Budhead,a Fork Head/HNF-3 Homologue, Is Expressed during Axis Formation and Head Specification in Hydra
Open accessAbstract
Accumulating evidence indicates that a common set of genes and mechanisms regulates the developmental processes of a variety of triploblastic organisms despite large variation in their body plans. To what extent these same genes and mechanisms are also conserved among diploblasts, which arose earlier in metazoan evolution, is unclear. We have characterized a hydra homologue of the fork head/HNF-3 class of winged-helix proteins, termed budhead, whose expression patterns suggest a role(s) similar to that found in vertebrates. The vertebrate HNF-3 beta homologues are expressed early in embryogenesis in regions that have organizer properties, and later they have several roles, among them an important role in rostral head formation. In the adult hydra, where axial patterning processes are continuously active, budhead is expressed in the upper part of the head, which has organizer properties. It is also expressed during the formation of a new axis as part of the development of a bud, hydra's asexual form of reproduction. Expression during later stages of budding, during head regeneration and the formation of ectopic heads, indicates a role in head formation. It is likely that budhead plays a critical role in head as well as axis formation in hydra.
Integrity signals
Registry
Cites
Statistics
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?
Fox gene expression in Nematostella and Hydra suggests that the mucociliary epithelium around the gastric opening represents the ancient site of activity of the foxA, B, C, D, E superfamily.
“in Nematostella, foxB [122] and foxA [123] are expressed in the ectodermal ciliated pharynx and foxC [122] in pharyngeal endoderm; in Hydra, foxA/budhead [124] is likewise expressed in the endoderm around the oral opening, suggesting that the mucociliary epithelium around the gastric opening represents the ancient site of activity of the foxA, B, C, D, E superfamily.”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [124]
Cites
Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589 · see citing works
Molecular cloning: A laboratory manual
Deininger, P. L. (1990) · Analytical Biochemistry · doi:10.1016/0003-2697(90)90595-z · Cited by 84,684 · see citing works
Frohman, M. A., Dush, M. K., & Martin, G. R. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.23.8998 · Cited by 4,545 · see citing works
PAUP (phylogenetic analysis using parsimony)
(2008) · Springer eBooks · doi:10.1007/978-1-4020-6754-9_12413 · Cited by 4,424 · see citing works
Homeobox genes and axial patterning
McGinnis, W., & Krumlauf, R. (1992) · Cell · doi:10.1016/0092-8674(92)90471-n · Cited by 2,674 · see citing works
Appendix G: In Situ Hybridization: An Improved Whole-Mount Method for Xenopus Embryos
Harland, R. M. (1991) · Methods in cell biology · doi:10.1016/s0091-679x(08)60307-6 · Cited by 2,048 · see citing works
2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans
Wilson, R. K., Ainscough, R., Anderson, K., Baynes, C., Berks, M., Bonfield, J., Burton, J., Connell, M. A. O., Copsey, T., Cooper, J., et al. (1994) · Nature · doi:10.1038/368032a0 · Cited by 1,459 · see citing works
In situ hybridization; a practical approach
(1993) · International Journal of Biochemistry · doi:10.1016/0020-711x(93)90093-t · Cited by 1,240 · see citing works
HNF-3β is essential for node and notochord formation in mouse development
Ang, S., & Rossant, J. (1994) · Cell · doi:10.1016/0092-8674(94)90522-3 · Cited by 981 · see citing works
Weigel, D., Jürgens, G., Küttner, F., Seifert, E., & Jäckle, H. (1989) · Cell · doi:10.1016/0092-8674(89)90133-5 · Cited by 794 · see citing works
Weinstein, D. C., Altaba, A. R. I., Chen, W. S., Hoodless, P. A., Prezioso, V. R., Jessell, T. M., & Darnell, J. E., Jr. (1994) · Cell · doi:10.1016/0092-8674(94)90523-1 · Cited by 783 · see citing works
Sasaki, H., & Hogan, B. L. M. (1993) · Development · doi:10.1242/dev.118.1.47 · Cited by 672 · see citing works
Five years on the wings of fork head
