Integrative and Comparative Biology Advance Access originally published online on June 1, 2007
Integrative and Comparative Biology 2007 47(3):401-408; doi:10.1093/icb/icm020
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The contribution of neural crest cells to the nuchal bone and plastron of the turtle shell
*Department of Biology, Swarthmore College, 500 College Avenue, Swarthmore, PA 19081 USA; Swarthmore College, presently at Department of Chemistry, University of Wisconsin, Madison, WI 53706; Science Division, Friends Central School, 1101 City Avenue, Wynnewood, PA 19096 USA; Biology Department, Millersville University, PO Box 1002, Millersville, PA 17551 USA
Correspondence: 1E-mail: sgilber1{at}swarthmore.edu
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The origin of the turtle plastron is not well understood, and these nine bones have been homologized to the exoskeletal components of the clavicles, the interclavicular bone, and gastralia. Earlier data from our laboratory showed that the plastral bone-forming cells stained positively for HNK-1 and PDGFR
, two markers of skeletogenic neural crest cells. We have now shown that the HNK-1+ cells are also positive for p75 and FoxD3, affirming their neural crest identity. These cells originate from the dorsal neural tube of stage-17 turtle embryos, several days after the original wave of neural crest cells have migrated and differentiated. Moreover, we have demonstrated the existence of a staging area, above the neural tube and vertebrae, where these late-emigrating neural crest cells collect. After residing in the carapacial staging area, these cells migrate to form the plastral bones. We also demonstrate that one bone of the carapace, the nuchal bone, also stains with HNK-1 and with antibodies to PDGFR. The nuchal bone shares several other properties with the plastral bones, suggesting that it, too, is derived from neural crest cells. Alligator gastralia stain for HNK-1, while their ribs do not, thus suggesting that the gastralial precursor may also be derived from neural crest cells. |
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The turtle shell is a remarkable evolutionary novelty specific to the order Chelonia. While some turtles have a leatherback or a soft-shell, these species appear to have been derived from hard-shelled turtles. This article will report on the bony component of those hard shell species of the genera Emys and Chelydra. This shell is composed of two main parts, the dorsal carapace and the ventral plastron, connected along the midflanks by lateral bridges. Altogether, the shell contains over 50 dermal bones found in no other vertebrate order, and the presence of this bony casing has necessitated extensive modifications of the tetrapod body plan (Zangerl 1969
). While dermal ossification itself is a primitive character for vertebrates (Smith and Hall 1993), the turtle shell represents an extreme development of the dermal skeleton among tetrapods.
The evolutionary and developmental origins of turtle shell bones are extremely controversial (Pennisi 2004). We have proposed (Cebra-Thomas et al. 2005) that the carapace originates in a two-step manner, including an fibroblast growth factor (FGF)-dependent stage and a bone morphogenetic proteins (BMP)-dependent stage. First, FGFs synthesized in the carapacial ridge attract rib-precursor cells into the dermis and coordinate the expansion of the dorsal dermis and ribs. Second, BMPs secreted by the rib as it undergoes endochondral ossification induce the dermis to ossify. This forms the major portion of the carapacial plate.
We have also proposed that the nine plastral bones form from the trunk neural crest. Clark et al. (2001) demonstrated that each of the plastral bones from 50d turtle embryos (near the time of hatching) was formed by intramembranous ossification and stained positively with the HNK-1 antibody and with antibodies directed against PDGFR. These are two markers of skeletogenic neural crest. More recently, Cebra-Thomas et al. (2007) examined earlier-stage Trachemys embryos and demonstrated the existence of a population of late-forming cells arising from the dorsal roof of the neural tube and which stained positively for HNK-1, FoxD3, and p75. While neither HNK-1 nor PDGFR are completely specific for neural crest cells and their derivatives, the combination of HNK-1, p75 and FoxD3 is. HNK-1 is a widely used marker for neural crest cells, although this antibody detects not only cells of the neural crest lineage, but also stains cerebellar neurons, motor neurons, and certain leucocytes (Tucker et al. 1984; Erickson et al. 1989; Chou et al. 2002). PDGFR is detected not only on skeletogenic neural crest cells, but also on rib precursors and in the embryonic mesenchymal cells contributing to bone, hair, mammary gland, gut, and lung (Orr-Urtreger and Lonai 1992; Betsholtz et al. 2001; Hoch and Soriano 2003). FoxD3 is found predominantly in neural crest cells, although it is also seen in mammalian embryonic stem cells (Steiner et al. 2006); and although p75 has been observed on myoblasts and hippocampal neurons (Erck et al. 1998; Salama-Cohen et al. 2006) it is often used as a marker for neural crest cells and their derivatives (Rao and Anderson 1997; Young et al. 1998; Abzhanov et al. 2003). The evidence strongly suggests that there is a population of neural crest cells (positive for HNK-1, FoxD3, p75) that emerges late from the turtle neural tube and which forms the plastral bones of the turtle (Cebra-Thomas et al. 2007)
In this article, we extend the evidence that the plastron forms from trunk neural crest cells by showing that the alligator gastralia (thought to be evolutionary homologues of the paired plastral bones) also stain positively for HNK-1, and we provide evidence that the most anterior bone of the carapace, the nuchal bone, is also made from neural crest cells.
