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Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer
Abstract
An abundant cDNA enriched in Spemann's organizer, cerberus, was isolated by differential screening. It encodes a secreted protein that is expressed in the anterior endomesoderm. Microinjection of cerberus mRNA into Xenopus embryos induces ectopic heads, and duplicated hearts and livers. The results suggest a role for a molecule expressed in the anterior endoderm in the induction of head structures in the vertebrate embryo.
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“In the extra-cellular matrix, a number of secreted proteins that bind to Wnts and prevent their interaction with either Fz or LRP5/6 to antagonize Wnt signaling have been identified. These include Dickkopf (Dkk) proteins,16 Wnt-inhibitor protein (WIF),17 soluble Frizzled-related proteins (SFRP),18 Cerebrus,19 Frzb20 and the context dependent Wnt inhibitor Wise.21”
From Wnt signal transduction pathways (2008) · cites this paper as [19]
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“Cerberus was discovered in Xenopus as a head-inducing secreted factor that is expressed in the anterior endoderm of Spemann ’ s organizer 173 and was identi fi ed as a multifunctional inhibitor of Nodal, BMP, and Wnt signaling.”
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“Antisense riboprobes for noggin (Smith and Harland, 1992), chordin (Sasai et al., 1994), goosecoid (gsc) (Cho et al., 1991), cerberus (Bouwmeester et al., 1996), Sox2 (Mizuseki et al., 1998), opl (Kuo et al., 1998), dkk-1 (Glinka et al., 1998), hex (Newman et al., 1997), otx2 (Pannese et al.,…”
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“Cerberus and Cerberus-like proteins like Charon bind directly to Nodal, inhibit its binding to receptors, and thus regulate embryonic patterning (Bouwmeester et al. 1996; Piccolo et al. 1999; Bertocchini and Stern 2002; Silva et al. 2003; Hashimoto et al. 2004; Marques et al. 2004; Yamamoto et al. 2004; Tavares et al.…”
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Zorn, A. M. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00360-8 · Cited by 238
Posteriorization by FGF, Wnt, and Retinoic Acid Is Required for Neural Crest Induction
Villanueva, S., Glavic, Á., Ruiz-Rudolph, P., & Mayor, R. (2002) · Developmental Biology · doi:10.1006/dbio.2001.0485 · Cited by 234
“…plate border does not receive such signals or these are inhibited by other agents produced by the anterior regions of the embryo, such as cerberus or dkk1, two known Wnts inhibitors (Bouwmeester et al., 1996; Glinka et al., 1998), and, as a consequence, does not develop as neural crest cells.”
BackgroundRegulation of Wnt/LRP Signaling by Distinct Domains of Dickkopf Proteins
Brott, B. K., & Sokol, S. Y. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.17.6100-6110.2002 · Cited by 234
“Additionally, Wnt signaling is regulated by several extracellular antagonists, including Frizzled-related proteins (38, 49, 50), Cerberus (4), and WIF-1 (19).”
BackgroundHarland, R. M. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00096-4 · Cited by 234
Barrantes, I. D. B., Elia, A., Wünsch, K., de Angelis, M. H., Mak, T. W., Rossant, J., Conlon, R. A., Gossler, A., & de la Pompa, J. L. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80212-7 · Cited by 233
“revealed by misexpression studies [54].”
Patterning the Xenopus blastula
Heasman, J. (1997) · Development · doi:10.1242/dev.124.21.4179 · Cited by 232
A small population of anterior cells patterns the forebrain during zebrafish gastrulation
Houart, C., Westerfield, M., & Wilson, S. W. (1998) · Nature · doi:10.1038/35853 · Cited by 231
“Signals from endoderm in anterior regions of mouse and frog embryos are required for anterior developmen”
BackgroundA Gene Expression Screen in Zebrafish EmbryogenesisPreprint
Kudoh, T., Tsang, M., Hukriede, N. A., Chen, X., Dedekian, M., Clarke, C. J., Kiang, A., Schultz, S., Epstein, J. A., Toyama, R., et al. (2001) · Genome Research · doi:10.1101/gr.209601 · Cited by 231
“Molecules that can modulate the activity of signal transduction pathways appear to be quite common, although their role in development is only partially understood (Smith and Harland 1992; Sasai et al. 1994; Bouwmeester et al. 1996; Rattner et al. 1997; Massague 1998; Hsieh et al. 1999; Wotton et al. 1999; Kim et al.…”
BackgroundAvsian-Kretchmer, O., & Hsueh, A. J. W. (2003) · Molecular Endocrinology · doi:10.1210/me.2003-0227 · Cited by 228
Neural and Head Induction by Insulin-like Growth Factor Signals
Pera, E. M., Wessely, O., Li, S.-Y., & Robertis, E. M. D. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00069-7 · Cited by 229
Self-citationInitial patterning of the central nervous system: How many organizers?