Kaufmann, E., & Knöchel, W. (1996) · Mechanisms of Development · doi:10.1016/0925-4773(96)00539-4 · Cited by 660 · see citing works
In situ hybridization; a practical approach
(1993) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(93)90060-h · Cited by 652 · see citing works
Monaghan, A. P., Kaestner, K. H., Grau, E., & Schütz, G. (1993) · Development · doi:10.1242/dev.119.3.567 · Cited by 497 · see citing works
Tao, W., & Lai, E. (1992) · Neuron · doi:10.1016/0896-6273(92)90210-5 · Cited by 415 · see citing works
Altaba, A. R. I., & Jessell, T. M. (1992) · Development · doi:10.1242/dev.116.1.81 · Cited by 329 · see citing works
HNF-3β as a regulator of floor plate development
Sasaki, H., & Hogan, B. L. M. (1994) · Cell · doi:10.1016/0092-8674(94)90176-7 · Cited by 295 · see citing works
Strähle, U., Blader, P., Henrique, D., & Ingham, P. W. (1993) · Genes & Development · doi:10.1101/gad.7.7b.1436 · Cited by 279 · see citing works
Pattern formation. A primer in developmental biology
Swanson, G. (1985) · FEBS Letters · doi:10.1016/0014-5793(85)81359-4 · Cited by 257 · see citing works
Tissue dynamics of steady state growth in Hydra littoralis. II. Patterns of tissue movement
Campbell, R. D. (1967) · Journal of Morphology · doi:10.1002/jmor.1051210103 · Cited by 238 · see citing works
The Ras signaling pathway in Drosophila
Wassarman, D. A., Therrien, M., & Rubin, G. M. (1995) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(95)90052-7 · Cited by 233 · see citing works
Clevidence, D. E., Overdier, D. G., Tao, W., Qian, X., Pani, L., Lai, E., & Costa, R. H. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.9.3948 · Cited by 230 · see citing works
Grossniklaus, U., Pearson, R. K., & Gehring, W. J. (1992) · Genes & Development · doi:10.1101/gad.6.6.1030 · Cited by 229 · see citing works
McGinnis, N., Kuziora, M. A., & McGinnis, W. J. (1990) · Cell · doi:10.1016/0092-8674(90)90500-e · Cited by 225 · see citing works
Dirksen, M., & Jamrich, M. (1992) · Genes & Development · doi:10.1101/gad.6.4.599 · Cited by 225 · see citing works
Self-citationTissue dynamics of steady state growth in Hydra littoralis
Campbell, R. D. (1967) · Developmental Biology · doi:10.1016/0012-1606(67)90039-5 · Cited by 217 · see citing works
Kaestner, K. H., Hiemisch, H., Luckow, B., & Schütz, G. (1994) · Genomics · doi:10.1006/geno.1994.1191 · Cited by 204 · see citing works
CnNK-2,an NK-2 Homeobox Gene, Has a Role in Patterning the Basal End of the Axis in Hydra
Grens, A., Gee, L., Fisher, D. A., & Bode, H. R. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0321 · Cited by 192 · see citing works
Self-citationPani, L., Overdier, D. G., Porcella, A., Qian, X., Lai, E., & Costa, R. H. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.9.3723 · Cited by 188 · see citing works
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
Detection of homeobox genes in development and evolution.
Murtha, M. T., Leckman, J. F., & Ruddle, F. H. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.23.10711 · Cited by 168 · see citing works
Miller, L. M., Gallegos, M. E., Morisseau, B. A., & Kim, S. K. (1993) · Genes & Development · doi:10.1101/gad.7.6.933 · Cited by 164 · see citing works
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
Self-citationBudding inHydra attenuata:Bud stages and fate map
Otto, J. J., & Campbell, R. D. (1977) · Journal of Experimental Zoology · doi:10.1002/jez.1402000311 · Cited by 143 · see citing works
Six members of the mouse forkhead gene family are developmentally regulated.
Kaestner, K. H., Lee, K. H., Schlöndorff, J. S., Hiemisch, H., Monaghan, A. P., & Schütz, G. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.16.7628 · Cited by 143 · see citing works
MORPHOGENESIS AND PATTERN FORMATION IN HYDROIDS
Webster, G. (1971) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1971.tb01178.x · Cited by 132 · see citing works
Shenk, M. A., Bode, H. R., & Steele, R. E. (1993) · Development · doi:10.1242/dev.117.2.657 · Cited by 129 · see citing works
Self-citationDevelopmentally regulated Drosophila gene family encoding the fork head domain.
