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The bHLH-PAS Transcription Factor Dysfusion Regulates Tarsal Joint Formation in Response to Notch Activity during Leg Development


One of the keys of the evolutionary success of arthropods, the most diversified group of animals, is the acquisition of joints that allow the articulation of their appendages. Two main kinds of joints with different morphologies and evolutionary origin are found in the fly leg: the proximal or “true” joints that are motile due to muscular attachment and the distal joints that are immotile. A common event during joint formation is the activation of the Notch pathway at the presumptive joints along the leg proximo-distal axis. In this work we investigated how the same pathway, Notch, can control the formation of such homologous although different structures. We described that the transcription factor Dysfusion (Dys) is a Notch target required for distal joint development and that is sufficient to induce joint-like structures when ectopically expressed. Dys controls two important morphogenetic events that direct tarsal joint development such as programed cell death and epithelial cell shape. Moreover, we identified a regulatory DNA sequence that controls dys expression in the tarsal segment by direct binding of the transcriptional effector of the Notch pathway Su(H). Thus, Notch controls the development of proximal vs distal joints by the recruitment of specific downstream target genes such as dys.


Vyšlo v časopise: The bHLH-PAS Transcription Factor Dysfusion Regulates Tarsal Joint Formation in Response to Notch Activity during Leg Development. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004621
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004621

Souhrn

One of the keys of the evolutionary success of arthropods, the most diversified group of animals, is the acquisition of joints that allow the articulation of their appendages. Two main kinds of joints with different morphologies and evolutionary origin are found in the fly leg: the proximal or “true” joints that are motile due to muscular attachment and the distal joints that are immotile. A common event during joint formation is the activation of the Notch pathway at the presumptive joints along the leg proximo-distal axis. In this work we investigated how the same pathway, Notch, can control the formation of such homologous although different structures. We described that the transcription factor Dysfusion (Dys) is a Notch target required for distal joint development and that is sufficient to induce joint-like structures when ectopically expressed. Dys controls two important morphogenetic events that direct tarsal joint development such as programed cell death and epithelial cell shape. Moreover, we identified a regulatory DNA sequence that controls dys expression in the tarsal segment by direct binding of the transcriptional effector of the Notch pathway Su(H). Thus, Notch controls the development of proximal vs distal joints by the recruitment of specific downstream target genes such as dys.


Zdroje

1. CohenSM (1990) Specification of limb development in the Drosophila embryo by positional cues from segmentation genes. Nature 343: 173–177.

2. EstellaC, VoutevR, MannRS (2012) A dynamic network of morphogens and transcription factors patterns the fly leg. Curr Top Dev Biol 98: 173–198.

3. Diaz-BenjumeaFJ, CohenB, CohenSM (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372: 175–179.

4. LecuitT, CohenSM (1997) Proximal-distal axis formation in the Drosophila leg. Nature 388: 139–145.

5. CampbellG, WeaverT, TomlinsonA (1993) Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74: 1113–1123.

6. EstellaC, McKayDJ, MannRS (2008) Molecular integration of wingless, decapentaplegic, and autoregulatory inputs into Distalless during Drosophila leg development. Dev Cell 14: 86–96.

7. GiorgianniMW, MannRS (2011) Establishment of medial fates along the proximodistal axis of the Drosophila leg through direct activation of dachshund by Distalless. Dev Cell 20: 455–468.

8. Abu-ShaarM, MannRS (1998) Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125: 3821–3830.

9. GalindoMI, BishopSA, GreigS, CousoJP (2002) Leg patterning driven by proximal-distal interactions and EGFR signaling. Science 297: 256–259.

10. CampbellG (2002) Distalization of the Drosophila leg by graded EGF-receptor activity. Nature 418: 781–785.

11. BishopSA, KleinT, AriasAM, CousoJP (1999) Composite signalling from Serrate and Delta establishes leg segments in Drosophila through Notch. Development 126: 2993–3003.

12. de CelisJF, TylerDM, de CelisJ, BraySJ (1998) Notch signalling mediates segmentation of the Drosophila leg. Development 125: 4617–4626.

