A Transcription Factor Is Wound-Induced at the Planarian Midline and Required for Anterior Pole Regeneration

English version České info

Planarian regeneration requires positional information to specify the identity of tissues to be replaced as well as pluripotent neoblasts capable of differentiating into new cell types. We found that wounding elicits rapid expression of a gene encoding a Forkhead-family transcription factor, FoxD. Wound-induced FoxD expression is specific to the ventral midline, is regulated by Hedgehog signaling, and is neoblast-independent. FoxD is subsequently expressed within a medial subpopulation of neoblasts at wounds involving head regeneration. Ultimately, FoxD is co-expressed with multiple anterior markers at the anterior pole. Inhibition of FoxD with RNA interference (RNAi) results in the failure to specify neoblasts expressing anterior markers (notum and prep) and in anterior pole formation defects. FoxD(RNAi) animals fail to regenerate a new midline and to properly pattern the anterior blastema, consistent with a role for the anterior pole in organizing pattern of the regenerating head. Our results suggest that wound signaling activates a forkhead transcription factor at the midline and, if the head is absent, FoxD promotes specification of neoblasts at the prior midline for anterior pole regeneration.

Vyšlo v časopise: A Transcription Factor Is Wound-Induced at the Planarian Midline and Required for Anterior Pole Regeneration. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1003999
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003999

Souhrn

Zdroje

1. WagnerDE, WangIE, ReddienPW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332: 811–816.

2. ReddienPW, Sánchez AlvaradoA (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20: 725–757.

3. WenemoserD, LapanSW, WilkinsonAW, BellGW, ReddienPW (2012) A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26: 988–1002.

4. YazawaS, UmesonoY, HayashiT, TaruiH, AgataK (2009) Planarian Hedgehog/Patched establishes anterior-posterior polarity by regulating Wnt signaling. Proc Natl Acad Sci U S A 106: 22329–22334.

5. RinkJC, GurleyKA, ElliottSA, Sánchez AlvaradoA (2009) Planarian Hh signaling regulates regeneration polarity and links Hh pathway evolution to cilia. Science 326: 1406–1410.

6. GurleyKA, RinkJC, Sánchez AlvaradoA (2008) Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319: 323–327.

7. PetersenCP, ReddienPW (2008) Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319: 327–330.

8. PetersenCP, ReddienPW (2011) Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 332: 852–855.

9. ReddienPW, BermangeAL, KiczaAM, Sánchez AlvaradoA (2007) BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 134: 4043–4051.

10. GaviñoMA, ReddienPW (2011) A Bmp/Admp regulatory circuit controls maintenance and regeneration of dorsal-ventral polarity in planarians. Curr Biol 21: 294–299.

11. MolinaMD, NetoA, MaesoI, Gomez-SkarmetaJL, SaloE, et al. (2011) Noggin and noggin-like genes control dorsoventral axis regeneration in planarians. Curr Biol 21: 300–305.

12. AdellT, SaloE, BoutrosM, BartschererK (2009) Smed-Evi/Wntless is required for beta-catenin-dependent and -independent processes during planarian regeneration. Development 136: 905–910.

13. IglesiasM, Almuedo-CastilloM, AboobakerAA, SaloE (2011) Early planarian brain regeneration is independent of blastema polarity mediated by the Wnt/beta-catenin pathway. Dev Biol 358: 68–78.

14. ReddienPW (2011) Constitutive gene expression and the specification of tissue identity in adult planarian biology. Trends Genet 27: 277–285.

15. WitchleyJN, MayerM, WagnerDE, OwenJH, ReddienPW (2013) Muscle cells provide instructions for planarian regeneration. Cell Rep 4: 633–641.

16. CebriaF, KobayashiC, UmesonoY, NakazawaM, MinetaK, et al. (2002) FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 419: 620–624.

17. FelixDA, AboobakerAA (2010) The TALE class homeobox gene Smed-prep defines the anterior compartment for head regeneration. PLoS Genet 6: e1000915.

18. GurleyKA, ElliottSA, SimakovO, SchmidtHA, HolsteinTW, et al. (2010) Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev Biol 347: 24–39.

19. BlassbergRA, FelixDA, Tejada-RomeroB, AboobakerAA (2013) PBX/extradenticle is required to re-establish axial structures and polarity during planarian regeneration. Development 140: 730–739.

20. ChenCC, WangIE, ReddienPW (2013) pbx is required for pole and eye regeneration in planarians. Development 140: 719–729.

21. HayashiT, MotoishiM, YazawaS, ItomiK, TanegashimaC, et al. (2011) A LIM-homeobox gene is required for differentiation of Wnt-expressing cells at the posterior end of the planarian body. Development 138: 3679–3688.