Häcker, U., Grossniklaus, U., Gehring, W. J., & Jäckle, H. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.18.8754 · Cited by 118 · see citing works
Altaba, A. R. I., Placzek, M., Baldassare, M., Dodd, J., & Jessell, T. M. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1216 · Cited by 117 · see citing works
Knöchel, S., Lef, J., Clement, J. H., Klocke, B., Hille, S., Köster, M., & Knöchel, W. (1992) · Mechanisms of Development · doi:10.1016/0925-4773(92)90007-7 · Cited by 109 · see citing works
Studies on pattern regulation in hydra
Webster, G., & Wolpert, L. (1966) · Development · doi:10.1242/dev.16.1.91 · Cited by 107 · see citing works
Li, C., Lai, C.-C., Sigman, D. S., & Gaynor, R. B. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.17.7739 · Cited by 107 · see citing works
Denmat, S. H., Werner, M., Sentenac, A., & Thuriaux, P. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.5.2905 · Cited by 103 · see citing works
Bassel‐Duby, R., Hernandez, M. D., Yang, Q., Rochelle, J. M., Seldin, M. F., & Williams, R. S. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.7.4596 · Cited by 102 · see citing works
Pattern Formation: A Primer in Developmental Biology
Malacinski, G. M., & Bryant, S. V. (1984) · Medical Entomology and Zoology · Cited by 87 · see citing works
Altaba, A. R. I., Cox, C. M., Jessell, T. M., & Klar, A. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.17.8268 · Cited by 87 · see citing works
Cloning and Biological Function of Laminin in Hydra vulgaris
Sarras, M. P., Li, Y., Grens, A., Zhang, X., Aǵbaş, A., Huff, J. K., John, P. L. S., & Abrahamson, D. R. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1201 · Cited by 82 · see citing works
Nardelli‐Haefliger, D., & Shankland, M. (1992) · Development · doi:10.1242/dev.116.3.697 · Cited by 78 · see citing works
Experimental and Theoretical Advances in Biological Pattern Formation
Othmer, H. G., Maini, P. K., & Murray, J. D. (1993) · Springer eBooks · doi:10.1007/978-1-4615-2433-5 · Cited by 76 · see citing works
Schierwater, B., Murtha, M. T., Dick, M. H., Ruddle, F. H., & Buss, L. W. (1991) · Journal of Experimental Zoology · doi:10.1002/jez.1402600316 · Cited by 75 · see citing works
Pattern formation in the immortal Hydra
Müller, W. A. (1996) · Trends in Genetics · doi:10.1016/0168-9525(96)81419-3 · Cited by 73 · see citing works
Differential expression of fork head genes during early Xenopus and zebrafish development
Dirksen, M., & Jamrich, M. (1995) · Developmental Genetics · doi:10.1002/dvg.1020170203 · Cited by 66 · see citing works
Self-citationMüller, W. A. (1990) · Differentiation · doi:10.1111/j.1432-0436.1990.tb00754.x · Cited by 62 · see citing works
Ras pathways in Caenorhabditis elegans
Kayne, P. S., & Sternberg, P. W. (1995) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(95)90051-9 · Cited by 62 · see citing works
Expression of Cnox-2, a HOM/HOX Gene, Is Suppressed during Head Formation in Hydra
Shenk, M. A., Gee, L., Steele, R. E., & Bode, H. R. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1290 · Cited by 61 · see citing works
Self-citationTranscription factors and head formation in vertebrates
Bally‐Cuif, L., & Boncinelli, E. (1997) · BioEssays · doi:10.1002/bies.950190207 · Cited by 59 · see citing works
Kuhn, K., Streit, B., & Schierwater, B. (1996) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.1996.0055 · Cited by 58 · see citing works
Zhu, G., Muller, E. G., Amacher, S. L., Northrop, J. L., & Davis, T. N. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.3.1779-1787.1993 · Cited by 57 · see citing works
Aerne, B. L., Baader, C. D., & Schmid, V. J. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1168 · Cited by 54 · see citing works
Specification of anteroposterior cell fates in Caenorhabditis elegans by Drosophila Hox proteins
Hunter, C. P., & Kenyon, C. J. (1995) · Nature · doi:10.1038/377229a0 · Cited by 52 · see citing works
INTERCELLULAR SIGNALING AND SIGNAL TRANSDUCTION IN C. ELEGANS
