Tropocollagen (TC) and hydroxyapatite (HAP) interfaces are one of the main load bearing entities in bone family of materials. Atomistic interactions in such interfaces occur in a variety of chemical environments under a range of biomechanical loading conditions. It is challenging to investigate such interactions using traditional analytical or using classical molecular simulation approaches owing to their limitations in predicting bond strength change as a function of change in chemical environment. In the present work, 3D ab initio molecular dynamics simulations are used to understand such atomistic interactions by analyzing tensile strain dependent deformation mechanism and strength of two structurally distinct idealized TC-HAP interfaces in hydrated as well as unhydrated environments. Analyses suggest that the presence of water molecules leads to modification of H-bond density at the interfaces that also depends upon the level of strain. TC molecules become stiffer in the presence of water due to the presence of H-bonds. Bond forming-and-breaking cycle change as a function of H-bond density lies at the heart of TC-HAP interfacial shear deformation. Consequently, interfaces with TC molecule placed flat on the HAP crystal surface experience significantly higher shear stress during deformation in comparison to the interfaces with TC molecule placed with their axes perpendicular to the HAP surface.

References

References
1.
Currey
,
J. D.
,
1977
, “
Mechanical-Properties of Mother of Pearl in Tension
,”
Proc. Royal Soc. London, Series B
,
196
(
1125
), pp.
443
463
.10.1098/rspb.1977.0050
2.
Rho
,
J. Y.
,
Kuhn-Spearing
,
L.
, and
Zioupos
,
P.
,
1998
, “
Mechanical Properties and the Hierarchical Structure of Bone
,”
Med. Eng. Phys.
,
20
(
2
), pp.
92
102
.10.1016/S1350-4533(98)00007-1
3.
Weiner
,
S.
, and
Wagner
,
H. D.
,
1998
, “
The Material Bone: Structure Mechanical Function Relations
,”
Ann. Rev. Mater. Sci.
,
28
, pp.
271
298
.10.1146/annurev.matsci.28.1.271
4.
Ji
,
B.
, and
Gao
,
H.
,
2004
, “
Mechanical Properties of Nanostructure of Biological Materials
,”
J. Mech. Phys. Solids
,
52
, pp.
1963
2000
.10.1016/j.jmps.2004.03.006
5.
Jager
, I
.
, and
Fratzl
,
P.
,
2000
, “
Mineralized Collagen Fibrils: A Mechanical Model With a Staggered Arrangement of Mineral Particles
,”
Biophys. J.
,
79
(
4
), pp.
1737
1746
.10.1016/S0006-3495(00)76426-5
6.
Fratzl
,
P.
,
Gupta
,
H. S.
,
Paschalis
,
E. P.
, and
Roschger
,
P.
,
2004
, “
Structure and Mechanical Quality of the Collagen-Mineral Nano-Composite in Bone
,”
J. Mater. Chem.
,
14
(
14
), pp.
2115
2123
.10.1039/b402005g
7.
Gupta
,
H. S.
,
Seto
,
J.
,
Wagermaier
,
W.
,
Zaslansky
,
P.
,
Boesecke
,
P.
, and
Fratzl
,
P.
,
2006
, “
Cooperative Deformation of Mineral and Collagen in Bone at the Nanoscale
,
Proc. Natl. Acad. Sci. U.S.A.
,
103
, pp.
17741
17746
.10.1073/pnas.0604237103
8.
Gupta
,
H. S.
,
Wagermaier
,
W.
,
Zickler
,
G. A.
,
Aroush
,
D. R.-B.
,
Funari
,
S. S.
,
Roschger
,
P.
,
Wagner
,
H.-D.
, and
Fratzl
,
P.
,
2005
, “
Nanoscale Deformation Mechanisms in Bone
,”
Nano Lett.
,
5
(
10
), pp.
2108
2111
.10.1021/nl051584b
9.
Sasaki
,
N.
, and
Odajima
,
S.
,
1996
, “
Stress-Strain Curve and Young’s Modulus of a Collagen Molecule as Determined by the X-Ray Diffraction Technique
,”
J. Biomech.
,
29
(
5
), pp.
655
658
.10.1016/0021-9290(95)00110-7
10.
Eppell
,
S. J.
,
Smith
,
B. N.
,
Kahn
,
H.
, and
Ballarini
,
R.
,
2005
, “
Nano Measurements With Micro-Devices: Mechanical Properties of Hydrated Collagen Fibrils
,”
J. R. Soc., Interface
,
3
, pp.
117
121
.10.1098/rsif.2005.0100
11.
Hodge
,
A. J.
, and
Petruska
,
J. A.
,
1963
, “
Recent Studies With the Electron Microscope on Ordered Aggregates of the Tropocollagen Macromolecule
,”
Aspects of Protein Structure. Proceedings of a Symposium
,
G. N.
Ramachandran
, ed.,
Academic
,
New York
, pp.
289
300
.
12.
Fantner
,
G. E.
,
Hassenkam
,
T.
,
Kindt
,
J. H.
,
Weaver
,
J. C.
,
Birkedal
,
H.
,
Pechenik
,
L.
