The COP9 Signalosome Converts Temporal Hormone Signaling to Spatial Restriction on Neural Competence

English version České info

A critical step in building a functional nervous system is to generate neurons at the appropriate locations. Neural competence is acquired at the precursor stage with the expression of specific transcription factors. One such critical factor is Senseless (Sens), as precursors lacking Sens fail to develop to neurons. Here we describe the critical role of protein complex COP9 signalosome (CSN) that regulates Sens expression by integrating temporal and spatial information. This was studied in developing Drosophila wing tissues, in which the anterior wing margin develops neuron-innervated bristles, while the posterior wing margin develops non-innervated bristles. The CSN complex is required for the anterior-posterior difference in spatial patterning of neuron formation, and posterior cells lacking CSN develop innervated bristles like anterior cells. CSN accomplishes this by transforming the temporal hormonal ecdysone signaling from activation to repression of downstream target BR-Z1. As BR-Z1 itself is a transcription activator, repression of BR-Z1 in turn leads to repression of Sens in posterior wing margin, eventually terminating the neural competence. Repression of BR-Z1 expression requires the interaction between the CSN complex and the ecdysone receptors. Our results suggest a novel CSN-mediated regulation that converts temporal hormone signaling to the patterning of neurons at the right place.

Vyšlo v časopise: The COP9 Signalosome Converts Temporal Hormone Signaling to Spatial Restriction on Neural Competence. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004760
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004760

Souhrn

Zdroje

1. RomaniS, CampuzanoS, MacagnoER, ModolellJ (1989) Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development. Genes Dev 3: 997–1007.

2. CubasP, de CelisJF, CampuzanoS, ModolellJ (1991) Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev 5: 996–1008.

3. NoloR, AbbottLA, BellenHJ (2000) Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102: 349–362.

4. Jafar-NejadH, TienAC, AcarM, BellenHJ (2006) Senseless and Daughterless confer neuronal identity to epithelial cells in the Drosophila wing margin. Development 133: 1683–1692.

5. SchubigerM, CarreC, AntoniewskiC, TrumanJW (2005) Ligand-dependent de-repression via EcR/USP acts as a gate to coordinate the differentiation of sensory neurons in the Drosophila wing. Development 132: 5239–5248.

6. RiddifordLM (1993) Hormone receptors and the regulation of insect metamorphosis. Receptor 3: 203–209.

7. HuetF, RuizC, RichardsG (1995) Sequential gene activation by ecdysone in Drosophila melanogaster: the hierarchical equivalence of early and early late genes. Development 121: 1195–1204.

8. ThummelCS (1995) From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell 83: 871–877.

9. ThummelCS (1996) Flies on steroids–Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet 12: 306–310.

10. ThummelCS (2001) Molecular mechanisms of developmental timing in C. elegans and Drosophila. Dev Cell 1: 453–465.

11. YaoTP, FormanBM, JiangZ, CherbasL, ChenJD, et al. (1993) Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366: 476–479.

12. King-JonesK, ThummelCS (2005) Nuclear receptors–a perspective from Drosophila. Nat Rev Genet 6: 311–323.

13. DiBelloPR, WithersDA, BayerCA, FristromJW, GuildGM (1991) The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics 129: 385–397.

14. BayerCA, HolleyB, FristromJW (1996) A switch in broad-complex zinc-finger isoform expression is regulated posttranscriptionally during the metamorphosis of Drosophila imaginal discs. Dev Biol 177: 1–14.

15. BelyaevaES, VlassovaIE, BiyashevaZM, KakpakovVT, RichardsG, et al. (1981) Cytogenetic analysis of the 2B3-4-2B11 region of the X chromosome of Drosophila melanogaster. II. Changes in 20-OH ecdysone puffing caused by genetic defects of puff 2B5. Chromosoma 84: 207–219.

16. KarimFD, GuildGM, ThummelCS (1993) The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development 118: 977–988.

17. KissI, BenczeG, FodorG, SzabadJ, FristromJW (1976) Prepupal larval mosaics in Drosophila melanogaster. Nature 262: 136–138.

18. BelyaevaES, AizenzonMG, SemeshinVF, KissII, KoczkaK, et al. (1980) Cytogenetic analysis of the 2B3-4–2B11 region of the X-chromosome of Drosophila melanogaster. I. Cytology of the region and mutant complementation groups. Chromosoma 81: 281–306.

