Sea urchin skeletogenesis

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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.

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]

References

  1. ^ a b c d e 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. ^ a b c Gilbert, Scott F. (2006). Developmental Biology: Eighth Edition. Sunderland, Massachusetts: Sinauer Associates, Inc. ISBN 0-87893-250-X.
  4. ^ a b 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.
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