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Germ-layer origin and morphogenesis of teeth of the Mexican axolotl.a, A sketch of the germ-layer origin of teeth in the Mexican axolotl. ECT teeth, green; END teeth, red; teeth of mixed origin, red–green (the colouring in the key is a qualitative guide to the ratio of the components in each tooth field). Cartilages visualized using alcian blue. b, Comparative developmental morphogenesis of the mouth region and the germ-layer origin of teeth of vertebrate (upper row) and an axolotl (lower row) embryo. In the majority of vertebrates, the mouth develops from a stomodeum with teeth distributed in invaginated ECT. In contrast, in urodeles the mouth develops from a stomodeal collar with an oral epithelium either of a dual origin, with teeth of ECT or END, or of a mixed origin. PQ, palatoquadrate; TR, trabecula cranii; n, nose; e, eye.
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The oral cavity of vertebrates is generally thought to arise as an ectodermal invagination. Consistent with this, oral teeth are proposed to arise exclusively from ectoderm, contributing to tooth enamel epithelium, and from neural crest derived mesenchyme, contributing to dentin and pulp. Yet in many vertebrate groups, teeth are not restricted only...
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Background
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Citations
... Key evidence for the 'inside-out' hypothesis included the claims that endoderm is required for tooth development [16,41,42], the interpretation of conodont elements as the first oropharyngeal denticles prior to the origin of jaws [16] and the discovery of patterned tooth whorls in thelodonts [19], suggesting the presence of a dental lamina [8]. All of these arguments have been refuted [11,18,38,40,43], undermining the 'inside-out' hypothesis. ...
Teeth are a key vertebrate innovation; their evolution is generally associated with the origin of jawed vertebrates. However, tooth-like structures already occur in jawless stem-gnathostomes; heterostracans bear denticles and morphologically distinct tubercles on their oral plates. We analysed the histology of the heterostracan denticles and plates to elucidate their morphogenesis and test their homology to the gnathostome oral skeleton. We identified a general model of growth for heterostracan oral plates that exhibit proximal episodic addition of tubercle rows. The distal hook exhibits truncated lamellae compatible with resorption, but we observe growth layers to be continuous between denticles. The denticles show no evidence of patterns of apposition or replacement indicating tooth homology. The oral plates and dermal skeleton share the same histological layers. The denticles grew in a manner comparable to the oral plate tubercles and the rest of the dermal skeleton. Our test of phylogenetic congruence reveals that the distribution of internal odontodes is discontinuous, indicating that the capacity to form internal odontodes evolved independently several times among stem-gnathostomes. Our results support the ‘outside-in’ hypothesis and the origin of teeth through the spread of odontogenic competence from extra-oral to oral epithelia and the subsequent co-option to a tooth function in gnathostomes.
... The germ layer origin of the epithelia involved (whether ectoderm or endoderm) has played a central role in elucidating the development and evolution of these organs, as well as in understanding their disorders. Yet germ layer boundaries have been notoriously difficult to identify, requiring most often transgenic reporter lines [5,[14][15][16][17]. This is especially the case for the oropharynx, where ectoderm and endoderm directly appose each other at multiple sites. ...
... Using lineage tracing with CDCFDA, we also examined the fate of the outer ectodermal layer (periderm equivalent) in axolotl. The oral area at stage 36 consists of a double-layered ectoderm, while the inner region of the prospective mouth is filled with a compact mass of endoderm [14,19]. The mouth opens at stage 43, when the oral membrane is perforated [14,19]. ...
... The oral area at stage 36 consists of a double-layered ectoderm, while the inner region of the prospective mouth is filled with a compact mass of endoderm [14,19]. The mouth opens at stage 43, when the oral membrane is perforated [14,19]. The first pouches contact the ectoderm already at stage 24 [41], but gill slits are wide open only at stage 43. ...
