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Craniofacial development is initiated with the establishment of an embryo's anteroposterior axis, marking a critical evolutionary step in vertebrates with the emergence of neural crest and ectodermal placodes. Recent studies have elucidated the generation and influence of neural crest cells in morphogenesis, highlighting their interaction with various epithelial sources which have been identified as active participants rather than passive bystanders. This review aims to synthesize innovative research in the field, demonstrating the complexities of craniofacial tissue interaction and the role of signaling pathways such as Fgf in developmental processes.
Developmental Biology, 2011
Classic neontology (comparative embryology and anatomy), through the application of the concept of homology, has demonstrated that the development of the gnathostome (jawed vertebrate) skull is characterized both by a fidelity to the gnathostome bauplan and the exquisite elaboration of final structural design. Just as homology is an old concept amended for modern purposes, so are many of the questions regarding the development of the skull. With due deference to Geoffroy-St. Hilaire, Cuvier, Owen, Lankester et al., we are still asking: How are bauplan fidelity and elaboration of design maintained, coordinated, and modified to generate the amazing diversity seen in cranial morphologies? What establishes and maintains pattern in the skull? Are there universal developmental mechanisms underlying gnathostome autapomorphic structural traits? Can we detect and identify the etiologies of heterotopic (change in the topology of a developmental event), heterochronic (change in the timing of a developmental event), and heterofacient (change in the active capacetence, or the elaboration of capacity, of a developmental event) changes in craniofacial development within and between taxa? To address whether jaws are all made in a like manner (and if not, then how not), one needs a starting point for the sake of comparison. To this end, we present here a "hinge and caps" model that places the articulation, and subsequently the polarity and modularity, of the upper and lower jaws in the context of cranial neural crest competence to respond to positionally located epithelial signals. This model expands on an evolving model of polarity within the mandibular arch and seeks to explain a developmental patterning system that apparently keeps gnathostome jaws in functional registration yet tractable to potential changes in functional demands over time. It relies upon a system for the establishment of positional information where pattern and placement of the "hinge" is driven by factors common to the junction of the maxillary and mandibular branches of the first arch and of the "caps" by the signals emanating from the distal-most first arch midline and the lamboidal junction (where the maxillary branch meets the frontonasal processes). In this particular model, the functional registration of jaws is achieved by the integration of "hinge" and "caps" signaling, with the "caps" sharing at some critical level a developmental history that potentiates their own coordination. We examine the evidential foundation for this model in mice, examine the robustness with which it can be applied to other taxa, and examine potential proximate sources of the signaling centers. Lastly, as developmental biologists have long held that the anterior-most mesendoderm (anterior archenteron roof or prechordal plate) is in some way integral to the normal formation of the head, including the cranial skeletal midlines, we review evidence that the seminal patterning influences on the early anterior ectoderm extend well beyond the neural plate and are just as important to establishing pattern within the cephalic ectoderm, in particular for the "caps" that will yield medial signaling centers known to coordinate jaw development.
Methods Mol Biol, 2008
Among the symposia held at the seminal meeting of the European Society for Evolutionary Developmental Biology was one centered on the development and evolution of the vertebrate head, an exquisitely complex anatomical system. The articles presented at this meeting have been gathered in a special issue of the Journal of Experimental Zoology, and are here reviewed by the organizers of the symposia. These articles cover a breadth of subjects, including interactions between cells derived from the different germ layers, such as those underlying neural crest cell migration and fate and cranial muscle specification, as well as placode development and the origin, development, and evolution of important evolutionary innovations such as jaws and the trabecula cranii. In this introduction, we provide a short historical overview of themes of research into the fundamental organization, structure, and development of the vertebrate head, including the search for head segmentation and the relevance of the New Head Hypothesis, and subsequently present the topics discussed in each of the articles. This overview of the past and the present of head evo-devo is then followed by a glimpse at its possible future and a brief examination of the utility of the notions of heterochrony, heterotopy, and heterofacience in describing evolutionarily important changes in developmental events.
