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Molecular mechanics of mineralized collagen fibrils in bone.

Nair AK, Gautieri A, Chang SW, Buehler MJ - Nat Commun (2013)

Bottom Line: Here we perform full-atomistic calculations of the three-dimensional molecular structure of a mineralized collagen protein matrix to try to better understand its mechanical characteristics under tensile loading at various mineral densities.We find that as the mineral density increases, the tensile modulus of the network increases monotonically and well beyond that of pure collagen fibrils.These findings reveal the mechanism by which bone is able to achieve superior energy dissipation and fracture resistance characteristics beyond its individual constituents.

View Article: PubMed Central - PubMed

Affiliation: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.

ABSTRACT
Bone is a natural composite of collagen protein and the mineral hydroxyapatite. The structure of bone is known to be important to its load-bearing characteristics, but relatively little is known about this structure or the mechanism that govern deformation at the molecular scale. Here we perform full-atomistic calculations of the three-dimensional molecular structure of a mineralized collagen protein matrix to try to better understand its mechanical characteristics under tensile loading at various mineral densities. We find that as the mineral density increases, the tensile modulus of the network increases monotonically and well beyond that of pure collagen fibrils. Our results suggest that the mineral crystals within this network bears up to four times the stress of the collagen fibrils, whereas the collagen is predominantly responsible for the material's deformation response. These findings reveal the mechanism by which bone is able to achieve superior energy dissipation and fracture resistance characteristics beyond its individual constituents.

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Variation of the gap-to-overlap length ratio as the applied stress increases for different HAP contents.The deformation mechanism of non-mineralized collagen fibrils is molecular straightening in the crimped and loosely packed gap region (at small deformations), followed by molecular stretching (across the full D-period) at larger deformations. These mechanisms result in an initial increase in the gap/overlap ratio, which then remains constant, as is observed in the non-mineralized model reported here (where the gap/overlap ratio increases from 0–20 MPa stress). In contrast, in the mineralized cases the deformation mechanism is radically changed. Indeed, in the lower mineralized model (20% HAP) we do not observe any significant change in the gap/overlap ratio, suggesting that the D-period deforms rather uniformly, due to the stiffening effect of HAP mainly in the gap region. However, in the highly mineralized model (40% HAP), the trend is inverted, where the gap/overlap region decreases, suggesting that in this case the gap region is stiffer and that deformation takes place primarily in the overlap region. The error bars are obtained from the maximum and minimum values of the periodic box length along the x direction obtained after equilibration of each sample, which is utilized to compute the gap and overlap lengths.
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f4: Variation of the gap-to-overlap length ratio as the applied stress increases for different HAP contents.The deformation mechanism of non-mineralized collagen fibrils is molecular straightening in the crimped and loosely packed gap region (at small deformations), followed by molecular stretching (across the full D-period) at larger deformations. These mechanisms result in an initial increase in the gap/overlap ratio, which then remains constant, as is observed in the non-mineralized model reported here (where the gap/overlap ratio increases from 0–20 MPa stress). In contrast, in the mineralized cases the deformation mechanism is radically changed. Indeed, in the lower mineralized model (20% HAP) we do not observe any significant change in the gap/overlap ratio, suggesting that the D-period deforms rather uniformly, due to the stiffening effect of HAP mainly in the gap region. However, in the highly mineralized model (40% HAP), the trend is inverted, where the gap/overlap region decreases, suggesting that in this case the gap region is stiffer and that deformation takes place primarily in the overlap region. The error bars are obtained from the maximum and minimum values of the periodic box length along the x direction obtained after equilibration of each sample, which is utilized to compute the gap and overlap lengths.

Mentions: To understand the deformation mechanism for mineralized and non-mineralized samples at different deformation states, we compute the deformation fields within the fibrils. We observe that as the loading increases, there is no significant movement or coalescence of the HAP crystals in the gap region when the loading increases from 20–100 MPa. However, for the 0% case, the collagen molecule undergoes significant deformation in the gap region as the applied stress increases. We compute the deformation in the collagen microfibril for all three cases at applied stresses of 20, 60 and 100 MPa. As seen in Fig. 4, the gap-to-overlap ratio for 0% case increases with the applied stress, indicating that for pure collagen the gap region deforms significantly compared with the overlap region to accommodate the external load. This behaviour is consistent with earlier tensile tests on collagen microfibril30. Clearly, the presence of HAP alters the deformation mechanism of the collagen fibril. For the 20% mineral-density case, the gap-to-overlap ratio is nearly constant for increases in applied stress, whereas for the 40% case the gap-to-overlap ratio decreases as the applied stress increases. This shows that a higher mineral content leads to more deformation in the overlap region compared with the gap region, where the interaction between HAP and collagen limits the deformation within collagen molecules. It has been previously suggested that the interaction between mineral and collagen is mainly due to electrostatic interactions and hydrogen bonding32. An analysis of the number of hydrogen bonds between the mineral and collagen in the gap region shows that the mineralized case has ~18–20% more hydrogen bonds compared with the non-mineralized case, where the hydrogen bonding occurs solely between the chains within the collagen molecule. Another important mechanism of load transfer between collagen and HAP is due to salt bridges (electrostatic interactions between charged moieties). Although in the non-mineralized fibril this type of non-covalent interaction is minor, it becomes rather important in the mineralized samples. As shown in Fig. 5, the vast majority of salt bridges are formed within the mineral crystals; however, a non-negligible number of salt bridges are formed between mineral crystals and collagen, providing an effective load transfer mechanism between the mineral and organic phase that also enhances energy dissipation. This further explains our finding that the overlap region deforms more compared with gap region in the mineralized cases, a clear distinction from the mechanics of pure collagen fibrils.


