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Tenocyte contraction induces crimp formation in tendon-like tissue

  • Andreas Herchenhan
  • Nicholas S. Kalson
  • David F. Holmes
  • Patrick Hill
  • Karl E. KadlerEmail author
  • Lee MargettsEmail author
Open Access
Original Paper

Abstract

Tendons are composed of longitudinally aligned collagen fibrils arranged in bundles with an undulating pattern, called crimp. The crimp structure is established during embryonic development and plays a vital role in the mechanical behaviour of tendon, acting as a shock-absorber during loading. However, the mechanism of crimp formation is unknown, partly because of the difficulties of studying tendon development in vivo. Here, we used a 3D cell culture system in which embryonic tendon fibroblasts synthesise a tendon-like construct comprised of collagen fibrils arranged in parallel bundles. Investigations using polarised light microscopy, scanning electron microscopy and fluorescence microscopy showed that tendon constructs contained a regular pattern of wavy collagen fibrils. Tensile testing indicated that this superstructure was a form of embryonic crimp producing a characteristic toe region in the stress–strain curves. Furthermore, contraction of tendon fibroblasts was the critical factor in the buckling of collagen fibrils during the formation of the crimp structure. Using these biological data, a finite element model was built that mimics the contraction of the tendon fibroblasts and monitors the response of the Extracellular matrix. The results show that the contraction of the fibroblasts is a sufficient mechanical impulse to build a planar wavy pattern. Furthermore, the value of crimp wavelength was determined by the mechanical properties of the collagen fibrils and inter-fibrillar matrix. Increasing fibril stiffness combined with constant matrix stiffness led to an increase in crimp wavelength. The data suggest a novel mechanism of crimp formation, and the finite element model indicates the minimum requirements to generate a crimp structure in embryonic tendon.

Keywords

Finite element modelling Chick embryonic tendon Crimp Collagen Tension Extracellular matrix 

Abbreviations

ECMT

Embryonic chick metatarsal tendon

FEA

Finite element analysis

FEM

Finite element modelling

SEM

Scanning electron microscopy

ECM

Extracellular matrix

PPLM

Plane polarised light microscopy

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Andreas Herchenhan
    • 1
  • Nicholas S. Kalson
    • 1
  • David F. Holmes
    • 1
  • Patrick Hill
    • 2
  • Karl E. Kadler
    • 1
    Email author
  • Lee Margetts
    • 3
    Email author
  1. 1.Faculty of Life Sciences, Wellcome Trust Centre for Cell-Matrix ResearchUniversity of ManchesterManchesterUK
  2. 2.School of Chemical Engineering and Analytical ScienceUniversity of ManchesterManchesterUK
  3. 3.High Performance Computing, Research Computing ServicesUniversity of ManchesterManchesterUK

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