Theory in Biosciences, 2005
Vertebrate head development is a classical topic lately invigorated by methodological as well as conceptual advances. In contrast to the classical segmentalist views going back to idealistic morphology, the head is now seen not as simply an extension of the trunk, but as a structure patterned by different mechanisms and tissues. Whereas the trunk paraxial mesoderm imposes its segmental pattern on adjacent tissues such as the neural crest derivatives, in the head the neural crest cells carry pattern information needed for proper morphogenesis of mesodermal derivatives, such as the cranial muscles. Neural crest cells make connective tissue components which attach the muscle fiber to the skeletal elements. These crest cells take their origin from the same visceral arch as the muscle cells, even when the skeletal elements to which the muscle attaches are from another arch. The neural crest itself receives important patterning influences from the pharyngeal endoderm. The origin of jaws can be seen as an exaptation in which a heterotopic shift of the expression domains of regulatory genes was a necessary step that enabled this key innovation. The jaws are patterned by Dlx genes expressed in a nested pattern along the proximo-distal axis, analogous to the anterior-posterior specification governed by ARTICLE IN PRESS www.elsevier.de/thbio 1431-7613/$ -see front matter
Developmental Dynamics, 2006
Craniofacial malformations are involved in three fourths of all congenital birth defects in humans, affecting the development of head, face, or neck. Tremendous progress in the study of craniofacial development has been made that places this field at the forefront of biomedical research. A concerted effort among evolutionary and developmental biologists, human geneticists, and tissue engineers has revealed important information on the molecular mechanisms that are crucial for the patterning and formation of craniofacial structures. Here, we highlight recent advances in our understanding of evo-devo as it relates to craniofacial morphogenesis, fate determination of cranial neural crest cells, and specific signaling pathways in regulating tissue-tissue interactions during patterning of craniofacial apparatus and the morphogenesis of tooth, mandible, and palate. Together, these findings will be beneficial for the understanding, treatment, and prevention of human congenital malformations and establish the foundation for craniofacial tissue regeneration.
Theoretical Biology Forum; 106 (1-2), 2013
Modularity in biological systems is a central theme in current research. However, there are some problems related to the vague definitions of the concept of a module that impede both its empirical application and the comparison of data from different studies. In this article, we propose to characterize this concept which is consistent with the diverse ways in which it is conceptualized in the specialist literature. We test our characterization by analyzing the case study of the craniofacial complex. We conclude that the proposed delimitation allows a better understanding of modules since it differentiates between the concept of the module as a state (morphofunctional modules) and as a process (a product of ontogenetic or phylogenetic history).
Animal Biology, 2006
The vertebrate cranium consists of three parts: neuro-, viscero-and dermatocranium, which differ in both developmental and phylogenetic origin. Traditionally, developmental origin has been used as a criterion for homology, but this becomes problematic when skull elements such as the parietal bone are now shown, by modern fate-mapping studies, to have different developmental origins in different groups of tetrapods. This indicates a flexibility of developmental programmes and regulatory pathways which has probably been very important in cranial evolution. The trabecula cranii is an intriguing cranial element in the anterior cranial base in vertebrates. It forms a viscerocranial part of the neurocranium and is believed to be neural crest-derived in gnathostomes, but a similarly named structure in lampreys has been shown to have a mesodermal origin. Topographically, this trabecula seems to be homologous to the gnathostome trabecula cranii, and might also have the same function: to form a border between adjacent morphogenetic domains, to constrain and redirect growth of both brain and stomodeum and thus to refine developmental schedules of both. We suggest that such a border zone can recruit cells from either the mesoderm (as in the lamprey) or from the neural crest (as in the gnathostomes investigated), and still retain its homology. In our view, the trabecula is an interface element that integrates the respective divergent morphogenetics programs of the preotic head into a balanced unit; we suggest that such a definition can be used to define "the sameness" of this element throughout vertebrates.
Developmental …, 2004
Cartilage of the vertebrate jaw is derived from cranial neural crest cells that migrate to the first pharyngeal arch and form a dorsal bmaxillaryQ and a ventral bmandibularQ condensation. It has been assumed that the former gives rise to palatoquadrate and the latter to Meckel's (mandibular) cartilage. In anamniotes, these condensations were thought to form the framework for the bones of the adult jaw and, in amniotes, appear to prefigure the maxillary and mandibular facial prominences. Here, we directly test the contributions of these neural crest condensations in axolotl and chick embryos, as representatives of anamniote and amniote vertebrate groups, using molecular and morphological markers in combination with vital dye labeling of late-migrating cranial neural crest cells. Surprisingly, we find that both palatoquadrate and Meckel's cartilage derive solely from the ventral bmandibularQ condensation. In contrast, the dorsal bmaxillaryQ condensation contributes to trabecular cartilage of the neurocranium and forms part of the frontonasal process but does not contribute to jaw joints as previously assumed. These studies reveal the morphogenetic processes by which cranial neural crest cells within the first arch build the primordia for jaw cartilages and anterior cranium. D 2004 Elsevier Inc. All rights reserved.
