The DOI matches its Crossref record; 30 of the 30 references it cites were found in a registry or an index.
Unexpected complexity of the Wnt gene family in a sea anemone
Abstract
The Wnt gene family encodes secreted signalling molecules that control cell fate in animal development and human diseases. Despite its significance, the evolution of this metazoan-specific protein family is unclear. In vertebrates, twelve Wnt subfamilies were defined, of which only six have counterparts in Ecdysozoa (for example, Drosophila and Caenorhabditis). Here, we report the isolation of twelve Wnt genes from the sea anemone Nematostella vectensis, a species representing the basal group within cnidarians. Cnidarians are diploblastic animals and the sister-group to bilaterian metazoans. Phylogenetic analyses of N. vectensis Wnt genes reveal a thus far unpredicted ancestral diversity within the Wnt family. Cnidarians and bilaterians have at least eleven of the twelve known Wnt gene subfamilies in common; five subfamilies appear to be lost in the protostome lineage. Expression patterns of Wnt genes during N. vectensis embryogenesis indicate distinct roles of Wnts in gastrulation, resulting in serial overlapping expression domains along the primary axis of the planula larva. This unexpectedly complex inventory of Wnt family signalling factors evolved in early multi-cellular animals about 650 million years (Myr) ago, predating the Cambrian explosion by at least 100 Myr (refs 5, 8). It emphasizes the crucial function of Wnt genes in the diversification of eumetazoan body plans.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Nematostella has several clusters of homeobox genes (56)(57)(58), but only those on scaffolds 3 and 61 are embedded within the ancestral eumetazoan Hox context, providing independent support for the assignment of these homeobox genes as bona fide Nematostella Hox genes (54,56,59).”
From Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization (2007) · cites this paper as [58]
In the citing paper
“S. purpuratus has WntA, previously reported as being absent from deuterostomes (29).”
From The Genome of the Sea Urchin Strongylocentrotus purpuratus (2006) · cites this paper as [29]
In the citing paper
“These patterns are reminiscent of the nested expression domains of Wnt ligands in the Nematostella embryos 20 .”
From Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans (2014) · cites this paper as [20]
Citations
Cites
Convergence of Wnt, ß-Catenin, and Cadherin Pathways
Nelson, W. J., & Nusse, R. (2004) · Science · doi:10.1126/science.1094291 · Cited by 2,537
The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain
McMahon, A. P., & Bradley, A. (1990) · Cell · doi:10.1016/0092-8674(90)90385-r · Cited by 1,540
WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra
Hobmayer, B., Rentzsch, F., Kuhn, K., Happel, C. M., von Laue, C. C., Snyder, P., Rothbächer, U., & Holstein, T. W. (2000) · Nature · doi:10.1038/35025063 · Cited by 599
Estimating metazoan divergence times with a molecular clock
Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J., & McPeek, M. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401670101 · Cited by 461
Function and evolution of the plant MADS-box gene family
Ng, M., & Yanofsky, M. F. (2001) · Nature Reviews Genetics · doi:10.1038/35056041 · Cited by 438
Hox genes and chordate evolution.