Sternberg, P. W. (1993) · Annual Review of Genetics · doi:10.1146/annurev.ge.27.120193.002433 · Cited by 51 · see citing works
Holland, P. W. H., Ingham, P. W., & Krauss, S. J. K. (1992) · Nature · doi:10.1038/358627a0 · Cited by 50 · see citing works
Presence of eight distinct homeobox‐containing genes in cnidarians
Naito, M., Ishiguro, H., Fujisawa, T., & Kurosawa, Y. (1993) · FEBS Letters · doi:10.1016/0014-5793(93)80668-k · Cited by 44 · see citing works
Mackem, S., & Mahon, K. A. (1991) · Development · doi:10.1242/dev.112.3.791 · Cited by 43 · see citing works
Sugiyama, T., & Fujisawa, T. (1977) · Development · doi:10.1242/dev.42.1.65 · Cited by 41 · see citing works
Miles, A., & Miller, D. J. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0057 · Cited by 36 · see citing works
Hope, I. A. (1994) · Development · doi:10.1242/dev.120.3.505 · Cited by 32 · see citing works
Cell differentiation in the head of Hydra
DUBEL, S. J. (1989) · Differentiation · doi:10.1111/j.1432-0436.1989.tb00737.x · Cited by 30 · see citing works
Studies On the Organizer Problem in Pelmatohydra Oligactis
Li, H. P., & Yao, T. (1945) · Journal of Experimental Biology · doi:10.1242/jeb.21.3-4.155 · Cited by 30 · see citing works
Avian cellular homolog of the qin oncogene.
Chang, H. W., Li, J., Kretzschmar, D., & Vogt, P. K. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.2.447 · Cited by 28 · see citing works
Sanyal, S. (1966) · PubMed · Cited by 28 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The new animal phylogeny: Reliability and implications
Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud'homme, B., & de Rosa, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4453 · Cited by 512 · see citing works
Regulatory phases of early liver development: paradigms of organogenesis
Zaret, K. S. (2002) · Nature Reviews Genetics · doi:10.1038/nrg837 · Cited by 504 · see citing works
Martindale, M. Q., Pang, K., & Finnerty, J. R. (2004) · Development · doi:10.1242/dev.01119 · Cited by 396 · see citing works
Stem cell differentiation trajectories in Hydra resolved at single-cell resolution
Siebert, S., Farrell, J. A., Cazet, J. F., Abeykoon, Y., Primack, A. S., Schnitzler, C. E., & Juliano, C. E. (2019) · Science · doi:10.1126/science.aav9314 · Cited by 350 · see citing works
Formation of the head organizer in hydra involves the canonical Wnt pathway.
Broun, M., Gee, L., Reinhardt, B., & Bode, H. R. (2005) · Development · doi:10.1242/dev.01848 · Cited by 287 · see citing works
Self-citationCnidarians: An evolutionarily conserved model system for regeneration?
Holstein, T. W., Hobmayer, E., & Technau, U. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10227 · Cited by 225 · 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
Zaret, K. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9228 · Cited by 209 · see citing works
HyBra1, a Brachyury homologue, acts during head formation in Hydra
Technau, U., & Bode, H. R. (1999) · Development · doi:10.1242/dev.126.5.999 · Cited by 201 · see citing works
Self-citationSilencing of Developmental Genes in Hydra
Lohmann, J. U., Endl, I., & Bosch, T. C. G. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9407 · Cited by 204 · see citing works
Bosch, T. C. G. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.12.012 · Cited by 186 · see citing works
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
Hydra, a fruitful model system for 270 years
Galliot, B. (2012) · The International Journal of Developmental Biology · doi:10.1387/ijdb.120086bg · Cited by 174 · see citing works
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 · 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
Fritzenwanker, J. H., Saina, M., & Technau, U. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.08.014 · Cited by 165 · 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
Hemmrich, 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 · see citing works
It takes guts: the Drosophila hindgut as a model system for organogenesis.
