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PubMed2003

Novel regulatory sequence -82/-62 functions as a key element to drive the somite-specificity of zebrafish myf-5.

Myf-5, a transcription factor that controls muscle differentiation, is expressed in somites during early embryogenesis. However, gene regulation of myf-5 is poorly understood and detailed functional analysis of the regulatory cis-elements is needed. In zebrafish, the myf-5 upstream sequence from -82 to -62 (-82/-62) was fused with a basal promoter and transferred to fertilized zebrafish eggs. The -82/-62 cassette drove green fluorescent protein (GFP) reporter gene expression specifically in the somites. Moreover, GFP signals were detected exclusively in the somites of 28-hpf embryos derived from eggs injected with pCMV-5x(-82/-62), which contained five copies of the -82/-62 cassette inserted within cytomegalovirus promoter/enhancer. Thus, the -82/-62 cassette, conserved in mouse myf-5, functions to drive somite-specific expression and to repress nonspecific expression during the early development of zebrafish embryos. Mutated sequence analysis of -82/-62 cassette showed that the -70/-62 sequence was the key element for controlling myf-5 specificity. The putative CCAAT-like box, located at -66/-62, could not direct somite-specific expression. A DNA-protein complex was specifically formed between the -70/-62 probe and embryonic nuclear extracts. We conclude that the -70/-62 motif is essential for controlling somite-specific expression and the CCAAT-like box is essential for activating gene transcription.

Animals↗
PubMed2005

Cells of all somitic compartments are determined with respect to segmental identity.

Development of somite cells is orchestrated by two regulatory processes. Differentiation of cells from the various somitic compartments into different anlagen and tissues is regulated by extrinsic signals from neighboring structures such as the notochord, neural tube, and surface ectoderm. Morphogenesis of these anlagen to form specific structures according to the segmental identity of each somite is specified by segment-specific positional information, based on the Hox-code. It has been shown that following experimental rotation of presomitic mesoderm or newly formed somites, paraxial mesodermal cells adapt to the altered signaling environment and differentiate according to their new orientation. In contrast, presomitic mesoderm or newly formed somites transplanted to different segmental levels keep their primordial segmental identity and form ectopic structures according to their original position. To determine whether all cells of a segment, including the dorsal and ventral compartment, share the same segmental identity, presomitic mesoderm or newly formed somites were rotated and transplanted from thoracic to cervical level. These experiments show that cells from all compartments of a segment are able to interpret extrinsic local signals correctly, but form structures according to their original positional information and maintain their original Hox expression in the new environment.

Animals↗
PubMed1998

Apoptosis of epaxial myotome in Danforth's short-tail (Sd) mice in somites that form following notochord degeneration.

Danforth's short-tail (Sd) mouse is a semidominant mutation that prevents completion of notochord development. In homozygous mutant mice, the notochord completely degenerates at embryonic day 9.5 (E9. 5), whereas the neural tube and somites continue to form, permitting analysis of somite development in the absence of inductive signals from the notochord and floor plate. In the somites formed after notochord degeneration, Myf5 expression initiates in a normal temporal sequence, but instead of the normal restriction to the dorsomedial somite, its expression extends into the ventral somite. MyoD, myogenin, and myosin heavy chain are normally expressed in the ventral myotome and there is normal development of hypaxial muscles. In contrast, subsequent to initial Myf5 expression, muscle gene expression was not detected in the dorsal myotome and a high level of apoptosis was observed with significantly decreased formation of epaxial muscles. The apoptosis of epaxial muscle in somites that formed after notochord degeneration is consistent with a role for the notochord in the survival and differentiation of the dorsal myotome.

Animals↗
PubMed2002

Localized BMP4-noggin interactions generate the dynamic patterning of noggin expression in somites.

