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DOI: 10.1002/DVDY.24304
REVIEW
DEVELOPMENTAL DYNAMICS
The development of a vertebrate neural epithelium with well-organized apico-basal polarity and a central lumen is essential
for its proper function. However, how this polarity is established during embryonic development and the potential inuence
of surrounding signals and tissues on such organization has remained less understood. In recent years the combined superior
transparency and genetics of the zebrash embryo has allowed for in vivo visualization and quantication of the cellular and
molecular dynamics that govern neural tube structure. Here, we discuss recent studies revealing how co-ordinated cellcell
interactions coupled with adjacent tissue dynamics are critical to regulate nal neural tissue architecture. Furthermore, new
ndings show how the spatial regulation and timing of orientated cell division is key in dening precise lumen formation at
the tissue midline. In addition, we compare zebrash neurulation with that of amniotes and amphibians in an attempt to
understand the conserved cellular mechanisms driving neurulation and resolve the apparent differences among animals.
Zebrash neurulation not only offers fundamental insights into early vertebrate brain development but also the opportunity
to explore in vivo cell and tissue dynamics during complex three-dimensional animal morphogenesis. Developmental Dynamics
C 2015 Wiley Periodicals, Inc.
245:197208, 2016. V
Key words: zebrash; neurulation; morphogenesis
Submitted 22 April 2015; First Decision 15 June 2015; Accepted 3 July 2015; Published online 14 July 2015
Introduction
Vertebrate Neural Tube Formation
The embryonic stages of central nervous system (CNS) development that result in the formation of a tubular structure are called
neurulation. The neural tube is an epithelium with well-defined
apico-basal polarity, which is a fundamental feature for further
brain development and function. Despite many years of research,
the molecular details of neurulation are not fully understood,
conceivably because of significant variation in this morphogenetic process among animal models. The cellular basis of vertebrate neurulation has been extensively investigated in avian,
amphibian and mouse embryos due to its propensity for dysregulation, resulting in neural tube defects (such as anencephaly and
spina bifida), one of the most common forms of human birth
defects (Colas and Schoenwolf, 2001; Copp et al., 2003). These
studies show that neural tube formation begins from an initial
flat sheet of cells called the neural plate that rolls up and fuses
Grant sponsor: Fondecyt; Grant number: 11110106; Grant sponsor:
Conicyt/ECOS; Grant number: C13B03.
*Correspondence to: Claudio Araya, Laboratory of Developmental Biology,
Instituto de Ciencias Marinas y Limnol
ogicas, Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja s/n, 5090000, Valdivia, Chile.
E-mail: claudio.araya@uach.cl
197
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Fig. 1. Zebrafish neurulation. AD0 : Transverse brightfield time-lapse images to show tissue movements of neurulation in the zebrafish (Danio
rerio) at the levels of the hindbrain and spinal cord. In all panels, the neural plate has been pseudocolored in yellow. In E and E0 the enveloping
layer has been pseudocolored in pale blue while the mesoderm in highlighted in red. AA0 : At 1011 hpf the neural plate is sitting over an underlying mesoderm. BB0 : By 1213 hpf, the neural plate has already converged toward the midline to generate a solid neural keel. CC0 : At 1517 hpf,
the solid neural keel changes shape to form another solid structure called the neural rod. DD0 : By 1820 hpf, the solid neural rod transforms into
the neural tube. EE0 : Tissue organization in the zebrafish neural plate. For simplicity only half of the neural plate is shown. While in anterior
regions such as the hindbrain, the neural plate is a multi-layered tissue, in more posterior regions (spinal cord) the neural plate is single-layered.
Note that in brain regions the lateral head mesoderm is often a single-layer, whereas in more posterior regions the underlying mesoderm is
arranged into compact tissue giving rise to somites. hpf, hours post fertilization; pm, paraxial mesoderm; nt, notochord; evl enveloping layer; np,
neural plate; mes, mesoderm. Arrows in B indicate tissue movements. Scale bar 50 mm. F,G: Representative stages of zebrafish neurulation
showing major cell and tissue rearrangements. EVL cells are showing in blue, np cells are showing in yellow, and mes cells are showing in pale
red. Extracellular matrix (ECM) is showing in red and is deposited between the neural tissue and the underlying mesoderm throughout neurulation.
