The Prefoldin Complex Regulates Chromatin Dynamics during Transcription Elongation

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Transcriptional elongation requires the concerted action of several factors that allow RNA polymerase II to advance through chromatin in a highly processive manner. In order to identify novel elongation factors, we performed systematic yeast genetic screening based on the GLAM (Gene Length-dependent Accumulation of mRNA) assay, which is used to detect defects in the expression of long transcription units. Apart from well-known transcription elongation factors, we identified mutants in the prefoldin complex subunits, which were among those that caused the most dramatic phenotype. We found that prefoldin, so far involved in the cytoplasmic co-translational assembly of protein complexes, is also present in the nucleus and that a subset of its subunits are recruited to chromatin in a transcription-dependent manner. Prefoldin influences RNA polymerase II the elongation rate in vivo and plays an especially important role in the transcription elongation of long genes and those whose promoter regions contain a canonical TATA box. Finally, we found a specific functional link between prefoldin and histone dynamics after nucleosome remodeling, which is consistent with the extensive network of genetic interactions between this factor and the machinery regulating chromatin function. This study establishes the involvement of prefoldin in transcription elongation, and supports a role for this complex in cotranscriptional histone eviction.

Vyšlo v časopise: The Prefoldin Complex Regulates Chromatin Dynamics during Transcription Elongation. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003776
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003776

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Zdroje

1. PeralesR, BentleyD (2009) “Cotranscriptionality”: the transcription elongation complex as a nexus for nuclear transactions. Mol Cell 36 : 178–191.

2. RondonAG, JimenoS, AguileraA (2010) The interface between transcription and mRNP export: from THO to THSC/TREX-2. Biochim Biophys Acta 1799 : 533–538.

3. LiJ, GilmourDS (2011) Promoter proximal pausing and the control of gene expression. Curr Opin Genet Dev 21 : 231–235.

4. ReeseJC (2012) The control of elongation by the yeast Ccr4-Not complex. Biochim Biophys Acta 1829(1): 127–33.

5. SvejstrupJQ (2007) Contending with transcriptional arrest during RNAPII transcript elongation. Trends Biochem Sci 32 : 165–171.

6. Gomez-HerrerosF, de Miguel-JimenezL, Morillo-HuescaM, Delgado-RamosL, Munoz-CentenoMC, et al. (2012) TFIIS is required for the balanced expression of the genes encoding ribosomal components under transcriptional stress. Nucleic Acids Res 40(14): 6508–19.

7. AdelmanK, MarrMT, WernerJ, SaundersA, NiZ, et al. (2005) Efficient release from promoter-proximal stall sites requires transcript cleavage factor TFIIS. Mol Cell 17 : 103–112.

8. KulishD, StruhlK (2001) TFIIS enhances transcriptional elongation through an artificial arrest site in vivo. Mol Cell Biol 21 : 4162–4168.

9. HughesAL, JinY, RandoOJ, StruhlK (2012) A Functional Evolutionary Approach to Identify Determinants of Nucleosome Positioning: A Unifying Model for Establishing the Genome-wide Pattern. Mol Cell 48 : 5–15.

10. FuchsSM, LaribeeRN, StrahlBD (2009) Protein modifications in transcription elongation. Biochim Biophys Acta 1789 : 26–36.

11. PeteschSJ, LisJT (2012) Overcoming the nucleosome barrier during transcript elongation. Trends Genet 28 : 285–294.

12. van VugtJJ, RanesM, CampsteijnC, LogieC (2007) The ins and outs of ATP-dependent chromatin remodeling in budding yeast: biophysical and proteomic perspectives. Biochim Biophys Acta 1769 : 153–171.

13. FormosaT (2012) The role of FACT in making and breaking nucleosomes. Biochim Biophys Acta 1819 : 247–255.

14. SmolleM, VenkateshS, GogolMM, LiH, ZhangY, et al. (2012) Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat Struct Mol Biol 19 : 884–892.

15. CarrozzaMJ, LiB, FlorensL, SuganumaT, SwansonSK, et al. (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123 : 581–592.

16. LiB, HoweL, AndersonS, YatesJR (2003) The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J Biol Chem 278 : 8897–8903.