Holland, P., & Garcia-Fernàndez, J. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0034 · Cited by 432
Evolution of Key Cell Signaling and Adhesion Protein Families Predates Animal Origins
King, N., Hittinger, C. T., & Carroll, S. B. (2003) · Science · doi:10.1126/science.1083853 · Cited by 424
Origins of Bilateral Symmetry: Hox and Dpp Expression in a Sea Anemone
Finnerty, J. R., Pang, K., Burton, P., Paulson, D., & Martindale, M. Q. (2004) · Science · doi:10.1126/science.1091946 · Cited by 407
Self-citationMartindale, M. Q., Pang, K., & Finnerty, J. R. (2004) · Development · doi:10.1242/dev.01119 · Cited by 396
Self-citationChristian, J. L., McMahon, J. A., McMahon, A. P., & Moon, R. T. (1991) · Development · doi:10.1242/dev.111.4.1045 · Cited by 374
Research works printed but not linked: 2
- Bridge D., 1995, Mol. Biol. Evol., 12, 679
- Technau U., 2003, Int. J. Dev. Biol., 47, 531
Cited by
Sorted by citations
Wnt/β-Catenin Signaling in Development and Disease
Clevers, H. (2006) · Cell · doi:10.1016/j.cell.2006.10.018 · Cited by 5,568
Wnt/β-catenin signaling and disease
Clevers, H., & Nusse, R. (2012) · Cell · doi:10.1016/j.cell.2012.05.012 · Cited by 5,554
Wnt/β-Catenin Signaling, Disease, and Emerging Therapeutic Modalities
Nusse, R., & Clevers, H. (2017) · Cell · doi:10.1016/j.cell.2017.05.016 · Cited by 4,342
Wnt/β-catenin signalling: function, biological mechanisms, and therapeutic opportunities
Liu, J., Xiao, Q., Xiao, J., Niu, C., Li, Y., Zhang, X., Zhou, Z., Shu, G., & Yin, G. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00762-6 · Cited by 2,519
Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution
Carroll, S. B. (2008) · Cell · doi:10.1016/j.cell.2008.06.030 · Cited by 2,067
Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555
Self-citationThe many faces and functions of β‐catenin
Valenta, T., Hausmann, G., & Basler, K. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.150 · Cited by 1,598
Wnt Signaling: Multiple Pathways, Multiple Receptors, and Multiple Transcription Factors
Gordon, M. D., & Nusse, R. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.r600015200 · Cited by 1,333
Towards an integrated view of Wnt signaling in development
van Amerongen, R., & Nusse, R. (2009) · Development · doi:10.1242/dev.033910 · Cited by 1,213
The Genome of the Sea Urchin Strongylocentrotus purpuratus
Sodergren, E., Weinstock, G. M., Davidson, E. H., Cameron, R. A., Gibbs, R. A., Angerer, R. C., Angerer, L. M., Arnone, M. I., Burgess, D. R., Burke, R. D., et al. (2006) · Science · doi:10.1126/science.1133609 · Cited by 1,132
Evolution at Two Levels: On Genes and Form
Carroll, S. B. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030245 · Cited by 882
Albalat, R., & Cañestro, C. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.39 · Cited by 775
Xie, H. M., Vučetić, S., Iakoucheva, L. M., Oldfield, C. J., Dunker, A. K., Uversky, V. N., & Zoran Obradovic, A. (2007) · Journal of Proteome Research · doi:10.1021/pr060392u · Cited by 572
Wnt Signaling and the Polarity of the Primary Body Axis
Petersen, C. P., & Reddien, P. W. (2009) · Cell · doi:10.1016/j.cell.2009.11.035 · Cited by 544
The deep evolution of metazoan microRNAs
Wheeler, B. M., Heimberg, A. M., Moy, V. N., Sperling, E. A., Holstein, T. W., Heber, S., & Peterson, K. J. (2009) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00302.x · Cited by 534
Self-citationComparative Aspects of Animal Regeneration
Brockes, J. P., & Kumar, A. (2008) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.24.110707.175336 · Cited by 491
More than just orphans: are taxonomically-restricted genes important in evolution?
Khalturin, K., Hemmrich, G., Fraune, S., Augustin, R., & Bosch, T. C. G. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.07.006 · Cited by 426
Three decades of Wnts: a personal perspective on how a scientific field developed
Nusse, R., & VARMUS, H. E. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.146 · Cited by 427
Alternative Wnt Signaling Is Initiated by Distinct Receptors
van Amerongen, R., Mikels, A. J., & Nusse, R. (2008) · Science Signaling · doi:10.1126/scisignal.135re9 · Cited by 408