19. ZhouX, RiddifordLM (2002) Broad specifies pupal development and mediates the ‘status quo’ action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development 129: 2259–2269.

20. WeiN, DengXW (1992) COP9: a new genetic locus involved in light-regulated development and gene expression in arabidopsis. Plant Cell 4: 1507–1518.

21. WeiN, ChamovitzDA, DengXW (1994) Arabidopsis COP9 is a component of a novel signaling complex mediating light control of development. Cell 78: 117–124.

22. ChamovitzDA, WeiN, OsterlundMT, von ArnimAG, StaubJM, et al. (1996) The COP9 complex, a novel multisubunit nuclear regulator involved in light control of a plant developmental switch. Cell 86: 115–121.

23. WeiN, DengXW (2003) The COP9 signalosome. Annu Rev Cell Dev Biol 19: 261–286.

24. WeiN, SerinoG, DengXW (2008) The COP9 signalosome: more than a protease. Trends Biochem Sci 33: 592–600.

25. LyapinaS, CopeG, ShevchenkoA, SerinoG, TsugeT, et al. (2001) Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292: 1382–1385.

26. WuJT, LinHC, HuYC, ChienCT (2005) Neddylation and deneddylation regulate Cul1 and Cul3 protein accumulation. Nat Cell Biol 7: 1014–1020.

27. WuJT, ChanYR, ChienCT (2006) Protection of cullin-RING E3 ligases by CSN-UBP12. Trends Cell Biol 16: 362–369.

28. Bech-OtschirD, KraftR, HuangX, HenkleinP, KapelariB, et al. (2001) COP9 signalosome-specific phosphorylation targets p53 to degradation by the ubiquitin system. EMBO J 20: 1630–1639.

29. UhleS, MedaliaO, WaldronR, DumdeyR, HenkleinP, et al. (2003) Protein kinase CK2 and protein kinase D are associated with the COP9 signalosome. EMBO J 22: 1302–1312.

30. WeeS, GeyerRK, TodaT, WolfDA (2005) CSN facilitates Cullin-RING ubiquitin ligase function by counteracting autocatalytic adapter instability. Nat Cell Biol 7: 387–391.

31. OronE, TullerT, LiL, RozovskyN, YekutieliD, et al. (2007) Genomic analysis of COP9 signalosome function in Drosophila melanogaster reveals a role in temporal regulation of gene expression. Mol Syst Biol 3: 108.

32. OronE, MannervikM, RencusS, Harari-SteinbergO, Neuman-SilberbergS, et al. (2002) COP9 signalosome subunits 4 and 5 regulate multiple pleiotropic pathways in Drosophila melanogaster. Development 129: 4399–4409.

33. DoronkinS, DjagaevaI, BeckendorfSK (2003) The COP9 signalosome promotes degradation of Cyclin E during early Drosophila oogenesis. Dev Cell 4: 699–710.

34. KnowlesA, KohK, WuJT, ChienCT, ChamovitzDA, et al. (2009) The COP9 signalosome is required for light-dependent timeless degradation and Drosophila clock resetting. J Neurosci 29: 1152–1162.

35. DjagaevaI, DoronkinS (2009) Dual regulation of dendritic morphogenesis in Drosophila by the COP9 signalosome. PLoS One 4: e7577.

36. DjagaevaI, DoronkinS (2009) COP9 limits dendritic branching via Cullin3-dependent degradation of the actin-crosslinking BTB-domain protein Kelch. PLoS One 4: e7598.

37. WuJT, LinWH, ChenWY, HuangYC, TangCY, et al. (2011) CSN-mediated deneddylation differentially modulates Ci(155) proteolysis to promote Hedgehog signalling responses. Nat Commun 2: 182.

38. Mummery-WidmerJL, YamazakiM, StoegerT, NovatchkovaM, BhaleraoS, et al. (2009) Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. Nature 458: 987–992.

39. HartensteinV, PosakonyJW (1989) Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107: 389–405.

40. RhyuMS, JanLY, JanYN (1994) Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76: 477–491.

41. PiH, WuHJ, ChienCT (2001) A dual function of phyllopod in Drosophila external sensory organ development: cell fate specification of sensory organ precursor and its progeny. Development 128: 2699–2710.

