The ventralizing activity of Radar, a maternally expressed bone morphogenetic protein, reveals complex bone morphogenetic protein interactions controlling dorso-ventral patterning in zebrafish

Goutel, Carole; Kishimoto, Yasuyuki; Schulte‐Merker, Stefan; Rosa, Frédéric

doi:10.1016/s0925-4773(00)00470-6

Cited by 32 publications

(49 citation statements)

References 65 publications

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“…To directly address this issue, we tested the ability of Rdr DN to abolish the ventralizing effects of ectopic Rdr activity by coinjecting both mRNAs. As expected from rdr ventralizing activity (18), 100% (n ϭ 78) of embryos injected with rdr were strongly ventralized (Fig. 1N).…”

Section: Resultssupporting

confidence: 81%

“…18) could be required in this process, we sought to carry out loss-of-Mrdr function experiments. In contrast to gtMOs, MOs targeted to the 5Ј end of transcripts (''atgMOs'') have been shown to interfere not only with zygotic, but also with maternal gene function in zebrafish (23,28).…”

Section: Resultsmentioning

confidence: 99%

“…RNA transcriptions, mRNA͞MO injections, and in situ hybridization were performed as described (18,23).…”

Section: Methodsmentioning

confidence: 99%

“…We have previously argued against the idea that the onset of bmps expression does not require induction because it could be enhanced on misexpression of zebrafish radar (rdr) mRNA, which encodes a secreted transforming growth factor (TGF)-␤ molecule homologous to mammalian GDF6 (18,19). Interestingly, rdr mRNA is maternally supplied in the zebrafish egg (18).…”

mentioning

confidence: 99%

“…Interestingly, rdr mRNA is maternally supplied in the zebrafish egg (18). Together with its gain-of-function phenotype, its early expression suggests that maternal rdr (Mrdr) could play a role in the early regulation of bmps.…”

mentioning

confidence: 99%

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Maternal induction of ventral fate by zebrafish radar

Sidi

Goutel

Peyriéras

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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In vertebrate embryos, maternal determinants are thought to preestablish the dorsoventral axis by locally activating zygotic ventral-and dorsal-specifying genes, e.g., genes encoding bone morphogenetic proteins (BMPs) and BMP inhibitors, respectively. Whereas the canonical Wnt͞␤-catenin pathway fulfills this role dorsally, the existence of a reciprocal maternal ventralizing signal remains hypothetical. Maternal noncanonical Wnt͞Ca 2؉ signaling may promote ventral fates by suppressing Wnt͞␤-catenin dorsalizing signals; however, whether any maternal determinant is directly required for the activation of zygotic ventral-specifying genes is unknown. Here, we show that such a function is achieved, in part, in the zebrafish embryo by the maternally encoded transforming growth factor ␤ (TGF-␤) signaling molecule, Radar. Lossof-function experiments, together with epistasis analyses, identify maternal Radar as an upstream activator of bmps expression. Maternal induction of bmps by Radar is essential for zebrafish development as its removal results in larval-lethal dorsalized phenotypes. Double-morphant analyses further suggest that Radar functions through the TGF-␤ receptor Alk8 to initiate the expression of bmp genes. Our results support the existence of a previously uncharacterized maternal ventralizing pathway. They might further indicate that maternal TGF-␤͞Rdr and Wnt͞Ca 2؉ pathways complementarily specify ventral cell fates, with the former triggering bmps expression and the latter indirectly repressing genes encoding BMP antagonists.T he degree to which the maternal genome contributes to vertebrate embryogenesis is a classical issue in developmental biology that remains largely unresolved. Pioneering work in amphibians, however, has led to models stressing its importance, especially in the control of early embryonic dorsoventral (DV) patterning (1, 2). Smith (3), for example, advanced a classical model for mesoderm induction that relied, in part, on two maternal signals: (i) a ventralizing signal emanating from ventral vegetal blastomeres inducing ventral mesoderm; and (ii) a reciprocal vegetal dorsalizing signal, inducing the Spemann organizer in the overlying prospective dorsal mesoderm. Since the establishment of this model, substantial efforts have been made to identify the molecules involved in both induction processes.Studies in Xenopus and zebrafish have shown that the Wnt͞ ␤-catenin pathway likely underlies the maternal dorsalizing signal. Members of the pathway, including Dishevelled and ␤-catenin, are dorsally enriched as soon as the first cell cycle of Xenopus development (4, 5). In zebrafish, ␤-catenin and the ichabod (ich) gene product, which ensures nuclear accumulation of ␤-catenin, are essential for dorsal specification. In heterozygous embryos derived from ich homozygous mutant mothers, the activation of zygotic dorsal-specifying genes (e.g., chordino (din)͞chordin, goosecoid, the homeobox gene bozozok (boz)͞ dharma, and the nodal gene squint) is abolished. As a consequence, ich mutants fail to fo...

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Section: Resultssupporting

confidence: 81%

Section: Resultsmentioning

confidence: 99%

“…RNA transcriptions, mRNA͞MO injections, and in situ hybridization were performed as described (18,23).…”

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Maternal induction of ventral fate by zebrafish radar

Sidi

Goutel

Peyriéras

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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Extracellular modulation of BMP activity in patterning the dorsoventral axis

Little

Mullins

2006

Birth Defects Research Pt C

102

125

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Signaling via bone morphogenetic proteins (BMPs) regulates a vast array of diverse biological processes in the developing embryo and in postembryonic life. Many insights into BMP signaling derive from studies of the BMP signaling gradients that pattern cell fates along the embryonic dorsal-ventral (DV) axis of both vertebrates and invertebrates. This review examines recent developments in the field of DV patterning by BMP signaling, focusing on extracellular modulation as a key mechanism in the formation of BMP signaling gradients in Drosophila, Xenopus, and zebrafish.

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Maternal factors in zebrafish development

Pelegri

2003

Developmental Dynamics

213

136

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All processes that occur before the activation of the zygotic genome at the midblastula transition are driven by maternal products, which are produced during oogenesis and stored in the mature oocyte. Upon egg activation and fertilization, these maternal factors initiate developmental cascades that carry out the embryonic developmental program. Even after the initiation of zygotic gene expression, perduring maternal products continue performing essential functions, either together with other maternal factors or through interactions with newly expressed zygotic products. Advances in zebrafish research have placed this organism in a unique position to contribute to a detailed understanding of the role of maternal factors in early vertebrate development. This review summarizes our knowledge on the processes involved in the production and redistribution of maternal factors during zebrafish oogenesis and early development, as well as our understanding of the function of these factors in axis formation, germ layer and germ cell specification, and other early embryonic processes. Developmental Dynamics 228:535-554, 2003.

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The ventralizing activity of Radar, a maternally expressed bone morphogenetic protein, reveals complex bone morphogenetic protein interactions controlling dorso-ventral patterning in zebrafish

Cited by 32 publications

References 65 publications

Maternal induction of ventral fate by zebrafish radar

Maternal induction of ventral fate by zebrafish radar

Extracellular modulation of BMP activity in patterning the dorsoventral axis

Maternal factors in zebrafish development

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