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Controls Gliogenesis by Regulating the Transient Expression of the Gcm/Glide Fate Determinant
The Gcm/Glide transcription factor is transiently expressed and required in the Drosophila nervous system. Threshold Gcm/Glide levels control the glial versus neuronal fate choice, and its perdurance triggers excessive gliogenesis, showing that its tight and dynamic regulation ensures the proper balance between neurons and glia. Here, we present a genetic screen for potential gcm/glide interactors and identify genes encoding chromatin factors of the Trithorax and of the Polycomb groups. These proteins maintain the heritable epigenetic state, among others, of HOX genes throughout development, but their regulatory role on transiently expressed genes remains elusive. Here we show that Polycomb negatively affects Gcm/Glide autoregulation, a positive feedback loop that allows timely accumulation of Gcm/Glide threshold levels. Such temporal fine-tuning of gene expression tightly controls gliogenesis. This work performed at the levels of individual cells reveals an undescribed mode of Polycomb action in the modulation of transiently expressed fate determinants and hence in the acquisition of specific cell identity in the nervous system.
Vyšlo v časopise: Controls Gliogenesis by Regulating the Transient Expression of the Gcm/Glide Fate Determinant. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003159
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003159Souhrn
The Gcm/Glide transcription factor is transiently expressed and required in the Drosophila nervous system. Threshold Gcm/Glide levels control the glial versus neuronal fate choice, and its perdurance triggers excessive gliogenesis, showing that its tight and dynamic regulation ensures the proper balance between neurons and glia. Here, we present a genetic screen for potential gcm/glide interactors and identify genes encoding chromatin factors of the Trithorax and of the Polycomb groups. These proteins maintain the heritable epigenetic state, among others, of HOX genes throughout development, but their regulatory role on transiently expressed genes remains elusive. Here we show that Polycomb negatively affects Gcm/Glide autoregulation, a positive feedback loop that allows timely accumulation of Gcm/Glide threshold levels. Such temporal fine-tuning of gene expression tightly controls gliogenesis. This work performed at the levels of individual cells reveals an undescribed mode of Polycomb action in the modulation of transiently expressed fate determinants and hence in the acquisition of specific cell identity in the nervous system.
Zdroje
1. HosoyaT, TakizawaK, NittaK, HottaY (1995) glial cells missing: a binary switch between neuronal and glial determination in Drosophila. Cell 82 : 1025–1036.
2. JonesBW, FetterRD, TearG, GoodmanCS (1995) glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 82 : 1013–1023.
3. VincentS, VoneschJL, GiangrandeA (1996) Glide directs glial fate commitment and cell fate switch between neurones and glia. Development 122 : 131–139.
4. Akiyama-OdaY, HosoyaT, HottaY (1998) Alteration of cell fate by ectopic expression of Drosophila glial cells missing in non-neural cells. Dev Genes Evol 208 : 578–585.
5. BernardoniR, MillerAA, GiangrandeA (1998) Glial differentiation does not require a neural ground state. Development 125 : 3189–3200.
6. FliciH, ErkosarB, KomonyiO, KaratasOF, LaneveP, et al. (2011) Gcm/Glide-dependent conversion into glia depends on neural stem cell age, but not on division, triggering a chromatin signature that is conserved in vertebrate glia. Development 138 : 4167–4178.
7. MillerAA, BernardoniR, GiangrandeA (1998) Positive autoregulation of the glial promoting factor glide/gcm. Embo J 17 : 6316–6326.
8. RagoneG, Van De BorV, SorrentinoS, KammererM, GalyA, et al. (2003) Transcriptional regulation of glial cell specification. Dev Biol 255 : 138–150.
9. De IacoR, SoustelleL, KammererM, SorrentinoS, JacquesC, et al. (2006) Huckebein-mediated autoregulation of Glide/Gcm triggers glia specification. Embo J 25 : 244–254.
10. SoustelleL, RoyN, RagoneG, GiangrandeA (2008) Control of gcm RNA stability is necessary for proper glial cell fate acquisition. Mol Cell Neurosci 37 : 657–662.
11. HoMS, ChenH, ChenM, JacquesC, GiangrandeA, et al. (2009) Gcm protein degradation suppresses proliferation of glial progenitors. Proc Natl Acad Sci U S A 106 : 6778–6783.
