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Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer

BACKGROUND: The embryonic organizer (i.e., Spemann organizer) has a pivotal role in the establishment of the dorsoventral (DV) axis through the coordination of BMP signaling. However, as impaired organizer function also results in anterior and posterior truncations, it is of interest to determine if...

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Autores principales: Varga, Máté, Maegawa, Shingo, Weinberg, Eric S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3120780/
https://www.ncbi.nlm.nih.gov/pubmed/21575247
http://dx.doi.org/10.1186/1471-213X-11-26
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author Varga, Máté
Maegawa, Shingo
Weinberg, Eric S
author_facet Varga, Máté
Maegawa, Shingo
Weinberg, Eric S
author_sort Varga, Máté
collection PubMed
description BACKGROUND: The embryonic organizer (i.e., Spemann organizer) has a pivotal role in the establishment of the dorsoventral (DV) axis through the coordination of BMP signaling. However, as impaired organizer function also results in anterior and posterior truncations, it is of interest to determine if proper anteroposterior (AP) pattern can be obtained even in the absence of early organizer signaling. RESULTS: Using the ventralized, maternal effect ichabod (ich) mutant, and by inhibiting BMP signaling in ich embryos, we provide conclusive evidence that AP patterning is independent of the organizer in zebrafish, and is governed by TGFβ, FGF, and Wnt signals emanating from the germ-ring. The expression patterns of neurectodermal markers in embryos with impaired BMP signaling show that the directionality of such signals is oriented along the animal-vegetal axis, which is essentially concordant with the AP axis. In addition, we find that in embryos inhibited in both Wnt and BMP signaling, the AP pattern of such markers is unchanged from that of the normal untreated embryo. These embryos develop radially organized trunk and head tissues, with an outer neurectodermal layer containing diffusely positioned neuronal precursors. Such organization is reflective of the presumed eumetazoan ancestor and might provide clues for the evolution of centralization in the nervous system. CONCLUSIONS: Using a zebrafish mutant deficient in the induction of the embryonic organizer, we demonstrate that the AP patterning of the neuroectoderm during gastrulation is independent of DV patterning. Our results provide further support for Nieuwkoop's "two step model" of embryonic induction. We also show that the zebrafish embryo can form a radial diffuse neural sheath in the absence of both BMP signaling and the early organizer.
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spelling pubmed-31207802011-06-23 Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer Varga, Máté Maegawa, Shingo Weinberg, Eric S BMC Dev Biol Research Article BACKGROUND: The embryonic organizer (i.e., Spemann organizer) has a pivotal role in the establishment of the dorsoventral (DV) axis through the coordination of BMP signaling. However, as impaired organizer function also results in anterior and posterior truncations, it is of interest to determine if proper anteroposterior (AP) pattern can be obtained even in the absence of early organizer signaling. RESULTS: Using the ventralized, maternal effect ichabod (ich) mutant, and by inhibiting BMP signaling in ich embryos, we provide conclusive evidence that AP patterning is independent of the organizer in zebrafish, and is governed by TGFβ, FGF, and Wnt signals emanating from the germ-ring. The expression patterns of neurectodermal markers in embryos with impaired BMP signaling show that the directionality of such signals is oriented along the animal-vegetal axis, which is essentially concordant with the AP axis. In addition, we find that in embryos inhibited in both Wnt and BMP signaling, the AP pattern of such markers is unchanged from that of the normal untreated embryo. These embryos develop radially organized trunk and head tissues, with an outer neurectodermal layer containing diffusely positioned neuronal precursors. Such organization is reflective of the presumed eumetazoan ancestor and might provide clues for the evolution of centralization in the nervous system. CONCLUSIONS: Using a zebrafish mutant deficient in the induction of the embryonic organizer, we demonstrate that the AP patterning of the neuroectoderm during gastrulation is independent of DV patterning. Our results provide further support for Nieuwkoop's "two step model" of embryonic induction. We also show that the zebrafish embryo can form a radial diffuse neural sheath in the absence of both BMP signaling and the early organizer. BioMed Central 2011-05-16 /pmc/articles/PMC3120780/ /pubmed/21575247 http://dx.doi.org/10.1186/1471-213X-11-26 Text en Copyright ©2011 Varga et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Varga, Máté
Maegawa, Shingo
Weinberg, Eric S
Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer
title Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer
title_full Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer
title_fullStr Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer
title_full_unstemmed Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer
title_short Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer
title_sort correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3120780/
https://www.ncbi.nlm.nih.gov/pubmed/21575247
http://dx.doi.org/10.1186/1471-213X-11-26
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