Interactions between BMP4 and its inhibitor, noggin, regulate patterning of somites and neural crest. During mesoderm development, noggin mRNA is expressed in the intermediate mesoderm. Upon segmentation, it is detected in the lateral portion of epithelial somites becoming progressively medialized as they mature. In dissociated segments, noggin becomes transiently confined to the dorsomedial lip of the dermomyotome. Here, we investigated the factor(s) that control this lateral-to-medial shift in transcription of somitic noggin. Inhibition of BMP activity in the caudal lateral plate/intermediate mesoderm prevented noggin transcription in the lateral somite. Further rostrally (or later in development), inhibition of tube-derived BMP, but not of Wnt activity, prevented initial noggin expression in the dorsomedial lip of the dermomyotome. Moreover, BMP4 was sufficient to trigger initial expression of noggin even in the absence of ectoderm and/or neural tube, suggesting a direct action on the dorsomedial somite. Thus, the patterns of noggin transcription in somites are directly regulated by BMP4 activities emanating first from the mesoderm and later from the neural tube. Expression patterns of BMP4 and of type IA BMP receptors are spatiotemporally compatible with this lateral-to-medial shift. These results highlight the existence in the neural tube-mesoderm complex of a regulatory loop by which BMP positively regulates transcription of noggin, which in turn represses further ligand activity.

Animals↗
PubMed2005

Expression of a novel somite-formation-related gene, AmphiSom, during amphioxus development.

A novel gene, AmphiSom, was identified in amphioxus Branchiostoma belcheri tsingtauense. Its sequence and developmental expression pattern were determined. AmphiSom transcripts were first detected in the presomitic mesoderm at the late gastrula stage and reached the highest level in the forming and nascent somites in neurulae. However, the expression of AmphiSom was rapidly down-regulated after somites were formed. It was maintained in the most anterior somite and most posterior somite at neurula stages. By 48 h, AmphiSom transcripts were detected only in the developing tail bud but were no longer detected in 72-h larva. Our data demonstrated that the AmphiSom gene is expressed during the development of somites in amphioxus and could play a role in somite formation.

Animals↗
PubMed2004

A proliferative role for Wnt-3a in chick somites.

The proper patterning of somites to give rise to sclerotome, dermomyotome, and myotome involves the coordination of many different cellular processes, including lineage specification, cell proliferation, cell death, and differentiation, by intercellular signals. One such family of secreted signaling proteins known to influence somite patterning is the Wnt family. Although the participation of Wnt-3a in the patterning of dorsal structures in the somite is well established, no clear consensus has emerged about the cellular processes that are governed by Wnt-3a in the somite. The recent demonstration that Wnt-3a has a proliferative role in the neural tube [Development 129 (2002) 2087] suggested that Wnt-3a might also act to regulate proliferation in somites. To test this hypothesis, we first analyzed the effects of Wnt-3a on segmental plate and somite explants (from Hamburger and Hamilton stage 10 chick embryos) grown in culture. These studies indicate that Wnt-3a is capable of maintaining and/or inducing expression of both Pax-3 and Pax-7, transcription factors that have been implicated in proliferation. To directly test for a role in proliferation, explants were immunostained with antibodies against phospho-histone H3. Explants treated with Wnt-3a show an increase in the percentage of cells expressing phospho-histone H3 as compared to controls. To test the proliferative effect of Wnt-3a in vivo, we ectopically expressed Wnt-3a in chick neural tubes via electroporation. Consistent with previous studies, ectopic expression of Wnt-3a in vivo results in a mediolateral expansion of the dermomyotome and myotome. We now show that proliferation of dorsal/dermomyotomal cells is significantly enhanced by ectopic Wnt-3a. Collectively, our explant and in vivo studies indicate that an increase in proliferation plays an important role in the expansion of the dermomyotome and myotome in Wnt-3a-treated embryos. Furthermore, our results demonstrate that small changes in proliferation can dramatically influence patterning and morphogenesis.

Animals↗
PubMed2003

Contribution of somitic cells to the avian ribs.

The traditional view that all parts of the ribs originate from the sclerotome of the thoracic somites has recently been challenged by an alternative view suggesting that only the proximal rib derives from the sclerotome, while the distal rib arises from regions of the dermomyotome. In view of this continuing controversy and to learn more about the cell interactions during rib morphogenesis, this study aimed to reveal the precise contributions made by somitic cells to the ribs and associated tissues of the thoracic cage. A replication-deficient lacZ-encoding retrovirus was utilized to label cell populations within distinct regions of somites 19-26 in stage 13-18 chick embryos. Analysis of the subsequent contributions made by these cells revealed that the thoracic somites are the sole source of cells for the ribs. More precisely, it is the sclerotome compartment of the somites that contributes cells to both the proximal and distal elements of the ribs, confirming the traditional view of the origin of the ribs. Results also indicate that the precursor cells of the ribs and intercostal muscles are intimately associated within the somite, a relationship that may be essential for proper rib morphogenesis. Finally, the data from this study also show that the distal ribs are largely subject to resegmentation, although cell mixing may occur at the most sternal extremities.

