PRMT4 Is a Novel Coactivator of c-Myb-Dependent Transcription in Haematopoietic Cell Lines

English version České info

Protein arginine methyltransferase 4 (PRMT4)–dependent methylation of arginine residues in histones and other chromatin-associated proteins plays an important role in the regulation of gene expression. However, the exact mechanism of how PRMT4 activates transcription remains elusive. Here, we identify the chromatin remodeller Mi2α as a novel interaction partner of PRMT4. PRMT4 binds Mi2α and its close relative Mi2β, but not the other components of the repressive Mi2-containing NuRD complex. In the search for the biological role of this interaction, we find that PRMT4 and Mi2α/β interact with the transcription factor c-Myb and cooperatively coactivate c-Myb target gene expression in haematopoietic cell lines. This coactivation requires the methyltransferase and ATPase activity of PRMT4 and Mi2, respectively. Chromatin immunoprecipitation analysis shows that c-Myb target genes are direct transcriptional targets of PRMT4 and Mi2. Knockdown of PRMT4 or Mi2α/β in haematopoietic cells of the erythroid lineage results in diminished transcriptional induction of c-Myb target genes, attenuated cell growth and survival, and deregulated differentiation resembling the effects caused by c-Myb depletion. These findings reveal an important and so far unknown connection between PRMT4 and the chromatin remodeller Mi2 in c-Myb signalling.

Vyšlo v časopise: PRMT4 Is a Novel Coactivator of c-Myb-Dependent Transcription in Haematopoietic Cell Lines. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003343
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003343

Souhrn

Zdroje

1. Di LorenzoA, BedfordMT (2011) Histone arginine methylation. FEBS Lett 585 : 2024–2031.

2. BachandF (2007) Protein arginine methyltransferases: from unicellular eukaryotes to humans. Eukaryot Cell 6 : 889–898.

3. BedfordMT, ClarkeSG (2009) Protein arginine methylation in mammals: who, what, and why. Mol Cell 33 : 1–13.

4. LeeYH, StallcupMR (2009) Minireview: protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol Endocrinol 23 : 425–433.

5. ChenD, MaH, HongH, KohSS, HuangSM, et al. (1999) Regulation of transcription by a protein methyltransferase. Science 284 : 2174–2177.

6. MaH, BaumannCT, LiH, StrahlBD, RiceR, et al. (2001) Hormone-dependent, CARM1-directed, arginine-specific methylation of histone H3 on a steroid-regulated promoter. Curr Biol 11 : 1981–1985.

7. BauerUM, DaujatS, NielsenSJ, NightingaleK, KouzaridesT (2002) Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep 3 : 39–44.

8. AnW, KimJ, RoederRG (2004) Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117 : 735–748.

9. CovicM, HassaPO, SaccaniS, BuerkiC, MeierNI, et al. (2005) Arginine methyltransferase CARM1 is a promoter-specific regulator of NF-kappaB-dependent gene expression. Embo J 24 : 85–96.

10. HassaPO, CovicM, BedfordMT, HottigerMO (2008) Protein arginine methyltransferase 1 coactivates NF-kappaB-dependent gene expression synergistically with CARM1 and PARP1. J Mol Biol 377 : 668–678.

11. MetivierR, PenotG, HubnerMR, ReidG, BrandH, et al. (2003) Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115 : 751–763.

12. WagnerS, WeberS, KleinschmidtMA, NagataK, BauerUM (2006) SET-mediated promoter hypoacetylation is a prerequisite for coactivation of the estrogen-responsive pS2 gene by PRMT1. J Biol Chem 281 : 27242–27250.

13. BalintBL, SzantoA, MadiA, BauerUM, GaborP, et al. (2005) Arginine methylation provides epigenetic transcription memory for retinoid-induced differentiation in myeloid cells. Mol Cell Biol 25 : 5648–5663.

14. DaujatS, BauerUM, ShahV, TurnerB, BergerS, et al. (2002) Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr Biol 12 : 2090–2097.

15. HuangS, LittM, FelsenfeldG (2005) Methylation of histone H4 by arginine methyltransferase PRMT1 is essential in vivo for many subsequent histone modifications. Genes Dev 19 : 1885–1893.

16. JacobsonRH, LadurnerAG, KingDS, TjianR (2000) Structure and function of a human TAFII250 double bromodomain module. Science 288 : 1422–1425.

17. YadavN, LeeJ, KimJ, ShenJ, HuMC, et al. (2003) Specific protein methylation defects and gene expression perturbations in coactivator-associated arginine methyltransferase 1-deficient mice. Proc Natl Acad Sci U S A 100 : 6464–6468.

18. KimD, LeeJ, ChengD, LiJ, CarterC, et al. (2010) Enzymatic activity is required for the in vivo functions of CARM1. J Biol Chem 285 : 1147–1152.

