Echinoderms as Blueprints for Biocalcification: Regulation of Skeletogenic Genes and Matrices

Abstract

Echinoderms have an extensive endoskeleton composed of magnesian calcite, a form of calcium carbonate that contains small amounts of magnesium carbonate and occluded matrix proteins. Adult sea urchins have several calcified structures, including test, teeth, and spines, composed of numerous ossicles which form a three-dimensional meshwork of mineral trabeculae, the stereom. The biomineral development begins in 24-hour-old embryos within the primary mesenchyme cells (PMCs), the only cells producing a set of necessary matrix proteins. The deposition of the biomineral occurs in a privileged extracellular space produced by the fused filopodial processes of the PMCs. We showed for the first time that signals from ectoderm cells overlying PMCs play an important role in the regulation of biomineralization-related genes. It is believed that growth factors are produced by ectoderm cells and released into the blastocoel where they interact with cognate receptor tyrosine kinases restricted to PMCs, which activate signaling cascades regulating the expression of biomineralization-related genes. We demonstrated the implication of a TGF-beta family factor by a perturbation model in which skeleton elongation was indirectly blocked by monoclonal antibodies to an extracellular matrix (ECM) protein located on the apical surface of ectoderm. Thus, it was inferred that interfering with the binding of the ECM ligand, a member of the discoidin family, to its cell surface receptor, a βC integrin, disrupts the ectodermal cell signaling cascade, resulting in reduced or aberrant skeletons. During the last few years, we analyzed the expression of biomineralization-related genes in other examples of experimentally induced skeleton malformations, produced by the exposure to toxic metals, such as Cd and Mn or ionizing radiations, such as UV-B and X-rays. Besides the obvious toxicological implication, since the mis-expression of spicule matrix genes paralleled skeleton defects, we believe that by means of these studies we can dissect the molecular steps taking place and possibly understand the physiological events regulating embryonic biomineralization.

The Skeleton of Postmetamorphic Echinoderms in a Changing World

“…Very little is known about cell signaling and proteins involved in biomineralization in postmetamorphic echinoderms (Killian and Wilt, 2008;Matranga et al, 2011). In contrast, biomineralization control in sea urchin embryos and larvae has been extensively studied (see reviews by Killian and Wilt, 2008;Matranga et al, 2011Matranga et al, , 2013.…”

“…In contrast, biomineralization control in sea urchin embryos and larvae has been extensively studied (see reviews by Killian and Wilt, 2008;Matranga et al, 2011Matranga et al, , 2013. In embryos and larvae, biomineralization of spicules is carried out by primary mesenchyme cells expressing genes whose transcription is controlled by numerous factors (see Ettensohn, 2009, for a review).…”

“…In embryos and larvae, biomineralization of spicules is carried out by primary mesenchyme cells expressing genes whose transcription is controlled by numerous factors (see Ettensohn, 2009, for a review). Ectoderm cells are also involved in guiding the primary mesenchyme cells and were demonstrated to be involved in the regulation of biomineralizationrelated genes by the production of growth factors (Matranga et al, 2011). It is not known if the same processes occur in postmetamorphic biomineralization, although the expression of similar genes and the transcription of related proteins is reported in adult skeleton-forming cells (Drager et al, 1989;Livingston et al, 2006;Mann et al, 2008aMann et al, , b, 2010Killian et al, 2010).…”

Manganese: A New Emerging Contaminant in the Environment

“…Changes in shape and differentiation of embryo structures lead to the formation of a pluteus, the first larval stage. Genus-specific spicule growth and patterning is completed at this stage, directed by the spatial-temporal regulated expression of bio-mineralization related genes (Zito et al, 2005;Matranga et al, 2011). Sea urchin development from the blastula to the pluteus stage is showed in figure 2.…”

Effects of exposure to gadolinium on the development of geographically and phylogenetically distant sea urchins species

“…cadmium and manganese), UVB and X rays inhibits skeletogenesis (Filosto et al, 2008;Pinsino et al, 2011;Bonaventura et al, 2005;Matranga et al, 2010). The sea urchin larval skeleton is produced by the primary mesenchyme cells (PMCs) that migrate into the blastocoel during gastrulation, forming two ventrolateral clusters that secrete the spicule rudiment (Killian and Wilt, 2008;Matranga et al, 2011). Elongation and branching of the spicules produce the threedimensional pluteus endoskeleton, with specific features depending on the sea urchin species (Zito el al., 2015).…”