Expression of spatially regulated genes in the sea urchin embryo

doi:10.1016/S0959-437X(05)80283-7

Current Opinion in Genetics & Development

Volume 2, Issue 2, 1992, Pages 260-268

https://doi.org/10.1016/S0959-437X(05)80283-7 Get rights and content

Spatially controlled genes expressed in the early sea urchin embryo have been characterized, and the patterns of expression in terms of the mechanisms by which this embryo accomplishes its initial set of founder cell specifications are the subject of current discussion. Sea urchin transcription factors that have been cloned are classified with respect to their target sites and the genes they regulate. Among the best known of the sea urchin cis-regulatory systems is that controlling expression of the Cyllla gene, which encodes an aboral ectoderm-specific cytoskeletal actin. The Cyllla regulatory domain includes approximately 20 sites of DNA-protein interaction, serviced by about ten different factors. Certain of these factors are known to negatively control spatial expression, while others positively regulate temporal activation and the level of Cyllla gene expression. Differential, lineage-specific gene expression is instituted in the sea urchin embryo by mid-late cleavage, prior to any cell migration or overt differentiation, and shortly following lineage segregation.

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Strongylocentrotus purpuratus Otx (SpOtx) is required simultaneously in sea urchin development for the activation of endo16 in the vegetal plate and for the activation of spec2a in the aboral ectoderm. Because Otx binding sites alone do not appear to be responsible for the spatially restricted expression of spec2a, additional DNA elements were sought. We show here that consensus Otx binding sites fused to basal promoters are sufficient to activate CAT reporter gene expression in all cell types, although expression in endomesoderm progenitors is enhanced. On the other hand, three non-Otx elements derived from the spec2a enhancer are needed together with Otx sites for specifically aboral ectoderm expression. A DNA element termed Y/CBF, lying just downstream from an Otx site within the spec2a enhancer, mediates general activation in the ectoderm. A second element lying between the Otx and Y/CBF sites, called OER, functions to prevent expression in the oral ectoderm. A third site, called ENR, overlapping another Otx site, is required to repress endoderm expression. Three distinct DNA binding proteins interact sequence specifically at the Y/CBF, OER, and ENR elements. The spec2a enhancer thus consists of closely linked activator and repressor elements that function collectively to cause expression of the spec2a gene in the aboral ectoderm.
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In embryos of indirectly developing echinoids, the secondary (oral–aboral) larval axis is established after fertilization by an as yet undiscovered process. One of the earliest manifestations of this axis is an asymmetry in mitochondrial respiration, with the prospective oral side of the embryo exhibiting a higher rate of respiration than the prospective aboral side. We show here that respiratory asymmetry can be experimentally induced within embryos by immobilizing them in tight clusters of four (“rosettes”). Within such clusters a redox gradient is established from the inside to the outside of the rosette. Vital staining of clustered embryos demonstrates that the side of the embryo facing the outside of the rosette (i.e., the most oxidizing) tends to become the oral side, while the side facing the inside tends to become the aboral side. Effective entrainment of the oral–aboral axis requires that the embryos remain immobilized in rosettes until the hatching blastula stage. To begin to investigate the molecular mechanisms underlying this effect we made use of P3A2, a transcriptional regulatory protein whose activity is spatially modulated along the oral–aboral axis. When synthetic mRNA encoding P3A2 fused to the VP16 activation domain is injected into eggs, it activates embryonic expression of a green fluorescent protein reporter gene containing a basal promoter and a single strong P3A2 target site. In embryo rosettes, such activation occurs predominantly on the outside of the rosette, suggesting that the activity of the P3A2 protein is spatially regulated by the respiratory asymmetry established by clustering the embryos. These findings are discussed with reference to earlier work on both oral–aboral axis specification and P3A2 and used to develop a testable model of the mechanism of oral–aboral axis specification in the sea urchin embryo.
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We discuss recent progress in understanding how cell fates are specified along the animal–vegetal axis of the sea urchin embryo. This process is initiated by cell-autonomous, maternally directed, mechanisms that establish three unique gene-regulatory domains. These domains are defined by distinct sets of vegetalizing (β-catenin) and animalizing transcription factor (ATF) activities and their region of overlap in the macromeres, which specifies these cells as early mesendoderm. Subsequent signaling among cleavage-stage blastomeres further subdivides fates of macromere progeny to yield major embryonic tissues. Zygotically produced Wnt8 reinforces maternally regulated levels of nuclear β-catenin in vegetal derivatives to down regulate ATF activity and further promote mesendoderm fates. Signaling through the Notch receptor from the vegetal micromere lineages diverts adjacent mesendoderm to secondary mesenchyme fates. Continued Wnt signaling expands the vegetal domain of β-catenin's transcriptional regulatory activity and competes with animal signaling factors, including BMP2/4, to specify the endoderm–ectoderm border within veg₁ progeny. This model places new emphasis on the importance of the ratio of maternally regulated vegetal and animal transcription factor activities in initial specification events along the animal–vegetal axis.
Comparative biochemical analysis of sea urchin peristome and rat tail tendon collagen
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We report here a biochemical comparison between type I rat tail tendon collagen and collagen isolated from sea urchin peristome tissue. The sea urchin collagen consisted of two species of apparent mol masses, 140 and 116 kDa. Amino acid compositional analysis of the 140 and 116 kDa species revealed the presence of hydroxyproline and hydroxylysine as well as a glycine content of 28.1 mol.%. In solubility experiments the rat tail tendon collagen was found to precipitate at sodium chloride concentrations between 1 and 2 M while peristome collagen remained soluble at salt concentrations as high as 4 M. Incubation of the peristome and rat tail tendon collagen preparations with a sea urchin collagenase/gelatinase resulted in cleavage of the former but not the latter collagen. Upon heat denaturation at 60°C, however, the rat tail tendon collagen served as a substrate for the gelatinase. Cyanogen bromide cleavage of rat tail and peristome collagens generated largely unique peptide maps. Collectively, these results suggest that structural differences exist between echinoderm and vertebrate type 1 collagens.
Expression of the actin gene family in embryos of the sea urchin Lytechinus pictus
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The genome of the sea urchinLytechinus pictusincludes genes encoding four cytoskeletal actins LpC1–4 and the muscle actin LpM. Gene-specific probes corresponding to 3′ noncoding termini have been used to characterize their patterns of expression byin situhybridization. The gene encoding LpC1 actin, which is most similar in sequence to theStrongylocentrotus purpuratusCyI actin, has a complex developmental profile of expression. LpC1 transcripts become prominent in the archenteron and secondary mesenchyme cells of embryos, as well as in adult testis and ovary. The LpC2 actin gene is predominantly expressed in aboral ectoderm of embryos, similarly to the pattern of expression of its closest relatives inS. purpuratus,the SpCyIIIa and SpCyIIIb actin genes. The LpC3 actin gene is expressed at low levels in secondary mesenchyme cells. The LpC4 actin gene is expressed in a subset of primary mesenchyme cells which may be actively engaged in skeletogenesis. Transcripts of the LpM gene accumulate in esophageal muscle cells beginning during gastrulation before overt differentiation. Each of theL. pictusactin genes has a distinct pattern of expression, none of which is identical to that of anyS. purpuratusactin gene. These results indicate that the regulation of expression of members of the actin gene family, even those likely to have common ancestors, has diverged as these sea urchin species diverged.
TwocisElements Collaborate to Spatially Repress Transcription from a Sea Urchin Promoter
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The expression pattern of many territory-specific genes in metazoan embryos is maintained by an active process of negative spatial regulation. However, the mechanism of this strategy of gene regulation is not well understood in any system. Here we show that reporter constructs containing regulatory sequence for theSM30-α gene ofStronglyocentrotus purpuratusare expressed in a pattern congruent with that of the endogenousSM30gene(s), largely as a result of active transcriptional repression in cell lineages in which the gene is not normally expressed. Chloramphenicol acetyl transferase assays of deletion constructs from the 2600-bp upstream region showed that repressive elements were present in the region from −1628 to −300.In situhybridization analysis showed that the spatial fidelity of expression was severely compromised when the region from −1628 to −300 was deleted. Two highly repetitive sequence motifs, (G/A/C)CCCCT and (T/C)(T/A/C)CTTTT(T/A/C), are present in the −1628 to −300 region. Representatives of these elements were analyzed by gel mobility shift experiments and were found to interact specifically with proteins in crude nuclear extracts. When oligonucleotides containing either sequence element were co-injected with a correctly regulated reporter as potential competitors, the reporter was expressed in inappropriate cells. When composite oligonucleotides, containing both sequence elements, were fused to a misregulated reporter, the expression of the reporter in inappropriate cells was suppressed. Comparison of composite oligonucleotides with oligonucleotides containing single constituent elements show that both sequence elements are required for effective spatial regulation. Thus, both individual elements are required, but only a composite element containing both elements is sufficient to function as a tissue-specific repressive element.