19. WuJ, XuW (2012) Histone H3R17me2a mark recruits human RNA polymerase-associated factor 1 complex to activate transcription. Proc Natl Acad Sci U S A 109 : 5675–5680.

20. YangY, LuY, EspejoA, WuJ, XuW, et al. (2010) TDRD3 is an effector molecule for arginine-methylated histone marks. Mol Cell 40 : 1016–1023.

21. FengQ, YiP, WongJ, O'MalleyBW (2006) Signaling within a coactivator complex: methylation of SRC-3/AIB1 is a molecular switch for complex disassembly. Mol Cell Biol 26 : 7846–7857.

22. NaeemH, ChengD, ZhaoQ, UnderhillC, TiniM, et al. (2007) The activity and stability of the transcriptional coactivator p/CIP/SRC-3 are regulated by CARM1-dependent methylation. Mol Cell Biol 27 : 120–134.

23. XuW, ChenH, DuK, AsaharaH, TiniM, et al. (2001) A transcriptional switch mediated by cofactor methylation. Science 294 : 2507–2511.

24. Chevillard-BrietM, TroucheD, VandelL (2002) Control of CBP co-activating activity by arginine methylation. Embo J 21 : 5457–5466.

25. XuW, ChoH, KadamS, BanayoEM, AndersonS, et al. (2004) A methylation-mediator complex in hormone signaling. Genes Dev 18 : 144–156.

26. Torres-PadillaME, ParfittDE, KouzaridesT, Zernicka-GoetzM (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445 : 214–218.

27. WuQ, BruceAW, JedrusikA, EllisPD, AndrewsRM, et al. (2009) CARM1 is required in embryonic stem cells to maintain pluripotency and resist differentiation. Stem Cells 27 : 2637–2645.

28. DacwagCS, BedfordMT, SifS, ImbalzanoAN (2009) Distinct protein arginine methyltransferases promote ATP-dependent chromatin remodeling function at different stages of skeletal muscle differentiation. Mol Cell Biol 29 : 1909–1921.

29. El MessaoudiS, FabbrizioE, RodriguezC, ChuchanaP, FauquierL, et al. (2006) Coactivator-associated arginine methyltransferase 1 (CARM1) is a positive regulator of the Cyclin E1 gene. Proc Natl Acad Sci U S A 103 : 13351–13356.

30. MarfellaCG, ImbalzanoAN (2007) The Chd family of chromatin remodelers. Mutat Res 618 : 30–40.

31. MansfieldRE, MusselmanCA, KwanAH, OliverSS, GarskeAL, et al. (2011) Plant homeodomain (PHD) fingers of CHD4 are histone H3-binding modules with preference for unmodified H3K4 and methylated H3K9. J Biol Chem 286 : 11779–11791.

32. MusselmanCA, RamirezJ, SimsJK, MansfieldRE, OliverSS, et al. (2012) Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression. Proc Natl Acad Sci U S A 109 : 787–792.

33. BouazouneK, MitterwegerA, LangstG, ImhofA, AkhtarA, et al. (2002) The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. Embo J 21 : 2430–2440.

34. TongJK, HassigCA, SchnitzlerGR, KingstonRE, SchreiberSL (1998) Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395 : 917–921.

35. XueY, WongJ, MorenoGT, YoungMK, CoteJ, et al. (1998) NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2 : 851–861.

36. ZhangY, LeRoyG, SeeligHP, LaneWS, ReinbergD (1998) The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95 : 279–289.

37. WilliamsCJ, NaitoT, ArcoPG, SeavittJR, CashmanSM, et al. (2004) The chromatin remodeler Mi-2beta is required for CD4 expression and T cell development. Immunity 20 : 719–733.

38. MurawskaM, KunertN, van VugtJ, LangstG, KremmerE, et al. (2008) dCHD3, a novel ATP-dependent chromatin remodeler associated with sites of active transcription. Mol Cell Biol 28 : 2745–2757.

39. SaetherT, BergeT, LedsaakM, MatreV, Alm-KristiansenAH, et al. (2007) The chromatin remodeling factor Mi-2alpha acts as a novel co-activator for human c-Myb. J Biol Chem 282 : 13994–14005.

40. AllenRD3rd, BenderTP, SiuG (1999) c-Myb is essential for early T cell development. Genes Dev 13 : 1073–1078.

41. MucenskiML, McLainK, KierAB, SwerdlowSH, SchreinerCM, et al. (1991) A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 65 : 677–689.

42. KimJ, LeeJ, YadavN, WuQ, CarterC, et al. (2004) Loss of CARM1 results in hypomethylation of thymocyte cyclic AMP-regulated phosphoprotein and deregulated early T cell development. J Biol Chem 279 : 25339–25344.

