Ion-association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate

Habraken, Wouter J. E. M.; Tao, Jinhui; Brylka, Laura; Friedrich, Heiner; Bertinetti, Luca; Schenk, Anna S.; Verch, Andreas; Dmitrović, Vladimir; Bomans, Paul H. H.; Frederik, Peter M.; Lavèn, Jozua; Schoot, Paul van der; Aichmayer, Barbara; DeYoreo, James J.; Sommerdijk, Nico A. J. M.

doi:10.1038/ncomms2490

Cited by 685 publications

(969 citation statements)

References 56 publications

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“…Removal of nitrate by evaporation of the HNO3-H2O azeotrope drives cluster formation only as a crystalline solid. This 'classical' growth mechanism, a description of metal oxide formation without polynuclear cluster assembly prior to crystallization, bypasses the unstable solution cluster state that usually results in aggregation and production of an insoluble hydroxide (Baumgartner et al, 2013;Gebauer et al, 2014;Gebauer et al, 2008;Habraken et al, 2013). Crystallization of clusters without initial persistence in solution has not previously been considered as a way to isolate highly reactive clusters.…”

Section: Resultsmentioning

confidence: 99%

Crystallizing Elusive Chromium Polycations

Wang

Fullmer

Bandeira

et al. 2016

Chem

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SUMMARYOxo and oxo-hydroxo metal clusters are commonly isolated from aqueous solutions with capping ligands to prevent precipitation of metal hydroxides. Few simple molecular oxo-hydroxo metal clusters are readily synthesized and isolated without these capping ligands. Yet uncapped clusters are important in metal oxide growth and for applications hindered by auxiliary ligands. Uncapped clusters containing transition metals with partially filled d shells are especially difficult to preparethey rapidly aggregate and precipitate, preventing isolation of the initial cluster form. Herein, we elucidate a cluster self-assembly and crystallization process that has yielded a new uncapped oxo-hydroxo cluster containing Zn 2+ , Al 3+ , and the open-shell transition metal ion Cr 3+ , i.e., [ZnO4Al5.1Cr6.9(OH)24(H2O)12Zn(H2O)3] 8+ . For decades, clusters of Cr 3+ and Zn 2+ have been synthesis targets in polyoxocation chemistry, but they have resisted isolation and crystallization. We control pHdriven hydrolysis by oxidative dissolution of zinc in the reaction solution, rather than by addition of hydroxide. The control gained by Zn dissolution allows metal nitrate concentrations 10× higher than conventional hydroxide addition. Therefore, a high nitrate concentration further suppresses cluster self-assembly in the bulk. Contrary to common cluster growth studies, the fully assembled cluster is not observed spectroscopically in the bulk reaction solution from which the clusters are crystallized. Instead, the reaction solution is dominated by monomeric and dimeric metal species, even while the solution actively grows crystals. Evaporation of the HNO3-H2O azeotrope at the solution surface allows simultaneous cluster self-assembly and crystallization. Because these reactive clusters do not accumulate in the bulk solution and are isolated by crystallization, the state that often results in uncontrolled precipitation of metal hydroxide is avoided. The proposed formation pathway opens new opportunities to explore and augment the composition space and reaction chemistry of compositionally complex oxo-hydroxo clusters, particularly those comprising metals with partially filled d shells. The Bigger PictureAqueous metal-oxide clusters are important in natural processes, in synthesis, and in technology. In nature, they are central to contaminant transport, mineral growth, photosynthesis, and biomineralization. In synthesis, they provide nanometric forms with size dependent properties, and they are pre-assembled building blocks for materials. Fabricating functional metal oxide clusters and cluster-based materials in water minimizes environmental impact. Clusters synthesized and manipulated in water provide understanding of natural processes and inspire biomimetic materials; i.e. for artificial photosynthesis.While synthesis of functional clusters is accomplished with great control in organic solvents; it doesn't offer the simplicity and sustainability of aqueous synthesis. But aqueous syntheses that provide well-controlled cluster and mate...

