The structure and micromechanics of elastic tissue

Abstract

Elastin is a major component of tissues such as lung and blood vessels, and endows them with the long-range elasticity necessary for their physiological functions. Recent research has revealed the complexity of these elastin structures and drawn attention to the existence of extensive networks of fine elastin fibres in tissues such as articular cartilage and the intervertebral disc. Nonlinear microscopy, allowing the visualization of these structures in living tissues, is informing analysis of their mechanical properties. Elastic fibres are complex in composition and structure containing, in addition to elastin, an array of microfibrillar proteins, principally fibrillin. Raman microspectrometry and X-ray scattering have provided new insights into the mechanisms of elasticity of the individual component proteins at the molecular and fibrillar levels, but more remains to be done in understanding their mechanical interactions in composite matrices. Elastic tissue is one of the most stable components of the extracellular matrix, but impaired mechanical function is associated with ageing and diseases such as atherosclerosis and diabetes. Efforts to understand these associations through studying the effects of processes such as calcium and lipid binding and glycation on the mechanical properties of elastin preparations in vitro have produced a confusing picture, and further efforts are required to determine the molecular basis of such effects.

Keywords: elastic fibre; elastic protein; tissue micromechanics.

Figure 1.

Elastin fibres in connective tissues as revealed in fresh, unstained tissue by two-photon fluorescence (green). Collagen is visualized by second harmonic generation (blue) and cell boundaries by coherent anti-Stokes Raman scattering from CH₂ bonds in cellular lipids (red). Sources of tissue: (a) equine metacarpophalangeal joint; (b) equine tail; (c) human omentum; (d) human abdominal subcutis; (e) porcine heart; (f) porcine aorta.

Figure 2.

Scanning electron micrograph of the elastin structure of ligamentum nuchae elastin (by kind permission of Prof. Michel Spina).

Figure 3.

False-colour images of a viable human subcutaneous small resistance artery at neutral luminal pressure (a) and 30 mm Hg (b). SHG (blue) reveals collagen, and TPF (green) reveals autofluorescent proteins. Fibres seen in green are elastin. Increased luminal pressure causes the innermost layer of elastin to stretch radially, revealing the interconnectivity of the elastin fibres. The vessel is oriented at an angle to the imaging plane, so that the top of the images is in the adventitia, and the bottom passes through the lumen.

Figure 4.

TPF images of equine articular cartilage at (a) 0%, (b) 4% and (c) 8% applied tensile strain. (d) An overlay showing elastin fibres which can be individually tracked between the images. (e) A histogram showing the differences between the predicted and measured elastin fibre angles at both 4% and 8% strain. The shaded area shows the limited range where the values agree within the uncertainty of the measurements. Fibre orientation data before and after the application of tensile strain are included in the electronic supplementary material.

Figure 5.

Thermoelasticity of nuchal elastin fibres from bovine nuchal ligament. Fibres were immerzed in deionized water and held at constant 20% extension whilst force was measured as temperature was increased from room temperature to 60°C. Changes in stress were analysed on the basis of the theory of rubber-like elasticity [36], according to which the ratio of energetic components, f_e, to the total force, f, is given by the relation: where the derivative is taken at constant pressure, length and fluid equilibrium, T is the absolute temperature, V_i and V are sample volumes before and after elongation, β_eq is the thermal expansion coefficient and α is the fractional increase in length. See [37] for further details. The raw thermoelasticity data are included in the electronic supplementary material.

Figure 6.

Stress–strain behaviour of lamprey cartilage (branchial, pericardial, annular and piston) proteins prepared by cyanogen bromide extraction. Data for bovine nuchal elastin fibres are shown for comparison. Measurements were made in deionized water at room temperature. See [37] for further details. The raw stress–strain measurements for each material are included in the electronic supplementary material.