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Materials and methods |
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Embryonated Trachemys scripta eggs at various days’ incubation were purchased from the Kliebert Turtle and Alligator Farm (Hammond, LA, USA). The eggs were rinsed in water and 70% ethanol. Embryos were isolated by dissection, staged according to Greenbaum (2002
), fixed overnight with cold 4% paraformaldehyde (Sigma) in PBS, washed, and embedded in Paraplast+ paraffin wax. Transverse sections of 8 µm were cut with a Hacker–Bright rotary microtome and adhered to SuperFrost+ slides (Fisher). Multiple (3–5) embryos were examined at each stage.
The primary antibodies used for immunohistochemistry were HNK-1 (purified anti-CD57, Pharminogen, San Diego, CA, USA), anti-p75 low-affinity neurotrophin receptor (Chemicon, Temecula, CA, USA), anti-FoxD3 (a gift from Dr P. Labosky, Vanderbilt University) and C5 (anti-melanoblast lineage; a gift from Dr D. Fisher, Dana-Farber Cancer Institute). For antibody staining, paraffin sections were dewaxed and rehydrated. Endogenous peroxidase activity was blocked using H2O2. For anti-FoxD3 only, the antigens were unmasked by treating the sections for 30 min at 95°C with Unmasking Solution (Zymed, San Francisco, CA, USA). The blocking solution, peroxidase-conjugated secondary antibodies, streptavidin-HRP and peroxidase substrate DAB (Zymed Histostain kit) were used in a protocol adapted from Rice et al. (2000). Slides used as negative controls were incubated without the primary antibodies. The slides were counterstained with Meyer's hematoxylin (Sigma) and mounted with glycerol polyvinyl alcohol (Zymed).
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Contributions of neural crest cells to the bones of the plastron |
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The plastron is generally composed of nine bones, each formed by intramembranous ossification (Rathke 1898
; Zangerl 1969; Gilbert et al. 2001). The paired epiplastra and the central entoplastron form the three anterior bones of the plastron. Posterior to these, the paired hyoplastra form the axillary buttresses and the anterior portion of the bridge. The hypoplastra form the inguinal buttress and the posterior bridge region. The hyoplastron and the hypoplastron form the anterior and posterior rims, respectively, of the central umbilical fontanel. This fontanel surrounds the yolk stalk that connects to the gut. The paired xiphiplastra bones form the posterior lobe of the plastron. The plastron begins to ossify before the time of hatching, but fusion of these bones into the plastral plate does not occur until later. In Trachemys (the red-eared slider turtle) and Chelydra (the snapping turtle), the three ossification centers corresponding to the three anterior plastral bones fuse first, around the time of hatching. The more posterior plastral bones fuse later, forming sutures that will allow growth (Gilbert et al. 2001; Clark et al. 2001). As the plastral bones form, condensed mesenchyme is seen in advance of the calcified (alizarin-stained) tissue, and these bones form in a two-step process involving the formation of a primary ossification site, followed by the secondary expansion of that center (Burke. 1989a; Gilbert et al. 2001). We had previously demonstrated that the plastral bones of hatchling turtles are formed by intramembranous ossification and that they express HNK-1 and PDGFR, two markers of skeletogenic neural crest cells (NCCs: Clark et al. 2001; Fig. 1H,I) When we stained earlier embryos to look for the precursors of the plastral bones (Cebra-Thomas et al. 2007), we have found a thick band of HNK-1+ cells in the carapacial dermis that appears to be a "staging area" for these cells (Fig. 1A,B). These HNK-1+ cells could be seen migrating ventrally through the embryo and aggregating in the ventral region to form bone (Fig. 1C–E). These cells did not stain with C5, a pan-specific antibody that detects the melanocyte lineage (Nishimura et al. 2005; Cebra-Thomas et al. 2007).
