1 Department of Cell Biology and Neuroscience, Montana State University,
Bozeman, MT 59717, USA
2 Stowers Institute for Medical Research, Kansas City, MO 64110, USA
* Author for correspondence (e-mail: lefcort{at}montana.edu)
Accepted 29 October 2004
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SUMMARY |
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Key words: Chick, Neural crest, DRG, SG, Cell migration, Time-lapse imaging
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Introduction |
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The routes navigated by migrating trunk neural crest cells have been well
characterized: those neural crest cells that take a ventromedial route migrate
through the somatic mesoderm, stop midway along and lateral to the neural
tube, coalesce and give rise to the DRG. A subpopulation of trunk neural crest
cells that continue ventrally past the formation site of DRG accumulate
dorsolateral to the dorsal aorta and give rise to the SG. Neural crest cells
that migrate dorsolaterally underneath the ectoderm become melanocytes
(Tosney, 1978;
Erickson et al., 1980
;
Theiry et al., 1982
;
Loring and Erickson, 1987
).
Neural crest cell migration through the somites is patterned: cells enter the
rostral half but avoid the caudal half of the somite
(Keynes and Stern, 1984
;
Rickman et al., 1985
;
Bronner-Fraser, 1986
), and this
stereotypy generates segregated streams of cells, which form the basis for the
metameric pattern of the DRG, SG and spinal motor axons
(Bronner-Fraser, 1986
;
Lallier and Bronner-Fraser,
1988
; Oakley and Tosney,
1993
). Experimental evidence implicates extrinsic environmental
cues, localized in the somites, in guiding trunk neural crest cells. When
presumptive somites are rotated by 180°, neural crest cells and motor
axons migrate through the (now) caudal somite
(Bronner-Fraser and Stern,
1991
). This segregation of neural crest cells to follow a specific
migratory route or corridor suggests that the function of the operative
molecular mechanisms is to generate segregated lateral structures, such as the
DRG and SG.
Studies investigating the expression patterns of candidate molecules
influencing the migratory patterns of neural crest cells in vitro
(Erickson and Perris, 1993)
and in vivo (Bronner-Fraser,
1986
) have implicated neuregulins, bone morphogenetic proteins
(BMPs), semaphorins/collapsins and the Eph/ephrins family of molecules
(Krull, 2001
;
Graham, 2003
). Upon entering
the sclerotome, Eph-family receptors and their ephrin ligands mediate
repulsive interactions between neural crest and caudal half-sclerotome cells,
thereby restricting neural precursors to specific territories in the
developing nervous system (Krull et al.,
1997
; Wang and Anderson,
1997
). In addition to avoiding the actively inhibitory cues
present in the caudal half of each somite, there is evidence for the presence
of attractive, positive molecular interactions that influence neural crest
cell migration through the rostral half of each somite
(Koblar et al., 2000
;
Krull, 2001
). The stop signals
that regulate the cessation of migration at sites of DRG formation are less
characterized, however; an intact ß-catenin signaling pathway within
neural crest cells is required for the formation of DRG anlagen
(Hari et al., 2002
) and DRG
often form in aberrant locations in the absence of sonic hedgehog signaling
(Fedtsova et al., 2003
).
Sympathetic precursors respond to the local secretion of BMP-4 from the dorsal
aorta, which is necessary for inducing differentiation of mature sympathetic
ganglia, although its exact role in the migration of neural crest cells has
not been elucidated (Reissmann et al.,
1996
; Shah et al., 1996;
Schneider et al., 1999
;
McPherson et al., 2000
).
Targeted deletion of neuregulin, erbB2 or erbB3 genes all result in a marked
hypoplasia of the primary chain of SG
(Britsch et al., 1998
). In
these mutants, neural crest cells emigrate normally from the neural tube but
fail to migrate ventrally toward the dorsal aorta and hence to contribute to
SG anlagen formation; instead their migration is arrested dorsally in the
vicinity of the DRG anlagen. Thus, these data implicate neuregulin and its
receptors in the ventral migration of neural crest cells, although the
mechanisms by which they effect migration remain incompletely characterized.
Another guidance molecule, Sema3A and its receptor neuropilin-1 are required
for the arrest and aggregation of sympathetic neural precursors at their
normal site dorsolateral to the dorsal aorta
(Kawasaki et al., 2002
;
Bron et al., 2004
), although
the cellular mechanisms mediating these steps have not been elucidated.
