Sea urchin skeletogenesis

Last updated

Skeletogenesis is a key morphogenetic event in the embryonic development of vertebrates and is of equal, although transient, importance in the development of the sea urchin, a marine invertebrate. [1] The larval sea urchin does not resemble its adult form, because the sea urchin is an indirect developer, meaning its larva form must undergo metamorphosis to form the juvenile adult. Here, the focus is on skeletogenesis in the sea urchin species Strongylocentrotus purpuratus , as this species has been most thoroughly studied and characterized.

Contents

Morphological changes

Skeletogenesis begins in the early sea urchin blastula (9–10 hours post fertilization) when the primary mesenchyme cells (PMCs), the sole descendants of the large micromere daughter cells, [2] undergo an epithelial–mesenchymal transition (EMT) and break away from the apical layer, thus entering the blastocoel, [3] forming a cell cluster at the vegetal pole. [1] It is a key interaction between the two principal populations of mesodermal cells in the sea urchin embryo, PMCs and secondary mesenchyme cells (SMCs), that regulates SMC fates and the process of skeletogenesis. In a wild type embryo, skeletal elements are exclusively produced by PMCs. [4] Due to their nature in giving rise to the larval skeleton, they are sometimes called the skeletogenic mesenchyme. [3] Certain SMCs have a skeletogenic potential, however, signals transmitted by the PMCs suppress this potential in the SMCs and direct these cells into alternative developmental pathways. [4]

Once in the blastocoel, the mesenchyme cells extend and contract long, thin processes called filopodia. The filopodia are 250 nm in diameter and 25 um long. At this point, the filopodia appear to move randomly along the surface of the inner blastocoel, making and breaking filopodial connections to the blastocoel wall. During the gastrula stage, once the blastopore has formed, the PMCs are localized within the prospective ventrolateral (from front to side) region of the blastocoel. It is here that they fuse into syncytial cables, forming the axis for the calcium carbonate (CaCO3) (and a small amount, 5%, of MgCO3) spicules of the larval skeletal rods, 13.5 hours post fertilization. [3] Both optical birefringence and X-ray diffraction indicated that the spicules are crystalline. [1] Upon reaching the pluteus stage (24 hours post fertilization), an abundance of extracellular matrix is also found associated with the syncytia and blastocoel wall. [1] From gastrula to pluteus stages the skeleton grows in both size and complexity. Once the organism undergoes metamorphosis to form the juvenile sea urchin, the larval skeleton is “lost”, making its existence critical yet seemingly transient in the overall life cycle of the sea urchin. [1] The skeleton of the pluteus does, however, give rise to the spines of the juvenile sea urchin. [5] These spines usually measure 1-3 centimeters in length and 1-2 millimeters thick, and in some species, may be poisonous.

Molecular regulation

The molecular mechanisms of skeletogenesis involve several PMC-specific gene products. These include Msp30, a sulfate cell-surface glycoprotein which has been implicated in calcium uptake and deposition, and SM50, SM30, and PM27 which are three proteins of the spicule matrix. SM50 and PM27 are thought to be structurally similar, nonglycosylated, basic proteins whereas SM30 is an acidic glycoprotein. The specific roles of these matrix proteins has yet to be fully elucidated, but it is thought that they may function in the nucleation or orientation of crystal growth. It has also been found that the msp130 gene exhibits a complex pattern of spatial regulation within the PMC syncytium during skeletogenesis. It is suggested that the ectoderm may play a role in controlling skeletal morphogenesis by regulating the expression of PMC-specific gene products involved in spicule biogenesis. [6]

Evolution

The extent to which the molecular mechanisms underlying skeletogenesis in larval sea urchins has been characterized has led to comparative evolutionary developmental studies in distantly-related sea urchins, as well as other echinoderms, with the aim of understanding how this character has evolved. [7] [8] These studies, and others, [9] [10] have revealed that numerous differences have arisen during the evolution of the sea urchin clade in spatiotemporal gene expression of several transcription factors comprising the gene regulatory network driving skeletogenic specification. However, there are also striking similarities in the signaling systems that position these cells in the embryo. [11] Despite differences in timing of mesodermal ingression into the blastocoel and spatiotemporal differences in transcription factor gene expression, ancestral state reconstruction of genes critical to the specification of sea urchin skeletogenic cells supports the homology of this cell type, [12] suggesting it arose some time before the divergence of cidaroids and euechinoids over 268 million years ago. [13]