17. VenkateshS, SmolleM, LiH, GogolMM, SaintM, et al. (2012) Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489 : 452–455.

18. BuratowskiS (2009) Progression through the RNA polymerase II CTD cycle. Mol Cell 36 : 541–546.

19. OhtakiA, NoguchiK, YohdaM (2010) Structure and function of archaeal prefoldin, a co-chaperone of group II chaperonin. Front Biosci 15 : 708–717.

20. Martin-BenitoJ, BoskovicJ, Gomez-PuertasP, CarrascosaJL, SimonsCT, et al. (2002) Structure of eukaryotic prefoldin and of its complexes with unfolded actin and the cytosolic chaperonin CCT. EMBO J 21 : 6377–6386.

21. SiegertR, LerouxMR, ScheuflerC, HartlFU, MoarefiI (2000) Structure of the molecular chaperone prefoldin: unique interaction of multiple coiled coil tentacles with unfolded proteins. Cell 103 : 621–632.

22. SimonsCT, StaesA, RommelaereH, AmpeC, LewisSA, et al. (2004) Selective contribution of eukaryotic prefoldin subunits to actin and tubulin binding. J Biol Chem 279 : 4196–4203.

23. LacefieldS, SolomonF (2003) A novel step in beta-tubulin folding is important for heterodimer formation in Saccharomyces cerevisiae. Genetics 165 : 531–541.

24. SiegersK, BolterB, SchwarzJP, BottcherUM, GuhaS, et al. (2003) TRiC/CCT cooperates with different upstream chaperones in the folding of distinct protein classes. EMBO J 22 : 5230–5240.

25. GeisslerS, SiegersK, SchiebelE (1998) A novel protein complex promoting formation of functional alpha -⁠ and gamma-tubulin. EMBO J 17 : 952–966.

26. VainbergIE, LewisSA, RommelaereH, AmpeC, VandekerckhoveJ, et al. (1998) Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93 : 863–873.

27. LundinVF, LerouxMR, StirlingPC (2010) Quality control of cytoskeletal proteins and human disease. Trends Biochem Sci 35 : 288–297.

28. Morillo-HuescaM, VantiM, ChavezS (2006) A simple in vivo assay for measuring the efficiency of gene length-dependent processes in yeast mRNA biogenesis. FEBS J 273 : 756–769.

29. GaillardH, TousC, BotetJ, Gonzalez-AguileraC, QuinteroMJ, et al. (2009) Genome-wide analysis of factors affecting transcription elongation and DNA repair: a new role for PAF and Ccr4-not in transcription-coupled repair. PLoS Genet 5: e1000364.

30. KroganNJ, KimM, TongA, GolshaniA, CagneyG, et al. (2003) Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol 23 : 4207–4218.

31. LiJ, MoazedD, GygiSP (2002) Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J Biol Chem 277 : 49383–49388.

32. ChavezS, AguileraA (1997) The yeast HPR1 gene has a functional role in transcriptional elongation that uncovers a novel source of genome instability. Genes Dev 11 : 3459–3470.

33. KremerSB, KimS, JeonJO, MoustafaYW, ChenA, et al. (2012) Role of Mediator in regulating Pol II elongation and nucleosome displacement in Saccharomyces cerevisiae. Genetics 191 : 95–106.

34. KrukJA, DuttaA, FuJ, GilmourDS, ReeseJC (2011) The multifunctional Ccr4-Not complex directly promotes transcription elongation. Genes Dev 25 : 581–593.

35. RondonAG, GallardoM, Garcia-RubioM, AguileraA (2004) Molecular evidence indicating that the yeast PAF complex is required for transcription elongation. EMBO Rep 5 : 47–53.

36. BricmontPA, DaughertyJR, CooperTG (1991) The DAL81 gene product is required for induced expression of two differently regulated nitrogen catabolic genes in Saccharomyces cerevisiae. Mol Cell Biol 11 : 1161–1166.

37. MassonJY, RamotarD (1998) The transcriptional activator Imp2p maintains ion homeostasis in Saccharomyces cerevisiae. Genetics 149 : 893–901.

