Retinoic Acid and Pitx2 Regulate Early Neural Crest Survival and Migration in Craniofacial and Ocular Development

Chawla, Bahaar; Schley, Elisa; Williams, Antionette L.; Bohnsack, Brenda L.

doi:10.1002/bdrb.21177

Cited by 46 publications

(47 citation statements)

References 54 publications

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“…There are contrasting studies with regards to RA in NC development. Both increases and decreases in RA appear to negatively affect NC cell survival and migration, suggesting that its levels are tightly regulated to allow for normal embryonic development (Chawla, Schley, Williams, & Bohnsack, 2016). …”

Section: | Signaling Events Regulating Nc Inductionmentioning

confidence: 99%

Specifying neural crest cells: From chromatin to morphogens and factors in between

Rogers

Nie

2018

WIREs Developmental Biology

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Neural crest (NC) cells are a stem-like multipotent population of progenitor cells that are present in vertebrate embryos, traveling to various regions in the developing organism. Known as the "fourth germ layer", these cells originate in the ectoderm between the neural plate (NP), which will become the brain and spinal cord, and nonneural tissues that will become the skin and the sensory organs. NC cells can differentiate into more than 30 different derivatives in response to the appropriate signals including, but not limited to, craniofacial bone and cartilage, sensory nerves and ganglia, pigment cells, and connective tissue. The molecular and cellular mechanisms that control the induction and specification of NC cells include epigenetic control, multiple interactive and redundant transcriptional pathways, secreted signaling molecules, and adhesion molecules. NC cells are important not only because they transform into a wide variety of tissue types, but also because their ability to detach from their epithelial neighbors and migrate throughout developing embryos utilizes mechanisms similar to those used by metastatic cancer cells. In this review, we discuss the mechanisms required for the induction and specification of NC cells in various vertebrate species, focusing on the roles of early morphogenesis, cell adhesion, signaling from adjacent tissues, and the massive transcriptional network that controls the formation of these amazing cells. This article is categorized under: Nervous System Development > Vertebrates: General Principles Gene Expression and Transcriptional Hierarchies > Regulatory Mechanisms Gene Expression and Transcriptional Hierarchies > Gene Networks and Genomics Signaling Pathways > Cell Fate Signaling.

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Section: | Signaling Events Regulating Nc Inductionmentioning

confidence: 99%

Specifying neural crest cells: From chromatin to morphogens and factors in between

Rogers

Nie

2018

WIREs Developmental Biology

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“…Zebrafish (Danio rerio) were raised in a breeding colony under a 14-hr light/10-hr dark cycle as previously described (Bohnsack et al, 2011a(Bohnsack et al, , 2011b(Bohnsack et al, , 2012Bohnsack and Kahana, 2013;Chawla et al, 2016). Embryos were maintained at 28.5 degrees Celsius and staged as previously described (Kimmel et al, 1995).…”

Section: Animal Care/animal Strainsmentioning

confidence: 99%

“…The cranial neural crest, which arises from the prosencephalon, mesencephalon, and rhombencephalon, follows specific migratory pathways into the craniofacial region (Trainor and Tam, 1995;Trainor, 2005;Bohnsack and Kahana, 2013;Chawla et al, 2016). At the same time that the jaw and pharyngeal arches are forming, a subgroup of neural crest cells, which initially populates the periocular mesenchyme, enters the eye (Johnston, 1966;Johnston et al, 1979;Creuzet et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Differences in neural crest sensitivity to ethanol account for the infrequency of anterior segment defects in the eye compared with craniofacial anomalies in a zebrafish model of fetal alcohol syndrome

Eason

Williams

Chawla

et al. 2017

Birth Defects Research

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Background Ethanol (ETOH) exposure during pregnancy is associated with craniofacial and neurologic abnormalities, but infrequently disrupts the anterior segment of the eye. In these studies, we used zebrafish to investigate differences in the teratogenic effect of ETOH on craniofacial, periocular, and ocular neural crest. Methods Zebrafish eye and neural crest development was analyzed via live imaging, TUNEL assay, immunostaining, detection of reactive oxygen species, and in situ hybridization. Results Our studies demonstrated that foxd3-positive neural crest cells in the periocular mesenchyme and developing eye were less sensitive to ETOH than sox10-positive craniofacial neural crest cells that form the pharyngeal arches and jaw. ETOH increased apoptosis in the retina, but did not affect survival of periocular and ocular neural crest cells. ETOH also did not increase reactive oxygen species within the eye. In contrast, ETOH increased ventral neural crest apoptosis and reactive oxygen species production in the facial mesenchyme. In the eye and craniofacial region, sod2 showed high levels of expression in the anterior segment and in the setting of Sod2 knockdown, low levels of ETOH decreased migration of foxd3-positive neural crest cells into the developing eye. However, ETOH had minimal effect on the periocular and ocular expression of transcription factors (pitx2 and foxc1) that regulate anterior segment development. Conclusions Neural crest cells contributing to the anterior segment of the eye exhibit increased ability to withstand ETOH-induced oxidative stress and apoptosis. These studies explain the rarity of anterior segment dysgenesis despite the frequent craniofacial abnormalities in fetal alcohol syndrome.

