Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T02:25:16.308Z Has data issue: false hasContentIssue false

Computational multiscale studies of collagen tissues in the context of brittle bone disease osteogenesis imperfecta

Published online by Cambridge University Press:  01 February 2011

Simone Vesentini
Affiliation:
[email protected] Politecnico di Milano Milano, Italy
Alfonso Gautieri
Affiliation:
[email protected] Massachusetts Institute of Technology Cambridge, Massachusetts, United States
Alberto Redaelli
Affiliation:
[email protected] Politecnico di Milano Milano, Italy
Markus J. Buehler
Affiliation:
[email protected] Massachusetts Institute of Technology Laboratory for Atomistic and Molecular Mechanics, Department of Civil and Environmental Engineering, Cambridge, Massachusetts, United States
Get access

Abstract

Osteogenesis imperfecta (abbreviated as OI) is a genetic disorder in collagen characterized by mechanically weakened tendon, fragile bones, skeletal deformities and in severe cases prenatal death. Even though many studies have attempted to associate specific mutation types with phenotypic severity, the molecular and mesoscale mechanisms by which a single point mutation influences the mechanical behavior of tissues at multiple length-scales remain unknown. Here we review results of a hierarchy of full atomistic and mesoscale simulations that demonstrated that OI mutations severely compromise the mechanical properties of collagenous tissues at multiple scales, from single molecules to collagen fibrils. Notably, mutations that lead to the most severe OI phenotype correlate with the strongest effects, leading to weakened intermolecular adhesion, increased intermolecular spacing, reduced stiffness, as well as a reduced failure strength of collagen fibrils (Gautieri et al., Biophys. J., 2009). Our study explains how single point mutations can control the breakdown of tissue at much larger length-scales, a question of great relevance for a broad class of genetic diseases. Furthermore, by extending the MARTINI coarse-grained force field, we provide a new modeling tool to study collagen molecules and fibrils at much larger scales than accessible to existing full atomistic models, while incorporating key chemical and mechanical features and thereby presents a powerful approach to computational materiomics (Gautieri et al., Journal of Chemical Theory and Computation, 2010). We describe the coarse-graining approach and present preliminary findings based on this model in applying it to large-scale models of molecular assemblies into fibrils.

Type
Research Article
Copyright
Copyright © Materials Research Society 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1 Peltonen, L., Palotie, A., and Prockop, D. J., A defect in the structure of type I procollagen in a patient who had osteogenesis imperfecta: excess mannose in the COOH-terminal propeptide. Proceedings Of The National Academy Of Sciences Of The United States Of America, 1980. 77: p. 61796183.Google Scholar
2 Rainey, J. and Goh, M., An interactive triple-helical collagen builder. Bioinformatics, 2004. 20(15): p. 24582459.Google Scholar
3 Gautieri, A., Buehler, M. J., and Redaelli, A., Deformation rate controls elasticity and unfolding pathway of single tropocollagen molecules. Journal of the Mechanical Behavior of Biomedical Materials, 2009. 2(2): p. 130137.Google Scholar
4 Gautieri, A. et al. , Mechanical properties of physiological and pathological models of collagen peptides investigated via steered molecular dynamics simulations. Journal Of Biomechanics, 2008. 41(14): p. 30733077.Google Scholar
5 Buehler, M.J., Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. P. Natl. Acad. Sci. USA, 2006. 103(33): p. 1228512290.Google Scholar
6 Buehler, M.J., Nanomechanics of collagen fibrils under varying cross-link densities: Atomistic and continuum studies. Journal of the Mechanical Behavior of Biomedical Materials, 2008. 1(1): p. 5967.Google Scholar
7 Sun, Y.L. et al. , Stretching type II collagen with optical tweezers. Journal Of Biomechanics, 2004. 37(11): p. 16651669.Google Scholar
8 Sasaki, N. and Odajima, S., Stress-strain curve and Young's modulus of a collagen molecule as determined by the X-ray diffraction technique. Journal of Biomechanics, 1996. 29(5): p. 655658.Google Scholar
9 Gautieri, A. et al. , Single molecule effects of osteogenesis imperfecta mutations in tropocollagen protein domains. Protein Science, 2009. 18(1): p. 161168.Google Scholar
10 Gautieri, A. et al. , Molecular and Mesoscale Mechanisms of Osteogenesis Imperfecta Disease in Collagen Fibrils. Biophysical Journal, 2009. 97(3): p. 857865.Google Scholar
11 Misof, K. et al. , Collagen from the osteogenesis imperfecta mouse model (oim) shows reduced resistance against tensile stress. Journal Of Clinical Investigation, 1997. 100(1): p. 4045.Google Scholar
12 Gautieri, A. et al. , Coarse-Grained Model of Collagen Molecules Using an Extended MARTINI Force Field. Journal of Chemical Theory and Computation, 2010. 6(4): p. 12101218.Google Scholar
13 Vesentini, S. et al. , Molecular assessment of the elastic properties of collagen-like homotrimer sequences. Biomechanics And Modeling In Mechanobiology, 2005. 3(4): p. 224234.Google Scholar
14 Buehler, M.J., Atomistic modeling of elasticity, plasticity and fracture of protein crystals. Journal of Computational and Theoretical Nanoscience, 2006. 3(5): p. 670683 Google Scholar
15 Lorenzo, A.C. and Caffarena, E.R., Elastic properties, Young's modulus determination and structural stability of the tropocollagen molecule: a computational study by steered molecular dynamics. Journal Of Biomechanics, 2005. 38(7): p. 15271533.Google Scholar
16 Sasaki, N. and Odajima, S., Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. Journal Of Biomechanics, 1996. 29(9): p. 11311136.Google Scholar
17 Buehler, M.J. and Yung, Y.C., Deformation and failure of protein materials in physiologically extreme conditions and disease. Nat Mater, 2009. 8(3): p. 175–88.Google Scholar