Skip to main content

Viscoelasticity, Energy Storage and Transmission and Dissipation by Extracellular Matrices in Vertebrates

  • Chapter
Collagen

Abstract

The extracellular matrix (ECM) of vertebrates is an important biological mechanotransducer that prevents premature mechanical failure of tissues and stores and transmits energy created by muscular deformation. It also transfers large amounts of excess energy to muscles for dissipation as heat, and in some cases, the ECM itself dissipates energy locally. Beyond these functions, ECMs regulate their size and shape as a result of the changing external loads. Changes in tissue metabolism are transduced into increases or decreases in synthesis and catabolism of the components of ECMs. Viscoelasticity is an important feature of the mechanical behavior of ECMs. This parameter, however, complicates the understanding of ECM behavior since it contains both viscous and elastic contributions in most real-time measurements made on vertebrate tissues.

The purpose of this chapter is to examine how time-dependent (viscous) and timeindependent (elastic) mechanical behaviors of an ECMare related to the hierarchical structure of vertebrate tissues and the macromolecular components found in specific tissues. In most ECMs, energy storage is believed to involve elastic stretching of collagen triple helices found in the cross-linked collagen fibrils comprising vertebrate connective tissues, and energy dissipation is believed to involve sliding of such collagen fibrils by each other during tissue deformation. It may be concluded that viscoelasticity differs markedly among different ECMs and is related to ECM hierarchical structure at the molecular and supramolecular levels of any particular vertebrate tissue.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alexander R M (1983) Animal Mechanics (2nd ed.). Blackwell Scientific, Oxford, UK.

    Google Scholar 

  • Alexander R M (1984) Elastic energy stores in running vertebrates. A. Zool. 24, 85–94.

    Google Scholar 

  • Arnoczky S P (1992) Gross and vascular anatomy of the meniscus and its role in meniscal healing, regeneration, and remodeling. In: Mow V C, Arnoczky S P, and Jackson D W (Eds.), Knee Meniscus: Basic and Clinical Foundations, Raven Press, New York, pp. 1–14.

    Google Scholar 

  • Birk D E, Zycband E I, Winkelmann D A, Trelstad R L (1989) Collagen fibrillogenesis in situ: Fibril segments are intermediates in matrix assembly. Proc. Natl. Acad. Sci. U S A 86:4549–4553.

    Article  Google Scholar 

  • Christiansen D L, Huang E K, Silver F H (2000) Assembly of type I collagen: Fusions of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol. 19:409–420.

    Article  Google Scholar 

  • Dunn M G, Silver F H (1983) Viscoelastic behavior of human connective tissue: Relative contribution of viscous and elastic components. Connect. Tissue Res. 12: 59–70.

    Article  Google Scholar 

  • Freeman J W, Silver, F H (2004a) Analysis of mineral deposition in turkey tendons and self-assembled collagen fibers using mechanical techniques. Connect. Tissue Res. 45: 131–141.

    Article  Google Scholar 

  • Freeman J W, Silver F H (2004b) Elastic energy storage in unimineralized and mineralized extracellular matrices (ECMs): A comparison between molecular modeling and experimental measurements. J. Theor. Biol. 229: 371–381.

    Article  Google Scholar 

  • Freeman J W, Silver F H (2005) The effects of prestrain on in vitro mineralization of self-assembled collagen fibers. Connect. Tissue Res. 46: 107–155.

    Article  Google Scholar 

  • Landis W J, Silver, F H (2002) The structure and function of normally mineralizing tendons. Comp. Biochem. Physiol. A, 133: 1135–1157.

    Article  Google Scholar 

  • Landis W J, Silver F H, Freeman J (2006) Collagen as a scaffold for biomimetic mineralization of vertebrate tissues. J. Mater. Chem. 16: 1495–1503.

    Article  Google Scholar 

  • McBride D J (1984) Hind Limb Extensor Tendon Development in the Chick: A Light and Transmission Electron Microscopic Study. M.S. Thesis in Physiology, Rutgers University, Piscataway, NJ.

    Google Scholar 

  • McBride D J, Hahn R, Silver F H (1985) Morphological characterization of tendon development during chick embryogenesis: Measurement of birefringence retardation. Int. J. Biol. Macromol. 7: 71–76.

    Article  Google Scholar 

  • McBride D J, Trelstad R L, Silver, F H (1988) Structural and mechanical assessment of developing chick tendon. Int. J. Biol. Macromol. 10: 194–200.

    Article  Google Scholar 

  • Mosler E, Folkhard W, Knorzer E., Nemetschek-Gansler H, Nemetschek T H, Koch M H (1985) Stress-induced molecular arrangement in tendon collagen. J. Mol. Biol. 182: 589–596.

    Article  Google Scholar 

  • Paterlini M G, Nemethy G, Scheraga H A (1995) The energy of formation of internal loops in triple-helical collagen polypeptides. Biopolymers 35: 607–619.

    Article  Google Scholar 

  • Rigby B J (1964) Effect of cyclic extension on the physical properties of tendon collagen and its possible relation to biological aging of collagen. Nature 202: 1072–1074.

    Article  Google Scholar 

  • Schoenfeld A, Landis W J, Kay D. (2007) Meniscal tissue engineering. Am. J. Orthop. 36:614–620.

    Google Scholar 

  • Seehra G P, Silver F H (2006) Viscoelastic properties of acid- and alkaline-treated human dermis: A correlation between total surface charge and elastic modulus. Skin Res. Technol. 12:190–198.

    Article  Google Scholar 

  • Silver, F H (2006) Mechanosensing and Mechanochemical Transduction in Extracellular Matrix: Biological, Chemical, Engineering and Physiological Aspects, Springer, New York.

