Follistatin antagonizes Activin signaling and acts with Notum to direct planarian head regeneration

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 4, 2013, Pages 1363-1368

  Roberts Galbraith, Rachel H ^a   Newmark, Phillip A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; FOLLISTATIN; NOTUM; SMAD2 PROTEIN; SMAD3 PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL TYPE; EMBRYO DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATION; SIGNAL TRANSDUCTION; TURBELLARIA;

ACTIVINS; ANIMALS; BODY PATTERNING; FOLLISTATIN; GENE KNOCKDOWN TECHNIQUES; GENES, HELMINTH; HELMINTH PROTEINS; MOLECULAR SEQUENCE DATA; PLANARIANS; PLURIPOTENT STEM CELLS; REGENERATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WNT PROTEINS;

AMPHIBIA; ANIMALIA; PLANARIA; TURBELLARIA;

EID: 84872839322     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1214053110     Document Type: Article

References (54)

1. Forsthoefel DJ, Newmark PA (2009) Emerging patterns in planarian regeneration. Curr Opin Genet Dev 19(4):412-420.
2. Gurley KA, Rink JC, Sánchez Alvarado A (2008) Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319(5861):323-327.
3. Petersen CP, Reddien PW (2008) Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319(5861):327-330.
4. Iglesias M, Gomez-Skarmeta JL, Saló E, Adell T (2008) Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development 135(7):1215-1221.
5. Gurley KA, et al. (2010) Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev Biol 347(1):24-39.
6. Petersen CP, Reddien PW (2009) A wound-induced Wnt expression program controls planarian regeneration polarity. Proc Natl Acad Sci USA 106(40):17061-17066.
7. Wenemoser D, Lapan SW, Wilkinson AW, Bell GW, Reddien PW (2012) A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26(9):988-1002.
8. Rink JC, Gurley KA, Elliott SA, Sánchez Alvarado A (2009) Planarian Hh signaling regulates regeneration polarity and links Hh pathway evolution to cilia. Science 326(5958):1406-1410.
9. Yazawa S, Umesono Y, Hayashi T, Tarui H, Agata K (2009) Planarian Hedgehog/Patched establishes anterior-posterior polarity by regulating Wnt signaling. Proc Natl Acad Sci USA 106(52):22329-22334.
10. Petersen CP, Reddien PW (2011) Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 332(6031):852-855.
11. Reddien PW, Bermange AL, Kicza AM, Sánchez Alvarado A (2007) BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 134(22):4043-4051.
12. Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332(6031):811-816.
13. Morgan T (1898) Experimental studies of the regeneration of Planaria maculata. Arch Entwicklungsmech Org 7(2-3):364-397.
14. Koinuma S, Umesono Y, Watanabe K, Agata K (2003) The expression of planarian brain factor homologs, DjFoxG and DjFoxD. Gene Expr Patterns 3(1):21-27.
15. Blount AL, et al. (2009) FoxL2 and Smad3 coordinately regulate follistatin gene transcription. J Biol Chem 284(12):7631-7645.
16. Kashimada K, et al. (2011) FOXL2 and BMP2 act cooperatively to regulate follistatin gene expression during ovarian development. Endocrinology 152(1):272-280.
17. Nishimura K, Kitamura Y, Taniguchi T, Agata K (2010) Analysis of motor function modulated by cholinergic neurons in planarian Dugesia japonica. Neuroscience 168(1):18-30.
18. Cebrià F, et al. (2002) The expression of neural-specific genes reveals the structural and molecular complexity of the planarian central nervous system. Mech Dev 116(1-2): 199-204.
19. Cebrià F, et al. (2002) FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 419(6907):620-624.
20. Nakamura T, et al. (1990) Activin-binding protein from rat ovary is follistatin. Science 247(4944):836-838.
21. Fainsod A, et al. (1997) The dorsalizing and neural inducing gene follistatin is an antagonist of BMP-4. Mech Dev 63(1):39-50.
22. Hashimoto M, et al. (1992) Follistatin is a developmentally regulated cytokine in neural differentiation. J Biol Chem 267(11):7203-7206.
23. Bickel D, Shah R, Gesualdi SC, Haerry TE (2008) Drosophila Follistatin exhibits unique structural modifications and interacts with several TGF-beta family members. Mech Dev 125(1-2):117-129.
24. Iemura S, et al. (1998) Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo. Proc Natl Acad Sci USA 95(16):9337-9342.
