cyPhyRNA-seq: a genome-scale RNA-seq method to detect active self-cleaving ribozymes by capturing RNAs with 2ʹ,3ʹ cyclic phosphates and 5ʹ hydroxyl ends

References

• Guerrier-Takada C, Gardiner K, Marsh T, et al. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell. 1983;35(3):849–857.
   PubMed Web of Science ®Google Scholar
• Peebles CL, Perlman PS, Mecklenburg KL, et al. A self-splicing RNA excises an intron lariat. Cell. 1986;44(2):213–223.
   PubMed Web of Science ®Google Scholar
• Nissen P, Hansen J, Ban N, et al. The structural basis of ribosome activity in peptide bond synthesis. Science. 2000;289(5481):920–930.
   PubMed Web of Science ®Google Scholar
• Jimenez RM, Polanco JA, Lupták A. Chemistry and biology of self-cleaving ribozymes. Trends Biochem Sci. 2015;40(11):648–661.
   PubMed Web of Science ®Google Scholar
• Prody GA, Bakos JT, Buzayan JM, et al. Autolytic processing of dimeric plant virus satellite RNA. Science. 1986;231(4745):1577–1580.
   PubMed Web of Science ®Google Scholar
• Buzayan JM, Gerlach WL, Bruening G. Satellite tobacco ringspot virus RNA: a subset of the RNA sequence is sufficient for autolytic processing. Proc Natl Acad Sci U S A. 1986;83(23):8859–8862.
   PubMed Web of Science ®Google Scholar
• Wu HN, Lin YJ, Lin FP, et al. Human hepatitis delta virus RNA subfragments contain an autocleavage activity. Proc Natl Acad Sci U S A. 1989;86(6):1831–1835.
   PubMed Web of Science ®Google Scholar
• Saville BJ, Collins RA. A site-specific self-cleavage reaction performed by a novel RNA in neurospora mitochondria. Cell. 1990;61(4):685–696.
   PubMed Web of Science ®Google Scholar
• Winkler WC, Nahvi A, Roth A, et al. Control of gene expression by a natural metabolite-responsive ribozyme. Nature. 2004;428(6980):281–286.
   PubMed Web of Science ®Google Scholar
• Roth A, Weinberg Z, Chen AGY, et al. A widespread self-cleaving ribozyme class is revealed by bioinformatics. Nat Chem Biol. 2014;10(1):56–60.
   PubMed Web of Science ®Google Scholar
• Weinberg Z, Kim PB, Chen TH, et al. New classes of self-cleaving ribozymes revealed by comparative genomics analysis. Nat Chem Biol. 2015;11(8):606–610.
   PubMed Web of Science ®Google Scholar
• Chen Y, Qi F, and Gao F, et al. Hovlinc is a recently evolved class of ribozyme found in human lncRNA. Nat Chem Biol. 2021
   Web of Science ®Google Scholar
• Ferbeyre G, Smith JM, Cedergren R. Schistosome satellite DNA encodes active hammerhead ribozymes. Mol Cell Biol. 1998;18(7):3880–3888.
   PubMed Web of Science ®Google Scholar
• Cervera A, De La Peña M. Eukaryotic penelope-like retroelements encode hammerhead ribozyme motifs. Mol Biol Evol. 2014;31(11):2941–2947.
   PubMed Web of Science ®Google Scholar
• Eickbush DG, Eickbush TH. R2 retrotransposons encode a self-cleaving ribozyme for processing from an rRNA cotranscript▿. Mol Cell Biol. 2010;30(13):3142–3150.
   PubMed Web of Science ®Google Scholar
• Bringaud F, Bartholomeu DC, Blandin G, et al. The trypanosoma cruzi L1Tc and NARTc non-LTR retrotransposons show relative site specificity for insertion. Mol Biol Evol. 2006;23(2):411–420.
   PubMed Web of Science ®Google Scholar
• Salehi-Ashtiani K, Lupták A, Litovchick A, et al. A genomewide search for ribozymes reveals an HDV-like sequence in the human CPEB3 gene. Science. 2006;313(5794):1788–1792.
   PubMed Web of Science ®Google Scholar
• Weinberg CE, Weinberg Z, Hammann C. Novel ribozymes: discovery, catalytic mechanisms, and the quest to understand biological function. Nucleic Acids Res. 2019;47(18):9480–9494.
   PubMed Web of Science ®Google Scholar
• Weinberg Z, Lünse CE, Corbino KA, et al. Detection of 224 candidate structured RNAs by comparative analysis of specific subsets of intergenic regions. Nucleic Acids Res. 2017;45(18):10811–10823.