Interestingly, it has been shown that trunk neural crest cells do not respond
to guidance cues known to influence the cranial neural crest
(Bronner-Fraser, 1993
),
indicating differences in either the environmental guidance cues present at
the two levels and/or in the guidance receptors expressed by cranial versus
trunk neural crest.
Due to their dorsal-to-ventral migration to deep within the embryo, the
cell-cell and cell-environment interactions that mediate DRG and SG formation
have been difficult to analyze in intact developing embryos. Cell tracking
studies of fluorescently labeled cranial neural crest cells revealed a rich
set of cell migratory behaviors, including collective chain-like cell
arrangements, suggesting that a sophisticated set of underlying patterning
mechanisms and extrinsic cues play a role in sculpting the migration pattern
(Kulesa and Fraser, 1998;
Teddy and Kulesa, 2004
). By
contrast, there is a paucity of knowledge on the migratory behaviors of neural
crest cells in the trunk region. A very useful trunk explant technique
designed to image the early sorting of trunk neural crest cells into streams
(Krull et al., 1995
) is
insufficient for imaging later events, due to complications with tissue
thickness and the beating of the developing heart. Several groups have used
transverse slice explants to study early events in the development of the PNS
(Hotary et al., 1996
;
Krull and Kulesa, 1998
).
However, this system is not ideal for imaging structures that develop along
the vertebrate rostrocaudal axis, such as the DRG and SG.
In this study, we investigated the cellular dynamics that mediate DRG and
SG formation. We followed fluorescently labeled trunk neural crest cells using
a novel sagittal explant technique and time-lapse confocal microscopy
(Kasemeier et al., 2004). To
our knowledge, this is the first study in which DRG and SG formation has been
described in spatiotemporal detail. We show that along their dorsoventral
migratory route, trunk neural crest cells are highly motile and dynamically
interact with neighboring cells and the environment via an elaborate extension
and retraction of filopodia. Some cells migrate collectively, forming
chain-like arrangements that stretch from the DRG to the SG. Surprisingly, the
segregated pattern of neural crest cell streams is not maintained once cells
arrive at the presumptive SG sites. Instead, cells disperse and intermix along
the anterior-posterior axis and contact cells in the neighboring SG sites.
Here we document this segregation process in detail and reveal for the first
time the highly dynamic filopodial activity that transforms an initially
continuous stream of cells into discrete, segregated SG. By imaging crest
cells we also found that rerouting of neural crest cells between developing
DRG and SG is temporally regulated in that early migrating cells, but not
later migrating cells, can reverse their direction of migration once they have
arrived in their target ganglion (DRG versus SG). The diverse cell migratory
behaviors and active reorganization at the target sites suggest that cell-cell
and cell-environment interactions are coordinated with dynamic molecular
processes to ultimately sculpt the organization of the PNS.
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Materials and methods |
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Preparation of sagittal explants
Embryos were removed from the egg using a paper ring (Whatman, #1001185),
cleaned in warmed Ringer's solution, and the surrounding membranes were
carefully removed using forceps. Sagittal explants of embryos ranging from HH
stage 17-22 were prepared by using the trunk sagittal explant technique
described in Kasemeier et al. (Kasemeier
et al., 2004) and also briefly described below. A trunk explant
was made from the region between the forelimbs and hind limbs. A cut along the
midline of the spinal column was made with a tungsten needle to splay open the
spinal cord. A razor blade was then inserted into the incision made with the
tungsten needle (A-M Systems, 717000) and sliced through the embryo to produce
two sagittal explants that can be cultured medial (cut) or lateral side
down.
A Millipore culture plate insert (Millipore, PICMORG50) was prepared by
coating with 20 µg/ml of fibronectin (Gibco, 33016-015). To increase image
resolution, we used a modified six-well dish with a hole in the center of the
bottom of the well, and a coverslip sealed with vacuum grease over the hole
(Kulesa and Fraser, 1998). The
sagittal explant was then transferred onto the Millipore filter with a few
drops of neural basal medium (Gibco, 21103-049) supplemented with B27 (Gibco,
17504-044). The filter with explant was then transferred into the coverslipped
well filled with supplemented neural basal media. Sufficient media was added
so that the level of the Millipore filter was reached (for media exchange
through the filter to the tissue) but not too much so that the filter floated
in the well. The other wells were filled with sterile water and the dish was
covered and sealed with parafilm to create a humidified chamber to place on
the heated microscope stage.
