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The Wnt code: cnidarians signal the way
Abstract
Cnidarians are the simplest metazoans with a nervous system. They are well known for their regeneration capacity, which is based on the restoration of a signalling centre (organizer). Recent work has identified the canonical Wnt pathway in the freshwater polyp Hydra, where it acts in organizer formation and regeneration. Wnt signalling is also essential for cnidarian embryogenesis. In the sea anemone Nematostella vectensis 11 of the 12 known wnt gene subfamilies were identified. Different wnt genes exhibit serial and overlapping expression domains along the oral-aboral axis of the embryo (the 'wnt code'). This is reminiscent of the hox code (cluster) in bilaterian embryogenesis that is, however, absent in cnidarians. It is proposed that the common ancestor of cnidarians and bilaterians invented a set of wnt genes that patterned the ancient main body axis. Major antagonists of Wnt ligands (e.g. Dkk 1/2/4) that were previously known only from chordates, are also present in cnidarians and exhibit a similar conserved function. The unexpectedly high level of genetic complexity of wnt genes evolved in early multi-cellular animals about 650 Myr ago and suggests a radical expansion of the genetic repertoire, concurrent with the evolution of multi-cellularity and the diversification of eumetazoan body plans.
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“or even the formation of multiple polyp heads52.”
From Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis (2014) · cites this paper as [52]
Citations
Cites
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Cited by
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“Notably, a remarkably diverse Wnt repertoire is already present in Cnidarians, an ancient metazoan phylum that includes fresh water polyps and sea anemones (Guder et al., 2006).”
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BackgroundResultInfluentialSclerostin and Dickkopf-1 as Therapeutic Targets in Bone Diseases
Ke, H. Z., Richards, W. G., Li, X., & Ominsky, M. S. (2012) · Endocrine Reviews · doi:10.1210/er.2011-1060 · Cited by 409
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“The human genome has 13 subfamilies of Wnt signaling proteins that can be recognized by protein sequence similarities (Guder et al., 2006).”
Multiple Wnts are involved in Hydra organizer formation and regeneration
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Self-citationNiehrs, C. (2010) · Development · doi:10.1242/dev.039651 · Cited by 283
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BackgroundInfluentialRiesgo, A., Farrar, N., Windsor, P. J., Giribet, G., & Leys, S. P. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu057 · Cited by 266
“Notably, however, in Dictyostelium, the signaling system involved in forming fruiting bodies contains several elements considered to be critical for Wnt signaling: Fz receptors, GSK3 , and -catenin homologs (called GSKA and aardvark in this organism) and a dkk (Guder et al. 2006; Harwood 2008).”
BackgroundEvolutionary crossroads in developmental biology: Cnidaria
Technau, U., & Steele, R. E. (2011) · Development · doi:10.1242/dev.048959 · Cited by 274
Alternative Wnt Pathways and ReceptorsPreprint
van Amerongen, R. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a007914 · Cited by 224
“At the tissue level, the response is ultimately controlled by a “Wnt code” or “Wnt landscape” that integrates the complex expression patterns and different signaling inputs of multiple Wnt ligands and (ant)agonists (Gleason et al. 2006; Guder et al. 2006; Green et al. 2008; Zinovyeva et al. 2008; van Amerongen and Nus…”
BackgroundThe Evolution of the Wnt PathwayPreprint
Holstein, T. W. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a007922 · Cited by 222
“Because b-catenin and Wnt3 act in an autoregulatory loop, a gradient of Wnt3 will result in a graded distribution of nuclear b-catenin along the body column (Guder et al. 2006a).”
BackgroundMethodInfluentialSelf-citationCnidarians and the evolutionary origin of the nervous system
Watanabe, H., Fujisawa, T., & Holstein, T. W. (2009) · Development, Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01103.x · Cited by 206
Self-citationMii, Y., & Taira, M. (2009) · Development · doi:10.1242/dev.032524 · Cited by 205
“Although Drosophila does not have sFRP genes, at least one has been found in the Nematostella genome (Guder et al., 2006), suggesting that the regulatory interactions between sFRP and Wnt existed in the ancestral eumetazoan.”
