Division of Biology 139-74, California Institute of Technology, Pasadena, CA 91125, USA
* Author for correspondence (e-mail: mccauley{at}gg.caltech.edu)
Accepted 24 February 2003
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SUMMARY |
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Key words: Cranial neural crest, Lamprey, DiI
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INTRODUCTION |
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In an early attempt to study neural crest derivatives in the basal-most
vertebrate, ablation experiments were performed in the lamprey in which the
presumptive neural crest was extirpated resulting in lack of cartilage in the
branchial arches (Langille and Hall,
1988). However, this approach cannot distinguish whether neural
crest cells themselves contribute to the cartilage of the branchial arches or
if interactions between these cells and other tissues are required for
cartilage formation. Scanning electron microscopy (SEM) has also provided
important insight into the pathways of cranial neural crest migration in the
Japanese lamprey, Lampetra japonica
(Horigome et al., 1999
;
Kuratani et al., 1999
;
Kuratani et al., 2001
) but
does not allow definitive distinction of neural crest cells from other
mesenchymal populations. Furthermore, it is not possible to determine the
sites of origin or migratory pathways at particular axial levels.
In order to unambiguously follow neural crest migratory pathways in lamprey, it is necessary to perform vital dye labeling of small groups of cells in living embryos, thus allowing one to identify and follow cells from discrete sites of origin to their final destinations. We have undertaken a detailed study of migratory pathways of the cranial neural crest during development in the lamprey, Petromyzon marinus, using the lipophilic dye DiI to label small populations in the dorsal neural tube. We have focused on the cranial neural crest because migratory pathways at this axial level are well documented in a number of species, allowing a comparative analysis of these cells and their behavior between agnathans and gnathostomes. We have examined both the superficial migration of neural crest cells and their deeper, internal migration within the branchial arches. The results show that the general patterns of cranial neural crest migration from dorsal neural tube to ventral branchial arches are conserved throughout vertebrates, with cells migrating in identifiable streams. In particular, migration at the levels of the midbrain and most rostral hindbrain into the first branchial arch and midregion of the hindbrain into the second branchial arch appear very similar between multiple species. However, interesting differences are also observed between agnathans and gnathostomes, particularly at the level of the mid to caudal hindbrain. Neural crest cells arising from the mid-hindbrain displayed extensive caudal migration, and those originating from the more caudal hindbrain migrated in both rostral and caudal directions. Furthermore, neural crest cells from different axial levels populated the same arch. Importantly, no neural crest contribution to cranial sensory ganglia was noted, suggesting they may be entirely placode derived in the lamprey. The results suggest that there are fewer constraints to rostrocaudal migration of cranial neural crest cells in lamprey and that such constraints as well as additional neural crest derivatives may have arisen later in gnathostomes.
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MATERIALS AND METHODS |
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Embryos were staged according to the staging criteria established by Tahara
(Tahara, 1988) for
Lampetra reissneri. Developmental stages between Lampetra
and Petromyzon appear similar in morphology. P. marinus
zygotes (0-6 hours, stage 2) are 1 mm in size and go through gastrulation by
64-108 hours (stages 12-16). The embryos hatch between days 10 and 13, and are
3-5 mm in length (stages 24-25).
DiI labeling
Fertilization membranes were removed from stage 21 embryos with sharpened
forceps. Embryos were then held in place, dorsal side upwards, in 1 mm
depressions in an agarose-coated dish. DiI (CM-DiI, Molecular Probes, Eugene,
OR) was dissolved in ethanol and diluted in 0.3 M sucrose to 0.5 µg/µl.
Dilute DiI was backfilled into pulled glass electrodes and a single bolus was
pressure-injected beneath the ectoderm at the dorsal midline of embryos
(Fig. 1). Labeled embryos were
allowed to develop to stage 22-23 or to stage
25-26
(Tahara, 1988
) and fixed in 4%
paraformaldehyde (PFA). Selected embryos were embedded in 5% agarose and
vibratome sectioned (50 µm) to determine accurately cranial neural crest
cell migratory pathways internally. Sections (10 µm) were cut from embryos
embedded in Epon/Araldite. To determine the timing of late neural crest cell
migration, demembranated stage 21 embryos were first allowed to develop 24
hours, to stage 22, then labeled and fixed at stage 25 as described above.