Related Research Articles

<span class="mw-page-title-main">Sea urchin</span> Class of marine invertebrates

Sea urchins are spiny, globular echinoderms in the class Echinoidea. About 950 species of sea urchin are distributed on the seabeds of every ocean and inhabit every depth zone from the intertidal seashore down to 5,000 meters. The spherical, hard shells (tests) of sea urchins are round and covered in spines. Most urchin spines range in length from 3 to 10 cm, with outliers such as the black sea urchin possessing spines as long as 30 cm (12 in). Sea urchins move slowly, crawling with tube feet, and also propel themselves with their spines. Although algae are the primary diet, sea urchins also eat slow-moving (sessile) animals. Predators that eat sea urchins include a wide variety of fish, starfish, crabs, marine mammals, and humans.

<span class="mw-page-title-main">Blastulation</span> Sphere of cells formed during early embryonic development in animals

Blastulation is the stage in early animal embryonic development that produces the blastula. In mammalian development the blastula develops into the blastocyst with a differentiated inner cell mass and an outer trophectoderm. The blastula is a hollow sphere of cells known as blastomeres surrounding an inner fluid-filled cavity called the blastocoel. Embryonic development begins with a sperm fertilizing an egg cell to become a zygote, which undergoes many cleavages to develop into a ball of cells called a morula. Only when the blastocoel is formed does the early embryo become a blastula. The blastula precedes the formation of the gastrula in which the germ layers of the embryo form.

<span class="mw-page-title-main">Gastrulation</span> Stage in embryonic development in which germ layers form

Gastrulation is the stage in the early embryonic development of most animals, during which the blastula, or in mammals the blastocyst, is reorganized into a two-layered or three-layered embryo known as the gastrula. Before gastrulation, the embryo is a continuous epithelial sheet of cells; by the end of gastrulation, the embryo has begun differentiation to establish distinct cell lineages, set up the basic axes of the body, and internalized one or more cell types including the prospective gut.

<span class="mw-page-title-main">Blastocoel</span> Fluid-filled or yolk-filled cavity that forms in the blastula

The blastocoel, also spelled blastocoele and blastocele, and also called cleavage cavity, or segmentation cavity is a fluid-filled or yolk-filled cavity that forms in the blastula during very early embryonic development. At this stage in mammals the blastula develops into the blastocyst containing an inner cell mass, and outer trophectoderm.

<span class="mw-page-title-main">GLI2</span> Protein-coding gene in the species Homo sapiens

Zinc finger protein GLI2 also known as GLI family zinc finger 2 is a protein that in humans is encoded by the GLI2 gene. The protein encoded by this gene is a transcription factor.

<span class="mw-page-title-main">Lateral plate mesoderm</span>

The lateral plate mesoderm is the mesoderm that is found at the periphery of the embryo. It is to the side of the paraxial mesoderm, and further to the axial mesoderm. The lateral plate mesoderm is separated from the paraxial mesoderm by a narrow region of intermediate mesoderm. The mesoderm is the middle layer of the three germ layers, between the outer ectoderm and inner endoderm.

<span class="mw-page-title-main">Paraxial mesoderm</span>

Paraxial mesoderm, also known as presomitic or somitic mesoderm, is the area of mesoderm in the neurulating embryo that flanks and forms simultaneously with the neural tube. The cells of this region give rise to somites, blocks of tissue running along both sides of the neural tube, which form muscle and the tissues of the back, including connective tissue and the dermis.

<span class="mw-page-title-main">Apical ectodermal ridge</span>

The apical ectodermal ridge (AER) is a structure that forms from the ectodermal cells at the distal end of each limb bud and acts as a major signaling center to ensure proper development of a limb. After the limb bud induces AER formation, the AER and limb mesenchyme—including the zone of polarizing activity (ZPA)—continue to communicate with each other to direct further limb development.

<span class="mw-page-title-main">Mesenchyme</span> Type of animal embryonic connective tissue

Mesenchyme is a type of loosely organized animal embryonic connective tissue of undifferentiated cells that give rise to most tissues, such as skin, blood or bone. The interactions between mesenchyme and epithelium help to form nearly every organ in the developing embryo.

In the field of developmental biology, regional differentiation is the process by which different areas are identified in the development of the early embryo. The process by which the cells become specified differs between organisms.