Background
Previous studies have reported that periderm (the outer ectodermal layer) in zebrafish partially expands into the mouth and pharyngeal pouches, but does not reach the medial endoderm, where the pharyngeal teeth develop. Instead, periderm-like cells, arising independently from the outer periderm, cover prospective tooth-forming epithelia and are crucial for tooth germ initiation. Here we test the hypothesis that restricted expansion of periderm is a teleost-specific character possibly related to the derived way of early embryonic development. To this end, we performed lineage tracing of the periderm in a non-teleost actinopterygian species possessing pharyngeal teeth, the sterlet sturgeon (Acipenser ruthenus), and a sarcopterygian species lacking pharyngeal teeth, the axolotl (Ambystoma mexicanum).
Results
In sturgeon, a stratified ectoderm is firmly established at the end of gastrulation, with minimally a basal ectodermal layer and a surface layer that can be homologized to a periderm. Periderm expands to a limited extent into the mouth and remains restricted to the distal parts of the pouches. It does not reach the medial pharyngeal endoderm, where pharyngeal teeth are located. Thus, periderm in sturgeon covers prospective odontogenic epithelium in the jaw region (oral teeth) but not in the pharyngeal region. In axolotl, like in sturgeon, periderm expansion in the oropharynx is restricted to the distal parts of the opening pouches. Oral teeth in axolotl develop long before mouth opening and possible expansion of the periderm into the mouth cavity.
Conclusions
Restricted periderm expansion into the oropharynx appears to be an ancestral feature for osteichthyans, as it is found in sturgeon, zebrafish and axolotl. Periderm behavior does not correlate with presence or absence of oral or pharyngeal teeth, whose induction may depend on ‘ectodermalized’ endoderm. It is proposed that periderm assists in lumenization of the pouches to create an open gill slit. Comparison of basal and advanced actinopterygians with sarcopterygians (axolotl) shows that different trajectories of embryonic development converge on similar dynamics of the periderm: a restricted expansion into the mouth and prospective gill slits.
... This then prompts the question of whether tooth-like structuresodontodes -were the first adornment of the vertebrate skin surface, and whether trunk or cranial neural crest offered the first instigation of a secretory odontoblast in the skin or mouth of early vertebrates. The fact that odontodes can be of mixed origin, i.e., an epithelial (endoderm or ectoderm; Soukup et al., 2008) cell contribution for the enamel/enameloid and an ectomesenchymal (neural crest-derived) contribution to produce dentine, potentially complicates the true origins of this innovation. Given what is known about the collaborative epithelial and ectomesenchymal development of teeth, and most other epithelial appendages, (Thesleff et al., 1995;Thesleff and Sharpe, 1997;Dassule and McMahon, 1998;Peters and Balling, 1999), it is unlikely that any odontode, past or present, formed without this collaborative initiation, regardless of final form, i.e., whether enamel-like tissues were present with dentine or not. ...
... The dentition is formed as a result of interaction between epithelial and mesenchymal layers. The participating epithelial layer may be ectodermal in origin as in the case of oral teeth of reptiles (Buchtová et al., 2008;Cobourne et al., 2004) or endodermal as in pharyngeal teeth in fishes and amphibians (Fraser et al., 2009;Soukup et al., 2008;Van der Heyden and Huysseune, 2000). ...
... The current difficulties in the study of non-canonical organ regeneration in salamanders are mainly due to: (1) The small number of researchers; (2) The lack of technical means for the study; and (3) The lack of background and resources for the study. Recent progress in embryo, tissue and cell transplantation [58,[64][65][66][67][68][69], virusmediated cell labeling [70,71], transgenic [72][73][74][75][76][77][78][79], tissue clearing [80][81][82][83] and live imaging [77,[83][84][85][86], gene editing [87][88][89][90], de novo sequencing [88,[91][92][93][94][95][96][97], singlecell [7,[98][99][100][101][102][103][104][105] and spatiotemporal [7,[103][104][105][106][107] multiomics technologies (Figure 2) have dramatically expanded knowledge about embryonic and tissue development, and the evolution of animal behavior and have advanced human understanding of the spatiotemporal dynamics of cells and genes at the genetic, transcriptional, and protein levels during the regeneration of canonical organs in salamanders, and their regulation of regeneration. Currently, models of pneumonectomy, hepatectomy, nephrectomy, and renal drug injury have been successfully constructed in salamanders, based on which we have discovered the regenerative potential of salamander alveolar epithelial cells, hepatocytes, and other cells and structures such as the alveoli, glomeruli, and renal tubules. ...