F: At neural plate stages, neural cells are irregular in shape and thought to be organized within the superficial-deep axis of the neural anlage and
few cells undergo division. G: By neural keel stages, neural cells undergo elongation and intercalation within its superficial-deep axis. H: At neural
rod stages, neural progenitors changes its mitotic spindle orientation in 90deg and undergo polarized midline crossing cell division (Tawk et al.,
2007). Apical information is enriched at cleavage plane of dividing cells (green) 90degrees. Midline apical deposition is also found in neural cells
prior the midline-crossing division (green dots, Buckley et al., 2013). I: Finally, by neural tube stages, neural cells show well-established apical
(green) and basal (purple) polarity and a central lumen is formed. In all pictures, dividing cells appear in gray.
Zebrash Neurulation
Live imaging shows that zebrafish neural tube formation occurs
through a series of steps that differs slightly from most amniote
and amphibian embryos. A simple brightfield microscopy
approach has revealed that zebrafish neural tube formation is initiated at around 1011 hr postfertilization (hpf), when both the left
and right sides of the neural plate begin to converge toward the
dorsal embryonic midline (Fig. 1AA0 ,F). Later on, at 12 hpf, neuroectodermal cells begin to internalize at the midline and have
generated a solid neural keel by around 13 hpf (Fig. 1BB0 ,G).
Then, by 1517 hpf, the solid keel progresses to another solid
structure, the neural rod, which presents with a more cylindricallike morphology (Fig. 1CC0 ,H). Gradually the neural rod develops
well-defined apico-basal polarity with opposing apical surfaces
along a midline seam and finally, by 18 hpf, the neural rod has
transformed into a hollow neural tube by generating a lumen (Fig.
1DD0 ,I) (Schimtz et al., 1993; Papan and Campos-Ortega, 1997;
Kunz, 2004; Lowery and Sive, 2005; Ciruna et al., 2006; Hong and
Brewster, 2006). Therefore, while teleost zebrafish embryo neurulation proceeds by tissue internalization and subsequent cell rearrangement at the midline to form a lumen instead of the dorsal
folding that occurs in amniotes, the end result is the generation of
DEVELOPMENTAL DYNAMICS
Fig. 2. Cell and tissue organization during vertebrate neurulation. For simplicity only neural ectoderm (neural plate) and nonneural ectoderm (nnect) tissues have been considered. In all diagrams, grey cells with white nuclei represent a polarized epithelial organization while white cells with
gray nuclei represent nonpolarized tissue. Arrows indicate tissue movements A: Classical primary neurulation in the chick embryo (Gallus gallus).
This involves the invagination of an existing epithelium at the midline and lumen formation by rolling or folding up to form the neural tube. B: Neurulation in the frog Xenopus laevis involves the invagination of a bi-layered neural plate and the formation of a central lumen by tissue invagination.
C: Teleost neurulation in the zebrafish embryo (Danio rerio). This process shows similarities to both primary and secondary neurulation in other vertebrates. The neural plate converges and internalizes to form solid keel and subsequently rod primordia. Cell divisions occur at the midline of the
rod, the apical surface is established and cavitation generates a central lumen. The superficial grey epithelium here represents the enveloping layer
(EVL), a simple flattened epithelium of nonneural ectoderm, which covers the embryo. D: Classical secondary neurulation in the chick embryo (Gallus gallus). This is characterized by condensation of mesenchyme cells to form a solid primordium, which then undergoes an epithelial transition
to generate multiple lumens, which finally coalesce to form a continuous apical surface at the neural tube stage. In figures A and B, ng indicates
neural groove. Figure A adapted from Schoenwolf (1991), Figure B adapted from Schroeder (1970), Figure C adapted from a time-lapse movie (C.
Araya), and Figure D adapted from Colas and Schoenwolf (2001).