The scleraxis protein is a member of the basic helix-loop-helix (bHLH) superfamily of transcription factors. Currently two genes have been identified to code for identical scleraxis proteins.

<i>Strongylocentrotus purpuratus</i> Species of sea urchin

Strongylocentrotus purpuratus is a species of sea urchin in the family Strongylocentrotidae commonly known as the purple sea urchin. It lives along the eastern edge of the Pacific Ocean extending from Ensenada, Mexico, to British Columbia, Canada. This sea urchin species is deep purple in color, and lives in lower inter-tidal and nearshore sub-tidal communities. Its eggs are orange when secreted in water. January, February, and March function as the typical active reproductive months for the species. Sexual maturity is reached around two years. It normally grows to a diameter of about 10 cm (4 inches) and may live as long as 70 years.

<span class="mw-page-title-main">Homeobox protein goosecoid</span> Protein-coding gene in the species Homo sapiens

Homeobox protein goosecoid(GSC) is a homeobox protein that is encoded in humans by the GSC gene. Like other homeobox proteins, goosecoid functions as a transcription factor involved in morphogenesis. In Xenopus, GSC is thought to play a crucial role in the phenomenon of the Spemann-Mangold organizer. Through lineage tracing and timelapse microscopy, the effects of GSC on neighboring cell fates could be observed. In an experiment that injected cells with GSC and observed the effects of uninjected cells, GSC recruited neighboring uninjected cells in the dorsal blastopore lip of the Xenopus gastrula to form a twinned dorsal axis, suggesting that the goosecoid protein plays a role in the regulation and migration of cells during gastrulation.

<span class="mw-page-title-main">Cytoneme</span>

Cytonemes are thin, cellular projections that are specialized for exchange of signaling proteins between cells. Cytonemes emanate from cells that make signaling proteins, extending directly to cells that receive signaling proteins. Cytonemes also extend directly from cells that receive signaling proteins to cells that make them.

<i>Eucidaris tribuloides</i> Species of echinoderm

Eucidaris tribuloides, the slate pencil urchin, is a species of cidaroid sea urchins that inhabits littoral regions of the Atlantic Ocean. As a member of the basal echinoid order Cidaroida, its morphological, developmental and molecular genetic characteristics make it a phylogenetically interesting species.

<span class="mw-page-title-main">Ingression (biology)</span>

Ingression is one of the many changes in the location or relative position of cells that takes place during the gastrulation stage of embryonic development. It produces an animal's mesenchymal cells at the onset of gastrulation. During the epithelial–mesenchymal transition (EMT), the primary mesenchyme cells (PMCs) detach from the epithelium and become internalized mesenchyme cells that can migrate freely.

<span class="mw-page-title-main">MYF5</span> Protein-coding gene in the species Homo sapiens

Myogenic factor 5 is a protein that in humans is encoded by the MYF5 gene. It is a protein with a key role in regulating muscle differentiation or myogenesis, specifically the development of skeletal muscle. Myf5 belongs to a family of proteins known as myogenic regulatory factors (MRFs). These basic helix loop helix transcription factors act sequentially in myogenic differentiation. MRF family members include Myf5, MyoD (Myf3), myogenin, and MRF4 (Myf6). This transcription factor is the earliest of all MRFs to be expressed in the embryo, where it is only markedly expressed for a few days. It functions during that time to commit myogenic precursor cells to become skeletal muscle. In fact, its expression in proliferating myoblasts has led to its classification as a determination factor. Furthermore, Myf5 is a master regulator of muscle development, possessing the ability to induce a muscle phenotype upon its forced expression in fibroblastic cells.

Margaret Buckingham, is a British developmental biologist working in the fields of myogenesis and cardiogenesis. She is an honorary professor at the Pasteur Institute in Paris and emeritus director in the Centre national de la recherche scientifique (CNRS). She is a member of the European Molecular Biology Organization, the Academia Europaea and the French Academy of Sciences.

<span class="mw-page-title-main">TBX15</span> Human protein and coding gene

T-box transcription factor TBX15 is protein that is encoded in humans by the Tbx15 gene, mapped to Chromosome 3 in mice and Chromosome 1 in humans. Tbx15 is a transcription factor that plays a key role in embryonic development. Like other members of the T-box subfamily, Tbx15 is expressed in the notochord and primitive streak, where it assists with the formation and differentiation of the mesoderm. It is steadily downregulated after segmentation of the paraxial mesoderm.

