Transcriptome Wide Annotation of Eukaryotic RNase III Reactivity and Degradation Signals

PLoS Genetics

Volumn 11, Issue 2, 2015, Pages 1-29

  Gagnon, Jules ^a   Lavoie, Mathieu ^a   Catala, Mathieu ^a   Malenfant, Francis ^a   Elela, Sherif Abou ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBONUCLEASE III; DOUBLE STRANDED RNA; FUNGAL RNA; RNT1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTOME;

ARTICLE; CATALYSIS; CONTROLLED STUDY; FUNGAL GENE; GENE EXPRESSION; GENE SEQUENCE; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC REGULATION; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; RNA CLEAVAGE; RNA DEGRADATION; RNA STABILITY; SACCHAROMYCES CEREVISIAE; TRANSCRIPTOMICS; BIOSYNTHESIS; CONFORMATION; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; MOLECULAR GENETICS;

EUKARYOTA;

BASE SEQUENCE; GENE EXPRESSION REGULATION, FUNGAL; MOLECULAR SEQUENCE ANNOTATION; NUCLEIC ACID CONFORMATION; RIBONUCLEASE III; RNA STABILITY; RNA, DOUBLE-STRANDED; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; TRANSCRIPTOME;

EID: 84924354128     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005000     Document Type: Article

References (69)