DEVELOPMENTAL DYNAMICS
DEVELOPMENTAL DYNAMICS
Fig. 3. Intrinsic and extrinsic mechanisms driving zebrafish neural tube morphogenesis. AC: Intrinsic mechanisms of teleost neurulation. Transverse confocal sections taken from time-lapse movies of zebrafish embryos labeled with membrane-tagged GFP. In all pictures, arrows indicate
the presence of the apical midline seam. A: By 20 hpf, wild-type (wt) embryos develop a neural tube with a single apical midline seam. B: Noncanonical Wnt/PCP mutant trilobite (tri) generates an aberrant neural tube with duplicated apical midlines. C: N-cadherin/cdh2 mutants fail to
undergo tissue invagination and embryos develop a T-shaped neural tube with abnormal apical midline seam configuration. DG: Extrinsic mechanisms of zebrafish neurulation. D: Series of confocal images taken from a timelapse movie using Histone2B-GFP (H2B-GFP) to label nuclei and
pseudocoloured to highlight the relationship of the neural plate (yellow), mesoderm (red) and the enveloping layer (EVL in white) during zebrafish
neurulation. EE0 : Cell movements between the neural plate (yellow) and underlying mesoderm (red) are tightly coupled during the initial stages of
neurulation. Arrowhead indicates the position of the dorsal midline. F: Tracks contrasting cell movements between wild-type embryos (purple neural plate and blue mesodermal cells) and mesoderm-less embryos (right, purple neural plate cells). Note the lack of coordination in cell movements
in MZoep mutant embryos. G: By 20 hpf, mesoderm-less embryos (Nodal/MZoep) develop an aberrant neural tube morphology and disorganized
apico-basal polarity as judged by the localization of the apical marker ZO-1. In all pictures, hpf indicates hr postfertilization and yellow dots indicate neural tissue. Figure B, adapted from Tawk et al., (2007), Figure D-G adapted from Araya et al., (2014).
(Ciruna et al., 2006; Tawk et al., 2007; Yang et al., 2009). Early
observations from the Campos-Ortega laboratory elegantly demonstrated that although the early zebrafish neural anlage is not a
conventional polarized tissue, neural plate morphogenesis occurs
as a coherent epithelial-like tissue as cells maintain their relative
position among neighbors while undergoing midline internalization (Papan and Campos-Ortega, 1994). At the cellular level, these
convergence movements of neural plate cells are thought to be
partially mediated by the activity of the noncanonical Wnt-PCP
pathway (Tada and Kai, 2009, 2012). During neural tube formation in both mice and amphibians, for instance, Wnt-PCP pathway genes are required for the coordinated convergence of
neuroprogenitor cells toward the dorsal midline (Murdoch et al.,
2001; Darken et al., 2002; Goto and Keller, 2002). The noncanonical Wnt/PCP pathway has also been proposed to act during
zebrafish neuroepithelial morphogenesis. Confocal time-lapse
analysis shows that Wnt/PCP pathway trilobite/strabismus
mutant embryos generate a wider and thicker neural primordium
from the early stages of neurulation (Fig. 3B) (Ciruna et al., 2006;
Tawk et al., 2007). Ciruna and colleagues (2006) interpret the
abnormal neural tube of MZtri as a consequence of the impaired
intercalation of neural cells during the neural keel-rod transition
(1517 hpf), thus attributing a cell autonomous role for the PCP
pathway during neurulation. Furthermore, they saw an
DEVELOPMENTAL DYNAMICS
nonneural ectoderm is required to complete neural plate convergence and to subsequently close the neural tube dorsally
(Schoenwolf, 1988; Moury and Schoenwolf, 1995). Recent functional studies along with live tissue quantification in the bilayered amphibian neural plate suggest that extrinsic pulling forces
produced by deep cells on the overlying nonneural ectoderm
depend on the cellcell adhesion molecule E-Cadherin and the
extracellular matrix (ECM) receptor, Integrin-1 (Morita et al.,
2012). In teleost fishes, the nonneural ectoderm layer is organized
differently to other vertebrates (Kunz, 2004). At early stages of
neurulation, the zebrafish neural anlage is covered by an overlying squamous epithelium termed the enveloping layer (EVL),
which remains almost motionless during the whole process of
neuruation and is, therefore, highly unlikely to exert any forces
on the neural tissue (Figs. 1F, 2C). Recent findings, however,
reveal that adjacent mesoderm is critical to coordinate cell movements within the neural plate toward the dorsal midline to form a
normal neural keel structure and generate a coherent and correctly polarized midline seam (Fig. 3D) (Araya et al., 2014). Moreover, quantification of cell and tissue behaviors in wild-type
embryos demonstrates that neural ectoderm and the underlying
mesoderm exhibit tightly coupled dorsal movements toward the
embryonic midline (Fig. 3E,F).
