Histone Methylation Restrains the Expression of Subtype-Specific Genes during Terminal Neuronal Differentiation in

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Although epigenetic control of stem cell fate choice is well established, little is known about epigenetic regulation of terminal neuronal differentiation. We found that some differences among the subtypes of Caenorhabditis elegans VC neurons, particularly the expression of the transcription factor gene unc-4, require histone modification, most likely H3K9 methylation. An EGF signal from the vulva alleviated the epigenetic repression of unc-4 in vulval VC neurons but not the more distant nonvulval VC cells, which kept unc-4 silenced. Loss of the H3K9 methyltransferase MET-2 or H3K9me2/3 binding proteins HPL-2 and LIN-61 or a novel chromodomain protein CEC-3 caused ectopic unc-4 expression in all VC neurons. Downstream of the EGF signaling in vulval VC neurons, the transcription factor LIN-11 and histone demethylases removed the suppressive histone marks and derepressed unc-4. Behaviorally, expression of UNC-4 in all the VC neurons caused an imbalance in the egg-laying circuit. Thus, epigenetic mechanisms help establish subtype-specific gene expression, which are needed for optimal activity of a neural circuit.

Vyšlo v časopise: Histone Methylation Restrains the Expression of Subtype-Specific Genes during Terminal Neuronal Differentiation in. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1004017
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004017

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Zdroje

1. HsiehJ, GageFH (2004) Epigenetic control of neural stem cell fate. Curr Opin Genet Dev 14: 461–469.

2. BoyerLA, PlathK, ZeitlingerJ, BrambrinkT, MedeirosLA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349–353.

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

4. Roman-TruferoM, Mendez-GomezHR, PerezC, HijikataA, FujimuraY, et al. (2009) Maintenance of undifferentiated state and self-renewal of embryonic neural stem cells by Polycomb protein Ring1B. Stem Cells 27: 1559–1570.

5. ZhangM, ChungSH, Fang-YenC, CraigC, KerrRA, et al. (2008) A self-regulating feed-forward circuit controlling C. elegans egg-laying behavior. Curr Biol 18: 1445–1455.

6. BanyIA, DongMQ, KoelleMR (2003) Genetic and cellular basis for acetylcholine inhibition of Caenorhabditis elegans egg-laying behavior. J Neurosci 23: 8060–8069.

7. Von StetinaSE, FoxRM, WatkinsKL, StarichTA, ShawJE, et al. (2007) UNC-4 represses CEH-12/HB9 to specify synaptic inputs to VA motor neurons in C. elegans. Genes Dev 21: 332–346.

8. PoyurovskyMV, JacqX, MaC, Karni-SchmidtO, ParkerPJ, et al. (2003) Nucleotide binding by the Mdm2 RING domain facilitates Arf-independent Mdm2 nucleolar localization. Mol Cell 12: 875–887.

9. FaberPW, VoisineC, KingDC, BatesEA, HartAC (2002) Glutamine/proline-rich PQE-1 proteins protect Caenorhabditis elegans neurons from huntingtin polyglutamine neurotoxicity. Proc Natl Acad Sci U S A 99: 17131–17136.

10. ZahnTR, MacmorrisMA, DongW, DayR, HuttonJC (2001) IDA-1, a Caenorhabditis elegans homolog of the diabetic autoantigens IA-2 and phogrin, is expressed in peptidergic neurons in the worm. J Comp Neurol 429: 127–143.

11. WhiteJG, SouthgateE, ThomsonJN, BrennerS (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314: 1–340.

12. EissenbergJC (2012) Structural biology of the chromodomain: form and function. Gene 496: 69–78.

13. AndersenEC, HorvitzHR (2007) Two C. elegans histone methyltransferases repress lin-3 EGF transcription to inhibit vulval development. Development 134: 2991–2999.

14. LamelzaP, BhallaN (2012) Histone methyltransferases MES-4 and MET-1 promote meiotic checkpoint activation in Caenorhabditis elegans. PLoS Genet 8: e1003089.

15. CloughE, MoonW, WangS, SmithK, HazelriggT (2007) Histone methylation is required for oogenesis in Drosophila. Development 134: 157–165.

16. SchultzDC, AyyanathanK, NegorevD, MaulGG, RauscherFJ3rd (2002) SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 16: 919–932.

17. TowbinBD, Gonzalez-AguileraC, SackR, GaidatzisD, KalckV, et al. (2012) Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150: 934–947.