1. Rabani M, Levin JZ, Fan L, Adiconis X, Raychowdhury R, et al. (2011) Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat Biotechnol 29: 436–442. doi: 10.1038/nbt.1861 21516085
2. Cheadle C, Fan J, Cho-Chung YS, Werner T, Ray J, et al. (2005) Control of gene expression during T cell activation: alternate regulation of mRNA transcription and mRNA stability. BMC Genomics 6: 75. 15907206
3. Romero-Santacreu L, Moreno J, Perez-Ortin JE, Alepuz P, (2009) Specific and global regulation of mRNA stability during osmotic stress in Saccharomyces cerevisiae. RNA 15: 1110–1120. doi: 10.1261/rna.1435709 19369426
4. Cereghino GP, Scheffler IE, (1996) Genetic analysis of glucose regulation in saccharomyces cerevisiae: control of transcription versus mRNA turnover. Embo J 15: 363–374. 8617211
5. Rodda SJ, Kavanagh SJ, Rathjen J, Rathjen PD, (2002) Embryonic stem cell differentiation and the analysis of mammalian development. Int J Dev Biol 46: 449–458. 12141431
6. Castilla-Llorente V, Nicastro G, Ramos A, (2013) Terminal loop-mediated regulation of miRNA biogenesis: selectivity and mechanisms. Biochem Soc Trans 41: 861–865. doi: 10.1042/BST20130058 23863145
7. Parker R, (2012) RNA degradation in Saccharomyces cerevisae. Genetics 191: 671–702. doi: 10.1534/genetics.111.137265 22785621
8. Chakravarthy S, Sternberg SH, Kellenberger CA, Doudna JA, (2010) Substrate-specific kinetics of Dicer-catalyzed RNA processing. J Mol Biol 404: 392–402. doi: 10.1016/j.jmb.2010.09.030 20932845
9. Nicholson AW, (2014) Ribonuclease III mechanisms of double-stranded RNA cleavage. Wiley Interdiscip Rev RNA 5: 31–48. doi: 10.1002/wrna.1195 24124076
10. Lamontagne B, Ghazal G, Lebars I, Yoshizawa S, Fourmy D, et al. (2003) Sequence dependence of substrate recognition and cleavage by yeast RNase III. J Mol Biol 327: 985–1000. 12662924
11. Lim B, Sim SH, Sim M, Kim K, Jeon CO, et al. (2012) RNase III controls the degradation of corA mRNA in Escherichia coli. J Bacteriol 194: 2214–2220. doi: 10.1128/JB.00099-12 22343302
12. Membrillo-Hernandez J, Lin EC, (1999) Regulation of expression of the adhE gene, encoding ethanol oxidoreductase in Escherichia coli: transcription from a downstream promoter and regulation by fnr and RpoS. J Bacteriol 181: 7571–7579. 10601216
13. Ge D, Lamontagne B, Abou Elela S, (2005) RNase III-Mediated Silencing of a Glucose-Dependent Repressor in Yeast. Curr Biol 15: 140–145. 15668170
14. Lavoie M, Ge D, Abou Elela S, (2012) Regulation of conditional gene expression by coupled transcription repression and RNA degradation. Nucleic Acids Res 40: 871–883. doi: 10.1093/nar/gkr759 21933814
15. Catala M, Lamontagne B, Larose S, Ghazal G, Abou Elela S, (2004) Cell cycle-dependent nuclear localization of yeast RNase III is required for efficient cell division. Mol Biol Cell 15: 3015–3030. 15090619
16. David L, Huber W, Granovskaia M, Toedling J, Palm CJ, et al. (2006) A high-resolution map of transcription in the yeast genome. Proc Natl Acad Sci U S A 103: 5320–5325. 16569694
17. Lund E, Dahlberg JE, (2006) Substrate selectivity of exportin 5 and Dicer in the biogenesis of microRNAs. Cold Spring Harb Symp Quant Biol 71: 59–66. 17381281
18. Zhang K, Nicholson AW, (1997) Regulation of ribonuclease III processing by double-helical sequence antideterminants. Proc Natl Acad Sci U S A 94: 13437–13441. 9391043
19. Lee HY, Zhou K, Smith AM, Noland CL, Doudna JA, (2013) Differential roles of human Dicer-binding proteins TRBP and PACT in small RNA processing. Nucleic Acids Res 41: 6568–6576. doi: 10.1093/nar/gkt361 23661684
20. Gu S, Jin L, Zhang Y, Huang Y, Zhang F, et al. (2012) The loop position of shRNAs and pre-miRNAs is critical for the accuracy of dicer processing in vivo. Cell 151: 900–911. doi: 10.1016/j.cell.2012.09.042 23141545
21. Ma H, Wu Y, Choi JG, Wu H, (2013) Lower and upper stem-single-stranded RNA junctions together determine the Drosha cleavage site. Proc Natl Acad Sci U S A 110: 20687–20692. doi: 10.1073/pnas.1311639110 24297910
22. Lamontagne B, Abou Elela S, (2004) Evaluation of the RNA determinants for bacterial and yeast RNase III binding and cleavage. J Biol Chem 279: 2231–2241. 14581474