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“However, the evolution of posterior Wnt signalling has likely been complex in bilaterians, for example, Wnt8 is not expressed at this location in annelids and therefore its role must be played by one or several other Wnts ligands in these animals.”
BackgroundInfluentialOrigins of neurogenesis, a cnidarian view
Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., & Chera, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.563 · Cited by 168
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“…Wnts expressed at the oral pole, and that of fast-diffusing inhibitors perhaps by antagonists of the sFRP and Dickkopf families, gene sequences for which are found in the Nematostella and Hydra genomes (Guder et al., 2006a; Guder et al., 2006b; Lee et al., 2006) and in our Clytia EST collections.”
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Self-citationRandall, C. J., & Szmant, A. M. (2009) · Biological Bulletin · doi:10.1086/bblv217n3p269 · Cited by 154
Medusozoan genomes inform the evolution of the jellyfish body plan
Khalturin, K., Shinzato, C., Khalturina, M., Hamada, M., Fujie, M., Koyanagi, R., Kanda, M., Goto, H., Anton‐Erxleben, F., Toyokawa, M., et al. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-0853-y · Cited by 135
Pre-bilaterian origin of the blastoporal axial organizer
Kraus, Y., Aman, A., Technau, U., & Genikhovich, G. (2016) · Nature Communications · doi:10.1038/ncomms11694 · Cited by 143
WLS Retrograde Transport to the Endoplasmic Reticulum during Wnt Secretion
Yu, J., Chia, J., Canning, C. A., Jones, C. M., Bard, F., & Virshup, D. M. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.03.016 · Cited by 143
“Initially identified in genetic screens, WLS encodes a multipass transmembrane protein that is evolutionarily conserved in metazoans from cnidarians to C. elegans to human (Bänziger et al., 2006; Bartscherer et al., 2006; Goodman et al., 2006; Guder et al., 2006).”
BackgroundLeininger, S., Adamski, M., Bergum, B., Guder, C., Liu, J., Laplante, M., Bråte, J., Hoffmann, F., Fortunato, S., Jordal, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4905 · Cited by 136
Self-citationHow do they do Wnt they do?: regulation of transcription by the Wnt/β‐catenin pathway
Archbold, H. C., Yang, Y., Chen, L., & Cadigan, K. M. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02293.x · Cited by 149
“When one considers that the oral pole of cnidarians likely corresponds to the posterior end of the body plan (Meinhardt 2002, Guder et al. 2006, Niehrs 2010), it appears that the role of high levels of Wnt/b-catenin signalling in promoting posterior identity may be very ancient and predate the…”
BackgroundEarly development and axis specification in the sea anemone Nematostella vectensis
Fritzenwanker, J. H., Genikhovich, G., Kraus, Y. A., & Technau, U. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.07.029 · Cited by 140
CBP/p300 are bimodal regulators of Wnt signaling
Li, J., Sutter, C., Parker, D. S., Blauwkamp, T. A., Fang, M., & Cadigan, K. M. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601667 · Cited by 141
“The Wnt/b-catenin (b-cat) pathway is a signaling cascade that is highly conserved from cnidarians to humans (Cadigan and Nusse, 1997; Guder et al, 2006).”
BackgroundHydra and the evolution of stem cells
Bosch, T. C. G. (2009) · BioEssays · doi:10.1002/bies.200800183 · Cited by 140
Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer
Nakamura, Y., Tsiairis, C. D., Özbek, S., & Holstein, T. W. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018109108 · Cited by 134
“An autoregulatory positive feedback loop of Wnt/β-catenin signaling has been previously suggested to control HyWnt3 expression (5, 6, 14).”