At present, the molecular mechanisms by which adjacent tissues, such as mesoderm, influence vertebrate neurulation are far
from understood. One possibility is to consider the underlying
mesodermal tissue as a source of ventraldorsal molecular cues
that can directly influence neural tissue organization and dynamics. This is perhaps most relevant to the most anterior brain
regions where the neural plate is multi-layered and cells must
thus maintain their relative superficial/deep positions during dorsal convergence (Hong and Brewster, 2006). Such vertical cues
could help to control both cell displacement and tissue adhesiveness within the neural plate. So far, however, there is no direct
evidence for such cues and so future studies carefully examining
spatio-temporal changes in gene expression are needed.
Alternatively, the mesoderm could be envisaged as a physical
substrate for converging neural plate cells. The close proximity
between the mesoderm and the neural plate might be enhanced
by the early deposition of basal ECM components such as Laminin and Fibronectin, which become firmly assembled between
these two tissues just before neurulation in zebrafish (10 hpf)
(Fig. 1F) (Latimer and Jessen, 2010). Basal lamina proteins are
also progressively assembled at the deep surface of the neural
plate in amniote embryos, at the junction between neural and
nonneural ectoderm layers (Martins-Green and Erickson, 1986;
Tuckett and Morriss-Kay, 1986; Morita et al., 2012). Evidence
from mouse and chicken suggests that upon interaction between
these two adjacent tissues, a series of cell shape changes are triggered that are required to complete neurulation (Martins-Green,
1988; Colas and Schoenwolf, 2001).
A third mechanism by which surrounding tissues influence neural tube formation is that adjacent tissues significantly constrain
the space by which neural plate cells can undergo collective displacements. In teleost fish, the neural plate is sandwiched between
the overlying EVL layer and subjacent mesoderm, thus forming a
narrow corridor through which neural cells can move (Fig. 1F). In
this situation, migrating neural plate cells display parallel and
smooth trajectories across the developing superficial-deep axis
(Araya et al., 2014), resembling laminar flows of viscous liquids
(Constantinescu, 1995). By analogy, loss of mesoderm generates
DEVELOPMENTAL DYNAMICS
Fig. 4. Apical cell polarity during zebrafish neurulation. A: Time series of a neural rod cell before, during and following C-division (12ss14ss).
Cells are labelled with Par3-GFP, a nuclear label (H2B-RFP) and a membrane label (Cherry-CAAX). Dotted lines show the tissue midline, dashed
lines show the basal edges of the tissue. ML, indicates midline. Before division, Par3-GFP accumulates in multiple relatively large puncta in the
cell cortex, approximately at the point where the cell intersects the tissue midline (20 mins). Upon entry into telophase, Par3-GFP is distributed to
the cleavage plane of dividing cells. As cells complete cytokinesis, Par3-GFP localises more distinctly to a narrow region at the midline (1 hr, 15
min). B: Model for establishment of cell polarity during zebrafish neurulation. During neural rod stages, contralateral cells integrate basal cues from
the basal lamina (laminin) and interdigitate across the tissue midline where nascent adhesions (magenta) may be formed. These adhesions may
then recruit puncta of apical polarity proteins (such as Par3 and ZO-1, green) to an approximate region around the tissue midline. Subsequently,
these puncta of Par3 could then recruit the centrosome (orange), which may then organize the microtubule cytoskeleton (blue arrows) from this
point. This microtubule cytoskeleton could then reinforce the localization of apical proteins to the midline, adding precision and allowing junctions
to mature. Blue arrows indicate direction of apical traffic. Figure A, adapted from Buckley et al., (2013).
DEVELOPMENTAL DYNAMICS
in PCP deficient zebrafish due to delayed convergence, elimination of Fz7 results in the complete absence of an apical midline.