   PubMed Web of Science ®Google Scholar
• Wang Z, Gerstein M, Snyder M. RNA-seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009;10(1):57–63.
   PubMed Web of Science ®Google Scholar
• Kukurba KR, Montgomery SB. RNA sequencing and analysis. Cold Spring Harb Protoc. 2015;2015(11):951–969.
   PubMedGoogle Scholar
• Hrdlickova R, Toloue M, Tian B. RNA-seq methods for transcriptome analysis. Wiley Interdiscip Rev RNA. 2017;8(1):e1364.
   Web of Science ®Google Scholar
• Hafner M, Landgraf P, Ludwig J, et al. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods. 2008;44(1):3–12.
   PubMed Web of Science ®Google Scholar
• Englert M, Beier H. Plant tRNA ligases are multifunctional enzymes that have diverged in sequence and substrate specificity from RNA ligases of other phylogenetic origins. Nucleic Acids Res. 2005;33(1):388–399.
   PubMed Web of Science ®Google Scholar
• Tanaka N, Shuman S. RtcB is the RNA ligase component of an Escherichia coli RNA repair operon. J Biol Chem. 2011;286(10):7727–7731.
   PubMed Web of Science ®Google Scholar
• Culver GM, McCraith SM, Consaul SA, et al. A 2ʹ-phosphotransferase implicated in tRNA splicing is essential in Saccharomyces cerevisiae. J Biol Chem. 1997;272(20):13203–13210.
   PubMed Web of Science ®Google Scholar
• Tanaka N, Chakravarty AK, Maughan B, et al. Novel mechanism of RNA repair by RtcB via sequential 2ʹ,3ʹ-cyclic phosphodiesterase and 3ʹ-phosphate/5ʹ-hydroxyl ligation reactions. J Biol Chem. 2011;286(50):43134–43143.
   PubMed Web of Science ®Google Scholar
• Schutz K, Hesselberth JR, Fields S. Capture and sequence analysis of RNAs with terminal 2ʹ,3ʹ-cyclic phosphates. RNA. 2010;16(3):621–631.
   PubMed Web of Science ®Google Scholar
• Peach SE, York K, Hesselberth JR. Global analysis of RNA cleavage by 5ʹ-hydroxyl RNA sequencing. Nucleic Acids Res. 2015;43(17):e108.
   PubMed Web of Science ®Google Scholar
• Head SR, Komori HK, LaMere SA, et al. Library construction for next-generation sequencing: overviews and challenges. BioTechniques. 2014;56(2):61–64. 66, 68, passim.
   PubMed Web of Science ®Google Scholar
• Pang YLJ, Abo R, Levine SS, et al. Diverse cell stresses induce unique patterns of tRNA up- and down-regulation: tRNA-seq for quantifying changes in tRNA copy number. Nucleic Acids Res. 2014;42(22):e170.
   PubMed Web of Science ®Google Scholar
• Das U, Chakravarty AK, Remus BS, et al. Rewriting the rules for end joining via enzymatic splicing of DNA 3ʹ-PO4 and 5ʹ-OH ends. Proc Natl Acad Sci U S A. 2013;110(51):20437–20442.
   PubMed Web of Science ®Google Scholar
• Zheng L, Falschlunger C, Huang K, et al. Hatchet ribozyme structure and implications for cleavage mechanism. Proc Natl Acad Sci U S A. 2019;116(22):10783–10791.
   PubMed Web of Science ®Google Scholar
• Riccitelli N, Lupták A. HDV family of self-cleaving ribozymes. Prog Mol Biol Transl Sci. 2013;120:123–171.
   PubMed Web of Science ®Google Scholar
• Remus BS, Shuman S. A kinetic framework for tRNA ligase and enforcement of a 2′-phosphate requirement for ligation highlights the design logic of an RNA repair machine. RNA. 2013;19(5):659–669.
   PubMed Web of Science ®Google Scholar
• Vušurović N, Altman RB, Terry DS, et al. Pseudoknot formation seeds the twister ribozyme cleavage reaction coordinate. J Am Chem Soc. 2017;139(24):8186–8193.
   PubMed Web of Science ®Google Scholar
• Gebetsberger J, Micura R. Unwinding the twister ribozyme: from structure to mechanism. Wiley Interdiscip Rev RNA. 2017;8(3):e1402.
   PubMed Web of Science ®Google Scholar
• Steiger MA, Kierzek R, Turner DH, et al. Substrate recognition by a yeast 2‘-Phosphotransferase involved in tRNA splicing and by its escherichia coli homolog. Biochemistry. 2001;40(46):14098–14105.
