Contributions of transcription and mRNA decay to gene expression dynamics of fission yeast in response to oxidative stress

RNA Biology

Volumn 11, Issue 6, 2014, Pages 702-714

  Marguerat, Samuel ^a,c   Lawler, Katherine ^b,d   Brazma, Alvis ^a   Bähler, Jur̈g ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Atf1; Fission yeast; Gene regulation; Mathematical modeling; mRNA turnover; Oxidative stress; Post transcriptional control; Ribosome biogenesis; RNA polymerase II

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; MESSENGER RNA; ACTIVATING TRANSCRIPTION FACTOR 1; ATF1 PROTEIN, S POMBE; PHOSPHOPROTEIN; REGULATORY RNA SEQUENCE; RIBOSOME PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; TRANSCRIPTOME;

ARTICLE; BIOGENESIS; ENVIRONMENTAL STRESS; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENOMICS; MOLECULAR DYNAMICS; NONHUMAN; OPEN READING FRAME; OXIDATIVE STRESS; PROTEIN DEGRADATION; RNA METABOLISM; RNA PROCESSING; RNA TRANSCRIPTION; SCHIZOSACCHAROMYCES POMBE; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; ADAPTATION; BIOLOGICAL MODEL; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NUCLEOTIDE MOTIF; POSITION WEIGHT MATRIX; REGULATORY RNA SEQUENCE; RNA STABILITY; SCHIZOSACCHAROMYCES;

ACTIVATING TRANSCRIPTION FACTOR 1; ADAPTATION, BIOLOGICAL; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; MODELS, BIOLOGICAL; NUCLEOTIDE MOTIFS; OXIDATIVE STRESS; PHOSPHOPROTEINS; POSITION-SPECIFIC SCORING MATRICES; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RIBOSOMAL PROTEINS; RNA STABILITY; RNA, MESSENGER; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84906351345     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.29196     Document Type: Article

References (70)

1. Keene JD. Minireview: global regulation and dynamics of ribonucleic Acid. Endocrinology 2010; 151:1391-7; PMID:20332203; http://dx.doi.org/10.1210/en. 2009-1250
2. Lackner DH, Beilharz TH, Marguerat S, Mata J, Watt S, Schubert F, Preiss T, Bähler J. A network of multiple regulatory layers shapes gene expression in fission yeast. Mol Cell 2007; 26:145-55; PMID:17434133; http://dx.doi.org/ 10.1016/j.molcel.2007.03.002
3. Thomsen S, Anders S, Janga SC, Huber W, Alonso CR. Genome-wide analysis of mRNA decay patterns during early Drosophila development. Genome Biol 2010; 11:R93; PMID:20858238; http://dx.doi.org/10.1186/gb-2010-11-9-r93
4. Lackner DH, Schmidt MW, Wu S, Wolf DA, Bähler J. Regulation of transcriptome, translation, and proteome in response to environmental stress in fission yeast. Genome Biol 2012; 13:R25; PMID:22512868; http://dx.doi.org/10. 1186/gb-2012-13-4-r25
5. Mata J, Marguerat S, Bähler J. Post-transcriptional control of gene expression: a genome-wide perspective. Trends Biochem Sci 2005; 30:506- 14; PMID:16054366; http://dx.doi.org/10.1016/j.tibs.2005.07.005
6. Pérez-Ortín JE, de Miguel-Jiménez L, Chávez S. Genome-wide studies of mRNA synthesis and degradation in eukaryotes. Biochim Biophys Acta 2012; 1819:604-15; PMID:22182827; http://dx.doi. org/10.1016/j.bbagrm.2011.12.002
7. Geisberg JV, Moqtaderi Z, Fan X, Ozsolak F, Struhl K. Global analysis of mRNA isoform half-lives reveals stabilizing and destabilizing elements in yeast. Cell 2014; 156:812-24; PMID:24529382; http://dx.doi.org/10.1016/j.cell.2013.12. 026
8. Wang Y, Liu CL, Storey JD, Tibshirani RJ, Herschlag D, Brown PO. Precision and functional specificity in mRNA decay. Proc Natl Acad Sci U S A 2002; 99:5860-5; PMID:11972065; http://dx.doi.org/10.1073/pnas.092538799
9. Yang E, van Nimwegen E, Zavolan M, Rajewsky N, Schroeder M, Magnasco M, Darnell JE Jr. Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res 2003; 13:1863-72; PMID:12902380