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HNK-1 is the "standard" marker for avian neural-crest cells (Tucker et al. 1984
; Rickman et al. 1985; Bronner-Fraser 1986; Erickson et al. 1989), and Hou (1999) and Hou and Takeuchi (1994) showed that turtle neural crest cells stained positively and strongly for HNK-1. However, although HNK-1 staining is commonly employed to identify neural crest cells, this epitope is also expressed on other cells, including a subset of neurons and leucocytes (Tucker et al. 1984; Erickson et al. 1989; Chou et al. 2002). Similarly, PDGFR is detected not only on skeletogenic neural crest cells, but also on rib precursors and in the embryonic mesenchyme cells contributing to bone, hair, mammary gland, gut, and lung (Orr-Urtreger and Lonai 1992; Betsholtz et al. 2001; Hoch and Soriano 2003). To confirm that the dispersed HNK-1+ cells in the carapacial dermis are neural crest cells, we examined the expression of FoxD3, a transcription factor necessary for specifying neural crest cells and regulating their cell-adhesion proteins (Labosky and Kaestner 1998; Kos et al. 2001; Cheung et al. 2005; Barembaum and Bronner-Fraser 2005; Tompers et al. 2005). Avian and murine FoxD3 are expressed in both migrating NCC and premigratory NCC in the neural tube (Labosky and Kaestner 1998; Kos et al. 2001). Its expression is virtually restricted to NCCs and their precursors, although it has also been shown to be necessary for the formation of the trophoblast lineage (Tompers et al. 2005). When we stained stage-17 T. scripta embryos with an antibody directed against FoxD3, we observed nuclear FoxD3+ cells in the neural tube (Fig. 1F), especially along the most dorsal cells, and in the dorsal carapacial dermis (Cebra-Thomas et al. 2007). The distribution of these FoxD3+ cells agrees with that of the HNK-1+ cells. Moreover, FoxD3 is not expressed in chick neural crest cells of the melanoblast lineage and is thought to repress melanoblast fate (Kos et al. 2001). This further argues against the cells of the carapacial staging area being melanocyte precursors.
Staining of dispersed cells within the dorsal dermis was also observed with an antibody against another marker for neural crest cells, the low affinity neurotrophin receptor p75 (Rao and Anderson 1997; Abzhanov et al. 2003; Takaki et al. 2006). We have detected p75+ and HNK-1+ condensations in the plastral mesenchyme and have seen these cells surrounding bone matrix (Fig. 1G). Therefore, these dorsal FoxD3+, p75+, HNK-1+ cells appear to represent a late-emerging population of trunk neural crest cells that are not found in chicks and mice and which migrate ventrally to form the plastral bones.
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Contributions of the neural crest to the nuchal bone of the carapace |
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SynopsisIntroductionMaterials and methodsContributions of neural crest...Contributions of the neural...HNK-1 staining in the...DiscussionAcknowledgmentsReferences |
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Most of the carapacial bones do not stain positively for HNK-1 or other neural crest markers. We find, however, that one bone of the carapace does stain positively for both HNK-1 and PDGFR
. This is the nuchal bone, the most anterior bone of the carapace. The nuchal bone has been described as forming differently from the other bones of the carapace (Gilbert et al. 2001). The nuchal bones of Chelydra and Trachemys form in two stages, each with an ossification center that expands outward by spicules, just like the plastral bones. These phases are referred to as primary and secondary, referring to both the modes of ossification and the elements themselves (Burke. 1989b).
The primary portion of the nuchal bone forms early (about stage 20–21), appearing as a thin band of condensed cells within the dermis, continuous across the midline and extending laterally around the margin to the level of the third marginal. The band is visible deep within the dermis before the actual deposition of calcium, and it underlies the marginal/vertebral sulci. Calcium deposition, as evidenced by positive staining with alizarin, starts bilaterally at the level of the first marginal scute and spreads along the bars medially and laterally. The second phase of nuchal ossification involves the nuchal plate. The nuchal plate forms as a loose lattice work of bone, much like the pattern seen in the initial stages of ossification in the skull-roofing bones. It begins in contact with the anterior-medial nuchal bar and extends laterally along the bar and posteriorly into the dermis above the neural spines of the last two cervical vertebrae. This posterior extension of secondary dermal bone forms the main body of the nuchal scute and lies under the first vertebral scute. It will eventually form a suture with the first neural bone, which develops around the neural spine of the first thoracic vertebra (Burke. 1989b; Gilbert et al. 2001).
Thus, the nuchal bone forms in a manner very much like that of the plastral bones (and like the bones of the head derived from the neural crest). Staining with HNK-1 and antibodies to PDGFRF strongly suggests that it has the same origin, namely, the neural crest. No other bone of the carapace stains with either of these two antibodies. This can be seen in a comparison of the development of the nuchal bone to that of the peripheral bones forming at the same time. Figure 2A–C shows that the nuchal bone of a 118d turtle hatchling stains positively with HNK-1 and with antibodies to PDGFR. The peripheral bone does not stain.