Stern, C. D. (2001) · Nature reviews. Neuroscience · doi:10.1038/35053563 · Cited by 224
“At about the same time, amphibian experiments had uncovered genes whose early misexpression causes the formation of either an ectopic hea”
BackgroundQin, K. H., Yu, M. S., Fan, J., Wang, H., Zhao, P., Zhao, G., Zeng, W., Chen, C., Wang, Y., Wang, A., et al. (2023) · Genes & Diseases · doi:10.1016/j.gendis.2023.01.030 · Cited by 243
“Cerberus Cerberus is an abundant organizer-specific gene that was isolated from Xenopus and can induce ectopic head formation.(291) It also plays an important role in cardiogenesis during vertebrate embryonic development.”
BackgroundBrugmann, S. A., Pandur, P., Kenyon, K. L., Pignoni, F., & Moody, S. A. (2004) · Development · doi:10.1242/dev.01516 · Cited by 224
“The animal pole was injected with mRNAs for noggin (50 pg), cerberus (50 pg) (Bouwmeester et al., 1996), bmp4 (50 pg), Wnt8 (50 pg) (Hoppler and Moon, 1998) or constitutively activated fgfr1 (cfgfr1, 50 pg) (Neilson and Friesel, 1996).”
MethodThe novel Cer-like protein Caronte mediates the establishment of embryonic left–right asymmetry
Esteban, C. R., Capdevila, J., Economides, A. N., Pascual, J., Ortiz, Á., & Belmonte, J. C. I. (1999) · Nature · doi:10.1038/45738 · Cited by 222
Leimeister, C., Bach, A., & Gessler, M. (1998) · Mechanisms of Development · doi:10.1016/s0925-4773(98)00072-0 · Cited by 222
“The first was Xenopus frzb-1, originally named frezzled, which was identified in a screen for cDNAs enriched in the Spemann organizer (Bouwmeester et al., 1996).”
Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis
Xanthos, J. B., Kofron, M. J., Wylie, C., & Heasman, J. (2001) · Development · doi:10.1242/dev.128.2.167 · Cited by 221
Patterning of the embryonic forebrain
Rubenstein, J. L. R., & Beachy, P. A. (1998) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(98)80004-4 · Cited by 219
Kim, S., Yamamoto, A., Bouwmeester, T., Agius, E., & Robertis, E. M. D. (1998) · Development · doi:10.1242/dev.125.23.4681 · Cited by 220
Self-citationYamamoto, A., Amacher, S. L., Kim, S., Geissert, D., Kimmel, C. B., & Robertis, E. M. D. (1998) · Development · doi:10.1242/dev.125.17.3389 · Cited by 219
Self-citationRider, C. C., & Mulloy, B. (2010) · Biochemical Journal · doi:10.1042/bj20100305 · Cited by 215
Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo
Camus, A., Perea-Gómez, A., Moreau, A., & Collignon, J. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.03.047 · Cited by 209
Patterning of the chick forebrain anlage by the prechordal plate
Pera, E. M., & Kessel, M. (1997) · Development · doi:10.1242/dev.124.20.4153 · Cited by 210
“An involvement of the primitive endoderm in head patterning, however, is indicated by the expression of the homeobox gene Hesx1 in mice and the secreted factor cerberus in the frog Xenopus laevis (Bouwmeester et al., 1996; Thomas and Beddington, 1996).”
BackgroundDick, A., Hild, M., Bauer, H., Imai, Y., Maifeld, H., Schier, A. F., Talbot, W. S., Bouwmeester, T., & Hammerschmidt, M. (2000) · Development · doi:10.1242/dev.127.2.343 · Cited by 208
Self-citationLinker, C., & Stern, C. D. (2004) · Development · doi:10.1242/dev.01445 · Cited by 206
“When Wnt antagonists and Cerberus are misexpressed with FGF4 and Smad6, the induction of both markers is abolished (0/6; Fig.”
Influential
Metadata
- Authors
- Bouwmeester, T., Kim, S.-H., Sasai, Y., Lu, B., & Robertis, E. M. D.
- Affiliations
- Howard Hughes Medical Institute (US)
- Venue
- Nature
- Published
- 1996-08
- Volume
- 382
- Issue
- 6592
- Pages
- 595-601
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2081939122
- Cited by
- 759
- References
- 44
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 15 · 2023: 11 · 2022: 10 · 2021: 7 · 2020: 9 · 2019: 6 · 2018: 10 · 2017: 13 · 2016: 14 · 2015: 14 · 2014: 10 · 2013: 21 · 2012: 23
- FWCI
- 23.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- Cerberus, Spemann's organizer, anterior endoderm, secreted proteins, head induction, Xenopus embryo, gene expression, embryonic induction
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Blastomeres, Digestive System, Embryonic Induction, Endoderm, Gastrula, Head, Mesoderm, Molecular Sequence Data, Proteins, RNA, Messenger, Tail, Ultraviolet Rays, Xenopus, Cell Polarity, In Situ Hybridization, DNA Primers, DNA, Complementary, Xenopus Proteins, Intercellular Signaling Peptides and Proteins
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