10. Narsai R, Howell KA, Millar AH, O'Toole N, Small I, Whelan J. Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. Plant Cell 2007; 19:3418-36; PMID:18024567; http://dx.doi.org/10.1105/tpc.107. 055046
11. Clark MB, Johnston RL, Inostroza-Ponta M, Fox AH, Fortini E, Moscato P, Dinger ME, Mattick JS. Genome-wide analysis of long noncoding RNA stability. Genome Res 2012; 22:885-98; PMID:22406755; http://dx.doi.org/10.1101/gr.131037. 111
12. Tani H, Mizutani R, Salam KA, Tano K, Ijiri K, Wakamatsu A, Isogai T, Suzuki Y, Akimitsu N. Genome-wide determination of RNA stability reveals hundreds of short-lived noncoding transcripts in mammals. Genome Res 2012; 22:947-56; PMID:22369889; http://dx.doi.org/10.1101/gr.130559.111
13. Windhager L, Bonfert T, Burger K, Ruzsics Z, Krebs S, Kaufmann S, Malterer G, L'Hernault A, Schilhabel M, Schreiber S, et al. Ultrashort and progressive 4sU-tagging reveals key characteristics of RNA processing at nucleotide resolution. Genome Res 2012; 22:2031-42; PMID:22539649; http://dx.doi.org/10.1101/gr.131847.111
14. Shalem O, Dahan O, Levo M, Martinez MR, Furman I, Segal E, Pilpel Y. Transient transcriptional responses to stress are generated by opposing effects of mRNA production and degradation. Mol Syst Biol 2008; 4:223; PMID:18854817; http://dx.doi.org/10.1038/msb.2008.59
15. Molin C, Jauhiainen A, Warringer J, Nerman O, Sunnerhagen P. mRNA stability changes precede changes in steady-state mRNA amounts during hyperosmotic stress. RNA 2009; 15:600-14; PMID:19223440; http://dx.doi.org/10. 1261/rna.1403509
16. Gao J, Wagnon JL, Protacio RM, Glazko GV, Beggs M, Raj V, Davidson MK, Wahls WP. A stress-activated, p38 mitogen-activated protein kinase-ATF/CREB pathway regulates post-transcriptional, sequence-dependent decay of target RNAs. Mol Cell Biol 2013; 33:3026-35; PMID:23732911; http://dx.doi.org/10.1128/MCB. 00349-13
17. Barenco M, Brewer D, Papouli E, Tomescu D, Callard R, Stark J, Hubank M. Dissection of a complex transcriptional response using genomewide transcriptional modelling. Mol Syst Biol 2009; 5:327; PMID:19920812; http://dx.doi.org/10.1038/msb.2009.84
18. Miller C, Schwalb B, Maier K, Schulz D, Dümcke S, Zacher B, Mayer A, Sydow J, Marcinowski L, Dölken L, et al. Dynamic transcriptome analysis measures rates of mRNA synthesis and decay in yeast. Mol Syst Biol 2011; 7:458; PMID:21206491; http://dx.doi.org/10.1038/msb.2010.112
19. Zeisel A, Köstler WJ, Molotski N, Tsai JM, Krauthgamer R, Jacob-Hirsch J, Rechavi G, Soen Y, Jung S, Yarden Y, et al. Coupled pre-mRNA and mRNA dynamics unveil operational strategies underlying transcriptional responses to stimuli. Mol Syst Biol 2011; 7:529; PMID:21915116; http://dx.doi.org/10.1038/msb.2011.62
20. García-Martínez J, Aranda A, Pérez-Ortín JE. Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms. Mol Cell 2004; 15:303-13; PMID:15260981; http://dx.doi.org/10.1016/j.molcel.2004.06.004
21. Dölken L, Ruzsics Z, Rädle B, Friedel CC, Zimmer R, Mages J, Hoffmann R, Dickinson P, Forster T, Ghazal P, et al. High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 2008; 14:1959- 72; PMID:18658122; http://dx.doi.org/10. 1261/rna.1136108
22. Munchel SE, Shultzaberger RK, Takizawa N, Weis K. Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol Biol Cell 2011; 22:2787-95; PMID:21680716; http://dx.doi.org/10.1091/mbc. E11-01-0028
23. Romero-Santacreu L, Moreno J, Pérez-Ortín JE, Alepuz P. Specific and global regulation of mRNA stability during osmotic stress in Saccharomyces cerevisiae. RNA 2009; 15:1110-20; PMID:19369426; http://dx.doi.org/10.1261/rna.1435709
