Abstract
The Wnt/β-catenin pathway plays an important role in axis formation and axial patterning during metazoan development. Wnt genes are expressed around the blastopore of prebilaterian and bilaterian embryos and create a gradient of ligands governing the primary oral-aboral body axis. Although this polarised Wnt signalling along a primary body axis is a conserved property of metazoan development, the mechanisms governing localised Wnt expression and secretion are poorly understood. We study these questions in the freshwater polyp Hydra, a classical model system for the analysis of morphogenetic gradients and modelling of de novo pattern formation processes. New data emphasise the importance of gene regulatory networks for the formation of Wnt secreting signalling centres. It is proposed that a twist of transcriptional control and gradient formation was essential for the formation of Wnt signalling centres in metazoan axis formation.
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Holstein TW (2012) The evolution of the Wnt pathway. Cold Spring Harb Perspect Biol (in press, doi: 10.1101/cshperspect.a007922)
Holstein TW, Watanabe H, Ozbek S (2011) Signaling pathways and axis formation in the lower metazoa. Curr Top Dev Biol 97:137–177
Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang JS, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PR, Zhang X, Aufschnaiter R, Eder MK, Gorny AK, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Bottger A, Tischler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TC, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE (2010) The dynamic genome of Hydra. Nature 464:592–596
Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94
Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M, Schierwater B (2006) Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol 55:97–115
Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, Holstein TW (2005) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433:156–160
Lee PN, Pang K, Matus DQ, Martindale MQ (2006) A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol
Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Ozbek S, Bode H, Holstein TW (2009) Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 330:186–199
Lee PN, Kumburegama S, Marlow HQ, Martindale MQ, Wikramanayake AH (2007) Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. Dev Biol
Momose T, Derelle R, Houliston E (2008) A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 135:2105–2113
Momose T, Houliston E (2007) Two oppositely localised frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol 5:e70
Wikramanayake AH, Hong M, Lee PN, Pang K, Byrum CA, Bince JM, Xu R, Martindale MQ (2003) An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation. Nature 426:446–450
De Robertis EM (2008) Evo-devo: variations on ancestral themes. Cell 132:185–195
Niehrs C (2010) On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137:845–857
Rentzsch F, Guder C, Vocke D, Hobmayer B, Holstein TW (2007) An ancient chordin-like gene in organizer formation of Hydra. Proc Natl Acad Sci U S A 104:3249–3254
Chourrout D, Delsuc F, Chourrout P, Edvardsen RB, Rentzsch F, Renfer E, Jensen MF, Zhu B, de Jong P, Steele RE, Technau U (2006) Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. Nature 442:684–687
Technau U, Steele RE (2011) Evolutionary crossroads in developmental biology: cnidaria. Development
Guder C, Philipp I, Lengfeld T, Watanabe H, Hobmayer B, Holstein TW (2006a) The Wnt code: cnidarians signal the way. Oncogene 25:7450–7460
Guder C, Pinho S, Nacak TG, Schmidt HA, Hobmayer B, Niehrs C, Holstein TW (2006b) An ancient Wnt-Dickkopf antagonism in Hydra. Development 133:901–911
Browne EN (1909) The production of new hydranths in hydra by the insertion of small grafts. J Exp Zool 7:1–37
Meinhardt H (2012) Modeling pattern formation in hydra: a route to understanding essential steps in development. Int J Dev Biol
Technau U, Cramer von Laue C, Rentzsch F, Luft S, Hobmayer B, Bode HR, Holstein TW (2000) Parameters of self-organization in Hydra aggregates. Proc Natl Acad Sci U S A 97:12127–12131
Nakamura Y, Tsiairis CD, Ozbek S, Holstein TW (2011) Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer. Proc Natl Acad Sci U S A 108:9137–9142
Hobmayer B, Rentzsch F, Kuhn K, Happel CM, von Laue CC, Snyder P, Rothbacher U, Holstein TW (2000) WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407:186–189
Philipp I, Aufschnaiter R, Ozbek S, Pontasch S, Jenewein M, Watanabe H, Rentzsch F, Holstein TW, Hobmayer B (2009) Wnt/beta-catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra. Proc Natl Acad Sci U S A 106:4290–4295
Broun M, Gee L, Reinhardt B, Bode HR (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132:2907–2916
Gierer A, Meinhardt H (1972) A theory of biological pattern formation. Kybernetik 12:30–39
Meinhardt H (2004a) Different strategies for midline formation in bilaterians. Nat Rev Neurosci 5:502–510
Meinhardt H (2004b) Models for the generation of the embryonic body axes: ontogenetic and evolutionary aspects. Curr Opin Genet Dev 14:446–454
MacWilliams HK (1983a) Hydra transplantation phenomena and the mechanism of hydra head regeneration. I. Properties of the head inhibition. Dev Biol 96:217–238
MacWilliams HK (1983b) Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of the head activation. Dev Biol 96:239–257
Meinhardt H (1993) A model for pattern formation of hypostome, tentacles, and foot in hydra: how to form structures close to each other, how to form them at a distance. Dev Biol 157:321–333
Gee L, Hartig J, Law L, Wittlieb J, Khalturin K, Bosch TC, Bode HR (2010) Beta-catenin plays a central role in setting up the head organizer in hydra. Dev Biol 340:116–124
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Holstein, T.W. (2013). Gradients and Regulatory Networks of Wnt Signalling in Hydra Pattern Formation. In: Capasso, V., Gromov, M., Harel-Bellan, A., Morozova, N., Pritchard, L. (eds) Pattern Formation in Morphogenesis. Springer Proceedings in Mathematics, vol 15. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20164-6_3
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DOI: https://doi.org/10.1007/978-3-642-20164-6_3
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