The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite

Wang, Yan; Azaı̈s, Thierry; Robin, Marc; Vallée, Anne; Catania, Chelsea; Patrick, Legriel,; Péhau‐Arnaudet, Gérard; Babonneau, Florence; Giraud‐Guille, Marie‐Madeleine; Nassif, Nadine

doi:10.1038/nmat3362

Cited by 506 publications

(528 citation statements)

References 53 publications

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“…Indeed, previous measurements of ACP and HAP nucleation rates demonstrated α is significantly reduced on collagen relative to its value in solution, leading to greatly enhanced nucleation rates (17). Both the DFS measurements and the MD simulations show that, for the collagenapatite interface, binding energies are hundreds of k B T. Thus, when CDAP nucleates, whether from ACP (45) or OCP, based on the results with collagen alignment on CDAP (100) faces we should expect preferential c-axis alignment both parallel to and orthogonal to the long axis of collagen. Moreover, the local variations in collagen orientation by up to 15°are then consistent with a similar spread in bone apatite c axis, as is observed (22).…”

Section: Results and Analysismentioning

confidence: 84%

Energetic basis for the molecular-scale organization of bone

Tao

Battle

Pan

et al. 2014

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

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The remarkable properties of bone derive from a highly organized arrangement of coaligned nanometer-scale apatite platelets within a fibrillar collagen matrix. The origin of this arrangement is poorly understood and the crystal structures of hydroxyapatite (HAP) and the nonmineralized collagen fibrils alone do not provide an explanation. Moreover, little is known about collagen-apatite interaction energies, which should strongly influence both the molecular-scale organization and the resulting mechanical properties of the composite. We investigated collagen-mineral interactions by combining dynamic force spectroscopy (DFS) measurements of binding energies with molecular dynamics (MD) simulations of binding and atomic force microscopy (AFM) observations of collagen adsorption on single crystals of calcium phosphate for four mineral phases of potential importance in bone formation. In all cases, we observe a strong preferential orientation of collagen binding, but comparison between the observed orientations and transmission electron microscopy (TEM) analyses of native tissues shows that only calcium-deficient apatite (CDAP) provides an interface with collagen that is consistent with both. MD simulations predict preferred collagen orientations that agree with observations, and results from both MD and DFS reveal large values for the binding energy due to multiple binding sites. These findings reconcile apparent contradictions inherent in a hydroxyapatite or carbonated apatite (CAP) model of bone mineral and provide an energetic rationale for the molecular-scale organization of bone.biomineralization | bone | protein-mineral interface | dynamic force spectroscopy B one is a natural protein-mineral composite consisting of nonstoichiometric nanometer-scale carbonated apatite crystallites inside a fibrillar protein matrix. The matrix is mainly composed of type I collagen and is organized on multiple length scales (1, 2). At the shortest scale, three polypeptide chains form a triple helix referred to as a tropocollagen molecule that is ∼300 nm in length and 1.5 nm in diameter. These helices are arranged in a quasi-hexagonal bundle in which they overlap and intertwine to form microfibrils containing "hole zones," where there is a gap between the N termini of one helix and the C termini of another (3-5). These microfibrils are further bundled both laterally and longitudinally to form native collagen (3, 4).Within this highly organized scaffold, apatite crystallites form nanometer-scale platelets (6-9) with their [001] axes preferentially aligned parallel to the fibril axis (10-15) and the platelet faces defined by {100} crystal planes (16). Recent in vitro investigations of hydroxyapatite (HAP) formation within collagen fibrils revealed a multistage process in which amorphous calcium phosphate (ACP) first infiltrated through the hole zones and then converted into HAP platelets with initial mineral deposition occurring near the hole zones (11, 13). In vitro transmission electron microscopy (TEM) and atomic force microscop...