Time-lapse video microscopy
GFP-labeled explants were visualized using a laser scanning confocal
microscope (Zeiss LSM). Optical thickness was set between 10 and 20 µm in
z-height with a 10x Neofluar (NA=0.30) lens. This optical
thickness was optimal for the observation and tracking of the maximal number
of cells as they migrated ventrally over longer time periods. The microscope
was surrounded with an incubator composed of a snug-fitting cardboard box
surrounded by thermal insulation (Reflectix, BP24025) and a tabletop incubator
(Lyon Electric, 950-107) fed into one side of the box
(Kasemeier et al., 2004). The
fluorescent GFP plasmid was excited with the 488 nm laser line using the FITC
filter. Time-lapse images were recorded every 10 minutes for an average of
between 24 and 36 hours. Images were digitally collected and analyzed using
Zeiss AIM software and ImageJ v1.30 software (developed at NIH and available
on the Internet at
http://rsb.info.nih.gov/ij/).
Static image analysis and rendering (depth-coding and embossing) was done
using Adobe photoshop 7.0. In total, 12 embryonic explants were imaged for
>24 hours and five for between 6 and 24 hours. For higher resolution
imaging, explants were mounted on a coverslip [as described in Kulesa and
Fraser (Kulesa and Fraser,
2002
)] and imaged for 4-6 hours with a 40x LD-Achroplan,
Zeiss objective on a laser scanning confocal microscope (Zeiss LSM Pascal on a
Zeiss Axiovert).
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Results |
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Neural crest cells arrive adjacent to the dorsal aorta and disperse rostrally and caudally
After neural crest cells successfully traversed the somite, they dispersed
along a thin corridor rostrally and caudally, bordered on one side by the
ventral, outer, sclerotome edge and on the other side by the dorsal aorta,
(Fig. 6A; see Movie 2 in the
supplementary material). The spatial restriction of neural crest cells to the
rostral sclerotome was maintained only until the cells approached the ventral
edge of the sclerotome. Once through the sclerotome, neural crest cells
deviated from the metameric pattern that dictated their migration through the
somites and instead spread contiguously rostrally and caudally away from their
axial level of origin. By tracking individual cells we found that crest cells
could move at least two segments rostrally or caudally, in agreement with
previously published analysis of static images (data not shown)
(Yip, 1986). However, in
previous studies, it was not determined how cells ended up at axial segments
other than their site of origin: i.e, by moving along the neural tube (site of
origin) or the dorsal aorta (target). While our imaging analysis did not focus
on neural crest cell behavior while still in the neural tube, our studies
clearly indicate extensive migration and reorganization of neural crest cells
once they arrive alongside the dorsal aorta.
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Discussion |
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Chain formation is a common configuration adopted by migrating cells in the developing nervous system
Time-lapse analyses confirmed previously published observations that neural
crest cell trajectories maintain a metameric pattern while navigating through
the anterior portion of the somites (reviewed by
Krull, 2001;
Kuan et al., 2004
) and that,
while migrating, neural crest cells display collective movements, forming
chain-like arrays. Furthermore, the behavior of crest cells while in the
chain, versus those that apparently break from the chain, suggests that
cell-cell and cell-environment contacts play a key role in cell guidance to
the DRG and SG. Neural crest cells sampled the posterior region of the somite,
but maintained stereotypical migratory patterns. Along the migratory route,
cells displayed active filopodia in the direction of travel and toward the
posterior region of the somite. All cells maintained two long, prominent
filopodial extensions parallel to the direction of travel, connecting them to
their chain neighbors ahead and behind. These trunk crest cell migratory
behaviors of chain migration are reminiscent of those exhibited by migrating
cranial neural crest and gut neural crest
(Kulesa and Fraser, 1998
;
Young et al., 2004a
) and have
not been reported in the ventral migration of trunk neural crest cells as they
project toward the dorsal aorta. The chains tended to stretch from the dorsal
to ventral edge of the somites and consisted on average of approximately five
to six cells. Chain migration of neuronal precursors appears to be a common
mechanism of cell migration, exhibited prominently by subventricular zone
neurons migrating to the adult olfactory bulb in mice
(Lois et al., 1996
).
Neural crest cells reorganize as they migrate
Reorganization of cells destined for the DRG and SG not only occurs at the
target locations but also while they are en route, as evidenced by our finding
of cells being able to reorient ventrally or dorsally from their original
location at early time points and contribute to the other ganglion type (i.e.