24. Fan J, Yang X, Wang W, Wood WH 3rd, Becker KG, Gorospe M. Global analysis of stress-regulated mRNA turnover by using cDNA arrays. Proc Natl Acad Sci U S A 2002; 99:10611-6; PMID:12149460; http://dx.doi.org/10.1073/pnas.162212399
25. Legen J, Kemp S, Krause K, Profanter B, Herrmann RG, Maier RM. Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J 2002; 31:171-88; PMID:12121447; http://dx.doi.org/10.1046/ j.1365-313X.2002.01349.x
26. Castells-Roca L, García-Martínez J, Moreno J, Herrero E, Bellí G, Pérez-Ortín JE. Heat shock response in yeast involves changes in both transcription rates and mRNA stabilities. PLoS One 2011; 6:e17272; PMID:21364882; http://dx.doi.org/10.1371/journal.pone.0017272
27. Molina-Navarro MM, Castells-Roca L, Bellí G, García- Martínez J, Marín-Navarro J, Moreno J, Pérez-Ortín JE, Herrero E. Comprehensive transcriptional analysis of the oxidative response in yeast. J Biol Chem 2008; 283:17908-18; PMID:18424442; http://dx.doi.org/10. 1074/jbc.M800295200
28. Elkon R, Zlotorynski E, Zeller KI, Agami R. Major role for mRNA stability in shaping the kinetics of gene induction. BMC Genomics 2010; 11:259; PMID:20409322; http://dx.doi.org/10.1186/1471-2164-11-259
29. Chechik G, Koller D. Timing of gene expression responses to environmental changes. J Comput Biol 2009; 16:279-90; PMID:19193146; http://dx.doi.org/10. 1089/cmb.2008.13TT
30. Chechik G, Oh E, Rando O, Weissman J, Regev A, Koller D. Activity motifs reveal principles of timing in transcriptional control of the yeast metabolic network. Nat Biotechnol 2008; 26:1251-9; PMID:18953355; http://dx.doi.org/10. 1038/nbt.1499
31. Lyne R, Burns G, Mata J, Penkett CJ, Rustici G, Chen D, Langford C, Vetrie D, Bähler J. Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 2003; 4:27; PMID:12854975; http://dx.doi.org/10.1186/1471-2164-4-27
32. Sandoval J, Rodríguez JL, Tur G, Serviddio G, Pereda J, Boukaba A, Sastre J, Torres L, Franco L, López-Rodas G. RNAPol-ChIP: a novel application of chromatin immunoprecipitation to the analysis of real-time gene transcription. Nucleic Acids Res 2004; 32:e88; PMID:15247321; http://dx.doi.org/10.1093/nar/gnh091
33. Kim TS, Liu CL, Yassour M, Holik J, Friedman N, Buratowski S, Rando OJ. RNA polymerase mapping during stress responses reveals widespread nonproductive transcription in yeast. Genome Biol 2010; 11:R75; PMID:20637075; http://dx.doi.org/10.1186/gb-2010-11-7-r75
34. Pelechano V, Jimeno-González S, Rodríguez-Gil A, García-Martínez J, Pérez-Ortín JE, Chávez S. Regulon-specific control of transcription elongation across the yeast genome. PLoS Genet 2009; 5:e1000614; PMID:19696888; http://dx.doi.org/10.1371/journal. pgen.1000614
35. Wu JQ, Snyder M. RNA polymerase II stalling: loading at the start prepares genes for a sprint. Genome Biol 2008; 9:220; PMID:18466645; http://dx.doi.org/10.1186/gb-2008-9-5-220
36. McKinlay A, Araya CL, Fields S. Genome-wide analysis of nascent transcription in Saccharomyces cerevisiae. G3 (Bethesda) 2011; 1:549-58; PMID:22384366; http://dx.doi.org/10.1534/g3.111.000810
37. Rabani M, Levin JZ, Fan L, Adiconis X, Raychowdhury R, Garber M, Gnirke A, Nusbaum C, Hacohen N, Friedman N, et al. Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat Biotechnol 2011; 29:436-42; PMID:21516085; http://dx.doi.org/10.1038/nbt.1861
38. Heard NA, Holmes CC, Stephens DA. A quantitative study of gene regulation involved in the immune response of Anopheline mosquitoes. J Am Stat Assoc 2006; 101:18-29; http://dx.doi.org/10.1198/016214505000000187