Molecular mechanics of mineralized collagen fibrils in bone.

Nair AK, Gautieri A, Chang SW, Buehler MJ - Nat Commun (2013)

Variation of the gap-to-overlap length ratio as the applied stress increases for different HAP contents.The deformation mechanism of non-mineralized collagen fibrils is molecular straightening in the crimped and loosely packed gap region (at small deformations), followed by molecular stretching (across the full D-period) at larger deformations. These mechanisms result in an initial increase in the gap/overlap ratio, which then remains constant, as is observed in the non-mineralized model reported here (where the gap/overlap ratio increases from 0–20 MPa stress). In contrast, in the mineralized cases the deformation mechanism is radically changed. Indeed, in the lower mineralized model (20% HAP) we do not observe any significant change in the gap/overlap ratio, suggesting that the D-period deforms rather uniformly, due to the stiffening effect of HAP mainly in the gap region. However, in the highly mineralized model (40% HAP), the trend is inverted, where the gap/overlap region decreases, suggesting that in this case the gap region is stiffer and that deformation takes place primarily in the overlap region. The error bars are obtained from the maximum and minimum values of the periodic box length along the x direction obtained after equilibration of each sample, which is utilized to compute the gap and overlap lengths.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3644085&req=5

f4: Variation of the gap-to-overlap length ratio as the applied stress increases for different HAP contents.The deformation mechanism of non-mineralized collagen fibrils is molecular straightening in the crimped and loosely packed gap region (at small deformations), followed by molecular stretching (across the full D-period) at larger deformations. These mechanisms result in an initial increase in the gap/overlap ratio, which then remains constant, as is observed in the non-mineralized model reported here (where the gap/overlap ratio increases from 0–20 MPa stress). In contrast, in the mineralized cases the deformation mechanism is radically changed. Indeed, in the lower mineralized model (20% HAP) we do not observe any significant change in the gap/overlap ratio, suggesting that the D-period deforms rather uniformly, due to the stiffening effect of HAP mainly in the gap region. However, in the highly mineralized model (40% HAP), the trend is inverted, where the gap/overlap region decreases, suggesting that in this case the gap region is stiffer and that deformation takes place primarily in the overlap region. The error bars are obtained from the maximum and minimum values of the periodic box length along the x direction obtained after equilibration of each sample, which is utilized to compute the gap and overlap lengths.
Mentions: To understand the deformation mechanism for mineralized and non-mineralized samples at different deformation states, we compute the deformation fields within the fibrils. We observe that as the loading increases, there is no significant movement or coalescence of the HAP crystals in the gap region when the loading increases from 20–100 MPa. However, for the 0% case, the collagen molecule undergoes significant deformation in the gap region as the applied stress increases. We compute the deformation in the collagen microfibril for all three cases at applied stresses of 20, 60 and 100 MPa. As seen in Fig. 4, the gap-to-overlap ratio for 0% case increases with the applied stress, indicating that for pure collagen the gap region deforms significantly compared with the overlap region to accommodate the external load. This behaviour is consistent with earlier tensile tests on collagen microfibril30. Clearly, the presence of HAP alters the deformation mechanism of the collagen fibril. For the 20% mineral-density case, the gap-to-overlap ratio is nearly constant for increases in applied stress, whereas for the 40% case the gap-to-overlap ratio decreases as the applied stress increases. This shows that a higher mineral content leads to more deformation in the overlap region compared with the gap region, where the interaction between HAP and collagen limits the deformation within collagen molecules. It has been previously suggested that the interaction between mineral and collagen is mainly due to electrostatic interactions and hydrogen bonding32. An analysis of the number of hydrogen bonds between the mineral and collagen in the gap region shows that the mineralized case has ~18–20% more hydrogen bonds compared with the non-mineralized case, where the hydrogen bonding occurs solely between the chains within the collagen molecule. Another important mechanism of load transfer between collagen and HAP is due to salt bridges (electrostatic interactions between charged moieties). Although in the non-mineralized fibril this type of non-covalent interaction is minor, it becomes rather important in the mineralized samples. As shown in Fig. 5, the vast majority of salt bridges are formed within the mineral crystals; however, a non-negligible number of salt bridges are formed between mineral crystals and collagen, providing an effective load transfer mechanism between the mineral and organic phase that also enhances energy dissipation. This further explains our finding that the overlap region deforms more compared with gap region in the mineralized cases, a clear distinction from the mechanics of pure collagen fibrils.

Bottom Line: Here we perform full-atomistic calculations of the three-dimensional molecular structure of a mineralized collagen protein matrix to try to better understand its mechanical characteristics under tensile loading at various mineral densities.We find that as the mineral density increases, the tensile modulus of the network increases monotonically and well beyond that of pure collagen fibrils.These findings reveal the mechanism by which bone is able to achieve superior energy dissipation and fracture resistance characteristics beyond its individual constituents.

View Article: PubMed Central - PubMed

Affiliation: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.

ABSTRACT
Bone is a natural composite of collagen protein and the mineral hydroxyapatite. The structure of bone is known to be important to its load-bearing characteristics, but relatively little is known about this structure or the mechanism that govern deformation at the molecular scale. Here we perform full-atomistic calculations of the three-dimensional molecular structure of a mineralized collagen protein matrix to try to better understand its mechanical characteristics under tensile loading at various mineral densities. We find that as the mineral density increases, the tensile modulus of the network increases monotonically and well beyond that of pure collagen fibrils. Our results suggest that the mineral crystals within this network bears up to four times the stress of the collagen fibrils, whereas the collagen is predominantly responsible for the material's deformation response. These findings reveal the mechanism by which bone is able to achieve superior energy dissipation and fracture resistance characteristics beyond its individual constituents.

Show MeSH
Related in: MedlinePlus