scholarly journals Hingepoints and neural folds reveal conserved features of primary neurulation in the zebrafish forebrain

2019 ◽  
Author(s):  
Jonathan M. Werner ◽  
Maraki Y. Negesse ◽  
Dominique L. Brooks ◽  
Allyson R. Caldwell ◽  
Jafira M. Johnson ◽  
...  

ABSTRACTPrimary neurulation is the process by which the neural tube, the central nervous system precursor, is formed from the neural plate. Incomplete neural tube closure occurs frequently, yet underlying causes remain poorly understood. Developmental studies in amniotes and amphibians have identified hingepoint and neural fold formation as key morphogenetic events and hallmarks of primary neurulation, the disruption of which causes neural tube defects. In contrast, the mode of neurulation in teleosts such as zebrafish has remained highly debated. Teleosts are thought to have evolved a unique pattern of neurulation, whereby the neural plate infolds in absence of hingepoints and neural folds (NFs), at least in the hindbrain/trunk where it has been studied. We report here on zebrafish forebrain morphogenesis where we identify these morphological landmarks. Our findings reveal a deeper level of conservation of neurulation than previously recognized and establish the zebrafish as a model to understand human neural tube development.

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Jonathan M. Werner ◽  
Maraki Y. Negesse ◽  
Dominique L. Brooks ◽  
Allyson R. Caldwell ◽  
Jafira M. Johnson ◽  
...  

AbstractPrimary neurulation is the process by which the neural tube, the central nervous system precursor, is formed from the neural plate. Incomplete neural tube closure occurs frequently, yet underlying causes remain poorly understood. Developmental studies in amniotes and amphibians have identified hingepoint and neural fold formation as key morphogenetic events and hallmarks of primary neurulation, the disruption of which causes neural tube defects. In contrast, the mode of neurulation in teleosts has remained highly debated. Teleosts are thought to have evolved a unique mode of neurulation, whereby the neural plate infolds in absence of hingepoints and neural folds, at least in the hindbrain/trunk where it has been studied. Using high-resolution imaging and time-lapse microscopy, we show here the presence of these morphological landmarks in the zebrafish anterior neural plate. These results reveal similarities between neurulation in teleosts and other vertebrates and hence the suitability of zebrafish to understand human neurulation.


2009 ◽  
Vol 150 (19) ◽  
pp. 873-882 ◽  
Author(s):  
József Gábor Joó

Neural tube defects are rare and mostly lethal malformations. The pattern of inheritance of these malformations is multifactorial, rendering the identification of the underlying causes. Numerous studies have been conducted to elucidate the genetic basis of the development of the central nervous system. Essential signaling pathways of the development of the central nervous system include the planar cell polarity pathway, which is important for the initiation of neural tube closure as well as well as sonic hedhehog pathway, which regulates the neural plate bending. Genes and their mutations influencing the different stages of neurulation have been investigated for their eventual role in the development of these malformations. Among the environmental factors, folic acid seems to be the most important modifier of the risk of human neural tube defects. Genes of the folate metabolism pathways have also been investigated to identify mutations resulting in increased risk of NTDs. In this review the author has attempted to summarize the knowledge on neural tube defects, with special regard to genetic factors of the etiology.


Development ◽  
1998 ◽  
Vol 125 (24) ◽  
pp. 4919-4930 ◽  
Author(s):  
M.A. Selleck ◽  
M.I. Garcia-Castro ◽  
K.B. Artinger ◽  
M. Bronner-Fraser

