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A review of phosphate mineral nucleation in biology and geobiology.

Omelon S, Ariganello M, Bonucci E, Grynpas M, Nanci A - Calcif. Tissue Int. (2013)

Bottom Line: Subsequent release of these P reserves into the local marine environment as Pi results in biologically induced phosphorite nucleation.Polyphosphates may be associated with biologically controlled apatite nucleation within vertebrates and invertebrates.Enzymatic polyphosphate depolymerization would increase apatite saturation to the level required for mineral nucleation, while matrix proteins would simultaneously control the progression of new biological apatite formation.

View Article: PubMed Central - PubMed

ABSTRACT
Relationships between geological phosphorite deposition and biological apatite nucleation have often been overlooked. However, similarities in biological apatite and phosphorite mineralogy suggest that their chemical formation mechanisms may be similar. This review serves to draw parallels between two newly described phosphorite mineralization processes, and proposes a similar novel mechanism for biologically controlled apatite mineral nucleation. This mechanism integrates polyphosphate biochemistry with crystal nucleation theory. Recently, the roles of polyphosphates in the nucleation of marine phosphorites were discovered. Marine bacteria and diatoms have been shown to store and concentrate inorganic phosphate (Pi) as amorphous, polyphosphate granules. Subsequent release of these P reserves into the local marine environment as Pi results in biologically induced phosphorite nucleation. Pi storage and release through an intracellular polyphosphate intermediate may also occur in mineralizing oral bacteria. Polyphosphates may be associated with biologically controlled apatite nucleation within vertebrates and invertebrates. Historically, biological apatite nucleation has been attributed to either a biochemical increase in local Pi concentration or matrix-mediated apatite nucleation control. This review proposes a mechanism that integrates both theories. Intracellular and extracellular amorphous granules, rich in both calcium and phosphorus, have been observed in apatite-biomineralizing vertebrates, protists, and atremate brachiopods. These granules may represent stores of calcium-polyphosphate. Not unlike phosphorite nucleation by bacteria and diatoms, polyphosphate depolymerization to Pi would be controlled by phosphatase activity. Enzymatic polyphosphate depolymerization would increase apatite saturation to the level required for mineral nucleation, while matrix proteins would simultaneously control the progression of new biological apatite formation.

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Analytical electron microscopic evidence of vesicle–mitochondrial interactions in mineralizing osteoblasts. a High-angle annular dark-field scanning TEM image of a dense granule-containing mitochondrion associating with a vesicle within an osteoblast in a mineralized nodule. The sample was prepared by high-pressure freezing and freeze substitution (HPF-FS). (Scale bar = 200 nm). b Voltex projection of a 3D tomographic reconstruction showing a mitochondrion conjoined with a vesicle. Dense granules are evident within the mitochondrion. Sample was prepared by HPF-FS. c Electron energy loss spectroscopy (EELS) of specified areas within the mitochondrion and vesicle in a. The mitochondrial granule and vesicle show characteristic calcium L2 and L3 edges at 346 eV. All spectra display carbon edges. d Orthoslices at 10-nm intervals through the tomographic reconstruction showing the mitochondrion–vesicle interface. The mitochondrial membrane is discontinuous where it conjoins the vesicle (arrows) [131]
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Fig3: Analytical electron microscopic evidence of vesicle–mitochondrial interactions in mineralizing osteoblasts. a High-angle annular dark-field scanning TEM image of a dense granule-containing mitochondrion associating with a vesicle within an osteoblast in a mineralized nodule. The sample was prepared by high-pressure freezing and freeze substitution (HPF-FS). (Scale bar = 200 nm). b Voltex projection of a 3D tomographic reconstruction showing a mitochondrion conjoined with a vesicle. Dense granules are evident within the mitochondrion. Sample was prepared by HPF-FS. c Electron energy loss spectroscopy (EELS) of specified areas within the mitochondrion and vesicle in a. The mitochondrial granule and vesicle show characteristic calcium L2 and L3 edges at 346 eV. All spectra display carbon edges. d Orthoslices at 10-nm intervals through the tomographic reconstruction showing the mitochondrion–vesicle interface. The mitochondrial membrane is discontinuous where it conjoins the vesicle (arrows) [131]

Mentions: Kashiwa and Komorous [135] demonstrated intra- and extracellular calcium- and P-rich spherules within fresh calcifying cartilage samples from regions preceding endochondral calcification. Kashiwa [143] also identified calcium- and P-rich granules within, and adjacent to, mature and hypertrophic calcifying chondrocytes when staining was performed on fresh samples to avoid the effects of sample preparation on unstable structures. Boonrungsiman et al. [131] observed Ca- and P-rich mitochondrial granules within mineralizing murine osteoblast cultures, and presented evidence of vesicle–mitochondrial interactions with high angle-annular dark-field scanning TEM of samples prepared with high-pressure freezing and freeze substitution (HPF-FS) (Fig. 3). Although the presence of these unstable, electron-dense, Ca- and P-containing granules has been identified by different groups, their specific composition is unknown. Fluorescence imaging has shown colocalization of polyPs within murine growth plate calcifying cartilage [31] but not at the resolution required to identify granules. How these granules are secreted into the ECM where they transform into carbonated apatite remains unknown. The realization of these phenomena must lie with the activity of matrix proteins.Fig. 3


A review of phosphate mineral nucleation in biology and geobiology.