While correct division orientation is clearly needed for normal
apical midline specialization, how this is coordinated in time and
space is totally unknown. It has been proposed that an intrinsic
timing mechanism operates to control cell polarization and
lumen formation in zebrafish. Using heterochronic cell transplantation experiments, Girdler and colleagues (2013) found that
C-division occurs within a specified time-window and that this
timing can even resist abnormal morphogenetic tissue environments and in vitro culture conditions. The mechanism by which
cells gauge and respond to developmental time is not yet known,
but cells do not seem to monitor time by counting the number of
cell cycles and in heterochronic environments, cell polarization
does not even require mirror-symmetric cell division (Girdler
et al., 2013). microRNAs have been suggested as possible molecular mediators of this developmental clock due to their roles in
several intracellular timers in C. elegans (Lee et al., 1993; Pasquinelli et al., 2000; Reinhart et al., 2000) and the requirement for
zebrafish brain morphogenesis (Giraldez et al., 2005). The above
example illustrates the importance of mechanisms that coordinate cell intrinsic programmes with morphogenetic movements
and environmental signals, both in time and space for correct
embryogenesis.
DEVELOPMENTAL DYNAMICS
tured on curved substrata this leads to a delay in closure of the posterior neuropore, the extent of which correlates with the angle of
curvature (van Straaten et al., 1993). The degree of axial curvature
also negatively correlates with the rate of neural tube closure
between different vertebrate species (Peeters et al., 1998). Thus, it is
possible that the zebrafish uses alternative mechanisms to overcome
high mechanical stress and minimize energy requirements. Division
and cellular remodeling may require less force generation than the
formation of neural folds and a hinge point, as in primary neurulation. Additionally, it is possible that the neural tissue of the zebrafish may contain fewer cells relative to other vertebrates. If this
were the case, the relative contribution of each constituent cell in
tissue-wide force generation would be much greater. The prevalence
of neurulation defects in other vertebrates is high (Copp et al.,
2013) but appears to be low in zebrafish and so the existence of
redundant mechanisms in zebrafish may also ensure that if one
mechanism goes wrong the crucial process of brain and spinal cord
development can still proceed.
Future Perspectives
There are significant differences in the process of neurulation
between fish and other vertebrates and it is, therefore, important to
analyze how far they possibly rely on the same basic mechanisms.
We have stressed in this review that the early cell and tissue organization (i.e., polarized vs. nonpolarized structure) play a significant role in the mechanisms of tissue internalization. In zebrafish
embryos, apico-basal identity is gradually established during the
course of neurulation and recent evidence suggests that the mechanism organizing such polarity at the midline is based on the integration of contralateral cellcell interaction and reinforced by
signals from the basal lamina. Moreover, the apparent discrepancy
between the alternative mechanisms used by teleost fish to make a
neural lumen, either with or without cell division, could be linked
to the existence of parallel redundant cellular and molecular mechanisms that underlie the maturation of apical junctional complexes
and drive cellular rearrangements. The high plasticity of neural
cells and the time delay before onset of polarity allows cells to
undergo complex tissue morphogenesis before they assemble stable apical junctions. Further in vivo analyses of cell dynamics
between teleosts and other vertebrate should establish true similarities and differences between teleost and other vertebrate neurulation. Particularly intriguing questions concern the mechanisms
that drive internalization of the fish neural plate to form the keel,
and the establishment of cellcell junctions across the midline of
the neural rod, which are essential to build a functional lumen.
Acknowledgments
We thank Jonathan Clarke and the Araya lab for helpful discussion
and comments on the manuscript and apologize to colleagues and
earlier researchers whose work could not be cited due to space constraints. We thank also Carlos Carmona-Fontaine for schematic
diagram in Figure 1.
References
per JC, Ju
licher F,
Aigouy B, Farhadifar R, Staple DB, Sagner A, Ro
Eaton S. 2010. Cell flow reorients the axis of planar polarity in
the wing epithelium of Drosophila. Cell 142:773786.
Araya C, Tawk M, Girdler GG, Costa M, Carmona-Fontaine C,
Clarke JDW. 2014. Mesoderm is required for coordinated cell
movements within zebrafish neural plate in vivo. Neural Dev 9:9.
DEVELOPMENTAL DYNAMICS
Biswas S, Emond MR, Jontes JD. 2010. Protocadherin-19 and Ncadherin interact to control cell movements during anterior neurulation. J Cell Biol 191:10291041.
