Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish

Holzschuh, Jochen; Wada, Naoki; Wada, Chikako; Schaffer, Ashleigh E.; Javidan, Yashar; Tallafuß, Alexandra; Bally‐Cuif, Laure; Schilling, Thomas F.

doi:10.1242/dev.01936

Cited by 82 publications

(93 citation statements)

References 58 publications

(66 reference statements)

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“…We blocked RA signaling at different time points post-gastrulation between 16 -30 hpf. In untreated embryos, the first endodermal pouch appears to be fully formed at around 18 hpf (our data; Crump et al, 2004;Holzschuh et al, 2005), the second at approximately 22 hpf, the third at 24 hpf, the fourth at 28 hpf, and the fifth at 30 hpf. Application of DEAB between 20 -30 hpf results in an underdeveloped pouch 4 and pouch 5 is missing (Fig.…”

Section: Ra Signaling Is Required For Endodermal Pouch Morphogenesissupporting

confidence: 50%

Retinoic acid is required for endodermal pouch morphogenesis and not for pharyngeal endoderm specification

Kopinke

Sasine

Swift

et al. 2006

Developmental Dynamics

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Because tissues from all three germ layers contribute to the pharyngeal arches, it is not surprising that all major signaling pathways are involved in their development. We focus on the role of retinoic acid (RA) signaling because it has been recognized for quite some time that alterations in this pathway lead to craniofacial malformations. Several studies exist that describe phenotypes observed upon RA perturbations in pharyngeal arch development; however, these studies did not address whether RA plays multiple roles at distinct time points during development. Here, we report the resulting phenotypes in the hindbrain, the neural crest-derived tissues, and the pharyngeal endoderm when RA synthesis is disrupted during zebrafish gastrulation and pharyngeal arch morphogenesis. Our results demonstrate that RA is required for the postgastrulation morphogenesis and segmentation of endodermal pouches, and that loss of RA does not affect the length of the pharyngeal ectoderm or medial endoderm along the anterior-posterior axis. We also provide evidence that RA is not required for the specification of pharyngeal pouch endoderm and that the pharyngeal endoderm consists of at least two different cell populations, of which the pouch endoderm is sensitive to RA and the more medial pharyngeal endoderm is not. These results demonstrate that the developmental processes underlying pharyngeal arch defects differ depending on when RA signaling is disturbed during development.

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Section: Ra Signaling Is Required For Endodermal Pouch Morphogenesissupporting

confidence: 50%

Retinoic acid is required for endodermal pouch morphogenesis and not for pharyngeal endoderm specification

Kopinke

Sasine

Swift

et al. 2006

Developmental Dynamics

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“…Notably, pharyngeal segmentation time is roughly twice as long in tilapia as in zebrafish, 30 hr versus 14-16 hr (Fig. 13B) (Holzschuh et al, 2005), which parallels the overall slower embryonic development of tilapia relative to zebrafish (Fujimura and Okada, 2007). Although in vivo studies of zebrafish pouch formation have shown that the first and second pouch primordia consist of groups of six to ten cells (Holzschuh et al, 2005), our histological observations show a number of cells several orders of magnitude higher in tilapia pouch primordia (Fig.…”

Section: History Of a Key Evolutionary Innovationmentioning

confidence: 53%

“…The pharyngeal wall is subsequently compartmentalized by a series of six outpocketings of endoderm called pharyngeal pouches (pp). In contrast to the two preotic NC populations that are spatially distinct prior to the onset of pouch formation, a single mass of postotic NC cells becomes segmented into five distinct populations after migration (Kimmel et al, 2001;Holzschuh et al, 2005). To determine if a similar sequence of events characterizes pharyngeal development in tilapia, we performed histological sections at various stages of arch morphogenesis, and whole-mount in situ hybridization with tilapia orthologues of genes expressed in NC and pp in zebrafish.…”

Section: Pharyngeal Arch Segmentation In Nile Tilapia Embryosmentioning

confidence: 99%

Embryonic Development and Skeletogenesis of the Pharyngeal Jaw Apparatus in the Cichlid Nile Tilapia (Oreochromis niloticus)

