The biological regulation of sea urchin larval skeletogenesis – From genes to biomineralized tissue

• Published in: Journal of structural biology Vol. 213; no. 4; p. 107797
• Main Authors: Gildor, Tsvia, Winter, Mark R., Layous, Majed, Hijaze, Eman, Ben-Tabou de-Leon, Smadar
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.12.2021
• Subjects: Animals; Biomineralization; Biomineralization - genetics; Calcification, Physiologic - genetics; Cell Movement - genetics; Embryo, Nonmammalian - cytology; Embryo, Nonmammalian - embryology; Embryo, Nonmammalian - metabolism; Epithelial-Mesenchymal Transition - genetics; Gene Expression Regulation, Developmental; Gene regulatory network; Larva - genetics; Larva - growth & development; Larva - metabolism; Morphogenesis - genetics; Sea urchin; Sea Urchins - embryology; Sea Urchins - genetics; Sea Urchins - metabolism; Skeletogenesis; Tubulogenesis; Vascular Endothelial Growth Factor; Vesicle diffusion; Skeletogenesis; Tubulogenesis; Biomineralization; Gene regulatory network; Vascular Endothelial Growth Factor; Sea urchin; Vesicle diffusion
• ISSN: 1047-8477; 1095-8657
• DOI: 10.1016/j.jsb.2021.107797

[Display omitted] •The sea urchin skeleton is generated by a sequence of morphogenetic processes.•Each morphogenetic process is controlled by a specific regulatory sub-circuit.•Mineral bearing vesicles perform an active diffusion motion in the skeletogenic cells.•Spicule elongation at the tips of the rods is driven by tips-specific regulatory states.•Possible common origin of sea urchin skeletogenesis and vertebrates’ vascularization. Biomineralization is the process in which soft organic tissues use minerals to produce shells, skeletons and teeth for various functions such as protection and physical support. The ability of the cells to control the time and place of crystal nucleation as well as crystal orientation and stiffness is far beyond the state-of-the art of human technologies. Thus, understanding the biological control of biomineralization will promote our understanding of embryo development as well as provide novel approaches for material engineering. Sea urchin larval skeletogenesis offers an excellent platform for functional analyses of both the molecular control system and mineral uptake and deposition. Here we describe the current understanding of the genetic, molecular and cellular processes that underlie sea urchin larval skeletogenesis. We portray the regulatory genes that define the specification of the skeletogenic cells and drive the various morphogenetic processes that occur in the skeletogenic lineage, including: epithelial to mesenchymal transition, cell migration, spicule cavity formation and mineral deposition into the spicule cavity. We describe recent characterizations of the size, motion and mineral concentration of the calcium-bearing vesicles in the skeletogenic cells. We review the distinct specification states within the skeletogenic lineage that drive localized skeletal growth at the tips of the spicules. Finally, we discuss the surprising similarity between the regulatory network and cellular processes that drive sea urchin skeletogenesis and those that control vertebrate vascularization. Overall, we illustrate the novel insights on the biological regulation and evolution of biomineralization, gained from studies of the sea urchin larval skeletogenesis.