Epifluorescence of embryos and sections was imaged using a Zeiss Axioskop 2
containing a rhodamine filter set. Images were collected using a Zeiss Axiocam
HRc imaging system.
|
AP2
AP2 in situ hybridization was performed as described by Meulemans
and Bronner-Fraser (Meulemans and
Bronner-Fraser, 2002).
Immunohistochemistry
Embryos fixed in 4% PFA and held in methanol were rehydrated into PBS, and
blocked for 1 hour at room temperature in PBS containing 1% heat-inactivated
goat serum and 1% BSA (PBS-SB), then treated with pre-adsorbed rabbit
-mouse Sox-10 (1/200; Chemicon) antibody (4°C, overnight). After
four 15 minutes washes in PBS, embryos were incubated in alkaline
phosphatase-conjugated goat
-rabbit secondary antibody (1/1000; 1 hour,
room temperature) and washed in PBS for 2 hours with agitation. Following
washes, embryos were developed in NBT/BCIP (Life Technologies) according to
manufacturer's instructions. A pan-Dlx antibody (kindly provided by Dr J.
Kohtz, from a construct by Dr G. Panganiban) was diluted 1/70 in PBS-SB as
described above. DiI-labeled tissue was preincubated 1 hour (room temperature)
in PBS-SB, then incubated at 4°C overnight, and rinsed for 3 hours in PBS.
Secondary antibody incubation (goat
-rabbit-alkaline phophatase)
followed by NBT/BCIP was performed as described above.
Neural crest cell ablation
The fertilization membranes were first removed from stage 21 embryos with
sharpened forceps. Sharpened tungsten needles were then used to make a small
longitudinal incision along the dorsal midline and neural crest cells were
scraped from the region dorsal to the hindbrain. After the operation, embryos
in lake water were held in agar-coated dishes at a constant 18°C and
allowed to develop to stage 26, and then were fixed in 4% PFA. Embryos were
discarded if the neural tube appeared to have been damaged in the operation.
Out of 30 embryos operated, 12 survived that appeared to have a complete
neural tube. These were chosen for subsequent observation.
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RESULTS |
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DiI labeling of cranial neural tube reveals axial differences in
cranial neural crest migratory patterns
In most species, neural crest cells begin their emigration from the neural
tube around the time of neural tube closure. Therefore, we labeled discrete
regions of the newly closed dorsal cranial neural tube of lamprey with focal
injections of the lipophilic dye, DiI, in order to mark newly formed cranial
neural crest cells. A single bolus of DiI was pressure injected beneath the
ectoderm at the dorsal midline (Fig.
1A) at selected levels along the rostrocaudal axis
(Fig. 1B). Embryos with label
in more than one site were discarded. When fixed and examined with
epi-illumination immediately after labeling, the focal DiI injections were
confirmed to be discrete and to have labeled only a small region
(Fig. 1A). For initial
experiments, embryos were labeled at stage 21, shortly after neural tube
formation, in order to mark early migrating neural crest cells. The migratory
pattern of neural crest cells was followed as a function of time, from 2-6
days post-injection, and at different axial levels. The number of embryos
examined after injection of DiI at each position along the neural axis is
indicated in Fig. 1C.
