J, Cech TR: Method for determining RNA 3′ ends and application to human telomerase RNA. Nucleic Acids Res 1996, 24:532-533.
  • [48]Schmid M, Jensen TH: The exosome: a multipurpose RNA-decay machine. Trends Biochem Sci 2008, 33:501-510.
  • [49]Schneider C, Kudla G, Wlotzka W, Tuck A, Tollervey D: Transcriptome-wide analysis of exosome targets. Mol Cell 2012, 48:422-433.
  • [50]Schilders G, Raijmakers R, Raats JM, Pruijn GJ: MPP6 is an exosome-associated RNA-binding protein involved in 5.8S rRNA maturation. Nucleic Acids Res 2005, 33:6795-6804.
  • [51]Berndt H, Harnisch C, Rammelt C, Stohr N, Zirkel A, Dohm JC, Himmelbauer H, Tavanez JP, Huttelmaier S, Wahle E: Maturation of mammalian H/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming. RNA 2012, 18:958-972.
  • [52]Reddy R, Tan EM, Henning D, Nohga K, Busch H: Detection of a nucleolar 7–2 ribonucleoprotein and a cytoplasmic 8–2 ribonucleoprotein with autoantibodies from patients with scleroderma. J Biol Chem 1983, 258:1383-1386.
  • [53]Hashimoto C, Steitz JA: Sequential association of nucleolar 7–2 RNA with two different autoantigen. J Biol Chem 1983, 258:1379-1382.
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