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Expression of spatially regulated genes in the sea urchin embryo

Development

J Biol Chem

Dev Biol

Development

Dev Biol

Dev Biol

Dev Biol

J Cell Biol

J Cell Biol

Genes Dev

Science

Genes Dev

Dev Biol

J Biol Chem

Dev Biol

Development

Dev Biol

Development

Genes Dev

Mol Marine Biol Biotech

J Biol Chem

Genes Dev

Spatial Mechanisms of Gene Regulation in Metazoan Embryos

Development

How Embryos Work: a Comparative View of Diverse Modes of Cell Fate Specification

Development

Lineage-Specific Gene Expression and the Regulative Capacities of the Sea urchin Embryo: a Proposed Mechanism

Development

Cell Type Specification During Sea Urchin Development

Trends Genet

Gene Activity in Early Development

Regulatory Elements from the Related Spec Genes of Strongylocentrotus purpuratus Yield Different Spatial Patterns with a lacZ Reporter Gene

Dev Biol

A Regulatory Domain that Directs Lineage-specific Expression of a Skeletal Matrix Protein Gene in the Sea Urchin Embryo

Gene Dev

Territorial Expression of Three Different trans-Genes in Early Sea Urchin Embryos by a Whole-Mount Fluorescence Procedure

Dev Biol

An Embryonic Enhancer Determines the Temporal Activation of a Sea Urchin Late H1 Gene

Mol Cell Biol