A Framework for the Establishment of a Cnidarian Gene Regulatory Network for “Endomesoderm” Specification: The Inputs of ß-Catenin/TCF Signaling
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Understanding the functional relationship between intracellular factors and extracellular signals is required for reconstructing gene regulatory networks (GRN) involved in complex biological processes. One of the best-studied bilaterian GRNs describes endomesoderm specification and predicts that both mesoderm and endoderm arose from a common GRN early in animal evolution. Compelling molecular, genomic, developmental, and evolutionary evidence supports the hypothesis that the bifunctional gastrodermis of the cnidarian-bilaterian ancestor is derived from the same evolutionary precursor of both endodermal and mesodermal germ layers in all other triploblastic bilaterian animals. We have begun to establish the framework of a provisional cnidarian "endomesodermal" gene regulatory network in the sea anemone, Nematostella vectensis, by using a genome-wide microarray analysis on embryos in which the canonical Wnt/ß-catenin pathway was ectopically targeted for activation by two distinct pharmaceutical agents (lithium chloride and 1-azakenpaullone) to identify potential targets of endomesoderm specification. We characterized 51 endomesodermally expressed transcription factors and signaling molecule genes (including 18 newly identified) with fine-scale temporal (qPCR) and spatial (in situ) analysis to define distinct co-expression domains within the animal plate of the embryo and clustered genes based on their earliest zygotic expression. Finally, we determined the input of the canonical Wnt/ß-catenin pathway into the cnidarian endomesodermal GRN using morpholino and mRNA overexpression experiments to show that NvTcf/canonical Wnt signaling is required to pattern both the future endomesodermal and ectodermal domains prior to gastrulation, and that both BMP and FGF (but not Notch) pathways play important roles in germ layer specification in this animal. We show both evolutionary conserved as well as profound differences in endomesodermal GRN structure compared to bilaterians that may provide fundamental insight into how GRN subcircuits have been adopted, rewired, or co-opted in various animal lineages that give rise to specialized endomesodermal cell types.
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The earliest function of the canonical Wnt pathway (signalling through b-catenin) is specification of the endomesoderm.
“While the posterior-anterior gradient of expression of Wnt ligands in larval and adult eumetazoans reflects the conserved role in axial patterning, the earliest function of the canonical Wnt pathway (signalling through b-catenin) is specification of the endomesoderm 19,51,52 .”
From Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans (2014) · cites this paper as [19]
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Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
Exploration, normalization, and summaries of high density oligonucleotide array probe level data
Irizarry, R. A. (2003) · Biostatistics · doi:10.1093/biostatistics/4.2.249 · Cited by 10,603 · see citing works
Bolstad, B. M., Irizarry, R. A., Åstrand, M., & Speed, T. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/19.2.185 · Cited by 8,185 · see citing works
A molecular mechanism for the effect of lithium on development.
Klein, P. S., & Melton, D. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8455 · Cited by 2,305 · see citing works
XTcf-3 Transcription Factor Mediates β-Catenin-Induced Axis Formation in Xenopus Embryos
Molenaar, M., van de Wetering, M., Oosterwegel, M., Peterson-Maduro, J., Godsave, S., Korinek, V., Roose, J., Destrée, O., & Clevers, H. (1996) · Cell · doi:10.1016/s0092-8674(00)80112-9 · Cited by 1,824 · see citing works
Newport, J. W., & Kirschner, M. W. (1982) · Cell · doi:10.1016/0092-8674(82)90272-0 · Cited by 1,619 · see citing works
A genomic regulatory network for development
Davidson, E. H., Rast, J. P., Oliveri, P., Ransick, A., Calestani, C., Yuh, C.-H., Minokawa, T., Amore, G., Hinman, V., Arenas-Mena, C., et al. (2002) · Science · doi:10.1126/science.1069883 · Cited by 1,567 · see citing works
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 · see citing works
