Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-29T08:02:34.345Z Has data issue: false hasContentIssue false

Entropic Elasticity Controls Nanomechanics of Single Tropocollagen Molecules

Published online by Cambridge University Press:  26 February 2011

Markus J. Buehler
Affiliation:
[email protected], MIT, Civil and Environmental Engrg, 77 Mass Ave, Cambridge, MA, 02139, United States, [email protected]
Sophie Wong
Affiliation:
[email protected], Massachusetts Institute of Technology, Department of Brain and Cognitive Sciences, 77 Massachusetts Ave., Cambridge, MA, 02139, United States
Get access

Abstract

We report molecular modeling of stretching single molecules of tropocollagen, the building block of collagen fibrils and fibers that provide mechanical support in connective tissues. For small deformation, we observe a dominance of entropic elasticity. At larger deformation, we find a transition to energetic elasticity, which is characterized by first stretching and breaking of hydrogen bonds, followed by deformation of covalent bonds in the protein backbone, eventually leading to molecular fracture. Our force-displacement curves show excellent quantitative agreement with optical tweezer experiments, suggesting a persistence length of approximately 16 nm. We demonstrate that assembly of single TC molecules into fibrils significantly decreases their flexibility, leading to decreased contributions of entropic effects during deformation. We develop a simple continuum model capable of describing entire deformation range of TC molecules.

Type
Research Article
Copyright
Copyright © Materials Research Society 2007

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

REFERENCES

1. Sun, Y.L., et al., Stretching type II collagen with optical tweezers. Journal Of Biomechanics, 2004. 37(11): p. 16651669.Google Scholar
2. Sun, Y.L., et al., Direct quantification of the flexibility of type I collagen monomer. Biochemical And Biophysical Research Communications, 2002. 295(2): p. 382386.Google Scholar
3. Ramachandran, G.N., Kartha, G., Structure of collagen. Nature, 1955. 176: p. 593595.Google Scholar
4. Rich, A. and Crick, F.H.C., The structure of collagen. Nature, 1955. 176: p. 915916.Google Scholar
5. Jager, I. and Fratzl, P., Mineralized collagen fibrils: A mechanical model with a staggered arrangement of mineral particles. Biophysical Journal, 2000. 79(4): p. 17371746.Google Scholar
6. Hulmes, D.J.S., et al., Radial Packing, Order, And Disorder In Collagen Fibrils. Biophysical Journal, 1995. 68(5): p. 16611670.Google Scholar
7. Weiner, S. and Wagner, H.D., The material bone: Structure mechanical function relations. Annual Review Of Materials Science, 1998. 28: p. 271298.Google Scholar
8. Screen, H.R.C., et al., Local strain measurement within tendon. Strain, 2004. 40(4): p. 157163.Google Scholar
9. Boedke, H.a.D., P., The native and denatured states of soluble collagen. J. Am. Chemical Society, 1956. 78: p. 42674280.Google Scholar
10. Oebrink, B., Non-aggregated tropocollagem at physiological p{H} and ionic strength. A chemical and physio-chemical characterization of tropocollagen isolated from the skin of lathyritic rats. European J. of Biochemistry, 1972. 25: p. 563572.Google Scholar
11. Utiyama, H., et al., Flexibility Of Tropocollagen From Sedimentation And Viscosity. Biopolymers, 1973. 12(1): p. 5364.Google Scholar
12. Nestler, F.H.M., et al., Flexibility Of Collagen Determined From Dilute-Solution Viscoelastic Measurements. Biopolymers, 1983. 22(7): p. 17471758.Google Scholar
13. Saito, T., et al., Semi-Flexibility Of Collagens In Solution. Biopolymers, 1982. 21(4): p. 715728.Google Scholar
14. Hofmann, H., et al., Localization Of Flexible Sites In Thread-Like Molecules From Electron-Micrographs - Comparison Of Interstitial, Basement-Membrane And Intima Collagens. Journal Of Molecular Biology, 1984. 172(3): p. 325343.Google Scholar
15. Sun, Y.L., Luo, Z.P., and An, K.N., Stretching short biopolymers using optical tweezers. Biochemical And Biophysical Research Communications, 2001. 286(4): p. 826830.Google Scholar
16. Buehler, M.J., Atomistic and continuum modeling of mechanical properties of collagen: Elasticity, fracture and self-assembly. J. Mater. Res., 2006. 21(8): p. 19471961.Google Scholar
17. 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
18. MacKerell, A.D., et al., All-atom empirical potential for molecular modeling and dynamics studies of proteins. Journal Of Physical Chemistry B, 1998. 102(18): p. 35863616.Google Scholar
19. Nelson, M.T., et al., NAMD: A parallel, object oriented molecular dynamics program. International Journal Of Supercomputer Applications And High Performance Computing, 1996. 10(4): p. 251268.Google Scholar
20. Humphrey, W., A., Dalke, and K., Schulten, VMD: Visual molecular dynamics. Journal Of Molecular Graphics, 1996. 14(1): p. 33.Google Scholar
21. Kramer, R.Z., et al., Staggered molecular packing in crystals of a collagen-like peptide with a single charged pair. Journal Of Molecular Biology, 2000. 301(5): p. 11911205.Google Scholar
22. Lu, H., et al., Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophysical Journal, 1998. 75(2): p. 662671.Google Scholar
23. Plimpton, S., Fast parallel algorithms for short-range molecular-dynamics. Journal of Computational Physics, 1995. 117: p. 119.Google Scholar
24. Courtney, T.H., Mechanical behavior of materials. 1990: McGraw-Hill.Google Scholar
25. Bustamante, C., et al., Entropic Elasticity Of Lambda-Phage Dna. Science, 1994. 265(5178): p. 15991600.Google Scholar
26. Marko, J.F. and Siggia, E.D., Stretching DNA. Macromolecules, 1995. 28(26): p. 87598770.Google Scholar
27. Miles, C.A. and A.J., Bailey, Thermally labile domains in the collagen molecule. Micron, 2001. 32(3): p. 325332.Google Scholar