Salamanders possess remarkable regenerative capacities for organ regeneration among tetrapod vertebrates. Previous research has primarily focused on studying the regeneration of canonical tissues or organs such as limbs, tail, brain, spinal cord, heart, and lens. The advancements made in these areas have broader implications for understanding regeneration and developing therapeutic approaches for these organs, not only in salamanders but also in other vertebrates. In recent years, there has been an increasing interest in studying the regeneration of non‐canonical organs in salamanders, such as the liver, lungs, kidneys, and pancreas. This diversification of research has opened up new avenues and provided potential solutions to challenging clinical problems. This review aims to summarize the progress made in the field of non‐canonical organ regeneration in salamanders and provides an outlook on future research directions.
... The multi-cusped complex crown morphology of molars is formed by the shaping of a geometrically complex interface between epithelial and mesenchymal tissues in developing teeth ( Figure 1C). Tooth development proceeds through the interaction between the ectoderm-(or endoderm-) derived dental epithelium (Soukup et al., 2008(Soukup et al., , 2013 and the neural crest-derived dental mesenchyme (Chai et al., 2000), and its developmental stages are termed bud, cap, and bell stages depending on the shape of dental epithelium. At the bud stage, an epithelial cell population, known as primary enamel knot (EK), appears at the tip of the bud ( Figure 1C.1). ...
Phylogenetically, the tribosphenic molars—prototypes of multi-cusped cheek teeth in marsupial and placental mammals—are derived from the single-cusped conical teeth of reptiles through the addition of cusps. Ontogenetically, mammalian molars are formed through the interface between the dental epithelium and mesenchyme (future enamel–dentin junction), becoming geometrically complex by adding epithelial signaling centers, called enamel knots, which determine future cusp positions. To re-evaluate cusp homologies in Mesozoic mammals from an ontogenetic perspective, this study tracked molar development in a living placental mammal species, the house shrew (Suncus murinus), whose molars are morphologically the least derived from tribosphenic prototypes. The development of shrew molars proceeded as if it replayed the evolutionary process of tribosphenic molars. The first formed enamel knots gave rise to the evolutionarily oldest cusps—upper paracone and lower protoconid. The order of formation of other enamel knots and their location in development seemed to trace the order of cusp appearance in evolution. The parallel relationship between ontogeny and phylogeny of mammalian molars, if any, suggests that a change in the timing between developmental events rather than a change in the morphogenetic mechanism itself, should have been a major causal factor for the evolutionary transformation of tooth morphology.
... The LG comprises multiple epithelial structures located in the external upper portion of the conjunctiva of the eyelid [10]. Elongation and branching of multiple epithelial buds from this region of the eyelid conjunctiva contribute to LG formation [11]. ...
The vertebrate body comprises four distinct cell populations: cells derived from (1) ectoderm, (2) mesoderm, (3) endoderm, and (4) neural crest cells, often referred to as the fourth germ layer. Neural crest cells arise when the neural plate edges fuse to form a neural tube, which eventually develops into the brain and spinal cord. To date, the embryonic origin of exocrine glands located in the head and neck remains under debate. In this study, transgenic TRiCK mice were used to investigate the germinal origin of the salivary and lacrimal glands. TRiCK mice express fluorescent proteins under the regulatory control of Sox1, T/Brachyury, and Sox17 gene expressions. These genes are representative marker genes for neuroectoderm (Sox1), mesoderm (T), and endoderm (Sox17). Using this approach, the cellular lineages of the salivary and lacrimal glands were examined. We demonstrate that the salivary and lacrimal glands contain cells derived from all three germ layers. Notably, a subset of Sox1-driven fluorescent cells differentiated into epithelial cells, implying their neural crest origin. Also, these Sox1-driven fluorescent cells expressed high levels of stem cell markers. These cells were particularly pronounced in duct ligation and wound damage models, suggesting the involvement of neural crest-derived epithelial cells in regenerative processes following tissue injury. This study provides compelling evidence clarifying the germinal origin of exocrine glands and the contribution of neural crest-derived cells within the glandular epithelium to the regenerative response following tissue damage.