25. Molina MD, Saló E, Cebrià F (2007) The BMP pathway is essential for re-specification and maintenance of the dorsoventral axis in regenerating and intact planarians. Dev Biol 311(1):79-94.
26. Gaviño MA, Reddien PW (2011) A Bmp/Admp regulatory circuit controls maintenance and regeneration of dorsal-ventral polarity in planarians. Curr Biol 21(4):294-299.
27. Xia Y, Schneyer AL (2009) The biology of activin: Recent advances in structure, regulation and function. J Endocrinol 202(1):1-12.
28. Reddien PW, Bermange AL, Murfitt KJ, Jennings JR, Sánchez Alvarado A (2005) Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev Cell 8(5):635-649.
29. Murry CE, Keller G (2008) Differentiation of embryonic stem cells to clinically relevant populations: Lessons from embryonic development. Cell 132(4):661-680.
30. Zhou J, et al. (2010) High-efficiency induction of neural conversion in human ESCs and human induced pluripotent stem cells with a single chemical inhibitor of transforming growth factor beta superfamily receptors. Stem Cells 28(10):1741-1750.
31. Smith JR, et al. (2008) Inhibition of Activin/Nodal signaling promotes specification of human embryonic stem cells into neuroectoderm. Dev Biol 313(1):107-117.
32. Bradham CA, et al. (2009) Chordin is required for neural but not axial development in sea urchin embryos. Dev Biol 328(2):221-233.
33. Hemmati-Brivanlou A, Kelly OG, Melton DA (1994) Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77(2):283-295.
34. Hemmati-Brivanlou A, Melton DA (1994) Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell 77(2):273-281.
35. Khokha MK, Yeh J, Grammer TC, Harland RM (2005) Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Dev Cell 8(3):401-411.
36. François V, Bier E (1995) Xenopus chordin and Drosophila short gastrulation genes encode homologous proteins functioning in dorsal-ventral axis formation. Cell 80(1): 19-20.
37. Holley SA, et al. (1995) A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376(6537):249-253.
38. Sasai Y, et al. (1994) Xenopus chordin: A novel dorsalizing factor activated by organizer- specific homeobox genes. Cell 79(5):779-790.
39. Rentzsch F, Guder C, Vocke D, Hobmayer B, Holstein TW (2007) An ancient chordinlike gene in organizer formation of Hydra. Proc Natl Acad Sci USA 104(9):3249-3254.
40. Eisenhoffer GT, Kang H, Sánchez Alvarado A (2008) Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 3(3):327-339.
41. Wagner DE, Ho JJ, Reddien PW (2012) Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 10(3): 299-311.
42. Lapan SW, Reddien PW (2011) dlx and sp6-9 control optic cup regeneration in a prototypic eye. PLoS Genet 7(8):e1002226.
43. Mannini L, et al. (2004) Djeyes absent (Djeya) controls prototypic planarian eye regeneration by cooperating with the transcription factor Djsix-1. Dev Biol 269(2): 346-359.
44. Pevny L, Placzek M (2005) SOX genes and neural progenitor identity. Curr Opin Neurobiol 15(1):7-13.
45. Mizuseki K, Kishi M, Shiota K, Nakanishi S, Sasai Y (1998) SoxD: An essential mediator of induction of anterior neural tissues in Xenopus embryos. Neuron 21(1):77-85.
46. Crémazy F, Berta P, Girard F (2000) Sox neuro, a new Drosophila Sox gene expressed in the developing central nervous system. Mech Dev 93(1-2):215-219.
47. Mizuseki K, Kishi M, Matsui M, Nakanishi S, Sasai Y (1998) Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development 125(4):579-587.
48. Lapan SW, Reddien PW (2012) Transcriptome analysis of the planarian eye identifies ovo as a specific regulator of eye regeneration. Cell Rep 2(2):294-307.
49. Weinstein DC, Hemmati-Brivanlou A (1999) Neural induction. Annu Rev Cell Dev Biol 15:411-433.
50. Cebrià F, Newmark PA (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(16):3691-3703.
51. Rouhana L, Vieira AP, Roberts-Galbraith RH, Newmark PA (2012) PRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells. Development 139(6):1083-1094.
52. Collins JJ III, et al. (2010) Genome-wide analyses reveal a role for peptide hormones in planarian germline development. PLoS Biol 8(10):e1000509.
53. Pearson BJ, et al. (2009) Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn 238(2):443-450.
54. Miller CM, Newmark PA (2012) An insulin-like peptide regulates size and adult stem cells in planarians. Int J Dev Biol 56(1-3):75-82.