New Partners in Regulation of Gene Expression: The Enhancer of Trithorax and Polycomb Corto Interacts with Methylated Ribosomal Protein L12 Its Chromodomain

English version České info

Chromodomains are found in many regulators of chromatin structure, and most of them recognize methylated lysines on histones. Here, we investigate the role of the Drosophila melanogaster protein Corto's chromodomain. The Enhancer of Trithorax and Polycomb Corto is involved in both silencing and activation of gene expression. Over-expression of the Corto chromodomain (CortoCD) in transgenic flies shows that it is a chromatin-targeting module, critical for Corto function. Unexpectedly, mass spectrometry analysis reveals that polypeptides pulled down by CortoCD from nuclear extracts correspond to ribosomal proteins. Furthermore, real-time interaction analyses demonstrate that CortoCD binds with high affinity RPL12 tri-methylated on lysine 3. Corto and RPL12 co-localize with active epigenetic marks on polytene chromosomes, suggesting that both are involved in fine-tuning transcription of genes in open chromatin. RNA–seq based transcriptomes of wing imaginal discs over-expressing either CortoCD or RPL12 reveal that both factors deregulate large sets of common genes, which are enriched in heat-response and ribosomal protein genes, suggesting that they could be implicated in dynamic coordination of ribosome biogenesis. Chromatin immunoprecipitation experiments show that Corto and RPL12 bind hsp70 and are similarly recruited on gene body after heat shock. Hence, Corto and RPL12 could be involved together in regulation of gene transcription. We discuss whether pseudo-ribosomal complexes composed of various ribosomal proteins might participate in regulation of gene expression in connection with chromatin regulators.

Vyšlo v časopise: New Partners in Regulation of Gene Expression: The Enhancer of Trithorax and Polycomb Corto Interacts with Methylated Ribosomal Protein L12 Its Chromodomain. PLoS Genet 8(10): e32767. doi:10.1371/journal.pgen.1003006
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003006

Souhrn

Zdroje

1. BannisterAJ, KouzaridesT (2011) Regulation of chromatin by histone modifications. Cell Res 21 : 381–395.

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

3. WinterS, FischleW, SeiserC (2008) Modulation of 14-3-3 interaction with phosphorylated histone H3 by combinatorial modification patterns. Cell Cycle 7 : 1336–1342.

4. ParoR, HognessDS (1991) The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A 88 : 263–267.

5. YapKL, ZhouMM (2011) Structure and mechanisms of lysine methylation recognition by the chromodomain in gene transcription. Biochemistry 50 : 1966–1980.

6. BallLJ, MurzinaNV, BroadhurstRW, RaineAR, ArcherSJ, et al. (1997) Structure of the chromatin binding (chromo) domain from mouse modifier protein 1. EMBO J 16 : 2473–2481.

7. MinJ, ZhangY, XuRM (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17 : 1823–1828.

8. BernsteinE, DuncanEM, MasuiO, GilJ, HeardE, AllisCD (2006) Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol Cell Biol 26 : 2560–2569.

9. MüllerJ, VerrijzerP (2009) Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr Opin Genet Dev 19 : 150–158.

10. BannisterAJ, ZegermanP, PartridgeJF, MiskaEA, ThomasJO, et al. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 : 120–124.

11. LachnerM, O'CarrollD, ReaS, MechtlerK, JenuweinT (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410 : 116–120.

12. HuangJ, BergerSL (2008) The emerging field of dynamic lysine methylation of non-histone proteins. Curr Opin Genet Dev 18 : 152–158.

13. SampathSC, MarazziI, YapKL, KrutchinskyAN, MecklenbraukerI, et al. (2007) Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly. Mol Cell 27 : 596–608.

14. GildeaJJ, LopezR, ShearnA (2000) A screen for new trithorax group genes identified little imaginal discs, the Drosophila melanogaster homologue of human retinoblastoma binding protein 2. Genetics 156 : 645–663.

15. LopezA, HiguetD, RossetR, DeutschJ, PeronnetF (2001) corto genetically interacts with Pc-G and trx-G genes and maintains the anterior boundary of Ultrabithorax expression in Drosophila larvae. Mol Genet Genomics 266 : 572–583.

16. SalvaingJ, DecovilleM, Mouchel-VielhE, BussièreM, DaulnyA, et al. (2006) Corto and DSP1 interact and bind to a maintenance element of the Scr Hox gene: understanding the role of Enhancers of trithorax and Polycomb. BMC Biol 4 : 9.

17. SalvaingJ, NagelAC, Mouchel-VielhE, BloyerS, MaierD, et al. (2008) The enhancer of trithorax and polycomb Corto interacts with Cyclin G in Drosophila. PLoS ONE 3: e1658.