22. Roberts-GalbraithRH, NewmarkPA (2013) Follistatin antagonizes Activin signaling and acts with Notum to direct planarian head regeneration. Proc Natl Acad Sci U S A 110: 1363–1368.

23. GaviñoMA, WenemoserD, WangIE, ReddienPW (2013) Tissue absence initiates regeneration through Follistatin-mediated inhibition of Activin signaling. eLiFE 2: e00247.

24. BenayounBA, CaburetS, VeitiaRA (2011) Forkhead transcription factors: key players in health and disease. Trends Genet 27: 224–232.

25. CarlssonP, MahlapuuM (2002) Forkhead transcription factors: key players in development and metabolism. Dev Biol 250: 1–23.

26. LehmannOJ, SowdenJC, CarlssonP, JordanT, BhattacharyaSS (2003) Fox's in development and disease. Trends Genet 19: 339–344.

27. HannenhalliS, KaestnerKH (2009) The evolution of Fox genes and their role in development and disease. Nat Rev Genet 10: 233–240.

28. WeigelD, JurgensG, KuttnerF, SeifertE, JackleH (1989) The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57: 645–658.

29. HackerU, KaufmannE, HartmannC, JurgensG, KnochelW, et al. (1995) The Drosophila fork head domain protein crocodile is required for the establishment of head structures. EMBO J 14: 5306–5317.

30. GrossniklausU, PearsonRK, GehringWJ (1992) The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev 6: 1030–1051.

31. CadiganKM, GrossniklausU, GehringWJ (1994) Localized expression of sloppy paired protein maintains the polarity of Drosophila parasegments. Genes Dev 8: 899–913.

32. YuJK, HollandND, HollandLZ (2003) AmphiFoxQ2, a novel winged helix/forkhead gene, exclusively marks the anterior end of the amphioxus embryo. Dev Genes Evol 213: 102–105.

33. DirksenML, JamrichM (1992) A novel, activin-inducible, blastopore lip-specific gene of Xenopus laevis contains a fork head DNA-binding domain. Genes Dev 6: 599–608.

34. KoinumaS, UmesonoY, WatanabeK, AgataK (2003) The expression of planarian brain factor homologs, DjFoxG and DjFoxD. Gene Expr Patterns 3: 21–27.

35. CebriaF, GuoT, JopekJ, NewmarkPA (2007) Regeneration and maintenance of the planarian midline is regulated by a slit orthologue. Dev Biol 307: 394–406.

36. DuboisF (1949) Contribution à l'étude de la migration des cellules. de régénération chez les Planaires dulcicoles. Bull Biol Fr Belg 83: 213–283.

37. PetersenCP, ReddienPW (2009) A wound-induced Wnt expression program controls planarian regeneration polarity. Proc Natl Acad Sci U S A 106: 17061–17066.

38. OgawaK, IshiharaS, SaitoY, MinetaK, NakazawaM, et al. (2002) Induction of a noggin-like gene by ectopic DV interaction during planarian regeneration. Dev Biol 250: 59–70.

39. IglesiasM, Gomez-SkarmetaJL, SaloE, AdellT (2008) Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development 135: 1215–1221.

40. KalderonD (2000) Transducing the hedgehog signal. Cell 103: 371–374.

41. MuroneM, RosenthalA, de SauvageFJ (1999) Hedgehog signal transduction: from flies to vertebrates. Exp Cell Res 253: 25–33.

42. NishimuraK, KitamuraY, TaniguchiT, AgataK (2010) Analysis of motor function modulated by cholinergic neurons in planarian Dugesia japonica. Neuroscience 168: 18–30.

43. CebriaF, NewmarkPA (2005) Planarian homologs of netrin and netrin receptor are required for proper regeneration of the central nervous system and the maintenance of nervous system architecture. Development 132: 3691–3703.

44. DrieverW, Nusslein-VolhardC (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54: 83–93.

45. DrieverW, Nusslein-VolhardC (1988) The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54: 95–104.

46. NanceJ (2005) PAR proteins and the establishment of cell polarity during C. elegans development. Bioessays 27: 126–135.

47. KieckerC, NiehrsC (2001) A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development 128: 4189–4201.

48. LapanSW, ReddienPW (2011) dlx and sp6-9 control optic cup regeneration in a prototypic eye. PLoS Genet 7: e1002226.

49. ScimoneML, SrivastavaM, BellGW, ReddienPW (2011) A regulatory program for excretory system regeneration in planarians. Development 138: 4387–4398.

50. PearsonBJ, EisenhofferGT, GurleyKA, RinkJC, MillerDE, et al. (2009) Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn 238: 443–450.

51. NewmarkPA, Sánchez AlvaradoA (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220: 142–153.

52. ScimoneML, MeiselJ, ReddienPW (2010) The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development 137: 1231–1241.