DRG versus SG; Fig. 5). These
data support those of Goldstein and Kalcheim
(Goldstein and Kalcheim,
1991), which indicated the existence of a common pool of neural
crest cells at each axial level that gave rise to both the SG and DRG at that
level. Using grafts of exclusively rostral somites, DRG size could be
increased, which resulted in a corresponding decrease in the SG at the same
axial level. Thus, at least a subpopulation of migrating neural crest cells
has the capacity to populate such functionally diverse structures as the DRG
and SG, a finding that has also been shown in grafting experiments in ovo
(Schweitzer et al., 1983). Reorientation of neural crest cells was also found
in the cranial crest by Kulesa and Fraser
(Kulesa and Fraser, 2000
), who
showed that hindbrain neural crest cells can reroute their migratory pathways
and compensate for missing neural crest cells in a neighboring population.
Why do these cells deviate from their neighbors and change their target
site? This subpopulation may remain in a more pluripotent, plastic stage
longer than its neighbors and hence not be fully committed to one particular
ganglion fate. In fact, a temporal pattern is observed in which early on crest
cells can change their location from SG to DRG and vice versa, but later are
prevented from doing so. As development ensues, the SG and DRG become
sufficiently differentiated that a `boundary' is established between the DRG
and SG, such that crest cells traveling in reverse of their initial migration
direction can no longer cross this boundary between the structures and are
forced back in their original directions. This may reflect an actual physical
boundary, perhaps composed of the known inhibitory proteoglycans that surround
the notochord (Tosney and Oakley,
1990; Landolt et al.,
1995
; Perris and Perissinotto,
2000
), and/or be the manifestation of the differentiation sensory
of distinct and sympathetic precursors that no longer respond to the local
cues in the other ganglion type's environment and/or become repulsed by cues
in the other (now aberrant) environment. Specific members of the bHLH class of
transcription factors have been elegantly shown to regulate the
differentiation of sensory (Ngn 1 and Ngn2) versus
sympathetic progenitors (Mash1), indicating a pre-specification of
subsets of migrating neural crest cells
(Parras et al., 2002
;
Zirlinger et al., 2002
;
Luo et al., 2003
). Evidence
also indicates a role for Wnt-1 in specifying sensory precursor fate
(Lee et al., 2004
;
Bronner-Fraser, 2004
) and for
BMPs in inducing the differentiation of sympathetic precursors
(Reissmann et al., 1996
; Shah
et al., 1996; Schneider et al.,
1999
; McPherson et al.,
2000
). However, the exact time and place of fate restriction of
migrating neural crest cells remains an important question that could be
resolved by combining molecular marker methods with time-lapse image
analysis.
Formation of iterated, discrete sympathetic ganglia is not the direct result of patterned crest cell migration through the somites
After making the lengthy dorsoventral migration and arriving at the site of
the incipient SG, neural crest cells fail to maintain segregated streams,
suggesting that the inhibitory factors that restricted the neural crest to the
anterior portion of the somite may no longer influence the neural crest once
the cells traverse the ventral border of the sclerotome. Instead, we show here
that individual SG arise as a consequence of extensive neural crest cell
reorganization, coalescence and finally condensation into discrete ganglia.
Furthermore, this segregation process is mediated by dynamic intercellular
contacts and reiterated extension and retraction of multiple filopodia, a
behavior that may also be exhibited by neighboring streams of migrating
cranial neural crest cells and by gut neural crest cell streams
(Kulesa and Fraser, 2000;
Young et al., 2004a
;
Teddy and Kulesa, 2004
).
Eph/ephrin interactions have been implicated in restricting the trunk
neural crest cells to the anterior portions of the somite
(Krull et al., 1997;
Wang and Anderson, 1997
). Once
they have migrated through the ventral border of the sclerotome, the fact that
neural crest cells are then free to spread rostrally and caudally suggests
that these inhibitory molecular mechanisms are no longer operative. Instead,
in the absence of inhibitory guidance cues, intercellular interactions among
crest cells may dominate. In the cranial region lateral to the neural tube, it
has been shown that neighboring neural crest cell streams interact extensively
(Kulesa and Fraser, 2000
).
Thus, if the neural crest cells relied on intrinsic destination cues from the
neural tube, this alteration in behavior from one of strict axial segregation
to one of extensive intermixing would not be expected. Instead, our data
suggest that the local environment near the site of the incipient SG plays an
important role in influencing the behavior of neural crest cells.