... incisors, canines, and molars, all of which come from separate parts of the oral epithelium (Smith, 2003 ;Soukup et al., 2008). ...
Introduction: Critical bone defect is osseous damage that would not able
to self-heals following accident, infection, tumor that still challenging
faced the specialist. Chitosan is a natural polysaccharide, regard as
osteoconductive materials to enhance ossification process. Beta-tricalcium
phosphate (β -TCP) is a synthetic bone substitute with micro- pores system
for the improvement of osteogenesis. The study aims to assessment the
osteogenic effect of chitosan hydrogel, beta tricalcium phosphate and their
combination on bone healing in rabbits by histological and
histomorphometrical analysis and evaluation the local expression of
transforming growth factor beta three (TGFβ3) by immunohistochemical
investigation.
Materials and methods: A total of 32 New Zealand rabbits aged about 6-8
months and weighted about 1.5-2.5 kg were used in this experimental
study. Intra bony defect of about 2 mm in diameter and 3 mm in depth were
created in the distal side of both right and left femurs bones for each rabbit.
These bony defects were divided into four groups:
1-Control group:(16 bony defect) each defect left to heal spontaneously.
2-Chitosan hydrogel group :(16 bony defect) each defect were treated with
0.5 ml of chitosan hydrogel.
3- β-TCP group :(16 bony defect) each defect were treated with 0.5 mg of
beta-tricalcium phosphate granules.
4- Combination group: (16 bony defect) each defects were treated with
(0.25 ml) of Chitosan and (0.25 mg) of β-TCP.ABSTRACT
IV
All 32 rabbits were sacrificed at 2 and 4 weeks healing intervals (16
rabbits for each) postoperatively.
Histological examination was performed under light microscope for all
bone section stained with Hematoxylin and Eosin with assessment of
histomorphometric analysis by using software image j for counting of bone
cells. Also Immunohistochemical detection of TGF-β3 by using
monoclonal antibody against TGF-β3.
Results: Histological evaluation of experimental and control groups after
2 and 4 weeks healing periods illustrated that chitosan hydrogel and
combination groups improved higher osteogenic capacity and early sign of
mineralization than Beta-tricalcium phosphate (β -TCP) and control
groups.
Histomorphometric analysis for almost all bone parameters used in
present study showed variant significant difference in all studied groups in
both healing durations. Immunohsitochemical result revealed strong
positive expression in osteoblasts, osteocytes and mesenchymal stromal
cells especially in chitosan hydrogel and combination groups after two
weeks healing interval.
Conclusion: The present study illustrated that the local application of
chitosan hydrogel and its combination with beta tricalcium phosphate in
intra bony defects may accelerate bone matrix formation and enhance
maturation and increased the expression TGF-β3 when compared with
others.
... incisors, canines, and molars, all of which come from separate parts of the oral epithelium (Smith, 2003 ;Soukup et al., 2008). ...
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... With the introduction of transgenic axolotls expressing ubiquitously a green fluorescent protein (GFP) [12], new possibilities opened. Grafting, in combination with transgenesis, proved at once very useful to reveal migratory patterns and the embryonic origin of tissues or structures [13][14][15]. ...
Embryo grafts have been an experimental pillar in developmental biology, and particularly, in amphibian biology. Grafts have been essential in constructing fate maps of different cell populations and migratory patterns. Likewise, autografts and allografts in older larvae or adult salamanders have been widely used to disentangle mechanisms of regeneration. The combination of transgenesis and grafting has widened even more the application of this technique.In this chapter, we provide a detailed protocol for embryo transplants in the axolotl (Ambystoma mexicanum
). The location and stages to label connective tissue, muscle, or blood vessels in the limb and blood cells in the whole animal. However, the potential of embryo transplants is enormous and impossible to cover in one chapter. Furthermore, we provide a protocol for blastema transplantation as an example of allograft in older larvae.Key wordsAxolotl EmbryosLateral Plate MesodermPresomitic MesodermConnective TissueBlood VesselsMuscleBlood Cells