Bit-Avragim N, Hellwig N, Rudolph F, Munson C, Stainier DY,
Abdelilah-Seyfried S. 2008. Divergent polarization mechanisms
during vertebrate epithelial development mediated by the
Crumbs complex protein Nagie oko. J Cell Sci 121:25032510.
Brook FA, Shum AS, Van Straaten HW, Copp AJ. 1991. Curvature
of the caudal region is responsible for failure of neural tube closure in the curly tail (ct) mouse embryo. Development 113:671
678.
Brun RB, Garson JA. 1983. Neurulation in the Mexican salamander
(Ambystoma mexicanum): a drug study and cell shape analysis
of the epidermis and the neural plate. J Embryol Exp Morphol
74:275295.
Buckley CE, Ren X, Ward LC, Girdler GC, Araya C, Green MJ,
Clark BS, Link BA, Clarke JD. 2013. Mirror-symmetric microtubule assembly and cell interactions drive lumen formation in the
zebrafish neural rod. EMBO J 32:3044.
Buckley CE, Clarke JD. 2014. Establishing the plane of symmetry
for lumen formation and bilateral brain formation in the zebrafish
neural rod. Semin Cell Dev Biol 31:100105.
Ciruna B, Jenny A, Lee D, Mlodzik M, Schier AF. 2006. Planar cell
polarity signalling couples cell division and morphogenesis during neurulation. Nature 439:220224.
Chan WY, Tam PPL. 1986. The histogenetic potential of neural
plate cells of early-somite-stage mouse embryos. J Embryol Exp
Morphol 96:183193.
Clarke J. 2009. Role of polarized cell divisions in zebrafish neural
tube formation. Curr Opin Neurobiol 19:134138.
Colas JF, Schoenwolf GC. 2001. Towards a cellular and molecular
understanding of neurulation. Dev Dyn 221:117145.
Constantinescu VN. 1995. Laminar viscous flow. New York:
Springer. 488 p.
Copp AJ, Greene ND, Murdoch JN. 2003. The genetic basis of
mammalian neurulation. Nat Rev Genet 4:784793.
Criley BB. 1969. Analysis of embryonic sources and mechanims of
development of posterior levels of chick neural tubes. J Morphol
128:465501.
Cui S, Otten C, Rohr S, Abdelilah-Seyfried S, Link BA. 2007. Analysis of aPKClambda and aPKCzeta reveals multiple and redundant functions during vertebrate retinogenesis. Mol Cell Neurosci
34:431444.
Darken RS, Scola AM, Rakeman AS, Das G, Mlodzik M, Wilson
PA. 2002. The planar polarity gene strabismus regulates convergent extension movements in Xenopus. EMBO J 21:4254.
Davidson LA, Keller RE. 1999. Neural tube closure in Xenopus laevis involves medial migration, directed protusive activity, cell
intercalation and convergent extension. Development 126:4547
4556.
Duband JL, Blavet C, Jarov A, Fournier-Thibault C. 2009. Spatiotemporal control of neural epithelial cell migration and
epithelium-to-mesenchyme transition during avian neural tube
development. Dev Growth Differ 51:2544.
Dzamba BJ, Jakab KR, Marsden M, Schwartz MA, DeSimone DW.
2009. Cadherin adhesion, tissue tension, and noncanical Wnt
signaling regulate fibronectin matrix organization. Dev Cell 16:
421432.
Elul T, Keller R. 2000. Monopolar protrusive activity: a new morphogenetic cell behaviour in the neural plate dependent on the
vertical interactions with the mesoderm in Xenopus. Dev Biol
224:319.
ttir
Fournier-Thibault C, Blavet C, Jarov A, Bajanca F, Thorsteinsdo
S, Duband JL. 2009. Sonic hedgehog regulates integrin activity,
cadherin contacts, and cell polarity to orchestrate neural tube
morphogenesis. J Neurosci 29:1250612520.
Freeman BG. 1972. Surface modifications of neural epithelial cells
during formation of the neural tube in the rat embryo. J Embryol
Exp Morphol 28:437448.
Geldmacher-Voss B, Reugels AM, Pauls S, Campos-Ortega JA.