18. RandoOJ (2007) Global patterns of histone modifications. Curr Opin Genet Dev 17: 94–99.

19. RechtsteinerA, ErcanS, TakasakiT, PhippenTM, EgelhoferTA, et al. (2010) The histone H3K36 methyltransferase MES-4 acts epigenetically to transmit the memory of germline gene expression to progeny. PLoS Genet 6: e1001091.

20. SchottS, CousthamV, SimonetT, BedetC, PalladinoF (2006) Unique and redundant functions of C. elegans HP1 proteins in post-embryonic development. Dev Biol 298: 176–187.

21. StudenckaM, WesolowskiR, OpitzL, Salinas-RiesterG, WisniewskiJR, et al. (2012) Transcriptional repression of Hox genes by C. elegans HP1/HPL and H1/HIS-24. PLoS Genet 8: e1002940.

22. StudenckaM, KonzerA, MoneronG, WenzelD, OpitzL, et al. (2012) Novel roles of Caenorhabditis elegans heterochromatin protein HP1 and linker histone in the regulation of innate immune gene expression. Mol Cell Biol 32: 251–265.

23. YamadaK, TsuchiyaJ, IinoY (2012) Mutations in the pqe-1 gene enhance transgene expression in Caenorhabditis elegans. G3 (Bethesda) 2: 741–751.

24. RajA, van den BogaardP, RifkinSA, van OudenaardenA, TyagiS (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5: 877–879.

25. CouteauF, GuerryF, MullerF, PalladinoF (2002) A heterochromatin protein 1 homologue in Caenorhabditis elegans acts in germline and vulval development. EMBO Rep 3: 235–241.

26. CuiM, ChenJ, MyersTR, HwangBJ, SternbergPW, et al. (2006) SynMuv genes redundantly inhibit lin-3/EGF expression to prevent inappropriate vulval induction in C. elegans. Dev Cell 10: 667–672.

27. CeolCJ, HorvitzHR (2001) dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development. Mol Cell 7: 461–473.

28. CousthamV, BedetC, MonierK, SchottS, KaraliM, et al. (2006) The C. elegans HP1 homologue HPL-2 and the LIN-13 zinc finger protein form a complex implicated in vulval development. Dev Biol 297: 308–322.

29. HarrisonMM, LuX, HorvitzHR (2007) LIN-61, one of two Caenorhabditis elegans malignant-brain-tumor-repeat-containing proteins, acts with the DRM and NuRD-like protein complexes in vulval development but not in certain other biological processes. Genetics 176: 255–271.

30. Koester-EiserfunkeN, FischleW (2011) H3K9me2/3 binding of the MBT domain protein LIN-61 is essential for Caenorhabditis elegans vulva development. PLoS Genet 7: e1002017.

31. CeolCJ, StegmeierF, HarrisonMM, HorvitzHR (2006) Identification and classification of genes that act antagonistically to let-60 Ras signaling in Caenorhabditis elegans vulval development. Genetics 173: 709–726.

32. BatesEA, VictorM, JonesAK, ShiY, HartAC (2006) Differential contributions of Caenorhabditis elegans histone deacetylases to huntingtin polyglutamine toxicity. J Neurosci 26: 2830–2838.

33. LiC, ChalfieM (1990) Organogenesis in C. elegans: positioning of neurons and muscles in the egg-laying system. Neuron 4: 681–695.

34. SundaramMV (2006) RTK/Ras/MAPK signaling. WormBook 1–19.

35. ClarkSG, SternMJ, HorvitzHR (1992) C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature 356: 340–344.

36. WuY, HanM, GuanKL (1995) MEK-2, a Caenorhabditis elegans MAP kinase kinase, functions in Ras-mediated vulval induction and other developmental events. Genes Dev 9: 742–755.

37. KatzWS, HillRJ, ClandininTR, SternbergPW (1995) Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates. Cell 82: 297–307.

38. ChangC, NewmanAP, SternbergPW (1999) Reciprocal EGF signaling back to the uterus from the induced C. elegans vulva coordinates morphogenesis of epithelia. Curr Biol 9: 237–246.

39. GreenwaldIS, SternbergPW, HorvitzHR (1983) The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell 34: 435–444.

40. BeitelGJ, TuckS, GreenwaldI, HorvitzHR (1995) The Caenorhabditis elegans gene lin-1 encodes an ETS-domain protein and defines a branch of the vulval induction pathway. Genes Dev 9: 3149–3162.