,
Cutroni
,
J. A.
,
Cidade
,
G. A. G.
,
Stucky
,
G. D.
,
Morse
,
D. E.
, and
Hansma
,
P. K.
,
2005
, “
Sacrificial Bonds and Hidden Length Dissipate Energy as Mineralized Fibrils Separate During Bone Fracture
,”
Nature Mater.
,
4
(
8
), pp.
612
616
.10.1038/nmat1428
13.
Thurner
,
P. J.
,
Erickson
,
B.
,
Jungmann
,
R.
,
Schriock
,
Z.
,
Weaver
,
J. C.
,
Fantner
,
G. E.
,
Schitter
,
G.
,
Morse
,
D. E.
, and
Hansma
,
P. K.
,
2007
, “
High-Speed Photography of Compressed Human Trabecular Bone Correlates Whitening to Microscopic Damage
,”
Eng. Fract. Mech.
,
74
(
12
), pp.
1928
1941
.10.1016/j.engfracmech.2006.05.024
14.
Gao
,
H.
,
2006
, “
Application of Fracture Mechanics Concepts to Hierarchical Biomechanics of Bone and Bone-Like Materials
,”
Int. J. Fracture
,
138
, pp.
101
137
.10.1007/s10704-006-7156-4
15.
Ji
,
B. H.
,
2008
, “
A Study of the Interface Strength Between Protein and Mineral in Biological Materials
,”
J. Biomech.
,
41
(
2
), pp.
259
266
.10.1016/j.jbiomech.2007.09.022
16.
Lorenzo
,
A. C.
, and
Caffarena
,
E. R. l.
,
2005
, “
Elastic Properties, Young’s Modulus Determination and Structural Stability of the Tropocollagen Molecule: A Computational Study by Steered Molecular Dynamics
,”
J. Biomech.
,
38
, pp.
1527
1533
.10.1016/j.jbiomech.2004.07.011
17.
Buehler
,
M. J.
,
2006
, “
Atomistic and Continuum Modeling of Mechanical Properties of Collagen: Elasticity, Fracture, and Self-Assembly
,”
J. Mater, Res.
,
21
(
8
), pp.
1947
1962
.10.1557/jmr.2006.0236
18.
Buehler
,
M. J.
,
2007
, “
Entropic Elasticity Controls Nanomechanics of Single Tropocollagen Molecules
,”
Biophys. J.
,
93
, pp.
37
43
.10.1529/biophysj.106.102616
19.
Ghosh
,
P.
,
Katti
,
D. R.
, and
Katti
,
K. S.
,
2007
, “
Mineral Proximity Influences Mechanical Response of Proteins in Biological Mineral-Protein Hybrid Systems
,”
Biomacromolecules
,
8
(
3
), pp.
851
856
.10.1021/bm060942h
20.
Bhowmik
,
R.
,
Katti
,
K. S.
,
Verma
,
D.
, and
Katti
,
D. R.
,
2007
, “
Probing Molecular Interactions in Bone Biomaterials: Through Molecular Dynamics and Fourier Transform Infrared Spectroscopy
,”
Mater. Sci. Eng.
,
27
, pp.
352
371
.10.1016/j.msec.2006.05.048
21.
Israelowitz
,
M.
,
Rizvi
,
S. W. H.
,
Kramer
,
J.
, and
Schroeder
,
H. P. v.
,
2005
, “
Computational Modeling of Type I Collagen Fibers to Determine the Extracellular Matrix Structure of Connective Tissues
,”
Protein Eng. Des. Sel.
,
18
(
7
), pp.
329
335
.10.1093/protein/gzi037
22.
Buehler
,
M. J.
,
2008
, “
Nanomechanics of Collagen Fibrils Under Varying Cross-Link Densities: Atomistic and Continuum Studies
,”
J. Mech. Behav. Biomed. Mater.
,
1
, pp.
59
67
.10.1016/j.jmbbm.2007.04.001
23.
Handgraaf
,
J. W.
, and
Zerbetto
,
F.
,
2006
, “
Molecular Dynamics Study of Onset of Water Gelation Around the Collagen Triple Helix
,”
Proteins: Struct., Funct., Bioinf.
,
64
(
3
), pp.
711
718
.10.1002/prot.21019
24.
Zhang
,
D.
,
Chippada
,
U.
, and
Jordan
,
K.
,
2007
, “
Effect of the Structural Water on the Mechanical Properties of Collagen-Like Microfibrils: A Molecular Dynamics Study
,”
Ann. Biomed. Eng.
,
35
, pp.
1216
1230
.10.1007/s10439-007-9296-8
25.
Radmer
,
R. J.
, and
Klein
,
T. E.
,
2006
, “
Triple Helical Structure and Stabilization of Collagen-Like Molecules With 4(R)-Hydroxyproline in the Xaa Position
,”
Biophys. J.
,
90
, pp.
578
588
.10.1529/biophysj.105.065276
26.
Dubey
,
D. K.
, and
Tomar
, V
.
,
2009
, “
Understanding the Influence of Structural Hierarchy and Its Coupling With Chemical Environment on the Strength of Idealized Tropocollagen–Hydroxyapatite Biomaterials
,”
J. Mech. Phys. Solids
,
57
(
10
), pp.
