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A Re-examination of the Selection of the Sensory Organ Precursor of the Bristle Sensilla of


The sensory organ precursor cell (SOP) that forms the mechanosensory bristles of the adult PNS of Drosophila is a paradigm to study neural precursor determination. The current model states that the SOP is selected in proneural clusters (PNCs) defined through the expression of the proneural genes. The selection occurs through lateral inhibition mediated by the Notch signalling pathway. The SOP is pre-selected by differential expression of Extramacrochaetae (Emc), the only member of the Id proteins in Drosophila, which inactivates the proneural factors. We have re-examined the selection process using novel markers and mutants. Our data suggest a different picture of SOP selection. We discovered a band–like region of varying proneural activity where the peaks constitute the proneural clusters. Within the PNC, a subgroup exists from which the SOP arises. The Notch pathway has two distinct functions in the subgroup and in the rest of the band. We show that so far one unappreciated essential role of the proneural genes is the neutralisation of the activity of Emc. Our data suggest that the selection of the SOP is more similar to neural selection in vertebrates than previously anticipated.


Vyšlo v časopise: A Re-examination of the Selection of the Sensory Organ Precursor of the Bristle Sensilla of. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004911
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004911

Souhrn

The sensory organ precursor cell (SOP) that forms the mechanosensory bristles of the adult PNS of Drosophila is a paradigm to study neural precursor determination. The current model states that the SOP is selected in proneural clusters (PNCs) defined through the expression of the proneural genes. The selection occurs through lateral inhibition mediated by the Notch signalling pathway. The SOP is pre-selected by differential expression of Extramacrochaetae (Emc), the only member of the Id proteins in Drosophila, which inactivates the proneural factors. We have re-examined the selection process using novel markers and mutants. Our data suggest a different picture of SOP selection. We discovered a band–like region of varying proneural activity where the peaks constitute the proneural clusters. Within the PNC, a subgroup exists from which the SOP arises. The Notch pathway has two distinct functions in the subgroup and in the rest of the band. We show that so far one unappreciated essential role of the proneural genes is the neutralisation of the activity of Emc. Our data suggest that the selection of the SOP is more similar to neural selection in vertebrates than previously anticipated.


Zdroje

1. HuangF, Dambly-ChaudièreC, GhysenA (1991) The emergence of sense organs in the wing disc of Drosophila. Development 111: 1087–1095.

2. Gómez-SkarmetaJL, CampuzanoS, JM (2003) Half a century of neural prepatterning: the story of a few bristles and many genes. Nat Rev Neurosci 4: 587–598.

3. MassariME, MurreC (2000) Helix-loop-Helix Proteins: Regulators of Transcription in Eucaryotic Organisms. MCB 20: 429–440.

4. CampuzanoS (2001) Emc, a negative HLH regulator with multiple functions in Drosophila development. Oncogene 20: 8299–8307.

5. BattacharyaA, BakerN (2011) A Network of Broadly Expressed HLH Genes Regulates Tissue-Specific Cell Fates. Cell 147: 881–892.

6. BertrandN, Castro, DS, GuillemotF (2002) Proneural genes and the specification of neural cell types. Nature Rev Neurosci 3: 517–530.

7. FortiniM (2009) Notch signalling: the core pathway and its posttranslational regulation. Dev Cell 16: 633–647.

8. BrayS (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678–689.

9. PitsoliC, DelidakisC (2005) The interplay between DSL proteins and ubiquitin ligases in Notch signaling. Development 132: 4041–4050.

10. Le BorgneR, BardinA, SchweisguthF (2005) The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 132: 1751–1762.

11. WangW, StruhlG (2005) Distinct roles for Mind bomb, Neuralized and Epsin in mediating DSL endocytosis and signaling in Drosophila. Development 132: 2883–2894.

12. YehE, ZhouL, RudzikN, BoulianneG (2000) Neuralized functions cell autonomously to regulate Drosophila sense organ development. Embo J 19: 4827–4837.

