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Tbx16 cooperates with Wnt11 in assembling the zebrafish organizer.

ABSTRACT: The organizer, the signaling center that specifies vertebrate axial polarity and the nervous system, is a dorsal midline mesodermal domain in the gastrula that will form prechordal plate and anterior notochord. We show that in zebrafish the organizer is not a single domain when it first arises in the nascent mesoderm at the onset of gastrulation. Rather, in the presumptive prechordal plate region, the organizer is subdivided into two side-by-side cellular fields. Within minutes, concurrent medial and anterior cellular movements merge, or 'coalesce', the two fields to form the well-known singular midline field. Coalescence forms a symmetrical domain because the cell movements on the left and right sides initiate simultaneously and occur synchronously. However, in embryos with reduced function of the T-box transcription factor Tbx16 (Spadetail) or its genetic target paraxial protocadherin (Papc), synchrony is lost, coalesence is disrupted, and the midline domain is misshaped. Furthermore, with combined loss of Tbx16 and Wnt11 (Silberblick), coalesence is essentially absent. Possibly as a consequence, both the anterior movement of presumptive prechordal plate and organizer function, as assayed by eye-field separation, are disrupted. Our findings thus reveal that Tbx16, in combination with Wnt11, are critical components not only in morphogenesis but also in initial assembly of the organizer.

SUBMITTER: Muyskens JB

PROVIDER: S-EPMC1862409 | biostudies-literature | 2007 Jan

REPOSITORIES: biostudies-literature

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Tbx16 cooperates with Wnt11 in assembling the zebrafish organizer.

Muyskens Jonathan B JB Kimmel Charles B CB

Mechanisms of development 20060926 1

The organizer, the signaling center that specifies vertebrate axial polarity and the nervous system, is a dorsal midline mesodermal domain in the gastrula that will form prechordal plate and anterior notochord. We show that in zebrafish the organizer is not a single domain when it first arises in the nascent mesoderm at the onset of gastrulation. Rather, in the presumptive prechordal plate region, the organizer is subdivided into two side-by-side cellular fields. Within minutes, concurrent media ...[more]

PMID: 17081734

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Project description:BackgroundA complex network of signaling pathways and transcription factors regulates vertebrate mesoderm development. Zebrafish mutants provide a powerful tool for examining the roles of individual genes in such a network. spadetail (spt) is a mutant with a lesion in tbx16, a T-box transcription factor involved in mesoderm development; the mutant phenotype includes disrupted primitive red blood cell formation as well as disrupted somitogenesis. Despite much recent progress, the downstream targets of tbx16 remain incompletely understood. The current study was carried out to test whether any of the five major signaling pathways are regulated by tbx16 during two specific stages of mesoderm development: primitive red blood cell formation in the intermediate mesoderm and somite formation in the tail paraxial mesoderm. This test was performed using Gene Set Enrichment Analysis, which identifies coordinated changes in expression among a priori sets of genes associated with biological features or processes.ResultsOur Gene Set Enrichment Analysis results identify Wnt and retinoic acid signaling as likely downstream targets of tbx16 in the developing zebrafish intermediate mesoderm, the site of primitive red blood cell formation. In addition, such results identify retinoic acid signaling as a downstream target of tbx16 in the developing zebrafish posterior somites. Finally, using candidate gene identification and in situ hybridization, we provide expression domain information for 25 additional genes downstream of tbx16 that are outside of both pathways; 23 were previously unknown downstream targets of tbx16, and seven had previously uncharacterized expression in zebrafish.ConclusionsOur results suggest that (1) tbx16 regulates Wnt signaling in the developing zebrafish intermediate mesoderm, the site of primitive red blood cell formation, and (2) tbx16 regulates retinoic acid signaling at two distinct embryonic locations and developmental stages, which may imply ongoing spatio-temporal regulation throughout mesoderm development.

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Tbx16 cooperates with Wnt11 in assembling the zebrafish organizer.

Publications

Tbx16 cooperates with Wnt11 in assembling the zebrafish organizer.

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