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“…Animal models of RA embryopathy, as described throughout this review, have pinpointed specific time frames in rodents, birds, frogs, and zebrafish, during which different cranial neural crest populations are sensitive to increased RA exposure. Taken together, these studies demonstrate that short pulses of RA throughout gastrulation and somitogenesis have deleterious effects on the pharyngeal arches and frontonasal process, resulting in irreversible jaw, middle ear, and midface abnormalities that recapitulate the human findings (Abe et al, 2008;Alexandre et al, 1996;Chawla et al, 2016;Dekker et al, 1992;Ellies et al, 1997;Gitton et al, 2010;Hart, McCue, Ragland, Winn, & Unger, 1990;Lee et al, 2001;Lee et al, 1995;Mallo, 1997;Mark et al, 1995;Marshall et al, 1992;Plant et al, 2000;Vieux-Rochas et al, 2007). Consequently, the decrease in neural crest cells in the frontonasal process and first pharyngeal arch accounts for the midface hypoplasia and micrognathia.…”

Section: Congenital Craniofacial and Ocular Diseases Resulting Frommentioning

confidence: 71%

What's retinoic acid got to do with it? Retinoic acid regulation of the neural crest in craniofacial and ocular development

Williams

Bohnsack

2019

Genesis

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Vertebrate models, from zebrafish to mouse, and experimental tools, such as reporter transgenes, inhibitors of RA synthesis, and selective antagonists for RARs, have been successfully used to decipher retinoid functions during development at the cellular and molecular levels.Numerous examples from animal models and human diseases highlight the importance of RA in regulating neural crest contributions to craniofacial and ocular structures. The neural crest is a set of transient embryonic stem cells unique to vertebrates that originate at the border of the neural plate spanning the embryo from the diencephalon to the lumbosacral spinal cord. Neural crest cells undergo extensive and coordinated movements away from folds of the neural F I G U R E 1 Neural crest derivatives in the craniofacial region. (a) The neural crest is a transient population of embryonic stem cells that delaminate from the edge of the neural tube spanning from the diencephalon (Di) to the lumbosacral spinal cord (SpC). Neural crest cells that originate from the diencephalon and anterior mesencephalon (AM) migrate dorsal and ventral to the eye to populate the POM and frontonasal process (FNP). These cells migrate toward regions of high RA levels within the telencephalon (Te), POM, and frontonasal process. Neural crest cells from the posterior mesencephalon (PM) migrate into the first pharyngeal arch. Neural crest cells from the rhombencephalon, which are patterned by a RA gradient, migrate into the first through fourth pharyngeal arches in an anterior (AR) to posterior (PR) pattern. (b) The cranial neural crest is important in the development of the craniofacial skeleton. Neural crest cells in the frontonasal process give rise to the frontal bone (Fr), nasal bone (Na), and philtrum (Ph) in the midline of the face. The anterior portion of the first pharyngeal arch forms the maxillary (Mx) and zygomatic (Zy) bones while the posterior aspect gives rise to the mandible (Mn), The third and fourth pharyngeal arches both contribute to the hyoid (Ny) bone in the neck. (c) Neural crest cells, which are derived from the anterior mesenchyme and diencephalon, populate the periocular mesenchyme and migrate into the anterior segment of the eye. Ocular structures derived from the neural crest include the corneal stroma (CS), corneal endothelium (CEn), trabecular meshwork (TM), sclera (Scl), iris stroma (IS), uveal melanocytes (me), ciliary body muscle (CBM), and the tendons of the extraocular muscles (Tn). The corneal epithelium (CEp) and lens are derived from surface ectoderm while the ciliary body epithelium (CBE), retina (Ret), and retinal pigmented epithelium (RPE) arise from neuroepithelium. Schlemm's canal (SC) and extraocular muscles (EOM) originate from mesoderm. (d) Neural crest cells are also important in middle ear development. Vibrations are transmitted from the external ear, which consists of the pinna, auditory canal, and the tympanic membrane (Tym). The tympanic membrane is attached to the malleus in the middle ear. Both the malleus and the incus...

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Retinoic Acid and Pitx2 Regulate Early Neural Crest Survival and Migration in Craniofacial and Ocular Development

Cited by 46 publications

References 54 publications

Specifying neural crest cells: From chromatin to morphogens and factors in between

Specifying neural crest cells: From chromatin to morphogens and factors in between

Differences in neural crest sensitivity to ethanol account for the infrequency of anterior segment defects in the eye compared with craniofacial anomalies in a zebrafish model of fetal alcohol syndrome

What's retinoic acid got to do with it? Retinoic acid regulation of the neural crest in craniofacial and ocular development

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