Expression in Planarian Neoblasts after Injury Controls Anterior Pole Regeneration

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Some animals are capable of regenerating organs damaged or removed by injury, and this ability likely requires precise control of secreted proteins that promote growth. Planarians are flatworms that can regenerate any missing tissues by regulating the activity of adult stem cells that can produce any specialized cell type. We identify the zic-1 gene as activated in planarian stem cells by injury and needed for head regeneration after decapitation. This gene's product likely acts as a transcription factor to produce cells that secrete a growth-promoting protein, NOTUM, at the tip of the regenerating tissue outgrowth to organize and enable head regeneration. These results suggest that regeneration requires specialized uses of stem cell descendants to orchestrate new tissue production following injury.

Vyšlo v časopise: Expression in Planarian Neoblasts after Injury Controls Anterior Pole Regeneration. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004452
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004452

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1. TanakaEM, ReddienPW (2011) The cellular basis for animal regeneration. Dev Cell 21: 172–185.

2. RinkJC (2013) Stem cell systems and regeneration in planaria. Dev Genes Evol 223: 67–84.

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

4. ReddienPW, OviedoNJ, JenningsJR, JenkinJC, Sánchez AlvaradoA (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327–1330.

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

6. HayashiT, AsamiM, HiguchiS, ShibataN, AgataK (2006) Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev Growth Differ 48: 371–380.

7. WenemoserD, ReddienPW (2010) Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 344: 979–991.

8. GuedelhoeferOCt, Sánchez AlvaradoA (2012) Amputation induces stem cell mobilization to sites of injury during planarian regeneration. Development 139: 3510–3520.

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

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

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

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

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

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

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

16. LiuSY, SelckC, FriedrichB, LutzR, Vila-FarreM, et al. (2013) Reactivating head regrowth in a regeneration-deficient planarian species. Nature 500: 81–84.

17. SikesJM, NewmarkPA (2013) Restoration of anterior regeneration in a planarian with limited regenerative ability. Nature 500: 77–80.

18. UmesonoY, TasakiJ, NishimuraY, HroudaM, KawaguchiE, et al. (2013) The molecular logic for planarian regeneration along the anterior-posterior axis. Nature 500: 73–76.

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

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

21. Gonzalez-SastreA, MolinaMD, SalóE (2012) Inhibitory Smads and bone morphogenetic protein (BMP) modulate anterior photoreceptor cell number during planarian eye regeneration. Int J Dev Biol 56: 155–163.

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

23. MolinaMD, SalóE, CebriaF (2007) The BMP pathway is essential for re-specification and maintenance of the dorsoventral axis in regenerating and intact planarians. Dev Biol 311: 79–94.

24. 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.

25. GavinoMA, WenemoserD, WangIE, ReddienPW (2013) Tissue absence initiates regeneration through Follistatin-mediated inhibition of Activin signaling. Elife 2: e00247.

26. 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.

27. ZhangD, ChanJD, NogiT, MarchantJS (2011) Opposing roles of voltage-gated Ca2+ channels in neuronal control of regenerative patterning. J Neurosci 31: 15983–15995.

28. OviedoNJ, MorokumaJ, WalentekP, KemaIP, GuMB, et al. (2010) Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. Dev Biol 339: 188–199.

29. OviedoNJ, LevinM (2007) smedinx-11 is a planarian stem cell gap junction gene required for regeneration and homeostasis. Development 134: 3121–3131.

30. BeaneWS, MorokumaJ, LemireJM, LevinM (2013) Bioelectric signaling regulates head and organ size during planarian regeneration. Development 140: 313–322.

31. BeaneWS, MorokumaJ, AdamsDS, LevinM (2011) A chemical genetics approach reveals H,K-ATPase-mediated membrane voltage is required for planarian head regeneration. Chem Biol 18: 77–89.

32. 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.

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

34. GiraldezAJ, CopleyRR, CohenSM (2002) HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev Cell 2: 667–676.

35. GerlitzO, BaslerK (2002) Wingful, an extracellular feedback inhibitor of Wingless. Genes Dev 16: 1055–1059.

36. FlowersGP, TopczewskaJM, TopczewskiJ (2012) A zebrafish Notum homolog specifically blocks the Wnt/beta-catenin signaling pathway. Development 139: 2416–2425.

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

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

39. MarzM, SeebeckF, BartschererK (2013) A Pitx transcription factor controls the establishment and maintenance of the serotonergic lineage in planarians. Development 140: 4499–4509.

40. CurrieKW, PearsonBJ (2013) Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians. Development 140: 3577–3588.

41. ScimoneML, LapanSW, ReddienPW (2014) A forkhead transcription factor is wound-induced at the planarian midline and required for anterior pole regeneration. PLoS Genet 10: e1003999.

42. FujimiTJ, HatayamaM, ArugaJ (2012) Xenopus Zic3 controls notochord and organizer development through suppression of the Wnt/beta-catenin signaling pathway. Dev Biol 361: 220–231.