13. Campos-OrtegaJA, KnustE (1990) Molecular analysis of a cellular decision during embryonic development of Drosophila melanogaster: epidermogenesis or neurogenesis. Eur J Biochem 190: 1–10.

14. CubasP, ModolellJ (1992) The extramachrochaete gene provides information for sensory organ patterning. EMBO J 11: 3385.

15. De JoussineauC, SouléJ, MartinM, AnguilleC, MontcourrierP, et al. (2004) Delta-promoted filopodia mediate long-range lateral inhibition in Drosophila. Nature 426: 555–559.

16. CohenM, GeorgiouM, StevensonNL, MiodownikM, BaumB (2010) Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition. Dev Cell 19: 78–89.

17. SeugnetL, SimpsonP, HaenlinM (1997) Transcriptional regulation of Notch and Delta: requirement for neuroblast segregation in Drosophila. Development 124: 2015–2025.

18. ChanetS, VodovarN, MayauV, SchweisguthF (2009) Genome engineering-based analysis of Bearded family genes reveals both functional redundancy and a nonessential function in lateral inhibition in Drosophila. Genetics 182: 1101–1108.

19. KoelzerS, KleinT (2003) A Notch independent function of Suppressor of Hairless during the development of the bristle sensory organ precursor cell of Drosophila. Development 130: 1973–1988.

20. FurriolsM, BrayS (2001) A model response element detects Suppressor of Hairless-dependent molecular switch. Curr Biol 11: 60–64.

21. HousdenBE, MillenK, BraySJ (2012) Drosophila Reporter Vectors Compatible with ΦC31 Integrase Transgenesis Techniques and Their Use to Generate New Notch Reporter Fly Lines. G3 2: 79–82.

22. CastroB, BaroloS, BaileyA, PosakonyJW (2005) Lateral inhibition in proneural clusters: cis-regulatory logic and default repression by Suppressor of Hairlesss. Development 132: 3333–3344.

23. KasparM, SchneiderM, ChiaW, KleinT (2008) klumpfuss is involved in the determination of sensory organ precursors in Drosophila. Dev Biol 324: 177–191.

24. Le BorgneR, RemaudS, HamelS, SchweisguthF (2005) Two distinct E3 ubiquitin ligases have complementary functions in the regulation of delta and serrate signaling in Drosophila. PLoS Biol 3: e96.

25. LaiEC, RoegiersF, QinX, JanYN, RubinGM (2005) The ubiquitin ligase Drosophila Mind bomb promotes Notch signaling by regulating the localization and activity of Serrate and Delta. Development 132: 2319–2332.

26. SchweisguthF, PosakonyJW (1994) Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis. Development 120: 1433–1441.

27. ParksAL, HuppertSS, MuskavitchMA (1997) The dynamics of neurogenic signalling underlying bristle development in Drosophila melanogaster. Mech Dev 63: 61–74.

28. ParksAL, ShalabyNA, MuskavitchMA (2008) Notch and suppressor of Hairless regulate levels but not patterns of Delta expression in Drosophila. Genesis 46: 265–275.

29. MarcelliniS, SimpsonP (2006) Two or four bristles: functional evolution of an enhancer of scute in Drosophilidae. PLoS Biol 4: 0040386.

30. CuliJ, ModolellJ (1998) Proneural gene self-stimulation in neural precursors: an essential mechanism for sense organ development that is regulated by Notch signalling. Genes & Dev 12: 2036–2047.

31. 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 And Development 5: 996–1008.

32. García-BellidoA, SantamariaP (1978) Developmental Analysis of the Achaete-Scute System of DROSOPHILA MELANOGASTER. Genetics 88: 469–486.

33. ReesJS, LoweN, ArmeanIM, RooteJ, JohnsonG, et al. (2011) In vivo analysis of proteomes and interactomes using Parallel Affinity Capture (iPAC) coupled to mass spectrometry. Mol Cell Proteomics 6: M110.002386.