Self-citationThe specificities of protein kinase inhibitors: an update
BAIN, J., McLAUCHLAN, H., ELLIOTT, M., & COHEN, P. (2003) · Biochemical Journal · doi:10.1042/bj20021535 · Cited by 1,369 · see citing works
Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells
Stambolic, V., Ruel, L., & Woodgett, J. R. (1996) · Current Biology · doi:10.1016/s0960-9822(02)70790-2 · Cited by 1,321 · see citing works
Yost, C., Torres, M., Miller, J., Huang, E., Kimelman, D., & Moon, R. T. (1996) · Genes & Development · doi:10.1101/gad.10.12.1443 · Cited by 1,167 · see citing works
A major developmental transition in early xenopus embryos: II. control of the onset of transcription
Newport, J., & Kirschner, M. (1982) · Cell · doi:10.1016/0092-8674(82)90273-2 · Cited by 1,055 · see citing works
Gene regulatory networks for development
Levine, M., & Davidson, E. H. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408031102 · Cited by 796 · see citing works
Hemmati‐Brivanlou, A., Kelly, O., & Melton, D. A. (1994) · Cell · doi:10.1016/0092-8674(94)90320-4 · Cited by 761 · see citing works
Hacohen, N., Krämer, S., Sutherland, D., Hiromi, Y., & Krasnow, M. A. (1998) · Cell · doi:10.1016/s0092-8674(00)80919-8 · Cited by 750 · see citing works
The zebrafish midblastula transition
Kane, D. A., & Kimmel, C. B. (1993) · Development · doi:10.1242/dev.119.2.447 · Cited by 722 · see citing works
Requirement for β-Catenin in Anterior-Posterior Axis Formation in Mice
Huelsken, J., Vogel, R., Brinkmann, V., Erdmann, B., Birchmeier, C., & Birchmeier, W. (2000) · Journal of Cell Biology · doi:10.1083/jcb.148.3.567 · Cited by 717 · see citing works
Unexpected complexity of the Wnt gene family in a sea anemone
Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., Technau, U., von Haeseler, A., Hobmayer, B., Martindale, M. Q., et al. (2005) · Nature · doi:10.1038/nature03158 · Cited by 599 · see citing works
Self-citation(1940) · Andalas University Repository (Andalas University) · Cited by 591 · see citing works
Pharmacological inhibitors of glycogen synthase kinase 3
Meijer, L., Flajolet, M., & Greengard, P. (2004) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2004.07.006 · Cited by 586 · see citing works
New aspects of Wnt signaling pathways in higher vertebrates
Huelsken, J., & Birchmeier, W. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00231-8 · Cited by 552 · see citing works
Wnt Signaling Controls the Phosphorylation Status of β-Catenin
van Noort, M., Meeldijk, J., van der Zee, R., Destrée, O., & Clevers, H. C. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111635200 · Cited by 468 · see citing works
Nuclear β-catenin is required to specify vegetal cell fates in the sea urchin embryo
Logan, C. Y., Miller, J. R., Ferkowicz, M. J., & McClay, D. R. (1999) · Development · doi:10.1242/dev.126.2.345 · Cited by 456 · see citing works
Synexpression groups in eukaryotes
Niehrs, C., & Pollet, N. (1999) · Nature · doi:10.1038/990025 · Cited by 440 · see citing works
Origins of Bilateral Symmetry: <i>Hox</i> and <i>Dpp</i> 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 · see citing works
Self-citationMartindale, M. Q., Pang, K., & Finnerty, J. R. (2004) · Development · doi:10.1242/dev.01119 · Cited by 396 · see citing works
Self-citationNodal and BMP2/4 Signaling Organizes the Oral-Aboral Axis of the Sea Urchin Embryo
Duboc, V., Röttinger, É., Besnardeau, L., & Lepage, T. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00056-5 · Cited by 353 · see citing works
Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development
Edgar, B. A., Kiehle, C. P., & Schubiger, G. (1986) · Cell · doi:10.1016/0092-8674(86)90771-3 · Cited by 340 · see citing works
A Provisional Regulatory Gene Network for Specification of Endomesoderm in the Sea Urchin Embryo
Davidson, E. H., Rast, J. P., Oliveri, P., Ransick, A., Calestani, C., Yuh, C., Minokawa, T., Amore, G., Hinman, V. F., Arenas‐Mena, C., et al. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0635 · Cited by 338 · see citing works
An ancient role for nuclear β-catenin in the evolution of axial polarity and germ layer segregation
Wikramanayake, A. H., Hong, M., Lee, P. N., Pang, K., Byrum, C. A., Bince, J. M., Xu, R., & Martindale, M. Q. (2003) · Nature · doi:10.1038/nature02113 · Cited by 324 · see citing works
Self-citationSakanaka, C., Weiss, J. B., & Williams, L. T. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3020 · Cited by 302 · see citing works
The Culture, Sexual and Asexual Reproduction, and Growth of the Sea Anemone Nematostella vectensis
Hand, C., & Uhlinger, K. R. (1992) · Biological Bulletin · doi:10.2307/1542110 · Cited by 288 · see citing works
Wikramanayake, A. H., Huang, L., & Klein, W. H. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.16.9343 · Cited by 287 · see citing works
Evolutionary crossroads in developmental biology: Cnidaria
Technau, U., & Steele, R. E. (2011) · Development · doi:10.1242/dev.048959 · Cited by 274 · see citing works
Developmental gene regulatory network architecture across 500 million years of echinoderm evolution
Hinman, V. F., Nguyen, A. T., Cameron, R. A., & Davidson, E. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2235868100 · Cited by 272 · see citing works
Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes
Gazave, E., Lapébie, P., Richards, G. S., Brunet, F., Ereskovsky, A. V., Degnan, B. M., Borchiellini, C., Vervoort, M., & Renard, E. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-249 · Cited by 266 · see citing works
DNA-replication checkpoint control at the Drosophila midblastula transition
Sibon, O. C. M., Stevenson, V. A., & Theurkauf, W. E. (1997) · Nature · doi:10.1038/40439 · Cited by 258 · see citing works
Independent evolution of striated muscles in cnidarians and bilaterians
Steinmetz, P. R. H., Kraus, J. E. M., Larroux, C., Hammel, J. U., Amon-Hassenzahl, A., Houliston, E., Wörheide, G., Nickel, M., Degnan, B. M., & Technau, U. (2012) · Nature · doi:10.1038/nature11180 · Cited by 252 · see citing works
A Regulatory Gene Network That Directs Micromere Specification in the Sea Urchin Embryo
Oliveri, P., Carrick, D. M., & Davidson, E. H. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0627 · Cited by 251 · see citing works
A Wnt- and β-catenin-dependent pathway for mammalian cardiac myogenesis
Nakamura, T., Sano, M., Songyang, Z., & Schneider, M. D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0935626100 · Cited by 248 · see citing works
Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D., & Martindale, M. Q. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20698 · Cited by 247 · see citing works
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 241 · see citing works
Self-citationβ-catenin mediates the specification of endoderm cells in ascidian embryos
Imai, K. S., Takada, N., Satoh, N., & Satou, Y. (2000) · Development · doi:10.1242/dev.127.14.3009 · Cited by 236 · see citing works
Molecular 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 · see citing works
Self-citationA gene regulatory network controlling the embryonic specification of endoderm
Peter, I. S., & Davidson, E. H. (2011) · Nature · doi:10.1038/nature10100 · Cited by 226 · see citing works
Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa)
Fritzenwanker, J. H., & Technau, U. (2002) · Development Genes and Evolution · doi:10.1007/s00427-002-0214-7 · Cited by 218 · see citing works
Rising starlet: the starlet sea anemone,Nematostella vectensis
Darling, J. A., Reitzel, A. M., Burton, P. M., Mazza, M. E., Ryan, J. F., Sullivan, J. C., & Finnerty, J. R. (2005) · BioEssays · doi:10.1002/bies.20181 · Cited by 214 · see citing works
Bolouri, H., & Davidson, E. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1533293100 · Cited by 212 · see citing works
LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo
Sherwood, D. R., & McClay, D. R. (1999) · Development · doi:10.1242/dev.126.8.1703 · Cited by 211 · see citing works
Origin and evolution of endoderm and mesoderm
Technau, U., & Scholz, C. B. (2003) · The International Journal of Developmental Biology · doi:10.1387/ijdb.14756329 · Cited by 208 · see citing works
The evolution of metazoan axial properties
Martindale, M. Q. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1725 · Cited by 204 · see citing works
Self-citationLapraz, F., Besnardeau, L., & Lepage, T. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000248 · Cited by 202 · see citing works
Duloquin, L., Lhomond, G., & Gache, C. (2007) · Development · doi:10.1242/dev.005108 · Cited by 193 · see citing works
Sweet, H. C., Gehring, M. E., & Ettensohn, C. A. (2002) · Development · doi:10.1242/dev.129.8.1945 · Cited by 188 · see citing works
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 185 · see citing works
Self-citationA glimpse into the molecular entrails of endoderm formationPreprint
Stainier, D. Y. R. (2002) · Genes & Development · doi:10.1101/gad.974902 · Cited by 177 · see citing works
GSK3β/shaggy mediates patterning along the animal-vegetal axis of the sea urchin embryo
Emily-Fenouil, F., Ghiglione, C., Lhomond, G., Lepage, T., & Gache, C. (1998) · Development · doi:10.1242/dev.125.13.2489 · Cited by 171 · see citing works
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 170 · see citing works
Momose, T., Derelle, R., & Houliston, E. (2008) · Development · doi:10.1242/dev.021543 · Cited by 170 · see citing works
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 · see citing works
Fritzenwanker, J. H., Saina, M., & Technau, U. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.08.014 · Cited by 165 · see citing works
A muscle-specific transgenic reporter line of the sea anemone, <i>Nematostella vectensis</i>
Renfer, E., Amon-Hassenzahl, A., Steinmetz, P. R. H., & Technau, U. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909148107 · Cited by 164 · see citing works
Two 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 · see citing works
Vertebrate mesendoderm induction and patterning
Kimelman, D., & Griffin, K. J. P. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00095-2 · Cited by 159 · see citing works
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 · see citing works
Self-citationGould, T. D., Zarate, C. A., & Manji, H. K. (2004) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v65n0103 · Cited by 156 · see citing works
Evolutionary plasticity of developmental gene regulatory network architecture
Hinman, V. F., & Davidson, E. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709994104 · Cited by 154 · see citing works
Röttinger, É., Saudemont, A., Duboc, V., Besnardeau, L., McClay, D. R., & Lepage, T. (2007) · Development · doi:10.1242/dev.014282 · Cited by 152 · see citing works
Rodaway, A. R. F., & Patient, R. K. (2001) · Cell · doi:10.1016/s0092-8674(01)00307-5 · Cited by 150 · see citing works
Gene regulatory network controlling embryonic specification in the sea urchin
Oliveri, P., & Davidson, E. H. (2004) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2004.06.004 · Cited by 149 · see citing works
Gene Regulation: Gene Control Network in Development
de‐Leon, S. B., & Davidson, E. H. (2007) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.biophys.35.040405.102002 · Cited by 147 · see citing works
Brachyury, the blastopore and the evolution of the mesoderm
Technau, U. (2001) · BioEssays · doi:10.1002/bies.1114 · Cited by 145 · see citing works
Extavour, C. G., Pang, K., Matus, D. Q., & Martindale, M. Q. (2005) · Evolution & Development · doi:10.1111/j.1525-142x.2005.05023.x · Cited by 144 · see citing works
Self-citationRoure, A., Rothbächer, U., Robin, F., Kalmár, É., Ferone, G., Lamy, C., Missero, C., Müller, F., & Lemaire, P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000916 · Cited by 143 · see citing works
Scholz, C. B., & Technau, U. (2003) · Development Genes and Evolution · doi:10.1007/s00427-002-0272-x · Cited by 142 · see citing works
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 · see citing works
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 · see citing works
TCF: transcriptional activator or repressor?
Bienz, M. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80013-6 · Cited by 135 · see citing works
Glycogen Synthase Kinase 3: A Target for Novel Mood Disorder Treatments
Gould, T. D., & Manji, H. K. (2006) · doi:10.1002/0470052171.ch7 · Cited by 135 · see citing works
TCF Is the Nuclear Effector of the β-Catenin Signal That Patterns the Sea Urchin Animal–Vegetal Axis
Vonica, A., Weng, W., Gumbiner, B. M., & Venuti, J. M. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9551 · Cited by 135 · see citing works
Lee, P. N., Kumburegama, S., Marlow, H. Q., Martindale, M. Q., & Wikramanayake, A. H. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.05.040 · Cited by 135 · see citing works
Self-citationMatus, D. Q., Magie, C. R., Pang, K., Martindale, M. Q., & Thomsen, G. H. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.09.032 · Cited by 134 · see citing works
Self-citationA genetic regulatory network for Xenopus mesendoderm formation
Loose, M., & Patient, R. K. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.04.014 · Cited by 132 · see citing works
Gastrulation in the cnidarian Nematostella vectensis occurs via invagination not ingression
Magie, C. R., Daly, M., & Martindale, M. Q. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.02.044 · Cited by 132 · see citing works
Self-citationA Developmental Perspective: Changes in the Position of the Blastopore during Bilaterian Evolution
Martindale, M. Q., & Hejnol, A. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.07.024 · Cited by 130 · see citing works
Self-citationRöttinger, É., Besnardeau, L., & Lepage, T. (2004) · Development · doi:10.1242/dev.01000 · Cited by 130 · see citing works
Matus, D. Q., Thomsen, G. H., & Martindale, M. Q. (2006) · Current Biology · doi:10.1016/j.cub.2006.01.052 · Cited by 129 · see citing works
Self-citationA Gene Regulatory Network Subcircuit Drives a Dynamic Pattern of Gene Expression
Smith, J., Theodoris, C. V., & Davidson, E. H. (2007) · Science · doi:10.1126/science.1146524 · Cited by 127 · see citing works
A simple plan-Cnidarians and the origins of developmental mechanisms
Ball, E. E., Hayward, D. C., Saint, R., & Miller, D. J. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1402 · Cited by 123 · see citing works
Abel, T. G., Michelson, A. M., & Maniatis, T. (1993) · Development · doi:10.1242/dev.119.3.623 · Cited by 123 · see citing works
Neuroanatomy of sea spiders implies an appendicular origin of the protocerebral segment
Maxmen, A., Browne, W. E., Martindale, M. Q., & Giribet, G. (2005) · Nature · doi:10.1038/nature03984 · Cited by 118 · see citing works
Self-citationGSK3β inhibition promotes melanogenesis in mouse B16 melanoma cells and normal human melanocytes
Bellei, B., Flori, E., Izzo, E., Maresca, V., & Picardo, M. (2008) · Cellular Signalling · doi:10.1016/j.cellsig.2008.06.001 · Cited by 113 · see citing works
Maduro, M., Lin, R., & Rothman, J. H. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0721 · Cited by 111 · see citing works
McClay, D. R., Peterson, R. E., Range, R., Winter-Vann, A. M., & Ferkowicz, M. J. (2000) · Development · doi:10.1242/dev.127.23.5113 · Cited by 111 · see citing works
The Radiata and the evolutionary origins of the bilaterian body plan
Martindale, M. Q., Finnerty, J. R., & Henry, J. Q. (2002) · Molecular Phylogenetics and Evolution · doi:10.1016/s1055-7903(02)00208-7 · Cited by 110 · see citing works
Self-citationNodal and BMP2/4 pattern the mesoderm and endoderm during development of the sea urchin embryo
Duboc, V., Lapraz, F., Saudemont, A., Bessodes, N., Mekpoh, F., Haillot, E., Quirin, M., & Lepage, T. (2009) · Development · doi:10.1242/dev.042531 · Cited by 108 · see citing works
A BMP pathway regulates cell fate allocation along the sea urchin animal- vegetal embryonic axis
Angerer, L. M., Oleksyn, D. W., Logan, C. Y., McClay, D. R., Dale, L., & Angerer, R. C. (2000) · Development · doi:10.1242/dev.127.5.1105 · Cited by 108 · see citing works
Sweet, H. C., Hodor, P. G., & Ettensohn, C. A. (1999) · Development · doi:10.1242/dev.126.23.5255 · Cited by 107 · see citing works
Did homeodomain proteins duplicate before the origin of angiosperms, fungi, and metazoa?
Geeta, R., Janssen, B. J., Kellogg, E. A., & Sinha, N. R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.13749 · Cited by 107 · see citing works
Darras, S., Gerhart, J. C., Terasaki, M., Kirschner, M. W., & Lowe, C. J. (2011) · Development · doi:10.1242/dev.059493 · Cited by 106 · see citing works
ZUR EXPERIMENTELLEN ANALYSE DER WIRKUNG DES LITHIUMS AUF DEN SEEIGELKEIM
RUNNSTRÖM, J. (1928) · Acta Zoologica · doi:10.1111/j.1463-6395.1928.tb01170.x · Cited by 104 · see citing works
Cell cycle transition in early embryonic development of Xenopus laevis
Masui, Y. (1998) · Biology of the Cell · doi:10.1016/s0248-4900(99)80011-2 · Cited by 103 · see citing works
Functional roles of Notch signaling in the cnidarian Nematostella vectensis
Marlow, H. Q., Röttinger, É., Boekhout, M., & Martindale, M. Q. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.11.012 · Cited by 101 · see citing works
Self-citationDynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo
Croce, J. C., & McClay, D. R. (2009) · Development · doi:10.1242/dev.044149 · Cited by 99 · see citing works
Layden, M. J., Boekhout, M., & Martindale, M. Q. (2012) · Development · doi:10.1242/dev.073221 · Cited by 98 · see citing works
Self-citationCell type specification during sea urchin development
Cameron, R. A., & Davidson, E. H. (1991) · Trends in Genetics · doi:10.1016/0168-9525(91)90367-y · Cited by 97 · see citing works
Ishikawa, A., Kitajima, S., Takahashi, Y., Kokubo, H., Kanno, J., Inoue, T., & Saga, Y. (2004) · Mechanisms of Development · doi:10.1016/j.mod.2004.08.003 · Cited by 96 · see citing works
Mesodermal anatomies in cnidarian polyps and medusae
Seipel, K., & Schmid, V. J. (2006) · The International Journal of Developmental Biology · doi:10.1387/ijdb.062150ks · Cited by 95 · see citing works
Evidence for engrailed-Independent wingless Autoregulation in Drosophila
Yoffe, K. B., Manoukian, A. S., Wilder, E. L., Brand, A. H., & Perrimon, N. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1243 · Cited by 94 · see citing works
Matus, D. Q., Thomsen, G. H., & Martindale, M. Q. (2007) · Development Genes and Evolution · doi:10.1007/s00427-006-0122-3 · Cited by 92 · see citing works
Self-citationCell type specification during sea urchin development
Cameron, R. A. (1991) · Trends in Genetics · doi:10.1016/0168-9525(91)90140-l · Cited by 92 · see citing works
Sherwood, D. R., & McClay, D. R. (2001) · Development · doi:10.1242/dev.128.12.2221 · Cited by 89 · see citing works
Cell-Cell Adhesion in the Cnidaria: Insights Into the Evolution of Tissue Morphogenesis
Magie, C. R., & Martindale, M. Q. (2008) · Biological Bulletin · doi:10.2307/25470665 · Cited by 89 · see citing works
Self-citationAn evolutionary conserved role of Wnt signaling in stem cell fate decision
Teo, R., Möhrlen, F., Plickert, G., Müller, W. A., & Uri Frank, A. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.10.009 · Cited by 86 · see citing works
Early evolution of a homeobox gene: the parahox gene Gsx in the Cnidaria and the Bilateria
Finnerty, J. R., Paulson, D. A., Burton, P. M., Pang, K., & Martindale, M. Q. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03041.x · Cited by 85 · see citing works
Self-citationWindsor, P. J., & Leys, S. P. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00434.x · Cited by 84 · see citing works
Modeling DNA Sequence-Based cis-Regulatory Gene Networks
Bolouri, H., & Davidson, E. H. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0617 · Cited by 82 · see citing works
Kumburegama, S., Wijesena, N. M., Xu, R., & Wikramanayake, A. H. (2011) · EvoDevo · doi:10.1186/2041-9139-2-2 · Cited by 76 · see citing works
A role for maternal β‐catenin in early mesoderm induction in Xenopus
Schohl, A., & Fagotto, F. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg328 · Cited by 74 · see citing works
Fernandez-Serra, M., Consales, C., Livigni, A., & Arnone, M. I. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2003.12.029 · Cited by 72 · see citing works
Network design principles from the sea urchin embryo
Davidson, E. H. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.10.007 · Cited by 70 · see citing works
Smith, J., & Davidson, E. H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806442105 · Cited by 69 · see citing works
Wnt6 activates endoderm in the sea urchin gene regulatory network
Croce, J. C., Range, R., Wu, S.-Y., Miranda, E., Lhomond, G., Peng, J., Lepage, T., & McClay, D. (2011) · Development · doi:10.1242/dev.058792 · Cited by 69 · see citing works
Insights from diploblasts; the evolution of mesoderm and muscle
Burton, P. M. (2007) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21150 · Cited by 69 · see citing works
Uncoupling gastrulation and mesoderm differentiation in the Drosophila embryo.
Ip, Y. T., Maggert, K. A., & Levine, M. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06926.x · Cited by 69 · see citing works
Sineva, G. S., & Pospelov, V. A. (2010) · Biology of the Cell · doi:10.1042/bc20100016 · Cited by 67 · see citing works
Hinman, V. F., Nguyen, A., & Davidson, E. H. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.09.006 · Cited by 67 · see citing works
The canonical Wnt pathway in embryonic axis polarity
Croce, J. C., & McClay, D. R. (2006) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2006.04.004 · Cited by 67 · see citing works
Sequential Signaling Crosstalk Regulates Endomesoderm Segregation in Sea Urchin Embryos
Sethi, A. J., Wikramanayake, R. M., Angerer, R. C., Range, R., & Angerer, L. M. (2012) · Science · doi:10.1126/science.1212867 · Cited by 66 · see citing works
Mazza, M. E., Pang, K., Martindale, M. Q., & Finnerty, J. R. (2007) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21158 · Cited by 57 · see citing works
Self-citationThe blastoporal organiser of a sea anemone
Kraus, Y. A., Fritzenwanker, J. H., Genikhovich, G., & Technau, U. (2007) · Current Biology · doi:10.1016/j.cub.2007.08.017 · Cited by 56 · see citing works
Trevino, M. A., Stefanik, D. J., Rodriguez, R., Harmon, S., & Burton, P. M. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22774 · Cited by 56 · see citing works
Röttinger, E., Croce, J., Lhomond, G., Besnardeau, L., Gache, C., & Lepage, T. (2006) · Development · doi:10.1242/dev.02603 · Cited by 54 · see citing works
Endomesoderm specification in Caenorhabditis elegans and other nematodes
Maduro, M. (2006) · BioEssays · doi:10.1002/bies.20480 · Cited by 47 · see citing works
Structure and evolution of the C. elegans embryonic endomesoderm network
Maduro, M. (2008) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2008.07.013 · Cited by 45 · see citing works
Sikes, J. M., & Bely, A. E. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.10.033 · Cited by 42 · see citing works
Glycogen synthase kinase 3 has a proapoptotic function in Hydra gametogenesis
Rentzsch, F., Hobmayer, B., & Holstein, T. W. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.10.007 · Cited by 36 · see citing works
Yasuoka, Y., Kobayashi, M., Kurokawa, D., Akasaka, K., Saiga, H., & Taira, M. (2009) · Development · doi:10.1242/dev.028530 · Cited by 36 · see citing works
Genikhovich, G., & Technau, U. (2011) · Development · doi:10.1242/dev.068122 · Cited by 35 · see citing works
The porcupine gene is required for wingless autoregulation in Drosophila
Manoukian, A. S., Yoffe, K. B., Wilder, E. L., & Perrimon, N. (1995) · Development · doi:10.1242/dev.121.12.4037 · Cited by 32 · see citing works
Gene Regulatory Network Analysis in Sea Urchin Embryos
Oliveri, P., & Davidson, E. H. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74032-7 · Cited by 27 · see citing works
Vandenberg, L. N., & Levin, M. G. (2010) · Development · doi:10.1242/dev.041798 · Cited by 27 · see citing works
Epigenetic silencing in embryogenesis
Meehan, R. R., Dunican, D. S., Ruzov, A. S., & Pennings, S. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.06.023 · Cited by 26 · see citing works
A comparative gene expression database for invertebrates
Ormestad, M., Martindale, M. Q., & Röttinger, É. (2011) · EvoDevo · doi:10.1186/2041-9139-2-17 · Cited by 22 · see citing works
Self-citationPlanarian GSK3s are involved in neural regeneration
Adell, T., Marsal, M., & Saló, E. (2008) · Development, Genes and Evolution · doi:10.1007/s00427-007-0199-3 · Cited by 21 · see citing works
LiCl Perturbs Ectodermal Veg1Lineage Allocations inStrongylocentrotus purpuratusEmbryos
Cameron, R. A., & Davidson, E. H. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8615 · Cited by 15 · see citing works
Thapsigargin-induced apoptosis was prevented by glycogen synthase kinase-3 inhibitors in PC12 cells
Takadera, T., Yoshikawa, R., & Ohyashiki, T. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.08.066 · Cited by 15 · see citing works
Early evolution of the LIM homeobox gene family
Srivastava, M., Larroux, C., Lu, D. R., Mohanty, K., Chapman, J., Degnan, B. M., & Rokhsar, D. S. (2010) · BMC Biology · doi:10.1186/1741-7007-8-4 · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 149 references couldn’t be matched to a known paper.
Research works printed but not linked: 5
- [3]Rodaway A, Patient R (2001) Mesendoderm. an ancient germ layer? Cell 105: 169– 172. 11336666
- [33]Technau U, Steele RE Evolutionary crossroads in developmental biology: Cnidaria. Development 138: 1447– 1458. PMC3062418 21389047
- [36]Byrum CA, Martindale QM (2003) Gastrulation in the Cnidara and Ctenophora. Gastrulation, From Cells to Embryo CSHL Press 33– 50.
- [38]Fautin DG, Mariscal R.N. (1991) Cnidaria: Anthozoa. New York: Wiley-Liss.
- [64]Cameron RA, Davidson EH (1997) LiCl perturbs ectodermal veg1 lineage allocations in Strongylocentrotus purpuratus embryos. Dev Biol 187: 236– 239. 9242420
Cited by
Sorted by citations
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 · see citing works
The genome of the jellyfish Clytia hemisphaerica and the evolution of the cnidarian life-cycle
Leclère, L., Horin, C., Chevalier, S., Lapébie, P., Dru, P., Péron, S., Jager, M., Condamine, T., Pottin, K., Romano, S., et al. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-0833-2 · Cited by 190 · see citing works
TALEN and CRISPR/Cas9-mediated genome editing in the early-branching metazoan Nematostella vectensis
Ikmi, A., McKinney, S. A., Delventhal, K. M., & Gibson, M. C. (2014) · Nature Communications · doi:10.1038/ncomms6486 · Cited by 165 · see citing works
Layden, M. J., Rentzsch, F., & Röttinger, É. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.222 · Cited by 148 · see citing works
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 · see citing works
Leininger, 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 · see citing works
Gut-like ectodermal tissue in a sea anemone challenges germ layer homology
Steinmetz, P. R. H., Aman, A. J., Kraus, J. E. M., & Technau, U. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0285-5 · Cited by 135 · see citing works
DuBuc, T. Q., Traylor‐Knowles, N., & Martindale, M. Q. (2014) · BMC Biology · doi:10.1186/1741-7007-12-24 · Cited by 138 · see citing works
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Duffy, D. J., Krstić, A., Schwarzl, T., Higgins, D. G., & Kölch, W. (2013) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-13-0560-t · Cited by 79 · see citing works
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Warner, J. F., Guerlais, V., Amiel, A., Johnston, H. T., Nedoncelle, K., & Röttinger, É. (2018) · Development · doi:10.1242/dev.162867 · Cited by 70 · see citing works
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Self-citationPerry, K. J., Lyons, D. C., Truchado-García, M., Fischer, A., Helfrich, L. W., Johansson, K. B., Diamond, J. C., Grande, C., & Henry, J. J. (2015) · Developmental Dynamics · doi:10.1002/dvdy.24308 · Cited by 63 · see citing works
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Tulin, S., Aguiar, D., Istrail, S., & Smith, J. (2013) · EvoDevo · doi:10.1186/2041-9139-4-16 · Cited by 54 · see citing works
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Servetnick, M. D., Steinworth, B. M., Babonis, L. S., Simmons, D., Salinas‐Saavedra, M., & Martindale, M. Q. (2017) · Development · doi:10.1242/dev.145839 · Cited by 45 · see citing works
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Wijesena, N. M., Simmons, D. K., & Martindale, M. Q. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701607114 · Cited by 36 · see citing works
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Schwaiger, M., Andrikou, C., Dnyansagar, R., Murguia, P. F., Paganos, P., Voronov, D., Zimmermann, B., Lebedeva, T. S., Schmidt, H. A., Genikhovich, G., et al. (2022) · Nature Ecology & Evolution · doi:10.1038/s41559-022-01905-w · Cited by 29 · see citing works
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Love, A. C. (2024) · Cambridge University Press eBooks · doi:10.1017/9781108616751 · Cited by 32 · see citing works
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Amiel, A., Foucher, K., Ferreira, S., & Röttinger, É. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2019.12.31.891804 · Cited by 27 · see citing works
Fischer, A., Pang, K., Henry, J. J., & Martindale, M. Q. (2014) · EvoDevo · doi:10.1186/2041-9139-5-4 · Cited by 28 · see citing works
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Clarke, D. N., Lowe, C. J., & Nelson, W. J. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.01.007 · Cited by 27 · see citing works
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Žídek, R., Machoň, O., & Kozmík, Z. (2018) · EvoDevo · doi:10.1186/s13227-018-0100-7 · Cited by 22 · see citing works
Ruocco, N., Fedele, A. M., Costantini, S., Romano, G., Ianora, A., & Costantini, M. (2017) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2017.04.022 · Cited by 22 · see citing works
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Self-citation
- Authors
- Röttinger, E., Dahlin, P., & Martindale, M. Q.
- Affiliations
- University of Hawaiʻi at Mānoa (US)
- Corresponding author
- Martindale, Mark Q.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-12-27
- Volume
- 8
- Issue
- 12
- Pages
- e1003164
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3531958
- OpenAlex
- W1989889624
- Cited by
- 140
- References
- 149
- Citations by year
- 2026: 3 · 2025: 14 · 2024: 10 · 2023: 3 · 2022: 10 · 2021: 5 · 2020: 5 · 2019: 12 · 2018: 12 · 2017: 13 · 2016: 16 · 2015: 13 · 2014: 15 · 2013: 9
- FWCI
- 4.75
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM093116, #GM093116)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Keywords
- gene regulatory networks, endomesoderm specification, Wnt/β-catenin signaling, Nematostella vectensis, germ layer specification, BMP signaling, FGF signaling, Notch signaling, transcription factors, zygotic gene expression, morpholino knockdown
- MeSH terms
- Amino Acid Sequence, Animals, Cell Differentiation, Cnidaria, Embryo, Nonmammalian, Endoderm, Mesoderm, Sea Anemones, Transcription Factors, Signal Transduction, Lithium Chloride, Gene Expression Regulation, Developmental, Cell Lineage, Evolution, Molecular, beta Catenin, Gene Regulatory Networks, Wnt Signaling Pathway
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