Lengyel, J., & Iwaki, D. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0577 · Cited by 157 · 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
Bode, H. R. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10225 · Cited by 146 · see citing works
Self-citationAutoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer
Nakamura, Y., Tsiairis, C. D., Özbek, S., & Holstein, T. W. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018109108 · Cited by 134 · see citing works
Characterization of the head organizer in hydra
Broun, M., & Bode, H. R. (2002) · Development · doi:10.1242/dev.129.4.875 · Cited by 127 · see citing works
Self-citationLeontovich, A. A., Zhang, J., Shimokawa, K., Nagase, H., & Sarras, M. P. (2000) · Development · doi:10.1242/dev.127.4.907 · Cited by 128 · see citing works
Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution
Arendt, D., Benito-Gutierrez, E., Brunet, T., & Marlow, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0286 · Cited by 112 · 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
Self-citationβ-catenin plays a central role in setting up the head organizer in hydra
Gee, L., Hartig, J. V., Law, L. Y., Wittlieb, J., Khalturin, K., Bosch, T. C. G., & Bode, H. R. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2009.12.036 · Cited by 105 · see citing works
Self-citationChera, S., Ghila, L., Wenger, Y., & Galliot, B. (2011) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2011.01250.x · Cited by 95 · see citing works
Broun, M., Sokol, S. Y., & Bode, H. R. (1999) · Development · doi:10.1242/dev.126.23.5245 · Cited by 91 · see citing works
Self-citationDunn, E. F., Moy, V. N., Angerer, L. M., Angerer, R. C., Morris, R. L., & Peterson, K. J. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2006.00134.x · Cited by 87 · see citing works
Shimizu, H., Zhang, X., Zhang, J., Leontovich, A. A., Fei, K., Li, Y., & Sarras, M. P. (2002) · Development · doi:10.1242/dev.129.6.1521 · Cited by 81 · see citing works
Homeobox Gene Diversification in the Calcareous Sponge, Sycon raphanus
Manuel, M., & Parco, Y. L. (2000) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.2000.0822 · Cited by 79 · see citing works
FoxO and Stress Responses in the Cnidarian Hydra vulgaris
Bridge, D. M., Theofiles, A. G., Holler, R. L., Marcinkevicius, E., Steele, R. E., & Martínez, D. E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011686 · Cited by 78 · see citing works
Self-citationLartillot, N., Gouar, M. L., & Adoutte, A. (2002) · Development, Genes and Evolution · doi:10.1007/s00427-002-0274-8 · Cited by 73 · see citing works
Evolution of the bilaterian mouth and anus
Nielsen, C., Brunet, T., & Arendt, D. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0641-0 · Cited by 70 · see citing works
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
Reitzel, A. M., Burton, P. M., Krone, C., & Finnerty, J. R. (2007) · Invertebrate Biology · doi:10.1111/j.1744-7410.2007.00081.x · Cited by 77 · see citing works
Oocyte Development in Hydra Involves Selection from Competent Precursor Cells
Miller, M. A., Technau, U., Smith, K. M., & Steele, R. E. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9790 · Cited by 77 · see citing works
Self-citationHydra, a niche for cell and developmental plasticity
Galliot, B., Miljkovic‐Licina, M., de Rosa, R., & Chera, S. (2006) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2006.05.005 · Cited by 73 · see citing works
The genetics of colony form and function in Caribbean Acropora corals
Hemond, E. M., Kaluziak, S. T., & Vollmer, S. V. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-1133 · Cited by 71 · see citing works
Hydra, the everlasting embryo, confronts aging
Martínez, D. E., & Bridge, D. M. (2012) · The International Journal of Developmental Biology · doi:10.1387/ijdb.113461dm · Cited by 71 · see citing works
Polyps, peptides and patterning
Bosch, T. C. G., & Fujisawa, T. (2001) · BioEssays · doi:10.1002/bies.1060 · Cited by 71 · see citing works
Deutzmann, R., Fowler, S. J., Zhang, X., Boone, K., Dexter, S., Boot-Handford, R., Rachel, R., & Sarras, M. P. (2000) · Development · doi:10.1242/dev.127.21.4669 · Cited by 70 · see citing works