23. Lebars I, Lamontagne B, Yoshizawa S, Aboul-Elela S, Fourmy D, (2001) Solution structure of conserved AGNN tetraloops: insights into Rnt1p RNA processing. Embo J 20: 7250–7258. 11743001
24. Ghazal G, Elela SA, (2006) Characterization of the reactivity determinants of a novel hairpin substrate of yeast RNase III. J Mol Biol 363: 332–344. 16962133
25. Ghazal G, Ge D, Gervais-Bird J, Gagnon J, Abou Elela S, (2005) Genome-wide prediction and analysis of yeast RNase III-dependent snoRNA processing signals. Mol Cell Biol 25: 2981–2994. 15798187
26. Catala M, Aksouh L, Abou Elela S, (2012) RNA-dependent regulation of the cell wall stress response. Nucleic Acids Res 40: 7507–7517. doi: 10.1093/nar/gks411 22576366
27. Ghazal G, Gagnon J, Jacques PE, Landry JR, Robert F, et al. (2009) Yeast RNase III triggers polyadenylation-independent transcription termination. Mol Cell 36: 99–109. doi: 10.1016/j.molcel.2009.07.029 19818713
28. Liang YH, Lavoie M, Comeau MA, Abou Elela S, Ji X (2014) Structure of a Eukaryotic RNase III Postcleavage Complex Reveals a Double-Ruler Mechanism for Substrate Selection. Mol Cell.
29. Greenbaum D, Jansen R, Gerstein M, (2002) Analysis of mRNA expression and protein abundance data: an approach for the comparison of the enrichment of features in the cellular population of proteins and transcripts. Bioinformatics 18: 585–596. 12016056
30. Lee A, Henras AK, Chanfreau G, (2005) Multiple RNA surveillance pathways limit aberrant expression of iron uptake mRNAs and prevent iron toxicity in S. cerevisiae. Mol Cell 19: 39–51. 15989963
31. Danin-Kreiselman M, Lee CY, Chanfreau G, (2003) RNAse III-mediated degradation of unspliced pre-mRNAs and lariat introns. Mol Cell 11: 1279–1289. 12769851
32. Morey JS, Ryan JC, Van Dolah FM, (2006) Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 8: 175–193. 17242735
33. Lee CY, Lee A, Chanfreau G, (2003) The roles of endonucleolytic cleavage and exonucleolytic digestion in the 5'-end processing of S. cerevisiae box C/D snoRNAs. Rna 9: 1362–1370. 14561886
34. Pellegrini O, Mathy N, Condon C, Benard L, (2008) In vitro assays of 5' to 3'-exoribonuclease activity. Methods Enzymol 448: 167–183. doi: 10.1016/S0076-6879(08)02609-8 19111176
35. Harigaya Y, Parker R, (2012) Global analysis of mRNA decay intermediates in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 109: 11764–11769. doi: 10.1073/pnas.1119741109 22752303
36. Lavoie M, Abou Elela S, (2008) Yeast ribonuclease III uses a network of multiple hydrogen bonds for RNA binding and cleavage. Biochemistry 47: 8514–8526. doi: 10.1021/bi800238u 18646867
37. Lamontagne B, Abou Elela S, (2007) Short RNA guides cleavage by eukaryotic RNase III. PLoS One 2: e472. 17534422
38. Osier MV, Zhao H, Cheung KH, (2004) Handling multiple testing while interpreting microarrays with the Gene Ontology Database. BMC Bioinformatics 5: 124. 15350198
39. Mewes HW, Frishman D, Guldener U, Mannhaupt G, Mayer K, et al. (2002) MIPS: a database for genomes and protein sequences. Nucleic Acids Res 30: 31–34. 11752246
40. Ludovico P, Sansonetty F, Corte-Real M, (2001) Assessment of mitochondrial membrane potential in yeast cell populations by flow cytometry. Microbiology 147: 3335–3343. 11739765
41. Williamson T, Adiamah D, Schwartz JM, Stateva L, (2012) Exploring the genetic control of glycolytic oscillations in Saccharomyces cerevisiae. BMC Syst Biol 6: 108. doi: 10.1186/1752-0509-6-108 22920924
42. Drinnenberg IA, Fink GR, Bartel DP, (2011) Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333: 1592. doi: 10.1126/science.1209575 21921191
43. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, et al. (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725–737. 15935759
44. van Dijk EL, Chen CL, d'Aubenton-Carafa Y, Gourvennec S, Kwapisz M, et al. (2011) XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475: 114–117. doi: 10.1038/nature10118 21697827
45. Folkes L, Moxon S, Woolfenden HC, Stocks MB, Szittya G, et al. (2012) PAREsnip: a tool for rapid genome-wide discovery of small RNA/target interactions evidenced through degradome sequencing. Nucleic Acids Res 40: e103. doi: 10.1093/nar/gks277 22467211