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Section: Resultsmentioning

confidence: 99%

Crystallizing Elusive Chromium Polycations

Wang

Fullmer

Bandeira

et al. 2016

Chem

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“…Biomineralization is initiated via amorphous calcium phosphate (ACP) precursors that infiltrate the extracellular collagen matrix and subsequently transform into intrafibrillar carbonated apatite 1. The ACP precursor phase, in turn, is produced by coalescence of prenucleation clusters of hydrated calcium and phosphate ionic aggregates 2. Although the mechanisms of intrafibrillar mineralization of collagen fibrils have been well established,1 the process by which ACP precursors are produced and transported to the extracellular mineralization sites has not been completely elaborated.…”

Section: Introductionmentioning

confidence: 99%

Contribution of Mitophagy to Cell‐Mediated Mineralization: Revisiting a 50‐Year‐Old Conundrum

et al. 2018

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Biomineralization in vertebrates is initiated via amorphous calcium phosphate (ACP) precursors. These precursors infiltrate the extracellular collagen matrix where they undergo phase transformation into intrafibrillar carbonated apatite. Although it is well established that ACP precursors are released from intracellular vesicles through exocytosis, an unsolved enigma in this cell‐mediated mineralization process is how ACP precursors, initially produced in the mitochondria, are translocated to the intracellular vesicles. The present study proposes that mitophagy provides the mechanism for transfer of ACP precursors from the dysfunctioned mitochondria to autophagosomes, which, upon fusion with lysosomes, become autolysosomes where the mitochondrial ACP precursors coalesce to form larger intravesicular granules, prior to their release into the extracellular matrix. Apart from endowing the mitochondria with the function of ACP delivery through mitophagy, the present results indicate that mitophagy, triggered upon intramitochondrial ACP accumulation in osteogenic lineage‐committed mesenchymal stem cells, participates in the biomineralization process through the BMP/Smad signaling pathway.

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“…Recent studies of calcite nucleation on self-assembled monolayers (16) or polysaccharide films (17) and calcium phosphate nucleation on collagen (18) show that Eqs. 1 and 3 give a reasonable description of template-directed nucleation and that the interfacial energy is indeed the governing parameter.…”

Section: Significancementioning

confidence: 99%

Reconciling disparate views of template-directed nucleation through measurement of calcite nucleation kinetics and binding energies

Hamm

Giuffre

Han

et al. 2014

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

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The physical basis for how macromolecules regulate the onset of mineral formation in calcifying tissues is not well established. A popular conceptual model assumes the organic matrix provides a stereochemical match during cooperative organization of solute ions. In contrast, another uses simple binding assays to identify good promoters of nucleation. Here, we reconcile these two views and provide a mechanistic explanation for template-directed nucleation by correlating heterogeneous nucleation barriers with crystal-substrate-binding free energies. We first measure the kinetics of calcite nucleation onto model substrates that present different functional group chemistries (carboxyl, thiol, phosphate, and hydroxyl) and conformations (C11 and C16 chain lengths). We find rates are substrate-specific and obey predictions of classical nucleation theory at supersaturations that extend above the solubility of amorphous calcium carbonate. Analysis of the kinetic data shows the thermodynamic barrier to nucleation is reduced by minimizing the interfacial free energy of the system, γ. We then use dynamic force spectroscopy to independently measure calcitesubstrate-binding free energies, ΔG b . Moreover, we show that within the classical theory of nucleation, γ and ΔG b should be linearly related. The results bear out this prediction and demonstrate that low-energy barriers to nucleation correlate with strong crystal-substrate binding. This relationship is general to all functional group chemistries and conformations. These findings provide a physical model that reconciles the long-standing concept of templated nucleation through stereochemical matching with the conventional wisdom that good binders are good nucleators. The alternative perspectives become internally consistent when viewed through the lens of crystal-substrate binding.B iological systems are unique in their ability to organize minerals into functional materials with complex patterns and architectures. A substantial body of evidence suggests specialized macromolecules, particularly proteins (1, 2) and carbohydrates (3, 4), provide preferential sites for nucleation to direct the placement, timing, and orientation of crystals (5), both intra-and extracellular. Within the biomineralization community, the conventional view of biologically directed nucleation is that macromolecular matrices present an interfacial match to the crystal lattice that assists in forming the crystal nucleus. This cooperative view of directed nucleation is rooted in the collective action of multiple residues that guide the organization of ions into a configuration defining the energetic minimum for the system. A series of in vitro observations have reinforced this picture by showing that highly ordered organic monolayers can control the location and orientation of calcite crystals precipitated from solution (6). In this approach, good templates are revealed through a direct functional assay, i.e., nucleation. Over the years, this view of mineralization, both in the context of natural stru...

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Ion-association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate

Cited by 685 publications

References 56 publications

Crystallizing Elusive Chromium Polycations

Crystallizing Elusive Chromium Polycations

Contribution of Mitophagy to Cell‐Mediated Mineralization: Revisiting a 50‐Year‐Old Conundrum

Reconciling disparate views of template-directed nucleation through measurement of calcite nucleation kinetics and binding energies

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