Burton, P. M., & Finnerty, J. R. (2009) · Development Genes and Evolution · doi:10.1007/s00427-009-0271-2 · Cited by 66 · see citing works
Galliot, B., & Miller, D. J. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(99)01888-0 · Cited by 65 · see citing works
Identification and characterization
Bernstein, J., & Reutzel‐Edens, S. M. (2019) · urn:isbn:978-1-118-41628-0 · Cited by 112 · see citing works
Lemon Encodes an Unusual Receptor Protein-Tyrosine Kinase Expressed during Gametogenesis in Hydra
Miller, M. A., & Steele, R. E. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9786 · Cited by 61 · see citing works
Self-citationA 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
Holland, L. Z. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00109-x · Cited by 59 · see citing works
Grens, A., Shimizu, H., Hoffmeister, S. A. H., Bode, H. R., & Fujisawa, T. (1999) · Development · doi:10.1242/dev.126.3.517 · Cited by 59 · see citing works
Self-citationThree homologous subunits form a high affinity peptide-gated ion channel in Hydra
Dürrnagel, S., Kuhn, A., Tsiairis, C. D., Williamson, M., Kalbacher, H., Grimmelikhuijzen, C. J. P., Holstein, T. W., & Gründer, S. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.059998 · Cited by 58 · see citing works
The novel peptide HEADY specifies apical fate in a simple radially symmetric metazoanPreprint
Lohmann, J. U., & Bosch, T. C. G. (2000) · Genes & Development · doi:10.1101/gad.830100 · Cited by 58 · 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
Conserved and divergent genes in apex and axis development of cnidarians
Galliot, B. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00141-6 · Cited by 56 · see citing works
Function and regulation ofFoxF1duringXenopusgut development
Tseng, H.-T., Shah, R., & Jamrich, M. (2004) · Development · doi:10.1242/dev.01234 · Cited by 56 · see citing works
Self-citationFedders, H., & Leippe, M. (2007) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2007.06.003 · Cited by 55 · see citing works
Generic injuries are sufficient to induce ectopic Wnt organizers in Hydra
Cazet, J. F., Cho, A., & Juliano, C. E. (2021) · eLife · doi:10.7554/elife.60562 · Cited by 54 · see citing works
Adoption of conserved developmental genes in development and origin of the medusa body plan
Kraus, J. E. M., Fredman, D., Wang, W., Khalturin, K., & Technau, U. (2015) · EvoDevo · doi:10.1186/s13227-015-0017-3 · Cited by 54 · see citing works
Isolation and characterization of five Fox (Forkhead) genes from the sponge Suberites domuncula
Adell, T., & Müller, W. E. G. (2004) · Gene · doi:10.1016/j.gene.2004.02.036 · Cited by 54 · see citing works
Mitgutsch, C., Hauser, F., & Grimmelikhuijzen, C. J. P. (1999) · Developmental Biology · doi:10.1006/dbio.1998.9150 · Cited by 53 · see citing works
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
Planaria FoxA (HNF3) homologue is specifically expressed in the pharynx-forming cells
Koinuma, S., Umesono, Y., Watanabe, K., & Agata, K. (2000) · Gene · doi:10.1016/s0378-1119(00)00426-1 · Cited by 52 · see citing works
Sullivan, J. C., Sher, D., Eisenstein, M., Shigesada, K., Reitzel, A. M., Marlow, H. Q., Levanon, D., Groner, Y., Finnerty, J. R., & Gat, U. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-228 · Cited by 52 · see citing works
Endl, I., Lohmann, J. U., & Bosch, T. C. G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1445 · Cited by 51 · see citing works
Fission in Sea Anemones: Integrative Studies of Life Cycle Evolution
Geller, J. B. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.4.615 · Cited by 45 · see citing works
Phylogenetic Context and Basal Metazoan Model Systems
Collins, A. G. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.4.585 · Cited by 45 · see citing works
Sher, D., Fishman, Y., Melamed‐Book, N., Zhang, M., & Zlotkin, E. (2007) · The FASEB Journal · doi:10.1096/fj.07-9133com · Cited by 43 · see citing works
Hym-301, a novel peptide, regulates the number of tentacles formed in hydra
