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Anthony Graham

Publications and source records attributed to Anthony Graham.

At least 19 recordsLinked to original sources

Developmental and evolutionary origins of the vertebrate dentition: molecular controls for spatio-temporal organisation of tooth sites in osteichthyans.

The rainbow trout (Oncorhynchus mykiss) as a developmental model surpasses both zebrafish and mouse for a more widespread distribution of teeth in the oro-pharynx as the basis for general vertebrate odontogenesis, one in which replacement is an essential requirement. Studies on the rainbow trout have led to the identification of the initial sequential appearance of teeth, through differential gene expression as a changing spatio-temporal pattern, to set in place the primary teeth of the first generation, and also to regulate the continuous production of replacement tooth families. Here we reveal gene expression data that address both the field and clone theories for patterning a polyphyodont osteichthyan dentition. These data inform how the initial pattern may be established through up-regulation at tooth loci from a broad odontogenic band. It appears that control and regulation of replacement pattern resides in the already primed dental epithelium at the sides of the predecessor tooth. A case is presented for the developmental changes that might have occurred during vertebrate evolution, for the origin of a separate successional dental lamina, by comparison with an osteichthyan tetrapod dentition (Ambystoma mexicanum). The evolutionary origins of such a permanent dental lamina are proposed to have occurred from the transient one demonstrated here in the trout. This has implications for phylogenies based on the homology of teeth as only those developed from a dental lamina. Utilising the data generated from the rainbow trout model, we propose this as a standard for comparative development and evolutionary theories of the vertebrate dentition.

Ambystoma↗

Vertebrate neurogenin evolution: long-term maintenance of redundant duplicates.

The majority of the cranial sensory neurons of vertebrates, including all of those concerned with the special senses of hearing, balance and taste, are derived from the neurogenic placodes. A number of studies have shown that the production of neuronal cells by the placodes is dependent upon the function of the neurogenin (ngn) gene family of basic helix-loop-helix transcription factors. One member of the gene family is expressed in each placode, suggesting that this specificity of expression could help to determine different neuronal classes. An interesting feature of this expression, however, is that the expression patterns vary amongst the vertebrates; for example, mammals and fish express ngn-1 in the ophthalmic trigeminal placode where birds use ngn-2. This prompted us to use phylogenetic and genomic analysis to unravel the evolutionary history of this gene family. We determined that the duplication that created the neurogenin-1 and -2 subfamilies occurred deep in the vertebrate lineage before the divergence of bony fish 450 million years ago and suggest that concurrent expression of both genes was probably maintained in all neurogenic placodes until after the divergence of birds and mammals 270 million years ago.

Animals↗

Vertebrate evolution: turning heads.

The skeleton of the neck and shoulders has undergone alterations during evolution, but muscle connectivity has not. A recent study suggests this is a result of neural crest cells defining attachment points and thus muscle connectivity.

Animals↗

Molecular evidence from Ciona intestinalis for the evolutionary origin of vertebrate sensory placodes.

Cranial sensory placodes are focused areas of the head ectoderm of vertebrates that contribute to the development of the cranial sense organs and their associated ganglia. Placodes have long been considered a key character of vertebrates, and their evolution is proposed to have been essential for the evolution of an active predatory lifestyle by early vertebrates. Despite their importance for understanding vertebrate origins, the evolutionary origin of placodes has remained obscure. Here, we use a panel of molecular markers from the Six, Eya, Pax, Dach, FoxI, COE and POUIV gene families to examine the tunicate Ciona intestinalis for evidence of structures homologous to vertebrate placodes. Our results identify two domains of Ciona ectoderm that are marked by the genetic cascade that regulates vertebrate placode formation. The first is just anterior to the brain, and we suggest this territory is equivalent to the olfactory/adenohypophyseal placodes of vertebrates. The second is a bilateral domain adjacent to the posterior brain and includes cells fated to form the atrium and atrial siphon of adult Ciona. We show this bares most similarity to placodes fated to form the vertebrate acoustico-lateralis system. We interpret these data as support for the hypothesis that sensory placodes did not arise de novo in vertebrates, but evolved from pre-existing specialised areas of ectoderm that contributed to sensory organs in the common ancestor of vertebrates and tunicates.

