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Initial Stages of Calcium Uptake and Mineral Deposition in Sea Urchin Embryos

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Initial Stages of Calcium Uptake and Mineral Deposition in Sea Urchin Embryos Initial stages of calcium uptake and mineral deposition in sea urchin embryos Netta Vidavskya, Sefi Addadib, Julia Mahamidc, Eyal Shimonid, David Ben-Ezrae, Muki Shpigele, Steve Weinera, and Lia Addadia,1 aDepartment of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel; bB-nano Ltd., Rehovot 76326, Israel; cDepartment of Molecular Structural Biology, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany; dDepartment of Chemical Research Support, Weizmann Institute of Science, Rehovot 76100, Israel; and eIsrael Oceanographic and Limnological Research, National Center for Mariculture, Eilat 88112, Israel Edited by Patricia M. Dove, Virginia Polytechnic Institute and State University, Blacksburg, VA, and approved October 31, 2013 (received for review July 10, 2013) Sea urchin larvae have an endoskeleton consisting of two calcitic fluorescent signal at the spicule tip (13). The dynamics of spicule spicules. We reconstructed various stages of the formation elongation also was studied in vivo by using calcein, which la- pathway of calcium carbonate from calcium ions in sea water to beled the surface of newly formed spicule areas (7, 14). Blocking mineral deposition and integration into the forming spicules. or interfering with calcium uptake by the cells, both in vivo and Monitoring calcium uptake with the fluorescent dye calcein shows in PMC cultures, shows that for the spicule to be formed, cal- that calcium ions first penetrate the embryo and later are de- cium first has to penetrate the cells (15–17). The manner in posited intracellularly. Surprisingly, calcium carbonate deposits are which calcium is transported to the PMCs is not known (7). It is distributed widely all over the embryo, including in the primary known that the ectoderm cells take part in spicule mineraliza- mesenchyme cells and in the surface epithelial cells. Using cryo- tion, especially in determining the placement of PMCs, which in SEM, we show that the intracellular calcium carbonate deposits turn specify the morphology of the spicule. The involvement of are contained in vesicles of diameter 0.5–1.5 μm. Using the newly ectoderm cells in calcium transport to the PMCs is not well developed airSEM, which allows direct correlation between fluo- understood, considering the fact that PMC cultures produce rescence and energy dispersive spectroscopy, we confirmed the spicules in the absence of ectoderm cells if growth factors are presence of solid calcium carbonate in the vesicles. This mineral introduced (8, 14, 18). phase appears as aggregates of 20–30-nm nanospheres, consistent Beniash et al. (19) showed that the PMCs contain electron- with amorphous calcium carbonate. The aggregates finally are in- dense granules of amorphous calcium carbonate (ACC) about troduced into the spicule compartment, where they integrate into 0.5–1.5 μm in diameter. These granules were assumed to in- the growing spicule. tegrate into the growing spicule after fusion with the syncytium membrane. The initial crystalline deposit in the syncytium is in biomineralization | mineralization pathway | sea urchin embryonic spicule | the form of a rhombohedral calcite crystal (20). The spicule transient precursor mineral phase | intracellular mineral deposition grows by the addition of transient ACC, which then partially CHEMISTRY transforms into calcite through secondary nucleation (21, 22). uring the biomineralization process, ions from the envi- The transformation from ACC to crystalline calcite is complex. Dronment are transported to the mineralization site by using Examination of the spicule surfaces with X-ray absorption different strategies, such as cell penetration through specific ion spectroscopy using extended X-ray absorption fine structure channels (1), delivery by vesicles (2), and formation of a pre- (EXAFS) and X-ray photoelectron emission microscopy (X- cursor amorphous mineral phase (3). The intracellular formation PEEM) showed three distinct mineral phases present in adjacent of a transient amorphous phase enables the mineral to be delivered sites at a scale of tens of nanometers. The initial phase, ACC1, is short-lived and presumably a hydrated ACC phase. The second efficiently to the mineralization site in a concentrated manner, thus BIOPHYSICS AND overcoming limitations of ion transport (4). phase, ACC2, is an intermediate transient form of ACC, whereas COMPUTATIONAL BIOLOGY The formation of calcite spicules by the embryonic sea urchin the third phase is crystalline calcite (21, 23). is a fascinating and well-documented example of a complex mul- tistage biomineralization process. Sea urchin embryos obtain cal- Significance