Migration of neural crest cells arising from the midbrain, rostral
hindbrain
Segmentation of the embryonic lamprey hindbrain is apparent only
transiently (Kuratani et al.,
1998a), making it difficult to find morphological markers
indicating rostrocaudal position. Therefore, the site of initial DiI
injections was determined by comparing labeled embryos with stage-matched
companion embryos stained for lamprey Pax2 expression
(Fig. 2). Pax2 marks the
mid-hindbrain boundary and the otic vesicle
(McCauley and Bronner-Fraser,
2002
), thus providing two positional markers for pinpointing the
site of the injection.
|
Migration of neural crest cells arising from the mid-region of the
hindbrain
We next examined neural crest migration from the hindbrain near the otic
vesicle. This region probably corresponds to the fourth to fifth hindbrain
rhombomere, though the unavailability of hindbrain molecular markers in the
lamprey prevents precise identification of the rhombomere of origin. Labeled
hindbrain neural crest cells were found within the second (hyoid) arch at
stages 23 (Fig. 3A) and 25
(Fig. 3F). Transverse sections
through a stage 23 embryo showed that migration in the hyoid arch occurred in
the lateral region subjacent to the ectoderm
(Fig. 3E). In horizontal
sections through stage 23 embryos, neural crest cells appeared to envelop the
mesoderm of the hyoid arch (Fig.
3C) both medially and laterally. Unexpectedly, we found that in
numerous cases, cells had migrated caudally along the entire length of the
presumptive pharyngeal region (Fig.
3B,C). At the time of fixation (stage 23), the mandibular and
hyoid regions had formed discrete arches as assessed by distinct endodermal
outpocketings that separate these arches and partition labeled cells. However,
the more caudal presumptive pharyngeal arch-forming region contained a column
of labeled cells that extended caudally beyond the posterior limit of the
developing pharynx (Fig. 3C).
Outpocketing of the caudal endoderm into pharyngeal pouches had not begun in
this region 48 hours after migratory cells were labeled (stage 23). A change
in the distribution of labeled neural crest cells within the arches was
observed by stage 25. In contrast to cells enveloping the mesodermal core both
medially and laterally, at this later stage, most labeled cells were now
restricted only to the region lateral to the mesoderm and adjacent to the
ectoderm (Fig. 3G).
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Migration of neural crest cells medial to the branchial arch
mesoderm
Ambiguity exists in the literature regarding patterns of neural crest
migration into the branchial arches of the lamprey. Damas
(Damas, 1944) reported
ectomescenchymal cells between the mesoderm and endoderm within the arches.
However, Neidert et al. (Neidert et al.,
2001
) found lamprey Dlx genes expressed in the neural crest
laterally between the ectoderm and a central core of mesoderm within each
arch. Kimmel et al. (Kimmel et al.,
2001
) suggested that in lamprey, neural crest cells involved in
the formation of branchial arch cartilages may migrate only lateral to the
mesoderm in the caudal branchial arches, in contrast to gnathostomes, where
neural crest cells completely surround the mesoderm
(Miller et al., 2000
), and
branchial arch cartilages form medial to the mesodermal core. By contrast,
Meulemans and Bronner-Fraser (Meulemans
and Bronner-Fraser, 2002
) found that AP2 is expressed in
lamprey cranial neural crest within each of the arches surrounding the
mesodermal core.
To resolve this discrepancy, we carefully examined sections through the
arches as a function of time and also compared the migration of DiI-labeled
cells with Dlx expression in the branchial arches (Figs
4,
5). Consistent with the
findings of Damas (Damas, 1944)
and Meulemans and Bronner-Fraser
(Meulemans and Bronner-Fraser,
2002
), we found that DiI-labeled neural crest cells migrating into
the presumptive branchial arches were positioned in a ring completely
surrounding the mesodermal core in each of the branchial arches
(Fig. 4D,
Fig. 5B,E). To determine
accurately the neural crest identity of cells in DiI-labeled embryos, we
compared the location of DiI-labeled cells with Dlx protein distribution
within an embryo. Interestingly, in our hands, a pan-Dlx antibody indicated
the presence of Dlx protein throughout the arches both lateral and medial to
the mesoderm in an overlapping pattern with DiI-labeled cells (compare
Fig. 5B with 5C, see also
Fig. 5F). This differs from the
report of Neidert et al. (Neidert et al.,
2001
) who showed Dlx expression only lateral to the
mesoderm in the lamprey. Taken together, these findings suggest that medial
migration of neural crest cells within the caudal branchial arches is not a
new feature of gnathostomes (Kimmel et
al., 2001
), but instead, the position of the branchial arch
cartilages depends on a mechanism independent of neural crest cell
migration.