Animals↗

The role of the endoderm in the development and evolution of the pharyngeal arches.

The oro-pharyngeal apparatus has its origin in a series of bulges found on the lateral surface of the embryonic head, the pharyngeal arches. Significantly, the development of these structures is extremely complex, involving interactions between a number of disparate embryonic cell types: ectoderm, endoderm, mesoderm and neural crest, each of which generates particular components of the arches, and whose development must be co-ordinated to generate the functional adult oro-pharyngeal apparatus. In the past most studies have emphasized the role played by the neural crest, which generates the skeletal elements of the arches, in directing pharyngeal arch development. However, it is now apparent that the pharyngeal endoderm plays an important role in directing arch development. Here we discuss the role of the pharyngeal endoderm in organizing the development of the pharyngeal arches, and the mechanisms that act to pattern the endoderm itself and those which direct its morphogenesis. Finally, we discuss the importance of modification to the pharyngeal endoderm during vertebrate evolution. In particular, we focus on the emergence of the parathyroid gland, which we have recently shown to be the result of the internalization of the gills.

Animals↗

The origin of the parathyroid gland.

It has long been held that the parathyroid glands and parathyroid hormone evolved with the emergence of the tetrapods, reflecting a need for new controls on calcium homeostasis in terrestrial, rather than aquatic, environments. Developmentally, the parathyroid gland is derived from the pharyngeal pouch endoderm, and studies in mice have shown that its formation is under the control of a key regulatory gene, Gcm-2. We have used a phylogenetic analysis of Gcm-2 to probe the evolutionary origins of the parathyroid gland. We show that in chicks, as in mice, Gcm-2 is expressed in the pharyngeal pouches and the forming parathyroid gland. We find that Gcm-2 is present not only in tetrapods but also in teleosts and chondrichthyans, and that in these species, Gcm-2 is expressed within the pharyngeal pouches and internal gill buds that derive from them in zebrafish (Danio rerio), a teleost, and dogfish (Scyliorhinus canicula), a chondrichthyan. We further demonstrate that Gcm-2 is required for the formation of the internal gill buds in zebrafish. We also have identified parathyroid hormone 1/2-encoding genes in fish and show that these genes are expressed by the gills. We further show that the gills express the calcium-sensing receptor, which is used in tetrapods to monitor serum calcium levels. These results indicate that the tetrapod parathyroid gland and the gills of fish are evolutionarily related structures, and that the parathyroid likely came into being as a result of the transformation of the gills during tetrapod evolution.

Amino Acid Sequence↗

Evolution and development: rise of the little squirts.

It used to be thought that only vertebrates possess neural crest cells, but a recent study has demonstrated the existence of neural crest-like cells in an ascidian urochordate. This alters our views on the evolution of the neural crest and of the vertebrates.

Animals↗

Conserved deployment of genes during odontogenesis across osteichthyans.

Odontogenesis has only been closely scrutinized at the molecular level in the mouse, an animal with an extremely restricted dentition of only two types and one set. However, within osteichthyans many species display complex and extensive dentitions, which questions the extent to which information from the mouse is applicable to all osteichthyans. We present novel comparative molecular and morphological data in the rainbow trout (Oncorhynchus mykiss) that show that three genes, essential for murine odontogenesis, follow identical spatial-temporal expression. Thus, at all tooth bud sites, epithelial genes Pitx-2 and Shh initiate the odontogenic cascade, resulting in dental mesenchymal Bmp-4 expression, importantly, including the previously unknown formation of replacement teeth. Significantly, this spatial-temporal sequence is the same for marginal and lingual dentitions, but we find notable differences regarding the deployment of Pitx-2 in the developing pharyngeal dentition. This difference may be highly significant in relation to the theory that dentitions may have evolved from pharyngeal tooth sets in jawless fishes. We have provided the first data on operational genes in tooth development to show that the same signalling genes choreograph this evolutionary stable event in fishes since the osteichthyan divergence 420 Myr ago, with the identical spatial-temporal expression as in mammals.

