Global analysis of RNA cleavage by 5'-hydroxyl RNA sequencing

Nucleic Acids Research

Volumn 43, Issue 17, 2015, Pages

  Peach, Sally E ^a   York, Kerri ^a   Hesselberth, Jay R ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' HYDROXYL RNA; ENDONUCLEASE; MESSENGER RNA; PROTEIN IRE1; RNA; RNA LIGASE; RTCB PROTEIN; SPLICING ENDONUCLEASE; TRANSFER RNA; UNCLASSIFIED DRUG; AMINO ACID TRANSFER RNA LIGASE; ESCHERICHIA COLI PROTEIN; RIBONUCLEASE; RTCB PROTEIN, E COLI;

ARTICLE; CODON; DNA SEQUENCE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; RNA CLEAVAGE; RNA SEQUENCE; RNA STRUCTURE; UNFOLDED PROTEIN RESPONSE; YEAST; CHEMISTRY; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; PROCEDURES; RNA STABILITY; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS;

AMINO ACYL-TRNA SYNTHETASES; ENDORIBONUCLEASES; ESCHERICHIA COLI PROTEINS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; RNA; RNA CLEAVAGE; RNA STABILITY; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, RNA; UNFOLDED PROTEIN RESPONSE;

EID: 84948993645     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv536     Document Type: Article

References (66)