Later DiI labeling suggests little spatiotemporal changes in
migratory pattern
In higher vertebrates, DiI labeling performed at progressively later stages
in chick and mouse (Serbedzija et al.,
1989; Serbedzija et al.,
1990
) has revealed that neural crest cells fill their derivatives
in a ventral-to-dorsal order, such that the earliest migrating cells populate
the most ventral derivatives. To test whether there was an orderly
contribution of neural crest derivatives in lamprey, DiI labeling was
performed at progressively later times. After labeling at stage 22, neural
crest cells originating from hindbrain
(Fig. 6B) or rostral spinal
cord regions (Fig. 6C; compare
to Fig. 6A) continued to
undergo ventral migration toward the pharyngeal arches and at stage 25 were
distributed similarly to those in embryos labeled at earlier stages (see
above). In two cases of labeling hindbrain neural crest cells, we found
extensive migration of cells into caudal branchial arches
(Fig. 6B). In addition to
ventral migration, caudal movement of cells appeared to continue at these
stages, with labeled migratory cells apparent in arches caudal to the initial
injection site (Fig. 6B). This
suggests that rostrocaudal migration of neural crest cells continued even in
late stages of migration. These results suggest that cranial neural crest
cells in lamprey do not fill their derivatives in a ventral to dorsal order as
they do in gnathostomes. Rather, both ventral and caudal migration appear to
continue in cells that emigrate from the neural tube at late times.
|
Stage 23 embryos were also injected in the caudal hindbrain region but in no case did we observe any migration away from the labeled site. This suggests that cranial neural crest cell emigration from the dorsal midline is completed by this stage (data not shown).
Ablation of the neural folds supports neural crest cell requirement
for melanocytes and dorsal fin
The DiI-labeling results above suggest that neural crest cells originating
from the caudal hindbrain and rostral trunk contribute to the dorsal fin. To
test this further, we removed a small region of the neural crest at the
hindbrain level in 30 stage 21 embryos. This neural crest removal resulted in
reduction of the dorsal fin (Fig.
7) and a concomitant loss of pigmentation in the affected area in
the 12 surviving embryos fixed at stage 25
(Fig. 7B) when compared with
control embryos (Fig. 7A).
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DISCUSSION |
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Rostrocaudal migration of branchial neural crest in lamprey
The present results, which are summarized in
Fig. 9, demonstrate that
cranial neural crest cells originating from the lamprey midbrain and rostral
hindbrain contribute cells to the first and second branchial arches, the
mandibular and hyoid arches of gnathostomes. This is similar to the migration
described through DiI labeling experiments in urodeles
(Epperlein et al., 2000) and
anurans (Collazo et al., 1993
),
with the exception of the degree of caudal migration observed from injections
into the rostral to mid-region of the hindbrain. Important differences between
lamprey and gnathostomes are particularly notable in caudal regions of the
hindbrain, where lamprey neural crest cells migrate extensively in both
rostral and caudal directions. In the chick and mouse, limited migration of
neural crest cells from individual rhombomeres to the adjacent rostral or
caudal rhombomere has been noted (Birgbauer
et al., 1995
). By contrast, this is greatly exaggerated in the
lamprey. Similarly, we find extensive migration of lamprey neural crest cells
originating from the hindbrain to more caudal positions in the ventral
pharyngeal region.
|
Some rostrocaudal migration of cranial neural crest cells has been noted in
other vertebrates, although not as marked as in the lamprey. When Schilling
and Kimmel (Schilling and Kimmel,
1994) performed a series of single cell labeling experiments in
zebrafish, they found that cranial neural crest cells contributed to the
caudal gill arches. Cells originating from a single axial level contributed
progeny in up to three adjacent arches. Furthermore, segmental restriction in
their migration appeared later, and in a rostrocaudal manner. Their results
suggest that similar mechanisms observed here in the lamprey may also exist in
other vertebrates, but are less obvious or have been missed.
