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First published online March 14, 2008
Journal of Experimental Biology 211, 1163-1168 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015461
Identification of novel genes including Dermo-1, a marker of dermal differentiation, expressed in trout somitic external cells
INRA (National Institute for Agricultural Research), Joint Research Unit for Fish Physiology, Biodiversity and the Environment, INRA Scribe, IFR140, Campus de Beaulieu, 35042, Rennes, France
* Author for correspondence (e-mail: pierre-yves.rescan{at}rennes.inra.fr)
Accepted 5 February 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: myogenesis, somite, dermomyotome, myotome, dermatome, Dermo-1, Pax7, Seraf, collectin, teleost
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). The development of the myotome begins before somite
formation with the expression of myogenic regulatory factors in the adaxial
cells located in the most medial presomitic mesoderm adjacent to the notochord
(Weinberg et al., 1996).
Shortly after somite formation, the adaxial cells differentiate and migrate
radially to reach the lateral surface of the myotome, where they form
peripheral slow-twitch muscle fibres
(Devoto et al., 1996). As
adaxial cells begin to differentiate deep in the somite, cells in the
posterior of the somite start to express myogenic regulatory factors. Later
on, behind the wave of adaxial cell migration, posterior somite cells
differentiate into medial fast muscle fibres. Cells of the sclerotome, for
their part, express Pax9 (Nornes et al.,
1996), twist (Stickney et al.,
2000), bapx1 (Yasutake et al.,
2004) and collagen I (Rescan
et al., 2005), and are initially present at the ventromedial
surface of the somite. As development proceeds, they migrate dorsally around
the notochord where, at a later stage, the vertebral column forms
(Morin-Kensicky and Eisen, 1997).
For many years, several authors have reported the presence of flattened
cells that are lateral to the developing fish myotome
(Waterman, 1969; Vegetti et
al., 1990; Johnston, 1993;
Lopez-Albors et al., 1998).
These cells do not exhibit any characteristics of immature muscle fibres, such
as the presence of contractile filaments
(Waterman, 1969;
Johnston, 1993;
Lopez-Albors, 1998;
Rescan et al., 2005;
Devoto et al., 2006), but
express the paired box transcription factors Pax3 and Pax7 suggesting that
they form a myogenic epithelium homologous to the amniote dermomyotome
(Devoto et al., 2006;
Groves et al., 2005;
Hammond et al., 2007;
Feng et al., 2006;
Steinbacher et al., 2006;
Steinbacher et al., 2007). The
myogenic capacity of the external cells has recently been demonstrated in
zebrafish by vital dye staining and lineage tracking techniques, which
revealed that some external cells are incorporated into the myotome,
generating new myofibres contributing to the burst of growth taking place in
larval myotome (Hollway et al.,
2007; Stellabotte et al.,
2007). Furthermore vital dye staining and lineage tracking
techniques showed that external cells are initially present at the anterior
border of epithelial somites before migrating to the external surface of the
somite. Expression of collagen genes in somitic external cells of teleost
(Le Guellec et al., 2004;
Rescan et al., 2005)
substantiated the view that the external cell epithelium contributes to dermis
formation. The only dermal marker available to date is Dermo-1 (twist-2) a
basic helix–loop–helix (bHLH) transcription factor. In mouse,
Dermo-1 gene is expressed in the newly formed dermis and subsequently
restricted to the epidermal–dermal junction
(Li et al., 1995). In chick,
Dermo-1 transcript is detected in the mediodorsal subectodermal mesenchyme of
the integument (Scaal et al.,
2001). Dermo-1 is not an exclusive marker of the differentiating
dermis since it is also expressed in sclerotome and limb mesenchyme
(Li et al., 1995;
Scaal et al., 2001). However,
its crucial role in dermis formation has been demonstrated by the generation
of Dermo-1(–/–) mice that exhibit a thin, loose dermis
(Sosic et al., 2003). We
report in this study the cloning of a trout orthologue of Dermo-1 and
show that this gene is expressed in Pax7-positive somitic external cells,
indicating that these cells have dermis-related characteristics in addition to
exhibiting myogenic features. We also report here the identification of two
new genes expressed in external cells, a gene related to Seraf, which
encodes an EGF-like repeat autocrine factor involved in developmental
processes of Schwann cell lineage in chicken
(Wakamatsu et al., 2004), and
a gene encoding collectin sub-family member 12 (also called collectin 1
precursor CL-3), a transmembrane lectin potentially involved in innate
immunity and cell–cell interactions
(Drickamer and Taylor, 1993;
Hogenkamp et al., 2006). The
somitic expression of a collectin and a Seraf gene is reported for
the first time in vertebrates.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Whole-mount in situ hybridisation
Dermo-1, collectin subfamily member 12, Seraf and slow myosin
light chain 1 (GenBank accession no. 076946) cDNAs were derived from a
large-scale, rainbow trout 3' and 5' sequencing project
(Govoroun et al., 2006).