Animals↗
PubMed1998

Role of growth factors in shaping the developing somite.

In the vertebrate embryo, the lateral somite gives rise to limb bud and body wall muscles whereas the medial somite generates the axial musculature. We show that in chick embryos, this polarity along the medio-lateral axis is achieved through the antagonistic influences of the lateral plate and the medial neural tube. Bone morphogenetic protein 4 (BMP4) mediates the lateralising signal delivered by the lateral plate and is counteracted locally by Noggin expressed in the medial dermomyotome; Noggin expression in the somite is regulated by the Wntl protein which is expressed in the dorsal neural tube and mediates the medialising effect of the neural tube. Therefore, somite medio-lateral patterning results from a signalling cascade in which Wnt1 produced by the neural tube promotes noggin expression in the medial somite which in turn antagonises lateral plate-derived BMP4. This mechanism could lead to the establishment of a BMP4 activity gradient that would produce appropriate BMP4 signalling to generate medial and lateral somite patterning.

Animals↗
PubMed2000

The developmental fate of the rostral/caudal half of a somite for vertebra and rib formation: experimental confirmation of the resegmentation theory using chick-quail chimeras.

To determine whether resegmentation of somites forms the axial skeleton, we traced the development of the rostral and the caudal half of a somite during skeletogenesis in chick-quail chimeras by replacing the rostral or caudal half of a newly formed chick somite with that of a quail somite. The rostral half-somite transplant formed the caudal half of the vertebral body, the entire spinous process and the distal rib, while the caudal half-somite transplant formed the rostral half of vertebral body, the rostral half of spinous process, the vertebral arch, the transverse process and the entire rib. These findings confirm the resegmentation theory except the spinous process and the distal rib.

Animals↗
PubMed2003

The lateral somitic frontier: dorso-ventral aspects of anterio-posterior regionalization in avian embryos.

Patterning events along the anterior-posterior (AP) axis of vertebrate embryos result in the distribution of muscle and bone forming a highly effective functional system. A key aspect of regionalized AP patterning results from variation in the migratory pattern of somite cells along the dorsal-ventral (DV) axis of the body. This occurs as somite cell populations expand around the axis or migrate away from the dorsal midline and cross into the lateral plate. The fate of somitic cells has been intensely studied and many details have been reported about inductive signaling from other tissues that influence somite cell fate and behavior. We are interested in understanding the specific differences between somites in particular AP regions and how these differences contribute to the global pattern of the organism. Using orthotopic transplants of segmental plate between quail and chick embryos, we have mapped the interface of the somitic and lateral plate mesoderm during the formation of the body wall in cervical and thoracic regions. This interface does not change dramatically in the mid-cervical region, but undergoes extensive changes in the thoracic region. Based on this regional mapping and consistent with the extensive literature, we suggest a revised method of classifying regions of the body wall that relies on embryonic cell lineages rather than adult functional criteria.

Animals↗
PubMed2002

Cell dynamics during somite boundary formation revealed by time-lapse analysis.

We follow somite segmentation in living chick embryos and find that the shaping process is not a simple periodic slicing of tissue blocks but a much more carefully choreographed separation in which the somite pulls apart from the segmental plate. Cells move across the presumptive somite boundary and violate gene expression boundaries thought to correlate with the site of the somite boundary. Similarly, cells do not appear to be preassigned to a given somite as they leave the node. The results offer a detailed picture of somite shaping and provide a spatiotemporal framework for linking gene expression with cell movements.

Animals↗
PubMed2003

Myf5 expression in somites and limb buds of mouse embryos is controlled by two distinct distal enhancer activities.

The initiation of skeletal muscle development in the mouse embryo is strictly associated with the expression of the muscle-specific transcription factor Myf5, the first of four myogenic regulatory factors (MRFs) to be expressed in muscle progenitors, and ablation of the Myf5 gene prevents myogenesis. The complex spatiotemporal expression pattern of Myf5 depends on many discrete regulatory elements that are dispersed over long distances throughout the gene locus. These multiple control modules act differently in the various muscle precursor populations, presumably in response to diverse signals that control myogenesis. A potent enhancer region regulating Myf5 expression in limb muscles and somites has been identified previously at -58/-48 kb upstream of the transcriptional start site (Hadchouel et al., 2000). Here, we focus on the physical and functional dissection of this control region. We demonstrate that a conserved sequence of 270 bp located around -57 kb is required and sufficient to drive Myf5 expression in limbs and to maintain it in somites. A second enhancer nearby is responsible for Myf5 transcription in occipital/cranial somites. This enhancer activity also directs expression accurately to the myotome, preventing ectopic expression in the dermomyotome during the second phase of Myf5 gene activation in somites. Our data suggest that the enhancer identified here collaborates with other somitic enhancers to ensure correct myotomal Myf5 expression. Moreover, it constitutes an important element that mediates somitic expression after the initial and transient Myf5 activation through a previously described sonic hedgehog-dependent early epaxial enhancer.

