#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Stress-Induced Nuclear RNA Degradation Pathways Regulate Yeast Bromodomain Factor 2 to Promote Cell Survival


Cells adapt to changes in the environment through modulating gene expression at both the RNA and protein levels. RNA degradation plays a central role in this adaption response, by controlling the stability of specific mRNAs to optimize protein production in different conditions. In this study, we show that the gene encoding Bromodomain Factor 2 (BDF2) is tightly regulated according to environmental conditions by two distinct RNA degradation mechanisms. We show that these RNA degradation pathways are critical for cell growth in specific conditions. Our study suggests that environmental modulation of nuclear RNA degradation pathways is a previously unappreciated aspect of gene expression control.


Vyšlo v časopise: Stress-Induced Nuclear RNA Degradation Pathways Regulate Yeast Bromodomain Factor 2 to Promote Cell Survival. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004661
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004661

Souhrn

Cells adapt to changes in the environment through modulating gene expression at both the RNA and protein levels. RNA degradation plays a central role in this adaption response, by controlling the stability of specific mRNAs to optimize protein production in different conditions. In this study, we show that the gene encoding Bromodomain Factor 2 (BDF2) is tightly regulated according to environmental conditions by two distinct RNA degradation mechanisms. We show that these RNA degradation pathways are critical for cell growth in specific conditions. Our study suggests that environmental modulation of nuclear RNA degradation pathways is a previously unappreciated aspect of gene expression control.


Zdroje

1. KornbergRD (1974) Chromatin structure: a repeating unit of histones and DNA. Science 184: 868–871.

2. KornbergRD, LorchY (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98: 285–294.

3. WuJ, GrunsteinM (2000) 25 years after the nucleosome model: chromatin modifications. Trends Biochem Sci 25: 619–623.

4. StrahlBD, AllisCD (2000) The language of covalent histone modifications. Nature 403: 41–45 doi:10.1038/47412

5. KurdistaniSK, GrunsteinM (2003) Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol 4: 276–284 doi:10.1038/nrm1075

6. ZentnerGE, HenikoffS (2013) Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20: 259–266 doi:10.1038/nsmb.2470

7. ZengL, ZhouMM (2002) Bromodomain: an acetyl-lysine binding domain. FEBS Lett 513: 124–128.

8. DurantM, PughBF (2007) NuA4-directed chromatin transactions throughout the Saccharomyces cerevisiae genome. Mol Cell Biol 27: 5327–5335 doi:10.1128/MCB.00468-07

9. KroganNJ, KeoghM-C, DattaN, SawaC, RyanOW, et al. (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 12: 1565–1576.

10. LadurnerAG, InouyeC, JainR, TjianR (2003) Bromodomains mediate an acetyl-histone encoded antisilencing function at heterochromatin boundaries. Mol Cell 11: 365–376.

11. MatangkasombutO, BuratowskiRM, SwillingNW, BuratowskiS (2000) Bromodomain factor 1 corresponds to a missing piece of yeast TFIID. Genes Dev 14: 951–962.

12. GhaemmaghamiS, HuhW-K, BowerK, HowsonRW, BelleA, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737–741 doi:10.1038/nature02046

13. VolanakisA, PassoniM, HectorRD, ShahS, KilchertC, et al. (2013) Spliceosome-mediated decay (SMD) regulates expression of nonintronic genes in budding yeast. Genes Dev 27: 2025–2038 doi:10.1101/gad.221960.113

14. KoborMS, VenkatasubrahmanyamS, MeneghiniMD, GinJW, JenningsJL, et al. (2004) A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2: E131 doi:10.1371/journal.pbio.0020131

15. LuPYT, LévesqueN, KoborMS (2009) NuA4 and SWR1-C: two chromatin-modifying complexes with overlapping functions and components. Biochem Cell Biol 87: 799–815 doi:10.1139/O09-062

16. ChuaP, RoederGS (1995) Bdf1, a yeast chromosomal protein required for sporulation. Mol Cell Biol 15: 3685–3696.

17. GarabedianMV, NoguchiC, ZieglerMA, DasMM, SinghT, et al. (2012) The double-bromodomain proteins Bdf1 and Bdf2 modulate chromatin structure to regulate S-phase stress response in Schizosaccharomyces pombe. Genetics 190: 487–500 doi:10.1534/genetics.111.135459

18. FuJ, HouJ, LiuL, ChenL, WangM, et al. (2013) Interplay between BDF1 and BDF2 and their roles in regulating the yeast salt stress response. FEBS J 280: 1991–2001 doi:10.1111/febs.12219