Animals↗

Redefining the head-trunk interface for the neural crest.

The head-trunk interface lies at the occipito-cervical boundary, which corresponds to the somite 5/6 level. Previous studies have demonstrated that neural crest cells also behave differently either side of this boundary and that this may be due to intrinsic differences between cranial and trunk crest. However, it is also possible that some of the observed differences between cranial and trunk crest are assigned by environmental cues. We have therefore scrutinised the behaviour of the neural crest cells generated either side of the occipito-cervical boundary in chick and, interestingly, find that both behave in a truncal fashion by traversing the anterior half of their adjacent somites. Furthermore, although not previously described, we find that transient DRGs form opposite somites 4 and 5. Crest cells produced anterior of the somite 3/4 boundary avoid the somites and behave in a non-truncal fashion; these cells populate the pharyngeal arches, and thus contribute to the developing head. We have further shown, via somite transplantations, that differential behaviour of the posterior versus anterior occipital crest is assigned by the somites. If somites 1 to 3 are replaced by trunk somites, then the anterior occipital crest will behave in a truncal fashion by invading the somites. Correspondingly, if these anterior occipital somites are transplanted in place of trunk somites, they perturb the migration of trunk crest. Thus, for the neural crest, the head-trunk interface does not lie at the occipito-cervical boundary, but rather lies at the somite 3/4 level and is defined by the somites. The fact that this boundary lies at the somite 3/4 level in chick is significant as it reflects the more ancient posterior occipital boundary; in fish, only the first three somites contribute to the occipital bone.

Animals↗

The role of actin cables in directing the morphogenesis of the pharyngeal pouches.

The pharyngeal arches are separated by endodermal outpocketings, the pharyngeal pouches. These are structures of considerable importance; they are required to segregate the mesenchymal populations of each arch and to induce the formation of arch components, and they generate specific derivatives, including the parathyroid and the thymus. The pharyngeal pouches are first evident as localised sites at which the endoderm contacts the ectoderm, and they then expand along the proximodistal axis to generate the narrow, tight morphology of the mature pouch. We currently have no knowledge of the morphogenetic mechanisms that direct formation of the pharyngeal pouches. Here, in chick, we show that cells within the pharyngeal pouch endoderm have an abundance of apically located actin fibres that are networked within the endodermal sheet, via their insertion into N-cadherin adherens junctions, to form a web of supra-cellular actin cables. Cytochalasin D disruption of these actin structures results in the formation of aberrant pouches that fail to generate their normal slit-like morphology. This suggests that the process of pharyngeal pouch morphogenesis involves the constraining influence of these actin cables that direct expansion, within the pouch, along the proximodistal axis. These results, importantly, provide us with vital insights into how the pharyngeal pouches form their normal morphology. They also give evidence, for the first time, of actin cables functioning as constraints during complex vertebrate morphogenetic episodes.

Actins↗

Significance of the cranial neural crest.

The cranial neural crest has long been viewed as being of particular significance. First, it has been held that the cranial neural crest has a morphogenetic role, acting to coordinate the development of the pharyngeal arches. By contrast, the trunk crest seems to play a more subservient role in terms of embryonic patterning. Second, the cranial crest not only generates neurons, glia, and melanocytes, but additionally forms skeletal derivatives (bones, cartilage, and teeth, as well as smooth muscle and connective tissue), and this potential was thought to be a unique feature of the cranial crest. Recently, however, several studies have suggested that the cranial neural crest may not be so influential in terms of patterning, nor so exceptional in the derivatives that it makes. It is now becoming clear that the morphogenesis of the pharyngeal arches is largely driven by the pharyngeal endoderm. Furthermore, it is now apparent that trunk neural crest cells have skeletal potential. However, it has now been demonstrated that a key role for the cranial neural crest streams is to organise the innervation of the hindbrain by the cranial sensory ganglia. Thus, in the past few years, our views of the significance of the cranial neural crest for head development have been altered. Developmental Dynamics 229:5-13, 2004.