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Section: Results and Analysismentioning

confidence: 84%

Energetic basis for the molecular-scale organization of bone

Tao

Battle

Pan

et al. 2014

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

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“…Although the bio-mineralization process has been thought to be directed by acidic non-collagenous proteins, such as small integrin-binding ligand N-linked glycoprotein [68], it has been reported that type I collagen can initiate bio-mineralization in the absence of any other extracellular matrix molecules in vitro [69]. Currently, the significance and detailed mechanism of collagen cross-linking in the mineralization process remains unclear; however, it is possible that changes in collagen crosslinking may affect the inorganic phase of bone by controlling mineral nucleation.…”

Section: Collagen Cross-linkingmentioning

confidence: 99%

A paradigm shift for bone quality in dentistry: A literature review

Kuroshima

Kaku

Ishimoto

et al. 2017

Journal of Prosthodontic Research

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A B S T R A C TPurpose: The aim of this study was to present the current concept of bone quality based on the proposal by the National Institutes of Health (NIH) and some of the cellular and molecular factors that affect bone quality. Study selection: This is a literature review which focuses on collagen, biological apatite (BAp), and bone cells such as osteoblasts and osteocytes. Results: In dentistry, the term "bone quality" has long been considered to be synonymous with bone mineral density (BMD) based on radiographic and sensible evaluations. In 2000, the NIH proposed the concept of bone quality as "the sum of all characteristics of bone that influence the bone's resistance to fracture," which is completely independent of BMD. The NIH defines bone quality as comprising bone architecture, bone turnover, bone mineralization, and micro-damage accumulation. Moreover, our investigations have demonstrated that BAp, collagen, and bone cells such as osteoblasts and osteocytes play essential roles in controlling the current concept of bone quality in bone around hip and dental implants. Conclusion: The current concept of bone quality is crucial for understanding bone mechanical functions. BAp, collagen and osteocytes are the main factors affecting bone quality. Moreover, mechanical loading dynamically adapts bone quality. Understanding the current concept of bone quality is required in dentistry.

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“…At low concentrations of collagen reconstituted in vitro, the presence of negatively charged noncollagenous proteins can lead to in vivo-like intrafibrillar mineralization; whereas their absence results in the precipitation of extrafibrillar mineral globules 28 . However, at higher tissue-like densities of collagen fibrils, where dense monodispersed fibrils display cholesteric 3D alignment, the formation of intrafibrillar mineral has been shown to be possible without the involvement of noncollagenous proteins, and the morphology of the forming mineral reflects the spatial constraints of the dense collagen matrix 29 . As a consequence, the importance of mineral nucleators may well depend on the tissue suprafibrillar hierarchical architecture.…”

Section: General Inhibition Selective Promotion and Selective Inhibimentioning

confidence: 99%

“…Interfaces [47] Nuclear magnetic resonance spectroscopy* Molecular interactions [29] Subject categories…”

Section: Structures Labelingmentioning

confidence: 99%

A materials science vision of extracellular matrix mineralization

et al. 2016

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From an engineering perspective, skeletal tissues are remarkable structures in that they are lightweight, stiff and tough, yet produced at ambient conditions. The biomechanical success of skeletal tissues is largely attributable to the process of biomineralization -a tightly regulated, cell-driven formation of billions of inorganic nanocrystals formed from ions found abundantly in body fluids. In this Review, we discuss nature's strategies to produce and sustain appropriate biomechanical properties in mineralizing (by promotion of mineralization) and nonmineralizing (by inhibition of mineralization) tissues. We review how perturbations of biomineralization are controlled over a continuum which spans from the desirable (or defective in disease) mineralization of the skeleton, to pathological cardiovascular mineralization, and to mineralization of bioengineered constructs. A materials science vision of mineralization is presented with an emphasis on the micro-and nanostructure of mineralized tissues recently revealed by state-of-the-art analytical methods, and on how biomineralization-inspired designs are impacting the field of synthetic materials. Web summaryComplex mechanisms are at play in the biomineralization of skeletal tissues and in patholological calcification in the cardiovascular system. In this Review, the physiochemical and biomechanical properties of mineralized tissues, both physiologic and pathophysiologic, and analytical methods to elucidate their finer structure are discussed.

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The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite

Cited by 506 publications

References 53 publications

Energetic basis for the molecular-scale organization of bone

Energetic basis for the molecular-scale organization of bone

A paradigm shift for bone quality in dentistry: A literature review

A materials science vision of extracellular matrix mineralization

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