39. Amorim MJ, Cotobal C, Duncan C, Mata J. Global coordination of transcriptional control and mRNA decay during cellular differentiation. Mol Syst Biol 2010; 6:380; PMID:20531409; http://dx.doi.org/10.1038/msb.2010.38
40. Woolcock KJ, Stunnenberg R, Gaidatzis D, Hotz H-R, Emmerth S, Barraud P, Bühler M. RNAi keeps Atf1-bound stress response genes in check at nuclear pores. Genes Dev 2012; 26:683-92; PMID:22431512; http://dx.doi.org/10.1101/gad. 186866.112
41. Lempiäinen H, Shore D. Growth control and ribosome biogenesis. Curr Opin Cell Biol 2009; 21:855-63; PMID:19796927; http://dx.doi.org/10.1016/j.ceb. 2009.09.002
42. López-Maury L, Marguerat S, Bähler J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 2008; 9:583-93; PMID:18591982; http://dx.doi.org/10.1038/nrg2398
43. Jorgensen P, Rupes I, Sharom JR, Schneper L, Broach JR, Tyers M. A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev 2004; 18:2491-505; PMID:15466158; http://dx.doi.org/10.1101/gad.1228804
44. Tanay A, Regev A, Shamir R. Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. Proc Natl Acad Sci U S A 2005; 102:7203-8; PMID:15883364; http://dx.doi.org/10.1073/pnas.0502521102
45. Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bähler J. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 2003; 14:214-29; PMID:12529438; http://dx.doi.org/10.1091/mbc.E02-08-0499
46. Chen D, Wilkinson CRM, Watt S, Penkett CJ, Toone WM, Jones N, Bähler J. Multiple pathways differentially regulate global oxidative stress responses in fission yeast. Mol Biol Cell 2008; 19:308-17; PMID:18003976; http://dx.doi.org/10.1091/mbc.E07-08-0735
47. 2. PLoS One 2010; 5:e11620; PMID:20661279; http://dx.doi.org/10.1371/ journal.pone.0011620
48. Marguerat S, Jensen TS, de Lichtenberg U, Wilhelm BT, Jensen LJ, Bähler J. The more the merrier: comparative analysis of microarray studies on cell cycle-regulated genes in fission yeast. Yeast 2006; 23:261-77; PMID:16544289; http://dx.doi.org/10.1002/yea.1351
49. Elemento O, Slonim N, Tavazoie S. A universal framework for regulatory element discovery across all genomes and data types. Mol Cell 2007; 28:337- 50; PMID:17964271; http://dx.doi.org/10.1016/j.molcel.2007.09.027
50. Riordan DP, Herschlag D, Brown PO. Identification of RNA recognition elements in the Saccharomyces cerevisiae transcriptome. Nucleic Acids Res 2011; 39:1501-9; PMID:20959291; http://dx.doi.org/10.1093/nar/gkq920
51. rd, Bähler J, Russell P. Cip1 and Cip2 are novel RNA-recognition-motif proteins that counteract Csx1 function during oxidative stress. Mol Biol Cell 2006; 17:1176-83; PMID:16407405; http://dx.doi.org/10. 1091/mbc.E05-09-0847
52. Goodarzi H, Najafabadi HS, Oikonomou P, Greco TM, Fish L, Salavati R, Cristea IM, Tavazoie S. Systematic discovery of structural elements governing stability of mammalian messenger RNAs. Nature 2012; 485:264-8; PMID:22495308; http://dx.doi.org/10.1038/nature11013
53. Bergkessel M, Whitworth GB, Guthrie C. Diverse environmental stresses elicit distinct responses at the level of pre-mRNA processing in yeast. RNA 2011; 17:1461-78; PMID:21697354; http://dx.doi.org/10.1261/rna.2754011
54. Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. Rapid, transcript-specific changes in splicing in response to environmental stress. Mol Cell 2007; 27:928-37; PMID:17889666; http://dx.doi.org/10.1016/j.molcel.2007. 07.018
55. Rodríguez-Gabriel MA, Watt S, Bähler J, Russell P. Upf1, an RNA helicase required for nonsensemediated mRNA decay, modulates the transcriptional response to oxidative stress in fission yeast. Mol Cell Biol 2006; 26:6347-56; PMID:16914721; http://dx.doi.org/10.1128/MCB.00286-06
