Wnt signaling promotes oral but suppresses aboral structures in Hydractinia metamorphosis and regeneration

Development

Volumn 137, Issue 18, 2010, Pages 3057-3066

  Duffy, David J ^a   Plickert, Günter ^b   Kuenzel, Timo ^b   Tilmann, Wido ^b   Frank, Uri ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Axis formation; Cnidaria; Gonads; Hydractinia; Invertebrate; Metamorphosis; Oocytes; Oogonia; Organizer; Posterior patterning; Regeneration; RNAi; Sperm development; Sperm maturation; Tcf; Wnt; catenin

Indexed keywords

T CELL FACTOR PROTEIN; WNT PROTEIN; WNT3 PROTEIN; BETA CATENIN; BRACHYURY PROTEIN; FETOPROTEIN; T BOX TRANSCRIPTION FACTOR;

ARTICLE; COELENTERATE; DOWN REGULATION; GENE SEQUENCE; HYDRACTINIA ECHINATA; IN SITU HYBRIDIZATION; METAMORPHOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; REAL TIME POLYMERASE CHAIN REACTION; REGENERATION; RNA INTERFERENCE; UPREGULATION; ANATOMY AND HISTOLOGY; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; HYDROZOA; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALIA; CNIDARIA; HYDRACTINIA; INVERTEBRATA;

ANIMALS; BETA CATENIN; FETAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYDROZOA; METAMORPHOSIS, BIOLOGICAL; REGENERATION; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TCF TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 77956563332     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.046631     Document Type: Article

References (41)

