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PubMed2003

The emergent design of the neural tube: prepattern, SHH morphogen and GLI code.

The Sonic hedgehog (Shh) pathway plays an important role in the development of many tissues and organs. The secreted ligand Shh has been shown to act as a mitogen, morphogen and survival factor in different contexts whereas the three Gli transcription factors act as Shh mediators in a context-dependent combinatorial fashion. The common wisdom has been that Gli protein function is subject to Shh signaling. One can ask how Gli proteins act and what the nature of Shh signaling during CNS dorsal-ventral patterning is. Is it possible that Hedgehog signals are only one of several ways to regulate Gli activity? Moreover, in light of the partial rescue of the neural tube phenotype of Shh or Smoothened mutant embryos in Shh(-/-);Gli3(-/-), Smoothened(-/-);Gli3(-/-), and Shh(-/-);Rab23(-/-) double null embryos, one can consider the roles that the Shh-Gli pathway may have taken to orchestrate congruent prepattern and growth, and the importance of creating the correct number of precursors in patterning mechanisms.

Animals↗
PubMed2006

Mechanistic insight into how Shh patterns the vertebrate limb.

The hands and feet of a newborn baby are a beautiful reminder of the complexity of embryonic patterning. Classical studies on how these structures form have led to a theoretical framework for understanding, in general, how discrete groups of cells can instruct differential fates across a wider field through the action of long-range signals. The discovery just more than a decade ago that localized expression of Sonic hedgehog (Shh) differentially patterns structures across the limb field, resulting in digits with unique characteristics, provided a starting point for readdressing these models at a molecular level. Current research has revealed unexpected complexity in how a gradient of Shh activity is both established and received, prompting re-evaluation of the nature of patterning mechanisms within the limb.

Animals↗
PubMed2005

The mechanisms of dorsoventral patterning in the vertebrate neural tube.

We describe the essential features of and the molecules involved in dorsoventral (DV) patterning in the neural tube. The neural tube is, from its very outset, patterned in this axis as there is a roof plate, floor plate, and differing numbers and types of neuroblasts. These neuroblasts develop into different types of neurons which express a different range of marker genes. Early embryological experiments identified the notochord and the somites as being responsible for the DV patterning of the neural tube and we now know that 4 signaling molecules are involved and are generated by these surrounding structures. Fibroblast growth factors (FGFs) are produced by the caudal mesoderm and must be down-regulated before neural differentiation can occur. Retinoic acid (RA) is produced by the paraxial mesoderm and is an inducer of neural differentiation and patterning and is responsible for down-regulating FGF. Sonic hedgehog (Shh) is produced by the notochord and floor plate and is responsible for inducing ventral neural cell types in a concentration-dependent manner. Bone morphogenetic proteins (BMPs) are produced by the roof plate and are responsible for inducing dorsal neural cell types in a concentration-dependent manner. Subsequently, RA is used twice more. Once from the somites for motor neuron differentiation and secondly RA is used to define the motor neuron subtypes, but in the latter case it is generated within the neural tube from differentiating motor neurons rather than from outside. These 4 signaling molecules also interact with each other, generally in a repressive fashion, and DV patterning shows how complex these interactions can be.

Animals↗
PubMed2005

rap gene encodes Fizzy-related protein (Fzr) and regulates cell proliferation and pattern formation in the developing Drosophila eye-antennal disc.

The rap (retina aberrant in pattern) gene encodes the Fizzy-related protein (Fzr), which as an activator of the ubiquitin ligase complex; APC/C (anaphase promoting complex/cyclosome) facilitates the cell cycle stage-specific degradation of cyclins. Loss-of-function mutations in rap cause unscheduled accumulation of cyclin B in the developing eye imaginal disc, resulting in additional mitotic cycles and defective patterning of the developing Drosophila eye. Targeted mis-expression of rap/fzr in the eye primordial cells causes precocious cell cycle exit, and smaller primordial eye fields, which either eliminate or drastically reduce the size of the adult eye. Although mitosis is inhibited in the mis-expression animals, cells with abnormally large nuclei form tumor-like structures from continued endoreplication, cell growth and retinal differentiation. Interestingly, overexpression of Rap/Fzr in the eye primordia also increases the size of the antennal primordium resulting in the induction of ectopic antennae. These results suggest that Rap/Fzr plays an essential role in the timely exit of precursor cells from mitotic cycles and indicate that mechanisms that regulate cell cycle exit are critical during pattern formation and morphogenesis.