19. KapitzkyL, BeltraoP, BerensTJ, GassnerN, ZhouC, et al. (2010) Cross-species chemogenomic profiling reveals evolutionarily conserved drug mode of action. Mol Syst Biol 6: 451 doi:10.1038/msb.2010.107

20. WangJ, TadeoX, HouH, TuPG, ThompsonJ, et al. (2013) Epe1 recruits BET family bromodomain protein Bdf2 to establish heterochromatin boundaries. Genes Dev 27: 1886–1902 doi:10.1101/gad.221010.113

21. HarigayaY, ParkerR (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

22. KawashimaT, DouglassS, GabunilasJ, PellegriniM, ChanfreauGF (2014) Widespread Use of Non-productive Alternative Splice Sites in Saccharomyces cerevisiae. PLoS Genet 10: e1004249 doi:10.1371/journal.pgen.1004249

23. Danin-KreiselmanM, LeeCY, ChanfreauG (2003) RNAse III-mediated degradation of unspliced pre-mRNAs and lariat introns. Mol Cell 11: 1279–1289.

24. ZukerM (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415.

25. ChanfreauG, BuckleM, JacquierA (2000) Recognition of a conserved class of RNA tetraloops by Saccharomyces cerevisiae RNase III. Proc Natl Acad Sci U S A 97: 3142–3147 doi:10.1073/pnas.070043997

26. WangZ, HartmanE, RoyK, ChanfreauG, FeigonJ (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

27. RouskinS, ZubradtM, WashietlS, KellisM, WeissmanJS (2014) Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 505: 701–705 doi:10.1038/nature12894

28. LeeA, HenrasAK, ChanfreauG (2005) Multiple RNA surveillance pathways limit aberrant expression of iron uptake mRNAs and prevent iron toxicity in S. cerevisiae. Mol Cell 19: 39–51 doi:10.1016/j.molcel.2005.05.021

29. PelechanoV, ChávezS, Pérez-OrtínJE (2010) A complete set of nascent transcription rates for yeast genes. PLoS ONE 5: e15442 doi:10.1371/journal.pone.0015442

30. DichtlB, StevensA, TollerveyD (1997) Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes. EMBO J 16: 7184–7195 doi:10.1093/emboj/16.23.7184

31. YassourM, KaplanT, FraserHB, LevinJZ, PfiffnerJ, et al. (2009) Ab initio construction of a eukaryotic transcriptome by massively parallel mRNA sequencing. Proc Natl Acad Sci U S A 106: 3264–3269 doi:10.1073/pnas.0812841106

32. ZhangZ, DietrichFS (2005) Mapping of transcription start sites in Saccharomyces cerevisiae using 5′ SAGE. Nucleic Acids Res 33: 2838–2851 doi:10.1093/nar/gki583

33. LeeW, TilloD, BrayN, MorseRH, DavisRW, et al. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39: 1235–1244 doi:10.1038/ng2117

34. EgeciogluDE, HenrasAK, ChanfreauGF (2006) Contributions of Trf4p- and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12: 26–32 doi:10.1261/rna.2207206

35. LiangY-H, LavoieM, ComeauM-A, Abou ElelaS, JiX (2014) Structure of a eukaryotic RNase III postcleavage complex reveals a double-ruler mechanism for substrate selection. Mol Cell 54: 431–444 doi:10.1016/j.molcel.2014.03.006

36. SayaniS, ChanfreauGF (2012) Sequential RNA degradation pathways provide a fail-safe mechanism to limit the accumulation of unspliced transcripts in Saccharomyces cerevisiae. RNA 18: 1563–1572 doi:10.1261/rna.033779.112

37. AmraniN, GanesanR, KervestinS, MangusDA, GhoshS, et al. (2004) A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432: 112–118 doi:10.1038/nature03060

38. GalyV, GadalO, Fromont-RacineM, RomanoA, JacquierA, et al. (2004) Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 116: 63–73.

39. FendtS-M, SauerU (2010) Transcriptional regulation of respiration in yeast metabolizing differently repressive carbon substrates. BMC Syst Biol 4: 12 doi:10.1186/1752-0509-4-12

40. ChenL, LiuL, WangM, FuJ, ZhangZ, et al. (2013) Hal2p functions in Bdf1p-involved salt stress response in Saccharomyces cerevisiae. PLoS ONE 8: e62110 doi:10.1371/journal.pone.0062110

41. ZhaoJ, LinW, MaX, LuQ, MaX, et al. (2010) The protein kinase Hal5p is the high-copy suppressor of lithium-sensitive mutations of genes involved in the sporulation and meiosis as well as the ergosterol biosynthesis in Saccharomyces cerevisiae. Genomics 95: 290–298 doi:10.1016/j.ygeno.2010.02.010