1. Trotta, C.R., Miao, F., Arn, E.A., Stevens, S.W., Ho, C.K., Rauhut, R. and Abelson, J.N. (1997) The yeast tRNA splicing endonuclease: a tetrameric enzyme with two active site subunits homologous to the archaeal tRNA endonucleases. Cell, 89, 849-858.
2. Sidrauski, C. andWalter, P. (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell, 90, 1031-1039.
3. Luhtala, N. and Parker, R. (2010) T2 Family ribonucleases: ancient enzymes with diverse roles. Trends Biochem. Sci., 35, 253-259.
4. Cooper, D.A., Jha, B.K., Silverman, R.H., Hesselberth, J.R. and Barton, D.J. (2014) Ribonuclease L and metal-ion-independent endoribonuclease cleavage sites in host and viral RNAs. Nucleic Acids Res., 42, 5202-5216.
5. Ferré-D'Amaré, A.R. and Scott, W.G. (2010) Small self-cleaving ribozymes. Cold Spring Harb. Perspect. Biol., 2, a003574.
6. Roth, A., Weinberg, Z., Chen, A.G.Y., Kim, P.B., Ames, T.D. and Breaker, R.R. (2014) A widespread self-cleaving ribozyme class is revealed by bioinformatics. Nat. Chem. Biol., 10, 56-60.
7. Soukup, G.A. and Breaker, R.R. (1999) Relationship between internucleotide linkage geometry and the stability of RNA. RNA, 5, 1308-1325.
8. Schifano, J.M., Vvedenskaya, I.O., Knoblauch, J.G., Ouyang, M., Nickels, B.E. and Woychik, N.A. (2014) An RNA-seq method for defining endoribonuclease cleavage specificity identifies dual rRNA substrates for toxin MazF-mt3. Nat. Commun., 5, 3538.
9. German, M.A., Luo, S., Schroth, G., Meyers, B.C. and Green, P.J. (2009) Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat. Protoc., 4, 356-362.
10. Gu, W., Lee, H.-C., Chaves, D., Youngman, E.M., Pazour, G.J., Conte, D. and Mello, C.C. (2012) CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors. Cell, 151, 1488-1500.
11. Schutz, K., Hesselberth, J.R. and Fields, S. (2010) Capture and sequence analysis of RNAs with terminal 2', 3'-cyclic phosphates. RNA, 16, 621-631.
12. Cooper, D.A., Banerjee, S., Chakrabarti, A., García-Sastre, A., Hesselberth, J.R., Silverman, R.H. and Barton, D.J. (2014) Ribonuclease L targets distinct sites in influenza A virus RNAs. J. Virol., 89, 2764-2776.
13. Kimmig, P., Diaz, M., Zheng, J., Williams, C.C., Lang, A., Aragón, T., Li, H. and Walter, P. (2012) The unfolded protein response in fission yeast modulates stability of select mRNAs to maintain protein homeostasis. Elife, 1, e00048.
14. Greer, C.L., Peebles, C.L., Gegenheimer, P. and Abelson, J. (1983) Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell, 32, 537-546.
15. Phizicky, E.M., Schwartz, R.C. and Abelson, J. (1986) Saccharomyces cerevisiae tRNA ligase. Purification of the protein and isolation of the structural gene. J. Biol. Chem., 261, 2978-2986.
16. Tanaka, N., Chakravarty, A.K., Maughan, B. and Shuman, S. (2011) Novel mechanism of RNA repair by RtcB via sequential 2', 3'-cyclic phosphodiesterase and 3'-phosphate/5'-hydroxyl ligation reactions. J. Biol. Chem., 286, 43134-43143.
17. Desai, K.K. and Raines, R.T. (2012) tRNA ligase catalyzes the GTP-dependent ligation of RNA with 3'-phosphate and 5'-hydroxyl termini. Biochemistry, 51, 1333-1335.
18. Tanaka, N., Meineke, B. and Shuman, S. (2011) RtcB, a novel RNA ligase, can catalyze tRNA splicing and HAC1 mRNA splicing in vivo. J. Biol. Chem., 286, 30253-30257.
19. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
20. Karolchik, D., Barber, G.P., Casper, J., Clawson, H., Cline, M.S., Diekhans, M., Dreszer, T.R., Fujita, P.A., Guruvadoo, L., Haeussler, M. et al. (2014) The UCSC Genome Browser database: 2014 update. Nucleic Acids Res., 42, D764-D770.
21. Quinlan, A.R. and Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841-842.
22. Harigaya, Y. and Parker, R. (2012) Global analysis of mRNA decay intermediates in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A., 109, 11764-11769.
23. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nussbaum, C., Myers, R.M., Brown, M., Li, W. et al. (2008) Model-based Analysis of ChIP-Seq (MACS). Genome Biol., 9, R137.
24. Das, U., Chakravarty, A.K., Remus, B.S. and Shuman, S. (2013) Rewriting the rules for end joining via enzymatic splicing of DNA 3'-PO4 and 5'-OH ends. Proc. Natl. Acad. Sci. U.S.A., 110, 20437-20442.
25. Kivioja, T., Vähärautio, A., Karlsson, K., Bonke, M., Enge, M., Linnarsson, S. and Taipale, J. (2012) Counting absolute numbers of molecules using unique molecular identifiers. Nat. Methods, 9, 72-74.
26. Venema, J. and Tollervey, D. (1995) Two distinct recognition signals define the site of endonucleolytic cleavage at the 5'-end of yeast 18S rRNA. EMBO J., 14, 4883-4892.
27. Geerlings, T.H., Vos, J.C. and Raué, H.A. (2000) The final step in the formation of 25S rRNA in Saccharomyces cerevisiae is performed by 5'->3' exonucleases. RNA, 6, 1698-1703.
28. Sigurgeirsson, B., Emanuelsson, O. and Lundeberg, J. (2014) Analysis of stranded information using an automated procedure for strand specific RNA sequencing. BMC Genomics, 15, 631.
29. Petfalski, E. and Tollervey, D. (1998) Processing of the precursors to small nucleolar RNAs and rRNAs requires common components. Mol. Cell. Biol., 18, 1181-1189.
30. Giorgi, C., Fatica, A., Nagel, R. and Bozzoni, I. (2001) Release of U18 snoRNA from its host intron requires interaction of Nop1p with the Rnt1p endonuclease. EMBO J., 20, 6856-6865.
31. Wu, J. and Hopper, A.K. (2014) Healing for destruction: tRNA intron degradation in yeast is a two-step cytoplasmic process catalyzed by tRNA ligase Rlg1 and 5'-to-3' exonuclease Xrn1. Genes Dev., 28, 1556-1561.
32. Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M. and Snyder, M. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science, 320, 1344-1349.
33. Levin, J.Z., Yassour, M., Adiconis, X., Nusbaum, C., Thompson, D.A., Friedman, N., Gnirke, A. and Regev, A. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat. Chem. Biol., 7, 1-10.