38. AlepuzPM, de NadalE, ZapaterM, AmmererG, PosasF (2003) Osmostress-induced transcription by Hot1 depends on a Hog1-mediated recruitment of the RNA Pol II. EMBO J 22 : 2433–2442.

39. LerouxMR, FandrichM, KlunkerD, SiegersK, LupasAN, et al. (1999) MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin. EMBO J 18 : 6730–6743.

40. MalagonF, TongAH, ShaferBK, StrathernJN (2004) Genetic interactions of DST1 in Saccharomyces cerevisiae suggest a role of TFIIS in the initiation-elongation transition. Genetics 166 : 1215–1227.

41. ShawRJ, ReinesD (2000) Saccharomyces cerevisiae transcription elongation mutants are defective in PUR5 induction in response to nucleotide depletion. Mol Cell Biol 20 : 7427–7437.

42. BruneC, MunchelSE, FischerN, PodtelejnikovAV, WeisK (2005) Yeast poly(A)-binding protein Pab1 shuttles between the nucleus and the cytoplasm and functions in mRNA export. RNA 11 : 517–531.

43. Ghavi-HelmY, MichautM, AckerJ, AudeJC, ThuriauxP, et al. (2008) Genome-wide location analysis reveals a role of TFIIS in RNA polymerase III transcription. Genes Dev 22 : 1934–1947.

44. GovindCK, ZhangF, QiuH, HofmeyerK, HinnebuschAG (2007) Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol Cell 25 : 31–42.

45. Nadal-RibellesM, CondeN, FloresO, Gonzalez-VallinasJ, EyrasE, et al. (2012) Hog1 bypasses stress-mediated down-regulation of transcription by RNA polymerase II redistribution and chromatin remodeling. Genome Biol 13: R106.

46. SternerDE, LeeJM, HardinSE, GreenleafAL (1995) The yeast carboxyl-terminal repeat domain kinase CTDK-I is a divergent cyclin-cyclin-dependent kinase complex. Mol Cell Biol 15 : 5716–5724.

47. Rodriguez-GilA, Garcia-MartinezJ, PelechanoV, Munoz-Centeno MdeL, GeliV, et al. (2010) The distribution of active RNA polymerase II along the transcribed region is gene-specific and controlled by elongation factors. Nucleic Acids Res 38 : 4651–4664.

48. RheeHS, PughBF (2012) Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483 : 295–301.

49. MuellerCL, PorterSE, HoffmanMG, JaehningJA (2004) The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Mol Cell 14 : 447–456.

50. MasonPB, StruhlK (2005) Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol Cell 17 : 831–840.

51. CheungV, ChuaG, BatadaNN, LandryCR, MichnickSW, et al. (2008) Chromatin -⁠ and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6: e277.

52. MasonPB, StruhlK (2003) The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol Cell Biol 23 : 8323–8333.

53. KroganNJ, KeoghMC, 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.

54. CollinsSR, MillerKM, MaasNL, RoguevA, FillinghamJ, et al. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446 : 806–810.

55. CostanzoM, BaryshnikovaA, BellayJ, KimY, SpearED, et al. (2010) The genetic landscape of a cell. Science 327 : 425–431.

56. DehePM, DichtlB, SchaftD, RoguevA, PamblancoM, et al. (2006) Protein interactions within the Set1 complex and their roles in the regulation of histone 3 lysine 4 methylation. J Biol Chem 281 : 35404–35412.

57. ShilatifardA (2012) The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem 81 : 65–95.

58. Pray-GrantMG, DanielJA, SchieltzD, YatesJR (2005) Chd1 chromodomain links histone H3 methylation with SAGA -⁠ and SLIK-dependent acetylation. Nature 433 : 434–438.

59. LeeCK, ShibataY, RaoB, StrahlBD, LiebJD (2004) Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet 36 : 900–905.

60. SchwabishMA, StruhlK (2004) Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol Cell Biol 24 : 10111–10117.

61. BoulonS, Pradet-BaladeB, VerheggenC, MolleD, BoireauS, et al. (2010) HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA pol ymerase II. Mol Cell 39 : 912–924.

62. KukalevA, NordY, PalmbergC, BergmanT, PercipalleP (2005) Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat Struct Mol Biol 12 : 238–244.