Omelon S, Ariganello M, Bonucci E, Grynpas M, Nanci A - Calcif. Tissue Int. (2013)

Analytical electron microscopic evidence of vesicle–mitochondrial interactions in mineralizing osteoblasts. a High-angle annular dark-field scanning TEM image of a dense granule-containing mitochondrion associating with a vesicle within an osteoblast in a mineralized nodule. The sample was prepared by high-pressure freezing and freeze substitution (HPF-FS). (Scale bar = 200 nm). b Voltex projection of a 3D tomographic reconstruction showing a mitochondrion conjoined with a vesicle. Dense granules are evident within the mitochondrion. Sample was prepared by HPF-FS. c Electron energy loss spectroscopy (EELS) of specified areas within the mitochondrion and vesicle in a. The mitochondrial granule and vesicle show characteristic calcium L2 and L3 edges at 346 eV. All spectra display carbon edges. d Orthoslices at 10-nm intervals through the tomographic reconstruction showing the mitochondrion–vesicle interface. The mitochondrial membrane is discontinuous where it conjoins the vesicle (arrows) [131]
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3824353&req=5

Fig3: Analytical electron microscopic evidence of vesicle–mitochondrial interactions in mineralizing osteoblasts. a High-angle annular dark-field scanning TEM image of a dense granule-containing mitochondrion associating with a vesicle within an osteoblast in a mineralized nodule. The sample was prepared by high-pressure freezing and freeze substitution (HPF-FS). (Scale bar = 200 nm). b Voltex projection of a 3D tomographic reconstruction showing a mitochondrion conjoined with a vesicle. Dense granules are evident within the mitochondrion. Sample was prepared by HPF-FS. c Electron energy loss spectroscopy (EELS) of specified areas within the mitochondrion and vesicle in a. The mitochondrial granule and vesicle show characteristic calcium L2 and L3 edges at 346 eV. All spectra display carbon edges. d Orthoslices at 10-nm intervals through the tomographic reconstruction showing the mitochondrion–vesicle interface. The mitochondrial membrane is discontinuous where it conjoins the vesicle (arrows) [131]
Mentions: Kashiwa and Komorous [135] demonstrated intra- and extracellular calcium- and P-rich spherules within fresh calcifying cartilage samples from regions preceding endochondral calcification. Kashiwa [143] also identified calcium- and P-rich granules within, and adjacent to, mature and hypertrophic calcifying chondrocytes when staining was performed on fresh samples to avoid the effects of sample preparation on unstable structures. Boonrungsiman et al. [131] observed Ca- and P-rich mitochondrial granules within mineralizing murine osteoblast cultures, and presented evidence of vesicle–mitochondrial interactions with high angle-annular dark-field scanning TEM of samples prepared with high-pressure freezing and freeze substitution (HPF-FS) (Fig. 3). Although the presence of these unstable, electron-dense, Ca- and P-containing granules has been identified by different groups, their specific composition is unknown. Fluorescence imaging has shown colocalization of polyPs within murine growth plate calcifying cartilage [31] but not at the resolution required to identify granules. How these granules are secreted into the ECM where they transform into carbonated apatite remains unknown. The realization of these phenomena must lie with the activity of matrix proteins.Fig. 3

Bottom Line: Subsequent release of these P reserves into the local marine environment as Pi results in biologically induced phosphorite nucleation.Polyphosphates may be associated with biologically controlled apatite nucleation within vertebrates and invertebrates.Enzymatic polyphosphate depolymerization would increase apatite saturation to the level required for mineral nucleation, while matrix proteins would simultaneously control the progression of new biological apatite formation.

View Article: PubMed Central - PubMed

ABSTRACT
Relationships between geological phosphorite deposition and biological apatite nucleation have often been overlooked. However, similarities in biological apatite and phosphorite mineralogy suggest that their chemical formation mechanisms may be similar. This review serves to draw parallels between two newly described phosphorite mineralization processes, and proposes a similar novel mechanism for biologically controlled apatite mineral nucleation. This mechanism integrates polyphosphate biochemistry with crystal nucleation theory. Recently, the roles of polyphosphates in the nucleation of marine phosphorites were discovered. Marine bacteria and diatoms have been shown to store and concentrate inorganic phosphate (Pi) as amorphous, polyphosphate granules. Subsequent release of these P reserves into the local marine environment as Pi results in biologically induced phosphorite nucleation. Pi storage and release through an intracellular polyphosphate intermediate may also occur in mineralizing oral bacteria. Polyphosphates may be associated with biologically controlled apatite nucleation within vertebrates and invertebrates. Historically, biological apatite nucleation has been attributed to either a biochemical increase in local Pi concentration or matrix-mediated apatite nucleation control. This review proposes a mechanism that integrates both theories. Intracellular and extracellular amorphous granules, rich in both calcium and phosphorus, have been observed in apatite-biomineralizing vertebrates, protists, and atremate brachiopods. These granules may represent stores of calcium-polyphosphate. Not unlike phosphorite nucleation by bacteria and diatoms, polyphosphate depolymerization to Pi would be controlled by phosphatase activity. Enzymatic polyphosphate depolymerization would increase apatite saturation to the level required for mineral nucleation, while matrix proteins would simultaneously control the progression of new biological apatite formation.

Show MeSH
Related in: MedlinePlus