The innate immune repertoire in Cnidaria - ancestral complexity and stochastic gene loss
Miller, D. J., Hemmrich, G., Ball, E. E., Hayward, D. C., Khalturin, K., Funayama, N., Agata, K., & Bosch, T. C. G. (2007) · Genome biology · doi:10.1186/gb-2007-8-4-r59 · Cited by 395
Wnt/β-catenin signaling pathway in carcinogenesis and cancer therapy
Song, P., Gao, Z., Bao, Y., Chen, L., Huang, Y., Liu, Y., Dong, Q., & Wei, X. (2024) · Journal of Hematology & Oncology · doi:10.1186/s13045-024-01563-4 · Cited by 382
Smed- β catenin-1 Is Required for Anteroposterior Blastema Polarity in Planarian Regeneration
Petersen, C. P., & Reddien, P. W. (2008) · Science · doi:10.1126/science.1149943 · Cited by 364
Mesodermal Wnt2b signalling positively regulates liver specification
Ober, E. A., Verkade, H. M., Field, H. A., & Stainier, D. Y. R. (2006) · Nature · doi:10.1038/nature04888 · Cited by 354
Reconstructing immune phylogeny: new perspectives
Litman, G. W., Cannon, J. P., & Dishaw, L. J. (2005) · Nature reviews. Immunology · doi:10.1038/nri1712 · Cited by 352
WNT Signaling in Cardiac and Vascular Disease
Foulquier, S., Daskalopoulos, E. P., Lluri, G., Hermans, K. C. M., Deb, A., & Blankesteijn, W. M. (2017) · Pharmacological Reviews · doi:10.1124/pr.117.013896 · Cited by 350
Loh, K. M., van Amerongen, R., & Nusse, R. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.011 · Cited by 335
Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians
Technau, U., Rudd, S., Maxwell, P., Gordon, P. M. K., Saina, M., Grasso, L. C., Hayward, D. C., Sensen, C. W., Saint, R., Holstein, T. W., et al. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.09.007 · Cited by 337
Self-citationEvo-Devo: Variations on Ancestral Themes
Robertis, E. M. D. (2008) · Cell · doi:10.1016/j.cell.2008.01.003 · Cited by 350
Early evolution of animal cell signaling and adhesion genes
Nichols, S., Dirks, W., Pearse, J. S., & King, N. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604065103 · Cited by 330
Neuronal Transcriptome of Aplysia: Neuronal Compartments and Circuitry
Moroz, L. L., Edwards, J. R., Puthanveettil, S. V., Kohn, A. B., Ha, T. J., Heyland, A., Knudsen, B., Sahni, A., Yu, F., Liu, L., et al. (2006) · Cell · doi:10.1016/j.cell.2006.09.052 · Cited by 330
Rokas, A., & Carroll, S. B. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040352 · Cited by 315
The Origins of Multicellularity and the Early History of the Genetic Toolkit For Animal Development
Rokas, A. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091513 · Cited by 312
Sempere, L. F., Cole, C. N., McPeek, M. A., & Peterson, K. J. (2006) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21118 · Cited by 312
Multiple Wnts are involved in Hydra organizer formation and regeneration
Lengfeld, T., Watanabe, H., Simakov, O., Lindgens, D., Gee, L., Law, L. Y., Schmidt, H. A., Özbek, S., Bode, H. R., & Holstein, T. W. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.02.004 · Cited by 300
Self-citationTransgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis
Wittlieb, J., Khalturin, K., Lohmann, J. U., Anton‐Erxleben, F., & Bosch, T. C. G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510163103 · Cited by 298
From nerve net to nerve ring, nerve cord and brain — evolution of the nervous system
Arendt, D., Tosches, M. A., & Marlow, H. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.15 · Cited by 279
Niehrs, C. (2010) · Development · doi:10.1242/dev.039651 · Cited by 283
Higher-level metazoan relationships: recent progress and remaining questions
Edgecombe, G. D., Giribet, G., Dunn, C. W., Hejnol, A., Kristensen, R. M., Neves, R. C., Rouse, G. W., Worsaae, K., & Sørensen, M. V. (2011) · Organisms Diversity & Evolution · doi:10.1007/s13127-011-0044-4 · Cited by 290
The Ancestral Developmental Tool Kit of Land Plants
Floyd, S. K., & Bowman, J. L. (2006) · International Journal of Plant Sciences · doi:10.1086/509079 · Cited by 292
Simionato, E., Ledent, V., Richards, G. S., Thomas‐Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M., & Vervoort, M. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-33 · Cited by 292
Genesis and Expansion of Metazoan Transcription Factor Gene Classes