BackgroundMethodSelf-citationKhalturin, K., Anton-Erxleben, F., Milde, S., Plötz, C., Wittlieb, J., Hemmrich, G., & Bosch, T. C. G. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.06.013 · Cited by 125
“Of particular significance was the observation that Wnt and Notch, which are known to be required for controlling stem cells in vertebrates and insects (Mikels and Nusse, 2006; Guder et al., 2006; Bejsovec, 2006; Clevers, 2006; Bray, 2006, Chiba, 2006), appear to mediate the integration of extrinsic signals from the m…”
Clytia hemisphaerica: a jellyfish cousin joins the laboratory
Houliston, E., Momose, T., & Manuel, M. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.01.008 · Cited by 128
On the evolution of bilaterality
Genikhovich, G., & Technau, U. (2017) · Development · doi:10.1242/dev.141507 · Cited by 118
Early evolution of symmetry and polarity in metazoan body plans
Manuel, M. (2008) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2008.07.009 · Cited by 123
“We are thus reverting to the hypothesis, consistent with the swimming direction of bilaterian divergence [84,109,112] In the sea anemone, most of these Wnt genes are first expressed around the blastopore, and later on at the planula stage they become expressed along the oral–aboral axis, in…”
BackgroundResultEn1 and Wnt signaling in midbrain dopaminergic neuronal development
dos Santos, M. T. A., & Smidt, M. P. (2011) · Neural Development · doi:10.1186/1749-8104-6-23 · Cited by 116
“Wnt gene diversity is also observed in other animals like Drosophila, Caenorhabditis elegans and Xenopus, as well as in the ancient metazoan phylum Cnidarians [109], showing not only that Wnts are evolutionarily conserved but that Wnt gene diversity arose early in evolution and is in itself required for successful ani…”
BackgroundSawa, H., & Korswagen, H. C. (2013) · WormBook · doi:10.1895/wormbook.1.7.2 · Cited by 105
“It has been proposed that this staggered expression provides an ancestral mechanism for providing positional identity along the primary body axis (Guder et al., 2006; Martin and Kimelman, 2009) and an interesting possibility is that such a Wnt code is also important in providing positional information during C.”
Harterink, M., Kim, D. H., Middelkoop, T. C., Doan, T. D., van Oudenaarden, A., & Korswagen, H. C. (2011) · Development · doi:10.1242/dev.064733 · Cited by 112
“Phylogenetic analysis has shown that the SFRP family appeared very early in metazoan evolution, as clear SFRP orthologs are already present in the cnidarians Hydra and Nematostella vectensis (Guder et al., 2006a).”
BackgroundResultInfluentialDarras, S., Gerhart, J. C., Terasaki, M. R., Kirschner, M. W., & Lowe, C. J. (2011) · Development · doi:10.1242/dev.059493 · Cited by 107
“A similar activity has been shown during regeneration and homeostasis of adult body plan in planarians (Gurley et al., 2008; Iglesias et al., 2008; Petersen and Reddien, 2008) and cnidarians (Hydra) (Broun et al., 2005; Guder et al., 2006b; Hobmayer et al., 2000; Lengfeld et al., 2009).”
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“Phylogenetic analysis of vertebrate sfrp genes including newly found paralogues To understand how sfrp genes evolved with wnt genes, we refer here to the evolutional origin of sfrp genes (see reviews [Guder et al. 2006; Lee et al. 2006b] for the evolution of wnt genes).”
BackgroundThe origin and evolution of Wnt signalling
Holzem, M., Boutros, M., & Holstein, T. W. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00699-w · Cited by 110
“In Cnidaria, the so called ‘Wnt code’ has been described, which is governed by a Wnt signalling centre at the posterior end of the body axis 129 .”
Self-citationCell plasticity in homeostasis and regeneration
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“Indeed epithelial cells were shown to produce signaling molecules and epitheliopeptides involved in morphogenesis (Fujisawa, 2003; Guder et al., 2006; Lengfeld et al., 2009).”
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Watanabe, H., Hoang, V. T., Mättner, R. A., & Holstein, T. W. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.09.008 · Cited by 98
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Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis
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Self-citationPhylogenetic evidence for the modular evolution of metazoan signalling pathways
Babonis, L. S., & Martindale, M. Q. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0477 · Cited by 91
Frizzled7: A Promising Achilles’ Heel for Targeting the Wnt Receptor Complex to Treat Cancer
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“Wnt signalling in axial regeneration is also implicated in both Hydractinia (Teo et al. 2006; Duffy et al. 2010) and Hydra (Hobmayer et al. 2000; Broun et al. 2005; Guder et al. 2006; Lengfeld et al. 2009).”