Although we find that cells originating at a particular axial level can
populate different branchial arches, this does not necessarily rule out the
possibility that one axial level may contribute more cells to one arch than
others. In previous ablation studies, Langille and Hall
(Langille and Hall, 1988)
found a correlation between the removal of neural crest from a specific region
and the subsequent loss of cartilage from associated branchial arches.
However, they did not distinguish between a reduction and complete loss of
cartilage.
Positional identity in the pharyngeal region along the
anteroposterior axis
Our data suggest that neural crest cells in the caudal branchial region are
sequestered by the formation of the pharyngeal pouches. Therefore, it is
possible that pharyngeal identity occurs independent of neural crest cells and
that positional information may be conferred to the branchial neural crest
extrinsically only after the pouches have formed. Consistent with this, Veitch
et al. (Veitch et al., 1999)
showed in the chick that pharyngeal endoderm was patterned correctly in the
absence of neural crest.
There is evidence that retinoic acid (RA) signaling is important for proper
patterning of the pharyngeal endoderm in the mouse
(Wendling et al., 2000), but
not for the neural crest cells therein. In lamprey, Kuratani et al.
(Kuratani et al., 1998b
) have
demonstrated the importance of retinoic acid signaling in development of the
pharynx. Treatment of lamprey embryos with all-trans RA resulted in the loss
of anterior structures, including the pharynx
(Kuratani et al., 1998b
),
similar to the effect of RA treatment in other vertebrates. Effects on the
pharyngeal arches were concentration dependent, with rostral arches affected
by lower levels of RA treatment. Thus, positional identity along the
anteroposterior axis may depend on graded RA signaling. RA signaling has also
been shown to affect pharyngeal development in the invertebrate chordates,
amphioxus and ascidians (Escriva et al.,
2002
; Hinman and Degnan,
1998
). Taken together, such results suggest that pharyngeal
patterning in the lamprey probably occurs independently of neural crest cell
entry and depends on RA signaling.
Neural crest and the formation of branchial arch cartilages
In vertebrates, a subpopulation of neural crest cells differentiates into a
segmental set of cartilages that support the gill arches. Langille and Hall
(Langille and Hall, 1988) have
previously established that the neural crest is required for formation of
branchial arch cartilages in the lamprey. This set of cartilage bars is
located lateral to the gills in the lamprey pharyngeal walls, between the
ectoderm and the underlying core of mesoderm. By contrast, in gnathostome
fish, these cartilages are located medial to the mesoderm, between the
mesodermal core of the arch and the endoderm. This observation suggests
developmental differences in branchial arch cartilage formation between
agnathans and gnathostomes that lead to differential localization of branchial
arch cartilage condensations. Based on these topological differences, Kimmel
et al. (Kimmel et al., 2001
)
have suggested that the arrangement of the cartilage bars is related to the
migratory properties of the neural crest cells into this region. The
`outside-in' hypothesis proposes that the neural crest cells that invade the
mandibular arch segment of the lamprey undergo both medial and lateral
migration. By contrast, the neural crest cells that invade the caudal
branchial arches were proposed to migrate only along a lateral pathway in the
lamprey. In zebrafish, neural crest cells probably first migrate laterally
beneath the ectoderm into the pharyngeal arch region, and then subsequently
migrate medially to form a concentric ring about a core of mesoderm
(Miller et al., 2000
). Based
on the restriction of Dlx gene expression
(Neidert et al., 2001
) to the
lateral portion of the branchial arches in lamprey, Kimmel et al.
(Kimmel et al., 2001
) have
suggested that a medial migration of neural crest may not occur in the lamprey
and that this may explain the observation that the branchial arch cartilages
in gnathostomes are located medial to the mesodermal core, while in agnathans,
these cartilages are external, or lateral to the mesoderm. More recently,
however, Meulemans and Bronner-Fraser
(Meulemans and Bronner-Fraser,
2002
) have shown that another neural crest marker, AP2,
is located in a ring surrounding the mesodermal core of each pharyngeal arch.
