USF1 and hSET1A Mediated Epigenetic Modifications Regulate Lineage Differentiation and Transcription

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The interplay between polycomb and trithorax complexes has been implicated in embryonic stem cell (ESC) self-renewal and differentiation. It has been shown recently that WRD5 and Dpy-30, specific components of the SET1/MLL protein complexes, play important roles during ESC self-renewal and differentiation of neural lineages. However, not much is known about how and where specific trithorax complexes are targeted to genes involved in self-renewal or lineage-specification. Here, we report that the recruitment of the hSET1A histone H3K4 methyltransferase (HMT) complex by transcription factor USF1 is required for mesoderm specification and lineage differentiation. In undifferentiated ESCs, USF1 maintains hematopoietic stem/progenitor cell (HS/PC) associated bivalent chromatin domains and differentiation potential. Furthermore, USF1 directed recruitment of the hSET1A complex to the HoxB4 promoter governs the transcriptional activation of HoxB4 gene and regulates the formation of early hematopoietic cell populations. Disruption of USF or hSET1A function by overexpression of a dominant-negative AUSF1 mutant or by RNA-interference-mediated knockdown, respectively, led to reduced expression of mesoderm markers and inhibition of lineage differentiation. We show that USF1 and hSET1A together regulate H3K4me3 modifications and transcription preinitiation complex assembly at the hematopoietic-associated HoxB4 gene during differentiation. Finally, ectopic expression of USF1 in ESCs promotes mesoderm differentiation and enforces the endothelial-to-hematopoietic transition by inducing hematopoietic-associated transcription factors, HoxB4 and TAL1. Taken together, our findings reveal that the guided-recruitment of the hSET1A histone methyltransferase complex and its H3K4 methyltransferase activity by transcription regulator USF1 safeguards hematopoietic transcription programs and enhances mesoderm/hematopoietic differentiation.

Vyšlo v časopise: USF1 and hSET1A Mediated Epigenetic Modifications Regulate Lineage Differentiation and Transcription. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003524
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003524

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Zdroje

1. AzuaraV, PerryP, SauerS, SpivakovM, JorgensenHF, et al. (2006) Chromatin signatures of pluripotent cell lines. Nature cell biology 8: 532–538.

2. ChristophersenNS, HelinK (2010) Epigenetic control of embryonic stem cell fate. The Journal of experimental medicine 207: 2287–2295.

3. BernsteinBE, MikkelsenTS, XieX, KamalM, HuebertDJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315–326.

4. PanG, TianS, NieJ, YangC, RuottiV, et al. (2007) Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell stem cell 1: 299–312.

5. ZhaoXD, HanX, ChewJL, LiuJ, ChiuKP, et al. (2007) Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell stem cell 1: 286–298.

6. SharovAA, KoMS (2007) Human ES cell profiling broadens the reach of bivalent domains. Cell stem cell 1: 237–238.

7. LeeTI, JennerRG, BoyerLA, GuentherMG, LevineSS, et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301–313.

8. ShenX, LiuY, HsuYJ, FujiwaraY, KimJ, et al. (2008) EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Molecular cell 32: 491–502.

9. ShenX, KimW, FujiwaraY, SimonMD, LiuY, et al. (2009) Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139: 1303–1314.

10. CuiK, ZangC, RohTY, SchonesDE, ChildsRW, et al. (2009) Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell stem cell 4: 80–93.

11. AngYS, TsaiSY, LeeDF, MonkJ, SuJ, et al. (2011) Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145: 183–197.

12. JiangH, ShuklaA, WangX, ChenWY, BernsteinBE, et al. (2011) Role for Dpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains. Cell 144: 513–525.

13. WysockaJ, SwigutT, MilneTA, DouY, ZhangX, et al. (2005) WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121: 859–872.

14. DouY, MilneTA, RuthenburgAJ, LeeS, LeeJW, et al. (2006) Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nature structural & molecular biology 13: 713–719.

15. StewardMM, LeeJS, O'DonovanA, WyattM, BernsteinBE, et al. (2006) Molecular regulation of H3K4 trimethylation by ASH2L, a shared subunit of MLL complexes. Nature structural & molecular biology 13: 852–854.