41. FreydG, KimSK, HorvitzHR (1990) Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 344: 876–879.

42. GuptaBP, WangM, SternbergPW (2003) The C. elegans LIM homeobox gene lin-11 specifies multiple cell fates during vulval development. Development 130: 2589–2601.

43. ShiY, LanF, MatsonC, MulliganP, WhetstineJR, et al. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941–953.

44. MetzgerE, WissmannM, YinN, MullerJM, SchneiderR, et al. (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437: 436–439.

45. KatzDJ, EdwardsTM, ReinkeV, KellyWG (2009) A C. elegans LSD1 demethylase contributes to germline immortality by reprogramming epigenetic memory. Cell 137: 308–320.

46. ChenZ, ZangJ, WhetstineJ, HongX, DavrazouF, et al. (2006) Structural insights into histone demethylation by JMJD2 family members. Cell 125: 691–702.

47. WhetstineJR, NottkeA, LanF, HuarteM, SmolikovS, et al. (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125: 467–481.

48. LuY, ChangQ, ZhangY, BeezholdK, RojanasakulY, et al. (2009) Lung cancer-associated JmjC domain protein mdig suppresses formation of tri-methyl lysine 9 of histone H3. Cell Cycle 8: 2101–2109.

49. LickteigKM, DuerrJS, FrisbyDL, HallDH, RandJB, et al. (2001) Regulation of neurotransmitter vesicles by the homeodomain protein UNC-4 and its transcriptional corepressor UNC-37/groucho in Caenorhabditis elegans cholinergic motor neurons. J Neurosci 21: 2001–2014.

50. SzeJY, VictorM, LoerC, ShiY, RuvkunG (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560–564.

51. RingstadN, HorvitzHR (2008) FMRFamide neuropeptides and acetylcholine synergistically inhibit egg-laying by C. elegans. Nat Neurosci 11: 1168–1176.

52. AbhyankarMM, UrekarC, ReddiPP (2007) A novel CpG-free vertebrate insulator silences the testis-specific SP-10 gene in somatic tissues: role for TDP-43 in insulator function. J Biol Chem 282: 36143–36154.

53. FuentealbaRA, UdanM, BellS, WegorzewskaI, ShaoJ, et al. (2010) Interaction with polyglutamine aggregates reveals a Q/N-rich domain in TDP-43. J Biol Chem 285: 26304–26314.

54. BallasN, GrunseichC, LuDD, SpehJC, MandelG (2005) REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121: 645–657.

55. SinghSK, KagalwalaMN, Parker-ThornburgJ, AdamsH, MajumderS (2008) REST maintains self-renewal and pluripotency of embryonic stem cells. Nature 453: 223–227.

56. HsiehJ, NakashimaK, KuwabaraT, MejiaE, GageFH (2004) Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 101: 16659–16664.

57. BilodeauS, KageyMH, FramptonGM, RahlPB, YoungRA (2009) SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev 23: 2484–2489.

58. KahlP, GullottiL, HeukampLC, WolfS, FriedrichsN, et al. (2006) Androgen receptor coactivators lysine-specific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence. Cancer Res 66: 11341–11347.

59. MullerJM, IseleU, MetzgerE, RempelA, MoserM, et al. (2000) FHL2, a novel tissue-specific coactivator of the androgen receptor. EMBO J 19: 359–369.

60. GarrigaG, DesaiC, HorvitzHR (1993) Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans. Development 117: 1071–1087.

61. LingBM, BharathyN, ChungTK, KokWK, LiS, et al. (2012) Lysine methyltransferase G9a methylates the transcription factor MyoD and regulates skeletal muscle differentiation. Proc Natl Acad Sci U S A 109: 841–846.

62. HerzogM, JosseauxE, DedeurwaerderS, CalonneE, VolkmarM, et al. (2012) The histone demethylase Kdm3a is essential to progression through differentiation. Nucleic Acids Res 40: 7219–7232.

63. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.

64. SarinS, PrabhuS, O'MearaMM, Pe'erI, HobertO (2008) Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nat Methods 5: 865–867.

65. BigelowH, DoitsidouM, SarinS, HobertO (2009) MAQGene: software to facilitate C. elegans mutant genome sequence analysis. Nat Methods 6: 549.

66. BargmannCI, AveryL (1995) Laser killing of cells in Caenorhabditis elegans. Methods Cell Biol 48: 225–250.

67. KoelleMR, HorvitzHR (1996) EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins. Cell 84: 115–125.