Larroux, C., Luke, G. N., Koopman, P. A., Rokhsar, D. S., Shimeld, S. M., & Degnan, B. M. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn047 · Cited by 280
Evolutionary crossroads in developmental biology: Cnidaria
Technau, U., & Steele, R. E. (2011) · Development · doi:10.1242/dev.048959 · Cited by 274
Self-citationA Phylogenomic Investigation into the Origin of Metazoa
Ruiz‐Trillo, I., Roger, A. J., Burger, G., Gray, M. W., & Lang, B. F. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn006 · Cited by 270
Adamska, M., Degnan, S. M., Green, K. M., Adamski, M., Craigie, A., Larroux, C., & Degnan, B. M. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001031 · Cited by 257
Vertebrate-Type Intron-Rich Genes in the Marine Annelid Platynereis dumerilii
Raible, F., Tessmar-Raible, K., Osoegawa, K., Wincker, P., Jubin, C., Balavoine, G., Ferrier, D., Benes, V., de Jong, P., Weissenbach, J., et al. (2005) · Science · doi:10.1126/science.1119089 · Cited by 257
Axial patterning in cephalochordates and the evolution of the organizer
Yu, J., Satou, Y., Holland, N. D., Shin‐I, T., Kohara, Y., Satoh, N., Bronner-Fraser, M. E., & Holland, L. Z. (2007) · Nature · doi:10.1038/nature05472 · Cited by 256
Anatomy and development of the nervous system of Nematostella vectensis , an anthozoan cnidarian
Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D., & Martindale, M. Q. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20698 · Cited by 247
Self-citationRyan, J. F., Mazza, M. E., Pang, K., Matus, D. Q., Baxevanis, A. D., Martindale, M. Q., & Finnerty, J. R. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000153 · Cited by 244
Self-citationMolecular evidence for deep evolutionary roots of bilaterality in animal development
Matus, D. Q., Pang, K., Marlow, H. Q., Dunn, C. W., Thomsen, G. H., & Martindale, M. Q. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601257103 · Cited by 227
Self-citationRussell, J. J., Theriot, J. A., Sood, P., Marshall, W. F., Landweber, L. F., Fritz‐Laylin, L. K., Polka, J., Oliferenko, S., Gerbich, T. M., Gladfelter, A. S., et al. (2017) · BMC Biology · doi:10.1186/s12915-017-0391-5 · Cited by 236
Wnt5a can both activate and repress Wnt/β-catenin signaling during mouse embryonic development
van Amerongen, R., Fuerer, C., Mizutani, M., & Nusse, R. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.06.020 · Cited by 226
Gurley, K. A., Elliott, S. A., Simakov, O., Schmidt, H. A., Holstein, T. W., & Alvarado, A. S. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.08.007 · Cited by 212
Self-citationModels of Biological Pattern Formation: From Elementary Steps to the Organization of Embryonic Axes
Meinhardt, H. (2007) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(07)81001-5 · Cited by 219
The Evolution of the Wnt PathwayPreprint
Holstein, T. W. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a007922 · Cited by 222
Self-citationLarval body patterning and apical organs are conserved in animal evolution
Marlow, H. Q., Tosches, M. A., Tomer, R., Steinmetz, P. R. H., Lauri, A., Larsson, T., & Arendt, D. (2014) · BMC Biology · doi:10.1186/1741-7007-12-7 · Cited by 207
The evolution of metazoan axial properties
Martindale, M. Q. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1725 · Cited by 204
Self-citationExceptionally Preserved Jellyfishes from the Middle Cambrian
Cartwright, P., Halgedahl, S. L., Hendricks, J. R., Jarrard, R. D., Marques, A. C., Collins, A. G., & Lieberman, B. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001121 · Cited by 210
Origins and Evolution of Spliceosomal Introns
Rodríguez-Trelles, F., Tarrío, R., & Ayala, F. J. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090625 · Cited by 199
TGF-β and WNT signaling pathways in cardiac fibrosis: non-coding RNAs come into focus
Yousefi, F., Shabaninejad, Z., Vakili, S., Derakhshan, M., Movahedpour, A., Dabiri, H., Ghasemi, Y., Mahjoubin‐Tehran, M., Nikoozadeh, A., Savardashtaki, A., et al. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00555-4 · Cited by 201
Evolutionary conservation of the eumetazoan gene regulatory landscapePreprint