Trends in Genetics, 2002
The cranial neural crest originates at the dorsal margin of the neural tube and produces migratory cells that populate various locations in the head. They are a crucial factor in the development of the vertebrate head because they give rise to numerous differentiated cell types, including the cartilage, bone and connective tissues of the skull. Thus, the coordinated regulation of crest cell movement and patterning is pivotal to the acquisition of organized head structure. Two recent papers cast light on the molecular mechanisms and tissue interactions employed by an embryo to achieve this goal. Here, we discuss the implications of these findings in view of pre-existing principles of neural crest patterning. Crucially, these new data implicate, for the first time, that head skeletal patterning is controlled by tissue other than the neural crest.
Trends in Ecology & Evolution, 1993
Frontiers in Cell and Developmental Biology, 2022
Embryonic craniofacial development involves a series of cellular processes that drive patterning, outgrowth, and fusion of a number of independently forming components. The progression of growth and morphogenesis relies on cellular mechanisms such as differentiation, proliferation, migrations, transformation, and apoptosis to form the correct shape and structure in the developing embryo (Figure 1). During craniofacial development, the aforementioned processes are spatiotemporally constrained, allowing for multiple mechanisms within a relatively small region in order to create complex and intricate structures. Failure at any stage risks considerable consequences for the embryo, ranging from slight defects in craniofacial patterning to total inviability. The current Research Topic "Cellular Mechanisms During Normal and Abnormal Craniofacial Development" intends to examine and collate the most up-to-date studies on the cellular processes that drive embryonic craniofacial morphogenesis. In recent years, scientists have taken great strides towards attaining a better understanding of the cellular mechanisms involved in the fundamental aspects of craniofacial development. Seemingly disparate fields such as computer sciences, mathematics, tomographic and microscopic imaging, biochemistry, and molecular biology have come together to greatly enhance our understanding of how individual cells influence the overall patterning and morphogenesis of the embryonic face. This Research Topic includes 21 papers that focus on the cellular processes involved in the development of a variety of craniofacial structures such as palate, teeth, eyes, craniofacial muscles, as well as their contribution to associated developmental defects. Additionally, the importance of interaction between neural tissue and forming face is introduced and discussed. CELLULAR PROCESSES IN CRANIOFACIAL STRUCTURES SHAPING AND PATTERNING Murrilo-Rincón and Kaucka reviewed the complexity of craniofacial structure development from a cellular perspective. They focused on the cell fate specification in craniofacial structures from the
American Journal of Medical Genetics Part A, 2010
Approximately three quarters of children with birth defects have anomalies that affect the craniofacial structures. Defects in this area of the body result in lifelong disability, major challenges to families and society and often a serious effect on life expectancy. Surgery has been the primary intervention for these disorders, with frequently less than optimal outcomes and risk for additional morbidity and mortality. The challenge for clinicians caring for these children is to develop new methods for the treatment and prevention of these disorders. An understanding of the evolution of the head and the finely tuned temporospatial signaling pathways involved is critical to understanding the origins of the vertebrates as well as of human craniofacial malformations. In the future, these new approaches will be based upon our enhanced understanding of the developmental tool kit fashioned by evolution and the application of this knowledge toward the development of new diagnostic, pharmacologic, and genetic interventions for these disorders.
2003
The vertebrate head is a complex assemblage of cranial specializations, including the central and peripheral nervous systems, viscero-and neurocranium, musculature and connective tissue. The primary differences that exist between vertebrates and other chordates relate to their craniofacial organization. Therefore, evolution of the head is considered fundamental to the origins of vertebrates (Gans and Northcutt, 1983). The transition from invertebrate to vertebrate chordates was a multistep process, involving the formation and patterning of many new cell types and tissues. The evolution of early vertebrates, such as jawless fish, was accompanied by the emergence of a specialized set of cells, called neural crest cells which have long held a fascination for developmental and evolutionary biologists due to their considerable influence on the complex development of the vertebrate head. Although it has been classically thought that protochordates lacked neural crest counterparts, the recent identification and characterization of amphioxus and ascidian genes homologous to those involved in vertebrate neural crest development challenges this idea. Instead it suggests that the neural crest may not be a novel vertebrate cell population, but could have in fact originated from the protochordate dorsal midline epidermis. Consequently, the evolution of the neural crest cells could be reconsidered in terms of the acquisition of new cell properties such as delamination-migration and also multipotency which were key innovations that contributed to craniofacial development. In this review we discuss recent findings concerning the inductive origins of neural crest cells, as well as new insights into the mechanisms patterning this cell population and the subsequent influence this has had on craniofacial evolution.