BackgroundReconsidering regeneration in metazoans: an evo-devo approach
Tiozzo, S., & Copley, R. R. (2015) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2015.00067 · Cited by 87
“It has been shown that Wnts for example, coordinate tissue dedifferentiation and also tune progenitor cells during structure regeneration in cnidarians, planarian, amphibians and teleosts (Guder et al., 2006; Reddien, 2011; Jager et al., 2013; Lin et al., 2013; Wehner et al., 2014).”
BackgroundA two‐step process in the emergence of neurogenesis
Galliot, B., & Quiquand, M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07829.x · Cited by 77
Modeling pattern formation in hydra: a route to understanding essential steps in development
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“In hydra, Dkk1/2/4 has a graded distribution over the body column, excluding, however, the region where b-catenin is expressed (Augustin et al., 2006; Guder et al., 2006b; Fig.”
BackgroundAnteroposterior axis patterning by early canonical Wnt signaling during hemichordate development
Darras, S., Fritzenwanker, J. H., Uhlinger, K. R., Farrelly, E. R., Pani, A. M., Hurley, I. A., Norris, R. P., Osovitz, M., Terasaki, M., Wu, M., et al. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2003698 · Cited by 75
How animals get their skin patterns: fish pigment pattern as a live Turing wave
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“(Bode, 2003; Guder et al., 2006; Wolpert et al., 1971) When a planarian is cut into pieces, the complete structure is regenerated from each piece(Agata et al., 2007; Best and Morita, 1982), suggesting that there is no fixed origin of a “morphogen.””
Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation
DuBuc, T. Q., Stephenson, T. B., Rock, A. Q., & Martindale, M. Q. (2018) · Nature Communications · doi:10.1038/s41467-018-04184-x · Cited by 73
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“The genetic mechanisms underlying colony growth are poorly understood, but cnidarian genomes are known to contain many of the key genes expressed during coordinated development of bilaterians, such as Hox/ParaHox [9], Hedgehog [10], Wnt [11-13], TGFß/BMP [14,15], Notch [16,17] and other developmental signaling pathways”
BackgroundEvolutionary crossroads in developmental biology
Patel, N. H. (2012) · Development · doi:10.1242/dev.085464 · Cited by 77
Yu, J., & Virshup, D. M. (2014) · Bioscience Reports · doi:10.1042/bsr20140119 · Cited by 72
β-Catenin acts in a position-independent regeneration response in the simple eumetazoan Hydra
Gufler, S., Artes, B., Bielen, H., Krainer, I. M., Eder, M.-K., Falschlunger, J., Bollmann, A., Ostermann, T., Valovka, T., Hartl, M., et al. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.09.005 · Cited by 69
Self-citationJager, M., Dayraud, C., Mialot, A., Quéinnec, É., Guyader, H. L., & Manuel, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0084363 · Cited by 74
“The Wnt centre is posterior in bilaterian embryos [12,13,53], oral/posterior in cnidarian embryos, larvae and adult polyps [4,18,19,21,23,28,54], and posterior in a sponge larva [7,37,55].”
Riddiford, N. J., & Olson, P. D. (2011) · Development Genes and Evolution · doi:10.1007/s00427-011-0370-8 · Cited by 66
“2010) and cnidarians (Guder et al. 2006; Lee et al. 2006; Sullivan et al. 2007), showing that the Wnt gene family is a metazoan innovation (Richards and Degnan 2009).”
