scholarly journals Hallmarks of primary neurulation are conserved in the zebrafish forebrain

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Jonathan M. Werner ◽  
Maraki Y. Negesse ◽  
Dominique L. Brooks ◽  
Allyson R. Caldwell ◽  
Jafira M. Johnson ◽  
...  
Keyword(s):  
Neural Tube ◽  
Time Lapse ◽  
Neural Plate ◽  
Neural Tube Closure ◽  
Developmental Studies ◽  
Underlying Causes ◽  
The Central Nervous System ◽  
Resolution Imaging ◽  
Fold Formation ◽  
Anterior Neural Plate

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.

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 ◽  
...  
Keyword(s):  
Central Nervous System ◽  
Neural Tube ◽  
Neural Plate ◽  
Neural Tube Closure ◽  
Developmental Studies ◽  
Underlying Causes ◽  
The Central Nervous System ◽  
Neural Tube Development ◽  
Fold Formation ◽  
Tube Closure

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.

Gene activation during early stages of lens induction in Xenopus

Development ◽  
1998 ◽  
Vol 125 (17) ◽  
pp. 3509-3519 ◽  
Author(s):  
C.A. Zygar ◽  
T.L. Cook ◽  
R.M. Grainger
Keyword(s):  
Neural Tube ◽  
Gene Activation ◽  
Neural Plate ◽  
Neural Tube Closure ◽  
Gene Products ◽  
Optic Vesicle ◽  
Determination Process ◽  
Tightly Coupled ◽  
Anterior Neural Plate ◽  
Tube Closure

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.

scholarly journals Recent perspectives on the development of the central nervous system and the genetic background of neural tube defects

2009 ◽  
Vol 150 (19) ◽  
pp. 873-882 ◽  
Author(s):  
József Gábor Joó
Keyword(s):  
Central Nervous System ◽  
Nervous System ◽  
Neural Tube ◽  
Neural Tube Defects ◽  
Planar Cell Polarity ◽  
Genetic Basis ◽  
Neural Tube Closure ◽  
Increased Risk ◽  
Underlying Causes ◽  
The Central Nervous System

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.

scholarly journals Live imaging of apoptosis in a novel transgenic mouse highlights its role in neural tube closure

2011 ◽  
Vol 195 (6) ◽  
pp. 1047-1060 ◽  
Author(s):  
Yoshifumi Yamaguchi ◽  
Naomi Shinotsuka ◽  
Keiko Nonomura ◽  
Kiwamu Takemoto ◽  
Keisuke Kuida ◽  
...  
Keyword(s):  
Transgenic Mouse ◽  
Neural Tube ◽  
Resonance Energy Transfer ◽  
Resonance Energy ◽  
Time Lapse ◽  
Neural Tube Closure ◽  
Caspase Activation ◽  
Fluorescent Reporter ◽  
Time Lapse Imaging ◽  
Tube Closure

Many cells die during development, tissue homeostasis, and disease. Dysregulation of apoptosis leads to cranial neural tube closure (NTC) defects like exencephaly, although the mechanism is unclear. Observing cells undergoing apoptosis in a living context could help elucidate their origin, behavior, and influence on surrounding tissues, but few tools are available for this purpose, especially in mammals. In this paper, we used insulator sequences to generate a transgenic mouse that stably expressed a genetically encoded fluorescence resonance energy transfer (FRET)–based fluorescent reporter for caspase activation and performed simultaneous time-lapse imaging of apoptosis and morphogenesis in living embryos. Live FRET imaging with a fast-scanning confocal microscope revealed that cells containing activated caspases showed typical and nontypical apoptotic behavior in a region-specific manner during NTC. Inhibiting caspase activation perturbed and delayed the smooth progression of cranial NTC, which might increase the risk of exencephaly. Our results suggest that caspase-mediated cell removal facilitates NTC completion within a limited developmental window.

Inductive interactions direct early regionalization of the mouse forebrain

Development ◽  
1997 ◽  
Vol 124 (14) ◽  
pp. 2709-2718 ◽  
Author(s):  
K. Shimamura ◽  
J.L. Rubenstein
Keyword(s):  
Sonic Hedgehog ◽  
Bone Morphogenetic Proteins ◽  
Molecular Mechanisms ◽  
Neural Plate ◽  
Gene Encoding ◽  
Prechordal Plate ◽  
Optic Vesicles ◽  
The Central Nervous System ◽  
Anterior Neural Plate ◽  
Anterior Posterior

The cellular and molecular mechanisms that regulate regional specification of the forebrain are largely unknown. We studied the expression of transcription factors in neural plate explants to identify tissues, and the molecules produced by these tissues, that regulate medial-lateral and local patterning of the prosencephalic neural plate. Molecular properties of the medial neural plate are regulated by the prechordal plate perhaps through the action of Sonic Hedgehog. By contrast, gene expression in the lateral neural plate is regulated by non-neural ectoderm and bone morphogenetic proteins. This suggests that the forebrain employs the same medial-lateral (ventral-dorsal) patterning mechanisms present in the rest of the central nervous system. We have also found that the anterior neural ridge regulates patterning of the anterior neural plate, perhaps through a mechanism that is distinct from those that regulate general medial-lateral patterning. The anterior neural ridge is essential for expression of BF1, a gene encoding a transcription factor required for regionalization and growth of the telencephalic and optic vesicles. In addition, the anterior neural ridge expresses Fgf8, and recombinant FGF8 protein is capable of inducing BF1, suggesting that FGF8 regulates the development of anterolateral neural plate derivatives. Furthermore, we provide evidence that the neural plate is subdivided into distinct anterior-posterior domains that have different responses to the inductive signals from the prechordal plate, Sonic Hedgehog, the anterior neural ridge and FGF8. In sum, these results suggest that regionalization of the forebrain primordia is established by several distinct patterning mechanisms: (1) anterior-posterior patterning creates transverse zones with differential competence within the neural plate, (2) patterning along the medial-lateral axis generates longitudinally aligned domains and (3) local inductive interactions, such as a signal(s) from the anterior neural ridge, further define the regional organization.

