Systematic Analysis of the Role of RNA-Binding Proteins in the Regulation of RNA Stability

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Messenger RNAs (mRNAs) are the molecules that relay the information from genes (DNA) to proteins. Cells contain different amounts of each mRNA type depending on their function and their situation. The quantity of each mRNA depends on the balance between its production (transcription) and its degradation (mRNA decay). Recent studies have shown that the rate at which each mRNA is degraded is specific for every gene, but little is known about how this is regulated. In this work, we look at the role of a class of proteins that bind to RNA molecules (RNA-binding proteins, or RBPs) in the regulation of RNA decay. By systematically examining cells in which a single RBP has been inactivated we identify those that are important for RNA degradation. We found RBPs that make mRNAs more stable (that is, they are degraded more slowly) and others that make them unstable. These RBPs control the RNAs of genes with common features, suggesting that they provide a way of coordinating the function of groups of genes. However, for many genes we did not find RBPs that control their stability, indicating that other players are important to regulate RNA degradation.

Vyšlo v časopise: Systematic Analysis of the Role of RNA-Binding Proteins in the Regulation of RNA Stability. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004684
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004684

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Zdroje

1. Perez-OrtinJE (2007) Genomics of mRNA turnover. Brief Funct Genomic Proteomic 6: 282–291.

2. ElkonR, ZlotorynskiE, ZellerKI, AgamiR (2010) Major role for mRNA stability in shaping the kinetics of gene induction. BMC Genomics 11: 259.

3. HaoS, BaltimoreD (2009) The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules. Nat Immunol 10: 281–288.

4. Romero-SantacreuL, MorenoJ, Perez-OrtinJE, AlepuzP (2009) Specific and global regulation of mRNA stability during osmotic stress in Saccharomyces cerevisiae. RNA 15: 1110–1120.

5. ShalemO, DahanO, LevoM, MartinezMR, FurmanI, et al. (2008) Transient transcriptional responses to stress are generated by opposing effects of mRNA production and degradation. Mol Syst Biol 4: 223.

6. HerrickD, ParkerR, JacobsonA (1990) Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol Cell Biol 10: 2269–2284.

7. SachsAB (1993) Messenger RNA degradation in eukaryotes. Cell 74: 413–421.

8. Perez-OrtinJE, AlepuzP, ChavezS, ChoderM (2013) Eukaryotic mRNA decay: methodologies, pathways, and links to other stages of gene expression. J Mol Biol 425: 3750–3775.

9. MunchelSE, ShultzabergerRK, TakizawaN, WeisK (2011) Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol Biol Cell 22: 2787–2795.

10. SunM, SchwalbB, SchulzD, PirklN, EtzoldS, et al. (2012) Comparative dynamic transcriptome analysis (cDTA) reveals mutual feedback between mRNA synthesis and degradation. Genome Res 22: 1350–1359.

11. WangY, LiuCL, StoreyJD, TibshiraniRJ, HerschlagD, et al. (2002) Precision and functional specificity in mRNA decay. Proc Natl Acad Sci U S A 99: 5860–5865.

12. AmorimMJ, CotobalC, DuncanC, MataJ (2010) Global coordination of transcriptional control and mRNA decay during cellular differentiation. Mol Syst Biol 6: 380.

13. FriedelCC, DolkenL, RuzsicsZ, KoszinowskiUH, ZimmerR (2009) Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res 37: e115.

14. NeffAT, LeeJY, WiluszJ, TianB, WiluszCJ (2012) Global analysis reveals multiple pathways for unique regulation of mRNA decay in induced pluripotent stem cells. Genome Res 22: 1457–1467.

15. RabaniM, LevinJZ, FanL, AdiconisX, RaychowdhuryR, et al. (2011) Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat Biotechnol 29: 436–442.

16. YangE, van NimwegenE, ZavolanM, RajewskyN, SchroederM, et al. (2003) Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res 13: 1863–1872.

17. GarneauNL, WiluszJ, WiluszCJ (2007) The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8: 113–126.

18. AndersonJS, ParkerRP (1998) The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. Embo J 17: 1497–1506.

19. CollerJ, ParkerR (2004) Eukaryotic mRNA decapping. Annu Rev Biochem 73: 861–890.

20. CaoD, ParkerR (2001) Computational modeling of eukaryotic mRNA turnover. Rna 7: 1192–1212.

21. ParkerR (2012) RNA degradation in Saccharomyces cerevisae. Genetics 191: 671–702.

22. HeatonB, DeckerC, MuhlradD, DonahueJ, JacobsonA, et al. (1992) Analysis of chimeric mRNAs derived from the STE3 mRNA identifies multiple regions within yeast mRNAs that modulate mRNA decay. Nucleic Acids Res 20: 5365–5373.