Takahashi, T., Hatta, M., Yum, S., Gee, L., Ohtani, M., Fujisawa, T., & Bode, H. R. (2005) · Development · doi:10.1242/dev.01792 · Cited by 42 · see citing works
Self-citationReddy, P. C., Gungi, A., Ubhe, S., Pradhan, S. J., Kolte, A., & Galande, S. (2019) · Communications Biology · doi:10.1038/s42003-019-0680-3 · Cited by 40 · see citing works
Bridge, D. M., Stover, N. A., & Steele, R. E. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9653 · Cited by 40 · see citing works
Self-citationSweet Tooth, a Novel Receptor Protein-tyrosine Kinase with C-type Lectin-like Extracellular Domains
Reidling, J. C., Miller, M. A., & Steele, R. E. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.14.10323 · Cited by 40 · see citing works
Self-citationAppearance and disappearance of Syk family protein-tyrosine kinase genes during metazoan evolution
Steele, R. E., Stover, N. A., & Sakaguchi, M. (1999) · Gene · doi:10.1016/s0378-1119(99)00373-x · Cited by 39 · see citing works
Self-citationZhang, X., Fei, K., Aǵbaş, A., Li, Y., Zhang, J., O'Reilly, B., Deutzmann, R., & Sarras, M. P. (2002) · Development Genes and Evolution · doi:10.1007/s00427-002-0225-4 · Cited by 38 · see citing works
NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges
Gazave, E., Lapébie, P., Renard, E., Bézac, C., Boury-Esnault, N., Vacelet, J., Pérez, T., Manuel, M., & Borchiellini, C. (2008) · Development Genes and Evolution · doi:10.1007/s00427-008-0242-z · Cited by 42 · see citing works
Identification and characterization of VEGF and FGF from Hydra
Krishnapati, L. S., & Ghaskadbi, S. (2013) · The International Journal of Developmental Biology · doi:10.1387/ijdb.130077sg · Cited by 36 · see citing works
Expression of developmental genes during early embryogenesis of Hydra
Fröbius, A. C., Genikhovich, G., Kürn, U., Anton‐Erxleben, F., & Bosch, T. C. G. (2003) · Development Genes and Evolution · doi:10.1007/s00427-003-0344-6 · Cited by 35 · see citing works
Kostyuchenko, R. P., Козин, В. В., Filippova, N. A., & Sorokina, E. V. (2018) · Developmental Dynamics · doi:10.1002/dvdy.7 · Cited by 33 · see citing works
Patterning and cell differentiation inHydra: novel genes and the limits to conservation
Bosch, T. C. G., & Khalturin, K. (2002) · Canadian Journal of Zoology · doi:10.1139/z02-129 · Cited by 32 · see citing works
Fox (forkhead) genes are involved in the dorso-ventral patterning of the Xenopus mesoderm
El‐Hodiri, H. M., Bhatia‐Dey, N., Kenyon, K. L., Ault, K., Dirksen, M., & Jamrich, M. (2001) · The International Journal of Developmental Biology · doi:10.1387/ijdb.11291856 · Cited by 31 · see citing works
Self-citationA comprehensive study of arthropod and onychophoran Fox gene expression patterns
Janßen, R., Schomburg, C., Prpíc, N.-M., & Budd, G. E. (2022) · PLoS ONE · doi:10.1371/journal.pone.0270790 · Cited by 29 · see citing works
PI3K and ERK 1‐2 regulate early stages during head regeneration in hydra
Manuel, G. C., Reynoso‐Camacho, R., Gee, L., Salgado, L. M., & Bode, H. R. (2006) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2006.00847.x · Cited by 29 · see citing works
Self-citationCardenas, M. M., & Salgado, L. M. (2003) · Developmental Biology · doi:10.1016/j.ydbio.2003.08.022 · Cited by 28 · see citing works
Hoffmeister‐Ullerich, S., Herrmann, D., Kielholz, J., Schweizer, M., & Schaller, H. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2002.03159.x · Cited by 28 · see citing works
An Amphioxus Emx Homeobox Gene Reveals Duplication During Vertebrate Evolution
Williams, N. A., & Holland, P. W. H. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026251 · Cited by 28 · see citing works
The Src/Csk regulatory circuit arose early in metazoan evolution
Miller, M. A., Malik, I. A., Shenk, M. A., & Steele, R. E. (2000) · Oncogene · doi:10.1038/sj.onc.1203714 · Cited by 28 · see citing works
Self-citationHydra, a model system to trace the emergence of boundaries in developing eumetazoans
Böttger, A., & Hassel, M. (2012) · The International Journal of Developmental Biology · doi:10.1387/ijdb.113454ab · Cited by 27 · see citing works
Selective protein kinase inhibitors block head-specific differentiation in hydra