Animals↗
PubMed2003

Doubleridge, a mouse mutant with defective compaction of the apical ectodermal ridge and normal dorsal-ventral patterning of the limb.

doubleridge is a transgene-induced mutation characterized by polydactyly and syndactyly of the forelimbs. The transgene insertion maps to the proximal region of chromosome 19. During embryonic development of the mutant forelimb, delayed elevation and compaction of the apical ectodermal ridge (AER) produces a ridge that is abnormally broad and flat. Fgf8 expression persists in the ventral forelimb ectoderm of the mutant until E10.5. Strong expression of Fgf8 and other markers at the borders of the AER at E11.5 gives the appearance of a double ridge. At E11.5, apoptotic cells are distributed across the broadened ridge, but at E13.5, there is reduced apoptosis in the interdigital regions. The Shh expression domain is widely spaced at the posterior margin of the AER. The doubleridge AER is morphologically similar to that of En1 null mice, but the expression of En1 and Wnt7a is properly restricted in doubleridge, and the dorsal and ventral structures are correctly determined. doubleridge thus exhibits an unusual limb phenotype combining abnormal compaction of the AER with normal dorsal/ventral patterning.

Animals↗
PubMed1998

An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg.

Intercellular signaling through the EGF receptor (EGFR) patterns the Drosophila egg. The TGF alpha-like ligand Gurken signals from the oocyte to the receptor in the overlying somatic follicle cells. We show that in the dorsal follicle cells this initial paracrine signaling event triggers an autocrine amplification by two other EGFR ligands, Spitz and Vein. Spitz only becomes an effective ligand in the presence of the multitransmembrane domain protein Rhomboid. Consequent high-level EGFR activation leads to localized expression of the diffusible inhibitor Argos, which alters the profile of signaling. This sequential activation, amplification, and local inhibition of the EGFR forms an autoregulatory cascade that leads to the splitting of an initial single peak of signaling into two, thereby patterning the egg.

Animals↗
PubMed2001

Cytochrome P450s: coupling development and environment.

There is growing evidence that some members of the cytochrome P450 superfamily could be involved in the regulation of basic developmental processes such as pattern formation, morphogenesis, cell differentiation and growth. This development calls attention to the myriad small molecules metabolized by cytochrome P450s, some of which might function as the morphogens proposed by the Local Source-Dispersed Sink hypothesis. This new information also suggests a mechanism for the developmental toxicity of drugs and environmental pollutants: such compounds could interfere with normal development by altering the spatial and temporal expression patterns of cytochrome P450s required for normal development.

Animals↗
PubMed2000

Bottle cell formation in relation to mesodermal patterning in the Xenopus embryo.

The appearance of bottle cells at the dorsal vegetal/marginal boundary of Xenopus embryos marks the onset of blastopore formation. The conditions leading to this epithelial activity were investigated by inducing bottle cells ectopically in the animal region with VegT or different members of the transforming growth factor (TGF)-beta family. Morphological studies on the ectopic bottle cells indicate their close similarity to the endogenous bottle cells at the dorsal blastopore lip. The subepithelial cells of the induced animal region express mesodermal genes in a pattern reminiscent to that observed on the dorsal lip. Relating this expression pattern to the position of the ectopic bottle cells leads to the conclusion that bottle cells form in regions of high TGF-beta signalling. The specific inhibitory effects of cerberus on ectopically induced bottle cells revealed that nodal related growth factors are the intrinsic signals that elicit bottle cell formation in the normal embryo. In addition, fibroblast growth factor signalling is an essential precondition for this epithelial response as it is for mesoderm formation. We conclude that bottle cell formation in the epithelial layer of the gastrula is closely linked to mesodermal patterning in the subepithelial tissues.

Activins↗
PubMed1998

Mediolateral patterning of somites: multiple axial signals, including Sonic hedgehog, regulate Nkx-3.1 expression.