Schwaiger, M., Schönauer, A., Rendeiro, A. F., Pribitzer, C., Schauer, A., Gilles, A. F., Schinko, J. B., Renfer, E., Fredman, D., & Technau, U. (2014) · Genome Research · doi:10.1101/gr.162529.113 · Cited by 191
Self-citationRodríguez‐Lanetty, M., Phillips, W., & Weis, V. M. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-23 · Cited by 190
Amoutzias, G. D., Véron, A. S., Weiner, J. M., Robinson‐Rechavi, M., Bornberg‐Bauer, E., Oliver, S. G., & Robertson, D. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl211 · Cited by 190
A WNT of things to come: Evolution of Wnt signaling and polarity in cnidarians
LEE, P., PANG, K., Matus, D. Q., & Martindale, M. Q. (2006) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2006.05.002 · Cited by 180
Self-citationRyan, J. F., Burton, P. M., Mazza, M. E., Kwong, G. K., Mullikin, J. C., & Finnerty, J. R. (2006) · Genome biology · doi:10.1186/gb-2006-7-7-r64 · Cited by 188
The WNT signaling pathways in wound healing and fibrosis
Burgy, O., & Königshoff, M. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.03.017 · Cited by 175
Croce, J. C., & McClay, D. R. (2008) · Methods in molecular biology · doi:10.1007/978-1-60327-469-2_1 · Cited by 186
The Wnt code: cnidarians signal the way
Guder, C., Philipp, I., Lengfeld, T., Watanabe, H., Hobmayer, B., & Holstein, T. W. (2006) · Oncogene · doi:10.1038/sj.onc.1210052 · Cited by 177
Self-citationEvolution of striated muscle: Jellyfish and the origin of triploblasty
Seipel, K., & Schmid, V. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.03.032 · Cited by 172
Janßen, R., Gouar, M. L., Pechmann, M., Poulin, F., Bolognesi, R., Schwager, E. E., Hopfen, C., Colbourne, J. K., Budd, G. E., Brown, S. J., et al. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-374 · Cited by 178
Origins 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
FGF signalling controls formation of the apical sensory organ in the cnidarianNematostella vectensis
Rentzsch, F., Fritzenwanker, J. H., Scholz, C. B., & Technau, U. (2008) · Development · doi:10.1242/dev.020784 · Cited by 166
Self-citationAn ancient Wnt-Dickkopf antagonism inHydra
Guder, C., Pinho, S., Nacak, T. G., Schmidt, H. A., Hobmayer, B., Niehrs, C., & Holstein, T. W. (2006) · Development · doi:10.1242/dev.02265 · Cited by 168
Self-citationMomose, T., Derelle, R., & Houliston, E. (2008) · Development · doi:10.1242/dev.021543 · Cited by 170
Rentzsch, F., Anton, R., Saina, M., Hammerschmidt, M., Holstein, T. W., & Technau, U. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.06.003 · Cited by 169
Self-citationThe Bilaterian Head Patterning Gene six3/6 Controls Aboral Domain Development in a Cnidarian
Sinigaglia, C., Busengdal, H., Leclère, L., Technau, U., & Rentzsch, F. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001488 · Cited by 169
Self-citationTwo Oppositely Localised Frizzled RNAs as Axis Determinants in a Cnidarian Embryo
Momose, T., & Houliston, E. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050070 · Cited by 163
Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis
Magie, C. R., Pang, K., & Martindale, M. Q. (2005) · Development Genes and Evolution · doi:10.1007/s00427-005-0022-y · Cited by 158
Self-citationHemmrich, G., Khalturin, K., Böhm, A.-M., Puchert, M., Anton‐Erxleben, F., Wittlieb, J., Klostermeier, U. C., Rosenstiel, P. C., Oberg, H., Domazet‐Lošo, T., et al. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss134 · Cited by 159
Schwarz, J. A., Brokstein, P. B., Voolstra, C. R., Terry, A. Y., Miller, D. J., Szmant, A. M., Coffroth, M. A., & Medina, M. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-97 · Cited by 157
Layden, M. J., Rentzsch, F., & Röttinger, É. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.222 · Cited by 148
Philipp, I., Aufschnaiter, R., Özbek, S., Pontasch, S., Jenewein, M., Watanabe, H., Rentzsch, F., Holstein, T. W., & Hobmayer, B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812847106 · Cited by 152
Self-citationEarly origin of the bilaterian developmental toolkit
Erwin, D. H. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0038 · Cited by 158
Randall, C. J., & Szmant, A. M. (2009) · Biological Bulletin · doi:10.1086/bblv217n3p269 · Cited by 154