This calls into question the proposed `outside-in' hypothesis. Furthermore,
Damas (Damas, 1944
) inferred
the presence of neural crest cells medial to the mesodermal core in caudal
branchial arches of the lamprey. These discrepancies could only be reconciled
by using vital dye labeling to analyze the definitive distribution of neural
crest cells.
Our DiI labeling data suggest that the localization of cranial neural crest cells in the lamprey does not differ from that seen in the branchial arches of zebrafish. We find that neural crest cells completely surround the mesodermal core in each of the branchial arches (Figs 3, 4, 5), indicating that medial migration within the caudal branchial arches is not a new feature of gnathostomes. This suggests that another mechanism is responsible for the different differentiation properties seen in formation of the branchial arch cartilages in agnathans and gnathostomes.
Dlx genes also may play an important role in cartilage differentiation, as
suggested by Kimmel et al. (Kimmel et al.,
2001). We found pan-Dlx expression within neural crest cells in
both medial and lateral positions in the caudal branchial arches. By contrast,
Neidert et al. (Neidert et al.,
2001
) found that expression of four lamprey Dlx genes was confined
to the lateral region in branchial arches. This finding may suggest a
cartilage-specific Dlx domain in the lamprey branchial arches. There is
evidence that expression in chondrocytes of the Type II collagen gene,
Col2a1, is regulated in response to Dlx2, a downstream target of BMP2
signaling (Xu et al., 2001
).
However, virtually nothing is known of the developmental mechanisms governing
cartilage formation in the lamprey. Recent studies have established that
lamprey cranial cartilages are composed of a non-collagenous protein called
lamprin, while caudal branchial arch and pericardial cartilages are composed
of a different, as yet only partially characterized non-collagenous matrix
protein (McBurney and Wright,
1996
; McBurney et al.,
1996
; Morrison et al.,
2000
; Wright et al.,
2001
). Although the downstream targets involved in cartilage
formation differ between agnathans and gnathostomes, speculation regarding the
conservation of developmental mechanisms that regulate formation of the
branchial arch cartilages and the role of the neural crest awaits
identification of key elements in this pathway within the lamprey.
Lack of neural crest contribution to cranial ganglia
Our data from DiI labeling and Sox10 immunoreactivity failed to detect a
neural crest contribution to the cranial sensory ganglia, suggesting they may
be entirely of placodal origin. The input of the neural crest into sensory
ganglia would thus represent an important innovation of the neural crest in
the gnathostome lineage. The previous evidence that neural crest contributes
to cranial sensory ganglia in lamprey came from several studies showing HNK1
immunoreactivity in cells of fixed embryos
(Hirata et al., 1997;
Hirata et al., 1998
;
Morikawa et al., 2001
). The
HNK1 epitope serves as a good neural crest marker in some vertebrates, such as
chick and reptiles, but is not a pan-species marker. Furthermore, it cannot
distinguish neural crest from placodal cells. Interestingly, Hirata et al.
(Hirata et al., 1997
) found
that cranial neural crest derivatives did not express the HNK-1 carbohydrate,
with the exception of the cranial sensory ganglia. The only other evidence to
suggest a neural crest contribution to cranial sensory ganglia came from
extirpation experiments, but these gave contradictory results
(Newth, 1951
;
Newth, 1956
). We not only
noted a lack of neural crest contribution to rostral cranial ganglia like the
trigeminal ganglion, but also found no evidence of a neural crest contribution
to the more caudal epibranchial ganglia. The latter are solely placode derived
in birds. This may suggest that in the lamprey, all the cranial ganglia are
placode derived, and that the contribution of the neural crest to the rostral
cranial ganglia is a derived character in vertebrate evolution.
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Conclusions |
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ACKNOWLEDGMENTS |
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