16. ErnstP, FisherJK, AveryW, WadeS, FoyD, et al. (2004) Definitive hematopoiesis requires the mixed-lineage leukemia gene. Developmental cell 6: 437–443.

17. WangP, LinC, SmithER, GuoH, SandersonBW, et al. (2009) Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Molecular and cellular biology 29: 6074–6085.

18. LeeJ, SahaPK, YangQH, LeeS, ParkJY, et al. (2008) Targeted inactivation of MLL3 histone H3-Lys-4 methyltransferase activity in the mouse reveals vital roles for MLL3 in adipogenesis. Proceedings of the National Academy of Sciences of the United States of America 105: 19229–19234.

19. SoshnikovaN, DubouleD (2009) Epigenetic temporal control of mouse Hox genes in vivo. Science 324: 1320–1323.

20. PilatS, CarottaS, SchiedlmeierB, KaminoK, MairhoferA, et al. (2005) HOXB4 enforces equivalent fates of ES-cell-derived and adult hematopoietic cells. Proceedings of the National Academy of Sciences of the United States of America 102: 12101–12106.

21. SchiedlmeierB, SantosAC, RibeiroA, MoncautN, LesinskiD, et al. (2007) HOXB4's road map to stem cell expansion. Proceedings of the National Academy of Sciences of the United States of America 104: 16952–16957.

22. WangY, YatesF, NaveirasO, ErnstP, DaleyGQ (2005) Embryonic stem cell-derived hematopoietic stem cells. Proceedings of the National Academy of Sciences of the United States of America 102: 19081–19086.

23. SauvageauG, ThorsteinsdottirU, EavesCJ, LawrenceHJ, LargmanC, et al. (1995) Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes & development 9: 1753–1765.

24. AntonchukJ, SauvageauG, HumphriesRK (2002) HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell 109: 39–45.

25. KybaM, PerlingeiroRC, DaleyGQ (2002) HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 109: 29–37.

26. LiuHC, ShihLY, May ChenMJ, WangCC, YehTC, et al. (2011) Expression of HOXB genes is significantly different in acute myeloid leukemia with a partial tandem duplication of MLL vs. a MLL translocation: a cross-laboratory study. Cancer genetics 204: 252–259.

27. GiannolaDM, ShlomchikWD, JegathesanM, LiebowitzD, AbramsCS, et al. (2000) Hematopoietic expression of HOXB4 is regulated in normal and leukemic stem cells through transcriptional activation of the HOXB4 promoter by upstream stimulating factor (USF)-1 and USF-2. The Journal of experimental medicine 192: 1479–1490.

28. KiritoK, FoxN, KaushanskyK (2003) Thrombopoietin stimulates Hoxb4 expression: an explanation for the favorable effects of TPO on hematopoietic stem cells. Blood 102: 3172–3178.

29. ZhuJ, ZhangY, JoeGJ, PompettiR, EmersonSG (2005) NF-Ya activates multiple hematopoietic stem cell (HSC) regulatory genes and promotes HSC self-renewal. Proceedings of the National Academy of Sciences of the United States of America 102: 11728–11733.

30. ZhuJ, GiannolaDM, ZhangY, RiveraAJ, EmersonSG (2003) NF-Y cooperates with USF1/2 to induce the hematopoietic expression of HOXB4. Blood 102: 2420–2427.

31. LiX, WangS, LiY, DengC, SteinerLA, et al. (2011) Chromatin boundaries require functional collaboration between the hSET1 and NURF complexes. Blood 118: 1386–1394.

32. LiX, HuX, PatelB, ZhouZ, LiangS, et al. (2010) H4R3 methylation facilitates beta-globin transcription by regulating histone acetyltransferase binding and H3 acetylation. Blood 115: 2028–2037.

33. ClouaireT, WebbS, SkeneP, IllingworthR, KerrA, et al. (2012) Cfp1 integrates both CpG content and gene activity for accurate H3K4me3 deposition in embryonic stem cells. Genes & development 26: 1714–1728.

34. LiangSY, MoghimiB, Crusselle-DavisVJ, LinIJ, RosenbergMH, et al. (2009) Defective erythropoiesis in transgenic mice expressing dominant-negative upstream stimulatory factor. Molecular and cellular biology 29: 5900–5910.

