Morphogen gradients, positional information, and Xenopus : Interplay of theory and experiment

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 importan...

Section: From Organizer To Mesendoderm To Pharyngeal Endoderm: Succesmentioning

confidence: 98%

21^st Century neontology and the comparative development of the vertebrate skull

Depew

Simpson

2006

“…These include signalling from the Nieuwkoop Centre, the Spemann Centre, and the notochord (Green, 2002;Marti and Bovolenta, 2002;Ashe and Briscoe, 2006). Patterning of embryonic tissue by such morphogens is well established, but the mechanism by which such a patterning occurs is still obscure.…”

Section: Introductionmentioning

confidence: 99%

Two‐dimensional morphogen gradient in Xenopus: Boundary formation and real‐time transduction response

Kinoshita

Jullien

Gurdon

2006

Morphogen gradients play an important role in pattern formation in embryo. However, the interpretation of position in a morphogen gradient is not well understood. Because it is hard to analyze morphogen gradients especially in opaque embryos such as those of Xenopus, it is necessary to fix and section the embryo, thereby eliminating the possibility of real-time observation, and making more difficult the interpretation of events that take place in three dimensions. We describe here a two-dimensional preparation of cells from a Xenopus blastula animal cap, in which an activin concentration gradient appears to be formed and interpreted at the same rate and in the same way as in normal embryos. We use two-dimensional preparations of this kind to contribute the following new information about gradient formation and interpretation in embryo. We determine the dynamics of formation of an activin activity gradient in real time. We demonstrate that this gradient is established by diffusion of activin through intercellular space and does not require internalization of receptor or ligand. We also show that the generation of a boundary of gene expression depends on the interpretation, rather than a change of composition, of the concentration gradient. Developmental Dynamics 235:3189 -3198, 2006.

“…The organized operation of cell behaviors depends on temporal and spatial references settled by signaling centers, i.e., zones of polarizing activity (Freeman and Gurdon, 2002;Green, 2002). The isthmic organizer (IsO), a signaling center located at the midhindbrain (MHB) isthmus, regulates the patterning along the cephaliccaudal (cph-cd) axis of both the midand the hindbrain (Joyner et al, 2000;Olander et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Optic tectum morphogenesis: A step‐by‐step model based on the temporal–spatial organization of the cell proliferation. Significance of deterministic and stochastic components subsumed in the spatial organization

Rapacioli

Duarte

Celin

et al. 2012

Background: Cell proliferation plays an important morphogenetic role. This work analyzes the temporalspatial organization of cell proliferation as an attempt to understand its contribution to the chick optic tectum (OT) morphogenesis. Results: A morphogenetic model based on space-dependent differences in cell proliferation is presented. Step1: a medial zone of high mitotic density (mZHMD) appears at the caudal zone. Step2: the mZHMD expands cephalically forming the dorsal curvature and then duplicates into two bilateral ZHMDs (bZHMD). Step3: the bZHMDs move toward the central region of each hemitectum. Step4: the planar expansion of both bZHMD and a relative decrement in the dorsal midline growth produces a dorsal medial groove separating the tectal hemispheres. Step5: a relative caudal displacement of the bZHMDs produces the OT caudal curvature. Numerical sequences derived from records of mitotic cells spatial coordinates, analyzed as stochastic point processes, show that they correspond to 1/f (b) processes. The spatial organization subsumes deterministic and stochastic components. Conclusions: The deterministic component describes the presence of a long-range influence that installs an asymmetric distribution of cell proliferation, i.e., an asymmetrically located ZHMD that print space-dependent differences onto the tectal corticogenesis. The stochastic component reveals short-range anti-correlations reflecting spatial clusterization and synchronization between neighboring cells. Developmental Dynamics 241:1043-1061, 2012. V C 2012 Wiley Periodicals, Inc.Key words: developing CNS; mitotic cell organization; nonlinear analyses; morphogenesis Key findings:The signals representing the mitotic cell spatial organization display 1/f type spectrum. The signals subsume deterministic components that reveal the existence of long-range influences. The signals subsume stochastic fluctuations revealing short-range anti-correlations between adjacent cells. The differential displacements of zones of high mitotic density regulate planar expansion. The asymmetric proliferation prints space-dependent histogenetic changes to the tectal corticogenesis.