Avian eggshell formation reveals a new paradigm for vertebrate mineralization via vesicular amorphous calcium carbonate

Stapane, Lilian; Roy, Nathalie Le; Ezagal, Jacky; Rodríguez‐Navarro, Alejandro B.; Labas, Valérie; Combes‐Soia, Lucie; Hincke, Maxwell T.; Gautron, Joël

doi:10.1074/jbc.ra120.014542

Cited by 25 publications

(30 citation statements)

References 115 publications

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“…Membrane-bound, intracellular vesicles enriched in calcium and transporting it to the biomineralization site were not only observed in corals and anemones ( 25 ), but also in sea urchin embryos ( 40 ). Vesicles carrying ACC are extracellular in chicken eggshell formation, but they are also membrane-bound ( 41 ).…”

mentioning

confidence: 99%

From particle attachment to space-filling coral skeletons

Sun

Stifler

Chopdekar

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Reef-building corals and their aragonite (CaCO3) skeletons support entire reef ecosystems, yet their formation mechanism is poorly understood. Here we used synchrotron spectromicroscopy to observe the nanoscale mineralogy of fresh, forming skeletons from six species spanning all reef-forming coral morphologies: Branching, encrusting, massive, and table. In all species, hydrated and anhydrous amorphous calcium carbonate nanoparticles were precursors for skeletal growth, as previously observed in a single species. The amorphous precursors here were observed in tissue, between tissue and skeleton, and at growth fronts of the skeleton, within a low-density nano- or microporous layer varying in thickness from 7 to 20 µm. Brunauer-Emmett-Teller measurements, however, indicated that the mature skeletons at the microscale were space-filling, comparable to single crystals of geologic aragonite. Nanoparticles alone can never fill space completely, thus ion-by-ion filling must be invoked to fill interstitial pores. Such ion-by-ion diffusion and attachment may occur from the supersaturated calcifying fluid known to exist in corals, or from a dense liquid precursor, observed in synthetic systems but never in biogenic ones. Concomitant particle attachment and ion-by-ion filling was previously observed in synthetic calcite rhombohedra, but never in aragonite pseudohexagonal prisms, synthetic or biogenic, as observed here. Models for biomineral growth, isotope incorporation, and coral skeletons’ resilience to ocean warming and acidification must take into account the dual formation mechanism, including particle attachment and ion-by-ion space filling.

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mentioning

confidence: 99%

From particle attachment to space-filling coral skeletons

Sun

Stifler

Chopdekar

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…Hens show respiratory hyperventilation during shell formation to alleviate metabolic acidosis due to acidification of uterine fluid and plasma during shell formation [28]. Both components of the shell mineral (Ca 2+ and CO 3 2− ) are continuously supplied during eggshell formation via the blood plasma, firstly by trans-epithelial ionic transport through the uterine epithelium [20,29], and secondly, by vesicular secretion of ACC mineral particles [21].…”

Section: Molecular Control Of the Avian Eggshell Biomineralization Process Regulation Of Mineral Supply Necessary For Shell Formationmentioning

confidence: 99%

“…Graphical elements were from Servier Medical Art (https://smart.servier.com/), licensed under a Creative Commons Attribution 3.0 Unported License. Adapted from [20][21][22][23][24][25] in shell stiffness [49,54,59,60]. In addition, a common QTL for the breaking strength characteristics and shell stiffness was found on chromosome 2 [54].…”

Section: And 33mentioning

confidence: 99%

“…Transcriptomic approaches [22,92] revealed a large number of uterine ionic transporters by analogies with protein sequences of transporters previously described in mammalian or avian tissues (intestine, kidney). This information was used to update the initial model of ionic transport for supplying mineral precursors of the shell to the uterine fluid [21][22][23]. Recently, an additional process to provide CaCO 3 was revealed.…”

Section: Active and Continuous Supply Of The Ions Necessary For Shell Formationmentioning

confidence: 99%

“…Recently, an additional process to provide CaCO 3 was revealed. Extracellular vesicles (EVs, 100-400 nm), originating from uterine epithelial cells, deliver stabilized amorphous calcium carbonate (ACC) to the mineralization front [21,93].…”

Section: Active and Continuous Supply Of The Ions Necessary For Shell Formationmentioning

confidence: 99%

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Avian eggshell biomineralization: an update on its structure, mineralogy and protein tool kit

Gautron

Stapane

Roy

et al. 2021

BMC Mol and Cell Biol

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Background The avian eggshell is a natural protective envelope that relies on the phenomenon of biomineralization for its formation. The shell is made of calcium carbonate in the form of calcite, which contains hundreds of proteins that interact with the mineral phase controlling its formation and structural organization, and thus determine the mechanical properties of the mature biomaterial. We describe its mineralogy, structure and the regulatory interactions that integrate the mineral and organic constituents during eggshell biomineralization. Main Body. We underline recent evidence for vesicular transfer of amorphous calcium carbonate (ACC), as a new pathway to ensure the active and continuous supply of the ions necessary for shell mineralization. Currently more than 900 proteins and thousands of upregulated transcripts have been identified during chicken eggshell formation. Bioinformatic predictions address their functionality during the biomineralization process. In addition, we describe matrix protein quantification to understand their role during the key spatially- and temporally- regulated events of shell mineralization. Finally, we propose an updated scheme with a global scenario encompassing the mechanisms of avian eggshell mineralization. Conclusion With this large dataset at hand, it should now be possible to determine specific motifs, domains or proteins and peptide sequences that perform a critical function during avian eggshell biomineralization. The integration of this insight with genomic data (non-synonymous single nucleotide polymorphisms) and precise phenotyping (shell biomechanical parameters) on pure selected lines will lead to consistently better-quality eggshell characteristics for improved food safety. This information will also address the question of how the evolutionary-optimized chicken eggshell matrix proteins affect and regulate calcium carbonate mineralization as a good example of biomimetic and bio-inspired material design.

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