Pax7 exon 1 was obtained from the screening of a rainbow trout
bacterial artificial chromosome (BAC) library
(Palti et al., 2004) using
primers designed from salmon Pax7 cDNA sequence (Gottenspare et al.,
2006). Myogenin was previously characterised
(Rescan et al., 1995). All
digoxigenin-labelled antisense RNA probes were synthesised from a
PCR-amplified template using appropriate RNA polymerases. The embryos were
dechorionated with fine forceps and fixed overnight at 4°C in
paraformaldehyde in phosphate buffered saline (PBS). Specimens were dehydrated
and stored in methanol at –20°C. After rehydration in graded
methanol–PBS baths, embryos were processed according to established
automated procedures (Quiring et al.,
2004) with minor modifications. Double whole-mount in
situ hybridisations were performed as previously described
(Rescan et al., 2001).
Histological methods
For histological examinations, embryos were embedded in 30% ovalbumin, 0.5%
gelatine and 1% gluteraldehyde in PBS. Blocks were sectioned at 30 µm on a
Leica vibratome. Alternatively, embryos were dehydrated and mounted in
paraffin, and 10 µm sections were then prepared. Sections were
counterstained with nuclear Fast Red and mounted in Mowiol (Calbiochem, La
Jolla, CA, USA).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Groves et al.,
2005; Hammond et al.,
2007; Feng et al.,
2006; Steinbacher et al.,
2006; Macqueen et al.,
2007), we first analysed the expression of Pax7, a paired
homeodomain transcription factor that is involved in the emergence and
survival of muscle progenitors (Buckingham
and Relaix, 2007). Using an antisense riboprobe corresponding to
the first exon, we observed that the somitic expression of Pax7 was first
detected around the 20 somite stage and was restricted to the anterior part of
the 12–15 more rostral somites. Frontal sections in various staged
embryos confirmed the initial localisation of Pax7 transcript in the anterior
compartment of the somite and indicated that Pax7 transcript was excluded from
the adaxial cells (Fig. 1A). As
the somite matured rostro-caudally, Pax7 labelling progressively moved from
the anterior to the lateral part of the somite (not shown) to become, at the
end of the segmentation period, visible in the somitic external cells
(Fig. 1B) lateral to slow
fibres (Fig. 1C). We have
previously reported that external cells express collagen I (
1)
suggesting that they form an epithelium sharing many characteristics with
amniote dermatome (Rescan et al.,
2005). To further examine the relationship between the trout
external cell epithelium and amniote dermis we analysed the gene expression
pattern of Dermo-1 a reliable marker for the onset of dermis
differentiation (Li et al.,
1995). A trout Dermo-1 cDNA (GenBank accession no.
EU004088) was identified from a large-scale rainbow trout 3' and
5' sequencing project (Govoroun et
al., 2006). The trout Dermo-1 putative protein, which contains a
bHLH domain, showed 82% identity to mouse twist-related protein 2 (Dermo-1)
and only 65% identity to twist-related protein 1 (Fig. S1 in supplementary
material). Whole-mount in situ hybridisation indicated that the
expression of Dermo-1 started around the 10-somite stage [stage 10B of Ballard
(Ballard, 1973)] in the head
mesenchyme and in somites (Fig.
2A). No labelling was observed in the segmental plate from which
somites form. As somitogenesis proceeded rostro-caudally, the labelling
progressively appeared in more caudal somites
(Fig. 2B,C) and did not exhibit
any antero-posterior variation within individual somites. Transverse sections
indicated that Dermo-1 expression was initially present in the dorsal domain
of the somite (Fig. 2D),
immediately above the myogenin-positive adaxial cells
(Fig. 2H). As the somite
matured, Dermo-1 expression extended to the dorso-lateral domain of the somite
(Fig. 2E,F) partially
overlapping the myogenin-positive embryonic myotome
(Fig. 2I,J). At around the
20-somite stage, sclerotome cells located in the ventromedial region of the
somite started to express Dermo-1 (Fig.