12. SchuettengruberB, MartinezAM, IovinoN, CavalliG (2011) Trithorax group proteins: switching genes on and keeping them active. Nat Rev Mol Cell Biol 12 : 799–814.
13. RingroseL, ParoR (2007) Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134 : 223–232.
14. SchuettengruberB, ChourroutD, VervoortM, LeblancB, CavalliG (2007) Genome regulation by polycomb and trithorax proteins. Cell 128 : 735–745.
15. SchuettengruberB, CavalliG (2009) Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136 : 3531–3542.
16. KharchenkoPV, AlekseyenkoAA, SchwartzYB, MinodaA, RiddleNC, et al. (2010) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471 : 480–485.
17. EnderleD, BeiselC, StadlerMB, GerstungM, AthriP, et al. (2011) Polycomb preferentially targets stalled promoters of coding and noncoding transcripts. Genome Res 21 : 216–226.
18. BrookesE, de SantiagoI, HebenstreitD, MorrisKJ, CarrollT, et al. (2012) Polycomb Associates Genome-wide with a Specific RNA Polymerase II Variant, and Regulates Metabolic Genes in ESCs. Cell Stem Cell 10 : 157–170.
19. ToumaJJ, WeckerleFF, ClearyMD (2012) Drosophila Polycomb complexes restrict neuroblast competence to generate motoneurons. Development 139 : 657–666.
20. Van De BorV, HeitzlerP, LegerS, PlessyC, GiangrandeA (2002) Precocious expression of the Glide/Gcm glial-promoting factor in Drosophila induces neurogenesis. Genetics 160 : 1095–1106.
21. DominguezM, CampuzanoS (1993) asense, a member of the Drosophila achaete-scute complex, is a proneural and neural differentiation gene. Embo J 12 : 2049–2060.
22. BrandM, JarmanAP, JanLY, JanYN (1993) asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. Development 119 : 1–17.
23. AltenheinB, BeckerA, BusoldC, BeckmannB, HoheiselJD, et al. (2006) Expression profiling of glial genes during Drosophila embryogenesis. Dev Biol 296 : 545–560.
24. PapoulasO, BeekSJ, MoseleySL, McCallumCM, SarteM, et al. (1998) The Drosophila trithorax group proteins BRM, ASH1 and ASH2 are subunits of distinct protein complexes. Development 125 : 3955–3966.
25. CollinsRT, FurukawaT, TaneseN, TreismanJE (1999) Osa associates with the Brahma chromatin remodeling complex and promotes the activation of some target genes. Embo J 18 : 7029–7040.
26. BadenhorstP, VoasM, RebayI, WuC (2002) Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev 16 : 3186–3198.
27. JacquesC, SoustelleL, NagyI, DieboldC, GiangrandeA (2009) A novel role of the glial fate determinant glial cells missing in hematopoiesis. Int J Dev Biol 53 : 1013–1022.
28. CzerminB, MelfiR, McCabeD, SeitzV, ImhofA, et al. (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111 : 185–196.
29. MohanM, HerzHM, SmithER, ZhangY, JacksonJ, et al. The COMPASS family of H3K4 methylases in Drosophila. Mol Cell Biol 31 : 4310–4318.
30. GrimaudC, NegreN, CavalliG (2006) From genetics to epigenetics: the tale of Polycomb group and trithorax group genes. Chromosome Res 14 : 363–375.
31. TieF, BanerjeeR, StrattonCA, Prasad-SinhaJ, StepanikV, et al. (2009) CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136 : 3131–3141.
32. KwongC, AdryanB, BellI, MeadowsL, RussellS, et al. (2008) Stability and dynamics of polycomb target sites in Drosophila development. PLoS Genet 4: e1000178 doi:10.1371/journal.pgen.1000178.
33. SchuettengruberB, GanapathiM, LeblancB, PortosoM, JaschekR, et al. (2009) Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol 7: e13 doi:10.1371/journal.pbio.1000013..
34. SchwartzYB, KahnTG, StenbergP, OhnoK, BourgonR, et al. (2010) Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet 6: e1000805 doi:10.1371/journal.pgen.1000805..
35. KammererM, GiangrandeA (2001) Glide2, a second glial promoting factor in Drosophila melanogaster. Embo J 20 : 4664–4673.