18. SalvaingJ, LopezA, BoivinA, DeutschJS, PeronnetF (2003) The Drosophila Corto protein interacts with Polycomb-group proteins and the GAGA factor. Nucleic Acids Res 31 : 2873–2882.

19. StruhlG (1982) Spineless-aristapedia: a homeotic gene that does not control the development of specific compartments in Drosophila. Genetics 102 : 737–749.

20. KodjabachianL, DelaageM, MaurelC, MiassodR, JacqB, RossetR (1998) Mutations in ccf, a novel Drosophila gene encoding a chromosomal factor, affect progression through mitosis and interact with Pc-G mutations. Embo J 17 : 1063–1075.

21. PattatucciAM, OttesonDC, KaufmanTC (1991) A functional and structural analysis of the Sex combs reduced locus of Drosophila melanogaster. Genetics 129 : 423–441.

22. BrognaS, SatoTA, RosbashM (2002) Ribosome components are associated with sites of transcription. Mol Cell 10 : 93–104.

23. Porras-YakushiTR, WhiteleggeJP, ClarkeS (2006) A novel SET domain methyltransferase in yeast: Rkm2-dependent trimethylation of ribosomal protein L12ab at lysine 10. J Biol Chem 281 : 35835–35845.

24. PolevodaB, ShermanF (2007) Methylation of proteins involved in translation. Mol Microbiol 65 : 590–606.

25. SadaieM, ShinmyozuK, NakayamaJ (2008) A conserved SET domain methyltransferase, Set11, modifies ribosomal protein Rpl12 in fission yeast. J Biol Chem 283 : 7185–7195.

26. StruttH, ParoR (1997) The polycomb group protein complex of Drosophila melanogaster has different compositions at different target genes. Mol Cell Biol 17 : 6773–6783.

27. SmothersJF, HenikoffS (2001) The hinge and chromo shadow domain impart distinct targeting of HP1-like proteins. Mol Cell Biol 21 : 2555–2569.

28. BoehmK, SaundersA, WernerJ, LisT (2003) Transcription Factor and Polymerase Recruitment, Modification, and Movement on dhsp70 In Vivo in the Minutes following Heat Shock. Mol Cell Biol 23 : 7628–7637.

29. SaurinAJ, ShaoZ, Erdjument-BromageH, TempstP, KingstonRE (2001) A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 412 : 655–660.

30. GuruharshaKG, RualJF, ZhaiB, MintserisJ, VaidyaP, et al. (2011) A protein complex network of Drosophila melanogaster. Cell 147 : 690–703.

31. KimK, ChoiJ, HeoK, KimH, LevensD, et al. (2008) Isolation and characterization of a novel H1.2 complex that acts as a repressor of p53-mediated transcription. J Biol Chem 283 : 9113–9126.

32. BhavsarRB, MakleyLN, TsonisPA (2010) The other lives of ribosomal proteins. Hum Genomics 4 : 327–344.

33. FriedmanDI, SchauerAT, BaumannMR, BaronLS, AdhyaSL (1981) Evidence that ribosomal protein S10 participates in control of transcription termination. Proc Natl Acad Sci U S A 78 : 1115–1118.

34. IvanovAV, MalyginAA, KarpovaGG (2006) Eukaryotic ribosomal proteins: Interactions with their own pre-mRNAs and their involvement in splicing regulation. Molecular Biology 40 : 570–578.

35. DenellRE (1978) Homoeosis in Drosophila. II. a Genetic Analysis of Polycomb. Genetics 90 : 277–289.

36. FauvarqueMO, LaurentiP, BoivinA, BloyerS, Griffin-SheaR, et al. (2001) Dominant modifiers of the polyhomeotic extra-sex-combs phenotype induced by marked P element insertional mutagenesis in Drosophila. Genet Res 78 : 137–148.

37. Saebøe-LarssenS, LyamouriM, MerriamJ, OksvoldMP, LambertssonA (1998) Ribosomal protein insufficiency and the minute syndrome in Drosophila: a dose-response relationship. Genetics 148 : 1215–1224.

38. MelnickMB, NollE, PerrimonN (1993) The Drosophila stubarista phenotype is associated with a dosage effect of the putative ribosome-associated protein D-p40 on spineless. Genetics 135 : 553–564.

39. NiJQ, LiuLP, HessD, RietdorfJ, SunFL (2006) Drosophila ribosomal proteins are associated with linker histone H1 and suppress gene transcription. Genes Dev 20 : 1959–1973.

40. BatschéE, YanivM, MuchardtC (2006) The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat Struct Mol Biol 13 : 22–29.

41. AjuhP, KusterB, PanovK, ZomerdijkJC, MannM, LamondAI (2000) Functional analysis of the human CDC5L complex and identification of its components by mass spectrometry. EMBO J 19 : 6569–6581.

42. DeS, BrognaS (2010) Are ribosomal proteins present at transcription sites on or off ribosomal subunits? Biochem Soc Trans 38 : 1543–1547.