cium directly from sea water until they can feed (5). The calcium is transported from the sea water through various outer tissue layers With the onset of gastrulation, sea urchin embryos deposit and is deposited inside cells. This mineral is then translocated to a calcium carbonate endoskeleton consisting of two spicules. a delimited space inside a syncytium in which an endoskeleton Sea water is the source for the mineral ions, but the specific composed of two spicules, each of which diffracts X-rays as stages of the transport and deposition pathway are not well a single crystal of calcite, is formed (6). The cells responsible for understood. This study shows that the first-formed mineral is the formation of the syncytium are the primary mesenchyme cells deposited inside intracellular micrometer-size vesicles as solid (PMCs). The spicules mineralize within the syncytium space, nanospheres. Surprisingly, the initial deposits are distributed enveloped by a thin extracellular layer (7). The PMCs are be- widely inside the embryonic cells, including epithelial cells. The lieved to control the entire biomineralization process, because possibility that the whole embryo is geared toward depositing spicule formation occurs in isolated and cultured PMCs (8). In mineral for spicule formation or other purposes, may contribute the embryo, however, the calcium and carbonate ions from the to the understanding of biomineralization processes in general. sea water have to pass through various outer tissue layers. The Author contributions: N.V., S.W., and L.A. designed research; N.V., S.A., J.M., and E.S. cells of these tissues thus control the ultrastructural and chemical performed research; S.A., E.S., D.B.-E., and M.S. contributed new reagents/analytic tools; milieu in which mineralization by the PMCs occurs and are also N.V., S.A., S.W., and L.A. analyzed data; and N.V., S.W., and L.A. wrote the paper. involved in the process. The authors declare no conflict of interest. Calcein is a small fluorescent molecule that may be used to This article is a PNAS Direct Submission. label calcium ions (9–12). Calcium ion labeling experiments with 1To whom correspondence should be addressed. E-mail: [email protected]. calcein in PMC cultures first demonstrated the formation of This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. calcium granules inside PMCs, followed by the appearance of a 1073/pnas.1312833110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1312833110 PNAS | January 7, 2014 | vol. 111 | no. 1 | 39–44 Downloaded by guest on September 27, 2021 Although it is known that the spicules form through secondary nucleation of ACC, many stages of the mineralization pathway are not clear. Some of the open questions are fundamental for understanding spicule mineralization, namely, what is the cal- cium pathway from sea water to the syncytium, do ACC deposits also form in cells that are not PMCs, and how are the ACC deposits transported into the spicule compartment? To address these questions, we studied the calcium pathways in whole embryos. Results SEM imaging under cryogenic conditions was performed on sea urchin embryos and larvae at different stages post fertilization. Fig. 2. Cryo-SEM micrograph of a high-pressure frozen and freeze-frac- The sample preparation procedure involves only high-pressure tured sea urchin embryo at the gastrula stage showing the spicule (S) and adjacent mineral-bearing vesicles, packed with nanospheres (arrowheads). freezing and freeze fracture of unfixed and unstained embryos. BSE image in Fig. S3. Cryo-SEM allows high-resolution imaging of biological samples as close as possible to their native state, minimizing artifacts caused by chemical procedures and drying. A cryo-SEM image of were observed after 1 h (Fig. 3 A and D). The calcein label is A a sea urchin embryo at the late gastrula stage (Fig. 1 ) shows the observed as a disperse cloud confined mainly within the blasto- layer of epithelial cells, the invaginated archenteron, and the rel- coel. After a longer calcein pulse (40 min), the calcein label atively large cell free space called the blastocoel. In the blastocoel, appears as concentrated granules inside the epithelial cells and specialized PMCs are interconnected in a syncytium where the possibly the PMCs and other cells (Fig. 3 B and E). spicules are formed. Two fractured spicules (backscattered image A Surprisingly, when embryos were developed from fertilization in Fig. S1 ) surrounded by PMCs are visible within the blastocoel continuously inside calcein-labeled sea water, calcein was de- on the two sides of the invaginated archenteron. Of particular tected as concentrated micrometer-sized granules all over the interest is the presence of a multivesicular body adjacent to the embryo (Fig. 3 C and F). The fluorescent label is concentrated PMCs (Fig.
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