2003. A 90-degree rotation of the mitotic spindle changes the
orientation of mitoses of zebrafish neuroepithelial cells. Development 130:37673780.
DEVELOPMENTAL DYNAMICS
n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129:32813294.
Li S, Esterberg R, Lachance V, Ren D, Radde-Gallwitz K, Chi F,
Parent JL, Fritz A, Chen P. 2011. Rack1 is required for Vangl2
membrane localization and planar cell polarity signaling while
attenuating canonical Wnt activity. Proc Natl Acad Sci U S A
108:22642269.
Lowery LA, Sive H. 2004. Strategies of vertebrate neurulation and
a reevaluation of teleost neural tube formation. Mech Dev 121:
11891197.
Lowery LA, Sive H. 2005. Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie
oko and snakehead/atp1a1a.1 gene products. Development 132:
20572067.
Lowery LA, Sive H. 2009. Totally tubular: the mystery behind function and origin of the brain ventricular system. Bioessays 31:
446458.
Martins-Green M, Erickson CA. 1986. Development of the neural
tube basal lamina during neurulation and neural crest cell emigration in the trunk of the mouse embryo. J Embryol Exp Morphol 98:219236.
Martins-Green M. 1988. Origin of the dorsal surface of the neural
tube by progressive delamination of epidermal ectoderm and
neuroepithelium: implications for neurulation and neural tube
defects. Development 103:687706.
Menzies AS, Aszodi A, Williams SE, Pfeifer A, Wehman AM, Goh
KL, Mason CA, Fassler R, Gertler FB. 2004. Mena and
vasodilator-stimulated phosphoprotein are required for multiple
actin-dependent processes that shape the vertebrate nervous
system. J Neurosci 37:80298038.
Minc N, Bratman SV, Basu R, Chang F. 2009. Establishing new
sites of polarization by microtubules. Curr Biol 19:8394.
Minc N, Piel M. 2012. Predicting division plane position and orientation. Trends Cell Biol 4:193200.
Miyayama Y, Fujimoto T. 1997. Fine morphological study of neural
tube formation in the teleost, Oryzias latipes. 188:315330.
Morin X, Bellache Y. 2011. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev
Cell 21:102119.
Morita H, Kajiura-Kobayashi H, Takagi C, Yamamoto TS, Nonaka
S, Ueno N. 2012. Cell movements of the deep layer of nonneural ectoderm underlie complete neural tube closure in Xenopus. Development 139:14171426.
Moury JD, Schoenwolf GC. 1995. Cooperative model of epithelial
shaping and bending during avian neurulation: autonomous
movements of the neural plate, autonomous movements of the
epidermis, and interactions in the neural plate/epidermis transition zone. Dev Dyn 204:323337.
Munson C, Huisken J, Bit-Avragim N, Kuo T, Dong PD, Ober EA,
Verkade H, Abdelilah-Seyfried S, Stainier DY. 2008. Regulation
of neurocoel morphogenesis by Pard6 gamma b. Dev Biol 324:
4154.
Murdoch JN, Duodney K, Paternotte C, Copp AJ, Stanier P. 2001.
Severe neural tube defects in the loop-tail mouse result from
mutation of Lpp1, a novel gene involved in the floor plate specification. Hum Mol Genet 10:25932601.
Nishimura T, Honda H, Takeichi M. 2012. Planar cell polarity links
axes of spatial dynamics in neural-tube closure. Cell 149:1084
1097.
OBrien LE, Jou TS, Pollack AL, Zhang Q, Hansen SH, Yurchenco
P, Mostov KE. 2001. Rac1 orientates epithelial apical polarity
through effects on basolateral laminin assembly. Nat Cell Biol 9:
831838.
OConnell CB, Wang YL. 2000. Mammalian spindle orientation and
position respond to changes in cell shape in a dynein-dependent
fashion. Mol Biol Cell 5:17651774.
Palmer RE, Sullivan DS, Huffaker T, Koshland D. 1992. Role of
astral microtubules and actin in spindle orientation and migration
in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 119:
583593.
Papan C, Campos-Ortega JA. 1994. On the formation of the neural
keel and neural tube of the zebrafish Danio (Brachyodanio) rerio.
Rouxs Arch Dev Biol 203:178186.
DEVELOPMENTAL DYNAMICS