Pabic

Stellwag

Scemama

2009

The Anatomical Record

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The evolution of a specialized pharyngeal jaw apparatus (PJA) has been argued to be the key evolutionary innovation that allowed the explosive adaptive radiation of cichlid fishes in East African lakes. Subsequent studies together with recent molecular phylogenies have shown that similar innovations evolved independently several times within the teleosts, which poses the questions: (1) how similar are the developmental mechanisms responsible for these changes in divergent taxa and (2) how did such complex features arise independently in evolution? A detailed knowledge of PJA development in cichlids and other teleosts is needed to address these questions. Here, we provide a detailed account of the development of the PJA in one species of cichlid, the Nile tilapia (Oreochromis niloticus), from the early segmentation and patterning of its embryonic precursors -pharyngeal arches 3 to 7 -to its ossification. We find that pharyngeal segmentation occurs sequentially from anterior to posterior during early segmentation stages through the mid-pharyngula period. We show a clear combinatorial code of Hox gene expression such that each posterior arch is defined by a distinctive Hox signature. Posterior arch chondrogenesis in tilapia is essentially complete by the end of the hatching period, and most elements become ossified over the next two days. Our results reveal that both the fusion of lower jaw bones and articulation between the neurocranium and upper jaws occur during post-embryonic development. Abstract end data should be: Anat Rec, 292:1780Rec, 292: -1800Rec, 292: , 2009. V V C 2009 Wiley-Liss, Inc.

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“…In chick embryos, for example, Begbie et al (1999) demonstrated that Bmp7 is expressed in endodermal pouches at stage 13, at which neuroblasts start to delaminate and differentiate in embryos, and that it works as a potent inducer of epibranchial neurons in vitro. Two additional reports demonstrated a requirement for the endoderm-derived secreting molecules, FGF3 (Nechiporuk et al, 2005), BMP2b, and BMP5 (Holzschuh et al, 2005) for neurogenesis in the epibranchial ganglia in zebrafish. So far, however, no initial signal for the specification of the epibranchial placode has been identified.…”

Section: Fgf8 Is a Candidate Molecule For The Initial Specification Fmentioning

confidence: 99%

“…Begbie et al (1999) demonstrated that chick bone morphogenetic protein-7 (BMP7) is a signaling molecule that induces epibranchial placode-derived neurons. Endoderm-derived BMP2b/5 (Holzschuh et al, 2005) and FGF3 (Nechiporuk et al, 2005) were also shown to play crucial roles in epibranchial neurogenesis in zebrafish embryos.…”

Section: Introductionmentioning

confidence: 98%

Initial specification of the epibranchial placode in zebrafish embryos depends on the fibroblast growth factor signal

Nikaido

Doi

Shimizu³

et al. 2006

Developmental Dynamics

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In vertebrates, cranial sensory ganglia are mainly derived from ectodermal placodes, which are focal thickenings at characteristic positions in the embryonic head. Here, we provide the first description of the early development of the epibranchial placode in zebrafish embryos using sox3 as a molecular marker. By the one-somite stage, we saw a pair of single sox3-expressing domains appear lateral to the future hindbrain. The sox3 domain, which is referred to here as the early lateral placode, is segregated during the early phase of segmentation to form a pax2a-positive medial area and a pax2a-negative lateral area. The medial area subsequently developed to form the otic placode, while the lateral area was further segregated along the anteroposterior axis, giving rise to four sox3-positive subdomains by 26 hr postfertilization. Given their spatial relationship with the expression of the markers for the epibranchial ganglion, as well as their positions and temporal changes, we propose that these four domains correspond to the facial, glossopharyngeal, vagal, and posterior lateral line placodes in an anterior-to-posterior order. The expression of sox3 in the early lateral placode was absent in mutants lacking functional fgf8, while implantation of fibroblast growth factor (FGF) beads restored the sox3 expression. Using SU5402, which inhibits the FGF signal, we were able to demonstrate that formation of both the early lateral domains and later epibranchial placodes depends on the FGF signal operating at the beginning of somitogenesis. Together, these data provide evidence for the essential role of FGF signals in the development of the epibranchial placodes. Developmental Dynamics 236:564 -571, 2007.

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Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish

Cited by 82 publications

References 58 publications

Retinoic acid is required for endodermal pouch morphogenesis and not for pharyngeal endoderm specification

Retinoic acid is required for endodermal pouch morphogenesis and not for pharyngeal endoderm specification

Embryonic Development and Skeletogenesis of the Pharyngeal Jaw Apparatus in the Cichlid Nile Tilapia (Oreochromis niloticus)

Initial specification of the epibranchial placode in zebrafish embryos depends on the fibroblast growth factor signal

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