2E). Later on, Dermo-1-expressing sclerotome cells exhibited an
apparent migration towards the dorsal side of the notochord
(Fig. 2F), as was expected for
migrating sclerotome cells contributing to vertebral cartilage and connective
tissue. At the eyed stage, Dermo-1 expression was observed within the external
cell layer epithelium (Fig. 2G)
surrounding the myogenin-positive embryonic myotome
(Fig. 2K) and in postmigratory
sclerotome cells (Fig. 2G,K).
Taken together, our observations show that all the external cells in late
trout embryos express both the paired homeodomain transcription factor Pax7
and the dermal marker Dermo-1.
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Identification of two novel genes expressed in trout somitic external cells: collectin sub-family member 12 and Seraf
We screened eyed-stage embryos for genes expressed at the surface of the
myotome by random in situ hybridisation using riboprobes generated
from a normalised library prepared from trout multitissue cDNAs
(Govoroun et al., 2006). We
thus isolated two cDNA clones from this screening, one related to collectin
sub-family member 12 and the other to Seraf. The collectin cDNA (GenBank
accession no. EU008733) encoded an incomplete protein that exhibited
approximately 50% identity with chicken collectin sub-family member 12 and
very limited identity with other proteins. The deduced amino acid sequence of
the trout collectin cDNA included a carbohydrate recognition domain (CRD)
containing the conserved Gln–Pro–Asp motif involved in sugar
binding, as well as a collagen-like region consisting of Gly–X–Y
triplets (Fig. S2 in supplementary material). Whole-mount in situ
hybridisation showed that the expression of collectin sub-family member 12
started around the 10-somite stage (Fig.
3A). At this stage, collectin sub-family member 12 transcript was
detected in somites, lateral plate and cephalic mesenchyme
(Fig. 3A). As somitogenesis
proceeded along an antero-posterior axis, the labelling progressively appeared
in more caudal somites (Fig.
3B,C). Transverse sections showed that collectin transcript
initially accumulated in the dorsal domain of the somite
(Fig. 3D). As the somite
matured, collectin sub-family member 12 expression extended to a large domain
of the somite including the sclerotome at the ventromedial edge of the somite
(Fig. 3E). Later on, collectin
sub-family member 12 expression was observed in external cells surrounding the
primary myotome and sclerotome cells adjacent to the axial notochord
(Fig. 3F). At the eyed stage,
collectin sub-family member 12 expression was observed in branchial arches
(Fig. 3C), external cells,
sclerotome cells and epidermis (Fig.
3G).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Johnston, 1993;
Lopez-Albors et al., 1998).
The recent observation that this epithelium expresses Pax3 and/or Pax7
(Devoto et al., 2006;
Feng et al., 2006;
Hammond et al., 2007;
Steinbacher et al., 2006;
Steinbacher et al., 2007;
Macqueen et al., 2007), and
the experimental demonstration that external cells in zebrafish give rise to
new muscle fibres (Hollway et al.,
2007; Stellabote et al., 2007) have led to the suggestion that the
external cell epithelium is the evolutionary homologue of amniote
dermomyotome-generating myogenic cells for myotome growth
(Devoto et al., 2006;
Stellabote and Devoto, 2007). In line with these findings we show here that
all of the cells forming the external cell epithelium surrounding the trout
embryonic myotome are potentially myogenic as indicated by Pax7 expression.
The homology between teleost external cells and amniote dermomyotome implies
that some dermis-related characteristics might be associated in addition to
myogenic features. It has been shown that external cells of zebrafish
(Le Guellec et al., 2004) and
trout (Rescan et al., 2005)
express type I collagen, a major marker gene for dermis
(Epstein and Munderloh, 1978;
Niederreither et al., 1992).
Expanding these data, we further show in this study that all somitic external
cells in trout embryo also express Dermo-1, a twist-like bHLH transcription
factor that marks in amniotes the onset of dermis differentiation. Taken
together these observations indicate that trout external cells exhibit
features of bipotency and raise the important issue of the contribution of
external cells to dermis formation. One possibility is that trout somitic
external cells colonize the subectodermal space and give rise to dermis as
demonstrated for the (at least) bipotent cells present in the chick
dermomyotome sheet (Ben-Yair and Kalcheim,
2005). The other possibility is that external cells only
contribute to the production of the early collagenous stroma of the dermis.