To define the timing of neural crest formation, we challenged the fate of presumptive neural crest cells by grafting notochords, Sonic Hedgehog- (Shh) or Noggin-secreting cells at different stages of neurulation in chick embryos. Notochords or Shh-secreting cells are able to prevent neural crest formation at open neural plate levels, as assayed by DiI-labeling and expression of the transcription factor, Slug, suggesting that neural crest cells are not committed to their fate at this time. In contrast, the BMP signaling antagonist, Noggin, does not repress neural crest formation at the open neural plate stage, but does so if injected into the lumen of the closing neural tube. The period of Noggin sensitivity corresponds to the time when BMPs are expressed in the dorsal neural tube but are down-regulated in the non-neural ectoderm. To confirm the timing of neural crest formation, Shh or Noggin were added to neural folds at defined times in culture. Shh inhibits neural crest production at early stages (0-5 hours in culture), whereas Noggin exerts an effect on neural crest production only later (5-10 hours in culture). Our results suggest three phases of neurulation that relate to neural crest formation: (1) an initial BMP-independent phase that can be prevented by Shh-mediated signals from the notochord; (2) an intermediate BMP-dependent phase around the time of neural tube closure, when BMP-4 is expressed in the dorsal neural tube; and (3) a later pre-migratory phase which is refractory to exogenous Shh and Noggin.


Development ◽  
2002 ◽  
Vol 129 (10) ◽  
pp. 2507-2517 ◽  
Author(s):  
Patricia Ybot-Gonzalez ◽  
Patricia Cogram ◽  
Dianne Gerrelli ◽  
Andrew J. Copp

Neural tube closure is a fundamental embryonic event whose molecular regulation is poorly understood. As mouse neurulation progresses along the spinal axis, there is a shift from midline neural plate bending to dorsolateral bending. Here, we show that midline bending is not essential for spinal closure since, in its absence, the neural tube can close by a ‘default’ mechanism involving dorsolateral bending, even at upper spinal levels. Midline and dorsolateral bending are regulated by mutually antagonistic signals from the notochord and surface ectoderm. Notochordal signaling induces midline bending and simultaneously inhibits dorsolateral bending. Sonic hedgehog is both necessary and sufficient to inhibit dorsolateral bending, but is neither necessary nor sufficient to induce midline bending, which seems likely to be regulated by another notochordal factor. Attachment of surface ectoderm cells to the neural plate is required for dorsolateral bending, which ensures neural tube closure in the absence of sonic hedgehog signaling.


EBioMedicine ◽  
2015 ◽  
Vol 2 (6) ◽  
pp. 513-527 ◽  
Author(s):  
Chiharu Kimura-Yoshida ◽  
Kyoko Mochida ◽  
Kristina Ellwanger ◽  
Christof Niehrs ◽  
Isao Matsuo

2021 ◽  
Author(s):  
Neophytos Christodoulou ◽  
Paris Alexander Skourides

Neural tube closure (NTC) is a fundamental process during vertebrate embryonic development and is indispensable for the formation of the central nervous system. Here, using Xenopus laevis embryos, live imaging, single-cell tracking, optogenetics, and loss of function experiments we examine the contribution of convergent extension (CE) and apical constriction (AC) and we define the role of the surface ectoderm (SE) during NTC. We show that NTC is a two-stage process and that CE and AC do not overlap temporally while their spatial activity is distinct. PCP-driven CE is restricted to the caudal part of the neural plate (NP) and takes place during the first stage. CE is essential for correct positioning of the NP rostral most region in the midline of the dorsoventral axis. AC occurs after CE throughout the NP and is the sole contributor of anterior NTC. We go on to show that the SE is mechanically coupled with the NP providing resistive forces during NTC. Its movement towards the midline is passive and driven by forces generated through NP morphogenesis. Last, we show that increase of SE resistive forces is detrimental for NP morphogenesis, showing that correct SE development is permissive for NTC.