Patterns of conservation and change in honey bee developmental genesPreprint
Dearden, P. K., Wilson, M. J., Sablan, L., Osborne, P. W., Havler, M., McNaughton, E., Kimura, K., Milshina, N. V., Hasselmann, M., Gempe, T., et al. (2006) · Genome Research · doi:10.1101/gr.5108606 · Cited by 154
Helping Wingless take flight: how WNT proteins are secreted
Hausmann, G., Bänziger, C., & Basler, K. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2141 · Cited by 147
Phylogenetic analysis of CDK and cyclin proteins in premetazoan lineages
Cao, L., Chen, F., Yang, X., Xu, W., Xie, J., & Yu, L. (2014) · BMC Evolutionary Biology · doi:10.1186/1471-2148-14-10 · Cited by 147
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
Self-citationLeininger, 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
Evolutionary Dynamics of the wnt Gene Family: A Lophotrochozoan Perspective
Cho, S.-J., Vallès, Y., Giani, V. C., Seaver, E. C., & Weisblat, D. A. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq052 · Cited by 138
Röttinger, E., Dahlin, P., & Martindale, M. Q. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003164 · Cited by 140
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
Early 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
Self-citationThe origin of animal body plans: a view from fossil evidence and the regulatory genome
Erwin, D. H. (2020) · Development · doi:10.1242/dev.182899 · Cited by 133
BMPs and Chordin regulate patterning of the directive axis in a sea anemone
Saina, M., Genikhovich, G., Renfer, E., & Technau, U. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900151106 · Cited by 138
Self-citationAdamska, M., Larroux, C., Adamski, M., Green, K., Lovas, E., Koop, D., Richards, G. S., Zwafink, C., & Degnan, B. M. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00435.x · Cited by 139
Seaver, E. C., & Kaneshige, L. M. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.10.025 · Cited by 139
Early evolution of metazoan transcription factors
Degnan, B. M., Vervoort, M., Larroux, C., & Richards, G. S. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.09.008 · Cited by 137
The evolutionary origin of hedgehog proteins
Adamska, M., Matus, D. Q., Adamski, M., Green, K., Rokhsar, D. S., Martindale, M. Q., & Degnan, B. M. (2007) · Current Biology · doi:10.1016/j.cub.2007.08.010 · Cited by 137
Self-citationWnt/β-Catenin Signaling Pathway in the Development and Progression of Colorectal Cancer
He, K., & Gan, W.-J. (2023) · Cancer Management and Research · doi:10.2147/cmar.s411168 · Cited by 145
Metadata
- Authors
- Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., Technau, U., von Haeseler, A., Hobmayer, B., Martindale, M. Q., & Holstein, T. W.
- Affiliations
- Technische Universität Darmstadt (DE)
- University of Hawaiʻi at Mānoa (US)
- Universität Innsbruck (AT)
- John von Neumann Institute for Computing (DE)
- Heidelberg University (DE)
- Corresponding author
- Martindale, Mark Q.
- Holstein, Thomas W.
- Venue
- Nature
- Published
- 2005-01-13
- Volume
- 433
- Issue
- 7022
- Pages
- 156-160
- ISSN
- 1465-7392 (ISSN-L)
- 0028-0836
- 1476-4679
- OpenAlex
- W2155603123
- Semantic Scholar
- 7e9fcb05458c57b86ed8a841f431aa109a5baea4
- Cited by
- 599
- References
- 30
- Citations by year
- 2026: 14 · 2025: 21 · 2024: 24 · 2023: 14 · 2022: 26 · 2021: 17 · 2020: 17 · 2019: 32 · 2018: 26 · 2017: 17 · 2016: 27 · 2015: 26 · 2014: 28 · 2013: 27 · 2012: 31
- FWCI
- 44.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- JuSER (Forschungszentrum Jülich) (submittedVersion)
- 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 gene family, Nematostella vectensis, Cnidaria, embryonic development, gastrulation, planula larvae, Cambrian explosion, phylogenetic analysis, gene expression patterns
- MeSH terms
- Animals, Bayes Theorem, Cloning, Molecular, Multigene Family, Molecular Sequence Data, Phylogeny, RNA, Messenger, Sea Anemones, Sequence Alignment, Gene Expression Regulation, Developmental, Evolution, Molecular, Intercellular Signaling Peptides and Proteins, Embryonic Development, Wnt Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