56. Matia-González AM, Hasan A, Moe GH, Mata J, Rodríguez- Gabriel MA. Functional characterization of Upf1 targets in Schizosaccharomyces pombe. RNA Biol 2013; 10:1057-65; PMID:23619768; http://dx.doi.org/10.4161/rna. 24569
57. Garre E, Romero-Santacreu L, Barneo-Muñoz M, Miguel A, Pérez-Ortín JE, Alepuz P. Nonsense-mediated mRNA decay controls the changes in yeast ribosomal protein pre-mRNAs levels upon osmotic stress. PLoS One 2013; 8:e61240; PMID:23620734; http://dx.doi.org/10.1371/journal.pone. 0061240
58. Jeffares DC, Penkett CJ, Bähler J. Rapidly regulated genes are intron poor. Trends Genet 2008; 24:375- 8; PMID:18586348; http://dx.doi.org/10. 1016/j.tig.2008.05.006
59. Shalem O, Groisman B, Choder M, Dahan O, Pilpel Y. Transcriptome kinetics is governed by a genomewide coupling of mRNA production and degradation: a role for RNA Pol II. PLoS Genet 2011; 7:e1002273; PMID:21931566; http://dx.doi.org/10.1371/journal.pgen.1002273
60. Goler-Baron V, Selitrennik M, Barkai O, Haimovich G, Lotan R, Choder M. Transcription in the nucleus and mRNA decay in the cytoplasm are coupled processes. Genes Dev 2008; 22:2022-7; PMID:18676807; http://dx.doi.org/10.1101/ gad.473608
61. Harel-Sharvit L, Eldad N, Haimovich G, Barkai O, Duek L, Choder M. RNA polymerase II subunits link transcription and mRNA decay to translation. Cell 2010; 143:552-63; PMID:21074047; http://dx.doi.org/10.1016/j.cell.2010.10.033
62. Haimovich G, Medina DA, Causse SZ, Garber M, Millán-Zambrano G, Barkai O, Chávez S, Pérez- Ortín JE, Darzacq X, Choder M. Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis. Cell 2013; 153:1000-11; PMID:23706738; http://dx.doi.org/10.1016/j. cell.2013.05.012
63. Sun M, Schwalb B, Schulz D, Pirkl N, Etzold S, Larivière L, Maier KC, Seizl M, Tresch A, Cramer P. Comparative dynamic transcriptome analysis (cDTA) reveals mutual feedback between mRNA synthesis and degradation. Genome Res 2012; 22:1350- 9; PMID:22466169; http://dx.doi.org/10.1101/gr.130161.111
64. Sun M, Schwalb B, Pirkl N, Maier KC, Schenk A, Failmezger H, Tresch A, Cramer P. Global analysis of eukaryotic mRNA degradation reveals Xrn1- dependent buffering of transcript levels. Mol Cell 2013; 52:52-62; PMID:24119399; http://dx.doi.org/10.1016/j.molcel.2013.09.010
65. Dori-Bachash M, Shalem O, Manor YS, Pilpel Y, Tirosh I. Widespread promoter-mediated coordination of transcription and mRNA degradation. Genome Biol 2012; 13:R114; PMID:23237624; http://dx.doi.org/10.1186/gb-2012-13-12-r114
66. Bregman A, Avraham-Kelbert M, Barkai O, Duek L, Guterman A, Choder M. Promoter elements regulate cytoplasmic mRNA decay. Cell 2011; 147:1473- 83; PMID:22196725; http://dx.doi.org/10.1016/j.cell.2011.12.005
67. Trcek T, Larson DR, Moldón A, Query CC, Singer RH. Single-molecule mRNA decay measurements reveal promoter- regulated mRNA stability in yeast. Cell 2011; 147:1484-97; PMID:22196726; http://dx.doi.org/10.1016/j.cell.2011.11. 051
68. Sansó M, Vargas-Pérez I, García P, Ayté J, Hidalgo E. Nuclear roles and regulation of chromatin structure by the stress-dependent MAP kinase Sty1 of Schizosaccharomyces pombe. Mol Microbiol 2011; 82:542-54; PMID:21992435; http://dx.doi.org/10.1111/j.1365-2958.2011. 07851.x
69. Rodríguez-Gabriel MA, Burns G, McDonald WH, Martín V, Yates JR 3rd, Bähler J, Russell P. RNA-binding protein Csx1 mediates global control of gene expression in response to oxidative stress. EMBO J 2003; 22:6256-66; PMID:14633985; http://dx.doi.org/10.1093/emboj/cdg597
70. de Nadal E, Ammerer G, Posas F. Controlling gene expression in response to stress. Nat Rev Genet 2011; 12:833-45; PMID:22048664