36. GindhartJGJr, KaufmanTC (1995) Identification of Polycomb and trithorax group responsive elements in the regulatory region of the Drosophila homeotic gene Sex combs reduced. Genetics 139 : 797–814.
37. KassisJA (2002) Pairing-sensitive silencing, polycomb group response elements, and transposon homing in Drosophila. Adv Genet 46 : 421–438.
38. PaladiM, TepassU (2004) Function of Rho GTPases in embryonic blood cell migration in Drosophila. J Cell Sci 117 : 6313–6326.
39. SoustelleL, TrousseF, JacquesC, CeronJ, CochardP, et al. (2007) Neurogenic role of Gcm transcription factors is conserved in chicken spinal cord. Development 134 : 625–634.
40. SoustelleL, GiangrandeA (2007) Glial differentiation and the Gcm pathway. Neuron Glia Biol 3 : 5–16.
41. Van De BorV, WaltherR, GiangrandeA (2000) Some fly sensory organs are gliogenic and require glide/gcm in a precursor that divides symmetrically and produces glial cells. Development 127 : 3735–3743.
42. BernardoniR, VivancosV, GiangrandeA (1997) glide/gcm is expressed and required in the scavenger cell lineage. Dev Biol 191 : 118–130.
43. ChotardC, LeungW, SaleckerI (2005) glial cells missing and gcm2 cell autonomously regulate both glial and neuronal development in the visual system of Drosophila. Neuron 48 : 237–251.
44. SoustelleL, GiangrandeA (2007) Novel gcm-dependent lineages in the postembryonic nervous system of Drosophila melanogaster. Dev Dyn 236 : 2101–2108.
45. AkiyamaY, HosoyaT, PooleAM, HottaY (1996) The gcm-motif: a novel DNA-binding motif conserved in Drosophila and mammals. Proc Natl Acad Sci U S A 93 : 14912–14916.
46. AnderssonER, SandbergR, LendahlU (2011) Notch signaling: simplicity in design, versatility in function. Development 138 : 3593–3612.
47. TamkunJW, DeuringR, ScottMP, KissingerM, PattatucciAM, et al. (1992) brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68 : 561–572.
48. CollinsRT, TreismanJE (2000) Osa-containing Brahma chromatin remodeling complexes are required for the repression of wingless target genes. Genes Dev 14 : 3140–3152.
49. MarendaDR, ZralyCB, DingwallAK (2004) The Drosophila Brahma (SWI/SNF) chromatin remodeling complex exhibits cell-type specific activation and repression functions. Dev Biol 267 : 279–293.
50. BreilingA, O'NeillLP, D'EliseoD, TurnerBM, OrlandoV (2004) Epigenome changes in active and inactive polycomb-group-controlled regions. EMBO Rep 5 : 976–982.
51. PappB, MullerJ (2006) Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 20 : 2041–2054.
52. DejardinJ, RappaillesA, CuvierO, GrimaudC, DecovilleM, et al. (2005) Recruitment of Drosophila Polycomb group proteins to chromatin by DSP1. Nature 434 : 533–538.
53. CabreraCV, BotasJ, Garcia-BellidoA (1985) Distribution of Ultrabithorax proteins in mutants of Drosophila bithorax complex and its transregulatory genes. Nature 318 : 569.
54. BusturiaA, LloydA, BejaranoF, ZavortinkM, XinH, et al. (2001) The MCP silencer of the Drosophila Abd-B gene requires both Pleiohomeotic and GAGA factor for the maintenance of repression. Development 128 : 2163–2173.
55. BrackenAP, HelinK (2009) Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev Cancer 9 : 773–784.
56. PereiraJD, SansomSN, SmithJ, DobeneckerMW, TarakhovskyA, et al. (2010) Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc Natl Acad Sci U S A 107 : 15957–15962.
57. HirabayashiY, SuzkiN, TsuboiM, EndoTA, ToyodaT, et al. (2009) Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 63 : 600–613.
58. LiuJ, CasacciaP (2010) Epigenetic regulation of oligodendrocyte identity. Trends Neurosci 33 : 193–201.
59. LavrovS, DejardinJ, CavalliG (2004) Combined immunostaining and FISH analysis of polytene chromosomes. Methods Mol Biol 247 : 289–303.
60. SchneiderI (1972) Cell lines derived from late embryonic stages of Drosophila melanogaster. J Embryol Exp Morphol 27 : 353–365.
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