63. VisaN, PercipalleP (2010) Nuclear functions of actin. Cold Spring Harb Perspect Biol 2: a000620.

64. ObrdlikA, PercipalleP (2011) The F-actin severing protein cofilin-1 is required for RNA polymerase II transcription elongation. Nucleus 2 : 72–79.

65. WatanabeK, OzakiT, NakagawaT, MiyazakiK, TakahashiM, et al. (2002) Physical interaction of p73 with c-Myc and MM1, a c-Myc-binding protein, and modulation of the p73 function. J Biol Chem 277 : 15113–15123.

66. MousnierA, KubatN, Massias-SimonA, SegeralE, RainJC, et al. (2007) von Hippel Lindau binding protein 1-mediated degradation of integrase affects HIV-1 gene expression at a postintegration step. Proc Natl Acad Sci U S A 104 : 13615–13620.

67. LocascioA, BlazquezMA, AlabadiD (2013) Dynamic Regulation of Cortical Microtubule Organization through Prefoldin-DELLA Interaction. Curr Biol 23 : 804–809.

68. GinsburgDS, GovindCK, HinnebuschAG (2009) NuA4 lysine acetyltransferase Esa1 is targeted to coding regions and stimulates transcription elongation with Gcn5. Mol Cell Biol 29 : 6473–6487.

69. KristjuhanA, SvejstrupJQ (2004) Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J 23 : 4243–4252.

70. Gomez-HerrerosF, de Miguel-JimenezL, Millan-ZambranoG, PenateX, Delgado-RamosL, et al. (2012) One step back before moving forward: regulation of transcription elongation by arrest and backtracking. FEBS Lett 586 : 2820–2825.

71. BintuL, KopaczynskaM, HodgesC, LubkowskaL, KashlevM, et al. (2011) The elongation rate of RNA polymerase determines the fate of transcribed nucleosomes. Nat Struct Mol Biol 18 : 1394–1399.

72. KulaevaOI, GaykalovaDA, PestovNA, GolovastovVV, VassylyevDG, et al. (2009) Mechanism of chromatin remodeling and recovery during passage of RNA polymerase II. Nat Struct Mol Biol 16 : 1272–1278.

73. KuryanBG, KimJ, TranNN, LombardoSR, VenkateshS, et al. (2012) Histone density is maintained during transcription mediated by the chromatin remodeler RSC and histone chaperone NAP1 in vitro. Proc Natl Acad Sci U S A 109 : 1931–1936.

74. DekkerC, StirlingPC, McCormackEA, FilmoreH, PaulA, et al. (2008) The interaction network of the chaperonin CCT. EMBO J 27 : 1827–1839.

75. SawarkarR, SieversC, ParoR (2012) Hsp90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli. Cell 149 : 807–818.

76. TongAH, EvangelistaM, ParsonsAB, XuH, BaderGD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294 : 2364–2368.

77. MalloyLE, WenKK, PierickAR, WedemeyerEW, BergeronSE, et al. (2012) Thoracic aortic aneurysm (TAAD)-causing mutation in actin affects formin regulation of polymerization. J Biol Chem 287 : 28398–28408.

78. RaniPG, RanishJA, HahnS (2004) RNA polymerase II (Pol II)-TFIIF and Pol II-mediator complexes: the major stable Pol II complexes and their activity in transcription initiation and reinitiation. Mol Cell Biol 24 : 1709–1720.

79. ReeseJC, GreenMR (2003) Functional analysis of TFIID components using conditional mutants. Methods Enzymol 370 : 415–430.

80. BasehoarAD, ZantonSJ, PughBF (2004) Identification and distinct regulation of yeast TATA box-containing genes. Cell 116 : 699–709.

81. RosalenyLE, Ruiz-GarciaAB, Garcia-MartinezJ, Perez-OrtinJE, TorderaV (2007) The Sas3p and Gcn5p histone acetyltransferases are recruited to similar genes. Genome Biol 8: R119.

82. VantiM, GallasteguiE, RespaldizaI, Rodriguez-GilA, Gomez-HerrerosF, et al. (2009) Yeast genetic analysis reveals the involvement of chromatin reassembly factors in repressing HIV-1 basal transcription. PLoS Genet 5: e1000339.