TY - JOUR
T1 - Thermodynamic basis for evolution of apatite in calcified tissues
AU - Rollin-Martinet, Sabrina
AU - Navrotsky, Alexandra
AU - Champion, Eric
AU - Grossin, David
AU - Drouet, Christophe
N1 - Funding Information:
The authors thank the French Agence Nationale de la Recherche (ANR) for funding in the scope of the NanoBiocer program (ANR-07-BLAN-0373), as well as the Institut National Polytechnique de Toulouse (INPT) and the France Berkeley Fund (FBF) for co-funding. The authors also thank O. Trofymluk, K. Lilova, and A. V. Radha for experimental support.
PY - 2013
Y1 - 2013
N2 - Bone remodeling and tooth enamel maturation are biological processes that alter the physico-chemical features of biominerals with time. However, although the ubiquity of bone remodeling is clear, why is well-crystallized bone mineral systematically replaced by immature nanocrystalline inorganic material? In enamel, a clear evolution is also seen from the first mineral formed during the secretory stage and its mature well-crystalline form, which then changes little in the adult tooth. This contribution provides the thermodynamic basis underlying these biological phenomena. We determined, for the first time, the energetics of biomimetic apatites corresponding to an increasing degree of maturation. Our data point out the progressive evolution of the enthalpy (δH°f) and free energy (δG°f) of formation toward more negative values upon maturation. Entropy contributions to δG°f values remained small compared to enthalpy contributions. δH°f varied from -12 058.9 ± 12.2 to -12 771.0 ± 21.4 kJ/mol for maturation times increasing from 20 min to 3 weeks, approaching the value for stoichiometric hydroxyapatite, -13 431.0 ± 22.7 kJ/mol. Apatite thermodynamic stability increased as its composition moved toward stoichiometry. These findings imply diminishing aqueous solubility of calcium and phosphate ions as well as decreased surface reactivity. Such thermodynamically driven maturation is favorable for enamel maturation since this biomineral is intended to resist external aggressions such as contact with acids. In contrast, maintaining a metastable highly reactive and soluble form of apatite is essential to the effective participation of bone as a source of calcium and phosphate for homeostasis. Therefore our data strongly suggest that, far from being trivial, the intrinsic thermodynamic properties of apatite mineral represent a critical driving force for continuous bone remodeling, in contrast to current views favoring a purely biologically driven cycle. These thermodynamic data may prove helpful in other domains relating, for example, to apatite-based biomaterials development or in the field of (geo)microbiology.
AB - Bone remodeling and tooth enamel maturation are biological processes that alter the physico-chemical features of biominerals with time. However, although the ubiquity of bone remodeling is clear, why is well-crystallized bone mineral systematically replaced by immature nanocrystalline inorganic material? In enamel, a clear evolution is also seen from the first mineral formed during the secretory stage and its mature well-crystalline form, which then changes little in the adult tooth. This contribution provides the thermodynamic basis underlying these biological phenomena. We determined, for the first time, the energetics of biomimetic apatites corresponding to an increasing degree of maturation. Our data point out the progressive evolution of the enthalpy (δH°f) and free energy (δG°f) of formation toward more negative values upon maturation. Entropy contributions to δG°f values remained small compared to enthalpy contributions. δH°f varied from -12 058.9 ± 12.2 to -12 771.0 ± 21.4 kJ/mol for maturation times increasing from 20 min to 3 weeks, approaching the value for stoichiometric hydroxyapatite, -13 431.0 ± 22.7 kJ/mol. Apatite thermodynamic stability increased as its composition moved toward stoichiometry. These findings imply diminishing aqueous solubility of calcium and phosphate ions as well as decreased surface reactivity. Such thermodynamically driven maturation is favorable for enamel maturation since this biomineral is intended to resist external aggressions such as contact with acids. In contrast, maintaining a metastable highly reactive and soluble form of apatite is essential to the effective participation of bone as a source of calcium and phosphate for homeostasis. Therefore our data strongly suggest that, far from being trivial, the intrinsic thermodynamic properties of apatite mineral represent a critical driving force for continuous bone remodeling, in contrast to current views favoring a purely biologically driven cycle. These thermodynamic data may prove helpful in other domains relating, for example, to apatite-based biomaterials development or in the field of (geo)microbiology.
KW - Biomimetic
KW - Bone remodeling
KW - Calorimetry
KW - Enamel maturation
KW - Hydroxyapatite
KW - Metastability
KW - Nanocrystalline apatite
KW - Thermodynamics
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U2 - 10.2138/am.2013.4537
DO - 10.2138/am.2013.4537
M3 - Article
AN - SCOPUS:84888865096
SN - 0003-004X
VL - 98
SP - 2037
EP - 2045
JO - American Mineralogist
JF - American Mineralogist
IS - 11-12
ER -