Animals↗

Cannabinoid receptor, CB1, expression follows neuronal differentiation in the early chick embryo.

The role of the CB1 cannabinoid receptor and endocannabinoid signalling has been widely studied in the adult nervous system. However, an emerging body of evidence suggests that the CB1 receptor may also play a role during development. Here we have scrutinized the expression profile of the CB1 receptor from the onset of neurogenesis in the chick embryo. We find that this gene exhibits a dynamic expression pattern that spatially and temporally follows neuronal differentiation in the early embryo.

Animals↗

Development of the pharyngeal arches.

The oro-pharyngeal apparatus has its origin in a series of bulges that is found on the lateral surface of the embryonic head, the pharyngeal arches. The development of the pharyngeal arches is complex involving a number of disparate embryonic cell types: ectoderm, endoderm, neural crest and mesoderm, whose development must be co-ordinated to generate the functional adult apparatus. In the past, most studies have emphasised the role played by the neural crest, which generates the skeletal elements of the arches, in directing pharyngeal arch development, but it has also become apparent that the other tissues of the arches, most notably the endoderm, also plays a prominent role in directing arch development. Thus pharyngeal arch development is more complex, and more consensual, than was previously believed.

Animals↗

Jaw development: chinless wonders.

It has been suggested that the regionally restricted expression of Dlx genes acts to pattern the proximodistal axis of the pharyngeal arches during vertebrate development. Recently, clear evidence of this has emerged from Dlx-5; Dlx-6 double mutants, in which the lower jaw is transformed to an upper jaw.

Animals↗

Trunk neural crest has skeletogenic potential.

During early vertebrate development, neural crest cells emerge from the dorsal neural tube, migrate into the periphery, and form a wide range of derivatives. There is, however, a significant difference between the cranial and trunk neural crest with respect to the diversity of cell types that each normally produces. Thus, while crest cells from all axial levels form neurons, glia, and melanocytes, the cranial crest additionally generates skeletal derivatives such as bone and cartilage; trunk crest cells are generally thought to lack skeletogenic potential. Here, we show, however, that if avian trunk neural crest cells are cultured in appropriate media, they form both bone and cartilage cells, and if placed into the developing head, they contribute to cranial skeletal components. Thus, the neural crest from all axial levels can generate the full repertoire of crest derivatives. The skeletogenic potential of the trunk neural crest is significant, as it was likely realized in early vertebrates, which had extensive postcranial exoskeletal coverings.

Animals↗

Deficits in the posterior pharyngeal endoderm in the absence of retinoids.

Recent studies have shown that the pharyngeal endoderm plays a critically important role in directing the development of the pharyngeal region of the vertebrate embryo. We have, however, had few insights into how the pharyngeal endoderm itself is patterned. Recently, several studies have suggested that retinoic acid is required for the development of the pharyngeal endoderm. To study this proposal in greater depth, we have examined the development of the pharyngeal endoderm in the absence of retinoid signalling, by using the vitamin A- deficient (VAD) quail model system. We find in early stages that, in the absence of retinoids, this territory extends further caudally than normal. Furthermore, as development proceeds, we find that the first pouch invariably forms, that the second pouch is abnormal, and that the third and fourth pharyngeal pouches never form. We do find, however, that dorsoventral patterning of the pharyngeal endoderm is unaffected. Finally, we have examined the expression patterns of RALDH2 before and during early development of the pharyngeal pouches. We find that this enzyme is expressed adjacent to the pharyngeal endoderm in tissues around the regressing anterior intestinal portal and that from stage 12 onward its anterior limit of expression lies at the level of the second pouch. This finding helps explain why the first pouch always forms in the absence of retinoids, and why defects are seen starting with the second and most evidently in the caudal pouches.

Aldehyde Oxidoreductases↗