35. McKinney-FreemanSL, NaveirasO, YatesF, LoewerS, PhilitasM, et al. (2009) Surface antigen phenotypes of hematopoietic stem cells from embryos and murine embryonic stem cells. Blood 114: 268–278.

36. OshimaM, EndohM, EndoTA, ToyodaT, Nakajima-TakagiY, et al. (2011) Genome-wide analysis of target genes regulated by HoxB4 in hematopoietic stem and progenitor cells developing from embryonic stem cells. Blood 117: e142–150.

37. LancrinC, SroczynskaP, StephensonC, AllenT, KouskoffV, et al. (2009) The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 457: 892–895.

38. BeeT, SwiersG, MuroiS, PoznerA, NottinghamW, et al. (2010) Nonredundant roles for Runx1 alternative promoters reflect their activity at discrete stages of developmental hematopoiesis. Blood 115: 3042–3050.

39. OrkinSH, ZonLI (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132: 631–644.

40. ChoiK, KennedyM, KazarovA, PapadimitriouJC, KellerG (1998) A common precursor for hematopoietic and endothelial cells. Development 125: 725–732.

41. LengerkeC, SchmittS, BowmanTV, JangIH, Maouche-ChretienL, et al. (2008) BMP and Wnt specify hematopoietic fate by activation of the Cdx-Hox pathway. Cell stem cell 2: 72–82.

42. MurryCE, KellerG (2008) Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132: 661–680.

43. IacovinoM, ChongD, SzatmariI, HartweckL, RuxD, et al. (2011) HoxA3 is an apical regulator of haemogenic endothelium. Nature cell biology 13: 72–78.

44. KinderSJ, TsangTE, QuinlanGA, HadjantonakisAK, NagyA, et al. (1999) The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development 126: 4691–4701.

45. FehlingHJ, LacaudG, KuboA, KennedyM, RobertsonS, et al. (2003) Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130: 4217–4227.

46. HuangS, LiX, YusufzaiTM, QiuY, FelsenfeldG (2007) USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Molecular and cellular biology 27: 7991–8002.

47. van IngenH, van SchaikFM, WienkH, BalleringJ, RehmannH, et al. (2008) Structural insight into the recognition of the H3K4me3 mark by the TFIID subunit TAF3. Structure 16: 1245–1256.

48. LeeJH, TateCM, YouJS, SkalnikDG (2007) Identification and characterization of the human Set1B histone H3-Lys4 methyltransferase complex. J Biol Chem 282: 13419–13428.

49. LiuZ, ScannellDR, EisenMB, TjianR (2011) Control of embryonic stem cell lineage commitment by core promoter factor, TAF3. Cell 146: 720–731.

50. YokoyamaA, WangZ, WysockaJ, SanyalM, AufieroDJ, et al. (2004) Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 24: 5639–5649.

51. ChoYW, HongT, HongS, GuoH, YuH, et al. (2007) PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J Biol Chem 282: 20395–20406.

52. WestAG, HuangS, GasznerM, LittMD, FelsenfeldG (2004) Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Molecular cell 16: 453–463.

53. BrunAC, BjornssonJM, MagnussonM, LarssonN, LeveenP, et al. (2004) Hoxb4-deficient mice undergo normal hematopoietic development but exhibit a mild proliferation defect in hematopoietic stem cells. Blood 103: 4126–4133.

54. BjornssonJM, LarssonN, BrunAC, MagnussonM, AnderssonE, et al. (2003) Reduced proliferative capacity of hematopoietic stem cells deficient in Hoxb3 and Hoxb4. Molecular and cellular biology 23: 3872–3883.

55. MagnussonM, BrunAC, LawrenceHJ, KarlssonS (2007) Hoxa9/hoxb3/hoxb4 compound null mice display severe hematopoietic defects. Experimental hematology 35: 1421–1428.

56. ShenJ, QuCK (2008) In vitro hematopoietic differentiation of murine embryonic stem cells. Methods in molecular biology 430: 103–118.

57. BarskiA, CuddapahS, CuiK, RohTY, SchonesDE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823–837.