Metazoan tRNA introns generate stable circular RNAs in vivo

RNA

Volumn 21, Issue 9, 2015, Pages 1554-1565

  Lu, Zhipeng ^a   Filonov, Grigory S ^b   Noto, John J ^c   Schmidt, Casey A ^c   Hatkevich, Talia L ^c   Wen, Ying ^c   Jaffrey, Samie R ^b   Gregory Matera, A ^a,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Circular RNA; Expression system; Noncoding RNA ncRNA; TRNA processing

Indexed keywords

CIRCULAR RNA; RNA ISOFORM; TRANSFER RNA; UNCLASSIFIED DRUG; RNA; RNA, CIRCULAR; TRANSCRIPTOME;

ARTICLE; BIOGENESIS; BROCCOLI; CELLULAR DISTRIBUTION; DROSOPHILA; GENE EXPRESSION SYSTEM; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRON; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION; RNA DEGRADATION; RNA SEQUENCE; RNA SPLICING; RNA STABILITY; RNA STRUCTURE; RNA SYNTHESIS; RNA TRANSCRIPTION; SPINACH; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; FEMALE; GENETICS; HEK293 CELL LINE; MALE; METABOLISM; REPORTER GENE;

ANIMALIA; BRASSICA OLERACEA VAR. ITALICA; METAZOA; SPINACIA OLERACEA;

ANIMALS; DROSOPHILA; FEMALE; GENES, REPORTER; HEK293 CELLS; HUMANS; INTRONS; MALE; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA; RNA STABILITY; RNA, TRANSFER; TRANSCRIPTOME;

EID: 84939781879     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.052944.115     Document Type: Article

References (56)

