Silicateins, silicatein interactors and cellular interplay in sponge skeletogenesis: formation of glass fiber‐like spicules

• Published in: The FEBS journal Vol. 279; no. 10; pp. 1721 - 1736
• Main Authors: Wang, Xiaohong, Schloßmacher, Ute, Wiens, Matthias, Batel, Renato, Schröder, Heinz C., Müller, Werner E. G.
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01.05.2012
• Subjects: Animals; Aquatic life; Biochemistry; biomineralization; biosilica; Cathepsins - metabolism; Cellular biology; Cytoskeleton - metabolism; Enzymes; fractals; Invertebrates; Metazoa; Microscopy, Electron, Scanning; Models, Molecular; Porifera - metabolism; Porifera - physiology; Protein Conformation; Proteins; sclerocytes; silicatein; siliceous spicule; Silicon Dioxide - metabolism; silintaphin; sponges; Suberites domuncula; syneresis
• ISSN: 1742-464X; 1742-4658
• DOI: 10.1111/j.1742-4658.2012.08533.x

Biomineralization processes are characterized by controlled deposition of inorganic polymers/minerals mediated by functional groups linked to organic templates. One metazoan taxon, the siliceous sponges, has utilized these principles and even gained the ability to form these polymers/minerals by an enzymatic mechanism using silicateins. Silicateins are the dominant protein species present in the axial canal of the skeletal elements of the siliceous sponges, the spicules, where they form the axial filament. Silicateins also represent a major part of the organic components of the silica lamellae, which are cylindrically arranged around the axial canal. With the demosponge Suberites domuncula as a model, quantitative enzymatic studies revealed that both the native and the recombinant enzyme display in vitro the same biosilica‐forming activity as the enzyme involved in spicule formation in vivo. Monomeric silicatein molecules assemble into filaments via fractal intermediates, which are stabilized by the silicatein‐interacting protein silintaphin‐1. Besides the silicateins, a silica‐degrading enzyme silicase acting as a catabolic enzyme has been identified. Growth of spicules proceeds in vivo in two directions: first, by axial growth, a process that is controlled by evagination of cell protrusions and mediated by the axial filament‐associated silicateins; and second, by appositional growth, which is driven by the extraspicular silicateins, a process that provides the spicules with their final size and morphology. This radial layer‐by‐layer accretion is directed by organic cylinders that are formed around the growing spicule and consist of galectin and silicatein. The cellular interplay that controls the morphogenetic processes during spiculogenesis is outlined. Silicateins are sponge‐specific enzymes that facilitate silica polycondensation, resulting in biosilica formation. Biosilica represents the scaffold for the skeletal elements of the sponges, the spicules. The genes/cDNAs for the silicateins and the silintaphins are known. This review summarizes the characteristics of these proteins as well as the regulatory network underlying the formation of one of the most intricately structured skeletal structures of Metazoa, the siliceous spicules.