The axial structures, the notochord and the neural tube, play an essential role in the dorsoventral patterning of somites and in the differentiation of their many cell lineages. Here, we investigated the role of the axial structures in the mediolateral patterning of the somite by using a newly identified murine homeobox gene, Nkx-3.1, as a medial somitic marker in explant in vitro assays. Nkx-3.1 is dynamically expressed during somitogenesis only in the youngest, most newly-formed somites at the caudal end of the embryo. We found that the expression of Nkx-3.1 in pre-somitic tissue explants is induced by the notochord and maintained in newly-differentiated somites by the notochord and both ventral and dorsal parts of the neural tube. We showed that Sonic hedgehog (Shh) is one of the signaling molecules that can reproduce the effect of the axial structures by exposing explants to either COS cells transfected with a Shh expression construct or to recombinant SHH. Shh could induce and maintain Nkx-3.1 expression in pre-somitic mesoderm and young somites but not in more mature, differentiated ones. The effects of Shh on Nkr-3.1 expression were antagonized by a forskolin-induced increase in the activity of cyclic AMP-dependent protein kinase A. Additionally, we confirmed that the expression of the earliest expressed murine myogenic marker, myf 5, is also regulated by the axial structures but that Shh by itself is not capable of inducing or maintaining it. We suggest that the establishment of somitic medial and lateral compartments and the early events in myogenesis are governed by a combination of positive and inhibitory signals derived from the neighboring structures, as has previously been proposed for the dorsoventral patterning of somites.

Animals↗
PubMed1997

Differentiation of the vertebrate neural tube.

The vertebrate nervous system arises through a series of inductive interactions, beginning with the induction of the neural plate and the rostrocaudal patterning of the neural tube. The process continues with dorsoventral patterning of the neural tube, during which floor plate cells and motor neurons are induced ventrally by interactions of the neural tube with the notochord, and dorsal cell types are induced via neural plate/ectodermal interactions. Later interactions result in the formation of interneurons as well as neuronal migrations. Recent progress, guided in part by knowledge of evolutionary conservation of transcription factors and signaling pathways, is beginning to reveal the cellular and molecular bases of each of these steps in neuronal patterning.

Animals↗
PubMed2001

Axis formation and patterning in zebrafish.

A large collection of mutations affecting zebrafish embryogenesis was described in 1996. The cloning of the affected genes has now provided novel insights into the role and regulation of signaling by BMP, Nodal, Wnt, FGF, Hedgehog, Delta, Slit, retinoic acid and lipids. Detailed analyses have revealed a complex genetic network that patterns the early embryo.

Animals↗
PubMed2001

Nodal signaling in early vertebrate embryos: themes and variations.

The nodal family of TGFbeta-related ligands have emerged as critical regulators of early vertebrate embryogenesis. Recent studies in mice, fish, and frogs of nodals and their intracellular transducers allow a comparison of how this signaling pathway is used in the patterning of early embryos of these different vertebrates.

Animals↗
PubMed2003

Xanthophore migration from the dermis to the epidermis and dermal remodeling during Salamandra salamandra salamandra (L.) larval development.

During larval development of Salamandra salamandra salamandra chromatophores organize to form the definitive pigment pattern constituted by a black background with yellow patches that are characterized by epidermal xanthophores and dermal iridophores. Simultaneously the dermis undergoes remodeling from the larval stage to that typical of the adult. In the present study we ultrastucturally and immunocytochemically examined skin fragments of S. s. salamandra larvae and juveniles in order to investigate the modalities of xanthophore migration and differentiation in the context of dermal remodeling from the larval to adult stage. Semithin and thin sections showed that the dermis in newly born larvae consists of a compact connective tissue (basement lamella), to which fibroblasts and xanthophores adhere, and of a loose deep collagen layer. As larval development proceeds, fibroblasts and xanthophores invade the basement lamella, skin glands develop and the adult dermis forms. At metamorphosis, xanthophores reach the epidermis crossing through the basal lamina. We examined immunocytochemically the expression of signal molecules, such as fibronectin, vitronectin, beta1-integrin, chondroitin sulfate, E-cadherin, N-cadherin and plasminogen activator, which are known to be involved in regulating morphogenetic events. Their role in dermal remodeling and in pigment pattern formation is discussed.

Animals↗
PubMed1998

Smad2 role in mesoderm formation, left-right patterning and craniofacial development.