42. PickupAT, LamkaML, SunQ, YipML, LipshitzHD (2002) Control of photoreceptor cell morphology, planar polarity and epithelial integrity during Drosophila eye development. Development 129: 2247–2258.

43. ManningL, DoeCQ (1999) Prospero distinguishes sibling cell fate without asymmetric localization in the Drosophila adult external sense organ lineage. Development 126: 2063–2071.

44. RobinowS, WhiteK (1988) The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev Biol 126: 294–303.

45. CousoJP, BishopSA, Martinez AriasA (1994) The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development 120: 621–636.

46. BayerCA, von KalmL, FristromJW (1997) Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev Biol 187: 267–282.

47. MugatB, BroduV, Kejzlarova-LepesantJ, AntoniewskiC, BayerCA, et al. (2000) Dynamic expression of broad-complex isoforms mediates temporal control of an ecdysteroid target gene at the onset of Drosophila metamorphosis. Dev Biol 227: 104–117.

48. EmeryIF, BedianV, GuildGM (1994) Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis. Development 120: 3275–3287.

49. CherbasL, HuX, ZhimulevI, BelyaevaE, CherbasP (2003) EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130: 271–284.

50. SchubigerM, TrumanJW (2000) The RXR ortholog USP suppresses early metamorphic processes in Drosophila in the absence of ecdysteroids. Development 127: 1151–1159.

51. KoelleMR, TalbotWS, SegravesWA, BenderMT, CherbasP, et al. (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67: 59–77.

52. PintardL, KurzT, GlaserS, WillisJH, PeterM, et al. (2003) Neddylation and deneddylation of CUL-3 is required to target MEI-1/Katanin for degradation at the meiosis-to-mitosis transition in C. elegans. Curr Biol 13: 911–921.

53. RovaniMK, BrachmannCB, RamsayG, KatzenAL (2012) The dREAM/Myb-MuvB complex and Grim are key regulators of the programmed death of neural precursor cells at the Drosophila posterior wing margin. Dev Biol 372: 88–102.

54. OuCY, LinYF, ChenYJ, ChienCT (2002) Distinct protein degradation mechanisms mediated by Cul1 and Cul3 controlling Ci stability in Drosophila eye development. Genes Dev 16: 2403–2414.

55. WuK, ChenA, PanZQ (2000) Conjugation of Nedd8 to CUL1 enhances the ability of the ROC1-CUL1 complex to promote ubiquitin polymerization. J Biol Chem 275: 32317–32324.

56. ReadMA, BrownellJE, GladyshevaTB, HotteletM, ParentLA, et al. (2000) Nedd8 modification of cul-1 activates SCF(beta(TrCP))-dependent ubiquitination of IkappaBalpha. Mol Cell Biol 20: 2326–2333.

57. TsaiCC, KaoHY, YaoTP, McKeownM, EvansRM (1999) SMRTER, a Drosophila nuclear receptor coregulator, reveals that EcR-mediated repression is critical for development. Mol Cell 4: 175–186.

58. BaiJ, UeharaY, MontellDJ (2000) Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103: 1047–1058.

59. SedkovY, ChoE, PetrukS, CherbasL, SmithST, et al. (2003) Methylation at lysine 4 of histone H3 in ecdysone-dependent development of Drosophila. Nature 426: 78–83.

60. FrancisVA, ZorzanoA, TelemanAA (2010) dDOR is an EcR coactivator that forms a feed-forward loop connecting insulin and ecdysone signaling. Curr Biol 20: 1799–1808.

61. SawatsubashiS, MurataT, LimJ, FujikiR, ItoS, et al. (2010) A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev 24: 159–170.

62. DresselU, ThormeyerD, AltincicekB, PaululatA, EggertM, et al. (1999) Alien, a highly conserved protein with characteristics of a corepressor for members of the nuclear hormone receptor superfamily. Mol Cell Biol 19: 3383–3394.

63. ChauchereauA, GeorgiakakiM, Perrin-WolffM, MilgromE, LoosfeltH (2000) JAB1 interacts with both the progesterone receptor and SRC-1. J Biol Chem 275: 8540–8548.