23. ShawG, KamenR (1986) A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46: 659–667.

24. ChenCY, GherziR, OngSE, ChanEL, RaijmakersR, et al. (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107: 451–464.

25. Lykke-AndersenJ, WagnerE (2005) Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev 19: 351–361.

26. GoldstrohmAC, HookBA, SeayDJ, WickensM (2006) PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol 13: 533–539.

27. SimoneLE, KeeneJD (2013) Mechanisms coordinating ELAV/Hu mRNA regulons. Curr Opin Genet Dev 23: 35–43.

28. DrinnenbergIA, WeinbergDE, XieKT, MowerJP, WolfeKH, et al. (2009) RNAi in budding yeast. Science 326: 544–550.

29. ChangSS, ZhangZ, LiuY (2012) RNA interference pathways in fungi: mechanisms and functions. Annu Rev Microbiol 66: 305–323.

30. MuhlradD, ParkerR (1999) Recognition of yeast mRNAs as “nonsense containing” leads to both inhibition of mRNA translation and mRNA degradation: implications for the control of mRNA decapping. Mol Biol Cell 10: 3971–3978.

31. HaimovichG, MedinaDA, CausseSZ, GarberM, Millan-ZambranoG, et al. (2013) Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis. Cell 153: 1000–1011.

32. SunM, SchwalbB, PirklN, MaierKC, SchenkA, et al. (2013) Global analysis of eukaryotic mRNA degradation reveals Xrn1-dependent buffering of transcript levels. Mol Cell 52: 52–62.

33. StevensonAL, NorburyCJ (2006) The Cid1 family of non-canonical poly(A) polymerases. Yeast 23: 991–1000.

34. RisslandOS, NorburyCJ (2009) Decapping is preceded by 3′ uridylation in a novel pathway of bulk mRNA turnover. Nat Struct Mol Biol 16: 616–623.

35. KimDU, HaylesJ, KimD, WoodV, ParkHO, et al. (2010) Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 28: 617–623.

36. WoodV, HarrisMA, McDowallMD, RutherfordK, VaughanBW, et al. (2012) PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res 40: D695–699.

37. TusherVG, TibshiraniR, ChuG (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116–5121.

38. KanohJ, SugimotoA, YamamotoM (1995) Schizosaccharomyces pombe zfs1+ encoding a zinc-finger protein functions in the mating pheromone recognition pathway. Mol Biol Cell 6: 1185–1195.

39. CuthbertsonBJ, LiaoY, BirnbaumerL, BlackshearPJ (2008) Characterization of zfs1 as an mRNA-binding and -destabilizing protein in Schizosaccharomyces pombe. J Biol Chem 283: 2586–2594.

40. HarigayaY, TanakaH, YamanakaS, TanakaK, WatanabeY, et al. (2006) Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442: 45–50.

41. St-AndreO, LemieuxC, PerreaultA, LacknerDH, BahlerJ, et al. (2010) Negative regulation of meiotic gene expression by the nuclear poly(a)-binding protein in fission yeast. J Biol Chem 285: 27859–27868.

42. SugiyamaT, Sugioka-SugiyamaR (2011) Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast. Embo J 30: 1027–1039.

43. LemayJF, D'AmoursA, LemieuxC, LacknerDH, St-SauveurVG, et al. (2010) The nuclear poly(A)-binding protein interacts with the exosome to promote synthesis of noncoding small nucleolar RNAs. Mol Cell 37: 34–45.

44. LeeNN, ChalamcharlaVR, Reyes-TurcuF, MehtaS, ZofallM, et al. (2013) Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance. Cell 155: 1061–1074.

45. JinQW, McCollumD (2003) Scw1p antagonizes the septation initiation network to regulate septum formation and cell separation in the fission yeast Schizosaccharomyces pombe. Eukaryot Cell 2: 510–520.

46. KaragiannisJ, OultonR, YoungPG (2002) The Scw1 RNA-binding domain protein regulates septation and cell-wall structure in fission yeast. Genetics 162: 45–58.

47. TodaT, DhutS, Superti-FurgaG, GotohY, NishidaE, et al. (1996) The fission yeast pmk1+ gene encodes a novel mitogen-activated protein kinase homolog which regulates cell integrity and functions coordinately with the protein kinase C pathway. Mol Cell Biol 16: 6752–6764.

48. CalongeTM, NakanoK, ArellanoM, AraiR, KatayamaS, et al. (2000) Schizosaccharomyces pombe rho2p GTPase regulates cell wall alpha-glucan biosynthesis through the protein kinase pck2p. Mol Biol Cell 11: 4393–4401.

