Recent advances of shell matrix proteins and cellular orchestration in marine molluscan shell biomineralization

Abstract

Biomineralization refers to the dynamic physiological processes whereby living organisms elaborate mineralized tissues. The existence of extremely abundant molluscan species shows the diversity of mineralized tissues, since the majority of them (Conchifera) produce shells that vary in size and shape. Over the past decades, great progress has been made on the study of the cellular biology of shell biomineralization. The construction of the molluscan shell is the archetype of biologically controlled mineralization which requires specialized cellular machinery. It has been so far demonstrated that the cells involved in shell formation come from two different sources: outer mantle epithelial cells (OME) and circulating hemocytes. OMEs secrete the organic matrix, among which shell matrix proteins (SMPs) determine mineralogical and crystallographic properties of shell. Circulating hemocytes take part in the deposition of intracellular biominerals and deliver them to the mineralization sites. Many novel SMPs have been identified by using molecular biology techniques (i.e., gene cloning, in situ hybridization, immunohistochemistry) coupled with high-throughput sequencing data (genome, proteome, secretome and transcriptome), and their corresponding functions during the shell formation have also been confirmed. The cellular activity of OME and hemocytes during shell formation are significantly increased during shell regeneration process. A potential cellular basis model for molluscan shell formation is proposed. The shell matrix proteins, mostly secreted from OME, and a few secreted from hemocytes or other organs, are either directly delivered to the mineralization site via exosome or classical secretory pathway, or first transported to the hemolymph, and then engulfed by hemocytes (mainly granulocytes), which will disintegrate and release shell proteins and CaCO 3 crystals at the mineralization front. OME and hemocytes may also be involved in the nucleation and remodeling process of CaCO 3 ' mineral. These cells and cell products work co-operatively to produce an organo-mineral shell, which is composed of various biomineral ultra-structures and macromolecular organic components.