   PubMed Web of Science ®Google Scholar
• Emilsson GM, Nakamura S, Roth A, et al. Ribozyme speed limits. RNA. 2003;9(8):907–918.
   PubMed Web of Science ®Google Scholar
• Shigematsu M, Kawamura T, Kirino Y. Generation of 2ʹ,3ʹ-cyclic phosphate-containing RNAs as a hidden layer of the transcriptome. Front Genet. 2018;9:562.
   PubMed Web of Science ®Google Scholar
• Westermann AJ, Gorski SA, Vogel J. Dual RNA-seq of pathogen and host. Nat Rev Microbiol. 2012;10(9):618–630.
   PubMed Web of Science ®Google Scholar
• O’Neil D, Glowatz H, and Schlumpberger M. Ribosomal RNA depletion for efficient use of RNA-seq capacity. Curr Protoc Mol Biol. 2013; Chapter 4:Unit4.19
   PubMedGoogle Scholar
• Shigematsu M, Morichika K, Kawamura T, et al. Genome-wide identification of short 2ʹ,3ʹ-cyclic phosphate-containing RNAs and their regulation in aging. PLoS Genet. 2019;15(11):e1008469.
   PubMed Web of Science ®Google Scholar
• Herbert ZT, Kershner JP, Butty VL, et al. Cross-site comparison of ribosomal depletion kits for Illumina RNAseq library construction. BMC Genomics. 2018;19(1):199.
   PubMedGoogle Scholar
• Prezza G, Heckel T, Dietrich S, et al. Improved bacterial RNA-seq by Cas9-based depletion of ribosomal RNA reads. RNA. 2020;26(8):1069–1078.
   PubMed Web of Science ®Google Scholar
• Lu C, Meyers BC, Green PJ. Construction of small RNA cDNA libraries for deep sequencing. Methods. 2007;43(2):110–117.
   PubMed Web of Science ®Google Scholar
• Zhuang F, Fuchs RT, Robb GB. Small RNA expression profiling by high-throughput sequencing: implications of enzymatic manipulation. J Nucleic Acids. 2012;2012:360358.
   PubMedGoogle Scholar
• Kraus AJ, Brink BG, Siegel TN. Efficient and specific oligo-based depletion of rRNA. Sci Rep. 2019;9(1):12281.
   PubMedGoogle Scholar
• Deana A, Celesnik H, Belasco JG. The bacterial enzyme RppH triggers messenger RNA degradation by 5ʹ pyrophosphate removal. Nature. 2008;451(7176):355–358.
   PubMed Web of Science ®Google Scholar
• Stevens A. Purification and characterization of a Saccharomyces cerevisiae exoribonuclease which yields 5ʹ-mononucleotides by a 5ʹ leads to 3ʹ mode of hydrolysis. J Biol Chem. 1980;255(7):3080–3085.
   PubMed Web of Science ®Google Scholar
• Kawano M, Kawazu C, Lizio M, et al. Reduction of non-insert sequence reads by dimer eliminator LNA oligonucleotide for small RNA deep sequencing. BioTechniques. 2010;49(4):751–755.
   PubMed Web of Science ®Google Scholar
• Erber L, Hoffmann A, Fallmann J, et al. LOTTE-seq (Long hairpin oligonucleotide based tRNA high-throughput sequencing): specific selection of tRNAs with 3ʹ-CCA end for high-throughput sequencing. RNA Biol. 2020;17(1):23–32.
   PubMed Web of Science ®Google Scholar
• Perreault J, Weinberg Z, Roth A, et al. Identification of hammerhead ribozymes in all domains of life reveals novel structural variations. PLoS Comput Biol. 2011;7(5):e1002031.
   PubMed Web of Science ®Google Scholar
• Ule J, Jensen K, Mele A, et al. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods. 2005;37(4):376–386.
   PubMed Web of Science ®Google Scholar
• Uren PJ, Bahrami-Samani E, Burns SC, et al. Site identification in high-throughput RNA-protein interaction data. Bioinformatics. 2012;28(23):3013–3020.
   PubMed Web of Science ®Google Scholar
• Webb C-HT, Riccitelli NJ, Ruminski DJ, et al. Widespread occurrence of self-cleaving ribozymes. Science. 2009;326(5955):953.
   PubMed Web of Science ®Google Scholar
• Lindell M, Romby P, Wagner EGH. Lead(II) as a probe for investigating RNA structure in vivo. RNA. 2002;8(4):534–541.
   PubMed Web of Science ®Google Scholar
• Twittenhoff C, Brandenburg VB, Righetti F, et al. Lead-seq: transcriptome-wide structure probing in vivo using lead(II) ions. Nucleic Acids Res. 2020;48(12):e71.