43. DeS, VarsallyW, FalcianiF, BrognaS (2011) Ribosomal proteins' association with transcription sites peaks at tRNA genes in Schizosaccharomyces pombe. RNA 17 : 1713–1726.

44. ChandramouliP, TopfM, MénétretJF, EswarN, CannoneJJ, et al. (2008) Structure of the mammalian 80S ribosome at 8.7 A resolution. Structure 16 : 535–548.

45. DahlbergJE, LundE, GoodwinEB (2003) Nuclear translation: What is the evidence? RNA 9 : 1–8.

46. SchroderPA, MooreMJ (2005) Association of ribosomal proteins with nascent transcripts in S. cerevisiae. RNA 11 : 1521–1529.

47. CarrollAJ, HeazlewoodJL, ItoJ, MillarAH (2008) Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol Cell Proteomics 7 : 347–369.

48. StelzlU, WormU, LalowskiM, HaenigC, BrembeckFH, et al. (2005) A human protein-protein interaction network: a resource for annotating the proteome. Cell 122 : 957–968.

49. Porras-YakushiTR, WhiteleggeJP, ClarkeS (2007) Yeast ribosomal/cytochrome c SET domain methyltransferase subfamily: identification of Rpl23ab methylation sites and recognition motifs. J Biol Chem 282 : 12368–12376.

50. GraveleyBR, BrooksAN, CarlsonJW, DuffMO, LandolinJM, et al. (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471 : 473–479.

51. KomiliS, FarnyNG, RothFP, SilverPA (2007) Functional specificity among ribosomal proteins regulates gene expression. Cell 131 : 557–571.

52. BeltranS, AnguloM, PignatelliM, SerrasF, CorominasM (2007) Functional dissection of the ash2 and ash1 transcriptomes provides insights into the transcriptional basis of wing phenotypes and reveals conserved protein interactions. Genome Biol 8: R67.

53. SalvaingJ, Mouchel-VielhE, BloyerS, PreissA, PeronnetF (2008) Regulation of Abd-B expression by Cyclin G and Corto in the abdominal epithelium of Drosophila. Hereditas 145 : 138–146.

54. FaradjiF, BloyerS, Dardalhon-CuménalD, RandsholtNB, PeronnetF (2011) Drosophila melanogaster Cyclin G coordinates cell growth and cell proliferation. Cell Cycle 10 : 1–14.

55. FellerC, PrestelM, HartmannH, StraubT, SödingJ, BeckerPB (2011) The MOF-containing NSL complex associates globally with housekeeping genes, but activates only a defined subset. Nucleic Acids Res

56. TuWY, HuangYC, LiuLF, ChangLH, TamMF (2011) Rpl12p affects the transcription of the PHO pathway high-affinity inorganic phosphate transporters and repressible phosphatases. Yeast 28 : 481–493.

57. WarnerJR, McIntoshKB (2009) How common are extraribosomal functions of ribosomal proteins? Mol Cell 34 : 3–11.

58. DebatV, BloyerS, FaradjiF, GidaszewskiN, NavarroN, et al. (2011) Developmental Stability: A Major Role for Cyclin G in Drosophila melanogaster. PLoS Genet 7: e1002314.

59. KrattingerA, GendreN, RamaekersA, GrillenzoniN, StockerRF (2007) DmOAZ, the unique Drosophila melanogaster OAZ homologue is involved in posterior spiracle development. Dev Genes Evol 217 : 197–208.

60. HeberleinU, TjianR (1988) Temporal pattern of alcohol dehydrogenase gene transcription reproduced by Drosophila stage-specific embryonic extracts. Nature 331 : 410–415.

61. Mouchel-VielhE, RougeotJ, DecovilleM, PeronnetF (2011) The MAP kinase ERK and its scaffold protein MP1 interact with the chromatin regulator Corto during Drosophila wing tissue development. BMC Dev Biol 11 : 17.

62. RogersSL, RogersGC (2008) Culture of Drosophila S2 cells and their use for RNAi-mediated loss-of-function studies and immunofluorescence microscopy. Nat Protoc 3 : 606–611.

63. SalvaingJ, LopezA, BoivinA, DeutschJS, PeronnetF (2003) The Drosophila Corto protein interacts with Polycomb-group proteins and the GAGA factor. Nucleic Acids Res 31 : 2873–2882.

64. Pérez-LluchS, BlancoE, CarbonellA, RahaD, SnyderM, et al. (2011) Genome-wide chromatin occupancy analysis reveals a role for ASH2 in transcriptional pausing. Nucleic Acids Res 39 : 4628–4639.

65. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

66. RobinsonMD, OshlackA (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11: R25.

67. HuangDW, ShermanBT, LempickiRA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4 : 44–57.