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What sponges can tell us about the evolution of developmental processes
Adamska, M., Degnan, B. M., Green, K., & Zwafink, C. (2011) · Zoology · doi:10.1016/j.zool.2010.10.003 · Cited by 65
WNT5B in Physiology and Disease
Suthon, S., Perkins, R. S., Bryja, V., Miranda‐Carboni, G. A., & Krum, S. A. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.667581 · Cited by 72
Yap Promotes Noncanonical Wnt Signals From Cardiomyocytes for Heart Regeneration
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“Pending questions”
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BackgroundActivated cAMP receptors switch encystation into sporulation
Kawabe, Y., Morio, T., James, J. L., Prescott, A. R., Tanaka, Y., & Schaap, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901617106 · Cited by 59
Complex neural architecture in the diploblastic larva of Clava multicornis (Hydrozoa, Cnidaria)
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Wnt signaling in planarians: new answers to old questions
Almuedo‐Castillo, M., Sureda-Gómez, M., & Adell, T. (2012) · The International Journal of Developmental Biology · doi:10.1387/ijdb.113451ma · Cited by 58
Wnt signaling: the good and the bad
Chen, X., Yang, J., Evans, P. M., & Liu, C. (2008) · Acta Biochimica et Biophysica Sinica · doi:10.1111/j.1745-7270.2008.00440.x · Cited by 56
Schaffer, A., Bazarsky, M., Levy, K., Caspi, V. C., & Gat, U. (2016) · BMC Genomics · doi:10.1186/s12864-016-3027-1 · Cited by 62
Trevino, M. A., Stefanik, D. J., Rodriguez, R., Harmon, S., & Burton, P. M. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22774 · Cited by 56
“In Hydra, Wnt signaling promotes oral fates during regeneration, budding, and adult growth (Hobmayer et al., 2000; Broun et al., 2005; Guder et al., 2006; Lengfeld et al., 2009; Gee et al., 2010).”
BackgroundThe role of cnidarian developmental biology in unraveling axis formation and Wnt signaling
Holstein, T. W. (2022) · Developmental Biology · doi:10.1016/j.ydbio.2022.04.005 · Cited by 54
Self-citationWnt evolution and function shuffling in liberal and conservative chordate genomes
Somorjai, I., Martí‐Solans, J., Diaz-Gracia, M., Nishida, H., Imai, K. S., Escrivá, H., Cañestro, C., & Albalat, R. (2018) · Genome biology · doi:10.1186/s13059-018-1468-3 · Cited by 51
Genikhovich, G., & Technau, U. (2009) · Cold Spring Harbor Protocols · doi:10.1101/pdb.emo129 · Cited by 51
Surprisingly rich repertoire of Wnt genes in the demosponge Halisarca dujardini
Borisenko, I., Adamski, M., Ereskovsky, A. V., & Adamska, M. (2016) · BMC Evolutionary Biology · doi:10.1186/s12862-016-0700-6 · Cited by 50
Stem Cells, Patterning and Regeneration in Planarians: Self-Organization at the Organismal Scale
Rink, J. C. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7802-1_2 · Cited by 46
Evolution of Gene Expression across Species and Specialized Zooids in Siphonophora
Munro, C., Zapata, F., Howison, M., Siebert, S., & Dunn, C. W. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac027 · Cited by 46
“Indeed, across all cnidarians examined, Wnt3 has consistent localized expression at the oral pole, likely playing a role in axis formation and maintenance (Hobmayer et al. 2000; Guder et al. 2006; Momose et al. 2008; Nawrocki and Cartwright 2013; Hensel et al. 2014; Sanders and Cartwright 2015; Bagaeva et al. 2019).”
BackgroundA new paradigm for animal symmetry
Holló, G. (2015) · Interface Focus · doi:10.1098/rsfs.2015.0032 · Cited by 53
Temperature and insulin signaling regulate body size in Hydra by the Wnt and TGF-beta pathways
Mortzfeld, B. M., Taubenheim, J., Klimovich, A. V., Fraune, S., Rosenstiel, P. C., & Bosch, T. C. G. (2019) · Nature Communications · doi:10.1038/s41467-019-11136-6 · Cited by 46
Injury-induced MAPK activation triggers body axis formation in Hydra by default Wnt signaling
Tursch, A., Bartsch, N., Mercker, M., Schlüter, J., Lommel, M., Marciniak-Czochra, A. K., Özbek, S., & Holstein, T. W. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204122119 · Cited by 58
Self-citationKunttas‐Tatli, E., Roberts, D. M., & McCartney, B. M. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-04-0885 · Cited by 43
“INTRODUCTION Canonical Wnt signal transduction is an evolutionarily conserved pathway from hydra to humans that plays essential roles in embryonic development and adult tissue maintenance by regulating cellular differentiation, proliferation, and morphogenesis (Logan and Nusse, 2004; Guder et al., 2006).”