   PubMed Web of Science ®Google Scholar
• Luhtala N, Parker R. T2 family ribonucleases: ancient enzymes with diverse roles. Trends Biochem Sci. 2010;35(5):253–259.
   PubMed Web of Science ®Google Scholar
• Schifano JM, Vvedenskaya IO, Knoblauch JG, et al. An RNA-seq method for defining endoribonuclease cleavage specificity identifies dual rRNA substrates for toxin MazF-mt3. Nat Commun. 2014;5(1):3538.
   PubMedGoogle Scholar
• Thompson DM, Lu C, Green PJ, et al. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA. 2008;14(10):2095–2103.
   PubMed Web of Science ®Google Scholar
• Sambrook J, Fritsch E, and Maniatis T. Molecular cloning: a laboratory manual: vol. 2. 2nd S.l. Newyork: Cold Spring Harbor; 1989.
   Google Scholar
• Viollet S, Fuchs RT, Munafo DB, et al. T4 RNA ligase 2 truncated active site mutants: improved tools for RNA analysis. BMC Biotechnol. 2011;11(1):72.
   PubMedGoogle Scholar
• Seidl CI, Ryan K, Darlix J-L. Circular single-stranded synthetic DNA delivery vectors for microRNA. PLoS ONE. 2011;6(2):e16925.
   PubMed Web of Science ®Google Scholar
• Ling ML, Risman SS, Klement JF, et al. Abortive initiation by bacteriophage T3 and T7 RNA polymerases under conditions of limiting substrate. Nucleic Acids Res. 1989;17(4):1605–1618.
   PubMed Web of Science ®Google Scholar
• Lihanova Y, and Weinberg CE. Biochemical analysis of cleavage and ligation activities of the pistol ribozyme from Paenibacillus polymyxa. RNA Biol. 2021;1–9.
   Web of Science ®Google Scholar
• Lama L, Ryan K. Adenylylation of small RNA sequencing adapters using the TS2126 RNA ligase I. RNA. 2016;22(1):155–161.
   PubMed Web of Science ®Google Scholar
• Sambrook J, and Russell DW. Purification of nucleic acids by extraction with phenol:chloroform. CSH Protoc. 2006.
   Google Scholar
• Lorenz C. Analysen zur Temperaturabhängigkeit posttranskriptioneller Modifikationen in bakteriellen tRNAs. Leipzig University; 2020.
   Google Scholar
• Kivioja T, Vähärautio A, Karlsson K, et al. Counting absolute numbers of molecules using unique molecular identifiers. Nat Methods. 2011;9(1):72–74.
   PubMed Web of Science ®Google Scholar
• NCBI. Dsm644 annotation, asm19575v1. [cited 2019 oct 10]. https://www.ncbi.nlm.nih.gov/assembly/GCF_000195755.1/_ASM19575v1
   Google Scholar
• Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013;29(22):2933–2935.
   PubMed Web of Science ®Google Scholar
• Kalvari I, Nawrocki EP, Ontiveros-Palacios N, et al. Rfam 14: expanded coverage of metagenomic, viral and microRNA families. Nucleic Acids Res. 2021;49(D1):D192–D200.
   PubMed Web of Science ®Google Scholar
• Rfam. Hammerhead ribozyme type 2, cm: [cited 2019 Oct 10]. http://rfam.xfam.org/family/RF02276/cm.
   Google Scholar
• Smith T, Heger A, Sudbery I. UMI-tools: modeling sequencing errors in unique molecular identifiers to improve quantification accuracy. Genome Res. 2017;27(3):491–499.
   PubMed Web of Science ®Google Scholar
• Felix Krueger. TrimGalore. [cited 2020 Sep 9]. https://github.com/FelixKrueger/TrimGalore
   Google Scholar
• Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21.
   PubMed Web of Science ®Google Scholar
• Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–930.
   PubMed Web of Science ®Google Scholar
• Andrews S. Fastqc. [cited 2020 Apr 5]. https://github.com/s-andrews/FastQC.
   Google Scholar
• The Smith Lab. Piranha — CLIP- and RIP-seq peak caller | The smith lab. [cited 2020 Mar 15]. http://smithlabresearch.org/software/piranha/.
   Google Scholar
• Navarro Gonzalez J, Zweig AS, Speir ML, et al. The UCSC genome browser database: 2021 update. Nucleic Acids Res. 2021;49(D1):D1046–D1057.
   PubMed Web of Science ®Google Scholar
• Zweig AS, Karolchik D, Kuhn RM, et al. UCSC genome browser tutorial. Genomics. 2008;92(2):75–84.
   PubMed Web of Science ®Google Scholar