1702
1717
.10.1016/j.jmps.2009.07.002
27.
Dubey
,
D. K.
, and
Tomar
, V
.
,
2009
, “
Role of the Nanoscale Interfacial Arrangement in Mechanical Strength of Tropocollagen-Hydroxyapatite Based Hard Biomaterials
,”
Acta Biomater.
,
5
(
7
), pp.
2704
2716
.10.1016/j.actbio.2009.02.035
28.
Dubey
,
D. K.
, and
Tomar
,
V.
,
2009
, “
The Effect of Tensile and Compressive Loading on the Hierarchical Strength of Idealized Tropocollagen-Hydroxyapatite Biomaterials as a Function of the Chemical Environment
,”
J. Phys.: Condens. Matter
,
21
(
20
), p.
205103
.10.1088/0953-8984/21/20/205103
29.
Niebur
,
G.
,
2013
, available at http://www.nd.edu/~gniebur
30.
Almora-Barrios
,
N.
, and
de Leeuw
,
N. H.
,
2010
, “
A Density Functional Theory Study of the Interaction of Collagen Peptides With Hydroxyapatite Surfaces
,”
Langmuir
,
26
(
18
), pp.
14535
14542
.10.1021/la101151e
31.
Ching
,
W. Y.
,
Rulis
,
P.
, and
Misra
,
A.
,
2009
, “
Ab Initio Elastic Properties and Tensile Strength of Crystalline Hydroxyapatite
,”
Acta Biomater.
,
5
(
8
), pp.
3067
3075
.10.1016/j.actbio.2009.04.030
32.
Ren
,
F.
,
Leng
,
Y.
,
Xin
,
R.
, and
Ge
,
X.
,
2010
, “
Synthesis, Characterization and Ab Initio Simulation of Magnesium-Substituted Hydroxyapatite
,”
Acta Biomater.
,
6
(
7
), pp.
2787
2796
.10.1016/j.actbio.2009.12.044
33.
Chappell
,
H.
,
Duer
,
M.
,
Groom
,
N.
,
Pickard
,
C.
, and
Bristowe
,
P.
,
2008
, “
Probing the Surface Structure of Hydroxyapatite Using NMR Spectroscopy and First Principles Calculations
,”
Phys. Chem. Chem. Phys.
,
10
(
4
), pp.
600
606
.10.1039/b714512h
34.
Prockop
,
D. J.
, and
Kivirikko
,
K. I.
,
1995
, “
Collagens: Molecular Biology, Diseases, and Potentials for Therapy
,”
Ann. Rev. Biochem.
,
64
, pp.
403
434
.10.1146/annurev.bi.64.070195.002155
35.
Makarov
, V
.
,
Pettitt
,
B. M.
, and
Feig
,
M.
,
2002
, “
Solvation and Hydration of Proteins and Nucleic Acids: A Theoretical View of Simulations and Experiment
,”
Acc. Chem. Res.
,
35
, pp.
376
384
.10.1021/ar0100273
36.
Voth
,
G. A.
,
2006
, “
Computer Simulation of Proton Solvation and Transport in Aqueous and Biomolecular Systems
,”
Acc. Chem. Res.
,
39
(
2
), pp.
143
150
.10.1021/ar0402098
37.
Valiev
,
M.
,
Bylaska
,
E. J.
,
Govind
,
N.
,
Kowalski
,
K.
,
Straatsma
,
T. P.
,
Van Dam
,
H. J. J.
,
Wang
,
D.
,
Nieplocha
,
J.
,
Apra
,
E.
,
Windus
,
T. L.
, and
de Jong
,
W.
,
2010
, “
NWChem: A Comprehensive and Scalable Open-Source Solution for Large Scale Molecular Simulations
,”
Comput. Phys. Commun.
,
181
(
9
), pp.
1477
1489
.10.1016/j.cpc.2010.04.018
38.
Qin
,
Z.
,
Gautieri
,
A.
,
Nair
,
A. K.
,
Inbar
,
H.
, and
Buehler
,
M. J.
,
2012
, “
Thickness of Hydroxyapatite Nanocrystal Controls Mechanical Properties of the Collagen-Hydroxyapatite Interface
,”
Langmuir
,
28
(
4
), pp.
1982
1992
.10.1021/la204052a
39.
Dubey
,
D. K.
, and
Tomar
, V
.
,
2009
, “
Role of Hydroxyapatite Crystal Shape in Nanoscale Mechanical Behavior of Model Tropocollagen-Hydroxyapatite Hard Biomaterials
,”
Mater. Sci. Eng., C
,
29
(
7
), pp.
2133
2140
.10.1016/j.msec.2009.04.015
40.
Horstemeyer
,
M. F.
,
Baskes
,
M. I.
, and
Plimpton
,
S. J.
,
2001
, “
Length Scale and Time Scale Effects on the Plastic Flow of FCC Metals
,”
Acta Mater.
,
49
(
20
), pp.
4363
4374
.10.1016/S1359-6454(01)00149-5
You do not currently have access to this content.