Development ◽  
1998 ◽  
Vol 125 (17) ◽  
pp. 3509-3519 ◽  
Author(s):  
C.A. Zygar ◽  
T.L. Cook ◽  
R.M. Grainger

Several stages in the lens determination process have been defined, though it is not known which gene products control these events. At mid-gastrula stages in Xenopus, ectoderm is transiently competent to respond to lens-inducing signals. Between late gastrula and neural tube stages, the presumptive lens ectoderm acquires a lens-forming bias, becomes specified to form lens and begins differentiation. Several genes have been identified, either by expression pattern, mutant phenotype or involvement in crystallin gene regulation, that may play a role in lens bias and specification, and we focus on these roles here. Fate mapping shows that the transcriptional regulators Otx-2, Pax-6 and Sox-3 are expressed in the presumptive lens ectoderm prior to lens differentiation. Otx-2 appears first, followed by Pax-6, during the stages of lens bias (late neural plate stages); expression of Sox-3 follows neural tube closure and lens specification. We also demonstrate the expression of these genes in competent ectoderm transplanted to the lens-forming region. Expression of these genes is maintained or activated preferentially in ectoderm in response to the anterior head environment. Finally, we examined activation of these genes in response to early and late lens-inducing signals. Activation of Otx-2, Pax-6 and Sox-3 in competent ectoderm occurs in response to the early inducing tissue, the anterior neural plate. Since Sox-3 is activated following neural tube closure, we tested its dependence on the later inducing tissue, the optic vesicle, which contacts lens ectoderm at this stage. Sox-3 is not expressed in lens ectoderm, nor does a lens form, when the optic vesicle anlage is removed at late neural plate stages. Expression of these genes demarcates patterning events preceding differentiation and is tightly coupled to particular phases of lens induction.


Development ◽  
1970 ◽  
Vol 23 (2) ◽  
pp. 463-471
Author(s):  
Carl-Olof Jacobson

The morphogenetic movements of the ectoderm during neurulation include: (1) the movements taking place within the neural plate, which becomes longer and more concentrated in a medio-lateral direction (Jacobson, 1962); and (2) those found in the lateral epidermis layer which, in an epibolic way, moves in a dorsal direction, thus exerting a pushing effect on the lateral edges of the neural plate (Lewis, 1947). The former is, to a great extent, realized by a change of form of the neuroepithelium cells, from cuboidal in early neurulae to the high columnar cells observed during later phases of neural-tube closure. In the epidermis, on the other hand, the case is the reverse. The dorsal spreading of the layer is made possible by a flattening of the cells. In a series of papers, Brachet and his group have show that β-mercaptoethanol (HSCH2·CH2OH; in this article, called ME) inhibits neurulation (for review, see Brachet, 1964).


Neurosurgery ◽  
1986 ◽  
Vol 18 (5) ◽  
pp. 559-564 ◽  
Author(s):  
James N. Gilbert ◽  
Kenneth L. Jones ◽  
Lucy B. Rorke ◽  
Gerald F. Chernoff ◽  
Hector E. James

Abstract Complete gross and microscopic neuropathological examinations of 25 children who died with meningomyelocele, the Arnold-Chiari malformation, and hydrocephalus revealed a wide range and frequency of associated central nervous system malformations. The most remarkable of these anomalies were hypoplasia or aplasia of cranial nerve nuclei (20%), demonstrable obstruction of cerebrospinal fluid flow within the ventricular system (92%), cerebellar dysplasia (72%), a disorder of migration of cortical neurons (92%), fusion of the thalami (16%), agenesis of the corpus callosum (12%), and complete or partial agenesis of the olfactory tract and bulb (8%). The anomalies associated with posterior neural tube closure defects can no longer be considered secondary, but rather must be considered part of a spectrum of malformations caused by an unidentified primary insult to the central nervous system. The frequency and pattern of brain malformations associated with neural tube defects of some children with meningomyelocele suggest that such malformations may seriously affect intellectual outcome.


2008 ◽  
Vol 314 (2) ◽  
pp. 393-403 ◽  
Author(s):  
Julaine Roffers-Agarwal ◽  
Jennifer B. Xanthos ◽  
Katherine A. Kragtorp ◽  
Jeffrey R. Miller

Sign in / Sign up

Export Citation Format

Share Document