The segregation of neural crest cells into specific areas along the dorsal
aorta to form the SG suggests a local cell sorting mechanism. Neural crest
cells that fill into the areas between the forming SG ultimately coalesce with
one of the incipient SG. The mechanism driving the compaction of cells into
specific SG may be repulsive and/or attractive. A repulsive molecule(s) may
become expressed in the (nonpermissive) region between the developing SG that
causes the neural crest cells to move away from the interganglionic space and
toward the SG sites. By contrast, or in addition, a cell adhesive molecule may
be expressed by differentiating sympathetic precursors that induces the
neighboring neural crest cells to adhere and coalesce with the developing SG.
Our data clearly indicate that increased intercellular contact with another SG
is accompanied by decreased physical contact with a cell in the
interganglionic space. Sorting of neural crest cells into distinct
subpopulations also takes place in the cranial region of the developing
vertebrate nervous system. In the hindbrain, Eph/ephrin signals at the
rhombomere boundary sites act to sort individual cells into particular
rhombomeric segments (Xu et al.,
1999). Specifically, some gene expression boundaries appear to
correlate with rhombomere boundaries, suggesting a mechanism that relatively
precisely marks a border between two cell populations
(Xu et al., 1999
). The
expression of several cell adhesion molecules correlates with the onset of
cell coalescence into discrete SG: both N-cadherin and NCAM are expressed in
the nascent SG (Duband et al.,
1985
; Akiyata and Bronner-Fraser, 1992). However, the operative
molecular mechanisms mediating the segregation of neural crest cells into
discrete ganglia remain to be elucidated.
Our finding, based on imaging neural crest cells in their native
environment, of the dynamic behavior of neural crest cells en route to their
destination sites adds complexity to the idea that the metameric organization
of neural-crest-derived structures depends on the alternation of rostrocaudal
properties within the somite. Several classes of guidance molecules have
spatiotemporal patterns in the somites consistent with a role in neural crest
and/or axon guidance; including semaphorins, neuregulins and BMPs. However,
these studies cannot explain our finding of neural crest cell dispersion
adjacent to the dorsal aorta followed by crest cell re-segregation into
discrete ganglia. What are the molecular mechanisms mediating these distinct
behaviors? In-vitro studies have shown that a class of semaphorins, namely
Sema3A, induces the collapse of sympathetic and DRG growth cones and of
migrating neural crest cells in vitro
(Adams et al., 1997;
Eickholt et al., 1999
;
Vastrik et al., 1999
;
Bron et al., 2004
). RNA
interference of the sema3 receptor, neuropilin-1, in chick neural crest cells
causes the premature (i.e. dorsal) arrest of neural crest cells destined to
form SG (Bron et al., 2004
).
The phenotype of mice with targeted deletions of either Sema3A or its receptor
neuropilin 1 is complex (Kawasaki et al.,
2002
). Mutant mice neural crest cells migrate normally through the
sclerotome, reach the dorsal aorta and turn on MASH1. However, they fail to
arrest and aggregate at the dorsal aorta and hence to give rise to mature SG.
Disruptions in expression of Neuregulins and/or their ErbB family of tyrosine
kinase receptors results in severe hypoplasia of the primary sympathetic
ganglion chain. Mice with targeted deletions in either the ligand or its
receptors, exhibit a lack of neural crest precursor cells in the anlage of the
primary sympathetic ganglion chain (Britsch
et al., 1998
). Although very informative, studies addressing
whether these molecules regulate the dispersion and re-segregation of neural
crest cells once they reach the dorsal aorta will be required. The question
remains, Why set up a metameric migration pattern when in the end you
redistribute and refine at the target location
(Young et al., 2004b
)?
In summary, the time-lapse analysis has revealed particularly intriguing, unexpected aspects of DRG and SG formation. The trunk neural crest cell behaviors in chains mimic behaviors reported in cranial and gut neural crest cells. Surprisingly, these tightly segregated cell streams disperse uniformly once at their target site near the dorsal aorta, yet within hours these neural crest cells sort and reassemble themselves into discrete SG. What remains is a careful dissection of the molecular mechanisms that mediate the cellular phenomena orchestrating the formation of two of the major neural crest derivatives, the DRG and SG.
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ACKNOWLEDGMENTS |
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Footnotes |
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Supplementary material for this article is available at http://dev.biologists.org/cgi/content/full/132/2/235/DC1
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