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

Daniel Kopinke; Joshua Sasine; Jennifer Swift; W. Zac Stephens; Tatjana Piotrowski

doi:10.1002/dvdy.20905

Retinoic acid-induced developmental defects are mediated by RARbeta/RXR heterodimers in the pharyngeal endoderm

Development ◽

10.1242/dev.00428 ◽

2003 ◽

Vol 130 (10) ◽

pp. 2083-2093 ◽

Cited By ~ 73

Author(s):

N. Matt

Keyword(s):

Retinoic Acid ◽

Developmental Defects ◽

Pharyngeal Endoderm

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A Retinoic Acid Responsive Hoxa3 Transgene Expressed in Embryonic Pharyngeal Endoderm, Cardiac Neural Crest and a Subdomain of the Second Heart Field

PLoS ONE ◽

10.1371/journal.pone.0027624 ◽

2011 ◽

Vol 6 (11) ◽

pp. e27624 ◽

Cited By ~ 18

Author(s):

Nata Y. S.-G. Diman ◽

Sophie Remacle ◽

Nicolas Bertrand ◽

Jacques J. Picard ◽

Stéphane Zaffran ◽

...

Keyword(s):

Retinoic Acid ◽

Neural Crest ◽

Cardiac Neural Crest ◽

Second Heart Field ◽

Pharyngeal Endoderm ◽

Heart Field

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Endoderm Morphogenesis Reveals Integration of Distinct Processes in the Development and Evolution of Pharyngeal Arches

10.1101/260356 ◽

2018 ◽

Author(s):

Kazunori Okada ◽

Hiroshi Wada ◽

Shinji Takada

Keyword(s):

Retinoic Acid ◽

Comparative Analysis ◽

Retinoic Acid Signaling ◽

Pharyngeal Arches ◽

Developmental Defects ◽

Pharyngeal Endoderm ◽

Development And Evolution

ABSTRACTThe vertebrate pharyngeal arches (PAs) are established by a combination of two styles of segmentation; the most anterior 2 PAs are simultaneously but the others are sequentially formed. However, the mechanism underlying their coexistence is unclear. Here, we show that the simultaneous and sequential segmentation discretely proceeded, respectively, but were finally integrated at the second PP (PP2), by dynamic morphogenesis of pharyngeal endoderm in the zebrafish. The coordination of these 2 distinct processes appears to be common in the PA development of many vertebrates, in which specific developmental defects posterior to the PP2 are caused by mutations of particular genes or perturbation of retinoic acid signaling. Surprisingly, comparative analysis of PA segmentation showed that the combinatorial styles of PA development is present in shark but not in lamprey, suggesting that PA segmentation was modified in the stem gnathostomes corresponding to the drastic pharyngeal innovations, such as PA2-derived opercular.

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Expression of AmphiHox-1 and AmphiPax-1 in amphioxus embryos treated with retinoic acid: insights into evolution and patterning of the chordate nerve cord and pharynx

Development ◽

10.1242/dev.122.6.1829 ◽

1996 ◽

Vol 122 (6) ◽

pp. 1829-1838 ◽

Cited By ~ 11

Author(s):

L.Z. Holland ◽

N.D. Holland

Keyword(s):

Retinoic Acid ◽

Neural Crest ◽

Nerve Cord ◽

Hox Genes ◽

Expression Patterns ◽

Expression Domain ◽

Craniofacial Malformations ◽

Pharyngeal Arches ◽

Pharyngeal Endoderm ◽

Cerebral Vesicle

Excess all-trans retinoic acid (RA) causes severe craniofacial malformations in vertebrate embryos: pharyngeal arches are fused or absent, and a rostrad expansion of Hoxb-1 expression in the hindbrain shows that anterior rhombomeres are homeotically respecified to a more posterior identity. As a corollary, neural crest migration into the pharyngeal arches is abnormal. We administered excess RA to developing amphioxus, the closest invertebrate relative of the vertebrates and thus a key organism for understanding evolution of the vertebrate body plan. In normal amphioxus, the nerve cord has only a slight anterior swelling, the cerebral vesicle, and apparently lacks migratory neural crest. Nevertheless, excess RA similarly affects amphioxus and vertebrates. The expression domain of AmphiHox-1 (homologous to mouse Hoxb-1) in the amphioxus nerve cord is also extended anteriorly. For both the amphioxus and mouse genes, excess RA causes either (1) continuous expression throughout the preotic hindbrain (mouse) and from the level of somite 7 to the anterior end of the nerve cord (amphioxus) or (2) discontinuous expression with a gap in rhombomere 3 (mouse) and a gap at the posterior end of the cerebral vesicle (amphioxus). A comparison of these expression patterns suggests that amphioxus has a homolog of the vertebrate hindbrain, both preotic and postotic. Although RA alters the expression of AmphiHox-1 expression in the amphioxus nerve cord, it does not alter the expression of AmphiHox-1 in presomitic mesoderm or of alkali myosin light chain (AmphiMlc-alk) in somites, and the axial musculature and notochord develop normally. The most striking morphogenetic effect of RA on amphioxus larvae is the failure of mouth and gill slits to form. In vertebrates effects of excess RA on pharyngeal development have been attributed solely to the abnormal migratory patterns of Hox-expressing cranial neural crest cells. This cannot be true for amphioxus because of the lack of migratory neural crest. Furthermore, expression of Hox genes in pharyngeal tissues of amphioxus has not yet been detected. However, the absence of gill slits in RA-treated amphioxus embryos correlates with an RA-induced failure of AmphiPax-1 to become down-regulated in regions of pharyngeal endoderm that would normally fuse with the overlying ectoderm. In vertebrates, RA might similarly act via Pax-1/9, also expressed in pharyngeal endoderm, to impair pharyngeal patterning.

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The second pharyngeal pouch is generated by dynamic remodeling of endodermal epithelium in zebrafish

Development ◽

10.1242/dev.194738 ◽

2020 ◽

Vol 147 (24) ◽

pp. dev194738

Author(s):

Kazunori Okada ◽

Shinji Takada

Keyword(s):

Retinoic Acid ◽

Live Imaging ◽

Zebrafish Embryos ◽

Retinoic Acid Signaling ◽

Pharyngeal Pouch ◽

Pharyngeal Arches ◽

Pharyngeal Endoderm ◽

Cell Tracing ◽

The Future ◽

Epithelial Remodeling

ABSTRACTPharyngeal arches (PAs) are segmented by endodermal outpocketings called pharyngeal pouches (PPs). Anterior and posterior PAs appear to be generated by different mechanisms, but it is unclear how the anterior and posterior PAs combine. Here, we addressed this issue with precise live imaging of PP development and cell tracing of pharyngeal endoderm in zebrafish embryos. We found that two endodermal bulges are initially generated in the future second PP (PP2) region, which separates anterior and posterior PAs. Subsequently, epithelial remodeling causes contact between these two bulges, resulting in the formation of mature PP2 with a bilayered morphology. The rostral and caudal bulges develop into the operculum and gill, respectively. Development of the caudal PP2 and more posterior PPs is affected by impaired retinoic acid signaling or pax1a/b dysfunction, suggesting that the rostral front of posterior PA development corresponds to the caudal PP2. Our study clarifies an aspect of PA development that is essential for generation of a seamless array of PAs in zebrafish.

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