Fred Huffman Wilt is an American biologist who was elected a Fellow of the American Association for the Advancement of Science. His research currently includes the endoskeletal spicule of sea urchin embryos, and its biomineralization relative to its cellular and molecular foundation.

References

  1. 1 2 3 4 5 Decker GL, Lennarz WJ. (1988). "Skeletogenesis in the sea urchin embryo". Development. 103 (2): 231–247. doi:10.1242/dev.103.2.231. PMID   3066610.
  2. ↑ Ettensohn CA. (1992). "Cell interactions and mesodermal cell fates in the sea urchin embryo". Dev. Suppl.: 43–51. PMID   1299367.
  3. 1 2 3 Gilbert, Scott F. (2006). Developmental Biology: Eighth Edition. Sunderland, Massachusetts: Sinauer Associates, Inc. ISBN   0-87893-250-X.
  4. 1 2 Ettensohn CA, Ruffins SW. (1993). "Mesodermal cell interactions in the sea urchin embryo: properties of skeletogenic secondary mesenchyme cells". Development. 117 (4): 1275–1285. doi:10.1242/dev.117.4.1275. PMID   8404530.
  5. ↑ "SUE - P2M Animation".
  6. ↑ Guss KA, Ettensohn CA. (1997). "Skeletal morphogenesis in the sea urchin embryo: regulation of primary mesenchyme gene expression and skeletal rod growth by ectoderm-derived cues". Development. 124 (10): 1899–1908. doi: 10.1242/dev.124.10.1899 . PMID   9169837.
  7. ↑ Erkenbrack EM, Davidson EH. (2015). "Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses". Proceedings of the National Academy of Sciences USA. 112 (30): E4075-84. Bibcode:2015PNAS..112E4075E. doi: 10.1073/pnas.1509845112 . PMC   4522742 . PMID   26170318.
  8. ↑ Thompson, Jeffrey R.; Petsios, Elizabeth; Davidson, Eric H.; Erkenbrack, Eric M.; Gao, Feng; Bottjer, David J. (2015-10-21). "Reorganization of sea urchin gene regulatory networks at least 268 million years ago as revealed by oldest fossil cidaroid echinoid". Scientific Reports. 5: 15541. Bibcode:2015NatSR...515541T. doi:10.1038/srep15541. ISSN   2045-2322. PMC   4614444 . PMID   26486232.
  9. ↑ Erkenbrack, E. M.; Ako-Asare, K.; Miller, E.; Tekelenburg, S.; Thompson, J. R.; Romano, L. (2016). "Ancestral state reconstruction by comparative analysis of a GRN kernel operating in echinoderms". Development Genes and Evolution. 226 (1): 37–45. doi:10.1007/s00427-015-0527-y. ISSN   0949-944X. PMID   26781941. S2CID   6067524.
  10. ↑ Erkenbrack, E. M.; Davidson, E. H.; Peter, I. S. (2018). "Conserved regulatory state expression controlled by divergent developmental gene regulatory networks in echinoids". Development. 145 (24): dev167288. doi:10.1242/dev.167288. ISSN   0950-1991. PMC   6307887 . PMID   30470703.
  11. ↑ Erkenbrack, E. M.; Petsios, E. (2017). "A conserved role for VEGF signaling in specification of homologous mesenchymal cell types positioned at spatially distinct developmental addresses in early development of sea urchins". Journal of Experimental Zoology Part B. 328 (5): 423–432. doi: 10.1002/jez.b.22743 . ISSN   1552-5015. PMID   28544452.
  12. ↑ Erkenbrack, E. M.; Thompson, J. R. (2019). "Cell type phylogenetics informs the evolutionary origin of echinoderm larval skeletogenic cell identity". Communications Biology. 2: 160. doi:10.1038/s42003-019-0417-3. ISSN   2399-3642. PMC   6499829 . PMID   31069269.
  13. ↑ Thompson, J. R.; Erkenbrack, E. M.; Hinman, V. F.; McCauley, B. R.; Petsios, E.; Bottjer, D. J. (2017). "Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins". Proceedings of the National Academy of Sciences USA. 114 (23): 5870–5877. Bibcode:2017PNAS..114.5870T. doi: 10.1073/pnas.1610603114 . ISSN   1091-6490. PMC   5468677 . PMID   28584090.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.