1. Alexandrova, O., Schade, M., Bottger, A. and David, C. N. (2005). Oogenesis in Hydra: nurse cells transfer cytoplasm directly to the growing oocyte. Dev. Biol. 281, 91-101.
2. Amiel, A. and Houliston, E. (2009). Three distinct RNA localization mechanisms contribute to oocyte polarity establishment in the cnidarian Clytia hemisphaerica. Dev. Biol. 327, 191-203.
3. Broun, M., Gee, L., Reinhardt, B. and Bode, H. R. (2005). Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132, 2907-2916.
4. Chera, S., Ghila, L., Dobretz, K., Wenger, Y., Bauer, C., Buzgariu, W., Martinou, J.-C. and Galliot, B. (2009). Apoptotic cells provide an unexpected source of Wnt3 signaling to drive Hydra head regeneration. Dev. Cell 17, 279-289.
5. Frank, U., Leitz, T. and Müller, W. A. (2001). The hydroid Hydractinia: a versatile, informative cnidarian representative. BioEssays 23, 963-971.
6. Gajewski, M., Leitz, T., Schloessherr, J. and Plickert, G. (1996). LWamides from Cnidaria constitute a novel family of neuropeptides with morphogenetic activity. Roux's Arch. Dev. Biol. 205, 232-242.
7. Gee, L., Hartig, J., Law, L., Wittlieb, J., Khalturin, K., Bosch, T. C. G. and Bode, H. R. (2010). β-catenin plays a central role in setting up the head organizer in hydra. Dev. Biol. 340, 116-124.
8. Gurley, K. A., Rink, J. C. and Alvarado, A. S. (2008). β-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319, 323-327.
9. Hassel, M., Albert, K. and Hofheinz, S. (1993). Pattern formation in Hydra vulgaris is controlled by lithium-sensitive processes. Dev. Biol. 156, 362-371.
10. Hobmayer, B., Rentzsch, F., Kuhn, K., Happel, C. M., von Laue, C. C., Snyder, P., Rothbächer, U. and Holstein, T. W. (2000). WNT signaling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407, 186-189.
11. Hovanes, K., Li, T. W., Munguia, J. E., Truong, T., Milovanovic, T., Lawrence Marsh, J., Holcombe, R. F. and Waterman, M. L. (2001). β-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat. Genet. 28, 53-57.
12. Iglesias, M., Gomez-Skarmeta, J. L., Saló, E. and Adell, T. (2008). Silencing of Smed-βcatenin1 generates radial-like hypercephalized planarians. Development 135, 1215-1221.
13. Kunick, C., Lauenroth, K., Leost, M., Meijer, L. and Lemcke, T. (2004). 1-Azakenpaullone is a selective inhibitor of glycogen synthase kinase-3beta. Bioorg. Med. Chem. Lett. 14, 413-416.
14. Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., Technau, U., Haeseler, A. V., Hobmayer, B., Martindale, M. Q. et al. (2005). Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433, 156-160.
15. Lee, P. N., Kumburegama, S., Marlow, H. Q., Martindale, M. Q. and Wikramanayake, A. H. (2007). Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. Dev. Biol. 310, 169-186.
16. Lengfeld, T., Watanabe, H., Simakov, O., Lindgens, D., Gee, L., Law, L., Schmidt, H. A., Özbek, S., Bode, H. and Holstein, T. W. (2009). Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev. Biol. 330, 186-199.
17. MacWilliams, H. K. (1983). Hydra transplantation phenomena and the mechanism of Hydra head regeneration: I. properties of the head inhibition. Dev. Biol. 96, 217-238.
18. Mali, B., Soza-Ried, J., Frohme, M. and Frank, U. (2006). Structural but not functional conservation of an immune molecule: a tachylectin-like gene in Hydractinia. Dev. Comp. Immunol. 30, 275.
19. Meinhardt, H. (2002). The radial-symmetric hydra and the evolution of the bilateral body plan: an old body became a young brain. BioEssays 24, 185-191.
20. Meinhardt, H. (2009). Beta-catenin and axis formation in planarians. BioEssays 31, 5-9.
21. Momose, T. and Houliston, E. (2007). Two oppositely localised frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol. 5, e70.
22. Momose, T., Derelle, R. and Houliston, E. (2008). A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 135, 2105-2113.
23. Müller, W. A. (1964). Experimentele Untersuchungen über Stockentwicklung, Polypendifferenzierung und Sexualchimären bei Hydractinia echinata. Roux's Arch. für Entwicklungsmechanik 155, 181-268.
24. Müller, W. A. (1973). Induction of metamorphosis by bacteria and ions in the planulae of Hydractinia echinata; an approach to the mode of action. Publ. Seto. Mar. Biol. Lab. 20 (Proc. 2nd Int. Symp. Cnidaria), 195-208.
25. +-ATPase. Roux's Arch. für Entwicklungsmechanik 173, 122-135.
26. Müller, W. A., Plickert, G. and Berking, S. (1986). Regeneration in Hydrozoa: distal versus proximal transformation in Hydractinia. Roux's Arch. Dev. Biol. 195, 513-518.
27. Müller, W. A., Teo, R. and Frank, U. (2004a). Totipotent migratory stem cells in a hydroid. Dev. Biol. 275, 215-224.
28. Müller, W. A., Teo, R. and Möhrlen, F. (2004b). Patterning a multi-headed mutant in Hydractinia: enhancement of head formation and its phenotypic normalization. Int. J. Dev. Biol. 48, 9-15.
29. Müller, W. A., Frank, U., Teo, R., Mokady, O., Gütte, C. and Plickert, G. (2007). Wnt signaling in hydroid development: ectopic heads and giant buds induced by GSK-3 inhibitors. Int. J. Dev. Biol. 51, 211-220.
30. Niehrs, C. (2010). On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137, 845-857.
31. Petersen, C. P. and Reddien, P. W. (2008). Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319, 327-330.
32. Petersen, C. P. and Reddien, P. W. (2009). Wnt signaling and the polarity of the primary body axis. Cell 139, 1056-1068.
33. Plickert, G., Schetter, E., Verhey-van-Wijk, N., Schlossherr, J., Steinbüchel, M. and Gajewski, M. (2003). The role of a-amidated neuropeptides in hydroid development-LWamides and metamorphosis in Hydractinia echinata. Int. J. Dev. Biol. 47, 439-450.
34. Plickert, G., Jacoby, V., Frank, U., Müller, W. A. and Mokady, O. (2006). Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning. Dev. Biol. 298, 368-378.
35. Rebscher, N., Volk, C., Teo, R. and Plickert, G. (2008). The germ plasm component Vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata. Dev. Dyn. 237, 1736-1745.
36. Seipp, S., Schmich, J., Kehrwald, T. and Leitz, T. (2007). Metamorphosis of Hydractinia echinata - natural versus artificial induction and developmental plasticity. Dev. Genes Evol. 217, 385-394.
37. Stover, N. A. and Steele, R. E. (2001). Trans-spliced leader addition to mRNAs in a cnidarian. Proc. Natl. Acad. Sci. USA 98, 5693-5698.
38. Tanaka, E. M. and Weidinger, G. (2008). Heads or tails: can Wnt tell which one is up? Nat. Cell Biol. 10, 122-124.
39. Teo, R., Möhrlen, F., Plickert, G., Müller, W. A. and Frank, U. (2006). An evolutionary conserved role of Wnt-signaling in stem cell fate decision. Dev. Biol. 289, 91-99.
40. Wikramanayake, A. H., Hong, M., Lee, P. N., Pang, K., Byrum, C. A., Bince, J. M., Xu, R. and Martindale, M. Q. (2003). An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation. Nature 426, 446-450.
41. Yamaguchi, T. P., Takada, S., Yoshikawa, Y., Wu, N. and McMahon, A. P. (1999). T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 13, 3185-3190.