64. PollyP, HerdickM, MoehrenU, BaniahmadA, HeinzelT, et al. (2000) VDR-Alien: a novel, DNA-selective vitamin D(3) receptor-corepressor partnership. FASEB J 14: 1455–1463.

65. OlmaMH, RoyM, Le BihanT, SumaraI, MaerkiS, et al. (2009) An interaction network of the mammalian COP9 signalosome identifies Dda1 as a core subunit of multiple Cul4-based E3 ligases. J Cell Sci 122: 1035–1044.

66. OuCY, WangCH, JiangJ, ChienCT (2007) Suppression of Hedgehog signaling by Cul3 ligases in proliferation control of retinal precursors. Dev Biol 308: 106–119.

67. LinHC, WuJT, TanBC, ChienCT (2009) Cul4 and DDB1 regulate Orc2 localization, BrdU incorporation and Dup stability during gene amplification in Drosophila follicle cells. J Cell Sci 122: 2393–2401.

68. CampuzanoS, CarramolinoL, CabreraCV, Ruiz-GomezM, VillaresR, et al. (1985) Molecular genetics of the achaete-scute gene complex of D. melanogaster. Cell 40: 327–338.

69. StewartM, MurphyC, FristromJW (1972) The recovery and preliminary characterization of X chromosome mutants affecting imaginal discs of Drosophila melanogaster. Dev Biol 27: 71–83.

70. KissI, BeatonAH, TardiffJ, FristromD, FristromJW (1988) Interactions and developmental effects of mutations in the Broad-Complex of Drosophila melanogaster. Genetics 118: 247–259.

71. SchwedesC, TulsianiS, CarneyGE (2011) Ecdysone receptor expression and activity in adult Drosophila melanogaster. J Insect Physiol 57: 899–907.

72. GustafsonK, BoulianneGL (1996) Distinct expression patterns detected within individual tissues by the GAL4 enhancer trap technique. Genome 39: 174–182.

73. FietzMJ, JacintoA, TaylorAM, AlexandreC, InghamPW (1995) Secretion of the amino-terminal fragment of the hedgehog protein is necessary and sufficient for hedgehog signalling in Drosophila. Curr Biol 5: 643–650.

74. BellaicheY, GhoM, KaltschmidtJA, BrandAH, SchweisguthF (2001) Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nat Cell Biol 3: 50–57.

75. MilanM, Diaz-BenjumeaFJ, CohenSM (1998) Beadex encodes an LMO protein that regulates Apterous LIM-homeodomain activity in Drosophila wing development: a model for LMO oncogene function. Genes Dev 12: 2912–2920.

76. ZhouX, ZhouB, TrumanJW, RiddifordLM (2004) Overexpression of broad: a new insight into its role in the Drosophila prothoracic gland cells. J Exp Biol 207: 1151–1161.

77. ZhouL, SchnitzlerA, AgapiteJ, SchwartzLM, StellerH, et al. (1997) Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midline cells. Proc Natl Acad Sci U S A 94: 5131–5136.

78. XuT, RubinGM (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223–1237.

79. SkeathJB, PanganibanG, SelegueJ, CarrollSB (1992) Gene regulation in two dimensions: the proneural achaete and scute genes are controlled by combinations of axis-patterning genes through a common intergenic control region. Genes Dev 6: 2606–2619.

80. GotoS, HayashiS (1999) Proximal to distal cell communication in the Drosophila leg provides a basis for an intercalary mechanism of limb patterning. Development 126: 3407–3413.

81. TalbotWS, SwyrydEA, HognessDS (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73: 1323–1337.

82. O'NeillEM, RebayI, TjianR, RubinGM (1994) The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78: 137–147.

83. ZipurskySL, VenkateshTR, TeplowDB, BenzerS (1984) Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36: 15–26.

84. YipML, LamkaML, LipshitzHD (1997) Control of germ-band retraction in Drosophila by the zinc-finger protein HINDSIGHT. Development 124: 2129–2141.

85. SpanaEP, DoeCQ (1995) The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121: 3187–3195.

86. KanukaH, KuranagaE, TakemotoK, HiratouT, OkanoH, et al. (2005) Drosophila caspase transduces Shaggy/GSK-3beta kinase activity in neural precursor development. EMBO J 24: 3793–3806.