Cardenas, M., Fabila, Y., Yum, S., Cerbón, J., Böhmer, F., Wetzker, R., Fujisawa, T., Bosch, T. C. G., & Salgado, L. M. (2000) · Cellular Signalling · doi:10.1016/s0898-6568(00)00115-7 · Cited by 27 · see citing works
Yamada, A., & Martindale, M. Q. (2002) · Development Genes and Evolution · doi:10.1007/s00427-002-0248-x · Cited by 27 · see citing works
Coordinated Gene Expression and Chromatin Regulation during Hydra Head Regeneration
Murad, R., Macias-Muñoz, A., Wong, A., Ma, X., & Mortazavi, A. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab221 · Cited by 25 · see citing works
Evidence that polycystins are involved in Hydra cnidocyte discharge
McLaughlin, S. K. (2017) · Invertebrate Neuroscience · doi:10.1007/s10158-016-0194-3 · Cited by 25 · see citing works
Fabila, Y., Navarro, L., Fujisawa, T., Bode, H. R., & Salgado, L. M. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00351-9 · Cited by 22 · see citing works
Self-citationArvizu, F., Aguilera‐Méndez, A., & Salgado, L. M. (2006) · Differentiation · doi:10.1111/j.1432-0436.2006.00078.x · Cited by 21 · see citing works
Detection of Expression Patterns in Hydra Pattern Formation
Bode, H. R., Lengfeld, T., Hobmayer, B., & Holstein, T. W. (2008) · Methods in molecular biology · doi:10.1007/978-1-60327-469-2_7 · Cited by 20 · see citing works
Self-citationReddy, P. C., Unni, M., Gungi, A., Agarwal, P., & Galande, S. (2015) · Mechanisms of Development · doi:10.1016/j.mod.2015.08.005 · Cited by 19 · see citing works
Siebert, S., Thomsen, S., Reimer, M. M., & Bosch, T. C. G. (2005) · Mechanisms of Development · doi:10.1016/j.mod.2005.04.010 · Cited by 19 · see citing works
The Role of Hox Genes in Axial Patterning in Hydra1
Bode, H. R. (2001) · American Zoologist · doi:10.1668/0003-1569(2001)041[0621:trohgi]2.0.co;2 · Cited by 18 · see citing works
Self-citationFoot differentiation and genomic plasticity in Hydra: lessons from the PPOD gene family
Thomsen, S., & Bosch, T. C. G. (2006) · Development Genes and Evolution · doi:10.1007/s00427-005-0032-9 · Cited by 18 · see citing works
Epigenomic landscape of enhancer elements during Hydra head organizer formation
Reddy, P. C., Gungi, A., Ubhe, S., & Galande, S. (2020) · Epigenetics & Chromatin · doi:10.1186/s13072-020-00364-6 · Cited by 15 · see citing works
Barve, A., Ghaskadbi, S., & Ghaskadbi, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061062 · Cited by 16 · see citing works
New ideas on the origin of bilateral animals
Malakhov, V. V. (2004) · Russian Journal of Marine Biology · doi:10.1007/s11179-005-0019-4 · Cited by 15 · see citing works
- Authors
- Martinez, D. E., Dirksen, M.-L., Bode, P. M., Jamrich, M., Steele, R. E., & Bode, H. R.
- Affiliations
- Center for Biologics Evaluation and Research (US)
- University of California, Irvine (US)
- ORCID
- Steele, Robert E.
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 1997-12
- Volume
- 192
- Issue
- 2
- Pages
- 523-536
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2083306347
- Cited by
- 150
- References
- 72
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 4 · 2022: 2 · 2021: 6 · 2020: 3 · 2019: 6 · 2018: 4 · 2017: 2 · 2016: 1 · 2015: 3 · 2014: 3 · 2013: 3 · 2012: 4
- FWCI
- 14.43
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Society of Clinical Oncology
- National Institutes of Health (5p01hd027173-05, 5r01hd008086-22, 5r01rr009755-03)
- National Center for Research Resources (R01 RR09755)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01-HD08086, P01-HD27173)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Keywords
- winged helix transcription factor, Hydra, axis formation, budding, head regeneration, evolution of developmental genes
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Cloning, Molecular, DNA-Binding Proteins, Genes, Homeobox, Hydra, Molecular Sequence Data, Morphogenesis, Nuclear Proteins, Phylogeny, Proteins, Regeneration, Reproduction, Asexual, Transcription Factors, Protein Biosynthesis, Sequence Alignment, Sequence Homology, Amino Acid, Gene Expression Regulation, Developmental, Evolution, Molecular, Hepatocyte Nuclear Factor 3-beta
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