46. Chen JJ, Roberson PK, Schell MJ, (2010) The false discovery rate: a key concept in large-scale genetic studies. Cancer Control 17: 58–62. 20010520
47. Murie C, Woody O, Lee AY, Nadon R, (2009) Comparison of small n statistical tests of differential expression applied to microarrays. BMC Bioinformatics 10: 45. doi: 10.1186/1471-2105-10-45 19192265
48. Nadon R, Shoemaker J, (2002) Statistical issues with microarrays: processing and analysis. Trends Genet 18: 265–271. 12047952
49. Chanfreau G, Buckle M, Jacquier A, (2000) Recognition of a conserved class of RNA tetraloops by Saccharomyces cerevisiae RNase III. Proc Natl Acad Sci U S A 97: 3142–3147. 10716739
50. Wang Z, Hartman E, Roy K, Chanfreau G, Feigon J, (2011) Structure of a yeast RNase III dsRBD complex with a noncanonical RNA substrate provides new insights into binding specificity of dsRBDs. Structure 19: 999–1010. doi: 10.1016/j.str.2011.03.022 21742266
51. Huberts DH, Niebel B, Heinemann M, (2012) A flux-sensing mechanism could regulate the switch between respiration and fermentation. FEMS Yeast Res 12: 118–128. doi: 10.1111/j.1567-1364.2011.00767.x 22129078
52. Kim IS, Kim YS, Kim H, Jin I, Yoon HS, (2013) Saccharomyces cerevisiae KNU5377 stress response during high-temperature ethanol fermentation. Mol Cells 35: 210–218. doi: 10.1007/s10059-013-2258-0 23512334
53. Horak J, (2013) Regulations of sugar transporters: insights from yeast. Curr Genet 59: 1–31. doi: 10.1007/s00294-013-0388-8 23455612
54. Raab AM, Hlavacek V, Bolotina N, Lang C, (2011) Shifting the fermentative/oxidative balance in Saccharomyces cerevisiae by transcriptional deregulation of Snf1 via overexpression of the upstream activating kinase Sak1p. Appl Environ Microbiol 77: 1981–1989. doi: 10.1128/AEM.02219-10 21257817
55. Johnston M, (1999) Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet 15: 29–33. 10087931
56. Heyland J, Fu J, Blank LM, (2009) Correlation between TCA cycle flux and glucose uptake rate during respiro-fermentative growth of Saccharomyces cerevisiae. Microbiology 155: 3827–3837. doi: 10.1099/mic.0.030213-0 19684065
57. Fernandez-Cid A, Riera A, Herrero P, Moreno F, (2012) Glucose levels regulate the nucleo-mitochondrial distribution of Mig2. Mitochondrion 12: 370–380. doi: 10.1016/j.mito.2012.02.001 22353369
58. Cao H, Yue M, Li S, Bai X, Zhao X, et al. (2011) The impact of MIG1 and/or MIG2 disruption on aerobic metabolism of succinate dehydrogenase negative Saccharomyces cerevisiae. Appl Microbiol Biotechnol 89: 733–738. doi: 10.1007/s00253-010-2894-7 20938771
59. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, et al. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115–132. 9483801
60. Parenteau J, Durand M, Morin G, Gagnon J, Lucier JF, et al. (2011) Introns within ribosomal protein genes regulate the production and function of yeast ribosomes. Cell 147: 320–331. doi: 10.1016/j.cell.2011.08.044 22000012
61. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901–906. 10436161
62. Guthrie C, Fink GR, (1991) Guide to Yeast Genetics and Molecular Biology. San Diego, CA: Academic Press. 25144101
63. Burke PV, Kwast KE, Everts F, Poyton RO, (1998) A fermentor system for regulating oxygen at low concentrations in cultures of Saccharomyces cerevisiae. Appl Environ Microbiol 64: 1040–1044. 9501444
64. Huber W, Toedling J, Steinmetz LM, (2006) Transcript mapping with high-density oligonucleotide tiling arrays. Bioinformatics 22: 1963–1970. 16787969
65. Henras AK, Sam M, Hiley SL, Wu H, Hughes TR, et al. (2005) Biochemical and genomic analysis of substrate recognition by the double-stranded RNA binding domain of yeast RNase III. RNA 11: 1225–1237. 15987808
66. Martin M, (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal 17: 10–12.
67. Liao Y, Smyth GK, Shi W, (2013) The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res 41: e108. doi: 10.1093/nar/gkt214 23558742
68. Volejnikova A, Hlouskova J, Sigler K, Pichova A, (2013) Vital mitochondrial functions show profound changes during yeast culture ageing. FEMS Yeast Res 13: 7–15. doi: 10.1111/1567-1364.12001 22938652
69. Falcon S, Gentleman R, (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257–258. 17098774