Neurodevelopment

2020 ◽  
pp. 91-100
Author(s):  
Karl Zilles ◽  
Nicola Palomero-Gallagher
Keyword(s):  
Spinal Cord ◽  
Nervous System ◽  
Neural Tube ◽  
Neural Plate ◽  
Adult Brain ◽  
The Central Nervous System ◽  
Specialized Region ◽  
The Brain ◽  
Rostral Part ◽  
Human Nervous System

The pre- and post-natal development of the human nervous system is briefly described, with special emphasis on the brain, particularly the cerebral and cerebellar cortices. The central nervous system originates from a specialized region of the ectoderm—the neural plate—which develops into the neural tube. The rostral part of the neural tube forms the adult brain, whereas the caudal part (behind the fifth somite) differentiates into the spinal cord. The embryonic brain has three vesicular enlargements: the forebrain, the midbrain, and the hindbrain. The histogenesis of the spinal cord, hindbrain, cerebellum, and cerebral cortex, including myelination, is discussed. The chapter closes with a description of the development of the hemispheric shape and the formation of gyri.

scholarly journals Oriented cell divisions and cellular morphogenesis in the zebrafish gastrula and neurula: a time-lapse analysis

Development ◽  
1998 ◽  
Vol 125 (6) ◽  
pp. 983-994 ◽  
Author(s):  
M.L. Concha ◽  
R.J. Adams
Keyword(s):  
Cell Division ◽  
Time Lapse ◽  
Ventral Surface ◽  
Neural Plate ◽  
Common Mechanism ◽  
Gradual Transition ◽  
Animal Pole ◽  
Dorsal Midline ◽  
Vegetal Pole ◽  
The Central Nervous System

We have taken advantage of the optical transparency of zebrafish embryos to investigate the patterns of cell division, movement and shape during early stages of development of the central nervous system. The surface-most epiblast cells of gastrula and neurula stage embryos were imaged and analysed using a computer-based, time-lapse acquisition system attached to a differential interference contrast (DIC) microscope. We find that the onset of gastrulation is accompanied by major changes in cell behaviour. Cells collect into a cohesive sheet, apparently losing independent motility and integrating their behaviour to move coherently over the yolk in a direction that is the result of two influences: towards the vegetal pole in the movements of epiboly and towards the dorsal midline in convergent movements that strengthen throughout gastrulation. Coincidentally, the plane of cell division becomes aligned to the surface plane of the embryo and oriented in the anterior-posterior (AP) direction. These behaviours begin at the blastoderm margin and propagate in a gradient towards the animal pole. Later in gastrulation, cells undergo increasingly mediolateral-directed elongation and autonomous convergence movements towards the dorsal midline leading to an enormous extension of the neural axis. Around the equator and along the dorsal midline of the gastrula, persistent AP orientation of divisions suggests that a common mechanism may be involved but that neither oriented cell movements nor shape can account for this alignment. When the neural plate begins to differentiate, there is a gradual transition in the direction of cell division from AP to the mediolateral circumference (ML). ML divisions occur in both the ventral epidermis and dorsal neural plate. In the neural plate, ML becomes the predominant orientation of division during neural keel and nerve rod stages and, from late neural keel stage, divisions are concentrated at the dorsal midline and generate bilateral progeny (C. Papan and J. A. Campos-Ortega (1994) Roux's Arch. Dev. Biol. 203, 178–186). Coincidentally, cells on the ventral surface also orient their divisions in the ML direction, cleaving perpendicular to the direction in which they are elongated. The ML alignment of epidermal divisions is well correlated with cell shape but ML divisions within the neuroepithelium appear to be better correlated with changes in tissue morphology associated with neurulation.

scholarly journals Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm

Development ◽  
1998 ◽  
Vol 125 (24) ◽  
pp. 4919-4930 ◽  
Author(s):  
M.A. Selleck ◽  
M.I. Garcia-Castro ◽  
K.B. Artinger ◽  
M. Bronner-Fraser
Keyword(s):  
Neural Crest ◽  
Sonic Hedgehog ◽  
Neural Tube ◽  
Neural Crest Cells ◽  
Neural Plate ◽  
Bmp Signaling ◽  
Neural Tube Closure ◽  
Dorsal Neural Tube ◽  
Neural Ectoderm ◽  
Tube Closure

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.

Sonic hedgehog and the molecular regulation of mouse neural tube closure

Development ◽  
2002 ◽  
Vol 129 (10) ◽  
pp. 2507-2517 ◽  
Author(s):  
Patricia Ybot-Gonzalez ◽  
Patricia Cogram ◽  
Dianne Gerrelli ◽  
Andrew J. Copp
Keyword(s):  
Sonic Hedgehog ◽  
Neural Tube ◽  
Hedgehog Signaling ◽  
Neural Plate ◽  
Neural Tube Closure ◽  
Molecular Regulation ◽  
Sonic Hedgehog Signaling ◽  
Surface Ectoderm ◽  
Necessary And Sufficient ◽  
Tube Closure

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.

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