Developmental Biology, 2008
The vertebrate cranial base is a complex structure composed of bone, cartilage and other connective tissues underlying the brain; it is intimately connected with development of the face and cranial vault. Despite its central importance in craniofacial development, morphogenesis and tissue origins of the cranial base have not been studied in detail in the mouse, an important model organism. We describe here the location and time of appearance of the cartilages of the chondrocranium. We also examine the tissue origins of the mouse cranial base using a neural crest cell lineage cell marker, Wnt1-Cre/ R26R, and a mesoderm lineage cell marker, Mesp1-Cre/R26R. The chondrocranium develops between E11 and E16 in the mouse, beginning with development of the caudal (occipital) chondrocranium, followed by chondrogenesis rostrally to form the nasal capsule, and finally fusion of these two parts via the midline central stem and the lateral struts of the vault cartilages. X-Gal staining of transgenic mice from E8.0 to 10 days post-natal showed that neural crest cells contribute to all of the cartilages that form the ethmoid, presphenoid, and basisphenoid bones with the exception of the hypochiasmatic cartilages. The basioccipital bone and non-squamous parts of the temporal bones are mesoderm derived. Therefore the prechordal head is mostly composed of neural crestderived tissues, as predicted by the New Head Hypothesis. However, the anterior location of the mesoderm-derived hypochiasmatic cartilages, which are closely linked with the extra-ocular muscles, suggests that some tissues associated with the visual apparatus may have evolved independently of the rest of the "New Head".
Journal of Anatomy, 2005
Contemporary studies of vertebrate cranial development document the essential role played by the embryonic neural crest as both a source of adult tissues and a locus of cranial form and patterning. Yet corresponding and basic features of cranial evolution, such as the extent of conservation vs. variation among species in the contribution of the neural crest to specific structures, remain to be adequately resolved. Investigation of these features requires comparable data from species that are both phylogenetically appropriate and taxonomically diverse. One key group are amphibians, which are uniquely able to inform our understanding of the ancestral patterns of ontogeny in fishes and tetrapods as well as the evolution of presumably derived patterns reported for amniotes. Recent data support the hypothesis that a prominent contribution of the neural crest to cranial skeletal and muscular connective tissues is a fundamental property that evolved early in vertebrate history and is retained in living forms. The contribution of the neural crest to skull bones appears to be more evolutionarily labile than that of cartilages, although significance of the limited comparative data is difficult to establish at present. Results underline the importance of accurate and reliable homology assessments for evaluating the contrasting patterns of derivation reported for the three principal tetrapod models: mouse, chicken and frog.
Brain Research Reviews, 2007
Since the time of Ramon y Cajal, very significant progress has been accomplished in our knowledge of the fate of the early neural primordium. The origin of the peripheral nervous system from the transient and pluripotent embryonic structure, the neural crest has been fully deciphered through the use of appropriate cell marking techniques. Most of the pioneer work in this field was carried out in lower vertebrates up to 1950 and later on in the avian embryo. New techniques which allow the genetic labelling of embryonic cells by transgenesis are now applied in mammals and fish.
Developmental biology, 2016
The apparent evolvability of the vertebrate head skeleton has allowed a diverse array of shapes, sizes, and compositions of the head in order to better adapt species to their environments. This encompasses feeding, breathing, sensing, and communicating: the head skeleton somehow participated in the evolution of all these critical processes for the last 500 million years. Through evolution, present head diversity was made possible via developmental modifications to the first head skeletal genetic program. Understanding the development of the vertebrate common ancestor's head skeleton is thus an important step in identifying how different lineages have respectively achieved their many innovations in the head. To this end, cyclostomes (jawless vertebrates) are extremely useful, having diverged from jawed vertebrates approximately 400 million years ago, at the deepest node within living vertebrates. From this ancestral vantage point (that is, the node connecting cyclostomes and gnat...
Development
To investigate the influence of hindbrain segmentation on craniofacial patterning we have studied the long term fate of neural crest (NC) subpopulations of individual rhombomeres (r), using quail-chick chimeras. Mapping of all skeletal and muscle connective tissues developing from these small regions revealed several novel features of the cranial neural crest. First, the mandibular arch skeleton has a composite origin in which the proximal elements are r1+r2 derived, whereas more distal ones are exclusively midbrain derived. The most proximal region of the lower jaw is derived from second arch (r4) NC. Second, both the lower jaw and tongue skeleton display an organisation which precisely reflects the rostrocaudal order of segmental crest deployment from the embryonic hindbrain. Third, cryptic intraskeletal boundaries, which do not correspond to anatomical landmarks, form sharply defined interfaces between r1+r2, r4 and r6+r7 crest. Cells that survive the early apoptotic elimination ...
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