13. RauskolbC (2001) The establishment of segmentation in the Drosophila leg. Development 128: 4511–4521.

14. RauskolbC, IrvineKD (1999) Notch-mediated segmentation and growth control of the Drosophila leg. Dev Biol 210: 339–350.

15. BrayS, BernardF (2010) Notch Targets and Their Regulation. Curr Top Dev Biol 92: 253–275.

16. KerberB, MongeI, MuellerM, MitchellPJ, CohenSM (2001) The AP-2 transcription factor is required for joint formation and cell survival in Drosophila leg development. 128: 1231–1238.

17. MongeI, KrishnamurthyR, SimsD, HirthF, SpenglerM, et al. (2001) Drosophila transcription factor AP-2 in proboscis, leg and brain central complex development. Development 128: 1239–1252.

18. Snodgrass R (1935) Principles of Insect Morphology. New York: McGraw-Hill. pp. 83–99.

19. CasaresF, MannRS (2001) The ground state of the ventral appendage in Drosophila. Science 293: 1477–1480.

20. ManjonC, Sanchez-HerreroE, SuzanneM (2007) Sharp boundaries of Dpp signalling trigger local cell death required for Drosophila leg morphogenesis. Nat Cell Biol 9: 57–63.

21. de Celis IbeasJM, BraySJ (2003) Bowl is required downstream of Notch for elaboration of distal limb patterning. Development 130: 5943–5952.

22. MirthC, AkamM (2002) Joint development in the Drosophila leg: cell movements and cell populations. Dev Biol 246: 391–406.

23. TajiriR, MisakiK, YonemuraS, HayashiS (2010) Dynamic shape changes of ECM-producing cells drive morphogenesis of ball-and-socket joints in the fly leg. Development 137: 2055–2063.

24. TajiriR, MisakiK, YonemuraS, HayashiS (2011) Joint morphology in the insect leg: evolutionary history inferred from Notch loss-of-function phenotypes in Drosophila. Development 138: 4621–4626.

25. PueyoJI, CousoJP (2011) Tarsal-less peptides control Notch signalling through the Shavenbaby transcription factor. Dev Biol 355: 183–193.

26. BierE, VaessinH, Younger-ShepherdS, JanLY, JanYN (1992) deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev 6: 2137–2151.

27. GreenbergL, HatiniV (2011) Systematic expression and loss-of-function analysis defines spatially restricted requirements for Drosophila RhoGEFs and RhoGAPs in leg morphogenesis. Mech Dev 128: 5–17.

28. Adachi-YamadaT, O'ConnorMB (2002) Morphogenetic apoptosis: a mechanism for correcting discontinuities in morphogen gradients. Dev Biol 251: 74–90.

29. Van AelstL, SymonsM (2002) Role of Rho family GTPases in epithelial morphogenesis. Genes Dev 16: 1032–1054.

30. JiangL, CrewsST (2003) The Drosophila dysfusion basic helix-loop-helix (bHLH)-PAS gene controls tracheal fusion and levels of the trachealess bHLH-PAS protein. Mol Cell Biol 23: 5625–5637.

31. JiangL, CrewsST (2006) Dysfusion transcriptional control of Drosophila tracheal migration, adhesion, and fusion. Mol Cell Biol 26: 6547–6556.

32. JiangL, CrewsST (2007) Transcriptional specificity of Drosophila dysfusion and the control of tracheal fusion cell gene expression. J Biol Chem 282: 28659–28668.

33. JoryA, EstellaC, GiorgianniMW, SlatteryM, LavertyTR, et al. (2012) A survey of 6,300 genomic fragments for cis-regulatory activity in the imaginal discs of Drosophila melanogaster. Cell Rep 2: 1014–1024.

34. GuarnerA, ManjonC, EdwardsK, StellerH, SuzanneM, et al. (2014) The zinc finger homeodomain-2 gene of Drosophila controls Notch targets and regulates apoptosis in the tarsal segments. Dev Biol 385: 350–365.