42. Romero-SantacreuL, MorenoJ, Pérez-OrtínJE, AlepuzP (2009) Specific and global regulation of mRNA stability during osmotic stress in Saccharomyces cerevisiae. RNA 15: 1110–1120 doi:10.1261/rna.1435709

43. FavreC, AguilarPS, CarrilloMC (2008) Oxidative stress and chronological aging in glycogen-phosphorylase-deleted yeast. Free Radic Biol Med 45: 1446–1456 doi:10.1016/j.freeradbiomed.2008.08.021

44. ChangM, BellaouiM, BooneC, BrownGW (2002) A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc Natl Acad Sci USA 99: 16934–16939 doi:10.1073/pnas.262669299

45. KoçA, WheelerLJ, MathewsCK, MerrillGF (2004) Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools. J Biol Chem 279: 223–230 doi:10.1074/jbc.M303952200

46. TesauroC, Morozzo della RoccaB, OttavianiA, ColettaA, ZuccaroL, et al. (2013) Molecular mechanism of the camptothecin resistance of Glu710Gly topoisomerase IB mutant analyzed in vitro and in silico. Mol Cancer 12: 100 doi:10.1186/1476-4598-12-100

47. TkachJM, YimitA, LeeAY, RiffleM, CostanzoM, et al. (2012) Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress. Nat Cell Biol 14: 966–976 doi:10.1038/ncb2549

48. WangY, LiuCL, StoreyJD, TibshiraniRJ, HerschlagD, et al. (2002) Precision and functional specificity in mRNA decay. Proc Natl Acad Sci USA 99: 5860–5865 doi:10.1073/pnas.092538799

49. GarreE, Romero-SantacreuL, Barneo-MuñozM, MiguelA, Pérez-OrtínJE, et al. (2013) Nonsense-mediated mRNA decay controls the changes in yeast ribosomal protein pre-mRNAs levels upon osmotic stress. PLoS ONE 8: e61240 doi:10.1371/journal.pone.0061240

50. MatangkasombutO, BuratowskiS (2003) Different sensitivities of bromodomain factors 1 and 2 to histone H4 acetylation. Mol Cell 11: 353–363.

51. LundinC, NorthM, ErixonK, WaltersK, JenssenD, et al. (2005) Methyl methanesulfonate (MMS) produces heat-labile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res 33: 3799–3811 doi:10.1093/nar/gki681

52. FloydSR, PacoldME, HuangQ, ClarkeSM, LamFC, et al. (2013) The bromodomain protein Brd4 insulates chromatin from DNA damage signalling. Nature 498: 246–250 doi:10.1038/nature12147

53. GaytánBD, LoguinovAV, La Rosa DeVY, LerotJ-M, VulpeCD (2013) Functional genomics indicates yeast requires Golgi/ER transport, chromatin remodeling, and DNA repair for low dose DMSO tolerance. Front Genet 4: 154 doi:10.3389/fgene.2013.00154

54. GietzRD, SchiestlRH (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 31–34 doi:10.1038/nprot.2007.13

55. LongtineMS, McKenzieA, DemariniDJ, ShahNG, WachA, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961 doi:;10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U

56. WachA, BrachatA, PöhlmannR, PhilippsenP (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793–1808.

57. StuckeyS, StoriciF (2013) Gene knockouts, in vivo site-directed mutagenesis and other modifications using the delitto perfetto system in Saccharomyces cerevisiae. Meth Enzymol 533: 103–131 doi:10.1016/B978-0-12-420067-8.00008-8

58. ChanfreauG, RotondoG, LegrainP, JacquierA (1998) Processing of a dicistronic small nucleolar RNA precursor by the RNA endonuclease Rnt1. EMBO J 17: 3726–3737 doi:10.1093/emboj/17.13.3726

59. LamontagneB, ElelaSA (2001) Purification and characterization of Saccharomyces cerevisiae Rnt1p nuclease. Meth Enzymol 342: 159–167.

60. RondónAG, MischoHE, KawauchiJ, ProudfootNJ (2009) Fail-safe transcriptional termination for protein-coding genes in S. cerevisiae. Mol Cell 36: 88–98 doi:10.1016/j.molcel.2009.07.028

61. GhazalG, GagnonJ, JacquesP-E, LandryJ-R, RobertF, et al. (2009) Yeast RNase III triggers polyadenylation-independent transcription termination. Mol Cell 36: 99–109 doi:10.1016/j.molcel.2009.07.029

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#