    Google Scholar 

  • Silver F H, Birk D E (1984) Molecular structure of collagen in solution: Comparison of types I, II, III, and V. Int. J. Biol. Macromol. 6: 125–132.

    Article  Google Scholar 

  • Silver F H, Bradica G (2002) Mechanobiology of cartilage: how do internal and external stresses affect mechanochemical transduction and elastic energy storage? Biomechanics & Modeling in Mechanobiology 1: 1–19.

    Article  Google Scholar 

  • Silver F H, Christiansen D L (1999) Biomaterials Science and Biocompatibility, Chapter 6, Springer, New York.

    Google Scholar 

  • Silver F H, Siperko L M (2003) Mechanosensing and mechanochemical transduction. Crit. Rev. Biomed. Eng. 31: 255–331.

    Article  Google Scholar 

  • Silver F H, Christiansen D L, Snowhill P, Chen Y (2000) Role of storage on changes in the mechanical properties of tendon and self-assembled collagen fibers. Connect. Tissue Res. 41: 155–164.

    Article  Google Scholar 

  • Silver F H, Christiansen D L, Snowhill P B, Chen Y (2001a) Transition from viscous to elastic-based dependency of mechanical properties of self-assembled type I collagen fibers. J. Appl. Polym. Sci. 79: 134–142.

    Article  Google Scholar 

  • Silver F H, Freeman J W, Horvath I, Landis W J (2001b) Molecular basis for elastic energy storage in mineralized tendon. Biomacromolecules 2: 750–756.

    Article  Google Scholar 

  • Silver F H, Freeman J, DeVore D (2001c) Viscoelastic properties of human skin and processed dermis. Skin Res. Technol. 7: 18–25.

    Article  Google Scholar 

  • Silver F H, Horvath I, Foran D (2001d) Viscoelasticity of the vessel wall: Role of collagen and elastic fibers. Crit. Rev. Biomed. Eng. 29: 279–301.

    Google Scholar 

  • Silver F H, Bradica G, Tria A (2001e) Relationship among biomechanical, biochemical and cellular changes associated with osteoarthritis. Crit. Rev. Biomed. Eng. 29: 373–391.

    Google Scholar 

  • Silver F H, Bradica G, Tria A (2001f) Viscoelastic behavior of osteoarthritic cartilage. Connect. Tissue Res. 42: 223–233.

    Article  Google Scholar 

  • Silver F H, Seehra P, Freeman J W, DeVore D (2002a) Viscoelastic properties of young and old human dermis: Evidence that elastic energy storage occurs in the flexible regions of collagen and elastin. J. Appl. Polym. Sci. 86: 1978–1985.

    Article  Google Scholar 

  • Silver F H, Bradica G, Tria A (2002b) Elastic energy storage in human articular cartilage: Estimation of the elastic spring constant for type II collagen and changes associated with osteoarthritis. Matrix Biol. 21: 129–137.

    Article  Google Scholar 

  • Silver F H, Ebrahimi A, Snowhill P B (2002c) Viscoelastic properties of self-assembled type I collagen fibers: Molecular basis of elastic and viscous behaviors. Connect. Tissue Res. 43: 1–12.

    Article  Google Scholar 

  • Silver F H, Horvath I, Foran D J (2002d) Mechanical implications of the domain structure of fibril forming collagens: Comparison of the molecular and fibrillar flexibility of α -chains found in types I, II and III collagens. J. Theor. Biol. 216: 243–254.

    Article  Google Scholar 

  • Silver F H, Siperko L M, Seehra G P (2002e) Mechanobiology of force transduction in dermis. Skin Res. Technol. 8: 1–21.

    Google Scholar 

  • Silver F H, DeVore D, Siperko L M (2003a) Invited Review: Role of mechanophysiology in aging of ECM: Effects of changes in mechanochemical transduction. J. Appl. Physiol. 95: 2134–2141.

    Google Scholar 

  • Silver F H, Snowhill P B, Foran D (2003b) Mechanical behavior of vessel wall: A comparative study of aorta, vena cava, and carotid artery. Ann. Biomed. Eng. 31: 793–803.

    Article  Google Scholar 

  • Silver F H, Freeman J, Seehra G P (2003c) Collagen self-assembly and development of matrix mechanical properties. J. Biomech. 36: 1529–1553.

    Article  Google Scholar 

  • Silver F H, Bradica G., Tria A (2004) Do changes in mechanical properties of articular cartilage alter mechanochemical transduction and promote osteoarthritis? Matrix Biol. 23: 467–476.

    Article  Google Scholar 

  • Snowhill P B, Silver F H (2005) A mechanical model of porcine vascular tissues-Part II: Stress–strain and mechanical properties of juvenile porcine blood vessels. Cardiovasc. Eng. 5:157–169.

    Article  Google Scholar 

  • Snowhill P B, Foran D J, Silver F H (2004) A mechanical model of porcine vascular tissues-Part I. Determination of macromolecular component arrangement and volume fractions. Cardiovasc. Eng. 4: 281–294.

    Article  Google Scholar 

  • Wilson A M, McGuigan M P, Su A, van den Bogert A J (2001) Horses damp the spring in their step. Nature 414: 895–899.

    Article  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Silver, F., Landis, W. (2008). Viscoelasticity, Energy Storage and Transmission and Dissipation by Extracellular Matrices in Vertebrates. In: Fratzl, P. (eds) Collagen. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-73906-9_6

Download citation

  • DOI: https://doi.org/10.1007/978-0-387-73906-9_6

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-0-387-73905-2

  • Online ISBN: 978-0-387-73906-9

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics