Origins of neurogenesis, a cnidarian view

Galliot, Brigitte; Quiquand, Manon; Ghila, Luiza; de Rosa, Renaud; Miljkovic-Licina, Marijana; Chera, Simona

doi:10.1016/j.ydbio.2009.05.563

Cited by 168Marine Invertebrate Physiology and EcologyDevelopmental Biology and Gene RegulationNeurogenesis and neuroplasticity mechanisms

Origins of neurogenesis, a cnidarian view

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Galliot, Brigitte, Quiquand, Manon, Ghila, Luiza, de Rosa, Renaud, Miljkovic-Licina, Marijana, Chera, Simona·2009·Developmental Biology

DOI 10.1016/j.ydbio.2009.05.563

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Abstract

New perspectives on the origin of neurogenesis emerged with the identification of genes encoding post-synaptic proteins as well as many "neurogenic" regulators as the NK, Six, Pax, bHLH proteins in the Demosponge genome, a species that might differentiate sensory cells but no neurons. However, poriferans seem to miss some key regulators of the neurogenic circuitry as the Hox/paraHox and Otx-like gene families. Moreover as a general feature, many gene families encoding evolutionarily-conserved signaling proteins and transcription factors were submitted to a wave of gene duplication in the last common eumetazoan ancestor, after Porifera divergence. In contrast gene duplications in the last common bilaterian ancestor, Urbilateria, are limited, except for the bHLH Atonal-class. Hence Cnidaria share with Bilateria a large number of genetic tools. The expression and functional analyses currently available suggest a neurogenic function for numerous orthologs in developing or adult cnidarians where neurogenesis takes place continuously. As an example, in the Hydra polyp, the Clytia medusa and the Acropora coral, the Gsx/cnox2/Anthox-2 ParaHox gene likely supports neurogenesis. Also neurons and nematocytes (mechanosensory cells) share in hydrozoans a common stem cell and several regulatory genes indicating that they can be considered as sister cells. Performed in anthozoan and medusozoan species, these studies should tell us more about the way(s) evolution hazards achieved the transition from epithelial to neuronal cell fate, and about the robustness of the genetic circuitry that allowed neuromuscular transmission to arise and be maintained across evolution.

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Much of the molecular architecture underlying neurogenesis and neuron functioning is conserved between bilaterians and cnidarians.
“The publication of several cnidarian genomes has shown that much of the molecular architecture underlying neurogenesis and neuron functioning is conserved between bilaterians and cnidarians [17,47–51].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [49]

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International Union of Pharmacology: Approaches to the Nomenclature of Voltage-Gated Ion Channels
Catterall, W. A., Chandy, K. G., Clapham, D. E., Gutman, G. A., Hofmann, F., Harmar, A. J., Abernethy, D. R., & Spedding, M. (2003) · Pharmacological Reviews · doi:10.1124/pr.55.4.5 · Cited by 7,126 · see citing works
A gene complex controlling segmentation in Drosophila
Lewis, E. B. (1978) · Nature · doi:10.1038/276565a0 · Cited by 3,813 · see citing works
Function and regulation of CREB family transcription factors in the nervous system
Lonze, B. E., & Ginty, D. D. (2002) · Neuron · doi:10.1016/s0896-6273(02)00828-0 · Cited by 2,127 · see citing works
Proneural genes and the specification of neural cell types
Bertrand, N., Castro, D. S., & Guillemot, F. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn874 · Cited by 1,572 · see citing works
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., et al. (2008) · Nature · doi:10.1038/nature06617 · Cited by 1,139 · see citing works
Expression of engrailed proteins in arthropods, annelids, and chordates
Patel, N. H., Martı́n-Blanco, E., Coleman, K. G., Poole, S. J., Ellis, M. C., Kornberg, T. B., & Goodman, C. S. (1989) · Cell · doi:10.1016/0092-8674(89)90947-1 · Cited by 1,015 · see citing works
A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewalPreprint
Cox, D. N., Chao, A. T., Baker, J. J., Chang, L., Qiao, D., & Lin, H. (1998) · Genes & Development · doi:10.1101/gad.12.23.3715 · Cited by 965 · see citing works
Traite de zoologie
Grassé, P.-P., Bourdelle, E., Bourlière, F., & Dekeyser, P. L. (1955) · Cited by 933 · see citing works
The nuclear receptor ligand-binding domain: structure and function
Moras, D., & Gronemeyer, H. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80015-x · Cited by 838 · see citing works
The zootype and the phylotypic stage
Slack, J. M. W., Holland, P. W. H., & Graham, C. F. (1993) · Nature · doi:10.1038/361490a0 · Cited by 699 · see citing works
Disruption of CREB function in brain leads to neurodegeneration
Mantamadiotis, T., Lemberger, T., Bleckmann, S. C., Kern, H., Kretz, O., Villalba, A. M., Tronche, F., Kellendonk, C., Gau, D., Kapfhammer, J., et al. (2002) · Nature Genetics · doi:10.1038/ng882 · Cited by 684 · see citing works
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 · 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
Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo
Thomas, P. Q., & Beddington, R. S. P. (1996) · Current Biology · doi:10.1016/s0960-9822(96)00753-1 · Cited by 552 · see citing works
The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart developmentPreprint
Pereira, F. A., Qiu, Y., Zhou, G., Tsai, M., & Tsai, S. Y. (1999) · Genes & Development · doi:10.1101/gad.13.8.1037 · Cited by 526 · see citing works
The evolution of cell types in animals: emerging principles from molecular studies
Arendt, D. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2416 · Cited by 525 · see citing works
Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria
Denes, A. S., Jékely, G., Steinmetz, P. R. H., Raible, F., Snyman, H., Prud'homme, B., Ferrier, D. E. K., Balavoine, G., & Arendt, D. (2007) · Cell · doi:10.1016/j.cell.2007.02.040 · Cited by 480 · see citing works
The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster
Brooke, N. M., Garcia-Fernàndez, J., & Holland, P. W. H. (1998) · Nature · doi:10.1038/31933 · Cited by 468 · see citing works
A quantitative method for maceration of hydra tissue
David, C. N. (1973) · Development Genes and Evolution · doi:10.1007/bf00577724 · Cited by 446 · see citing works
Evolution of eyes and photoreceptor cell types
Arendt, D. (2003) · The International Journal of Developmental Biology · doi:10.1387/ijdb.14756332 · Cited by 430 · see citing works
Apoptotic Cells Provide an Unexpected Source of Wnt3 Signaling to Drive Hydra Head Regeneration
Chera, S., Ghila, L., Dobretz, K., Wenger, Y., Bauer, C., Buzgariu, W. C., Martinou, J., & Galliot, B. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.07.014 · Cited by 418 · see citing works
Self-citation
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 · see citing works
Investigating the origins of triploblasty: `mesodermal' gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa)
Martindale, M. Q., Pang, K., & Finnerty, J. R. (2004) · Development · doi:10.1242/dev.01119 · Cited by 396 · see citing works
Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution
Tessmar-Raible, K., Raible, F., Christodoulou, F., Guy, K., Rembold, M., Hausen, H., & Arendt, D. (2007) · Cell · doi:10.1016/j.cell.2007.04.041 · Cited by 384 · see citing works
Medusozoan Phylogeny and Character Evolution Clarified by New Large and Small Subunit rDNA Data and an Assessment of the Utility of Phylogenetic Mixture Models
Collins, A. G., Schuchert, P., Marques, A. C., Jankowski, T., Medina, M., & Schierwater, B. (2006) · Systematic Biology · doi:10.1080/10635150500433615 · Cited by 382 · see citing works
Skeletal muscle determination and differentiation: story of a core regulatory network and its context
Yun, K., & Wold, B. J. (1996) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(96)80091-3 · Cited by 358 · see citing works
Evo-Devo: Variations on Ancestral Themes
Robertis, E. M. D. (2008) · Cell · doi:10.1016/j.cell.2008.01.003 · Cited by 335 · see citing works
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 327 · 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
Spatial and temporal specification of neural fates by transcription factor codes
Guillemot, F. (2007) · Development · doi:10.1242/dev.006379 · Cited by 308 · see citing works
Mechanism of phototaxis in marine zooplankton
Jékely, G., Colombelli, J., Hausen, H., Guy, K., Stelzer, E., Nédélec, F., & Arendt, D. (2008) · Nature · doi:10.1038/nature07590 · Cited by 298 · see citing works
Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics
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 286 · see citing works
Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification
Rhinn, M., Dierich, A., Shawlot, W., Behringer, R. R., LeMeur, M., & Ang, S. (1998) · Development · doi:10.1242/dev.125.5.845 · Cited by 279 · see citing works
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 275 · see citing works
The role of Zic genes in neural development
Aruga, J. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.01.004 · Cited by 267 · see citing works
Wnt and TGF-β Expression in the Sponge Amphimedon queenslandica and the Origin of Metazoan Embryonic Patterning
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 · see citing works
Class-level relationships in the phylum Cnidaria: molecular and morphological evidence.
Bridge, D. M., Cunningham, C., DeSalle, R., & Buss, L. W. (1995) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040246 · Cited by 251 · see citing works
Dorsoventral patterning in the Drosophila central nervous system: the intermediate neuroblasts defective homeobox gene specifies intermediate column identity
Weiss, J. B., Von Ohlen, T., Mellerick, D. M., Dressler, G., Doe, C. Q., & Scott, M. P. (1998) · Genes & Development · doi:10.1101/gad.12.22.3591 · Cited by 250 · cited 1× · see citing works
“In Drosophila embryos, the Gsx ortholog named ind is expressed as a longitudinal band in the intermediate neuroectoderm where it promotes activation of proneural genes in the specific set of neuroblasts (Weiss et al., 1998).”
Background
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 · see citing works
Pre-Bilaterian Origins of the Hox Cluster and the Hox Code: Evidence from the Sea Anemone, Nematostella vectensis
Ryan, 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
International Union of Pharmacology. LXVI. Orphan Nuclear Receptors
Benoit, G., Cooney, A. J., Giguère, V., Ingraham, H. A., Lazar, M., Muscat, G. E. O., Perlmann, T., Renaud, J., Schwabe, J. W. R., Sladek, F. M., et al. (2006) · Pharmacological Reviews · doi:10.1124/pr.58.4.10 · Cited by 238 · see citing works
Neuroid Conduction and the Evolution of Conducting Tissues
Mackie, G. O. (1970) · The Quarterly Review of Biology · doi:10.1086/406645 · Cited by 230 · cited 1× · see citing works
“These molecular data actually fit with the three steps model proposed by George Mackie for the origin of neuromuscular transmission (Mackie, 1970) whereby muscle cells and nerve cells would have diverged from myoepithelial cells (see Figure 5a in Arendt, 2008).”
Result
The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach
(1995) · Proceedings of the Fourth International Symposium on Polarization Phenomena in Nuclear Reactions · doi:10.1007/978-3-0348-9219-3 · Cited by 227 · 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
The interstitial cell lineage of hydra: a stem cell system that arose early in evolution
Bode, H. R. (1996) · Journal of Cell Science · doi:10.1242/jcs.109.6.1155 · Cited by 223 · see citing works
Common molecular mechanisms in explicit and implicit memory
Barco, Á., Bailey, C. H., & Kandel, E. R. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03870.x · Cited by 217 · see citing works
Null mutation of mCOUP-TFI results in defects in morphogenesis of the glossopharyngeal ganglion, axonal projection, and arborizationPreprint
Qiu, Y., Pereira, F. A., DeMayo, F. J., Lydon, J. P., Tsai, S. Y., & Tsai, M. (1997) · Genes & Development · doi:10.1101/gad.11.15.1925 · Cited by 215 · see citing works
GLUTATHIONE CONTROL OF THE SPECIFIC FEEDING REACTIONS OF HYDRA
Loomis, W. F. (1955) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1955.tb35372.x · Cited by 209 · see citing works
Phylogenetic analysis of the human basic helix-loop-helix proteins
Ledent, V., Paquet, O., & Vervoort, M. (2002) · Genome biology · doi:10.1186/gb-2002-3-6-research0030 · Cited by 208 · see citing works
The evolution of nervous system centralization
Arendt, D., Denes, A. S., Jékely, G., & Tessmar-Raible, K. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2242 · Cited by 206 · see citing works
Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila
Hirth, F., Therianos, S., Loop, T., Gehring, W. J., Reichert, H., & Furukubo-Tokunaga, K. (1995) · Neuron · doi:10.1016/0896-6273(95)90169-8 · Cited by 200 · see citing works
The behavioral and developmental physiology of nematocysts
Kass‐Simon, G., & Scappaticci, A. A. (2002) · Canadian Journal of Zoology · doi:10.1139/z02-135 · Cited by 200 · see citing works
Hydra transplantation phenomena and the mechanism of Hydra head regeneration
MacWilliams, H. K. (1983) · Developmental Biology · doi:10.1016/0012-1606(83)90325-1 · Cited by 197 · see citing works
Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements
Chourrout, D., Delsuc, F., Chourrout, P., Edvardsen, R. B., Rentzsch, F., Renfer, E., Jensen, M. F., Zhu, B., de Jong, P., Steele, R. E., et al. (2006) · Nature · doi:10.1038/nature04863 · Cited by 197 · see citing works
COUP-TF orphan nuclear receptors in development and differentiation
Pereira, F. A., Tsai, M., & Tsai, S. Y. (2000) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000624 · Cited by 193 · see citing works
Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning
Gauchat, D., Mazet, F., Berney, C., Schummer, M., Kreger, S., Pawlowski, J., & Galliot, B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4493 · Cited by 190 · see citing works
Self-citation
Evolution of homeobox genes: Q50 Paired-like genes founded the Paired class
Galliot, B., de Vargas, C., & Miller, D. J. (1999) · Development Genes and Evolution · doi:10.1007/s004270050243 · Cited by 188 · see citing works
Self-citation
Systematic isolation of peptide signal molecules regulating development in hydra: LWamide and PW families
Takahashi, T., Muneoka, Y., Lohmann, J. U., de Haro, M. S. L., Solleder, G., Bosch, T. C. G., David, C. N., Bode, H. R., Koizumi, O., Shimizu, H., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.4.1241 · Cited by 186 · see citing works
The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis
Ryan, 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 185 · see citing works
COUP-TFI: an intrinsic factor for early regionalization of the neocortexPreprint
Zhou, C. J., Tsai, S. Y., & Tsai, M. (2001) · Genes & Development · doi:10.1101/gad.913601 · Cited by 184 · see citing works
Development of hydra lacking nerve and interstitial cells
Marcum, B. A., & Campbell, R. D. (1978) · Journal of Cell Science · doi:10.1242/jcs.29.1.17 · Cited by 183 · see citing works
One Billion Years of bZIP Transcription Factor Evolution: Conservation and Change in Dimerization and DNA-Binding Site Specificity
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 183 · see citing works
Elimination of Hydra interstitial and nerve cells by means of colchicine
Campbell, R. D. (1976) · Journal of Cell Science · doi:10.1242/jcs.21.1.1 · Cited by 182 · see citing works
Peptides in the Nervous Systems of Cnidarians: Structure, Function, and Biosynthesis
Grimmelikhuijzen, C. J. P., Leviev, I., & Carstensen, K. (1996) · International review of cytology · doi:10.1016/s0074-7696(08)61345-5 · Cited by 180 · 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 180 · see citing works
Role of Pax Genes in Eye Evolution
Kozmik, Z., Daube, M., Frei, E., Norman, B., Kos, L., Dishaw, L. J., Noll, M., & Piatigorsky, J. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00325-3 · Cited by 179 · see citing works
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 · see citing works
Having it both ways: Sox protein function between conservation and innovation
Guth, S. I. E., & Wegner, M. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8138-7 · Cited by 176 · see citing works
HOM/HOX homeobox genes are present in hydra (Chlorohydra viridissima) and are differentially expressed during regeneration
Schummer, M., Scheurlen, I., Schaller, C., & Galliot, B. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05233.x · Cited by 174 · see citing works
Self-citation
The NK homeobox gene cluster predates the origin of Hox genes.
Larroux, C., Fahey, B., Degnan, S. M., Adamski, M., Rokhsar, D. S., & Degnan, B. M. (2007) · Current Biology · doi:10.1016/j.cub.2007.03.008 · Cited by 173 · cited 2× · see citing works
“The msh/msx gene, a candidate regulator of neurogenesis: The msh/msx homeogene family is highly conserved from Porifera to bilaterians (Larroux et al., 2007).”
Background
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity
Larroux, C., Fahey, B., Liubicich, D., Hinman, V. F., Gauthier, M., Gongora, M., Green, K., Wörheide, G., Leys, S. P., & Degnan, B. M. (2006) · Evolution & Development · doi:10.1111/j.1525-142x.2006.00086.x · Cited by 173 · see citing works
Nanosecond-scale kinetics of nematocyst discharge
Nüchter, T., Benoit, M., Engel, U., Özbek, S., & Holstein, T. W. (2006) · Current Biology · doi:10.1016/j.cub.2006.03.089 · Cited by 171 · see citing works
An 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 171 · see citing works
Molecular evidence from Ciona intestinalis for the evolutionary origin of vertebrate sensory placodes
Mazet, F., Hutt, J. A., Milloz, J., Millard, J. C., Graham, A., & Shimeld, S. M. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.02.021 · Cited by 170 · see citing works
Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: Implications for the evolution of axial patterning
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 · see citing works
The origin of the myelination program in vertebrates
Zalc, B., Goujet, D. F., & Colman, D. (2008) · Current Biology · doi:10.1016/j.cub.2008.04.010 · Cited by 166 · 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
Sponge Genes Provide New Insight into the Evolutionary Origin of the Neurogenic Circuit
Richards, G. S., Simionato, E., Perron, M., Adamska, M., Vervoort, M., & Degnan, B. M. (2008) · Current Biology · doi:10.1016/j.cub.2008.06.074 · Cited by 165 · see citing works
Hydra: Research Methods
Lenhoff, H. M. (1983) · Springer eBooks · doi:10.1007/978-1-4757-0596-6 · 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
The cnidarian cnidocyte, a hightech cellular weaponry
Tardent, P. (1995) · BioEssays · doi:10.1002/bies.950170411 · Cited by 163 · see citing works
Vnd/nkx, ind/gsh, and msh/msx: conserved regulators of dorsoventral neural patterning?
Cornell, R. A., & Ohlen, T. L. V. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00049-5 · Cited by 161 · see citing works
The Biology of Nematocysts
Hessinger, D. A., & Lenhoff, H. M. (1989) · Cited by 160 · see citing works
Evolution and Functional Diversity of Jellyfish Opsins
Suga, H., Schmid, V. J., & Gehring, W. J. (2007) · Current Biology · doi:10.1016/j.cub.2007.11.059 · Cited by 160 · 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
Impulse conduction in a sponge
Leys, S. P., Mackie, G. O., & Meech, R. W. (1999) · Journal of Experimental Biology · doi:10.1242/jeb.202.9.1139 · Cited by 156 · see citing works
Retinoic acid X receptor in the diploblast, Tripedalia cystophora
Kostrouch, Z., Kostrouchová, M., Love, W. K., Jannini, E. A., Piatigorsky, J., & Rall, J. E. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.23.13442 · Cited by 153 · see citing works
Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development
Lichtneckert, R., & Reichert, H. (2005) · Heredity · doi:10.1038/sj.hdy.6800664 · Cited by 153 · see citing works
Conservation of Brachyury, Mef2, and Snail in the Myogenic Lineage of Jellyfish: A Connection to the Mesoderm of Bilateria
Spring, J., Yanze, N., Jösch, C., Middel, A. M., Winninger, B., & Schmid, V. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0616 · Cited by 152 · see citing works
Historical perspective on the development and evolution of eyes and photoreceptors
Gehring, W. J. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041900wg · Cited by 150 · see citing works
Cnidarian chemical neurotransmission, an updated overview
Kass-Simon, G., & Pierobon, P. (2007) · Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2006.09.008 · Cited by 150 · see citing works
Budhead,a Fork Head/HNF-3 Homologue, Is Expressed during Axis Formation and Head Specification in Hydra
Martinez, D. E., Dirksen, M.-L., Bode, P. M., Jamrich, M., Steele, R. E., & Bode, H. R. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8715 · Cited by 150 · see citing works
Epithelial Conduction in Hydromedusae
Mackie, G. O., & Passano, L. M. (1968) · The Journal of General Physiology · doi:10.1085/jgp.52.4.600 · Cited by 150 · see citing works
Assembly of the cnidarian camera-type eye from vertebrate-like components
Kozmik, Z., Ruzickova, J., Jonasova, K., Matsumoto, Y., Vopalensky, P., Kozmikova, I., Strnad, H., Kawamura, S., Piatigorsky, J., Paces, V., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800388105 · Cited by 147 · see citing works
Metamorphosin A: A Novel Peptide Controlling Development of the Lower Metazoan Hydractinia echinata (Coelenterata, Hydrozoa)
Leitz, T., Morand, K. L., & Mann, M. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1160 · Cited by 145 · see citing works
Cnidarians as a model system for understanding evolution and regeneration
Galliot, B., & Schmid, V. J. (2002) · The International Journal of Developmental Biology · doi:10.1387/ijdb.11902686 · Cited by 143 · see citing works
Self-citation
Evolutionary conservation of a cell fate specification gene: the Hydra achaete-scute homolog has proneural activity in Drosophila
Grens, A., Mason, E., Marsh, J. L., & Bode, H. R. (1995) · Development · doi:10.1242/dev.121.12.4027 · Cited by 143 · see citing works
Genetic analysis of developmental mechanisms in hydra. ii. isolation and characterization of an interstitial cell-deficient strain
Sugiyama, T., & Fujisawa, T. (1978) · Journal of Cell Science · doi:10.1242/jcs.29.1.35 · Cited by 142 · see citing works
Emerging roles for zic genes in early development
Merzdorf, C. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21098 · Cited by 140 · see citing works
Hydra and the evolution of stem cells
Bosch, T. C. G. (2009) · BioEssays · doi:10.1002/bies.200800183 · Cited by 140 · see citing works
Early mesencephalon/metencephalon patterning and development of the cerebellum.
Wassef, M., & Joyner, A. L. (1997) · PubMed · Cited by 139 · see citing works
Photoreceptors of cnidarians
Martin, V. J. (2002) · Canadian Journal of Zoology · doi:10.1139/z02-136 · Cited by 139 · see citing works
THE LIGHT RESPONSE AND THE RHYTHMIC POTENTIALS OF HYDRA
Passano, L. M., & McCullough, C. B. (1962) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.48.8.1376 · Cited by 137 · see citing works
floating head and masterblind Regulate Neuronal Patterning in the Roof of the Forebrain
Masai, I., Heisenberg, C., Barth, K., MacDonald, R. E., Adamek, S., & Wilson, S. W. (1997) · Neuron · doi:10.1016/s0896-6273(01)80045-3 · Cited by 136 · see citing works
The Hedgehog gene family of the cnidarian, Nematostella vectensis, and implications for understanding metazoan Hedgehog pathway evolution
Matus, 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
Localized expression of a dpp / BMP2 / 4 ortholog in a coral embryo
Hayward, D. C., Samuel, G., Pontynen, P. C., Catmull, J., Saint, R., Miller, D. J., & Ball, E. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.112021499 · Cited by 132 · see citing works
Physiology of a bidirectional, excitatory, chemical synapse
Anderson, P. A. V. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.53.3.821 · Cited by 132 · see citing works
Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria)
Denker, E., Manuel, M., Leclère, L., Guyader, H. L., & Rabet, N. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.12.023 · Cited by 130 · see citing works
Developmental Signaling in Hydra: What Does It Take to Build a “Simple” Animal?
Steele, R. E. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0744 · Cited by 129 · see citing works
The nervous systems of Cnidarians
Grimmelikhuijzen, C. J. P., & Westfall, J. A. (1995) · Experientia Supplementum · doi:10.1007/978-3-0348-9219-3_2 · Cited by 128 · see citing works
Central Neural Circuitry in the Jellyfish Aglantha
Mackie, G. O. (2004) · Neurosignals · doi:10.1159/000076155 · Cited by 128 · see citing works
FMRFamide immunoreactivity in the nervous system of the medusa Polyorchis penicillatus
Grimmelikhuijzen, C. J. P., & Spencer, A. N. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902300305 · Cited by 128 · see citing works
Molecular mechanism of chicken ovalbumin upstream promoter-transcription factor (COUP-TF) actions
Park, J., Tsai, S. Y., & Tsai, M. (2003) · The Keio Journal of Medicine · doi:10.2302/kjm.52.174 · Cited by 126 · see citing works
Transgenic stem cells in Hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation
Khalturin, 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 · see citing works
Pax genes and eye organogenesis
Pichaud, F., & Desplan, C. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00321-0 · Cited by 124 · see citing works
A simple visual system without neurons in jellyfish larvae
Nordström, K., Wallén, Seymour, J., & Nilsson, D. (2003) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.2003.2504 · Cited by 121 · see citing works
The origin and evolution of the nervous system
Ghysen, A. (2003) · The International Journal of Developmental Biology · doi:10.1387/ijdb.14756331 · Cited by 120 · see citing works
Pax gene diversity in the basal cnidarian Acropora millepora (Cnidaria, Anthozoa): Implications for the evolution of the Pax gene family
Miller, D. J., Hayward, D. C., Reece-Hoyes, J. S., Scholten, I., Catmull, J., Gehring, W. J., Callaerts, P., Larsen, J. E., & Ball, E. E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4475 · Cited by 119 · see citing works
Neuropeptides in cnidarians
Grimmelikhuijzen, C. J. P., Williamson, M., & Hansen, G. N. (2002) · Canadian Journal of Zoology · doi:10.1139/z02-137 · Cited by 119 · see citing works
Axial Patterning and Diversification in the Cnidaria Predate the Hox System
Kamm, K., Schierwater, B., Jakob, W., Dellaporta, S. L., & Miller, D. J. (2006) · Current Biology · doi:10.1016/j.cub.2006.03.036 · Cited by 116 · see citing works
EvoD/Vo: the origins of BMP signalling in the neuroectoderm
Mizutani, C. M., & Bier, E. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2417 · Cited by 113 · see citing works
A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra
Takahashi, T., Koizumi, O., Ariura, Y., Romanovitch, A. E., Bosch, T. C. G., Kobayakawa, Y., MOHRI, S., Bode, H. R., Yum, S., Hatta, M., et al. (2000) · Development · doi:10.1242/dev.127.5.997 · Cited by 112 · see citing works
Pacemaker Hierarchies Controlling the Behaviour of Hydras
Passano, L. M., & MCCULLOUGH, C. B. (1963) · Nature · doi:10.1038/1991174a0 · Cited by 101 · see citing works
HyBMP5-8b , a BMP5-8 orthologue, acts during axial patterning and tentacle formation in hydra
Reinhardt, B., Broun, M., Blitz, I. L., & Bode, H. R. (2003) · Developmental Biology · doi:10.1016/j.ydbio.2003.10.031 · Cited by 101 · see citing works
A peptide-gated ion channel from the freshwater polyp Hydra
Golubovic, A., Kuhn, A., Williamson, M., Kalbacher, H., Holstein, T. W., Grimmelikhuijzen, C. J. P., & Gründer, S. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m706849200 · Cited by 101 · see citing works
LWamides from Cnidaria constitute a novel family of neuropeptides with morphogenetic activity
Gajewski, M., Leitz, T., Schlo�herr, J., & Plickert, G. (1996) · Development Genes and Evolution · doi:10.1007/bf00365801 · Cited by 100 · see citing works
The Notch signaling pathway in the cnidarian Hydra
Käsbauer, T., Towb, P., Alexandrova, O., David, C. N., Dall'Armi, E., Staudigl, A., Stiening, B., & Böttger, A. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.11.022 · Cited by 99 · see citing works
Conservation of Hox/ParaHox-Related Genes in the Early Development of a Cnidarian
Yanze, N., Spring, J., Schmidli, C., & Schmid, V. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0299 · Cited by 99 · see citing works
The nervous systems of invertebrates: An evolutionary and comparative approach
Horridge, G. A. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)90003-9 · Cited by 98 · see citing works
Are Hox Genes Ancestrally Involved in Axial Patterning? Evidence from the Hydrozoan Clytia hemisphaerica (Cnidaria)
Chiori, R., Jager, M., Denker, E., Wincker, P., Silva, C. D., Guyader, H. L., Manuel, M., & Quéinnec, É. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004231 · Cited by 97 · see citing works
CnOtx, a Member of the Otx Gene Family, Has a Role in Cell Movement in Hydra
Smith, K. M., Gee, L., Blitz, I. L., & Bode, H. R. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9337 · Cited by 96 · see citing works
The Sine oculis/Six class family of homeobox genes in jellyfish with and without eyes: development and eye regeneration
Stierwald, M., Yanze, N., Bamert, R. P., Kammermeier, L., & Schmid, V. J. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.06.018 · Cited by 95 · 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
Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system
Miljkovic‐Licina, M., Gauchat, D., & Galliot, B. (2004) · Biosystems · doi:10.1016/j.biosystems.2004.05.030 · Cited by 93 · see citing works
Self-citation
FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian
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
Cngsc, a homologue of goosecoid, participates in the patterning of the head, and is expressed in the organizer region of Hydra
Broun, M., Sokol, S. Y., & Bode, H. R. (1999) · Development · doi:10.1242/dev.126.23.5245 · Cited by 91 · see citing works
Expression of Pax gene family members in the anthozoan cnidarian, Nematostella vectensis
Matus, D. Q., Pang, K., Daly, M., & Martindale, M. Q. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2006.00135.x · Cited by 91 · see citing works
Silencing of the hydra serine protease inhibitorKazal1gene mimics the humanSPINK1pancreatic phenotype
Chera, S., de Rosa, R., Miljkovic‐Licina, M., Dobretz, K., Ghila, L., Kaloulis, K., & Galliot, B. (2006) · Journal of Cell Science · doi:10.1242/jcs.02807 · Cited by 90 · see citing works
Self-citation
Head regeneration in wild-type hydra requires de novo neurogenesis
Miljkovic‐Licina, M., Chera, S., Ghila, L., & Galliot, B. (2007) · Development · doi:10.1242/dev.02804 · Cited by 90 · see citing works
Self-citation
The evolutionary emergence of cell type-specific genes inferred from the gene expression analysis of Hydra
Hwang, J. S., Ohyanagi, H., Hayakawa, S., Osato, N., Nishimiya‐Fujisawa, C., Ikeo, K., David, C. N., Fujisawa, T., & Gojobori, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0703331104 · Cited by 89 · see citing works
Beyond the Hox: how widespread is homeobox gene clustering?
Holland, P. W. H. (2001) · Journal of Anatomy · doi:10.1046/j.1469-7580.199.parts1-2.3.x · Cited by 89 · see citing works
The evolution of homeobox genes: Implications for the study of brain development.
Holland, P., & Takahashi, T. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.06.003 · Cited by 88 · see citing works
Neuronal cell fate specification in Drosophila
Jan, Y. N., & Jan, L. Y. (1994) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(94)90025-6 · Cited by 88 · see citing works
Nerve ring of the hypostome in Hydra. I. Its structure, development, and maintenance
Koizumi, O., Itazawa, M., Mizumoto, H., Minobe, S., Javois, L. C., Grimmelikhuijzen, C. J. P., & Bode, H. R. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903260103 · Cited by 88 · see citing works
Neuropeptides in Cnidarians
Grimmelikhuijzen, C. J. P., Williamson, M. P., & Hansen, G. N. (2004) · Springer eBooks · doi:10.1007/978-94-017-0998-9_5 · Cited by 86 · see citing works
An 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
Ultrastructural evidence for two‐cell and three‐cell neural pathways in the tentacle epidermis of the sea anemone Aiptasia pallida
Westfall, J. A., Elliott, C. F., & Carlin, R. W. (2002) · Journal of Morphology · doi:10.1002/jmor.1075 · Cited by 83 · see citing works
A Novel Neuropeptide, Hym-176, Induces Contraction of the Ectodermal Muscle in Hydra
Yum, S., Takahashi, T., Koizumi, O., Ariura, Y., Kobayakawa, Y., Mohri, S., & Fujisawa, T. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.8831 · Cited by 82 · see citing works
An ancient chordin-like gene in organizer formation of Hydra
Rentzsch, F., Guder, C., Vocke, D., Hobmayer, B., & Holstein, T. W. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604501104 · Cited by 81 · see citing works
Plasticity in the nervous system of adult hydra
Koizumi, O., & Bode, H. R. (1986) · Developmental Biology · doi:10.1016/0012-1606(86)90142-9 · Cited by 80 · see citing works
Rhopalia are integrated parts of the central nervous system in box jellyfish
Garm, A., Ekström, P., Boudes, M., & Nilsson, D.-E. (2006) · Cell and Tissue Research · doi:10.1007/s00441-005-0134-8 · Cited by 79 · see citing works
Gene structure and larval expression of cnox-2Am from the coral Acropora millepora
C. Hayward, D., Catmull, J., Reece-Hoyes, J. S., Berghammer, H., Dodd, H., Hann, S. J., Miller, D. J., & Ball, E. E. (2001) · Development Genes and Evolution · doi:10.1007/s004270000112 · Cited by 79 · see citing works
Ultrastructure of synapses in the first-evolved nervous systems
Westfall, J. A. (1996) · Journal of Neurocytology · doi:10.1007/bf02284838 · Cited by 78 · see citing works
Eye evolution: a question of genetic promiscuity
Nilsson, D. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.07.004 · Cited by 76 · see citing works
Polarised expression of FoxB and FoxQ2 genes during development of the hydrozoan Clytia hemisphaerica
Chevalier, S., Martin, A., Leclère, L., Amiel, A., & Houliston, E. (2006) · Development Genes and Evolution · doi:10.1007/s00427-006-0103-6 · Cited by 75 · see citing works
Control of planula migration by LWamide and RFamide neuropeptides inHydractinia echinata
Katsukura, Y., Andō, H., David, C. N., Grimmelikhuijzen, C. J. P., & Sugiyama, T. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.00974 · Cited by 75 · see citing works
Expansion of the SOX gene family predated the emergence of the Bilateria
Jager, M., Quéinnec, É., Houliston, E., & Manuel, M. (2006) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.12.005 · Cited by 73 · see citing works
The Evolution of Chordate Neural Segmentation
Mazet, F., & Shimeld, S. M. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0831 · Cited by 73 · see citing works
Components of both major axial patterning systems of the Bilateria are differentially expressed along the primary axis of a ‘radiate’ animal, the anthozoan cnidarian Acropora millepora
de Jong, D. M., Hislop, N. R., Hayward, D. C., Reece-Hoyes, J. S., Pontynen, P. C., Ball, E. E., & Miller, D. J. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.07.034 · Cited by 71 · see citing works
Early development, pattern, and reorganization of the planula nervous system in Aurelia (Cnidaria, Scyphozoa)
Nakanishi, N., Yuan, D., Jacobs, D. K., & Hartenstein, V. (2008) · Development Genes and Evolution · doi:10.1007/s00427-008-0239-7 · Cited by 71 · see citing works
A wide-range phylogenetic analysis of Zic proteins: Implications for correlations between protein structure conservation and body plan complexity
Aruga, J., Kamiya, A., Takahashi, H., Fujimi, T. J., Shimizu, Y., Ohkawa, K., Yazawa, S., Umesono, Y., Noguchi, H., Shimizu, T., et al. (2006) · Genomics · doi:10.1016/j.ygeno.2006.02.011 · Cited by 71 · see citing works
Reactivation of developmental programs: The cAMP-response element-binding protein pathway is involved in hydra head regeneration
Kaloulis, K., Chera, S., Hassel, M., Gauchat, D., & Galliot, B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306512101 · Cited by 70 · see citing works
Self-citation
Developmental roles of epithelial and interstitial cell lineages in hydra: Analysis of chimeras
Marcum, B. A., & Campbell, R. D. (1978) · Journal of Cell Science · doi:10.1242/jcs.32.1.233 · Cited by 70 · see citing works
Evolutionary aspects of developmentally regulated helix-loop-helix transcription factors in striated muscle of jellyfish
Müller, P., Seipel, K., Yanze, N., Reber-Müller, S., Streitwolf-Engel, R., Stierwald, M., Spring, J. Ü., & Schmid, V. (2003) · Developmental Biology · doi:10.1016/s0012-1606(02)00091-x · Cited by 69 · see citing works
Larval development in Cnidaria: A connection to bilateria?
Gröger, H., & Schmid, V. J. (2001) · genesis · doi:10.1002/gene.1013 · Cited by 69 · see citing works
Hydra regeneration and epitheliopeptides
Fujisawa, T. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10221 · Cited by 68 · see citing works
The ring nerve of the box jellyfish Tripedalia cystophora
Garm, A. L., Poussart, Y., Parkefelt, L., Ekström, P., & Nilsson, D.-E. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0393-7 · Cited by 67 · see citing works
Hyzic, theHydrahomolog of thezic/odd-pairedgene, is involved in the early specification of the sensory nematocytes
Lindgens, D., Holstein, T. W., & Technau, U. (2003) · Development · doi:10.1242/dev.00903 · Cited by 66 · see citing works
The importance of cnidarian synapses for neurobiology
Anderson, P. A. V., & Spencer, A. N. (1989) · Journal of Neurobiology · doi:10.1002/neu.480200513 · Cited by 66 · see citing works
prdl-a, a gene marker for hydra apical differentiation related to triploblastic paired-like head-specific genes
Gauchat, D., Kreger, S., Holstein, T. W., & Galliot, B. (1998) · Development · doi:10.1242/dev.125.9.1637 · Cited by 66 · see citing works
Self-citation
Origin of anterior patterning
Galliot, B., & Miller, D. J. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(99)01888-0 · Cited by 65 · see citing works
Self-citation
Inhibition of metamorphosis by RFamide neuropeptides in planula larvae of Hydractinia echinata
Katsukura, Y., David, C. N., Grimmelikhuijzen, C. J. P., & Sugiyama, T. (2003) · Development Genes and Evolution · doi:10.1007/s00427-003-0361-5 · Cited by 64 · see citing works
atonal- and achaete-scute-related genes in the annelid Platynereis dumerilii: insights into the evolution of neural basic-Helix-Loop-Helix genes
Simionato, E., Kerner, P., Dray, N., Gouar, M. L., Ledent, V., Arendt, D., & Vervoort, M. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-170 · Cited by 64 · see citing works
The cAMP Response Element Binding protein is involved in hydra regeneration
Galliot, B., Welschof, M., Schuckert, O., Hoffmeister, S. A. H., & Schaller, H. (1995) · Development · doi:10.1242/dev.121.4.1205 · Cited by 64 · see citing works
Self-citation
Expression of a Hox gene, Cnox-2, and the division of labor in a colonial hydroid
Cartwright, P., Bowsher, J. H., & Buss, L. W. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.5.2183 · Cited by 63 · see citing works
Hydra Peptide Project 1993–2007
Fujisawa, T. (2008) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2008.00997.x · Cited by 63 · see citing works
Developmental and evolutionary aspects of the basic helix–loop–helix transcription factors Atonal-like 1 and Achaete-scute homolog 2 in the jellyfish
Seipel, K., Yanze, N., & Schmid, V. J. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.01.035 · Cited by 62 · see citing works
Homologs of vascular endothelial growth factor and receptor, VEGF and VEGFR, in the jellyfish Podocoryne carnea
Seipel, K., Eberhardt, M., Müller, P., Pescia, E., Yanze, N., & Schmid, V. J. (2004) · Developmental Dynamics · doi:10.1002/dvdy.20139 · Cited by 62 · see citing works
Protochordate Zic genes define primitive somite compartments and highlight molecular changes underlying neural crest evolution
Gostling, N. J., & Shimeld, S. M. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03020.x · Cited by 62 · see citing works
Role of the neuropeptide head activator for growth and development in hydra and mammals
Schaller, H. C., Hoffmeister, S. A. H., & DUBEL, S. J. (1989) · Development · doi:10.1242/dev.107.supplement.99 · Cited by 61 · see citing works
A Dickkopf-3-related gene is expressed in differentiating nematocytes in the basal metazoan Hydra
Fedders, H., Augustin, R., & Bosch, T. C. G. (2004) · Development Genes and Evolution · doi:10.1007/s00427-003-0378-9 · Cited by 60 · see citing works
The Trichoplax PaxB Gene: A Putative Proto-PaxA/B/C Gene Predating the Origin of Nerve and Sensory Cells
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Plasticity in the nervous system of adult hydra
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sine oculis in basal Metazoa
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Self-citation
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Wassarman, P. M. (1992) · Medical Entomology and Zoology · Cited by 55 · see citing works
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Mokady, O., Dick, M. H., Lackschewitz, D., Schierwater, B., & Buss, L. W. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3673 · Cited by 53 · see citing works
Structure, histochemistry, ontogenetic development, and regeneration of the ocellus of Cladonema radiatum dujardin (cnidaria, hydrozoa, anthomedusae)
Weber, C. (1981) · Journal of Morphology · doi:10.1002/jmor.1051670306 · Cited by 53 · see citing works
Involvement of Hydra achaete–scute gene CnASH in the differentiation pathway of sensory neurons in the tentacles
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Characterization and expression analysis of an ancestor-type Pax gene in the hydrozoan jellyfish Podocoryne carnea
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The Embryonic Origin of Neurosensory Cells and the Role of Nerve Cells in Metamorphosis inPhialidium gregarium(Cnidaria, Hydrozoa)
Thomas, M. B., Freeman, G., & Martin, V. J. (1987) · International Journal of Invertebrate Reproduction and Development · doi:10.1080/01688170.1987.10510286 · Cited by 53 · see citing works

Flagged first, then by citations

Research works printed but not linked: 2

Bouillon, J., 1994b. Embranchement des cnidaires (Cnidaria). In: Grassé, P.P. (Ed.), Traité de Zoologie. Cnidaires, Cténaires, III. Fascicule II. Masson, Paris, pp. 1-28.
Holstein, T., Emschermann, P., 1995. Zytologie. In: Schwoerbel, J., Zwick, P. (Eds.), Cnidaria: Hydrozoa, Kamptozoa, 1. Gustav Fisher Verlag, Stuttgart, pp. 5-15.

Sorted by citations

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Self-citation
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Self-citation
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Self-citation
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Self-citation
"A Key Innovation in Animal Evolution, the Emergence of Neurogenesis
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Authors: Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., & Chera, S.
Affiliations: University of Geneva (CH)
Corresponding author: Galliot, Brigitte
ORCID: Galliot, Brigitte
Ghila, Luiza
Chera, Simona
Venue: Developmental Biology
Publisher: Elsevier BV
Published: 2009-08
Volume: 332
Issue: 1
Pages: 2-24
ISSN: 0012-1606 (ISSN-L)
DOI: 10.1016/j.ydbio.2009.05.563
OpenAlex: W2037815161
Cited by: 168
References: 274
Citations by year: 2026: 2 · 2025: 8 · 2024: 9 · 2023: 8 · 2022: 6 · 2021: 5 · 2020: 8 · 2019: 12 · 2018: 6 · 2017: 13 · 2016: 5 · 2015: 19 · 2014: 14 · 2013: 12 · 2012: 14
FWCI: 1.40
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1446 d)
Locations: Developmental Biology (publishedVersion)
PubMed (publishedVersion)
Archive ouverte UNIGE (University of Geneva) (acceptedVersion, other-oa)
Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
Funders: Canton de Genève
Topics: Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: Cnidaria, sponges, gene duplication, ParaHox genes, Hox genes, Acropora corals, nematocytes, stem cells, neuromuscular transmission
MeSH terms: Animals, Cnidaria, Biological Evolution, Nervous System, Neurogenesis

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