34. Kertesz, M., Wan, Y., Mazor, E., Rinn, J.L., Nutter, R.C., Chang, H.Y. and Segal, E. (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature, 467, 103-107.
35. Finley, D., Bartel, B. and Varshavsky, A. (1989) The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature, 338, 394-401.
36. Lacombe, T., García-Gómez, J.J., de la Cruz, J., Roser, D., Hurt, E., Linder, P. and Kressler, D. (2009) Linear ubiquitin fusion to Rps31 and its subsequent cleavage are required for the efficient production and functional integrity of 40S ribosomal subunits. Mol. Microbiol., 72, 69-84.
37. Tsuboi, T., Kuroha, K., Kudo, K., Makino, S., Inoue, E., Kashima, I. and Inada, T. (2012) Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3' end of aberrant mRNA. Mol. Cell, 46, 518-529.
38. Guydosh, N.R. and Green, R. (2014) Dom34 rescues ribosomes in 3' untranslated regions. Cell, 156, 950-962.
39. Shoemaker, C.J. and Green, R. (2012) Translation drives mRNA quality control. Nat. Struct. Mol. Biol., 19, 594-601.
40. Stevens, A. (2001) 5'-exoribonuclease 1: Xrn1. Methods Enzymol., 342, 251-259.
41. Ron, D. and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Publishing Group, 8, 519-529.
42. Gonzalez, T.N., Sidrauski, C., Dörfler, S. and Walter, P. (1999) Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J., 18, 3119-3132.
43. Sidrauski, C., Cox, J.S. and Walter, P. (1996) tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell, 87, 405-413.
44. Normington, K., Kohno, K., Kozutsumi, Y., Gething, M.J. and Sambrook, J. (1989) S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell, 57, 1223-1236.
45. Kimata, Y., Ishiwata-Kimata, Y., Yamada, S. and Kohno, K. (2006) Yeast unfolded protein response pathway regulates expression of genes for anti-oxidative stress and for cell surface proteins. Genes Cells, 11, 59-69.
46. Jiang, L., Schlesinger, F., Davis, C.A., Zhang, Y., Li, R., Salit, M., Gingeras, T.R. and Oliver, B. (2011) Synthetic spike-in standards for RNA-seq experiments. Genome Res., 21, 1543-1551.
47. Thompson, D.M. and Parker, R. (2009) The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J. Cell Biol., 185, 43-50.
48. Ingolia, N.T., Brar, G.A., Rouskin, S., McGeachy, A.M. and Weissman, J.S. (2012) The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat. Protoc., 7, 1534-1550.
49. Ito-Harashima, S., Kuroha, K., Tatematsu, T. and Inada, T. (2007) Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast. Genes Dev., 21, 519-524.
50. Lu, J. and Deutsch, C. (2008) Electrostatics in the ribosomal tunnel modulate chain elongation rates. J. Mol. Biol., 384, 73-86.
51. Brandman, O., Stewart-Ornstein, J., Wong, D., Larson, A., Williams, C.C., Li, G.-W., Zhou, S., King, D., Shen, P.S., Weibezahn, J. et al. (2012) A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell, 151, 1042-1054.
52. Doma, M.K. and Parker, R. (2006) Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature, 440, 561-564.
53. Dimitrova, L.N., Kuroha, K., Tatematsu, T. and Inada, T. (2009) Nascent peptide-dependent translation arrest leads to Not4p-mediated protein degradation by the proteasome. J. Biol. Chem., 284, 10343-10352.
54. Durand, S., Richard, G., Bontems, F. and Uzan, M. (2012) Bacteriophage T4 polynucleotide kinase triggers degradation of mRNAs. Proceedings of the National Academy of Sciences of the U.S.A., 109, 7073-7078.
55. Gould, P.S., Dyer, N.P., Croft, W., Ott, S. and Easton, A.J. (2014) Cellular mRNAs access second ORFs using a novel amino acid sequence-dependent coupled translation termination-reinitiation mechanism. RNA, 20, 373-381.
56. Stiebler, A.C., Freitag, J., Schink, K.O., Stehlik, T., Tillmann, B.A.M., Ast, J. and Bölker, M. (2014) Ribosomal readthrough at a short UGA stop codon context triggers dual localization of metabolic enzymes in fungi and animals. PLoS Genet., 10, e1004685.
57. Remus, B.S. and Shuman, S. (2014) Distinctive kinetics and substrate specificities of plant and fungal tRNA ligases. RNA, 20, 462-473.
58. Hollien, J. and Weissman, J.S. (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science, 313, 104-107.
59. Niwa, M., Patil, C.K., DeRisi, J. and Walter, P. (2005) Genome-scale approaches for discovering novel nonconventional splicing substrates of the Ire1 nuclease. Genome Biol., 6, R3.
60. Tam, A.B., Koong, A.C. and Niwa, M. (2014) Ire1 has distinct catalytic mechanisms for XBP1/HAC1 splicing and RIDD. Cell Rep., 9, 850-858.
61. Maurel, M., Chevet, E., Tavernier, J. and Gerlo, S. (2014) Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem. Sci., 39, 245-254.
62. de Vries, H., Rüegsegger, U., Hübner, W., Friedlein, A., Langen, H. and Keller, W. (2000) Human pre-mRNA cleavage factor II(m) contains homologs of yeast proteins and bridges two other cleavage factors. EMBO J., 19, 5895-5904.
63. Weitzer, S. and Martinez, J. (2007) The human RNA kinase hClp1 is active on 3' transfer RNA exons and short interfering RNAs. Nature, 447, 222-226.
64. Schaffer, A.E., Eggens, V.R.C., Caglayan, A.O., Reuter, M.S., Scott, E., Coufal, N.G., Silhavy, J.L., Xue, Y., Kayserili, H., Yasuno, K. et al. (2014) CLP1 founder mutation links tRNA splicing and maturation to cerebellar development and neurodegeneration. Cell, 157, 651-663.
65. Karaca, E., Weitzer, S., Pehlivan, D., Shiraishi, H., Gogakos, T., Hanada, T., Jhangiani, S.N., Wiszniewski, W., Withers, M., Campbell, I.M. et al. (2014) Human CLP1 mutations alter tRNA biogenesis, affecting both peripheral and central nervous system function. Cell, 157, 636-650.
66. Hanada, T., Weitzer, S., Mair, B., Bernreuther, C., Wainger, B.J., Ichida, J., Hanada, R., Orthofer, M., Cronin, S.J., Komnenovic, V. et al. (2013) CLP1 links tRNA metabolism to progressive motor-neuron loss. Nature, 495, 474-480.