Signalling by the transforming growth factor-beta (TGF-beta) superfamily of proteins depends on the phosphorylation and activation of SMAD proteins by heteromeric complexes of ligand-specific type I and type II receptors with serine/threonine-kinase activity. The vertebrate SMAD family includes at least nine members, of which Smad2 has been shown to mediate signalling by activin and TGF-beta. In Xenopus, Smad2 can induce dorsal mesoderm, mimicking Vg-1, activin and nodal. Here we investigate the function of Smad2 in mammalian development by generating two independent Smad2 mutant alleles in mice by gene targeting. We show that homozygous mutant embryos fail to form an organized egg cylinder and lack mesoderm, like mutant mice lacking nodal or ActRIB, the gene encoding the activin type-I receptor. About 20 per cent of Smad2 heterozygous embryos have severe gastrulation defects and lack mandibles or eyes, indicating that the gene dosage of Smad2 is critical for signalling. Mice trans-heterozygous for both Smad2 and nodal mutations display a range of phenotypes, including gastrulation defects, complex craniofacial abnormalities such as cyclopia, and defects in left-right patterning, indicating that Smad2 may mediate nodal signalling in these developmental processes. Our results show that Smad2 function is essential for early development and for several patterning processes in mice.

Abnormalities, Multiple↗
PubMed1998

Retinoic acid affects patterning along the anterior-posterior axis of the ascidian embryo.

Because retinoic acid (RA) is known to affect anterior posterior patterning in vertebrate embryos, it was questioned whether it shows similar effects in a more primitive chordate, the ascidian Halocynthia roretzi. Ascidian embryos treated with RA exhibited truncated phenotypes in a dose-dependent manner similar to the anterior truncations seen in vertebrate embryos. The most severely affected larvae possessed a round trunk without the papillae characteristic of the anterior terminal epidermis. Retinoic acid also altered the expression of HrHox-1 and Hroth in a dose-dependent manner. Expression of HrHox-1 increased, whereas expression of Hroth decreased with increasing levels of RA. In treated embryos, HrHox-1 was first expressed pan-ectodermally, then degraded in all but specific regions of the embryo. By contrast, initiation of Hroth expression was not affected, but epidermal expression was lost while expression in the neural tube narrowed toward the anterior in tail-bud embryos. These alterations in the expression of homeobox genes appear to correlate closely to the morphological defects elicited by RA treatment, suggesting broad conservation of developmental patterning mechanisms within the Phylum Chordata.

Animals↗
PubMed2005

Gene regulatory networks for development.

The genomic program for development operates primarily by the regulated expression of genes encoding transcription factors and components of cell signaling pathways. This program is executed by cis-regulatory DNAs (e.g., enhancers and silencers) that control gene expression. The regulatory inputs and functional outputs of developmental control genes constitute network-like architectures. In this PNAS Special Feature are assembled papers on developmental gene regulatory networks governing the formation of various tissues and organs in nematodes, flies, sea urchins, frogs, and mammals. Here, we survey salient points of these networks, by using as reference those governing specification of the endomesoderm in sea urchin embryos and dorsal-ventral patterning in the Drosophila embryo.

Animals↗
PubMed1999

Stripe formation in juvenile Pomacanthus explained by a generalized turing mechanism with chemotaxis.

Current interest in pattern formation can be traced to a seminal paper by Turing, who demonstrated that a system of reacting and diffusing chemicals, called morphogens, can interact so as to produce stable nonuniform concentration patterns in space. Recently, a Turing model has been suggested to explain the development of pigmentation patterns on species of growing angelfish such as Pomacanthus semicirculatus, which exhibit readily observed changes in the number, size, and orientation of colored stripes during development of juvenile and adult stages, but the model fails to predict key features of the observations on stripe formation. Here we develop a generalized Turing model incorporating cell growth and movement, we analyze the effects of these processes on patterning, and we demonstrate that the model can explain important features of pattern formation in a growing system such as Pomacanthus. The applicability of classical Turing models to biological pattern formation is limited by virtue of the sensitivity of patterns to model parameters, but here we show that the incorporation of growth results in robustly generated patterns without strict parameter control. In the model, chemotaxis in response to gradients in a morphogen distribution leads to aggregation of one type of pigment cell into a striped spatial pattern.

Animals↗
PubMed2006

Two-stage Turing model for generating pigment patterns on the leopard and the jaguar.

Based on the results of phylogenetic analysis, which showed that flecks are the primitive pattern of the felid family and all other patterns including rosettes and blotches develop from it, we construct a Turing reaction-diffusion model which generates spot patterns initially. Starting from this spotted pattern, we successfully generate patterns of adult leopards and jaguars by tuning parameters of the model in the subsequent phase of patterning.

Animals↗