43. NessSA, Kowenz-LeutzE, CasiniT, GrafT, LeutzA (1993) Myb and NF-M: combinatorial activators of myeloid genes in heterologous cell types. Genes Dev 7 : 749–759.

44. BurkO, MinkS, RingwaldM, KlempnauerKH (1993) Synergistic activation of the chicken mim-1 gene by v-myb and C/EBP transcription factors. Embo J 12 : 2027–2038.

45. NessSA, MarknellA, GrafT (1989) The v-myb oncogene product binds to and activates the promyelocyte-specific mim-1 gene. Cell 59 : 1115–1125.

46. GuccioneE, BassiC, CasadioF, MartinatoF, CesaroniM, et al. (2007) Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449 : 933–937.

47. HyllusD, SteinC, SchnabelK, SchiltzE, ImhofA, et al. (2007) PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev 21 : 3369–3380.

48. ChaykaO, KintscherJ, BraasD, KlempnauerKH (2005) v-Myb mediates cooperation of a cell-specific enhancer with the mim-1 promoter. Mol Cell Biol 25 : 499–511.

49. RamsayRG, GondaTJ (2008) MYB function in normal and cancer cells. Nat Rev Cancer 8 : 523–534.

50. BergeT, MatreV, BrendefordEM, SaetherT, LuscherB, et al. (2007) Revisiting a selection of target genes for the hematopoietic transcription factor c-Myb using chromatin immunoprecipitation and c-Myb knockdown. Blood Cells Mol Dis 39 : 278–286.

51. NakataY, ShetzlineS, SakashitaC, KalotaA, RallapalliR, et al. (2007) c-Myb contributes to G2/M cell cycle transition in human hematopoietic cells by direct regulation of cyclin B1 expression. Mol Cell Biol 27 : 2048–2058.

52. RowleyPT, Ohlsson-WilhelmBM, RudolphNS, FarleyBA, KosciolekB, et al. (1982) Hemin preferentially stimulates synthesis of alpha-globin in K562 human erythroleukemia cells. Blood 59 : 1098–1102.

53. RossonD, O'BrienTG (1995) Constitutive c-myb expression in K562 cells inhibits induced erythroid differentiation but not tetradecanoyl phorbol acetate-induced megakaryocytic differentiation. Mol Cell Biol 15 : 772–779.

54. Ramirez-CarrozziVR, NazarianAA, LiCC, GoreSL, SridharanR, ImbalzanoAN, et al. (2006) Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev 20 : 282–296.

55. SchultzDC, FriedmanJR, RauscherFJ3rd (2001) Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes Dev 15 : 428–443.

56. NaitoT, Gomez-Del ArcoP, WilliamsCJ, GeorgopoulosK (2007) Antagonistic interactions between Ikaros and the chromatin remodeler Mi-2beta determine silencer activity and Cd4 gene expression. Immunity 27 : 723–734.

57. ZhangJ, JacksonAF, NaitoT, DoseM, SeavittJ, et al. (2012) Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat Immunol 13 : 86–94.

58. Kowenz-LeutzE, PlessO, DittmarG, KnoblichM, LeutzA (2010) Crosstalk between C/EBPbeta phosphorylation, arginine methylation, and SWI/SNF/Mediator implies an indexing transcription factor code. Embo J 29 : 1105–1115.

59. WilczekC, ChaykaO, PlachetkaA, KlempnauerKH (2009) Myb-induced chromatin remodeling at a dual enhancer/promoter element involves non-coding rna transcription and is disrupted by oncogenic mutations of v-myb. J Biol Chem 284 : 35314–35324.

60. ShimonoY, MurakamiH, KawaiK, WadePA, ShimokataK, et al. (2003) Mi-2 beta associates with BRG1 and RET finger protein at the distinct regions with transcriptional activating and repressing abilities. J Biol Chem 278 : 51638–51645.

61. WatsonAA, MahajanP, MertensHD, DeeryMJ, ZhangW, et al. (2012) The PHD and Chromo Domains Regulate the ATPase Activity of the Human Chromatin Remodeler CHD4. J Mol Biol 422 : 3–17.

62. ZuberJ, ShiJ, WangE, RappaportAR, HerrmannH, et al. (2011) RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia. Nature 478 : 524–528.

63. KleinschmidtMA, StreubelG, SamansB, KrauseM, BauerUM (2008) The protein arginine methyltransferases CARM1 and PRMT1 cooperate in gene regulation. Nucleic Acids Res 36 : 3202–3213.

64. DeanA, ErardF, SchneiderAP, SchechterAN (1981) Induction of hemoglobin accumulation in human K562 cells by hemin is reversible. Science 212 : 459–461.