BackgroundBlanchoud, S., Rutherford, K., Zondag, L., Gemmell, N. J., & Wilson, M. J. (2018) · Scientific Reports · doi:10.1038/s41598-018-23749-w · Cited by 42
-Catenin-Dependent Wnt Signaling in C. elegans: Teaching an Old Dog a New TrickPreprint
Jackson, B. M., & Eisenmann, D. M. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a007948 · Cited by 44
“This evolutionary conservation suggests that cellular signaling mechanisms functioning in response to Wnts were part of the “developmental toolkit” in place at least 500 million years ago in the common ancestor to modern metazoans (Guder et al. 2006).”
BackgroundMethodInfluentialSignaling Pathways and Axis Formation in the Lower Metazoa
Holstein, T. W., Watanabe, H., & Özbek, S. (2011) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-385975-4.00012-7 · Cited by 44
“…Wnt gradients are not a novelty restricted to chordates or secondarily co-opted in various organisms (De Robertis, 2010; Hejnol and Martindale, 2009; Martindale and Hejnol, 2009), but that they probably represent an ancient feature (Guder et al., 2006a; Niehrs, 2010; Rentzsch et al., 2006, 2007).”
BackgroundInfluentialSelf-citationGruhl, A., & Okamura, B. (2012) · EvoDevo · doi:10.1186/2041-9139-3-10 · Cited by 41
“Recent experimental and gene expression data (especially those based on Wnt/β-catenin signalling) demonstrate that the development of polyps from planulae and of asexual buds is in accord with early morphology-based hypotheses for a homology of the cnidarian oral-aboral axis and the bilaterian anteroposterior axis [33…”
Genomic Variants Among Threatened Acropora Corals
Kitchen, S. A., Ratan, A., Bedoya-Reina, O. C., Burhans, R. C., Fogarty, N. D., Miller, W., & Baums, I. B. (2019) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400125 · Cited by 39
“Candidate Loci in Growth and Development Genes in the Wnt pathway are critical for pattern formation, tissue differentiation in developing embryos and tissue regeneration of Cnidaria (Guder et al. 2006).”
BackgroundWnt/frizzled family members mediate olfactory sensory neuron axon extension
Rodriguez‐Gil, D. J., & Greer, C. A. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21834 · Cited by 41
“The first OSN synapses appear in the OB around E15, but it is not until P21 that synapse formation reaches a peak (Hinds and Hinds, 1976).”
BackgroundRecent advances in genomics and transcriptomics of cnidarians
Technau, U., & Schwaiger, M. (2015) · Marine Genomics · doi:10.1016/j.margen.2015.09.007 · Cited by 38
Sponges as models to study emergence of complex animals
Adamska, M. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.05.026 · Cited by 34
“Expression of the Wnt ligands is almost universally associated with the posterior region of the bilaterians [93,94], while in cnidarians the posterior larval expression persists as apical (hypostomal) expression in polyps [69,95,96].”
BackgroundPosterior Wnts have distinct roles in specification and patterning of the planarian posterior region
Sureda-Gómez, M., Pascual-Carreras, E., & Adell, T. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161125970 · Cited by 32
“In cnidarians, it has been suggested that the patterning of the oral-aboral axis could be established by the cooperation between different Wnts, a “Wnt code”, which would exert the function of the Hox code in bilatelians [26].”
BackgroundThe WTX/AMER1 gene family: evolution, signature and function
Boutet, A., Comai, G., & Schedl, A. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-280 · Cited by 32
“More recently, however, Dkk genes have been described in the diploblastic hydra and sea anemone [9].”