1. Abelson J, Trotta CR, Li H. 1998. tRNA splicing. J Biol Chem 273: 12685-12688.
2. Altman S, Smith JD. 1971. Tyrosine tRNA precursor molecule polynu-cleotide sequence. Nat New Biol 233: 35-39.
3. Berezikov E, Robine N, Samsonova A, Westholm JO, Naqvi A, Hung JH, Okamura K, Dai Q, Bortolamiol-Becet D, Martin R, et al. 2011. Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome Res 21: 203-215.
4. Budde BS, Namavar Y, Barth PG, Poll-The BT, Nürnberg G, Becker C, van Ruissen F, Weterman MA, Fluiter K, te Beek ET, et al. 2008. tRNA splicing endonuclease mutations cause pontocerebellar hypo-plasia. Nat Genet 40: 1113-1118.
5. Capel B, Swain A, Nicolis S, Hacker A, Walter M, Koopman P, Goodfellow P, Lovell-Badge R. 1993. Circular transcripts of the tes-tis-determining gene Sry in adult mouse testis. Cell 73: 1019-1030.
6. ′ pre-tRNase). J Biol Chem 260: 9002-9008.
7. Chan PP, Lowe TM. 2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 37: D93-D97.
8. Cocquerelle C, Daubersies P, Majérus MA, Kerckaert JP, Bailleul B. 1992. Splicing with inverted order of exons occurs proximal to large introns. EMBO J 11: 1095-1098.
9. Danan M, Schwartz S, Edelheit S, Sorek R. 2012. Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res 40: 3131-3142.
10. Darty K, Denise A, Ponty Y. 2009. VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics 25: 1974-1975.
11. de Hoon MJ, Imoto S, Nolan J, Miyano S. 2004. Open source clustering software. Bioinformatics 20: 1453-1454.
12. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, et al. 2007. A genome-wide trans-genic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
13. ′-phosphate RNA splicing ligase characterization identifies the missing component in tRNA maturation. Proc Natl Acad Sci 108: 1290-1295.
14. Filonov GS, Moon JD, Svensen N, Jaffrey SR. 2014. Broccoli: rapid selection of an RNA mimic of green fluorescent protein by fluorescence-based selection and directed evolution. J Am Chem Soc 136: 16299-16308.
15. Ford E, Ares M Jr. 1994. Synthesis of circular RNA in bacteria and yeast using RNA cyclase ribozymes derived from a group I intron of phage T4. Proc Natl Acad Sci 91: 3117-3121.
16. Gardner EJ, Nizami ZF, Talbot CC Jr, Gall JG. 2012. Stable intronic sequence RNA (sisRNA), a new class of noncoding RNA from the oo-cyte nucleus of Xenopus tropicalis. Genes Dev 26: 2550-2559.
17. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, Yip KY, Robilotto R, Rechtsteiner A, Ikegami K, et al. 2010. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330: 1775-1787.
18. Good PD, Krikos AJ, Li SX, Bertrand E, Lee NS, Giver L, Ellington A, Zaia JA, Rossi JJ, Engelke DR. 1997. Expression of small, therapeutic RNAs in human cell nuclei. Gene Ther 4: 45-54.
19. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S. 1983. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35: 849-857.
20. Gustilo EM, Vendeix FA, Agris PF. 2008. tRNA's modifications bring order to gene expression. Curr Opin Microbiol 11: 134-140.
21. Hansen TB, Kjems J, Damgaard CK. 2013. Circular RNA and miR-7 in cancer. Cancer Res 73: 5609-5612.
22. Hentze MW, Preiss T. 2013. Circular RNAs: splicing's enigma variations. EMBO J 32: 923-925.
23. Hofacker IL. 2003. Vienna RNA secondary structure server. Nucleic Acids Res 31: 3429-3431.
24. Hofstetter H, Kressman A, Birnstiel ML. 1981. A split promoter for a eucaryotic tRNA gene. Cell 24: 573-585.
25. Jeck WR, Sharpless NE. 2014. Detecting and characterizing circular RNAs. Nat Biotechnol 32: 453-461.
26. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE. 2013. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19: 141-157.
27. Knapp G, Ogden RC, Peebles CL, Abelson J. 1979. Splicing of yeast tRNA precursors: structure of the reaction intermediates. Cell 18: 37-45.
28. Kosmaczewski SG, Edwards TJ, Han SM, Eckwahl MJ, Meyer BI, Peach S, Hesselberth JR, Wolin SL, Hammarlund M. 2014. The RtcB RNA ligase is an essential component of the metazoan unfolded protein response. EMBO Rep 15: 1278-1285.
29. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
30. Lasda E, Parker R. 2014. Circular RNAs: diversity of form and function. RNA 20: 1829-1842.
31. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
32. -ΔΔCt method. Methods 25: 402-408.
33. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
34. Lu Z, Matera AG. 2014. Vicinal: a method for the determination of ncRNA ends using chimeric reads from RNA-seq experiments. Nucleic Acids Res 42: e79.
35. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, et al. 2013. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495: 333-338.
36. Nigro JM, Cho KR, Fearon ER, Kern SE, Ruppert JM, Oliner JD, Kinzler KW, Vogelstein B. 1991. Scrambled exons. Cell 64: 607-613.
37. Pasman Z, Been MD, Garcia-Blanco MA. 1996. Exon circularization in mammalian nuclear extracts. RNA 2: 603-610.
38. Pellegrini O, Nezzar J, Marchfelder A, Putzer H, Condon C. 2003. Endonucleolytic processing of CCA-less tRNA precursors by RNase Z in Bacillus subtilis. EMBO J 22: 4534-4543.
39. Petkovic S, Müller S. 2015. RNA circularization strategies in vivo and in vitro. Nucleic Acids Res 43: 2454-2465.
40. Phizicky EM, Hopper AK. 2010. tRNA biology charges to the front. Genes Dev 24: 1832-1860.
41. Popow J, Englert M, Weitzer S, Schleiffer A, Mierzwa B, Mechtler K, Trowitzsch S, Will CL, Lührmann R, Söll D, et al. 2011. HSPC117 is the essential subunit of a human tRNA splicing ligase complex. Science 331: 760-764.
42. Popow J, Jurkin J, Schleiffer A, Martinez J. 2014. Analysis of orthologous groups reveals archease and DDX1 as tRNA splicing factors. Nature 511: 104-107.
43. Salgia SR, Singh SK, Gurha P, Gupta R. 2003. Two reactions of Haloferax volcanii RNA splicing enzymes: joining of exons and circularization of introns. RNA 9: 319-330.
44. Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO. 2012. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One 7: e30733.
45. Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO. 2013. Cell-type specific features of circular RNA expression. PLoS Genet 9: e1003777.
46. Schattner P, Brooks AN, Lowe TM. 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33: W686-W689.
47. Strack RL, Disney MD, Jaffrey SR. 2013. A superfolding Spinach2 reveals the dynamic nature of trinucleotide repeat-containing RNA. Nat Methods 10: 1219-1224.
48. Torres AG, Batlle E, Ribas de Pouplana L. 2014. Role of tRNA modifications in human diseases. Trends Mol Med 20: 306-314.
49. Wang PL, Bao Y, Yee MC, Barrett SP, Hogan GJ, Olsen MN, Dinneny JR, Brown PO, Salzman J. 2014. Circular RNA is expressed across the eukaryotic tree of life. PLoS One 9: e90859.
50. Weitzer S, Hanada T, Penninger JM, Martinez J. 2015. CLP1 as a novel player in linking tRNA splicing to neurodegenerative disorders. Wiley Interdiscip Rev RNA 6: 47-63.
51. Westholm JO, Miura P, Olson S, Shenker S, Joseph B, Sanfilippo P, Celniker SE, Graveley BR, Lai EC. 2014. Genome-wide analysis of Drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep 9: 1966-1980.
52. Will S, Reiche K, Hofacker IL, Stadler PF, Backofen R. 2007. Inferring noncoding RNA families and classes by means of genome-scale structure-based clustering. PLoS Comput Biol 3: e65.
53. Wolin SL, Matera AG. 1999. The trials and travels of tRNA. Genes Dev 13: 1-10.
54. ′ exonuclease Xrn1. Genes Dev 28: 1556-1561.
55. Zhang Y, Zhang XO, Chen T, Xiang JF, Yin QF, Xing YH, Zhu S, Yang L, Chen LL. 2013. Circular intronic long noncoding RNAs. Mol Cell 51: 792-806.
56. Zhang XO, Wang HB, Zhang Y, Lu X, Chen LL, Yang L. 2014. Complementary sequence-mediated exon circularization. Cell 159: 134-147.