Animals↗
PubMed2005

beta-Catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of paraxis.

The regulation of cell adhesion in epithelia is a fundamental process governing morphogenesis in embryos and a key step in the progression of invasive cancers. Here, we have analysed the molecular pathways controlling the epithelial organisation of somites. Somites are mesodermal epithelial structures of vertebrate embryos that undergo several changes in cell adhesion during early embryonic life. We show that Wnt6 in the ectoderm overlaying the somites, but not Wnt1 in the neighbouring neural tube, is the most likely candidate molecule responsible for the maintenance of the epithelial structure of the dorsal compartment of the somite: the dermomyotome. We characterised the signalling pathway that mediates Wnt6 activity. Our experiments suggest that the Wnt receptor molecule Frizzled7 probably transduces the Wnt6 signal. Intracellularly, this leads to the activation of the beta-catenin/LEF1-dependent pathway. Finally, we demonstrate that the bHLH transcription factor paraxis, which was previously shown to be a major player in the epithelial organisation of somites, is a target of the beta-catenin signal. We conclude that beta-catenin activity, initiated by Wnt6 and mediated by paraxis, is required for the maintenance of the epithelial structure of somites.

Animals↗
PubMed2006

Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk.

We have previously shown that endothelial cells of the aortic floor give rise to hematopoietic cells, revealing the existence of an aortic hemangioblast. It has been proposed that the restriction of hematopoiesis to the aortic floor is based on the existence of two different and complementary endothelial lineages that form the vessel: one originating from the somite would contribute to the roof and sides, another from the splanchnopleura would contribute to the floor. Using quail/chick orthotopic transplantations of paraxial mesoderm, we have traced the distribution of somite-derived endothelial cells during aortic hematopoiesis. We show that the aortic endothelium undergoes two successive waves of remodeling by somitic cells: one when the aortae are still paired, during which the initial roof and sides of the vessels are renewed; and a second, associated to aortic hematopoiesis, in which the hemogenic floor is replaced by somite endothelial cells. This floor thus appears as a temporary structure, spent out and replaced. In addition, the somite contributes to smooth muscle cells of the aorta. In vivo lineage tracing experiments with non-replicative retroviral vectors showed that endothelial cells do not give rise to smooth muscle cells. However, in vitro, purified endothelial cells acquire smooth muscle cells characteristics. Taken together, these data point to the crucial role of the somite in shaping the aorta and also give an explanation for the short life of aortic hematopoiesis.

Animals↗
PubMed1997

Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning.

In the vertebrate embryo, the lateral compartment of the somite gives rise to muscles of the limb and body wall and is patterned in response to lateral-plate-derived BMP4. Activation of the myogenic program distinctive to the medial somite, i.e. relatively immediate development of the epaxial muscle lineage, requires neutralization of this lateral signal. We have analyzed the properties of molecules likely to play a role in opposing lateral somite specification by BMP4. We propose that the BMP4 antagonist Noggin plays an important role in promoting medial somite patterning in vivo. We demonstrate that Noggin expression in the somite is under the control of a neural-tube-derived factor, whose effect can be mimicked experimentally by Wnt1. Wnt1 is appropriately expressed in the neural tube. Furthermore, we show that Sonic Hedgehog is able to activate ectopic expression of Noggin resulting in the blocking of BMP4 specification of the lateral somite. Our results are consistent with a model in which Noggin activation lies downstream of the SHH and Wnt signaling pathways.

Animals↗
PubMed2000

Anteroposterior patterning is required within segments for somite boundary formation in developing zebrafish.