BackgroundHox genes regulate asexual reproductive behavior and tissue segmentation in adult animals
Arnold, C. P., Migueles-Lozano, A., Mann, F. G., Nowotarski, S. H., Haug, J. O., Lange, J. J., Seidel, C. W., & Alvarado, A. S. (2021) · Nature Communications · doi:10.1038/s41467-021-26986-2 · Cited by 30
Evolution of developmental regulation in the vertebrate FgfD subfamily
Jovelin, R., Yan, Y., He, X., Catchen, J., Amores, A., Cañestro, C., Yokoi, H., & Postlethwait, J. H. (2009) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21307 · Cited by 33
“…genomic investigations reveal a surprisingly complete gene set already present in the last common ancestor of all metazoans (Technau et al., 2005; Guder et al., 2006; Nichols et al., 2006; Kasbauer et al., 2007; Matus et al., 2007), but this ancestral toolkit Published online in Wiley…”
Frazier, M., Helmkampf, M., Bellinger, M. R., Geib, S. M., & Takabayashi, M. (2017) · BMC Genomics · doi:10.1186/s12864-017-4090-y · Cited by 29
Dzobo, K., Thomford, N. E., & Senthebane, D. A. (2019) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2019.0147 · Cited by 29
“Wnt genes are conserved in animals, illustrating their importance and specific role that each Wnt signal plays in the development of animals (Guder et al., 2006; Kusserow et al., 2005).”
Harterink, M., & Korswagen, H. C. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02287.x · Cited by 29
“Depletion of Porc leads to a complete block in Wnt secretion and accumulation of Wnt in the ER (van den Heuvel et al. 1993), similar as observed in the murine Wnt3a (S209) mutant.”
BackgroundStumpf, M., Will, B., Wittig, K., Kasper, J., Fischer, B., Schmich, J., Seipp, S., & Leitz, T. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082738ms · Cited by 28
Sanders, S. M., & Cartwright, P. (2015) · Evolution & Development · doi:10.1111/ede.12165 · Cited by 28
“Cnidarian dickkopf (dkk) sequences were mined from both NCBI’s nr protein and Compagen (Hemmrich and Bosch 2008) databases and aligned using ClustalV (Sievers et al. 2011).”
MethodApcdd1 is a dual BMP/Wnt inhibitor in the developing nervous system and skin
Vonica, A., Bhat, N., Phan, K. D., Guo, J., Iancu, L., Weber, J. A., Karger, A., Cain, J. W., Wang, E. C. E., DeStefano, G. M., et al. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.03.015 · Cited by 29
Anton‐Erxleben, F., Thomas, A., Wittlieb, J., Fraune, S., & Bosch, T. C. G. (2009) · Zoology · doi:10.1016/j.zool.2008.09.002 · Cited by 27
Metadata
- Authors
- Guder, C., Philipp, I., Lengfeld, T., Watanabe, H., Hobmayer, B., & Holstein, T. W.
- Affiliations
- Heidelberg University (DE)
- Universität Innsbruck (AT)
- Corresponding author
- Holstein, T W
- Venue
- Oncogene
- Published
- 2006-12-04
- Volume
- 25
- Issue
- 57
- Pages
- 7450-7460
- ISSN
- 0950-9232 (ISSN-L)
- 1476-5594
- OpenAlex
- W1983253019
- Cited by
- 177
- References
- 80
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 4 · 2023: 3 · 2022: 9 · 2021: 8 · 2020: 1 · 2019: 11 · 2018: 9 · 2017: 6 · 2016: 11 · 2015: 8 · 2014: 15 · 2013: 7 · 2012: 14
- FWCI
- 1.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Oncogene (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Keywords
- Wnt signaling, Cnidaria, Nematostella vectensis, Hydra, regeneration, embryonic development, oral-aboral axis, Hox code, body plan evolution, gene family expansion
- MeSH terms
- Animals, Cnidaria, Hydra, Ligands, Models, Biological, Phylogeny, Sea Anemones, Signal Transduction, Evolution, Molecular, Body Patterning, Wnt Proteins, beta Catenin
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