35. EmmonsRB, DuncanD, EstesPA, KiefelP, MosherJT, et al. (1999) The spineless-aristapedia and tango bHLH-PAS proteins interact to control antennal and tarsal development in Drosophila. Development 126: 3937–3945.

36. WardMP, MosherJT, CrewsST (1998) Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis. Development 125: 1599–1608.

37. TajiriR, TsujiT, UedaR, SaigoK, KojimaT (2007) Fate determination of Drosophila leg distal regions by trachealess and tango through repression and stimulation, respectively, of Bar homeobox gene expression in the future pretarsus and tarsus. Dev Biol 303: 461–473.

38. OoeN, SaitoK, MikamiN, NakatukaI, KanekoH (2004) Identification of a novel basic helix-loop-helix-PAS factor, NXF, reveals a Sim2 competitive, positive regulatory role in dendritic-cytoskeleton modulator drebrin gene expression. Mol Cell Biol 24: 608–616.

39. BaroloS, StoneT, BangAG, PosakonyJW (2002) Default repression and Notch signaling: Hairless acts as an adaptor to recruit the corepressors Groucho and dCtBP to Suppressor of Hairless. Genes Dev 16: 1964–1976.

40. JiangL, PearsonJC, CrewsST (2010) Diverse modes of Drosophila tracheal fusion cell transcriptional regulation. Mech Dev 127: 265–280.

41. CoudercJL, GodtD, ZollmanS, ChenJ, LiM, et al. (2002) The bric a brac locus consists of two paralogous genes encoding BTB/POZ domain proteins and acts as a homeotic and morphogenetic regulator of imaginal development in Drosophila. Development 129: 2419–2433.

42. St PierreSE, GalindoMI, CousoJP, ThorS (2002) Control of Drosophila imaginal disc development by rotund and roughened eye: differentially expressed transcripts of the same gene encoding functionally distinct zinc finger proteins. Development 129: 1273–1281.

43. DuncanDM, BurgessEA, DuncanI (1998) Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor. Genes Dev 12: 1290–1303.

44. LeeS, KolodziejPA (2002) The plakin Short Stop and the RhoA GTPase are required for E-cadherin-dependent apical surface remodeling during tracheal tube fusion. Development 129: 1509–1520.

45. ChiharaT, KatoK, TaniguchiM, NgJ, HayashiS (2003) Rac promotes epithelial cell rearrangement during tracheal tubulogenesis in Drosophila. Development 130: 1419–1428.

46. TabataT (2001) Genetics of morphogen gradients. Nat Rev Genet 2: 620–630.

47. HaoI, GreenRB, DunaevskyO, LengyelJA, RauskolbC (2003) The odd-skipped family of zinc finger genes promotes Drosophila leg segmentation. Dev Biol 263: 282–295.

48. de CelisJF, BrayS (1997) Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124: 3241–3251.

49. PresenteA, ShawS, NyeJS, AndresAJ (2002) Transgene-mediated RNA interference defines a novel role for notch in chemosensory startle behavior. Genesis 34: 165–169.

50. ShellenbargerDL, MohlerJD (1978) Temperature-sensitive periods and autonomy of pleiotropic effects of l(1)Nts1, a conditional notch lethal in Drosophila. Dev Biol 62: 432–446.

51. JiangC, LamblinAF, StellerH, ThummelCS (2000) A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol Cell 5: 445–455.

52. GretherME, AbramsJM, AgapiteJ, WhiteK, StellerH (1995) The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev 9: 1694–1708.

53. DietzlG, ChenD, SchnorrerF, SuKC, BarinovaY, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151–156.

54. SosinskyA, BoninCP, MannRS, HonigB (2003) Target Explorer: An automated tool for the identification of new target genes for a specified set of transcription factors. Nucleic Acids Res 31: 3589–3592.

55. San-JuanBP, BaonzaA (2011) The bHLH factor deadpan is a direct target of Notch signaling and regulates neuroblast self-renewal in Drosophila. Dev Biol 352: 70–82.

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Genetika Reprodukčná medicína

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PLOS Genetics


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