Somite formation involves the establishment of a segmental prepattern in the presomitic mesoderm, anteroposterior patterning of each segmental primordium and formation of boundaries between adjacent segments. How these events are co-ordinated remains uncertain. In this study, analysis of expression of zebrafish mesp-a reveals that each segment acquires anteroposterior regionalisation when located in the anterior presomitic mesoderm. Thus anteroposterior patterning is occurring after the establishment of a segmental prepattern in the paraxial mesoderm and prior to somite boundary formation. Zebrafish fss(-), bea(-), des(-) and aei(-) embryos all fail to form somites, yet we demonstrate that a segmental prepattern is established in the presomitic mesoderm of all these mutants and hox gene expression shows that overall anteroposterior patterning of the mesoderm is also normal. However, analysis of various molecular markers reveals that anteroposterior regionalisation within each segment is disturbed in the mutants. In fss(-), there is a loss of anterior segment markers, such that all segments appear posteriorized, whereas in bea(-), des(-) and aei(-), anterior and posterior markers are expressed throughout each segment. Since somite formation is disrupted in these mutants, correct anteroposterior patterning within segments may be a prerequisite for somite boundary formation. In support of this hypothesis, we show that it is possible to rescue boundary formation in fss(-) through the ectopic expression of EphA4, an anterior segment marker, in the paraxial mesoderm. These observations indicate that a key consequence of the anteroposterior regionalisation of segments may be the induction of Eph and ephrin expression at segment interfaces and that Eph/ephrin signalling subsequently contributes to the formation of somite boundaries.

Amino Acid Sequence↗
PubMed2001

The role of presenilin 1 during somite segmentation.

The Notch signalling pathway plays essential roles during the specification of the rostral and caudal somite halves and subsequent segmentation of the paraxial mesoderm. We have re-investigated the role of presenilin 1 (Ps1; encoded by Psen1) during segmentation using newly generated alleles of the Psen1 mutation. In Psen1-deficient mice, proteolytic activation of Notch1 was significantly affected and the expression of several genes involved in the Notch signalling pathway was altered, including Delta-like3, Hes5, lunatic fringe (Lfng) and Mesp2. Thus, Ps1-dependent activation of the Notch pathway is essential for caudal half somite development. We observed defects in Notch signalling in both the caudal and rostral region of the presomitic mesoderm. In the caudal presomitic mesoderm, Ps1 was involved in maintaining the amplitude of cyclic activation of the Notch pathway, as represented by significant reduction of Lfng expression in Psen1-deficient mice. In the rostral presomitic mesoderm, rapid downregulation of the Mesp2 expression in the presumptive caudal half somite depends on Ps1 and is a prerequisite for caudal somite half specification. Chimaera analysis between Psen1-deficient and wild-type cells revealed that condensation of the wild-type cells in the caudal half somite was concordant with the formation of segment boundaries, while mutant and wild-type cells intermingled in the presomitic mesoderm. This implies that periodic activation of the Notch pathway in the presomitic mesoderm is still latent to segregate the presumptive rostral and caudal somite. A transient episode of Mesp2 expression might be needed for Notch activation by Ps1 to confer rostral or caudal properties. In summary, we propose that Ps1 is involved in the functional manifestation of the segmentation clock in the presomitic mesoderm.

Alleles↗
PubMed2002

Segmental relationship between somites and vertebral column in zebrafish.

The segmental heritage of all vertebrates is evident in the character of the vertebral column. And yet, the extent to which direct translation of pattern from the somitic mesoderm and de novo cell and tissue interactions pattern the vertebral column remains a fundamental, unresolved issue. The elements of vertebral column pattern under debate include both segmental pattern and anteroposterior regional specificity. Understanding how vertebral segmentation and anteroposterior positional identity are patterned requires understanding vertebral column cellular and developmental biology. In this study, we characterized alignment of somites and vertebrae, distribution of individual sclerotome progeny along the anteroposterior axis and development of the axial skeleton in zebrafish. Our clonal analysis of zebrafish sclerotome shows that anterior and posterior somite domains are not lineage-restricted compartments with respect to distribution along the anteroposterior axis but support a 'leaky' resegmentation in development from somite to vertebral column. Alignment of somites with vertebrae suggests that the first two somites do not contribute to the vertebral column. Characterization of vertebral column development allowed examination of the relationship between vertebral formula and expression patterns of zebrafish Hox genes. Our results support co-localization of the anterior expression boundaries of zebrafish hoxc6 homologs with a cervical/thoracic transition and also suggest Hox-independent patterning of regionally specific posterior vertebrae.

Animals↗