49. GuptaS, Mana-CapelliS, McLeanJR, ChenCT, RayS, et al. (2013) Identification of SIN pathway targets reveals mechanisms of crosstalk between NDR kinase pathways. Curr Biol 23: 333–338.

50. HoffmannB, NickelJ, SpeerF, SchaferB (2008) The 3′ ends of mature transcripts are generated by a processosome complex in fission yeast mitochondria. J Mol Biol 377: 1024–1037.

51. MatsuyamaA, AraiR, YashirodaY, ShiraiA, KamataA, et al. (2006) ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 24: 841–847.

52. GuhaS, Lopez-MauryL, ShawM, BahlerJ, NorburyCJ, et al. (2011) Transcriptional and cellular responses to defective mitochondrial proteolysis in fission yeast. J Mol Biol 408: 222–237.

53. MataJ, LyneR, BurnsG, BählerJ (2002) The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32: 143–147.

54. ChenD, TooneWM, MataJ, LyneR, BurnsG, et al. (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14: 214–229.

55. SinghG, Lykke-AndersenJ (2003) New insights into the formation of active nonsense-mediated decay complexes. Trends Biochem Sci 28: 464–466.

56. WenJ, BrognaS (2010) Splicing-dependent NMD does not require the EJC in Schizosaccharomyces pombe. Embo J 29: 1537–1551.

57. LemieuxC, MargueratS, LafontaineJ, BarbezierN, BahlerJ, et al. (2011) A Pre-mRNA degradation pathway that selectively targets intron-containing genes requires the nuclear poly(A)-binding protein. Mol Cell 44: 108–119.

58. Rodriguez-GabrielMA, BurnsG, McDonaldWH, MartinV, YatesJR3rd, et al. (2003) RNA-binding protein Csx1 mediates global control of gene expression in response to oxidative stress. EMBO J 22: 6256–6266.

59. SugiuraR, KitaA, ShimizuY, ShuntohH, SioSO, et al. (2003) Feedback regulation of MAPK signalling by an RNA-binding protein. Nature 424: 961–965.

60. RiordanDP, HerschlagD, BrownPO (2010) Identification of RNA recognition elements in the Saccharomyces cerevisiae transcriptome. Nucleic Acids Res 39: 1501–1509.

61. YamashitaA, ShichinoY, TanakaH, HiriartE, Touat-TodeschiniL, et al. (2012) Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes. Open Biol 2: 120014.

62. AmorimMJ, MataJ (2009) Rng3, a member of the UCS family of myosin co-chaperones, associates with myosin heavy chains cotranslationally. EMBO Rep 10: 186–191.

63. DuncanCD, MataJ (2011) Widespread cotranslational formation of protein complexes. PLoS Genet 7: e1002398.

64. DuncanCD, MataJ (2014) The translational landscape of fission-yeast meiosis and sporulation. Nat Struct Mol Biol 21: 641–647.

65. MataJ (2010) Genome-wide mapping of myosin protein-RNA networks suggests the existence of specialized protein production sites. Faseb J 24: 479–484.

66. Matia-GonzalezAM, HasanA, MoeGH, MataJ, Rodriguez-GabrielMA (2013) Functional characterization of Upf1 targets in Schizosaccharomyces pombe. RNA Biol 10: 1057–1065.

67. KennedyPJ, VashishtAA, HoeKL, KimDU, ParkHO, et al. (2008) A genome-wide screen of genes involved in cadmium tolerance in Schizosaccharomyces pombe. Toxicol Sci 106: 124–139.

68. SunLL, LiM, SuoF, LiuXM, ShenEZ, et al. (2013) Global analysis of fission yeast mating genes reveals new autophagy factors. PLoS Genet 9: e1003715.

69. GerberAP, HerschlagD, BrownPO (2004) Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol 2: E79.

70. KeeneJD (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8: 533–543.

71. BregmanA, Avraham-KelbertM, BarkaiO, DuekL, GutermanA, et al. (2011) Promoter elements regulate cytoplasmic mRNA decay. Cell 147: 1473–1483.

72. TrcekT, LarsonDR, MoldonA, QueryCC, SingerRH (2011) Single-molecule mRNA decay measurements reveal promoter- regulated mRNA stability in yeast. Cell 147: 1484–1497.

73. ForsburgSL, RhindN (2006) Basic methods for fission yeast. Yeast 23: 173–183.

74. LyneR, BurnsG, MataJ, PenkettCJ, RusticiG, et al. (2003) Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4: 27.

75. CrooksGE, HonG, ChandoniaJM, BrennerSE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188–1190.

76. RusticiG, MataJ, KivinenK, LioP, PenkettCJ, et al. (2004) Periodic gene expression program of the fission yeast cell cycle. Nat Genet 36: 809–817.