43. WarrN, Powles-GloverN, ChappellA, RobsonJ, NorrisD, et al. (2008) Zic2-associated holoprosencephaly is caused by a transient defect in the organizer region during gastrulation. Hum Mol Genet 17: 2986–2996.

44. LeeH, StultzBG, HurshDA (2007) The Zic family member, odd-paired, regulates the Drosophila BMP, decapentaplegic, during adult head development. Development 134: 1301–1310.

45. ArugaJ, KamiyaA, TakahashiH, FujimiTJ, ShimizuY, et al. (2006) A wide-range phylogenetic analysis of Zic proteins: implications for correlations between protein structure conservation and body plan complexity. Genomics 87: 783–792.

46. KuoJS, PatelM, GamseJ, MerzdorfC, LiuX, et al. (1998) Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. Development 125: 2867–2882.

47. NakataK, NagaiT, ArugaJ, MikoshibaK (1997) Xenopus Zic3, a primary regulator both in neural and neural crest development. Proc Natl Acad Sci U S A 94: 11980–11985.

48. MizusekiK, KishiM, MatsuiM, NakanishiS, SasaiY (1998) Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development 125: 579–587.

49. DiNardoS, O'FarrellPH (1987) Establishment and refinement of segmental pattern in the Drosophila embryo: spatial control of engrailed expression by pair-rule genes. Genes Dev 1: 1212–1225.

50. HoutmeyersR, SouopguiJ, TejparS, ArkellR (2013) The ZIC gene family encodes multi-functional proteins essential for patterning and morphogenesis. Cell Mol Life Sci 70: 3791–3811.

51. LapanSW, ReddienPW (2012) Transcriptome Analysis of the Planarian Eye Identifies ovo as a Specific Regulator of Eye Regeneration. Cell Rep 2: 294–307.

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

53. ReddienPW, NewmarkPA, Sánchez AlvaradoA (2008) Gene nomenclature guidelines for the planarian Schmidtea mediterranea. Dev Dyn 237: 3099–3101.

54. GuoT, PetersAH, NewmarkPA (2006) A Bruno-like gene is required for stem cell maintenance in planarians. Dev Cell 11: 159–169.

55. EisenhofferGT, KangH, Sánchez AlvaradoA (2008) Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 3: 327–339.

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

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

58. AdellT, CebriaF, SalóE (2010) Gradients in planarian regeneration and homeostasis. Cold Spring Harb Perspect Biol 2: a000505.

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

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

61. ForsthoefelDJ, ParkAE, NewmarkPA (2011) Stem cell-based growth, regeneration, and remodeling of the planarian intestine. Dev Biol 356: 445–459.

62. CowlesMW, BrownDD, NisperosSV, StanleyBN, PearsonBJ, et al. (2013) Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration. Development 140: 4691–4702.

63. WagnerDE, HoJJ, ReddienPW (2012) Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 10: 299–311.

64. 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.

65. PearsonBJ, Sánchez AlvaradoA (2008) Regeneration, stem cells, and the evolution of tumor suppression. Cold Spring Harb Symp Quant Biol 73: 565–572.

66. SandmannT, VoggMC, OwlarnS, BoutrosM, BartschererK (2011) The head-regeneration transcriptome of the planarian Schmidtea mediterranea. Genome Biol 12: R76.

67. 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.

68. MaurusD, HarrisWA (2009) Zic-associated holoprosencephaly: zebrafish Zic1 controls midline formation and forebrain patterning by regulating Nodal, Hedgehog, and retinoic acid signaling. Genes Dev 23: 1461–1473.

69. PourebrahimR, HoutmeyersR, GhogomuS, JanssensS, ThelieA, et al. (2011) Transcription factor Zic2 inhibits Wnt/beta-catenin protein signaling. J Biol Chem 286: 37732–37740.

70. BrownSA, WarburtonD, BrownLY, YuCY, RoederER, et al. (1998) Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat Genet 20: 180–183.

71. AdamidiC, WangY, GruenD, MastrobuoniG, YouX, et al. (2011) De novo assembly and validation of planaria transcriptome by massive parallel sequencing and shotgun proteomics. Genome Res 21: 1193–1200.

72. ReschAM, PalakodetiD, LuYC, HorowitzM, GraveleyBR (2012) Transcriptome analysis reveals strain-specific and conserved stemness genes in Schmidtea mediterranea. PLoS One 7: e34447.

73. SmythGK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.

74. LabbeRM, IrimiaM, CurrieKW, LinA, ZhuSJ, et al. (2012) A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells 30: 1734–1745.

75. ReddienPW, BermangeAL, MurfittKJ, JenningsJR, Sánchez AlvaradoA (2005) Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev Cell 8: 635–649.

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

77. KingRS, NewmarkPA (2013) In situ hybridization protocol for enhanced detection of gene expression in the planarian Schmidtea mediterranea. BMC Dev Biol 13: 8.