Further long-term fate mapping studies will be necessary to clarify the exact
role of the trout external cells in forming the integument with the epidermis.
In zebrafish, lineage-tracking experiments led to the observation that some
anterior somitic cells migrate dorsally and ventrally to a position consistent
with a dermal layer (Hollway et al.,
2007) but the relationship between zebrafish external cells and
the dermis still remains unclear. Regarding Dermo-1 function, it has been
shown that it acts as a repressor for MyoD activation (Gong and Li, 2001) and,
as such, Dermo-1 might play a role in preventing the entry of somitic external
cells into the myogenic programme. Dermo-1 also inhibits myogenin
transactiviting activity through competition for E-proteins
(Li et al., 1995). It is
therefore possible that Dermo-1, which is transiently expressed in some
domains of the trout embryonic myotome, a feature not observed in amniotes
(Li et al., 1995;
Scaal et al., 2001),
participates in the regulation of the early myogenic differentiation in this
fish species. The mechanisms by which Dermo-1 may regulate differentiation of
dermal cells are unknown. However, its crucial role in dermis formation has
been demonstrated by analysis of Dermo-1 null mutants that show an
atrophic dermis (Sosic et al.,
2003). The observation that in vertebrate embryos Dermo-1
transcript most often co-localizes with that of collagen I
(Li et al., 1995;
Niederreither et al., 1992)
(this study) is suggestive of a role for Dermo-1 in regulating collagen I
transcription in the external cells.
In addition to Pax7 and Dermo-1, trout external cells express collectin
sub-family member 12 and Seraf. Collectins are collagenous calcium-dependent
defence lectins involved in innate immunity through binding to oligosaccharide
structures and/or lipid moieties on the surface of micro-organisms. Collectin
sub-family member 12, which is a transmembrane domain-containing lectin, has
been shown to be expressed in most human adult tissues and mainly in vascular
cells (Hogenkamp et al.,
2006). Its developmental expression pattern, however, has not been
reported until now. In this study we show that collectin sub-family member 12
is notably expressed in epidermis and branchial arches. The localisation of
collectin transcript in epidermis and branchial arches is in agreement with
the role of these tissues as a first line of defence against pathogens. The
precise function of collectin sub-family member 12 in developing
somite/myotome as well as in sclerotome cells remains enigmatic. Given that
the C-type lectin CRD motif, which is present in collectins, mediates a
diversity of functions in cell recognition, cell–cell adhesion and
embryonic development (Drickamer and
Taylor, 1993), it is possible that somitic expression of this
lectin contributes to myotome and sclerotome morphogenesis.
The dynamic expression of a Seraf gene in trout developing somites
was unexpected because Seraf gene transcription in chicken embryo is
restricted to a subpopulation of migrating neural crest cells committed to
form Schwann cell precursors (Wakamatsu et
al., 2004). It is possible, given the ancient whole-genome
duplication that occurred in the teleost fish lineage, subsequent to its
divergence from mammals (Jaillon et al.,
2004) and the recent additional genome duplication event specific
to salmonids, that multiple Seraf orthologues with distinct
expression patterns co-exist in the trout genome. The presence in trout
databases of several EST cDNAs highly related but distinct from our cDNA clone
is in line with this interpretation. The function of Seraf protein remains
largely unknown. In chicken, Seraf acts in an autocrine/paracrine fashion on
Schwann cell precursors and regulates their distribution in embryos
(Wakamatsu et al., 2004).
Since Seraf protein shows significant sequence homology with Wnt inhibitory
factor 1, it is possible that Seraf produced by external cells controls
morphogenetic gradients of Wnt signalling activity in regions subjacent to the
ectodermal epidermis. It is interesting to note that Seraf transcript also
accumulates in dorsal and ventral tips of the myotome where new myofibres form
during the stratified hyperplasia
(Rowlerson and Veggetti, 2001;
Steinbacher et al., 2007),
suggesting that this gene may play a role in regulating stratified growth of
the second phase of myogenesis in fish.
The expression of Dermo-1, collectin sub-family member 12 and Seraf within the external cell layer epithelium was preceded by a complex transcription pattern in the early somite, notably affecting the primary myogenin-positive myotome. This contrasts with the expression of Pax7, which mirrors the migration of external cell progenitors from the anterior to the external surface of the somite. The mechanisms that govern the dynamic expression of Dermo-1, collectin sub-family member 12 and Seraf in somitic cells remain to be determined.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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