34. HeitzlerP, SimpsonP (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64: 1083–1092.

35. CastroB, BaroloS, BaileyA, PosakonyJW (2005) Lateral inhibition in proneural clusters: cis-regulatory logic and default repression by Suppressor of Hairless. Development 132: 3333–3344.

36. RodríguezI, HernándezR, ModolellJ, Ruiz-GómezM (1990) Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia. Embo Journal 9: 3583–3592.

37. KieckerC, LumsdenA (2012) The role of organizers in patterning the nervous system. Annu Rev Neurosci 35: 347–367.

38. AdamJC, MontellDJ (2004) A role for extra macrochaetae downstream of Notch in follicle cell differentiation. Development 131: 5971–5980.

39. BhattacharyaA, BakerNE (2009) The HLH protein Extramacrochaetae is required for R7 cell and cone cell fates in the Drosophila eye. Dev Biol 327: 288–300.

40. BaonzaA, de CelisJF, García-BellidoA (2000) Relationships between extramacrochaetae and Notch signalling in Drosophila wing development. Development 127: 2383–2393.

41. CronmillerC, CummingsCA (1993) The daughterless gene product in Drosophila is a nuclear protein that is broadly expressed throughout the organism during development. Mech Dev 42: 159–169.

42. Jafar-NejadH, TienA-C, AcarM, BellenHJ (2006) Sensless and Daughterless confer neuronal identity to epithelial cells in the Drosophiloa wing margin. Development 133: 1683–1692.

43. ZarifiI, KiparakiM, KoumbanakisKA, GiagtzoglouN, ZacharioudakiE, et al. (2012) Essential roles of Da transactivation domains in neurogenesis and in E(spl)-mediated repression. Mol Cell Biol 32: 4534–4548.

44. CabreraCV, AlonsoMC (1991) Transcriptional activation by heterodimers of the achaete-scute and daughterless gene products of Drosophila. Embo J 10: 2965–2973.

45. MurreC (2005) Helix-loop-helix proteins and lymphocyte development. Nature Immunology 6: 1079–1086.

46. BardinA, SchweisguthF (2006) Bearded family members inhibit Neuralized-mediated endocytosis and signaling activity of Delta in Drosophila. Dev Cell 10: 245–255.

47. SpeicherSA, ThomasU, HinzU, KnustE (1994) The Serrate locus of Drosophila and its role in morphogenesis of the wing imaginal discs: control of cell proliferation. Development 120: 535–544.

48. CrokerJA, ZiegenhornSL, HolmgrenRA (2006) Regulation of the Drosophila transcription factor, Cubitus interruptus, by two conserved domains. Dev Biol 291: 368–381.

49. de NavascuésJ, PerdigotoCN, BianY, SchneiderMH, BardinAJ, et al. (2012) Drosophila midgut homeostasis involves neutral competition between symmetrically dividing intestinal stem cells. EMBO J 31: 2473–2485.

50. MaroisE, MahmoudA, EatonS (2006) The endocytic pathway and formation of the Wingless morphogen gradient. Development 133: 307–317.

51. StruhlG, GreenwaldI (1999) Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 398: 522–525.

52. HuY, FortiniME (2003) Different cofactor activities in gamma-secretase assembly: evidence for a nicastrin-Aph-1 subcomplex. JCB 161: 685–690.

53. HuY, YEY, FortimniM (2002) Nicastrin is required for gamma-secretase cleavage of the Drosophila Notch receptor. Developmental Cell 1: 69–78.

54. MicchelliCA, RulifsonEJ, BlairSS (1997) The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development 124: 1485–1495.

55. LiY, BakerNE (2001) Proneural enhancement by Notch overcomes Suppressor-of-Hairless repressor function in the developing Drosophila eye. Curr Biol 11: 330–338.

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

57. ThomasU, SpeicherSA, KnustE (1991) The Drosophila gene Serrate encodes an EGF-like transmembrane protein with a complex expression pattern in embryos and wing discs. Development 111: 749–761.

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