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HNK-1 staining in the alligator gastralia |
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The three anterior bones of the plastron are believed to be homologous to the clavicles and intraclavicular bones of other reptilian lineages (Parker 1868; Zangerl 1969
; Rieppel 1996; Vickaryous and Hall 2006), while the three posterior sets of paired plastral bones are thought to be homologous to the gastralia (the "floating ribs" or "abdominal ribs") of other tetrapods (De Vos 1938; Zangerl 1939; Liem et al. 2001; Claessens 2004). Gastralia constitute free-floating bones, often segmented, in the ventral abdomens of extant crocodilians and Sphenodon (Fig. 2D,E) Large and complex gastralia, however, were prevalent in marine reptiles such as plesiosaurs, where they became plastron-like baskets that probably transmitted the propulsive force of the limbs to the body (Robinson 1977). Like the plastron, the gastralia are thought to be dermal exoskeleton (Knox 1869; Claessens 2004). Even though gastralia are found in very few extant vertebrates, they are thought to be plesiomorphic for the entire vertebrate clade (Baur 1889; Romer 1956) and are seen in the primitive sarcopterygian fishes. Claessens (2004) summarized: "Gastralia may be plesiomorphic for tetrapods, but are only retained in extant Crocodylia and Sphenodon, and possibly as part of the chelonian plastron." If the turtle plastron arose from reptilian gastralia, then we might expect to see NCC involvement in forming the alligator gastralia. We have data that these bones, too, contain HNK-1+ cells (Fig. 2F,G). These potential gastralial primordia, but not the larger rib cartilage, were surrounded by HNK-1+ cells. Our preliminary evidence, however, also suggests that the description of the development of the gastralia by Voeltzkow and Döderlein (1901) is erroneous. Gastralia appear to be neither intramembranous bone, nor are they dermal. Rather, we find them to be cartilaginous condensations in the muscular region of the ventrum. This does not rule out their being formed from neural crest cells of the trunk, and it is possible that both turtles (with their plastra) and alligators (with their gastralia) have a "staging area" for NCCs. We will be searching younger specimens for such an area. |
Discussion |
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SynopsisIntroductionMaterials and methodsContributions of neural crest...Contributions of the neural...HNK-1 staining in the...DiscussionAcknowledgmentsReferences |
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Although we have not yet been able to follow individual cells from the neural tube to the developing bones, immunohistochemical evidence supports our hypothesis that the entire plastron and the nuchal bone of the carapace are derived from neural crest cells. Moreover, these cells appear to be derived from the trunk neural crest. Trunk neural crest cells are not considered to be able to form bone, and such skeletogenic capabilities are usually seen as being reserved for the cranial neural crest. In most vertebrates studied, cell labeling studies have demonstrated that the cranial and facial dermal bones of the vertebrate exoskeleton (as well as the dentine of the teeth) come from the cranial region of the neural crest, while the trunk neural crest is unable to form bone (Patterson 1977
; Noden 1991; Couly et al. 1992, 1993; Smith and Hall 1990, 1993).
In contrast, Smith and Hall (1993) have noted that many groups of fossil fishes (especially the placoderms) have extensive exoskeletons and that certain extant fish have postcranial dermal denticles or medial ray fins whose structures can best be explained by formation from the trunk neural crest. Transplantation experiments (Smith et al. 1994) and cell marker analysis (Freitas et al. 2006) have suggested that the cells producing the dermal rays of the zebra fish caudal fin are derived, at least in part, from trunk neural crest.
The neural crest of the trunk can gain skeletogenic abilities after being kept in culture for two weeks (McGonnell and Graham 2002; Abzhanov et al. 2003). We believe that in producing a late population of neural crest cells, the turtle embryo may be reproducing such conditions, allowing the cells to become skeletogenic. Abzhanov and colleagues (2003) have correlated the skeletogenic capacity of neural crest cells with the lack of (or downregulation of) Hox gene expression. It is possible that in waiting such a long time to produce these neural crest cells or in having them wait in a staging area for a prolonged time, the turtle embryo produce a population of neural crest cells that arise after the period of Hox-gene expression in the neural tube begins. If so, the turtle embryo will have made a virtue of its slowness.
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Acknowledgments |
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The authors wish to thank K. McDow and C. Plafkin for their help on some of the experiments mentioned herein. They also wish to thank Dr J. Fallon and Dr M. Harris for the excellently preserved alligator embryos, and they thank laboratory manager G. Rivnak for her competence and patience. Funding was provided from Swarthmore College, the National Science Foundation (IBN-0316025) and the Howard Hughes Medical Institute. Conflict of interest: None declared.
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Footnotes |
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From the symposium "Linking Genes and Morphology in Vertebrates" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
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